Samir S Shah, MD, MSCE

We enter the new year still in the midst of the coronavirus disease 2019 (COVID-19) pandemic and remain humbled by its impact. It is remarkable how much, and how little, has changed. Hospitalists in the early days of the COVID-19 pandemic were struggling. We were caring for patients who were suffering and dying from a new and mysterious disease. There weren’t enough tests (or, if there were tests, there weren’t swabs).¹ We were using protocols for managing respiratory failure that, we would learn later, may not have been the best for improving outcomes. Rumors of unproven therapies came from everywhere: our patients, our colleagues, and even the highest realms of the federal government. We also knew very little about how best to protect ourselves. In many cases, we did not have enough personal protective equipment (PPE). There were no face shields, or “zoom rounds,” or even awareness that we probably shouldn’t sit in the tiny conference room (maskless) discussing patients with the large team of doctors, nurses, respiratory therapists, and social workers.

Perhaps worst of all, we were haunted. We were alarmed by the large numbers of young patients who were ill, and our elderly patients, many of whom we knew and had cared for many times, had suddenly just stopped showing up.² In our free moments, we worried about them; maybe they were afraid to come to the hospital, maybe they were home sick with COVID-19, or maybe they had died alone. And children, initially thought to be spared the most serious consequences of COVID-19, started coming to the hospital with a rare but severe new COVID-19-associated complication, termed multisystem inflammatory syndrome in children (MIS-C). We had to learn to manage yet another manifestation of COVID-19, largely through trial and error.

And, of course, clinical care was only one of our many responsibilities. We were also busy hunting for ventilators, setting up makeshift medical wards and intensive care units, revamping medical education, and scouring the literature for any information to help guide patient care. We worried about getting sick ourselves and bringing the disease home to our families. Our impatience grew as day after day there was no (and still is no) coordinated federal response.

A glimmer of hope slowly emerged. Our colleagues designed and rapidly evaluated respiratory protocols and provided early evidence about the strategies (eg, proning) that were associated with improved outcomes.³ Researchers began to generate knowledge and move us beyond rumors regarding potential therapies. We cheered as our administrators concocted unusual strategies to remedy the PPE and testing shortages.⁴

At the Journal of Hospital Medicine, we were faced with another challenge: How would we describe the chaos and the challenges of being a physician during the COVID-19 era? How would we document the way our colleagues were rising to the challenge and identifying opportunities to rethink hospital care in the United States?

In April, we began to receive a deluge of personal essays from frontline physicians about their experiences with COVID-19. Generally, medical journals publish and disseminate original, high-impact research. Personal essays rarely fit this model. Given the unprecedented circumstances, however, we decided these essays could help chronicle an important moment in medical history. In our May 2020 issue, we published only these essays. We continue to publish them online almost daily.

Some of the essays described how the healthcare system—previously thought to be hyperspecialized, profit-driven, and resistant to change—pivoted within days, as hospitalist physicians trained other physicians to “unspecialize” and pediatricians began to care for adults in an otherwise overwhelmed hospital system.^5,6 Another essay focused on the need to trust that medical students who had graduated early would be able to function as physicians.⁷ And yet another essay expressed concern about the widespread use of unproven therapies in hospitalized patients. “Even in times of global pandemic, we need to consider potential harms and adverse consequences of novel treatments,’’ the physicians wrote. “Sometimes inaction is preferable to action.”⁸

Several essays reflected on the impact of the pandemic on healthcare disparities, suggesting that the pandemic had made (the well-known but often ignored) differences in health outcomes between White patients and racial minorities more obvious. Still another essay reflected on the intersection between structural racism, poor access to care, and interpersonal racism, describing the grief caused by losses of Black lives to both police violence and COVID-19.⁹

There also were personal stories of hardship and survival. One hospitalist physician with asthma described coughing as ``the new leprosy.”¹⁰ She wrote, “This is a particularly unpropitious time in history to be a Chinese-American doctor who can’t stop coughing.”

There were drawbacks to our decision to focus on personal essays. Although it was clear even before the pandemic, COVID-19 has highlighted that a path for quick dissemination of original peer-reviewed research is needed. If existing medical journals do not fill that role, websites that publish and disseminate non–peer-reviewed work (aka, “preprints”) will become the preferred method for distribution of high-impact, timely original research.¹¹ The journal’s pivot to reviewing and publishing personal essays may have kept us from improving our approach to rapid peer review and dissemination. In those early days, however, there was no peer-reviewed work to publish, but there was an intense desire (from our members and physicians generally) for information and stories from the front lines. In a way, the essays we published were early “case reports,” that hypothesized about how we might rethink healthcare delivery in pandemic conditions.

Furthermore, our decision to solicit and publish personal essays addressing shortcomings of the federal response and consequences of the pandemic meant that the Journal of Hospital Medicine became part of the pandemic’s political discourse. As editors, we have historically kept the journal away from political arguments or endorsements. In this case, however, we decided that even if some of the opinions were political, they were an appropriate response to the widespread anti-science rhetoric endorsed by the current administration. The resultant erosion of trust in public health has undoubtedly contributed to persistence of the pandemic.¹² A stance against masks, for example, rejects the recommendations of nearly all scientists in favor of (a selfish and problematic idea of) “self-determination.” Those who proclaim that such a mandate infringes on their personal freedom reject evidence-based recommendations of scientists and disregard public health strategies meant to protect everyone.

As we reflect on the past year, our most important lesson may be that our previous emphasis on publishing high-impact original research likely missed important personal and professional insights, insights that could have changed practice, improved patient experience, and reduced physician burnout. Anecdotes are not scientific evidence, but we have discovered their incredible power to help us learn, empathize, commiserate, and survive. Hospitals learned that they must adapt in the moment, a notion that runs counter to the notoriously slow pace of change in paradigms of healthcare. Hospitalists learned to “find their battle buddies” to ward off isolation and to cherish their teams in the face of overwhelming trauma, an approach requiring empathy, humility, and compassion.¹³ We won’t soon forget that, when things were most dire, it was stories—not data—that gave us hope. We look forward to 2021 with great optimism. New vaccines and new federal leaders who value and respect science give us hope that the end of the pandemic is in sight. We are indebted to all frontline workers who have transformed care delivery and remained courageous in the face of great personal risk. As a journal, we will continue, as one scientist noted, to use our “platform for advocacy, unabashedly.”¹⁴

We enter the new year still in the midst of the coronavirus disease 2019 (COVID-19) pandemic and remain humbled by its impact. It is remarkable how much, and how little, has changed. Hospitalists in the early days of the COVID-19 pandemic were struggling. We were caring for patients who were suffering and dying from a new and mysterious disease. There weren’t enough tests (or, if there were tests, there weren’t swabs).¹ We were using protocols for managing respiratory failure that, we would learn later, may not have been the best for improving outcomes. Rumors of unproven therapies came from everywhere: our patients, our colleagues, and even the highest realms of the federal government. We also knew very little about how best to protect ourselves. In many cases, we did not have enough personal protective equipment (PPE). There were no face shields, or “zoom rounds,” or even awareness that we probably shouldn’t sit in the tiny conference room (maskless) discussing patients with the large team of doctors, nurses, respiratory therapists, and social workers.

Perhaps worst of all, we were haunted. We were alarmed by the large numbers of young patients who were ill, and our elderly patients, many of whom we knew and had cared for many times, had suddenly just stopped showing up.² In our free moments, we worried about them; maybe they were afraid to come to the hospital, maybe they were home sick with COVID-19, or maybe they had died alone. And children, initially thought to be spared the most serious consequences of COVID-19, started coming to the hospital with a rare but severe new COVID-19-associated complication, termed multisystem inflammatory syndrome in children (MIS-C). We had to learn to manage yet another manifestation of COVID-19, largely through trial and error.

And, of course, clinical care was only one of our many responsibilities. We were also busy hunting for ventilators, setting up makeshift medical wards and intensive care units, revamping medical education, and scouring the literature for any information to help guide patient care. We worried about getting sick ourselves and bringing the disease home to our families. Our impatience grew as day after day there was no (and still is no) coordinated federal response.

A glimmer of hope slowly emerged. Our colleagues designed and rapidly evaluated respiratory protocols and provided early evidence about the strategies (eg, proning) that were associated with improved outcomes.³ Researchers began to generate knowledge and move us beyond rumors regarding potential therapies. We cheered as our administrators concocted unusual strategies to remedy the PPE and testing shortages.⁴

At the Journal of Hospital Medicine, we were faced with another challenge: How would we describe the chaos and the challenges of being a physician during the COVID-19 era? How would we document the way our colleagues were rising to the challenge and identifying opportunities to rethink hospital care in the United States?

In April, we began to receive a deluge of personal essays from frontline physicians about their experiences with COVID-19. Generally, medical journals publish and disseminate original, high-impact research. Personal essays rarely fit this model. Given the unprecedented circumstances, however, we decided these essays could help chronicle an important moment in medical history. In our May 2020 issue, we published only these essays. We continue to publish them online almost daily.

Some of the essays described how the healthcare system—previously thought to be hyperspecialized, profit-driven, and resistant to change—pivoted within days, as hospitalist physicians trained other physicians to “unspecialize” and pediatricians began to care for adults in an otherwise overwhelmed hospital system.^5,6 Another essay focused on the need to trust that medical students who had graduated early would be able to function as physicians.⁷ And yet another essay expressed concern about the widespread use of unproven therapies in hospitalized patients. “Even in times of global pandemic, we need to consider potential harms and adverse consequences of novel treatments,’’ the physicians wrote. “Sometimes inaction is preferable to action.”⁸

Several essays reflected on the impact of the pandemic on healthcare disparities, suggesting that the pandemic had made (the well-known but often ignored) differences in health outcomes between White patients and racial minorities more obvious. Still another essay reflected on the intersection between structural racism, poor access to care, and interpersonal racism, describing the grief caused by losses of Black lives to both police violence and COVID-19.⁹

There also were personal stories of hardship and survival. One hospitalist physician with asthma described coughing as ``the new leprosy.”¹⁰ She wrote, “This is a particularly unpropitious time in history to be a Chinese-American doctor who can’t stop coughing.”

There were drawbacks to our decision to focus on personal essays. Although it was clear even before the pandemic, COVID-19 has highlighted that a path for quick dissemination of original peer-reviewed research is needed. If existing medical journals do not fill that role, websites that publish and disseminate non–peer-reviewed work (aka, “preprints”) will become the preferred method for distribution of high-impact, timely original research.¹¹ The journal’s pivot to reviewing and publishing personal essays may have kept us from improving our approach to rapid peer review and dissemination. In those early days, however, there was no peer-reviewed work to publish, but there was an intense desire (from our members and physicians generally) for information and stories from the front lines. In a way, the essays we published were early “case reports,” that hypothesized about how we might rethink healthcare delivery in pandemic conditions.

Furthermore, our decision to solicit and publish personal essays addressing shortcomings of the federal response and consequences of the pandemic meant that the Journal of Hospital Medicine became part of the pandemic’s political discourse. As editors, we have historically kept the journal away from political arguments or endorsements. In this case, however, we decided that even if some of the opinions were political, they were an appropriate response to the widespread anti-science rhetoric endorsed by the current administration. The resultant erosion of trust in public health has undoubtedly contributed to persistence of the pandemic.¹² A stance against masks, for example, rejects the recommendations of nearly all scientists in favor of (a selfish and problematic idea of) “self-determination.” Those who proclaim that such a mandate infringes on their personal freedom reject evidence-based recommendations of scientists and disregard public health strategies meant to protect everyone.

As we reflect on the past year, our most important lesson may be that our previous emphasis on publishing high-impact original research likely missed important personal and professional insights, insights that could have changed practice, improved patient experience, and reduced physician burnout. Anecdotes are not scientific evidence, but we have discovered their incredible power to help us learn, empathize, commiserate, and survive. Hospitals learned that they must adapt in the moment, a notion that runs counter to the notoriously slow pace of change in paradigms of healthcare. Hospitalists learned to “find their battle buddies” to ward off isolation and to cherish their teams in the face of overwhelming trauma, an approach requiring empathy, humility, and compassion.¹³ We won’t soon forget that, when things were most dire, it was stories—not data—that gave us hope. We look forward to 2021 with great optimism. New vaccines and new federal leaders who value and respect science give us hope that the end of the pandemic is in sight. We are indebted to all frontline workers who have transformed care delivery and remained courageous in the face of great personal risk. As a journal, we will continue, as one scientist noted, to use our “platform for advocacy, unabashedly.”¹⁴

We enter the new year still in the midst of the coronavirus disease 2019 (COVID-19) pandemic and remain humbled by its impact. It is remarkable how much, and how little, has changed. Hospitalists in the early days of the COVID-19 pandemic were struggling. We were caring for patients who were suffering and dying from a new and mysterious disease. There weren’t enough tests (or, if there were tests, there weren’t swabs).¹ We were using protocols for managing respiratory failure that, we would learn later, may not have been the best for improving outcomes. Rumors of unproven therapies came from everywhere: our patients, our colleagues, and even the highest realms of the federal government. We also knew very little about how best to protect ourselves. In many cases, we did not have enough personal protective equipment (PPE). There were no face shields, or “zoom rounds,” or even awareness that we probably shouldn’t sit in the tiny conference room (maskless) discussing patients with the large team of doctors, nurses, respiratory therapists, and social workers.

Perhaps worst of all, we were haunted. We were alarmed by the large numbers of young patients who were ill, and our elderly patients, many of whom we knew and had cared for many times, had suddenly just stopped showing up.² In our free moments, we worried about them; maybe they were afraid to come to the hospital, maybe they were home sick with COVID-19, or maybe they had died alone. And children, initially thought to be spared the most serious consequences of COVID-19, started coming to the hospital with a rare but severe new COVID-19-associated complication, termed multisystem inflammatory syndrome in children (MIS-C). We had to learn to manage yet another manifestation of COVID-19, largely through trial and error.

And, of course, clinical care was only one of our many responsibilities. We were also busy hunting for ventilators, setting up makeshift medical wards and intensive care units, revamping medical education, and scouring the literature for any information to help guide patient care. We worried about getting sick ourselves and bringing the disease home to our families. Our impatience grew as day after day there was no (and still is no) coordinated federal response.

A glimmer of hope slowly emerged. Our colleagues designed and rapidly evaluated respiratory protocols and provided early evidence about the strategies (eg, proning) that were associated with improved outcomes.³ Researchers began to generate knowledge and move us beyond rumors regarding potential therapies. We cheered as our administrators concocted unusual strategies to remedy the PPE and testing shortages.⁴

At the Journal of Hospital Medicine, we were faced with another challenge: How would we describe the chaos and the challenges of being a physician during the COVID-19 era? How would we document the way our colleagues were rising to the challenge and identifying opportunities to rethink hospital care in the United States?

In April, we began to receive a deluge of personal essays from frontline physicians about their experiences with COVID-19. Generally, medical journals publish and disseminate original, high-impact research. Personal essays rarely fit this model. Given the unprecedented circumstances, however, we decided these essays could help chronicle an important moment in medical history. In our May 2020 issue, we published only these essays. We continue to publish them online almost daily.

Some of the essays described how the healthcare system—previously thought to be hyperspecialized, profit-driven, and resistant to change—pivoted within days, as hospitalist physicians trained other physicians to “unspecialize” and pediatricians began to care for adults in an otherwise overwhelmed hospital system.^5,6 Another essay focused on the need to trust that medical students who had graduated early would be able to function as physicians.⁷ And yet another essay expressed concern about the widespread use of unproven therapies in hospitalized patients. “Even in times of global pandemic, we need to consider potential harms and adverse consequences of novel treatments,’’ the physicians wrote. “Sometimes inaction is preferable to action.”⁸

Several essays reflected on the impact of the pandemic on healthcare disparities, suggesting that the pandemic had made (the well-known but often ignored) differences in health outcomes between White patients and racial minorities more obvious. Still another essay reflected on the intersection between structural racism, poor access to care, and interpersonal racism, describing the grief caused by losses of Black lives to both police violence and COVID-19.⁹

There also were personal stories of hardship and survival. One hospitalist physician with asthma described coughing as ``the new leprosy.”¹⁰ She wrote, “This is a particularly unpropitious time in history to be a Chinese-American doctor who can’t stop coughing.”

There were drawbacks to our decision to focus on personal essays. Although it was clear even before the pandemic, COVID-19 has highlighted that a path for quick dissemination of original peer-reviewed research is needed. If existing medical journals do not fill that role, websites that publish and disseminate non–peer-reviewed work (aka, “preprints”) will become the preferred method for distribution of high-impact, timely original research.¹¹ The journal’s pivot to reviewing and publishing personal essays may have kept us from improving our approach to rapid peer review and dissemination. In those early days, however, there was no peer-reviewed work to publish, but there was an intense desire (from our members and physicians generally) for information and stories from the front lines. In a way, the essays we published were early “case reports,” that hypothesized about how we might rethink healthcare delivery in pandemic conditions.

Furthermore, our decision to solicit and publish personal essays addressing shortcomings of the federal response and consequences of the pandemic meant that the Journal of Hospital Medicine became part of the pandemic’s political discourse. As editors, we have historically kept the journal away from political arguments or endorsements. In this case, however, we decided that even if some of the opinions were political, they were an appropriate response to the widespread anti-science rhetoric endorsed by the current administration. The resultant erosion of trust in public health has undoubtedly contributed to persistence of the pandemic.¹² A stance against masks, for example, rejects the recommendations of nearly all scientists in favor of (a selfish and problematic idea of) “self-determination.” Those who proclaim that such a mandate infringes on their personal freedom reject evidence-based recommendations of scientists and disregard public health strategies meant to protect everyone.

As we reflect on the past year, our most important lesson may be that our previous emphasis on publishing high-impact original research likely missed important personal and professional insights, insights that could have changed practice, improved patient experience, and reduced physician burnout. Anecdotes are not scientific evidence, but we have discovered their incredible power to help us learn, empathize, commiserate, and survive. Hospitals learned that they must adapt in the moment, a notion that runs counter to the notoriously slow pace of change in paradigms of healthcare. Hospitalists learned to “find their battle buddies” to ward off isolation and to cherish their teams in the face of overwhelming trauma, an approach requiring empathy, humility, and compassion.¹³ We won’t soon forget that, when things were most dire, it was stories—not data—that gave us hope. We look forward to 2021 with great optimism. New vaccines and new federal leaders who value and respect science give us hope that the end of the pandemic is in sight. We are indebted to all frontline workers who have transformed care delivery and remained courageous in the face of great personal risk. As a journal, we will continue, as one scientist noted, to use our “platform for advocacy, unabashedly.”¹⁴

Last year we pledged to lead by example and improve representation within the Journal of Hospital Medicine community.¹ By emphasizing diversity, we expand the pool of faculty to whom leadership opportunities are available. A diverse team will put forth a broader range of ideas for consideration, spur greater innovation, and promote diversity in both published content and authorship, ensuring that the spectrum of content we publish reflects and benefits all patients to whom we provide care.

We write to share our progress, first reporting on gender equity. Currently, 45% of the journal leadership team are women, increased from 30% in 2018. In the past year, we also developed processes to collect peer reviewer and author demographic information through our manuscript management system. These processes helped us understand our baseline state.

Prior to developing these processes, we discussed our goals and potential approaches with Society of Hospital Medicine leaders; medical school deans of diversity, equity, and inclusion; department chairs in pediatrics and internal medicine; women, underrepresented minorities, and LGBTQ+ faculty; and trainees. We achieved consensus as a journal leadership team and implemented a new data collection system in July 2019. We focused on first and last authors given the importance of these positions for promotion and tenure. We requested that peer reviewers and authors provide demographic data, including gender (with nonbinary as an option), race, and ethnicity; “prefer not to answer” was a response option for each question. These data were not available during the manuscript decision process. Authors who did not submit information received up to three reminder emails from the Editor-in-Chief encouraging them to provide demographic information and stating the rationale for the request. We did not use gender identifying algorithms (eg, assignment of gender probability based on name) or visit professional websites; our intent was author self-identification.

We categorized Journal of Hospital Medicine article types as research, generally solicited, and generally unsolicited (Table). Among research articles, the proportion of women and men were similar with women accounting for 47% of first authors (vs 47% men) and 33% of last authors (vs 35% men) (Table). However, 27% of last authors left this field blank. Among solicited article types, there was an equal proportion of women and men for first but not for last authors. Among unsolicited article types, a smaller proportion of women accounted for first authors. While the proportion of women and men was equal among last authors, 45% left this field blank.

jhm01509517_t1.JPG

Collecting author demographics and reporting our data on gender represent an important first step for the journal. In the upcoming year, we will develop strategies to obtain more complete data and report our performance on race, ethnicity, and intersectionality, and continue deliberate efforts to improve equity within all areas of the journal, including reviewer, author, and editorial roles. We are committed to continue sharing our progress.

Last year we pledged to lead by example and improve representation within the Journal of Hospital Medicine community.¹ By emphasizing diversity, we expand the pool of faculty to whom leadership opportunities are available. A diverse team will put forth a broader range of ideas for consideration, spur greater innovation, and promote diversity in both published content and authorship, ensuring that the spectrum of content we publish reflects and benefits all patients to whom we provide care.

We write to share our progress, first reporting on gender equity. Currently, 45% of the journal leadership team are women, increased from 30% in 2018. In the past year, we also developed processes to collect peer reviewer and author demographic information through our manuscript management system. These processes helped us understand our baseline state.

Prior to developing these processes, we discussed our goals and potential approaches with Society of Hospital Medicine leaders; medical school deans of diversity, equity, and inclusion; department chairs in pediatrics and internal medicine; women, underrepresented minorities, and LGBTQ+ faculty; and trainees. We achieved consensus as a journal leadership team and implemented a new data collection system in July 2019. We focused on first and last authors given the importance of these positions for promotion and tenure. We requested that peer reviewers and authors provide demographic data, including gender (with nonbinary as an option), race, and ethnicity; “prefer not to answer” was a response option for each question. These data were not available during the manuscript decision process. Authors who did not submit information received up to three reminder emails from the Editor-in-Chief encouraging them to provide demographic information and stating the rationale for the request. We did not use gender identifying algorithms (eg, assignment of gender probability based on name) or visit professional websites; our intent was author self-identification.

We categorized Journal of Hospital Medicine article types as research, generally solicited, and generally unsolicited (Table). Among research articles, the proportion of women and men were similar with women accounting for 47% of first authors (vs 47% men) and 33% of last authors (vs 35% men) (Table). However, 27% of last authors left this field blank. Among solicited article types, there was an equal proportion of women and men for first but not for last authors. Among unsolicited article types, a smaller proportion of women accounted for first authors. While the proportion of women and men was equal among last authors, 45% left this field blank.

jhm01509517_t1.JPG

Collecting author demographics and reporting our data on gender represent an important first step for the journal. In the upcoming year, we will develop strategies to obtain more complete data and report our performance on race, ethnicity, and intersectionality, and continue deliberate efforts to improve equity within all areas of the journal, including reviewer, author, and editorial roles. We are committed to continue sharing our progress.

Last year we pledged to lead by example and improve representation within the Journal of Hospital Medicine community.¹ By emphasizing diversity, we expand the pool of faculty to whom leadership opportunities are available. A diverse team will put forth a broader range of ideas for consideration, spur greater innovation, and promote diversity in both published content and authorship, ensuring that the spectrum of content we publish reflects and benefits all patients to whom we provide care.

We write to share our progress, first reporting on gender equity. Currently, 45% of the journal leadership team are women, increased from 30% in 2018. In the past year, we also developed processes to collect peer reviewer and author demographic information through our manuscript management system. These processes helped us understand our baseline state.

Prior to developing these processes, we discussed our goals and potential approaches with Society of Hospital Medicine leaders; medical school deans of diversity, equity, and inclusion; department chairs in pediatrics and internal medicine; women, underrepresented minorities, and LGBTQ+ faculty; and trainees. We achieved consensus as a journal leadership team and implemented a new data collection system in July 2019. We focused on first and last authors given the importance of these positions for promotion and tenure. We requested that peer reviewers and authors provide demographic data, including gender (with nonbinary as an option), race, and ethnicity; “prefer not to answer” was a response option for each question. These data were not available during the manuscript decision process. Authors who did not submit information received up to three reminder emails from the Editor-in-Chief encouraging them to provide demographic information and stating the rationale for the request. We did not use gender identifying algorithms (eg, assignment of gender probability based on name) or visit professional websites; our intent was author self-identification.

We categorized Journal of Hospital Medicine article types as research, generally solicited, and generally unsolicited (Table). Among research articles, the proportion of women and men were similar with women accounting for 47% of first authors (vs 47% men) and 33% of last authors (vs 35% men) (Table). However, 27% of last authors left this field blank. Among solicited article types, there was an equal proportion of women and men for first but not for last authors. Among unsolicited article types, a smaller proportion of women accounted for first authors. While the proportion of women and men was equal among last authors, 45% left this field blank.

jhm01509517_t1.JPG

Collecting author demographics and reporting our data on gender represent an important first step for the journal. In the upcoming year, we will develop strategies to obtain more complete data and report our performance on race, ethnicity, and intersectionality, and continue deliberate efforts to improve equity within all areas of the journal, including reviewer, author, and editorial roles. We are committed to continue sharing our progress.

Children with neurologic impairment (NI; eg, hypoxic-­ischemic encephalopathy, muscular dystrophy) are characterized by functional and/or intellectual impairments resulting from a variety of neurologic diseases.¹ These children commonly have respiratory comorbidities, including central hypoventilation, impaired cough, and oromotor dysfunction, that may lead to chronic respiratory insufficiency and a need for chronic respiratory support at baseline.^2,3 Baseline respiratory support modalities can include supplemental oxygen, noninvasive positive pressure ventilation, or invasive mechanical ventilation.

Acute respiratory infections (ARI; eg, pneumonia, bronchiolitis) are the most common cause of hospitalization, intensive care unit (ICU) admission, and death for children with NI.^1,3 Discharge criteria for otherwise healthy children admitted to the hospital with ARI often include return to respiratory baseline.⁴ Children with complex chronic conditions have longer hospitalizations when hospitalized with respiratory infections,^5-7 because, in part, comorbidities and complications prolong the time to return to baseline. This prolonged return to respiratory baseline in combination with family knowledge, comfort, and skill in managing respiratory support and other complexities at home may alter discharge practices in the population of children with NI. In our clinical experience, discharge before return to baseline respiratory support occurs more frequently in children with NI than in otherwise healthy children when hospitalized with ARI. However, the consequences of discharging children with NI prior to return to respiratory baseline are unknown.

In this study, we sought to determine if discharge prior to return to baseline respiratory support is associated with reutilization among children with NI hospitalized with ARI. We hypothesized that patients discharged prior to return to respiratory baseline would have higher rates of 30-day hospital reutilization.

Study Design and Data Source

This single-center, retrospective cohort study of children hospitalized at Cincinnati Children’s Hospital Medical Center (CCHMC) used data from the Pediatric Health Information System (PHIS) and the electronic medical record (EMR). PHIS, an administrative database of 45 not-for-profit, tertiary care, US pediatric hospitals managed by Children’s Hospital Association (Lenexa, Kansas), was used to identify eligible children, examine demographic and clinical variables, and define outcomes. PHIS contains data regarding patient demographics, inpatient resource utilization, and diagnoses. Encrypted medical record numbers in PHIS allowed for local identification of patients’ medical records to complete EMR review to confirm eligibility and obtain detailed patient-level clinical information (eg, respiratory support needs) not available in PHIS.

Pilot medical record reviews allowed for standardized study definitions and procedures. All study staff underwent training with the primary investigator, including detailed review of 10 initial abstractions. Two investigators (K.M. and S.C.) performed repeat abstractions from 40 randomly selected records to enable assessment of interrater reliability. Average reliability, indicated by the κ statistic, indicated substantial to near-perfect reliability⁸ (κ = 0.97, 95% CI 0.90-1.00) for the primary exposure. EMR data were managed using Research Electronic Data Capture (REDCap, Nashville, Tennessee)⁹ and subsequently merged with PHIS data.

Study Population

Hospitalizations of children with NI aged 1 to 18 years at CCHMC between January 2010 and September 2015 were eligible for inclusion if they had a principal discharge diagnosis indicative of ARI and required increased respiratory support from baseline during hospitalization. NI was defined as a high-intensity, chronic neurological diagnosis with substantial functional impairments according to previously defined diagnosis codes.^1,10 ARI was identified using codes in the Clinical Classification Software (Agency for Healthcare Research and Quality, Rockville, MD) respiratory group indicative of ARI (eg, pneumonia, bronchiolitis, influenza; Appendix Table).

Children transferred to CCHMC were excluded because records from their initial illness presentation and management were not available. Because of expected differences in management and outcomes, children with a known diagnosis of tuberculosis or human immunodeficiency virus were excluded. Because exposure criteria were dependent on hospital discharge status, hospitalizations for children who died during admission (4 of 632 hospitalizations, 0.63%) were excluded from the final cohort (Appendix Figure).

Study Definitions

Baseline respiratory support (ie, “respiratory baseline”) was defined as the child’s highest level of respiratory support needed prior to admission when well (ie, no support, supplemental oxygen, continuous positive airway pressure [CPAP] or bilevel positive airway pressure [BiPAP], or ventilator support), and further characterized by night or day/night requirement. Respiratory baseline was identified using EMR documentation of home respiratory support use at the time of index admission. Return to respiratory baseline was defined as the date on which the child achieved documented home respiratory support settings, regardless of clinical symptoms.

Children may have required increased respiratory support from baseline at any time during hospitalization. Maximum respiratory support required was categorized as one of the following: (1) initiation of supplemental oxygen or increase in oxygen flow or duration; (2) initiation of CPAP or BiPAP; (3) increase in pressure settings or duration of pressure support for those with baseline CPAP, BiPAP, or ventilator use; and (4) initiation of full mechanical ventilation. Respiratory support categories were mutually exclusive: children requiring multiple types of increased respiratory support were classified for analysis by the most invasive form of respiratory support used (eg, a child requiring increase in both oxygen flow and pressure settings was categorized as an increase in pressure settings). Children who received heated high-flow nasal cannula therapy as maximum support were categorized as initiation or increase in oxygen support.

Time to return to respiratory baseline was defined as the difference in days between date of return to respiratory baseline and date of admission. Time to return to respiratory baseline was determined only for children who were discharged at respiratory baseline.

Primary Exposure and Outcome Measures

The primary exposure was hospital discharge before return to respiratory baseline (ie, discharge on higher respiratory support than at baseline settings). At our institution, standardized discharge criteria for children with NI do not exist. The primary outcome was all-cause, 30-day hospital reutilization, including hospital readmissions and emergency department (ED) revisits. Secondary outcomes included 30-day reutilization for ARI and hospital length of stay (LOS) in days.

Patient Demographics and Clinical Characteristics

Demographic and patient characteristics that might influence hospital discharge before return to respiratory baseline or readmission were obtained from PHIS (eg, demographic information, age, insurance type, measures of clinical complexity, illness severity) and by EMR review (eg, baseline respiratory support needs, maximum respiratory support during hospitalization). Measures of clinical complexity included comorbid complex chronic conditions (CCCs)^11-14 and technology dependence^14-16 using previously defined diagnostic codes. Measures of illness severity included sepsis¹⁷ and ICU-level care. At our institution, children with baseline ventilator use do not require admission to the ICU unless they are clinically unstable.

Statistical Analysis

Continuous variables were described using medians and interquartile ranges (IQR). Categorical variables were described using counts and percentages. Patient characteristics and outcomes were stratified by primary exposure and compared using chi-square test or Fisher exact test for categorical variables and Wilcoxon rank sum test for continuous variables.

To examine the independent association between discharge before return to respiratory baseline and hospital reutilization, a generalized estimating equation was used that included potential confounders while accounting for within-patient clustering. Patient demographics included age, race, ethnicity, and insurance type; measures of clinical complexity included number of CCCs, technology dependence, and baseline respiratory support; and measures of acute illness severity included ARI diagnosis, degree of increase in respiratory support during hospitalization, and ICU-level care. LOS was also included in the model as a covariate because of its expected association with both exposure and outcome.

Secondary analyses were conducted using the outcome of 30-day reutilization for ARI. Subgroup analysis excluding hospitalizations of children lost to follow-up (ie, no encounters in the 6 months after hospital discharge) was also conducted. All analyses were performed with SAS v9.3 (SAS Institute, Cary, North Carolina). P values < .05 were considered statistically significant. This study was approved by the Institutional Review Board.

Study Cohort

A total of 632 hospitalizations experienced by 366 children with NI who were admitted with ARI were included (Appendix Figure). Most children (66.4%) in the cohort experienced only one hospitalization, 17.5% had two hospitalizations, 7.9% had three hospitalizations, and 8.2% had four or more hospitalizations. The median age at hospitalization was 5.0 years (IQR 2.8-10.5) and most hospitalizations were for children who were male (56.6%), white (78.3%), non-Hispanic (96.0%), and publicly insured (51.7%; Table 1). More than one-quarter (28.6%) of hospitalizations were for children with four or more CCCs, and in 73.4% of hospitalizations, children were technology dependent (Table 1). Baseline respiratory support was common (46.8%), including home mechanical ventilation in 11.1% of hospitalizations (Table 1). Bacterial pneumonia, including aspiration pneumonia, was the most common discharge diagnosis (50.5%, Table 1).

steuart06700520e_t1.jpg

Demographic and Clinical Characteristics

Children were discharged before return to respiratory baseline in 30.4% of hospitalizations (Appendix Figure). Children discharged before return to respiratory baseline were older (median age 5.7 years, IQR 3.1-11.0, vs 4.9 years, IQR 2.6-9.7; P = .04) and more likely to be privately insured (54.2% vs 43.4%; P = .04), compared with children discharged at respiratory baseline (Table 1). Children discharged before return to respiratory baseline were also more likely to have a respiratory CCC (59.9% vs 30.9%; P < .001), have a respiratory technology dependence diagnosis code (44.8% vs 24.1%; P < .001), and have baseline respiratory support needs on EMR review (67.7% vs 37.7%; P < .001), compared with children discharged at baseline (Table 1).

Children discharged before return to respiratory baseline required significantly greater escalation in respiratory support during hospitalization, compared with children discharged at respiratory baseline, including higher rates of initiation of CPAP or BiPAP, increased pressure settings from baseline (for home CPAP, BiPAP, or ventilator users), and initiation of full mechanical ventilation (Table 1). Hospitalizations in which children were discharged before return to respiratory baseline were also more likely to include ICU care than were those for children discharged at baseline (52.1% vs 35.2%; P < .001; Table 1).

Clinical Outcomes and Utilization

Reutilization within 30 days occurred after 32.1% of hospitalizations, with 26.1% requiring hospital readmission and 6.0% requiring ED revisit (Table 2). There was no statistical association in either unadjusted (Table 2) or adjusted (Table 3) analysis between children discharged before return to respiratory baseline and 30-day all-cause hospital reutilizations, hospital readmissions, or ED revisits.

steuart06700520e_t2.jpg

In analysis of secondary outcomes, 30-day reutilization because of ARI occurred after 21.5% of hospitalizations, with 19.0% requiring hospital readmission and 2.5% requiring ED revisit. Median hospital LOS for the cohort was 4 days (IQR 2-8; Table 2). Hospitalizations in which children were discharged before return to respiratory baseline were longer than in those discharged at baseline (median 6 days, IQR 3-11, vs 4 days, IQR 2-7; P < .001; Table 2).

steuart06700520e_t3.jpg

For hospitalizations of children discharged at respiratory baseline, the median time to return to respiratory baseline was 3 days (IQR 1-5, complete range 0-80). In these encounters, discharge occurred soon after return to respiratory baseline (median 1 day, IQR 0-1.5, complete range 0-54).

In subgroup analysis excluding the 18 hospitalizations in which children were lost to follow-up (2.8% of the total cohort), discharge before return to respiratory baseline was not associated with 30-day all-cause hospital reutilization (Table 4).

steuart06700520e_t4.jpg

In this retrospective cohort study, children with NI hospitalized with ARI were frequently discharged using increased respiratory support from baseline. However, those discharged before return to respiratory baseline, despite their greater clinical complexity and acute illness severity, did not have increased hospital reutilization, compared with children discharged at respiratory baseline. Our findings suggest that discharge before return to baseline respiratory support after ARI may be clinically appropriate in some children with NI.

With the growing emphasis on decreasing hospital costs, concern exists that patients are being discharged from hospitals “quicker and sicker,”^18,19 with shortening lengths of stay and higher patient instability at discharge. Clinical instability at discharge has been associated with adverse postdischarge outcomes in adults with pneumonia^20-23; however, studies evaluating discharge readiness have not examined the population of children with NI. Our findings of no difference in reutilization for children with NI discharged before return to respiratory baseline, which would be expected to approximate one or more clinical instabilities, contrast these concerns.

Clinicians caring for children with NI hospitalized with ARI may find it difficult to determine a child’s discharge readiness, in part because many children with NI have longer times to return to respiratory baseline and some never return to their pre-­illness baseline.²⁴ In otherwise healthy children hospitalized with respiratory infections such as pneumonia, discharge criteria typically include complete wean from respiratory support prior to discharge.^4,25 In our study’s more complex children, whose parents already manage respiratory support at home, we hypothesize that discharging providers may be comfortable with discharge when the child has certain types of increased respiratory support compatible with home equipment, a parent skilled with monitoring the child’s respiratory status, and the support of an experienced outpatient provider and home nursing providers. At our institution, outpatient respiratory support weans are primarily performed by pediatric pulmonologists and, for isolated weaning of supplemental oxygen or time using support, by parents and outpatient pediatricians.

Another important factor in determining a child’s discharge readiness is the perspective of the child’s parent. Berry et al found that children whose parents believe they are not healthy enough for discharge are more likely to experience unplanned hospital readmissions,²⁴ signaling the role of child- and family-­specific factors in safe discharge decisions. Therefore, parents of children with NI should be proactively involved throughout the multidisciplinary discharge process,^26,27 including the decision to discharge before return to respiratory baseline. Parents have identified ongoing provider support, opportunities to practice home care skills, and written instructions with contingency plans as important components of discharge readiness.²⁸ Further work to create partnerships with these highly skilled caregivers in discharge decision making and transition planning are needed to promote safe discharge practices in this complex population.

In our study, children discharged before return to respiratory baseline were more likely to be older and privately insured compared with children discharged at respiratory baseline. Prior studies have found that social factors including low socioeconomic status influence ED provider admissions decisions for children with pneumonia.^29,30 However, the role of socioeconomic factors in provider discharge decisions for children with NI has not been assessed. These traits may also be proxy markers of other sociodemographic factors, such as parent education level, financial hardship influencing ability to participate in a child’s care at the bedside, access to comprehensive outpatient primary care, and availability of private home nursing. We hypothesize that these related characteristics directly and indirectly influence provider discharge decisions.

Discharging providers are likely more comfortable with discharge prior to return to respiratory baseline when the family has private duty nursing in the home. Home nurses can assist families in providing increased respiratory support and recognizing respiratory problems that may arise following discharge. However, home nursing shortages are common nationwide.^31,32 Low-income children, children with respiratory technology use, and children without Medicaid have been found to have larger gaps in home nursing availability.^31,32 Further studies are needed to understand the role of home nursing availability in provider discharge decisions in this population.

This study has several limitations. The retrospective design of this study creates the potential for residual confounding; there may be other clinical or demographic factors influencing hospital discharge decisions that we are unable to capture using EMR review, including parental knowledge and comfort managing illness, quality of discharge instructions, frequency of follow-up visits, and presence of skilled home nursing services. Categorization of children based on respiratory support status at discharge lends potential for misclassification of exposure; however, our substantial interrater reliability suggests that misclassification bias is small. This study’s primary finding indicated no difference between exposure groups; although we may be unable to detect small differences, we had sufficient power with our sample size to detect meaningful differences in reutilization outcomes.

This study was not designed to capture outpatient time to return to respiratory baseline; prospective studies are needed to identify rates of return to respiratory baseline following ARI in children with NI. We did not measure the level of respiratory support used by children at the time of discharge and, therefore, are unable to estimate the amount of respiratory support weaning needed following discharge or the compatibility of support with home equipment using our data. In addition, this study focused on respiratory support modalities and, thus, did not measure inpatient utilization of mucociliary clearance technologies that might be hypothesized to decrease the time to return to baseline respiratory support. Next steps in evaluating treatment of ARI include investigating the effect of mucociliary clearance on both exposure and outcome in this population.

There may be other clinically meaningful outcomes for this population apart from reutilization that we have not assessed in this study, including increased respiratory support required following discharge, primary care reutilization, healthcare costs, or parent satisfaction with timing of and outcomes after discharge. Finally, although our hospital has reutilization rates for children with NI that are similar to other institutions in the United States,³³ our results may not be generalizable to children with NI hospitalized at other institutions because local discharge processes and systems of care may be different. Prospective, multicenter investigation is needed to evaluate the clinical consequences of discharge before return to respiratory baseline more broadly.

At our institution, approximately one-quarter of children with NI hospitalized with ARI were discharged before return to respiratory baseline, but these children were not at increased risk of reutilization, compared with children discharged at respiratory baseline. Our findings suggest that return to baseline respiratory support might not be a necessary component of hospital discharge criteria. In otherwise clinically stable children with NI, discharge before return to respiratory baseline may be reasonable if their parents are comfortable managing respiratory support at home.

The authors thank Jonathan Rodean of the Children’s Hospital Association for his assistance with abstraction of PHIS data.

Children with neurologic impairment (NI; eg, hypoxic-­ischemic encephalopathy, muscular dystrophy) are characterized by functional and/or intellectual impairments resulting from a variety of neurologic diseases.¹ These children commonly have respiratory comorbidities, including central hypoventilation, impaired cough, and oromotor dysfunction, that may lead to chronic respiratory insufficiency and a need for chronic respiratory support at baseline.^2,3 Baseline respiratory support modalities can include supplemental oxygen, noninvasive positive pressure ventilation, or invasive mechanical ventilation.

Acute respiratory infections (ARI; eg, pneumonia, bronchiolitis) are the most common cause of hospitalization, intensive care unit (ICU) admission, and death for children with NI.^1,3 Discharge criteria for otherwise healthy children admitted to the hospital with ARI often include return to respiratory baseline.⁴ Children with complex chronic conditions have longer hospitalizations when hospitalized with respiratory infections,^5-7 because, in part, comorbidities and complications prolong the time to return to baseline. This prolonged return to respiratory baseline in combination with family knowledge, comfort, and skill in managing respiratory support and other complexities at home may alter discharge practices in the population of children with NI. In our clinical experience, discharge before return to baseline respiratory support occurs more frequently in children with NI than in otherwise healthy children when hospitalized with ARI. However, the consequences of discharging children with NI prior to return to respiratory baseline are unknown.

In this study, we sought to determine if discharge prior to return to baseline respiratory support is associated with reutilization among children with NI hospitalized with ARI. We hypothesized that patients discharged prior to return to respiratory baseline would have higher rates of 30-day hospital reutilization.

Study Design and Data Source

This single-center, retrospective cohort study of children hospitalized at Cincinnati Children’s Hospital Medical Center (CCHMC) used data from the Pediatric Health Information System (PHIS) and the electronic medical record (EMR). PHIS, an administrative database of 45 not-for-profit, tertiary care, US pediatric hospitals managed by Children’s Hospital Association (Lenexa, Kansas), was used to identify eligible children, examine demographic and clinical variables, and define outcomes. PHIS contains data regarding patient demographics, inpatient resource utilization, and diagnoses. Encrypted medical record numbers in PHIS allowed for local identification of patients’ medical records to complete EMR review to confirm eligibility and obtain detailed patient-level clinical information (eg, respiratory support needs) not available in PHIS.

Pilot medical record reviews allowed for standardized study definitions and procedures. All study staff underwent training with the primary investigator, including detailed review of 10 initial abstractions. Two investigators (K.M. and S.C.) performed repeat abstractions from 40 randomly selected records to enable assessment of interrater reliability. Average reliability, indicated by the κ statistic, indicated substantial to near-perfect reliability⁸ (κ = 0.97, 95% CI 0.90-1.00) for the primary exposure. EMR data were managed using Research Electronic Data Capture (REDCap, Nashville, Tennessee)⁹ and subsequently merged with PHIS data.

Study Population

Hospitalizations of children with NI aged 1 to 18 years at CCHMC between January 2010 and September 2015 were eligible for inclusion if they had a principal discharge diagnosis indicative of ARI and required increased respiratory support from baseline during hospitalization. NI was defined as a high-intensity, chronic neurological diagnosis with substantial functional impairments according to previously defined diagnosis codes.^1,10 ARI was identified using codes in the Clinical Classification Software (Agency for Healthcare Research and Quality, Rockville, MD) respiratory group indicative of ARI (eg, pneumonia, bronchiolitis, influenza; Appendix Table).

Children transferred to CCHMC were excluded because records from their initial illness presentation and management were not available. Because of expected differences in management and outcomes, children with a known diagnosis of tuberculosis or human immunodeficiency virus were excluded. Because exposure criteria were dependent on hospital discharge status, hospitalizations for children who died during admission (4 of 632 hospitalizations, 0.63%) were excluded from the final cohort (Appendix Figure).

Study Definitions

Baseline respiratory support (ie, “respiratory baseline”) was defined as the child’s highest level of respiratory support needed prior to admission when well (ie, no support, supplemental oxygen, continuous positive airway pressure [CPAP] or bilevel positive airway pressure [BiPAP], or ventilator support), and further characterized by night or day/night requirement. Respiratory baseline was identified using EMR documentation of home respiratory support use at the time of index admission. Return to respiratory baseline was defined as the date on which the child achieved documented home respiratory support settings, regardless of clinical symptoms.

Children may have required increased respiratory support from baseline at any time during hospitalization. Maximum respiratory support required was categorized as one of the following: (1) initiation of supplemental oxygen or increase in oxygen flow or duration; (2) initiation of CPAP or BiPAP; (3) increase in pressure settings or duration of pressure support for those with baseline CPAP, BiPAP, or ventilator use; and (4) initiation of full mechanical ventilation. Respiratory support categories were mutually exclusive: children requiring multiple types of increased respiratory support were classified for analysis by the most invasive form of respiratory support used (eg, a child requiring increase in both oxygen flow and pressure settings was categorized as an increase in pressure settings). Children who received heated high-flow nasal cannula therapy as maximum support were categorized as initiation or increase in oxygen support.

Time to return to respiratory baseline was defined as the difference in days between date of return to respiratory baseline and date of admission. Time to return to respiratory baseline was determined only for children who were discharged at respiratory baseline.

Primary Exposure and Outcome Measures

The primary exposure was hospital discharge before return to respiratory baseline (ie, discharge on higher respiratory support than at baseline settings). At our institution, standardized discharge criteria for children with NI do not exist. The primary outcome was all-cause, 30-day hospital reutilization, including hospital readmissions and emergency department (ED) revisits. Secondary outcomes included 30-day reutilization for ARI and hospital length of stay (LOS) in days.

Patient Demographics and Clinical Characteristics

Demographic and patient characteristics that might influence hospital discharge before return to respiratory baseline or readmission were obtained from PHIS (eg, demographic information, age, insurance type, measures of clinical complexity, illness severity) and by EMR review (eg, baseline respiratory support needs, maximum respiratory support during hospitalization). Measures of clinical complexity included comorbid complex chronic conditions (CCCs)^11-14 and technology dependence^14-16 using previously defined diagnostic codes. Measures of illness severity included sepsis¹⁷ and ICU-level care. At our institution, children with baseline ventilator use do not require admission to the ICU unless they are clinically unstable.

Statistical Analysis

Continuous variables were described using medians and interquartile ranges (IQR). Categorical variables were described using counts and percentages. Patient characteristics and outcomes were stratified by primary exposure and compared using chi-square test or Fisher exact test for categorical variables and Wilcoxon rank sum test for continuous variables.

To examine the independent association between discharge before return to respiratory baseline and hospital reutilization, a generalized estimating equation was used that included potential confounders while accounting for within-patient clustering. Patient demographics included age, race, ethnicity, and insurance type; measures of clinical complexity included number of CCCs, technology dependence, and baseline respiratory support; and measures of acute illness severity included ARI diagnosis, degree of increase in respiratory support during hospitalization, and ICU-level care. LOS was also included in the model as a covariate because of its expected association with both exposure and outcome.

Secondary analyses were conducted using the outcome of 30-day reutilization for ARI. Subgroup analysis excluding hospitalizations of children lost to follow-up (ie, no encounters in the 6 months after hospital discharge) was also conducted. All analyses were performed with SAS v9.3 (SAS Institute, Cary, North Carolina). P values < .05 were considered statistically significant. This study was approved by the Institutional Review Board.

Study Cohort

A total of 632 hospitalizations experienced by 366 children with NI who were admitted with ARI were included (Appendix Figure). Most children (66.4%) in the cohort experienced only one hospitalization, 17.5% had two hospitalizations, 7.9% had three hospitalizations, and 8.2% had four or more hospitalizations. The median age at hospitalization was 5.0 years (IQR 2.8-10.5) and most hospitalizations were for children who were male (56.6%), white (78.3%), non-Hispanic (96.0%), and publicly insured (51.7%; Table 1). More than one-quarter (28.6%) of hospitalizations were for children with four or more CCCs, and in 73.4% of hospitalizations, children were technology dependent (Table 1). Baseline respiratory support was common (46.8%), including home mechanical ventilation in 11.1% of hospitalizations (Table 1). Bacterial pneumonia, including aspiration pneumonia, was the most common discharge diagnosis (50.5%, Table 1).

steuart06700520e_t1.jpg

Demographic and Clinical Characteristics

Children were discharged before return to respiratory baseline in 30.4% of hospitalizations (Appendix Figure). Children discharged before return to respiratory baseline were older (median age 5.7 years, IQR 3.1-11.0, vs 4.9 years, IQR 2.6-9.7; P = .04) and more likely to be privately insured (54.2% vs 43.4%; P = .04), compared with children discharged at respiratory baseline (Table 1). Children discharged before return to respiratory baseline were also more likely to have a respiratory CCC (59.9% vs 30.9%; P < .001), have a respiratory technology dependence diagnosis code (44.8% vs 24.1%; P < .001), and have baseline respiratory support needs on EMR review (67.7% vs 37.7%; P < .001), compared with children discharged at baseline (Table 1).

Children discharged before return to respiratory baseline required significantly greater escalation in respiratory support during hospitalization, compared with children discharged at respiratory baseline, including higher rates of initiation of CPAP or BiPAP, increased pressure settings from baseline (for home CPAP, BiPAP, or ventilator users), and initiation of full mechanical ventilation (Table 1). Hospitalizations in which children were discharged before return to respiratory baseline were also more likely to include ICU care than were those for children discharged at baseline (52.1% vs 35.2%; P < .001; Table 1).

Clinical Outcomes and Utilization

Reutilization within 30 days occurred after 32.1% of hospitalizations, with 26.1% requiring hospital readmission and 6.0% requiring ED revisit (Table 2). There was no statistical association in either unadjusted (Table 2) or adjusted (Table 3) analysis between children discharged before return to respiratory baseline and 30-day all-cause hospital reutilizations, hospital readmissions, or ED revisits.

steuart06700520e_t2.jpg

In analysis of secondary outcomes, 30-day reutilization because of ARI occurred after 21.5% of hospitalizations, with 19.0% requiring hospital readmission and 2.5% requiring ED revisit. Median hospital LOS for the cohort was 4 days (IQR 2-8; Table 2). Hospitalizations in which children were discharged before return to respiratory baseline were longer than in those discharged at baseline (median 6 days, IQR 3-11, vs 4 days, IQR 2-7; P < .001; Table 2).

steuart06700520e_t3.jpg

For hospitalizations of children discharged at respiratory baseline, the median time to return to respiratory baseline was 3 days (IQR 1-5, complete range 0-80). In these encounters, discharge occurred soon after return to respiratory baseline (median 1 day, IQR 0-1.5, complete range 0-54).

In subgroup analysis excluding the 18 hospitalizations in which children were lost to follow-up (2.8% of the total cohort), discharge before return to respiratory baseline was not associated with 30-day all-cause hospital reutilization (Table 4).

steuart06700520e_t4.jpg

In this retrospective cohort study, children with NI hospitalized with ARI were frequently discharged using increased respiratory support from baseline. However, those discharged before return to respiratory baseline, despite their greater clinical complexity and acute illness severity, did not have increased hospital reutilization, compared with children discharged at respiratory baseline. Our findings suggest that discharge before return to baseline respiratory support after ARI may be clinically appropriate in some children with NI.

With the growing emphasis on decreasing hospital costs, concern exists that patients are being discharged from hospitals “quicker and sicker,”^18,19 with shortening lengths of stay and higher patient instability at discharge. Clinical instability at discharge has been associated with adverse postdischarge outcomes in adults with pneumonia^20-23; however, studies evaluating discharge readiness have not examined the population of children with NI. Our findings of no difference in reutilization for children with NI discharged before return to respiratory baseline, which would be expected to approximate one or more clinical instabilities, contrast these concerns.

Clinicians caring for children with NI hospitalized with ARI may find it difficult to determine a child’s discharge readiness, in part because many children with NI have longer times to return to respiratory baseline and some never return to their pre-­illness baseline.²⁴ In otherwise healthy children hospitalized with respiratory infections such as pneumonia, discharge criteria typically include complete wean from respiratory support prior to discharge.^4,25 In our study’s more complex children, whose parents already manage respiratory support at home, we hypothesize that discharging providers may be comfortable with discharge when the child has certain types of increased respiratory support compatible with home equipment, a parent skilled with monitoring the child’s respiratory status, and the support of an experienced outpatient provider and home nursing providers. At our institution, outpatient respiratory support weans are primarily performed by pediatric pulmonologists and, for isolated weaning of supplemental oxygen or time using support, by parents and outpatient pediatricians.

Another important factor in determining a child’s discharge readiness is the perspective of the child’s parent. Berry et al found that children whose parents believe they are not healthy enough for discharge are more likely to experience unplanned hospital readmissions,²⁴ signaling the role of child- and family-­specific factors in safe discharge decisions. Therefore, parents of children with NI should be proactively involved throughout the multidisciplinary discharge process,^26,27 including the decision to discharge before return to respiratory baseline. Parents have identified ongoing provider support, opportunities to practice home care skills, and written instructions with contingency plans as important components of discharge readiness.²⁸ Further work to create partnerships with these highly skilled caregivers in discharge decision making and transition planning are needed to promote safe discharge practices in this complex population.

In our study, children discharged before return to respiratory baseline were more likely to be older and privately insured compared with children discharged at respiratory baseline. Prior studies have found that social factors including low socioeconomic status influence ED provider admissions decisions for children with pneumonia.^29,30 However, the role of socioeconomic factors in provider discharge decisions for children with NI has not been assessed. These traits may also be proxy markers of other sociodemographic factors, such as parent education level, financial hardship influencing ability to participate in a child’s care at the bedside, access to comprehensive outpatient primary care, and availability of private home nursing. We hypothesize that these related characteristics directly and indirectly influence provider discharge decisions.

Discharging providers are likely more comfortable with discharge prior to return to respiratory baseline when the family has private duty nursing in the home. Home nurses can assist families in providing increased respiratory support and recognizing respiratory problems that may arise following discharge. However, home nursing shortages are common nationwide.^31,32 Low-income children, children with respiratory technology use, and children without Medicaid have been found to have larger gaps in home nursing availability.^31,32 Further studies are needed to understand the role of home nursing availability in provider discharge decisions in this population.

This study has several limitations. The retrospective design of this study creates the potential for residual confounding; there may be other clinical or demographic factors influencing hospital discharge decisions that we are unable to capture using EMR review, including parental knowledge and comfort managing illness, quality of discharge instructions, frequency of follow-up visits, and presence of skilled home nursing services. Categorization of children based on respiratory support status at discharge lends potential for misclassification of exposure; however, our substantial interrater reliability suggests that misclassification bias is small. This study’s primary finding indicated no difference between exposure groups; although we may be unable to detect small differences, we had sufficient power with our sample size to detect meaningful differences in reutilization outcomes.

This study was not designed to capture outpatient time to return to respiratory baseline; prospective studies are needed to identify rates of return to respiratory baseline following ARI in children with NI. We did not measure the level of respiratory support used by children at the time of discharge and, therefore, are unable to estimate the amount of respiratory support weaning needed following discharge or the compatibility of support with home equipment using our data. In addition, this study focused on respiratory support modalities and, thus, did not measure inpatient utilization of mucociliary clearance technologies that might be hypothesized to decrease the time to return to baseline respiratory support. Next steps in evaluating treatment of ARI include investigating the effect of mucociliary clearance on both exposure and outcome in this population.

There may be other clinically meaningful outcomes for this population apart from reutilization that we have not assessed in this study, including increased respiratory support required following discharge, primary care reutilization, healthcare costs, or parent satisfaction with timing of and outcomes after discharge. Finally, although our hospital has reutilization rates for children with NI that are similar to other institutions in the United States,³³ our results may not be generalizable to children with NI hospitalized at other institutions because local discharge processes and systems of care may be different. Prospective, multicenter investigation is needed to evaluate the clinical consequences of discharge before return to respiratory baseline more broadly.

At our institution, approximately one-quarter of children with NI hospitalized with ARI were discharged before return to respiratory baseline, but these children were not at increased risk of reutilization, compared with children discharged at respiratory baseline. Our findings suggest that return to baseline respiratory support might not be a necessary component of hospital discharge criteria. In otherwise clinically stable children with NI, discharge before return to respiratory baseline may be reasonable if their parents are comfortable managing respiratory support at home.

The authors thank Jonathan Rodean of the Children’s Hospital Association for his assistance with abstraction of PHIS data.

Children with neurologic impairment (NI; eg, hypoxic-­ischemic encephalopathy, muscular dystrophy) are characterized by functional and/or intellectual impairments resulting from a variety of neurologic diseases.¹ These children commonly have respiratory comorbidities, including central hypoventilation, impaired cough, and oromotor dysfunction, that may lead to chronic respiratory insufficiency and a need for chronic respiratory support at baseline.^2,3 Baseline respiratory support modalities can include supplemental oxygen, noninvasive positive pressure ventilation, or invasive mechanical ventilation.

Acute respiratory infections (ARI; eg, pneumonia, bronchiolitis) are the most common cause of hospitalization, intensive care unit (ICU) admission, and death for children with NI.^1,3 Discharge criteria for otherwise healthy children admitted to the hospital with ARI often include return to respiratory baseline.⁴ Children with complex chronic conditions have longer hospitalizations when hospitalized with respiratory infections,^5-7 because, in part, comorbidities and complications prolong the time to return to baseline. This prolonged return to respiratory baseline in combination with family knowledge, comfort, and skill in managing respiratory support and other complexities at home may alter discharge practices in the population of children with NI. In our clinical experience, discharge before return to baseline respiratory support occurs more frequently in children with NI than in otherwise healthy children when hospitalized with ARI. However, the consequences of discharging children with NI prior to return to respiratory baseline are unknown.

In this study, we sought to determine if discharge prior to return to baseline respiratory support is associated with reutilization among children with NI hospitalized with ARI. We hypothesized that patients discharged prior to return to respiratory baseline would have higher rates of 30-day hospital reutilization.

Study Design and Data Source

This single-center, retrospective cohort study of children hospitalized at Cincinnati Children’s Hospital Medical Center (CCHMC) used data from the Pediatric Health Information System (PHIS) and the electronic medical record (EMR). PHIS, an administrative database of 45 not-for-profit, tertiary care, US pediatric hospitals managed by Children’s Hospital Association (Lenexa, Kansas), was used to identify eligible children, examine demographic and clinical variables, and define outcomes. PHIS contains data regarding patient demographics, inpatient resource utilization, and diagnoses. Encrypted medical record numbers in PHIS allowed for local identification of patients’ medical records to complete EMR review to confirm eligibility and obtain detailed patient-level clinical information (eg, respiratory support needs) not available in PHIS.

Pilot medical record reviews allowed for standardized study definitions and procedures. All study staff underwent training with the primary investigator, including detailed review of 10 initial abstractions. Two investigators (K.M. and S.C.) performed repeat abstractions from 40 randomly selected records to enable assessment of interrater reliability. Average reliability, indicated by the κ statistic, indicated substantial to near-perfect reliability⁸ (κ = 0.97, 95% CI 0.90-1.00) for the primary exposure. EMR data were managed using Research Electronic Data Capture (REDCap, Nashville, Tennessee)⁹ and subsequently merged with PHIS data.

Study Population

Hospitalizations of children with NI aged 1 to 18 years at CCHMC between January 2010 and September 2015 were eligible for inclusion if they had a principal discharge diagnosis indicative of ARI and required increased respiratory support from baseline during hospitalization. NI was defined as a high-intensity, chronic neurological diagnosis with substantial functional impairments according to previously defined diagnosis codes.^1,10 ARI was identified using codes in the Clinical Classification Software (Agency for Healthcare Research and Quality, Rockville, MD) respiratory group indicative of ARI (eg, pneumonia, bronchiolitis, influenza; Appendix Table).

Children transferred to CCHMC were excluded because records from their initial illness presentation and management were not available. Because of expected differences in management and outcomes, children with a known diagnosis of tuberculosis or human immunodeficiency virus were excluded. Because exposure criteria were dependent on hospital discharge status, hospitalizations for children who died during admission (4 of 632 hospitalizations, 0.63%) were excluded from the final cohort (Appendix Figure).

Study Definitions

Baseline respiratory support (ie, “respiratory baseline”) was defined as the child’s highest level of respiratory support needed prior to admission when well (ie, no support, supplemental oxygen, continuous positive airway pressure [CPAP] or bilevel positive airway pressure [BiPAP], or ventilator support), and further characterized by night or day/night requirement. Respiratory baseline was identified using EMR documentation of home respiratory support use at the time of index admission. Return to respiratory baseline was defined as the date on which the child achieved documented home respiratory support settings, regardless of clinical symptoms.

Children may have required increased respiratory support from baseline at any time during hospitalization. Maximum respiratory support required was categorized as one of the following: (1) initiation of supplemental oxygen or increase in oxygen flow or duration; (2) initiation of CPAP or BiPAP; (3) increase in pressure settings or duration of pressure support for those with baseline CPAP, BiPAP, or ventilator use; and (4) initiation of full mechanical ventilation. Respiratory support categories were mutually exclusive: children requiring multiple types of increased respiratory support were classified for analysis by the most invasive form of respiratory support used (eg, a child requiring increase in both oxygen flow and pressure settings was categorized as an increase in pressure settings). Children who received heated high-flow nasal cannula therapy as maximum support were categorized as initiation or increase in oxygen support.

Time to return to respiratory baseline was defined as the difference in days between date of return to respiratory baseline and date of admission. Time to return to respiratory baseline was determined only for children who were discharged at respiratory baseline.

Primary Exposure and Outcome Measures

The primary exposure was hospital discharge before return to respiratory baseline (ie, discharge on higher respiratory support than at baseline settings). At our institution, standardized discharge criteria for children with NI do not exist. The primary outcome was all-cause, 30-day hospital reutilization, including hospital readmissions and emergency department (ED) revisits. Secondary outcomes included 30-day reutilization for ARI and hospital length of stay (LOS) in days.

Patient Demographics and Clinical Characteristics

Demographic and patient characteristics that might influence hospital discharge before return to respiratory baseline or readmission were obtained from PHIS (eg, demographic information, age, insurance type, measures of clinical complexity, illness severity) and by EMR review (eg, baseline respiratory support needs, maximum respiratory support during hospitalization). Measures of clinical complexity included comorbid complex chronic conditions (CCCs)^11-14 and technology dependence^14-16 using previously defined diagnostic codes. Measures of illness severity included sepsis¹⁷ and ICU-level care. At our institution, children with baseline ventilator use do not require admission to the ICU unless they are clinically unstable.

Statistical Analysis

Continuous variables were described using medians and interquartile ranges (IQR). Categorical variables were described using counts and percentages. Patient characteristics and outcomes were stratified by primary exposure and compared using chi-square test or Fisher exact test for categorical variables and Wilcoxon rank sum test for continuous variables.

To examine the independent association between discharge before return to respiratory baseline and hospital reutilization, a generalized estimating equation was used that included potential confounders while accounting for within-patient clustering. Patient demographics included age, race, ethnicity, and insurance type; measures of clinical complexity included number of CCCs, technology dependence, and baseline respiratory support; and measures of acute illness severity included ARI diagnosis, degree of increase in respiratory support during hospitalization, and ICU-level care. LOS was also included in the model as a covariate because of its expected association with both exposure and outcome.

Secondary analyses were conducted using the outcome of 30-day reutilization for ARI. Subgroup analysis excluding hospitalizations of children lost to follow-up (ie, no encounters in the 6 months after hospital discharge) was also conducted. All analyses were performed with SAS v9.3 (SAS Institute, Cary, North Carolina). P values < .05 were considered statistically significant. This study was approved by the Institutional Review Board.

Study Cohort

A total of 632 hospitalizations experienced by 366 children with NI who were admitted with ARI were included (Appendix Figure). Most children (66.4%) in the cohort experienced only one hospitalization, 17.5% had two hospitalizations, 7.9% had three hospitalizations, and 8.2% had four or more hospitalizations. The median age at hospitalization was 5.0 years (IQR 2.8-10.5) and most hospitalizations were for children who were male (56.6%), white (78.3%), non-Hispanic (96.0%), and publicly insured (51.7%; Table 1). More than one-quarter (28.6%) of hospitalizations were for children with four or more CCCs, and in 73.4% of hospitalizations, children were technology dependent (Table 1). Baseline respiratory support was common (46.8%), including home mechanical ventilation in 11.1% of hospitalizations (Table 1). Bacterial pneumonia, including aspiration pneumonia, was the most common discharge diagnosis (50.5%, Table 1).

steuart06700520e_t1.jpg

Demographic and Clinical Characteristics

Children were discharged before return to respiratory baseline in 30.4% of hospitalizations (Appendix Figure). Children discharged before return to respiratory baseline were older (median age 5.7 years, IQR 3.1-11.0, vs 4.9 years, IQR 2.6-9.7; P = .04) and more likely to be privately insured (54.2% vs 43.4%; P = .04), compared with children discharged at respiratory baseline (Table 1). Children discharged before return to respiratory baseline were also more likely to have a respiratory CCC (59.9% vs 30.9%; P < .001), have a respiratory technology dependence diagnosis code (44.8% vs 24.1%; P < .001), and have baseline respiratory support needs on EMR review (67.7% vs 37.7%; P < .001), compared with children discharged at baseline (Table 1).

Children discharged before return to respiratory baseline required significantly greater escalation in respiratory support during hospitalization, compared with children discharged at respiratory baseline, including higher rates of initiation of CPAP or BiPAP, increased pressure settings from baseline (for home CPAP, BiPAP, or ventilator users), and initiation of full mechanical ventilation (Table 1). Hospitalizations in which children were discharged before return to respiratory baseline were also more likely to include ICU care than were those for children discharged at baseline (52.1% vs 35.2%; P < .001; Table 1).

Clinical Outcomes and Utilization

Reutilization within 30 days occurred after 32.1% of hospitalizations, with 26.1% requiring hospital readmission and 6.0% requiring ED revisit (Table 2). There was no statistical association in either unadjusted (Table 2) or adjusted (Table 3) analysis between children discharged before return to respiratory baseline and 30-day all-cause hospital reutilizations, hospital readmissions, or ED revisits.

steuart06700520e_t2.jpg

In analysis of secondary outcomes, 30-day reutilization because of ARI occurred after 21.5% of hospitalizations, with 19.0% requiring hospital readmission and 2.5% requiring ED revisit. Median hospital LOS for the cohort was 4 days (IQR 2-8; Table 2). Hospitalizations in which children were discharged before return to respiratory baseline were longer than in those discharged at baseline (median 6 days, IQR 3-11, vs 4 days, IQR 2-7; P < .001; Table 2).

steuart06700520e_t3.jpg

For hospitalizations of children discharged at respiratory baseline, the median time to return to respiratory baseline was 3 days (IQR 1-5, complete range 0-80). In these encounters, discharge occurred soon after return to respiratory baseline (median 1 day, IQR 0-1.5, complete range 0-54).

In subgroup analysis excluding the 18 hospitalizations in which children were lost to follow-up (2.8% of the total cohort), discharge before return to respiratory baseline was not associated with 30-day all-cause hospital reutilization (Table 4).

steuart06700520e_t4.jpg

In this retrospective cohort study, children with NI hospitalized with ARI were frequently discharged using increased respiratory support from baseline. However, those discharged before return to respiratory baseline, despite their greater clinical complexity and acute illness severity, did not have increased hospital reutilization, compared with children discharged at respiratory baseline. Our findings suggest that discharge before return to baseline respiratory support after ARI may be clinically appropriate in some children with NI.

With the growing emphasis on decreasing hospital costs, concern exists that patients are being discharged from hospitals “quicker and sicker,”^18,19 with shortening lengths of stay and higher patient instability at discharge. Clinical instability at discharge has been associated with adverse postdischarge outcomes in adults with pneumonia^20-23; however, studies evaluating discharge readiness have not examined the population of children with NI. Our findings of no difference in reutilization for children with NI discharged before return to respiratory baseline, which would be expected to approximate one or more clinical instabilities, contrast these concerns.

Clinicians caring for children with NI hospitalized with ARI may find it difficult to determine a child’s discharge readiness, in part because many children with NI have longer times to return to respiratory baseline and some never return to their pre-­illness baseline.²⁴ In otherwise healthy children hospitalized with respiratory infections such as pneumonia, discharge criteria typically include complete wean from respiratory support prior to discharge.^4,25 In our study’s more complex children, whose parents already manage respiratory support at home, we hypothesize that discharging providers may be comfortable with discharge when the child has certain types of increased respiratory support compatible with home equipment, a parent skilled with monitoring the child’s respiratory status, and the support of an experienced outpatient provider and home nursing providers. At our institution, outpatient respiratory support weans are primarily performed by pediatric pulmonologists and, for isolated weaning of supplemental oxygen or time using support, by parents and outpatient pediatricians.

Another important factor in determining a child’s discharge readiness is the perspective of the child’s parent. Berry et al found that children whose parents believe they are not healthy enough for discharge are more likely to experience unplanned hospital readmissions,²⁴ signaling the role of child- and family-­specific factors in safe discharge decisions. Therefore, parents of children with NI should be proactively involved throughout the multidisciplinary discharge process,^26,27 including the decision to discharge before return to respiratory baseline. Parents have identified ongoing provider support, opportunities to practice home care skills, and written instructions with contingency plans as important components of discharge readiness.²⁸ Further work to create partnerships with these highly skilled caregivers in discharge decision making and transition planning are needed to promote safe discharge practices in this complex population.

In our study, children discharged before return to respiratory baseline were more likely to be older and privately insured compared with children discharged at respiratory baseline. Prior studies have found that social factors including low socioeconomic status influence ED provider admissions decisions for children with pneumonia.^29,30 However, the role of socioeconomic factors in provider discharge decisions for children with NI has not been assessed. These traits may also be proxy markers of other sociodemographic factors, such as parent education level, financial hardship influencing ability to participate in a child’s care at the bedside, access to comprehensive outpatient primary care, and availability of private home nursing. We hypothesize that these related characteristics directly and indirectly influence provider discharge decisions.

Discharging providers are likely more comfortable with discharge prior to return to respiratory baseline when the family has private duty nursing in the home. Home nurses can assist families in providing increased respiratory support and recognizing respiratory problems that may arise following discharge. However, home nursing shortages are common nationwide.^31,32 Low-income children, children with respiratory technology use, and children without Medicaid have been found to have larger gaps in home nursing availability.^31,32 Further studies are needed to understand the role of home nursing availability in provider discharge decisions in this population.

This study has several limitations. The retrospective design of this study creates the potential for residual confounding; there may be other clinical or demographic factors influencing hospital discharge decisions that we are unable to capture using EMR review, including parental knowledge and comfort managing illness, quality of discharge instructions, frequency of follow-up visits, and presence of skilled home nursing services. Categorization of children based on respiratory support status at discharge lends potential for misclassification of exposure; however, our substantial interrater reliability suggests that misclassification bias is small. This study’s primary finding indicated no difference between exposure groups; although we may be unable to detect small differences, we had sufficient power with our sample size to detect meaningful differences in reutilization outcomes.

This study was not designed to capture outpatient time to return to respiratory baseline; prospective studies are needed to identify rates of return to respiratory baseline following ARI in children with NI. We did not measure the level of respiratory support used by children at the time of discharge and, therefore, are unable to estimate the amount of respiratory support weaning needed following discharge or the compatibility of support with home equipment using our data. In addition, this study focused on respiratory support modalities and, thus, did not measure inpatient utilization of mucociliary clearance technologies that might be hypothesized to decrease the time to return to baseline respiratory support. Next steps in evaluating treatment of ARI include investigating the effect of mucociliary clearance on both exposure and outcome in this population.

There may be other clinically meaningful outcomes for this population apart from reutilization that we have not assessed in this study, including increased respiratory support required following discharge, primary care reutilization, healthcare costs, or parent satisfaction with timing of and outcomes after discharge. Finally, although our hospital has reutilization rates for children with NI that are similar to other institutions in the United States,³³ our results may not be generalizable to children with NI hospitalized at other institutions because local discharge processes and systems of care may be different. Prospective, multicenter investigation is needed to evaluate the clinical consequences of discharge before return to respiratory baseline more broadly.

At our institution, approximately one-quarter of children with NI hospitalized with ARI were discharged before return to respiratory baseline, but these children were not at increased risk of reutilization, compared with children discharged at respiratory baseline. Our findings suggest that return to baseline respiratory support might not be a necessary component of hospital discharge criteria. In otherwise clinically stable children with NI, discharge before return to respiratory baseline may be reasonable if their parents are comfortable managing respiratory support at home.

The authors thank Jonathan Rodean of the Children’s Hospital Association for his assistance with abstraction of PHIS data.

Adverse Childhood Experiences, or ACEs, include exposure to abuse, neglect, or household dysfunction (eg, having a parent who is mentally ill) as a child.¹ Exposure to ACEs affects health into adulthood, with a dose-response relationship between ACEs and a range of comorbidities.¹ Adults with 6 or more ACEs have a 20-year shorter life expectancy than do those with no ACEs.¹ Still, ACEs are static; once experienced, that experience cannot be undone. However, resilience, or positive adaptation in the context of adversity, can be protective, buffering the negative effects of ACEs.^2,3 Protective factors that promote resilience include social capital, such as positive relationships with caregivers and peers.³

With their clear link to health outcomes across the life-course, there is a movement for pediatricians to screen children for ACEs⁴ and to develop strategies that promote resilience in children, parents, and families. However, screening a child for adversity has challenges because younger children may not have experienced an adverse exposure, or they may be unable to voice their experiences. Studies have demonstrated that parental adversity, or ACEs, may be a marker for childhood adversity.^5,6 Biological models also support this potential intergenerational effect of ACEs. Chronic exposure to stress, including ACEs, results in elevated cortisol via a dysregulated hypothalamic-pituitary-adrenal axis, which results in chronic inflammation.⁷ This “toxic stress” is prolonged, severe in intensity, and can lead to epigenetic changes that may be passed on to the next generation.^8,9

Hospitalization of an ill child, and the transition to home after that hospitalization, is a stressful event for children and families.¹⁰ This stress may be relevant to parents that have a history of a high rate of ACEs or a current low degree of resilience. Our previous work demonstrated that, in the inpatient setting, parents with high ACEs (≥4) or low resilience have increased coping difficulty 14 days after their child’s hospital discharge.¹¹ Our objective here was to evaluate whether a parent’s ACEs and/or resilience would also be associated with that child’s likelihood of reutilization. We hypothesized that more parental ACEs and/or lower parental resilience would be associated with revisits the emergency room, urgent care, or hospital readmissions.

Participants and Study Design

We conducted a prospective cohort study of parents of hospitalized children recruited from the “Hospital-to-Home Outcomes” Studies (H2O I and H2O II).^12,13 H2O I and II were prospective, single-center, randomized controlled trials designed to determine the effectiveness of either a nurse-led transitional home visit (H2O I) or telephone call (H2O II) on 30-day unplanned healthcare reutilization. The trials and this study were approved by the Cincinnati Children’s Institutional Review Board. All parents provided written informed consent.

Details of H2O I and II recruitment and design have been described previously.^12,13 Briefly, children were eligible for inclusion in either study if they were admitted to our institution’s general Hospital Medicine or the Hospital Medicine Complex Care Services; for H2O I, children hospitalized on the Neurology and Neurosurgery services were also eligible.^12,13 Patients were excluded if they were discharged to a residential facility, if they lived outside the home healthcare nurse service area, if they were eligible for skilled home healthcare services (eg, intravenous antibiotics), or if the participating caregiver was non-English speaking.^12,13 In H2O I, families were randomized either to receive a single nurse home visit within 96 hours of discharge or standard of care. In H2O II, families enrolled were randomized to receive a telephone call by a nurse within 96 hours of discharge or standard of care. As we have previously published, randomization in both trials successfully balanced the intervention and control arms with respect to key demographic characteristics.^12,13 For the analyses presented here, we focused on a subset of caregivers 18 years and older whose children were enrolled in either H2O I or II between August 2015 and October 2016. In both H2O trials, face-to-face and paper-based questionnaires were completed by parents during the index hospitalization.

Outcome and Predictors

Our primary outcome was unanticipated healthcare reutilization defined as return to the emergency room, urgent care, or unplanned readmission within 30 days of hospital discharge, consistent with the H2O trials. This was measured using the primary institution’s administrative data supplemented by a utilization database shared across regional hospitals.¹⁴ Readmissions were identified as “unplanned” using a previously validated algorithm,¹⁵ and treated as a dichotomous yes/no variable.

Our primary predictors were parental ACEs and resilience (see Appendix Tables). The ACE questionnaire addresses abuse, neglect, and household dysfunction in the first 18 years of life.¹ It is composed of 10 questions, each with a yes/no response.¹ We defined parents as low (ACE 0), moderate (ACE 1-3), or high (ACE ≥4) risk a priori because previous literature has described poor outcomes in adults with 4 or more ACEs.¹⁶

Given the sensitive nature of the questions, respondents independently completed the ACE questionnaire on paper instead of via the face-to-face survey. Respondents returned the completed questionnaire to the research assistant in a sealed envelope. All families received educational information on relevant hospital and community-based resources (eg, social work).

Parental resilience was measured using the Brief Resilience Scale (BRS). The BRS is 6 items, each on a 5-point Likert scale. Responses were averaged, providing a total score of 1-5; higher scores are representative of higher resilience.¹⁷ We treated the BRS score as a continuous variable. BRS has been used in clinical settings; it has demonstrated positive correlation with social support and negative correlation with fatigue.¹⁷ Parents answered BRS questions during the index pediatric hospitalization in a face-to-face interview.

Parent and Child Characteristics

Parent and child sociodemographic variables were also obtained during the face-to-face interview. Parental variables included age, gender, educational attainment, household income, employment status, and financial and social strain.¹¹ Educational attainment was analyzed in 2 categories—high school or less vs more than high school—because most discharge instructions are written at a high school reading level.¹⁸ Parents reported their annual household income in the following categories: <$15,000; $15,000-$29,999; $30,000-$44,999; $45,000-$59,999; $60,000-$89,999; $90,000-$119,999; ≥$120,000. Employment was dichotomized as not employed/student vs any employment. Financial and social strain were assessed using a series of 9 previously described questions.¹⁹ These questions assessed, via self-report, a family’s ability to make ends meet, ability to pay rent/mortgage or utilities, need to move in with others because of financial reasons, and ability to borrow money if needed, as well as home ownership and parental marital status.^15,19 Strain questions were all dichotomous (yes/no, single/not single). A composite variable was then constructed that categorized those reporting no strain items, 1 to 2 items, 3 to 4 items, and 5 or more items.²⁰

Child variables included race, ethnicity, age, primary care access,²¹ payer, and H2O treatment arm. Race categories were white/Caucasian, black/African American, American Indian or Alaskan Native, Asian or Pacific Islander, and other; ethnicity categories were Hispanic/Latino, non-Hispanic/Latino, and unknown. Given relatively low numbers of children reported to be Hispanic/Latino, we combined race and ethnicity into a single variable, categorized as non-Hispanic/white, non-Hispanic/black, and multiracial/Hispanic/other. Primary care access was assessed using the access subscale to the Parent’s Perception of Primary Care questionnaire. This includes assessment of a family’s ability to travel to their doctor, to see their doctor for routine or sick care, and to get help or advice on evenings or weekends. Scores were categorized as always adequate, almost always adequate, or sometimes/never adequate.²¹ Payer was dichotomized to private or public/self-pay.

Statistical Analyses

We examined the distribution of outcomes, predictors, and covariates. We compared sociodemographic characteristics of those respondents and nonrespondents to the ACE screen using the chi-square test for categorical variables or the t test for continuous variables. We used logistic regression to assess for associations between the independent variables of interest and reutilization, adjusting for potential confounders. To build our adjusted, multivariable model, we decided a priori to include child race/ethnicity, primary care access, financial and social strain, and trial treatment arm. We treated the H2O I control group as the referent group. Other covariates considered for inclusion were caregiver education, household income, employment, and payer. These were included in multivariable models if bivariate associations were significant at the P < .1 level. We assessed an ACE-by-resilience interaction term because we hypothesized that those with more ACEs and lower resilience may have more reutilization outcomes than parents with fewer ACEs and higher resilience. We also evaluated interaction terms between trial arm assignment and predictors to assess effects that may be introduced by the randomization. Predictors in the final logistic regression model were significant at the P < .05 level. Logistic regression assumption of little or no multicollinearity among the independent variables was verified in the final models. All analyses were performed with Stata v16 (Stata Corp, College Station, Texas).

There were a total of 1,787 parent-child dyads enrolled in the H2O I and II during the study period; 1,320 parents (74%) completed the ACE questionnaire and were included the analysis. Included parents were primarily female and employed, as well as educated beyond high school (Table 1). Overall, 64% reported one or more ACEs (range 0 to 9); 45% reported 1to 3, and 19% reported 4 or more ACEs. The most commonly reported ACEs were divorce (n = 573, 43%), exposure to alcoholism (n = 306, 23%), and exposure to mental illness (n = 281, 21%; Figure 1). Parents had a mean BRS score of 3.97 (range 1.17-5.00), with the distribution shown in Figure 2.

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Of the 1,320 included patients, the average length of stay was 2.5 days, and 82% of hospitalizations were caused by acute medical issues (eg, bronchiolitis). A total of 211 children experienced a reutilization event within 30 days of discharge. In bivariate analysis, children with parents with 4 or more ACEs had a 2.02-times (95% CI 1.35-3.02) higher odds of experiencing a reutilization event than did those with parents reporting no ACEs. Parents with higher resilience scores had children with a lower odds of reutilization (odds ratio [OR] 0.77 95% CI 0.63-0.95).

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In addition to our a priori variables, parental education, employment, and insurance met our significance threshold for inclusion in the multivariable model. The ACE-by-resilience interaction term was not significant and not included in the model. Similarly, there was no significant interaction between ACE and resilience and H2O treatment arm; the interaction terms were not included in the final adjusted model, but treatment arm assignment was kept as a covariate. A total of 1,292 children, out of the 1,320 respondents, remained in the final multivariable model; the excluded 28 had incomplete covariate data but were not otherwise different. In this final adjusted model, children with parents reporting 4 or more ACEs had a 1.69-times (95% CI 1.11-2.60) greater odds of reutilization than did those with parents reporting no ACEs (Table 2). Resilience failed to reach statistical significance in the adjusted model (OR 0.86, 95% CI 0.70-1.07).

shah06840520e_f2.jpg

We found that high-risk parents (4 or more ACEs) had children with an increased odds of healthcare reutilization, suggesting intergenerational effects of ACEs. We did not find a similar effect relating to parental resilience. We also did not find an interaction between parental ACEs and resilience, suggesting that a parent’s reported degree of resilience does not modify the effect of ACEs on reutilization risk.

shah06840520e_t2.jpg

Parental adversity may be a risk factor for a child’s unanticipated reutilization. We previously demonstrated that parents with 4 or more ACEs have more coping difficulty than a parent with no ACEs after a child’s hospitalization.¹¹ It is possible that parents with high adversity may have poorer coping mechanisms when dealing with a stressful situation, such as a child’s hospitalization. This may have resulted in inequitable outcomes (eg, increased reutilization) for their children. Other studies have confirmed such an intergenerational effect of adversity, linking a parent’s ACEs with poor developmental, behavioral, and health outcomes in their children.^6,22,23 O’Malley et al showed an association of parental ACEs to current adversities,²⁴ such as insurance or housing concerns, that affect the entirety of the household, including children. In short, it appears that parental ACEs may be a compelling predictor of current childhood adversity.

Resilience buffers the negative effects of ACEs; however, we did not find significant associations between resilience and reutilization or an interaction between ACEs and resilience. The factors that may contribute to reutilization are complex. In our previous work, parental resilience was associated with coping difficulty after discharge; but again, did not interact with parental ACEs.¹¹ Here, we suggest that while resilience may buffer the negative effects of ACEs, that buffering may not affect the likelihood of reutilization. It is also possible that the BRS tool is of less relevance on how one handles the stress of a child’s hospitalization. While the BRS is one measure of resilience, there are many other relevant constructs to resilience, such as connection to social supports, that also may also contribute to risk of reutilization.²⁵

Reducing the stress of a hospitalization itself and promoting a safe transition from hospital to home is critical to improving child health outcomes. Our data here, and in our previous work, demonstrate that a history of adversity and one’s current coping ability may drive a parent’s response to a child’s hospitalization and affect their capacity to care for that child after hospital discharge.¹¹ Additional in-hospital supports like child life, behavioral health, or pastoral care could reduce the stress of the hospitalization while also building positive coping mechanisms.^26-29 A meta-analysis demonstrated that such coping interventions can help alleviate the stress of a hospitalization.³⁰ Hill et al demonstrated successful stress reduction in parents of hospitalized children using a “Coping Kit for Parents.”³¹ Further studies are warranted to understand which interventions are most effective for children and families and whether they could be more effectively deployed if the inpatient team knew more about parental ACEs.

Screening for parental ACEs could help to identify patients at highest risk for a poor transition to home. Therefore, screening for parental adversity in clinical settings, including inpatient settings, may be relevant and valuable.³² Additionally, by recognizing the high prevalence of ACEs in an inpatient setting, hospitals and healthcare organizations could be motivated to develop and enact trauma-informed approaches. A trauma-informed care approach recognizes the intersection of trauma with health and social problems. With this recognition, care teams can more sensitively address the trauma as they provide relevant services.³³ Trauma-informed care is a secondary public health prevention approach that would help team members identify the prevalence and effects of trauma via screening, recognize the signs of a maladaptive response to stress, and respond by integrating awareness of trauma into practice management.^28,34 Both the National Academy of Medicine and the Agency for Healthcare Research and Quality have called for such a trauma-informed approach in primary care.³⁵ In response, many healthcare organizations have developed trauma-informed practices to better address the needs of the populations they serve. For example, provider training on this approach has led to improved rapport in patient-provider relationships.³⁶

Although ACE awareness is a component of trauma-informed care, there are still limitations of the original ACE questionnaire developed by Felitti et al. The existing tool is not inclusive of all adversities a parent or child may face. Moreover, its focus is on past exposures and experiences and not current health-related social needs (eg, food insecurity) which have known linkages with a range of health outcomes and health disparities.³⁷ Additionally, the original ACE questionnaire was created as a population level tool and not as a screening tool. If used as a screening tool, providers may view the questions as too sensitive to ask, and parents may have difficulty responding to and understanding the relevance to their child’s care. Therefore, we suggest that more evidence is required to understand how to best adapt ACE questions into a screening processes that may be implemented in a medical setting.

More evidence is also needed to determine when and where such screening may be most useful. A primary care provider would be best equipped to screen caregivers for ACEs given their established relationship with parents and patients. Given the potential relevance of such information for inpatient care provision, information could then flow from primary care to the inpatient team. However, because not all patients have established primary care providers and only 4% of pediatricians screen for ACEs,³⁸ it is important for inpatient medical teams to understand their role in identifying and addressing ACEs during hospital stays. Development of a screening tool, with input from all stakeholders—including parents—that is valid and feasible for use in a pediatric inpatient setting would be an important step forward. This tool should be paired with training in how to discuss these topics in a trauma-informed, nonjudgmental, empathic manner. We see this as a way in which providers can more effectively elicit an accurate response while simultaneously educating parents on the relevance of such sensitive topics during an acute hospital stay. We also recommend that screening should always be paired with response capabilities that connect those who screen positive with resources that could help them to navigate the stress experienced during and after a child’s hospitalization. Furthermore, communication with primary care providers about parents that screen positive should be integrated into the transition process.

This work has several limitations. First, our study was a part of randomized controlled trials conducted in one academic setting, which thereby limits generalizability. For example, we limited our cohort to those who were English-speaking patients only. This may bias our results because respondents with limited English proficiency may have different risk profiles than their English-speaking peers. In addition, the administration of the both the ACE and resilience questionnaires occurred during an acutely stressful period, which may influence how a parent responds to these questions. Also, both of the surveys are self-reported by parents, which may be susceptible to memory and response biases. Relatedly, we had a high number of nonrespondents, particularly to the ACE questionnaire. Our results are therefore only relevant to those who chose to respond and cannot be applied to nonrespondents. Further work assessing why one does or does not respond to such sensitive questions is an important area for future inquiry. Lastly, our cohort had limited medical complexity; future studies may consider links between parental ACEs (and resilience) and morbidity experienced by children with medical complexity.

Parents history of adversity is linked to their children’s unanticipated healthcare reutilization after a hospital discharge. Screening for parental stressors during a hospitalization may be an important first step to connecting parents and children to evidence-based interventions capable of mitigating the stress of hospitalization and promoting better, more seamless transitions from hospital to home.

Group Members: The following H2O members are nonauthor contributors: JoAnne Bachus, BSN, RN; Monica Borell, BSN, RN; Lenisa V Chang, MA, PhD; Patricia Crawford, RN; Sarah Ferris, BA; Jennifer Gold, BSN, RN; Judy A Heilman, BSN, RN; Jane C Khoury, PhD; Pierce Kuhnell, MS; Karen Lawley, BSN, RN; Margo Moore, MS, BSN, RN; Lynne O’Donnell, BSN, RN; Sarah Riddle, MD; Susan N Sherman, DPA; Angela M Statile, MD, MEd; Karen P Sullivan, BSN, RN; Heather Tubbs-Cooley, PhD, RN; Susan Wade-Murphy, MSN, RN; and Christine M White, MD, MAT.

The authors also thank David Keller, MD, for his guidance on the study.

The authors have no financial relationships or conflicts of interest relevant to this article to disclose.

Supported by funds from the Academic Pediatric Young Investigator Award (Dr A Shah) and the Patient-Centered Outcomes Research Institute Award (IHS-1306-0081, to Dr K Auger, Dr S Shah, Dr H Sucharew, Dr J Simmons), the National Institutes of Health (1K23AI112916, to Dr AF Beck), and the Agency for Healthcare Research and Quality (1K12HS026393-01, to Dr A Shah, K08-HS024735- 01A1, to Dr K Auger). Dr J Haney received Summer Undergraduate Research Fellowship funding through the Summer Undergraduate Research Fellowship at Cincinnati Children’s Hospital Medical Center.

All statements in this report, including findings and conclusions, are solely those of the authors and do not necessarily represent the views of the Patient-Centered Outcomes Research Institute, its Board of Governors, or the Methodology Committee.

Adverse Childhood Experiences, or ACEs, include exposure to abuse, neglect, or household dysfunction (eg, having a parent who is mentally ill) as a child.¹ Exposure to ACEs affects health into adulthood, with a dose-response relationship between ACEs and a range of comorbidities.¹ Adults with 6 or more ACEs have a 20-year shorter life expectancy than do those with no ACEs.¹ Still, ACEs are static; once experienced, that experience cannot be undone. However, resilience, or positive adaptation in the context of adversity, can be protective, buffering the negative effects of ACEs.^2,3 Protective factors that promote resilience include social capital, such as positive relationships with caregivers and peers.³

With their clear link to health outcomes across the life-course, there is a movement for pediatricians to screen children for ACEs⁴ and to develop strategies that promote resilience in children, parents, and families. However, screening a child for adversity has challenges because younger children may not have experienced an adverse exposure, or they may be unable to voice their experiences. Studies have demonstrated that parental adversity, or ACEs, may be a marker for childhood adversity.^5,6 Biological models also support this potential intergenerational effect of ACEs. Chronic exposure to stress, including ACEs, results in elevated cortisol via a dysregulated hypothalamic-pituitary-adrenal axis, which results in chronic inflammation.⁷ This “toxic stress” is prolonged, severe in intensity, and can lead to epigenetic changes that may be passed on to the next generation.^8,9

Hospitalization of an ill child, and the transition to home after that hospitalization, is a stressful event for children and families.¹⁰ This stress may be relevant to parents that have a history of a high rate of ACEs or a current low degree of resilience. Our previous work demonstrated that, in the inpatient setting, parents with high ACEs (≥4) or low resilience have increased coping difficulty 14 days after their child’s hospital discharge.¹¹ Our objective here was to evaluate whether a parent’s ACEs and/or resilience would also be associated with that child’s likelihood of reutilization. We hypothesized that more parental ACEs and/or lower parental resilience would be associated with revisits the emergency room, urgent care, or hospital readmissions.

Participants and Study Design

We conducted a prospective cohort study of parents of hospitalized children recruited from the “Hospital-to-Home Outcomes” Studies (H2O I and H2O II).^12,13 H2O I and II were prospective, single-center, randomized controlled trials designed to determine the effectiveness of either a nurse-led transitional home visit (H2O I) or telephone call (H2O II) on 30-day unplanned healthcare reutilization. The trials and this study were approved by the Cincinnati Children’s Institutional Review Board. All parents provided written informed consent.

Details of H2O I and II recruitment and design have been described previously.^12,13 Briefly, children were eligible for inclusion in either study if they were admitted to our institution’s general Hospital Medicine or the Hospital Medicine Complex Care Services; for H2O I, children hospitalized on the Neurology and Neurosurgery services were also eligible.^12,13 Patients were excluded if they were discharged to a residential facility, if they lived outside the home healthcare nurse service area, if they were eligible for skilled home healthcare services (eg, intravenous antibiotics), or if the participating caregiver was non-English speaking.^12,13 In H2O I, families were randomized either to receive a single nurse home visit within 96 hours of discharge or standard of care. In H2O II, families enrolled were randomized to receive a telephone call by a nurse within 96 hours of discharge or standard of care. As we have previously published, randomization in both trials successfully balanced the intervention and control arms with respect to key demographic characteristics.^12,13 For the analyses presented here, we focused on a subset of caregivers 18 years and older whose children were enrolled in either H2O I or II between August 2015 and October 2016. In both H2O trials, face-to-face and paper-based questionnaires were completed by parents during the index hospitalization.

Outcome and Predictors

Our primary outcome was unanticipated healthcare reutilization defined as return to the emergency room, urgent care, or unplanned readmission within 30 days of hospital discharge, consistent with the H2O trials. This was measured using the primary institution’s administrative data supplemented by a utilization database shared across regional hospitals.¹⁴ Readmissions were identified as “unplanned” using a previously validated algorithm,¹⁵ and treated as a dichotomous yes/no variable.

Our primary predictors were parental ACEs and resilience (see Appendix Tables). The ACE questionnaire addresses abuse, neglect, and household dysfunction in the first 18 years of life.¹ It is composed of 10 questions, each with a yes/no response.¹ We defined parents as low (ACE 0), moderate (ACE 1-3), or high (ACE ≥4) risk a priori because previous literature has described poor outcomes in adults with 4 or more ACEs.¹⁶

Given the sensitive nature of the questions, respondents independently completed the ACE questionnaire on paper instead of via the face-to-face survey. Respondents returned the completed questionnaire to the research assistant in a sealed envelope. All families received educational information on relevant hospital and community-based resources (eg, social work).

Parental resilience was measured using the Brief Resilience Scale (BRS). The BRS is 6 items, each on a 5-point Likert scale. Responses were averaged, providing a total score of 1-5; higher scores are representative of higher resilience.¹⁷ We treated the BRS score as a continuous variable. BRS has been used in clinical settings; it has demonstrated positive correlation with social support and negative correlation with fatigue.¹⁷ Parents answered BRS questions during the index pediatric hospitalization in a face-to-face interview.

Parent and Child Characteristics

Parent and child sociodemographic variables were also obtained during the face-to-face interview. Parental variables included age, gender, educational attainment, household income, employment status, and financial and social strain.¹¹ Educational attainment was analyzed in 2 categories—high school or less vs more than high school—because most discharge instructions are written at a high school reading level.¹⁸ Parents reported their annual household income in the following categories: <$15,000; $15,000-$29,999; $30,000-$44,999; $45,000-$59,999; $60,000-$89,999; $90,000-$119,999; ≥$120,000. Employment was dichotomized as not employed/student vs any employment. Financial and social strain were assessed using a series of 9 previously described questions.¹⁹ These questions assessed, via self-report, a family’s ability to make ends meet, ability to pay rent/mortgage or utilities, need to move in with others because of financial reasons, and ability to borrow money if needed, as well as home ownership and parental marital status.^15,19 Strain questions were all dichotomous (yes/no, single/not single). A composite variable was then constructed that categorized those reporting no strain items, 1 to 2 items, 3 to 4 items, and 5 or more items.²⁰

Child variables included race, ethnicity, age, primary care access,²¹ payer, and H2O treatment arm. Race categories were white/Caucasian, black/African American, American Indian or Alaskan Native, Asian or Pacific Islander, and other; ethnicity categories were Hispanic/Latino, non-Hispanic/Latino, and unknown. Given relatively low numbers of children reported to be Hispanic/Latino, we combined race and ethnicity into a single variable, categorized as non-Hispanic/white, non-Hispanic/black, and multiracial/Hispanic/other. Primary care access was assessed using the access subscale to the Parent’s Perception of Primary Care questionnaire. This includes assessment of a family’s ability to travel to their doctor, to see their doctor for routine or sick care, and to get help or advice on evenings or weekends. Scores were categorized as always adequate, almost always adequate, or sometimes/never adequate.²¹ Payer was dichotomized to private or public/self-pay.

Statistical Analyses

We examined the distribution of outcomes, predictors, and covariates. We compared sociodemographic characteristics of those respondents and nonrespondents to the ACE screen using the chi-square test for categorical variables or the t test for continuous variables. We used logistic regression to assess for associations between the independent variables of interest and reutilization, adjusting for potential confounders. To build our adjusted, multivariable model, we decided a priori to include child race/ethnicity, primary care access, financial and social strain, and trial treatment arm. We treated the H2O I control group as the referent group. Other covariates considered for inclusion were caregiver education, household income, employment, and payer. These were included in multivariable models if bivariate associations were significant at the P < .1 level. We assessed an ACE-by-resilience interaction term because we hypothesized that those with more ACEs and lower resilience may have more reutilization outcomes than parents with fewer ACEs and higher resilience. We also evaluated interaction terms between trial arm assignment and predictors to assess effects that may be introduced by the randomization. Predictors in the final logistic regression model were significant at the P < .05 level. Logistic regression assumption of little or no multicollinearity among the independent variables was verified in the final models. All analyses were performed with Stata v16 (Stata Corp, College Station, Texas).

There were a total of 1,787 parent-child dyads enrolled in the H2O I and II during the study period; 1,320 parents (74%) completed the ACE questionnaire and were included the analysis. Included parents were primarily female and employed, as well as educated beyond high school (Table 1). Overall, 64% reported one or more ACEs (range 0 to 9); 45% reported 1to 3, and 19% reported 4 or more ACEs. The most commonly reported ACEs were divorce (n = 573, 43%), exposure to alcoholism (n = 306, 23%), and exposure to mental illness (n = 281, 21%; Figure 1). Parents had a mean BRS score of 3.97 (range 1.17-5.00), with the distribution shown in Figure 2.

shah06840520e_t1.jpg

Of the 1,320 included patients, the average length of stay was 2.5 days, and 82% of hospitalizations were caused by acute medical issues (eg, bronchiolitis). A total of 211 children experienced a reutilization event within 30 days of discharge. In bivariate analysis, children with parents with 4 or more ACEs had a 2.02-times (95% CI 1.35-3.02) higher odds of experiencing a reutilization event than did those with parents reporting no ACEs. Parents with higher resilience scores had children with a lower odds of reutilization (odds ratio [OR] 0.77 95% CI 0.63-0.95).

shah06840520e_f1.jpg

In addition to our a priori variables, parental education, employment, and insurance met our significance threshold for inclusion in the multivariable model. The ACE-by-resilience interaction term was not significant and not included in the model. Similarly, there was no significant interaction between ACE and resilience and H2O treatment arm; the interaction terms were not included in the final adjusted model, but treatment arm assignment was kept as a covariate. A total of 1,292 children, out of the 1,320 respondents, remained in the final multivariable model; the excluded 28 had incomplete covariate data but were not otherwise different. In this final adjusted model, children with parents reporting 4 or more ACEs had a 1.69-times (95% CI 1.11-2.60) greater odds of reutilization than did those with parents reporting no ACEs (Table 2). Resilience failed to reach statistical significance in the adjusted model (OR 0.86, 95% CI 0.70-1.07).

shah06840520e_f2.jpg

We found that high-risk parents (4 or more ACEs) had children with an increased odds of healthcare reutilization, suggesting intergenerational effects of ACEs. We did not find a similar effect relating to parental resilience. We also did not find an interaction between parental ACEs and resilience, suggesting that a parent’s reported degree of resilience does not modify the effect of ACEs on reutilization risk.

shah06840520e_t2.jpg

Parental adversity may be a risk factor for a child’s unanticipated reutilization. We previously demonstrated that parents with 4 or more ACEs have more coping difficulty than a parent with no ACEs after a child’s hospitalization.¹¹ It is possible that parents with high adversity may have poorer coping mechanisms when dealing with a stressful situation, such as a child’s hospitalization. This may have resulted in inequitable outcomes (eg, increased reutilization) for their children. Other studies have confirmed such an intergenerational effect of adversity, linking a parent’s ACEs with poor developmental, behavioral, and health outcomes in their children.^6,22,23 O’Malley et al showed an association of parental ACEs to current adversities,²⁴ such as insurance or housing concerns, that affect the entirety of the household, including children. In short, it appears that parental ACEs may be a compelling predictor of current childhood adversity.

Resilience buffers the negative effects of ACEs; however, we did not find significant associations between resilience and reutilization or an interaction between ACEs and resilience. The factors that may contribute to reutilization are complex. In our previous work, parental resilience was associated with coping difficulty after discharge; but again, did not interact with parental ACEs.¹¹ Here, we suggest that while resilience may buffer the negative effects of ACEs, that buffering may not affect the likelihood of reutilization. It is also possible that the BRS tool is of less relevance on how one handles the stress of a child’s hospitalization. While the BRS is one measure of resilience, there are many other relevant constructs to resilience, such as connection to social supports, that also may also contribute to risk of reutilization.²⁵

Reducing the stress of a hospitalization itself and promoting a safe transition from hospital to home is critical to improving child health outcomes. Our data here, and in our previous work, demonstrate that a history of adversity and one’s current coping ability may drive a parent’s response to a child’s hospitalization and affect their capacity to care for that child after hospital discharge.¹¹ Additional in-hospital supports like child life, behavioral health, or pastoral care could reduce the stress of the hospitalization while also building positive coping mechanisms.^26-29 A meta-analysis demonstrated that such coping interventions can help alleviate the stress of a hospitalization.³⁰ Hill et al demonstrated successful stress reduction in parents of hospitalized children using a “Coping Kit for Parents.”³¹ Further studies are warranted to understand which interventions are most effective for children and families and whether they could be more effectively deployed if the inpatient team knew more about parental ACEs.

Screening for parental ACEs could help to identify patients at highest risk for a poor transition to home. Therefore, screening for parental adversity in clinical settings, including inpatient settings, may be relevant and valuable.³² Additionally, by recognizing the high prevalence of ACEs in an inpatient setting, hospitals and healthcare organizations could be motivated to develop and enact trauma-informed approaches. A trauma-informed care approach recognizes the intersection of trauma with health and social problems. With this recognition, care teams can more sensitively address the trauma as they provide relevant services.³³ Trauma-informed care is a secondary public health prevention approach that would help team members identify the prevalence and effects of trauma via screening, recognize the signs of a maladaptive response to stress, and respond by integrating awareness of trauma into practice management.^28,34 Both the National Academy of Medicine and the Agency for Healthcare Research and Quality have called for such a trauma-informed approach in primary care.³⁵ In response, many healthcare organizations have developed trauma-informed practices to better address the needs of the populations they serve. For example, provider training on this approach has led to improved rapport in patient-provider relationships.³⁶

Although ACE awareness is a component of trauma-informed care, there are still limitations of the original ACE questionnaire developed by Felitti et al. The existing tool is not inclusive of all adversities a parent or child may face. Moreover, its focus is on past exposures and experiences and not current health-related social needs (eg, food insecurity) which have known linkages with a range of health outcomes and health disparities.³⁷ Additionally, the original ACE questionnaire was created as a population level tool and not as a screening tool. If used as a screening tool, providers may view the questions as too sensitive to ask, and parents may have difficulty responding to and understanding the relevance to their child’s care. Therefore, we suggest that more evidence is required to understand how to best adapt ACE questions into a screening processes that may be implemented in a medical setting.

More evidence is also needed to determine when and where such screening may be most useful. A primary care provider would be best equipped to screen caregivers for ACEs given their established relationship with parents and patients. Given the potential relevance of such information for inpatient care provision, information could then flow from primary care to the inpatient team. However, because not all patients have established primary care providers and only 4% of pediatricians screen for ACEs,³⁸ it is important for inpatient medical teams to understand their role in identifying and addressing ACEs during hospital stays. Development of a screening tool, with input from all stakeholders—including parents—that is valid and feasible for use in a pediatric inpatient setting would be an important step forward. This tool should be paired with training in how to discuss these topics in a trauma-informed, nonjudgmental, empathic manner. We see this as a way in which providers can more effectively elicit an accurate response while simultaneously educating parents on the relevance of such sensitive topics during an acute hospital stay. We also recommend that screening should always be paired with response capabilities that connect those who screen positive with resources that could help them to navigate the stress experienced during and after a child’s hospitalization. Furthermore, communication with primary care providers about parents that screen positive should be integrated into the transition process.

This work has several limitations. First, our study was a part of randomized controlled trials conducted in one academic setting, which thereby limits generalizability. For example, we limited our cohort to those who were English-speaking patients only. This may bias our results because respondents with limited English proficiency may have different risk profiles than their English-speaking peers. In addition, the administration of the both the ACE and resilience questionnaires occurred during an acutely stressful period, which may influence how a parent responds to these questions. Also, both of the surveys are self-reported by parents, which may be susceptible to memory and response biases. Relatedly, we had a high number of nonrespondents, particularly to the ACE questionnaire. Our results are therefore only relevant to those who chose to respond and cannot be applied to nonrespondents. Further work assessing why one does or does not respond to such sensitive questions is an important area for future inquiry. Lastly, our cohort had limited medical complexity; future studies may consider links between parental ACEs (and resilience) and morbidity experienced by children with medical complexity.

Parents history of adversity is linked to their children’s unanticipated healthcare reutilization after a hospital discharge. Screening for parental stressors during a hospitalization may be an important first step to connecting parents and children to evidence-based interventions capable of mitigating the stress of hospitalization and promoting better, more seamless transitions from hospital to home.

Group Members: The following H2O members are nonauthor contributors: JoAnne Bachus, BSN, RN; Monica Borell, BSN, RN; Lenisa V Chang, MA, PhD; Patricia Crawford, RN; Sarah Ferris, BA; Jennifer Gold, BSN, RN; Judy A Heilman, BSN, RN; Jane C Khoury, PhD; Pierce Kuhnell, MS; Karen Lawley, BSN, RN; Margo Moore, MS, BSN, RN; Lynne O’Donnell, BSN, RN; Sarah Riddle, MD; Susan N Sherman, DPA; Angela M Statile, MD, MEd; Karen P Sullivan, BSN, RN; Heather Tubbs-Cooley, PhD, RN; Susan Wade-Murphy, MSN, RN; and Christine M White, MD, MAT.

The authors also thank David Keller, MD, for his guidance on the study.

The authors have no financial relationships or conflicts of interest relevant to this article to disclose.

Supported by funds from the Academic Pediatric Young Investigator Award (Dr A Shah) and the Patient-Centered Outcomes Research Institute Award (IHS-1306-0081, to Dr K Auger, Dr S Shah, Dr H Sucharew, Dr J Simmons), the National Institutes of Health (1K23AI112916, to Dr AF Beck), and the Agency for Healthcare Research and Quality (1K12HS026393-01, to Dr A Shah, K08-HS024735- 01A1, to Dr K Auger). Dr J Haney received Summer Undergraduate Research Fellowship funding through the Summer Undergraduate Research Fellowship at Cincinnati Children’s Hospital Medical Center.

All statements in this report, including findings and conclusions, are solely those of the authors and do not necessarily represent the views of the Patient-Centered Outcomes Research Institute, its Board of Governors, or the Methodology Committee.

Adverse Childhood Experiences, or ACEs, include exposure to abuse, neglect, or household dysfunction (eg, having a parent who is mentally ill) as a child.¹ Exposure to ACEs affects health into adulthood, with a dose-response relationship between ACEs and a range of comorbidities.¹ Adults with 6 or more ACEs have a 20-year shorter life expectancy than do those with no ACEs.¹ Still, ACEs are static; once experienced, that experience cannot be undone. However, resilience, or positive adaptation in the context of adversity, can be protective, buffering the negative effects of ACEs.^2,3 Protective factors that promote resilience include social capital, such as positive relationships with caregivers and peers.³

With their clear link to health outcomes across the life-course, there is a movement for pediatricians to screen children for ACEs⁴ and to develop strategies that promote resilience in children, parents, and families. However, screening a child for adversity has challenges because younger children may not have experienced an adverse exposure, or they may be unable to voice their experiences. Studies have demonstrated that parental adversity, or ACEs, may be a marker for childhood adversity.^5,6 Biological models also support this potential intergenerational effect of ACEs. Chronic exposure to stress, including ACEs, results in elevated cortisol via a dysregulated hypothalamic-pituitary-adrenal axis, which results in chronic inflammation.⁷ This “toxic stress” is prolonged, severe in intensity, and can lead to epigenetic changes that may be passed on to the next generation.^8,9

Hospitalization of an ill child, and the transition to home after that hospitalization, is a stressful event for children and families.¹⁰ This stress may be relevant to parents that have a history of a high rate of ACEs or a current low degree of resilience. Our previous work demonstrated that, in the inpatient setting, parents with high ACEs (≥4) or low resilience have increased coping difficulty 14 days after their child’s hospital discharge.¹¹ Our objective here was to evaluate whether a parent’s ACEs and/or resilience would also be associated with that child’s likelihood of reutilization. We hypothesized that more parental ACEs and/or lower parental resilience would be associated with revisits the emergency room, urgent care, or hospital readmissions.

Participants and Study Design

We conducted a prospective cohort study of parents of hospitalized children recruited from the “Hospital-to-Home Outcomes” Studies (H2O I and H2O II).^12,13 H2O I and II were prospective, single-center, randomized controlled trials designed to determine the effectiveness of either a nurse-led transitional home visit (H2O I) or telephone call (H2O II) on 30-day unplanned healthcare reutilization. The trials and this study were approved by the Cincinnati Children’s Institutional Review Board. All parents provided written informed consent.

Details of H2O I and II recruitment and design have been described previously.^12,13 Briefly, children were eligible for inclusion in either study if they were admitted to our institution’s general Hospital Medicine or the Hospital Medicine Complex Care Services; for H2O I, children hospitalized on the Neurology and Neurosurgery services were also eligible.^12,13 Patients were excluded if they were discharged to a residential facility, if they lived outside the home healthcare nurse service area, if they were eligible for skilled home healthcare services (eg, intravenous antibiotics), or if the participating caregiver was non-English speaking.^12,13 In H2O I, families were randomized either to receive a single nurse home visit within 96 hours of discharge or standard of care. In H2O II, families enrolled were randomized to receive a telephone call by a nurse within 96 hours of discharge or standard of care. As we have previously published, randomization in both trials successfully balanced the intervention and control arms with respect to key demographic characteristics.^12,13 For the analyses presented here, we focused on a subset of caregivers 18 years and older whose children were enrolled in either H2O I or II between August 2015 and October 2016. In both H2O trials, face-to-face and paper-based questionnaires were completed by parents during the index hospitalization.

Outcome and Predictors

Our primary outcome was unanticipated healthcare reutilization defined as return to the emergency room, urgent care, or unplanned readmission within 30 days of hospital discharge, consistent with the H2O trials. This was measured using the primary institution’s administrative data supplemented by a utilization database shared across regional hospitals.¹⁴ Readmissions were identified as “unplanned” using a previously validated algorithm,¹⁵ and treated as a dichotomous yes/no variable.

Our primary predictors were parental ACEs and resilience (see Appendix Tables). The ACE questionnaire addresses abuse, neglect, and household dysfunction in the first 18 years of life.¹ It is composed of 10 questions, each with a yes/no response.¹ We defined parents as low (ACE 0), moderate (ACE 1-3), or high (ACE ≥4) risk a priori because previous literature has described poor outcomes in adults with 4 or more ACEs.¹⁶

Given the sensitive nature of the questions, respondents independently completed the ACE questionnaire on paper instead of via the face-to-face survey. Respondents returned the completed questionnaire to the research assistant in a sealed envelope. All families received educational information on relevant hospital and community-based resources (eg, social work).

Parental resilience was measured using the Brief Resilience Scale (BRS). The BRS is 6 items, each on a 5-point Likert scale. Responses were averaged, providing a total score of 1-5; higher scores are representative of higher resilience.¹⁷ We treated the BRS score as a continuous variable. BRS has been used in clinical settings; it has demonstrated positive correlation with social support and negative correlation with fatigue.¹⁷ Parents answered BRS questions during the index pediatric hospitalization in a face-to-face interview.

Parent and Child Characteristics

Parent and child sociodemographic variables were also obtained during the face-to-face interview. Parental variables included age, gender, educational attainment, household income, employment status, and financial and social strain.¹¹ Educational attainment was analyzed in 2 categories—high school or less vs more than high school—because most discharge instructions are written at a high school reading level.¹⁸ Parents reported their annual household income in the following categories: <$15,000; $15,000-$29,999; $30,000-$44,999; $45,000-$59,999; $60,000-$89,999; $90,000-$119,999; ≥$120,000. Employment was dichotomized as not employed/student vs any employment. Financial and social strain were assessed using a series of 9 previously described questions.¹⁹ These questions assessed, via self-report, a family’s ability to make ends meet, ability to pay rent/mortgage or utilities, need to move in with others because of financial reasons, and ability to borrow money if needed, as well as home ownership and parental marital status.^15,19 Strain questions were all dichotomous (yes/no, single/not single). A composite variable was then constructed that categorized those reporting no strain items, 1 to 2 items, 3 to 4 items, and 5 or more items.²⁰

Child variables included race, ethnicity, age, primary care access,²¹ payer, and H2O treatment arm. Race categories were white/Caucasian, black/African American, American Indian or Alaskan Native, Asian or Pacific Islander, and other; ethnicity categories were Hispanic/Latino, non-Hispanic/Latino, and unknown. Given relatively low numbers of children reported to be Hispanic/Latino, we combined race and ethnicity into a single variable, categorized as non-Hispanic/white, non-Hispanic/black, and multiracial/Hispanic/other. Primary care access was assessed using the access subscale to the Parent’s Perception of Primary Care questionnaire. This includes assessment of a family’s ability to travel to their doctor, to see their doctor for routine or sick care, and to get help or advice on evenings or weekends. Scores were categorized as always adequate, almost always adequate, or sometimes/never adequate.²¹ Payer was dichotomized to private or public/self-pay.

Statistical Analyses

We examined the distribution of outcomes, predictors, and covariates. We compared sociodemographic characteristics of those respondents and nonrespondents to the ACE screen using the chi-square test for categorical variables or the t test for continuous variables. We used logistic regression to assess for associations between the independent variables of interest and reutilization, adjusting for potential confounders. To build our adjusted, multivariable model, we decided a priori to include child race/ethnicity, primary care access, financial and social strain, and trial treatment arm. We treated the H2O I control group as the referent group. Other covariates considered for inclusion were caregiver education, household income, employment, and payer. These were included in multivariable models if bivariate associations were significant at the P < .1 level. We assessed an ACE-by-resilience interaction term because we hypothesized that those with more ACEs and lower resilience may have more reutilization outcomes than parents with fewer ACEs and higher resilience. We also evaluated interaction terms between trial arm assignment and predictors to assess effects that may be introduced by the randomization. Predictors in the final logistic regression model were significant at the P < .05 level. Logistic regression assumption of little or no multicollinearity among the independent variables was verified in the final models. All analyses were performed with Stata v16 (Stata Corp, College Station, Texas).

There were a total of 1,787 parent-child dyads enrolled in the H2O I and II during the study period; 1,320 parents (74%) completed the ACE questionnaire and were included the analysis. Included parents were primarily female and employed, as well as educated beyond high school (Table 1). Overall, 64% reported one or more ACEs (range 0 to 9); 45% reported 1to 3, and 19% reported 4 or more ACEs. The most commonly reported ACEs were divorce (n = 573, 43%), exposure to alcoholism (n = 306, 23%), and exposure to mental illness (n = 281, 21%; Figure 1). Parents had a mean BRS score of 3.97 (range 1.17-5.00), with the distribution shown in Figure 2.

shah06840520e_t1.jpg

Of the 1,320 included patients, the average length of stay was 2.5 days, and 82% of hospitalizations were caused by acute medical issues (eg, bronchiolitis). A total of 211 children experienced a reutilization event within 30 days of discharge. In bivariate analysis, children with parents with 4 or more ACEs had a 2.02-times (95% CI 1.35-3.02) higher odds of experiencing a reutilization event than did those with parents reporting no ACEs. Parents with higher resilience scores had children with a lower odds of reutilization (odds ratio [OR] 0.77 95% CI 0.63-0.95).

shah06840520e_f1.jpg

In addition to our a priori variables, parental education, employment, and insurance met our significance threshold for inclusion in the multivariable model. The ACE-by-resilience interaction term was not significant and not included in the model. Similarly, there was no significant interaction between ACE and resilience and H2O treatment arm; the interaction terms were not included in the final adjusted model, but treatment arm assignment was kept as a covariate. A total of 1,292 children, out of the 1,320 respondents, remained in the final multivariable model; the excluded 28 had incomplete covariate data but were not otherwise different. In this final adjusted model, children with parents reporting 4 or more ACEs had a 1.69-times (95% CI 1.11-2.60) greater odds of reutilization than did those with parents reporting no ACEs (Table 2). Resilience failed to reach statistical significance in the adjusted model (OR 0.86, 95% CI 0.70-1.07).

shah06840520e_f2.jpg

We found that high-risk parents (4 or more ACEs) had children with an increased odds of healthcare reutilization, suggesting intergenerational effects of ACEs. We did not find a similar effect relating to parental resilience. We also did not find an interaction between parental ACEs and resilience, suggesting that a parent’s reported degree of resilience does not modify the effect of ACEs on reutilization risk.

shah06840520e_t2.jpg

Parental adversity may be a risk factor for a child’s unanticipated reutilization. We previously demonstrated that parents with 4 or more ACEs have more coping difficulty than a parent with no ACEs after a child’s hospitalization.¹¹ It is possible that parents with high adversity may have poorer coping mechanisms when dealing with a stressful situation, such as a child’s hospitalization. This may have resulted in inequitable outcomes (eg, increased reutilization) for their children. Other studies have confirmed such an intergenerational effect of adversity, linking a parent’s ACEs with poor developmental, behavioral, and health outcomes in their children.^6,22,23 O’Malley et al showed an association of parental ACEs to current adversities,²⁴ such as insurance or housing concerns, that affect the entirety of the household, including children. In short, it appears that parental ACEs may be a compelling predictor of current childhood adversity.

Resilience buffers the negative effects of ACEs; however, we did not find significant associations between resilience and reutilization or an interaction between ACEs and resilience. The factors that may contribute to reutilization are complex. In our previous work, parental resilience was associated with coping difficulty after discharge; but again, did not interact with parental ACEs.¹¹ Here, we suggest that while resilience may buffer the negative effects of ACEs, that buffering may not affect the likelihood of reutilization. It is also possible that the BRS tool is of less relevance on how one handles the stress of a child’s hospitalization. While the BRS is one measure of resilience, there are many other relevant constructs to resilience, such as connection to social supports, that also may also contribute to risk of reutilization.²⁵

Reducing the stress of a hospitalization itself and promoting a safe transition from hospital to home is critical to improving child health outcomes. Our data here, and in our previous work, demonstrate that a history of adversity and one’s current coping ability may drive a parent’s response to a child’s hospitalization and affect their capacity to care for that child after hospital discharge.¹¹ Additional in-hospital supports like child life, behavioral health, or pastoral care could reduce the stress of the hospitalization while also building positive coping mechanisms.^26-29 A meta-analysis demonstrated that such coping interventions can help alleviate the stress of a hospitalization.³⁰ Hill et al demonstrated successful stress reduction in parents of hospitalized children using a “Coping Kit for Parents.”³¹ Further studies are warranted to understand which interventions are most effective for children and families and whether they could be more effectively deployed if the inpatient team knew more about parental ACEs.

Screening for parental ACEs could help to identify patients at highest risk for a poor transition to home. Therefore, screening for parental adversity in clinical settings, including inpatient settings, may be relevant and valuable.³² Additionally, by recognizing the high prevalence of ACEs in an inpatient setting, hospitals and healthcare organizations could be motivated to develop and enact trauma-informed approaches. A trauma-informed care approach recognizes the intersection of trauma with health and social problems. With this recognition, care teams can more sensitively address the trauma as they provide relevant services.³³ Trauma-informed care is a secondary public health prevention approach that would help team members identify the prevalence and effects of trauma via screening, recognize the signs of a maladaptive response to stress, and respond by integrating awareness of trauma into practice management.^28,34 Both the National Academy of Medicine and the Agency for Healthcare Research and Quality have called for such a trauma-informed approach in primary care.³⁵ In response, many healthcare organizations have developed trauma-informed practices to better address the needs of the populations they serve. For example, provider training on this approach has led to improved rapport in patient-provider relationships.³⁶

Although ACE awareness is a component of trauma-informed care, there are still limitations of the original ACE questionnaire developed by Felitti et al. The existing tool is not inclusive of all adversities a parent or child may face. Moreover, its focus is on past exposures and experiences and not current health-related social needs (eg, food insecurity) which have known linkages with a range of health outcomes and health disparities.³⁷ Additionally, the original ACE questionnaire was created as a population level tool and not as a screening tool. If used as a screening tool, providers may view the questions as too sensitive to ask, and parents may have difficulty responding to and understanding the relevance to their child’s care. Therefore, we suggest that more evidence is required to understand how to best adapt ACE questions into a screening processes that may be implemented in a medical setting.

More evidence is also needed to determine when and where such screening may be most useful. A primary care provider would be best equipped to screen caregivers for ACEs given their established relationship with parents and patients. Given the potential relevance of such information for inpatient care provision, information could then flow from primary care to the inpatient team. However, because not all patients have established primary care providers and only 4% of pediatricians screen for ACEs,³⁸ it is important for inpatient medical teams to understand their role in identifying and addressing ACEs during hospital stays. Development of a screening tool, with input from all stakeholders—including parents—that is valid and feasible for use in a pediatric inpatient setting would be an important step forward. This tool should be paired with training in how to discuss these topics in a trauma-informed, nonjudgmental, empathic manner. We see this as a way in which providers can more effectively elicit an accurate response while simultaneously educating parents on the relevance of such sensitive topics during an acute hospital stay. We also recommend that screening should always be paired with response capabilities that connect those who screen positive with resources that could help them to navigate the stress experienced during and after a child’s hospitalization. Furthermore, communication with primary care providers about parents that screen positive should be integrated into the transition process.

This work has several limitations. First, our study was a part of randomized controlled trials conducted in one academic setting, which thereby limits generalizability. For example, we limited our cohort to those who were English-speaking patients only. This may bias our results because respondents with limited English proficiency may have different risk profiles than their English-speaking peers. In addition, the administration of the both the ACE and resilience questionnaires occurred during an acutely stressful period, which may influence how a parent responds to these questions. Also, both of the surveys are self-reported by parents, which may be susceptible to memory and response biases. Relatedly, we had a high number of nonrespondents, particularly to the ACE questionnaire. Our results are therefore only relevant to those who chose to respond and cannot be applied to nonrespondents. Further work assessing why one does or does not respond to such sensitive questions is an important area for future inquiry. Lastly, our cohort had limited medical complexity; future studies may consider links between parental ACEs (and resilience) and morbidity experienced by children with medical complexity.

Parents history of adversity is linked to their children’s unanticipated healthcare reutilization after a hospital discharge. Screening for parental stressors during a hospitalization may be an important first step to connecting parents and children to evidence-based interventions capable of mitigating the stress of hospitalization and promoting better, more seamless transitions from hospital to home.

Group Members: The following H2O members are nonauthor contributors: JoAnne Bachus, BSN, RN; Monica Borell, BSN, RN; Lenisa V Chang, MA, PhD; Patricia Crawford, RN; Sarah Ferris, BA; Jennifer Gold, BSN, RN; Judy A Heilman, BSN, RN; Jane C Khoury, PhD; Pierce Kuhnell, MS; Karen Lawley, BSN, RN; Margo Moore, MS, BSN, RN; Lynne O’Donnell, BSN, RN; Sarah Riddle, MD; Susan N Sherman, DPA; Angela M Statile, MD, MEd; Karen P Sullivan, BSN, RN; Heather Tubbs-Cooley, PhD, RN; Susan Wade-Murphy, MSN, RN; and Christine M White, MD, MAT.

The authors also thank David Keller, MD, for his guidance on the study.

The authors have no financial relationships or conflicts of interest relevant to this article to disclose.

Supported by funds from the Academic Pediatric Young Investigator Award (Dr A Shah) and the Patient-Centered Outcomes Research Institute Award (IHS-1306-0081, to Dr K Auger, Dr S Shah, Dr H Sucharew, Dr J Simmons), the National Institutes of Health (1K23AI112916, to Dr AF Beck), and the Agency for Healthcare Research and Quality (1K12HS026393-01, to Dr A Shah, K08-HS024735- 01A1, to Dr K Auger). Dr J Haney received Summer Undergraduate Research Fellowship funding through the Summer Undergraduate Research Fellowship at Cincinnati Children’s Hospital Medical Center.

All statements in this report, including findings and conclusions, are solely those of the authors and do not necessarily represent the views of the Patient-Centered Outcomes Research Institute, its Board of Governors, or the Methodology Committee.

The first case of coronavirus disease 2019 (COVID-19) in the United States was identified in Washington state in late January 2020. As of mid-April 2020, the number of US cases has increased to more than 800,000 with over 40,000 deaths. The limited available knowledge to guide medical decision-making combined with rapid progression of the pandemic has resulted in an urgent need to better define clinical, radiologic, and laboratory features of the disease, predictors of disease progression, predominant modes of transmission, and effective treatments. This urgency has led to a flood of manuscript submissions, which strains the scientific vetting process and leads to the spread of medical misinformation and potential for serious harm. As an example, a small observational (noncontrolled) study that used an antimalarial drug to treat COVID-19 patients was touted by several national leaders as proof of its effectiveness, despite substantial methodologic limitations.^1,2 While the article has not yet been retracted, the International Society of Antimicrobial Chemotherapy, the publishing journal’s society sponsor, subsequently issued a statement that “the article does not meet the Society’s expected standard.”³

With these concerns in mind, we recognize the importance of addressing the current pandemic and identifying areas where we can advance the field responsibly in the face of limited evidence in a rapidly evolving situation. Hospitalists throughout the world are facing unprecedented leadership challenges, navigating ethical stressors, and redesigning their care systems while learning rapidly and adapting nimbly. In this issue, we share leadership strategies, explore ethical challenges and controversies, describe successful practices, and provide personal reflections from a diverse group of hospitalists and leaders. As a journal, we have intentionally avoided rapid publication of articles with substantial methodologic limitations that are unlikely to advance our knowledge of COVID-19 even though such articles may generate substantial media coverage. Different regions of the country are at different stages of the pandemic; some hospitals are experiencing high patient volumes and struggling with shortages of equipment and supplies, while others are weeks away from peak disease activity or have avoided periods of high prevalence altogether. These varied experiences offer an opportunity to share our learnings and perspectives as we wait for more definitive evidence on best management practices. As part of our commitment to our colleagues in healthcare and to the broader scientific community, all Journal of Hospital Medicine articles related to COVID-19 and published during the pandemic will be open access (ie, freely accessible).

The first case of coronavirus disease 2019 (COVID-19) in the United States was identified in Washington state in late January 2020. As of mid-April 2020, the number of US cases has increased to more than 800,000 with over 40,000 deaths. The limited available knowledge to guide medical decision-making combined with rapid progression of the pandemic has resulted in an urgent need to better define clinical, radiologic, and laboratory features of the disease, predictors of disease progression, predominant modes of transmission, and effective treatments. This urgency has led to a flood of manuscript submissions, which strains the scientific vetting process and leads to the spread of medical misinformation and potential for serious harm. As an example, a small observational (noncontrolled) study that used an antimalarial drug to treat COVID-19 patients was touted by several national leaders as proof of its effectiveness, despite substantial methodologic limitations.^1,2 While the article has not yet been retracted, the International Society of Antimicrobial Chemotherapy, the publishing journal’s society sponsor, subsequently issued a statement that “the article does not meet the Society’s expected standard.”³

With these concerns in mind, we recognize the importance of addressing the current pandemic and identifying areas where we can advance the field responsibly in the face of limited evidence in a rapidly evolving situation. Hospitalists throughout the world are facing unprecedented leadership challenges, navigating ethical stressors, and redesigning their care systems while learning rapidly and adapting nimbly. In this issue, we share leadership strategies, explore ethical challenges and controversies, describe successful practices, and provide personal reflections from a diverse group of hospitalists and leaders. As a journal, we have intentionally avoided rapid publication of articles with substantial methodologic limitations that are unlikely to advance our knowledge of COVID-19 even though such articles may generate substantial media coverage. Different regions of the country are at different stages of the pandemic; some hospitals are experiencing high patient volumes and struggling with shortages of equipment and supplies, while others are weeks away from peak disease activity or have avoided periods of high prevalence altogether. These varied experiences offer an opportunity to share our learnings and perspectives as we wait for more definitive evidence on best management practices. As part of our commitment to our colleagues in healthcare and to the broader scientific community, all Journal of Hospital Medicine articles related to COVID-19 and published during the pandemic will be open access (ie, freely accessible).

The first case of coronavirus disease 2019 (COVID-19) in the United States was identified in Washington state in late January 2020. As of mid-April 2020, the number of US cases has increased to more than 800,000 with over 40,000 deaths. The limited available knowledge to guide medical decision-making combined with rapid progression of the pandemic has resulted in an urgent need to better define clinical, radiologic, and laboratory features of the disease, predictors of disease progression, predominant modes of transmission, and effective treatments. This urgency has led to a flood of manuscript submissions, which strains the scientific vetting process and leads to the spread of medical misinformation and potential for serious harm. As an example, a small observational (noncontrolled) study that used an antimalarial drug to treat COVID-19 patients was touted by several national leaders as proof of its effectiveness, despite substantial methodologic limitations.^1,2 While the article has not yet been retracted, the International Society of Antimicrobial Chemotherapy, the publishing journal’s society sponsor, subsequently issued a statement that “the article does not meet the Society’s expected standard.”³

With these concerns in mind, we recognize the importance of addressing the current pandemic and identifying areas where we can advance the field responsibly in the face of limited evidence in a rapidly evolving situation. Hospitalists throughout the world are facing unprecedented leadership challenges, navigating ethical stressors, and redesigning their care systems while learning rapidly and adapting nimbly. In this issue, we share leadership strategies, explore ethical challenges and controversies, describe successful practices, and provide personal reflections from a diverse group of hospitalists and leaders. As a journal, we have intentionally avoided rapid publication of articles with substantial methodologic limitations that are unlikely to advance our knowledge of COVID-19 even though such articles may generate substantial media coverage. Different regions of the country are at different stages of the pandemic; some hospitals are experiencing high patient volumes and struggling with shortages of equipment and supplies, while others are weeks away from peak disease activity or have avoided periods of high prevalence altogether. These varied experiences offer an opportunity to share our learnings and perspectives as we wait for more definitive evidence on best management practices. As part of our commitment to our colleagues in healthcare and to the broader scientific community, all Journal of Hospital Medicine articles related to COVID-19 and published during the pandemic will be open access (ie, freely accessible).

Readmission rates are used as metrics for care quality and reimbursement, with penalties applied to hospitals with higher than expected rates¹ and up to 30% of pediatric readmissions deemed potentially preventable.² There is a paucity of information on how to prevent pediatric readmissions,³ yet pediatric hospitals are tasked with implementing interventions for readmission reduction.

The Hospital to Home Outcomes (H2O) trial was a 2-arm, randomized controlled trial in which patients discharged from hospital medicine and neuroscience services at a single institution were randomized to receive a single home visit from a registered nurse (RN) within 96 hours of discharge.⁴ RNs completed a structured nurse visit designed specifically for the trial. Lists of “red flags” or warning signs associated with common diagnoses were provided to assist RNs in standardizing education about when to seek additional care. The hypothesis was that the postdischarge visits would result in lower reutilization rates (unplanned readmissions, emergency department [ED] visits, and urgent care visits).⁵

Unexpectedly, children randomized to receive the postdischarge nurse visit had higher rates of 30-day unplanned healthcare reutilization, with children randomly assigned to the intervention demonstrating higher odds of 30-day healthcare use (OR 1.33; 95% CI 1.003-1.76).⁴ We sought to understand perspectives on these unanticipated findings by obtaining input from relevant stakeholders. There were 2 goals for the qualitative analysis: first, to understand possible explanations of the increased reutilization finding; second, to elicit suggestions for improving the nurse visit intervention.

We selected an in-depth qualitative approach, using interviews and focus groups to explore underlying explanations for the increase in 30-day unplanned healthcare reutilization among those randomized to receive the postdischarge nurse visit during the H2O trial.⁴ Input was sought from 4 stakeholder groups—parents, primary care physicians (PCPs), hospital medicine physicians, and home care RNs—in an effort to triangulate data sources and elicit rich and diverse opinions. Approval was obtained from the Institutional Review Board prior to conducting the study.

Recruitment
Parents

Because we conducted interviews approximately 1 year after the trial’s conclusion, we purposefully selected families who were enrolled in the latter portion of the H2O trial in order to enhance recall. Beginning with the last families in the study, we sequentially contacted families in reverse order. We contacted 10 families in each of 4 categories (intervention/reutilization, intervention/no reutilization, control/reutilization, control/no reutilization). A total of 3 attempts were made by telephone to contact each family. Participants received a grocery store gift card for participating in the study.

Primary Care Physicians

We conducted focus groups with a purposive sample of physicians recruited from 2 community practices and 1 hospital-­owned practice.

Hospital Medicine Physicians

We conducted focus groups with a purposive sample of physicians from our Division of Hospital Medicine. There was a varying level of knowledge of the original trial; however, none of the participants were collaborators in the trial.

Home Care RNs

We conducted focus groups with a subset of RNs who were involved with trial visits. All RNs were members of the pediatric home care division associated with the hospital with specific training in caring for patients at home.

Data Collection

The study team designed question guides for each stakeholder group (Appendix 1). While questions were tailored for specific stakeholders, all guides included the following topics: benefits and challenges of nurse visits, suggestions for improving the intervention in future trials, and reactions to the trial results (once presented to participants). Only the results of the intention-to-treat (ITT) analysis were shared with stakeholders because ITT is considered the gold standard for trial analysis and allows easy understanding of the results.

A single investigator (A.L.) conducted parental interviews by telephone. Focus groups for PCPs, hospital medicine physicians, and RN groups were held at practice locations in private conference rooms and were conducted by trained moderators (S.N.S., A.L., and H.T.C.). Moderators probed responses to the open-ended questions to delve deeply into issues. The question guides were modified in an iterative fashion to include new concepts raised during interviews or focus groups. All interviews and focus groups were recorded and transcribed verbatim with all identifiable information redacted.

Data Analysis

During multiple cycles of inductive thematic analysis,⁶ we examined, discussed, interpreted, and organized responses to the open-ended questions,^6,7 analyzing each stakeholder group separately. First, transcripts were shared with and reviewed by the entire multidisciplinary team (12 members) which included hospital medicine physicians, PCPs, home care nursing leaders, a nurse scientist, a parent representative, research coordinators, and a qualitative research methodologist. Second, team members convened to discuss overall concepts and ideas and created the preliminary coding frameworks. Third, a smaller subgroup (research coordinator [A.L]., hospital medicine physician [S.R.], parent representative [M.M.], and qualitative research methodologist [S.N.S.]), refined the unique coding framework for each stakeholder group and then independently applied codes to participant comments. This subgroup met regularly to reach consensus about the assigned codes and to further refine the codebooks. The codes were organized into major and minor themes based on recurring patterns in the data and the salience or emphasis given by participants. The subgroup’s work was reviewed and discussed on an ongoing basis by the entire multidisciplinary team. Triangulation of the data was achieved in multiple ways. The preliminary results were shared in several forums, and feedback was solicited and incorporated. Two of 4 members of the subgroup analytic team were not part of the trial planning or data collection, providing a potentially broader perspective. All coding decisions were maintained in an electronic database, and an audit trail was created to document codebook revisions.

A total of 33 parents participated in the interviews (intervention/readmit [8], intervention/no readmit [8], control/readmit [8], and control/no readmit [9]). Although we selected families from all 4 categories, we were not able to explore qualitative differences between these groups because of the relatively low numbers of participants. Parent data was very limited as interviews were brief and “control” parents had not received the intervention. Three focus groups were held with PCPs (7 participants in total), 2 focus groups were held with hospital medicine physicians (12 participants), and 2 focus groups were held with RNs (10 participants).

Goal 1: Explanation of Reutilization Rates

During interviews and focus groups, the results of the H2O trial were discussed, and stakeholders were asked to comment on potential explanations of the findings. 4 major themes and 5 minor themes emerged from analysis of the transcripts (summarized in Table 1).

riddle04770318e_t1.jpg

Theme 1: Appropriateness of Patient Reutilization

Hospital medicine physicians and home care RNs questioned whether the reutilization events were clinically indicated. RNs wondered whether children who reutilized the ED were also readmitted to the hospital; many perceived that if the child was ill enough to be readmitted, then the ED revisit was warranted (Table 2). Parents commented on parental decision-making and changes in clinical status of the child leading to reutilization (Table 2).

riddle04770318e_t2a.jpg

Theme 2: Impact of Red Flags/Warning Sign Instructions on Family’s Reutilization Decisions

riddle04770318e_t2b.jpg

Theme 3: Hospital-Affiliated RNs “Directing Traffic” Back to Hospital

Both physician groups were concerned that, because the study was conducted by hospital-employed nurses, families might have been more likely to reaccess care at the hospital. Thus, the connection with the hospital was strengthened in the H2O model, potentially at the expense of the connection with PCPs. Physicians hypothesized that families might “still feel part of the medical system,” so families would return to the hospital if there was a problem. PCPs emphasized that there may have been straightforward situations that could have been handled appropriately in the outpatient office (Table 2).

Theme 4: Home Visit RNs Had a Low Threshold for Escalating Care

Parents and PCPs hypothesized that RNs are more conservative and, therefore, would have had a low threshold to refer back to the hospital if there were concerns in the home. One parent commented: “I guess, nurses are just by trade accustomed to erring on the side of caution and medical intervention instead of letting time take its course. … They’re more apt to say it’s better off to go to the hospital and have everything be fine” (Table 2).

Minor Themes

Participants also explained reutilization in ways that coalesced into 5 minor themes: (1) families receiving a visit might perceive that their child was sicker; (2) patients in the control group did not reutilize enough; (3) receiving more education on a child’s illness drives reutilization; (4) provider access issues; and (5) variability of RN experience may determine whether escalated care. Supportive quotations found in Appendix 2.

We directly asked parents if they would want a nurse home visit in the future after discussing the results of the study. Almost all of the parents in the intervention group and most of the parents in the control group were in favor of receiving a visit, even knowing that patients who had received a visit were more likely to reutilize care.

Goal 2: Suggestions for Improving Intervention Design

Three major themes and 3 minor themes were related to improving the design of the intervention (Table 1).

Theme 1: Need for Improved Postdischarge Communication

All stakeholder groups highlighted postdischarge communication as an area that could be improved. Parents were frustrated with regard to attempts to connect with inpatient physicians after discharge. PCPs suggested developing pathways for the RN to connect with the primary care office as opposed to the hospital. Hospital medicine physicians discussed a lack of consensus regarding patient ownership following discharge and were uncertain about what types of postdischarge symptoms PCPs would be comfortable managing. RNs described specific situations when they had difficulty contacting a physician to escalate care (Table 3).

riddle04770318e_t3a.jpg

Theme 2: Individualizing Home Visits—One Size Does Not Fit All

All stakeholder groups also encouraged “individualization” of home visits according to patient and family characteristics, diagnosis, and both timing and severity of illness. PCPs recommended visits only for certain diagnoses. Hospital medicine physicians voiced similar sentiments as the PCPs and added that worrisome family dynamics during a hospitalization, such as a lack of engagement with the medical team, might also warrant a visit. RNs suggested visits for those families with more concerns, for example, those with young children or children recovering from an acute respiratory illness (Table 3).

riddle04770318e_t3b.jpg

Theme 3: Providing Context for and Framing of Red Flags

Physicians and nurses suggested providing more context to “red flag” instructions and education. RNs emphasized that some families seemed to benefit from the opportunity to discuss their postdischarge concerns with a medical professional. Others appreciated concrete written instructions that spelled out how to respond in certain situations (Table 3).

Minor Themes

Three minor themes were revealed regarding intervention design improvement (Table 1): (1) streamlining the discharge process; (2) improving the definition of the scope and goal of intervention; and (3) extending inpatient team expertise post discharge. Supportive quotations can be found in Appendix 3.

When stakeholders were asked about why postdischarge RN visits led to increased postdischarge urgent healthcare visits, they questioned the appropriateness of the reutilization events, wondered about the lack of context for the warning signs that nurses provided families as part of the intervention, worried that families were encouraged to return to the hospital because of the ties of the trial to the hospital, and suggested that RNs had a low threshold to refer patients back to the hospital. When asked about how to design an improved nurse visit to better support families, stakeholders emphasized improving communication, individualizing the visit, and providing context around the red-flag discussion, enabling more nuanced instructions about how to respond to specific events.

A synthesis of themes suggests that potential drivers for increased utilization rates may lie in the design and goals of the initial project. The intervention was designed to support families and enhance education after discharge, with components derived from pretrial focus groups with families after a hospital discharge.⁸ The intervention was not designed to divert patients from the ED nor did it enhance access to the PCP. A second trial of the intervention adapted to a phone call also failed to decrease reutilization rates.⁹ Both physician stakeholder groups perceived that the intervention directed traffic back to the hospital because of the intervention design. Coupled with the perception that the red flags may have changed a family’s threshold for seeking care and/or that an RN may be more apt to refer back to care, this failure to push utilization to the primary care office may explain the unexpected trial results. Despite the stakeholders’ perception of enhanced connection back to the hospital as a result of the nurse visit, in analysis of visit referral patterns, a referral was made directly back to the ED in only 4 of the 651 trial visits (Tubbs-Cooley H, Riddle SR, Gold JM, et al.; under review. Pediatric clinical and social concerns identified by home visit nurses in the immediate postdischarge period 2020).

Both H2O trials demonstrated improved recall of red flags by parents who received the intervention, which may be important given the stakeholders’ perspectives that the red flags may not have been contextualized well enough. Yet neither trial demonstrated any differences in postdischarge coping or time to return to normal routine. In interviews with parents, despite the clearly stated results of increased reutilization, intervention parents endorsed a desire for a home visit in the future, raising the possibility that our outcome measures did not capture parents’ priorities adequately.

When asked to recommend design improvements of the intervention, 2 major themes (improvement in communication and individualization of visits) were discussed by all stakeholder groups, providing actionable information to modify or create new interventions. Focus groups with clinicians suggested that communication challenges may have influenced reutilization likelihood during the postdischarge period. RNs expressed uncertainty about who to call with problems or questions at the time of a home visit. This was compounded by difficulty reaching physicians. Both hospital medicine physicians and PCPs identified system challenges including questions of patient ownership, variable PCP practice communication preferences, and difficulty in identifying a partnered staff member (on either end of the inpatient-outpatient continuum) who was familiar with a specific patient. While the communication issues raised may reflect difficulties in our local healthcare system, there is broad evidence of postdischarge communication challenges. In adults, postdischarge communication failures between home health staff and physicians are associated with an increased risk of readmission.¹⁰ The real or perceived lack of communication between inpatient and outpatient providers can add to parental confusion post discharge.¹¹ Although there have been efforts to improve the reliability of communication across this gulf,^12,13 it is not clear whether changes to discharge communication could help to avoid pediatric reutilization events.¹⁴

The theme of individualization of the home nurse visit is consistent with evidence regarding the impact of focusing the intervention on patients with specific diagnoses or demographics. In adults, reduced reutilization associated with postdischarge home nurse visits has been described in specific populations such as patients with heart failure and chronic obstructive pulmonary disease.¹⁵ Impact of home nurse visits on patients within diagnosis-specific populations with certain demographics (such as advanced age) has also been described.¹⁶ In the pediatric population, readmission rates vary widely by diagnosis.¹⁷ A systematic review of interventions to reduce pediatric readmissions found increased impact of discharge interventions in specific populations (asthma, oncology, and NICU).³

Next steps may lie in interventions in targeted populations that function as part of a care continuum bridging the patient from the inpatient to the outpatient setting. A home nurse visit as part of this discharge structure may prove to have more impact on reducing reutilization. One population which accounts for a large proportion of readmissions and where there has been recent focus on discharge transition of care has been children with medical complexity.¹⁸ This group was largely excluded from the H2O trial. Postdischarge home nurse visits in this population have been found to be feasible and address many questions and problems, but the effect on readmission is less clear.¹⁹ Family priorities and preferences related to preparation for discharge, including family engagement, respect for discharge readiness, and goal of returning to normal routines, may be areas on which to focus with future interventions in this population.²⁰ In summary, although widespread postdischarge interventions (home nurse visit⁴ and nurse telephone call⁹) have not been found to be effective, targeting interventions to specific populations by diagnosis or demographic factors may prove to be more effective in reducing pediatric reutilization.

There were several strengths to this study. This qualitative approach allowed us to elucidate potential explanations for the H2O trial results from multiple perspectives. The multidisciplinary composition of our analytic team and the use of an iterative process sparked diverse contributions in a dynamic, ongoing discussion and interpretation of our data.

This study should be considered in the context of several limitations. For families and RNs, there was a time lag between participation in the trial and participation in the qualitative study call or focus group which could lead to difficulty recalling details. Only families who received the intervention could give opinions on their experience of the nurse visit, while families in the control group were asked to hypothesize. Focus groups with hospital medicine physicians and PCPs were purposive samples, and complete demographic information of participants was not collected.

Key stakeholders reflecting on a postdischarge RN visit trial suggested multiple potential explanations for the unexpected increase in reutilization in children randomized to the intervention. Certain participants questioned whether all reutilization events were appropriate or necessary. Others expressed concerns that the H2O intervention lacked context and directed children back to the hospital instead of the PCP. Parents, PCPs, hospital medicine physicians, and RNs all suggested that future transition-focused interventions should enhance postdischarge communication, strengthen connection to the PCP, and be more effectively tailored to the needs of the individual patient and family.

Acknowledgments

Collaborators: H2O Trial Study Group: Joanne Bachus, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Monica L Borell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lenisa V Chang, MA, PhD; Patricia Crawford, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sarah A Ferris, BA, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Judy A Heilman BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Jane C Khoury, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen Lawley, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lynne O’Donnell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Hadley S Sauers-Ford, MPH, Department of Pediatrics, UC Davis Health, Sacramento, California; Anita N Shah, DO, MPH, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lauren G Solan, MD, Med, University of Rochester, Rochester, New York; Heidi J Sucharew, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen P Sullivan, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Christine M White, MD, MAT, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio.

Readmission rates are used as metrics for care quality and reimbursement, with penalties applied to hospitals with higher than expected rates¹ and up to 30% of pediatric readmissions deemed potentially preventable.² There is a paucity of information on how to prevent pediatric readmissions,³ yet pediatric hospitals are tasked with implementing interventions for readmission reduction.

The Hospital to Home Outcomes (H2O) trial was a 2-arm, randomized controlled trial in which patients discharged from hospital medicine and neuroscience services at a single institution were randomized to receive a single home visit from a registered nurse (RN) within 96 hours of discharge.⁴ RNs completed a structured nurse visit designed specifically for the trial. Lists of “red flags” or warning signs associated with common diagnoses were provided to assist RNs in standardizing education about when to seek additional care. The hypothesis was that the postdischarge visits would result in lower reutilization rates (unplanned readmissions, emergency department [ED] visits, and urgent care visits).⁵

Unexpectedly, children randomized to receive the postdischarge nurse visit had higher rates of 30-day unplanned healthcare reutilization, with children randomly assigned to the intervention demonstrating higher odds of 30-day healthcare use (OR 1.33; 95% CI 1.003-1.76).⁴ We sought to understand perspectives on these unanticipated findings by obtaining input from relevant stakeholders. There were 2 goals for the qualitative analysis: first, to understand possible explanations of the increased reutilization finding; second, to elicit suggestions for improving the nurse visit intervention.

We selected an in-depth qualitative approach, using interviews and focus groups to explore underlying explanations for the increase in 30-day unplanned healthcare reutilization among those randomized to receive the postdischarge nurse visit during the H2O trial.⁴ Input was sought from 4 stakeholder groups—parents, primary care physicians (PCPs), hospital medicine physicians, and home care RNs—in an effort to triangulate data sources and elicit rich and diverse opinions. Approval was obtained from the Institutional Review Board prior to conducting the study.

Recruitment
Parents

Because we conducted interviews approximately 1 year after the trial’s conclusion, we purposefully selected families who were enrolled in the latter portion of the H2O trial in order to enhance recall. Beginning with the last families in the study, we sequentially contacted families in reverse order. We contacted 10 families in each of 4 categories (intervention/reutilization, intervention/no reutilization, control/reutilization, control/no reutilization). A total of 3 attempts were made by telephone to contact each family. Participants received a grocery store gift card for participating in the study.

Primary Care Physicians

We conducted focus groups with a purposive sample of physicians recruited from 2 community practices and 1 hospital-­owned practice.

Hospital Medicine Physicians

We conducted focus groups with a purposive sample of physicians from our Division of Hospital Medicine. There was a varying level of knowledge of the original trial; however, none of the participants were collaborators in the trial.

Home Care RNs

We conducted focus groups with a subset of RNs who were involved with trial visits. All RNs were members of the pediatric home care division associated with the hospital with specific training in caring for patients at home.

Data Collection

The study team designed question guides for each stakeholder group (Appendix 1). While questions were tailored for specific stakeholders, all guides included the following topics: benefits and challenges of nurse visits, suggestions for improving the intervention in future trials, and reactions to the trial results (once presented to participants). Only the results of the intention-to-treat (ITT) analysis were shared with stakeholders because ITT is considered the gold standard for trial analysis and allows easy understanding of the results.

A single investigator (A.L.) conducted parental interviews by telephone. Focus groups for PCPs, hospital medicine physicians, and RN groups were held at practice locations in private conference rooms and were conducted by trained moderators (S.N.S., A.L., and H.T.C.). Moderators probed responses to the open-ended questions to delve deeply into issues. The question guides were modified in an iterative fashion to include new concepts raised during interviews or focus groups. All interviews and focus groups were recorded and transcribed verbatim with all identifiable information redacted.

Data Analysis

During multiple cycles of inductive thematic analysis,⁶ we examined, discussed, interpreted, and organized responses to the open-ended questions,^6,7 analyzing each stakeholder group separately. First, transcripts were shared with and reviewed by the entire multidisciplinary team (12 members) which included hospital medicine physicians, PCPs, home care nursing leaders, a nurse scientist, a parent representative, research coordinators, and a qualitative research methodologist. Second, team members convened to discuss overall concepts and ideas and created the preliminary coding frameworks. Third, a smaller subgroup (research coordinator [A.L]., hospital medicine physician [S.R.], parent representative [M.M.], and qualitative research methodologist [S.N.S.]), refined the unique coding framework for each stakeholder group and then independently applied codes to participant comments. This subgroup met regularly to reach consensus about the assigned codes and to further refine the codebooks. The codes were organized into major and minor themes based on recurring patterns in the data and the salience or emphasis given by participants. The subgroup’s work was reviewed and discussed on an ongoing basis by the entire multidisciplinary team. Triangulation of the data was achieved in multiple ways. The preliminary results were shared in several forums, and feedback was solicited and incorporated. Two of 4 members of the subgroup analytic team were not part of the trial planning or data collection, providing a potentially broader perspective. All coding decisions were maintained in an electronic database, and an audit trail was created to document codebook revisions.

A total of 33 parents participated in the interviews (intervention/readmit [8], intervention/no readmit [8], control/readmit [8], and control/no readmit [9]). Although we selected families from all 4 categories, we were not able to explore qualitative differences between these groups because of the relatively low numbers of participants. Parent data was very limited as interviews were brief and “control” parents had not received the intervention. Three focus groups were held with PCPs (7 participants in total), 2 focus groups were held with hospital medicine physicians (12 participants), and 2 focus groups were held with RNs (10 participants).

Goal 1: Explanation of Reutilization Rates

During interviews and focus groups, the results of the H2O trial were discussed, and stakeholders were asked to comment on potential explanations of the findings. 4 major themes and 5 minor themes emerged from analysis of the transcripts (summarized in Table 1).

riddle04770318e_t1.jpg

Theme 1: Appropriateness of Patient Reutilization

Hospital medicine physicians and home care RNs questioned whether the reutilization events were clinically indicated. RNs wondered whether children who reutilized the ED were also readmitted to the hospital; many perceived that if the child was ill enough to be readmitted, then the ED revisit was warranted (Table 2). Parents commented on parental decision-making and changes in clinical status of the child leading to reutilization (Table 2).

riddle04770318e_t2a.jpg

Theme 2: Impact of Red Flags/Warning Sign Instructions on Family’s Reutilization Decisions

riddle04770318e_t2b.jpg

Theme 3: Hospital-Affiliated RNs “Directing Traffic” Back to Hospital

Both physician groups were concerned that, because the study was conducted by hospital-employed nurses, families might have been more likely to reaccess care at the hospital. Thus, the connection with the hospital was strengthened in the H2O model, potentially at the expense of the connection with PCPs. Physicians hypothesized that families might “still feel part of the medical system,” so families would return to the hospital if there was a problem. PCPs emphasized that there may have been straightforward situations that could have been handled appropriately in the outpatient office (Table 2).

Theme 4: Home Visit RNs Had a Low Threshold for Escalating Care

Parents and PCPs hypothesized that RNs are more conservative and, therefore, would have had a low threshold to refer back to the hospital if there were concerns in the home. One parent commented: “I guess, nurses are just by trade accustomed to erring on the side of caution and medical intervention instead of letting time take its course. … They’re more apt to say it’s better off to go to the hospital and have everything be fine” (Table 2).

Minor Themes

Participants also explained reutilization in ways that coalesced into 5 minor themes: (1) families receiving a visit might perceive that their child was sicker; (2) patients in the control group did not reutilize enough; (3) receiving more education on a child’s illness drives reutilization; (4) provider access issues; and (5) variability of RN experience may determine whether escalated care. Supportive quotations found in Appendix 2.

We directly asked parents if they would want a nurse home visit in the future after discussing the results of the study. Almost all of the parents in the intervention group and most of the parents in the control group were in favor of receiving a visit, even knowing that patients who had received a visit were more likely to reutilize care.

Goal 2: Suggestions for Improving Intervention Design

Three major themes and 3 minor themes were related to improving the design of the intervention (Table 1).

Theme 1: Need for Improved Postdischarge Communication

All stakeholder groups highlighted postdischarge communication as an area that could be improved. Parents were frustrated with regard to attempts to connect with inpatient physicians after discharge. PCPs suggested developing pathways for the RN to connect with the primary care office as opposed to the hospital. Hospital medicine physicians discussed a lack of consensus regarding patient ownership following discharge and were uncertain about what types of postdischarge symptoms PCPs would be comfortable managing. RNs described specific situations when they had difficulty contacting a physician to escalate care (Table 3).

riddle04770318e_t3a.jpg

Theme 2: Individualizing Home Visits—One Size Does Not Fit All

All stakeholder groups also encouraged “individualization” of home visits according to patient and family characteristics, diagnosis, and both timing and severity of illness. PCPs recommended visits only for certain diagnoses. Hospital medicine physicians voiced similar sentiments as the PCPs and added that worrisome family dynamics during a hospitalization, such as a lack of engagement with the medical team, might also warrant a visit. RNs suggested visits for those families with more concerns, for example, those with young children or children recovering from an acute respiratory illness (Table 3).

riddle04770318e_t3b.jpg

Theme 3: Providing Context for and Framing of Red Flags

Physicians and nurses suggested providing more context to “red flag” instructions and education. RNs emphasized that some families seemed to benefit from the opportunity to discuss their postdischarge concerns with a medical professional. Others appreciated concrete written instructions that spelled out how to respond in certain situations (Table 3).

Minor Themes

Three minor themes were revealed regarding intervention design improvement (Table 1): (1) streamlining the discharge process; (2) improving the definition of the scope and goal of intervention; and (3) extending inpatient team expertise post discharge. Supportive quotations can be found in Appendix 3.

When stakeholders were asked about why postdischarge RN visits led to increased postdischarge urgent healthcare visits, they questioned the appropriateness of the reutilization events, wondered about the lack of context for the warning signs that nurses provided families as part of the intervention, worried that families were encouraged to return to the hospital because of the ties of the trial to the hospital, and suggested that RNs had a low threshold to refer patients back to the hospital. When asked about how to design an improved nurse visit to better support families, stakeholders emphasized improving communication, individualizing the visit, and providing context around the red-flag discussion, enabling more nuanced instructions about how to respond to specific events.

A synthesis of themes suggests that potential drivers for increased utilization rates may lie in the design and goals of the initial project. The intervention was designed to support families and enhance education after discharge, with components derived from pretrial focus groups with families after a hospital discharge.⁸ The intervention was not designed to divert patients from the ED nor did it enhance access to the PCP. A second trial of the intervention adapted to a phone call also failed to decrease reutilization rates.⁹ Both physician stakeholder groups perceived that the intervention directed traffic back to the hospital because of the intervention design. Coupled with the perception that the red flags may have changed a family’s threshold for seeking care and/or that an RN may be more apt to refer back to care, this failure to push utilization to the primary care office may explain the unexpected trial results. Despite the stakeholders’ perception of enhanced connection back to the hospital as a result of the nurse visit, in analysis of visit referral patterns, a referral was made directly back to the ED in only 4 of the 651 trial visits (Tubbs-Cooley H, Riddle SR, Gold JM, et al.; under review. Pediatric clinical and social concerns identified by home visit nurses in the immediate postdischarge period 2020).

Both H2O trials demonstrated improved recall of red flags by parents who received the intervention, which may be important given the stakeholders’ perspectives that the red flags may not have been contextualized well enough. Yet neither trial demonstrated any differences in postdischarge coping or time to return to normal routine. In interviews with parents, despite the clearly stated results of increased reutilization, intervention parents endorsed a desire for a home visit in the future, raising the possibility that our outcome measures did not capture parents’ priorities adequately.

When asked to recommend design improvements of the intervention, 2 major themes (improvement in communication and individualization of visits) were discussed by all stakeholder groups, providing actionable information to modify or create new interventions. Focus groups with clinicians suggested that communication challenges may have influenced reutilization likelihood during the postdischarge period. RNs expressed uncertainty about who to call with problems or questions at the time of a home visit. This was compounded by difficulty reaching physicians. Both hospital medicine physicians and PCPs identified system challenges including questions of patient ownership, variable PCP practice communication preferences, and difficulty in identifying a partnered staff member (on either end of the inpatient-outpatient continuum) who was familiar with a specific patient. While the communication issues raised may reflect difficulties in our local healthcare system, there is broad evidence of postdischarge communication challenges. In adults, postdischarge communication failures between home health staff and physicians are associated with an increased risk of readmission.¹⁰ The real or perceived lack of communication between inpatient and outpatient providers can add to parental confusion post discharge.¹¹ Although there have been efforts to improve the reliability of communication across this gulf,^12,13 it is not clear whether changes to discharge communication could help to avoid pediatric reutilization events.¹⁴

The theme of individualization of the home nurse visit is consistent with evidence regarding the impact of focusing the intervention on patients with specific diagnoses or demographics. In adults, reduced reutilization associated with postdischarge home nurse visits has been described in specific populations such as patients with heart failure and chronic obstructive pulmonary disease.¹⁵ Impact of home nurse visits on patients within diagnosis-specific populations with certain demographics (such as advanced age) has also been described.¹⁶ In the pediatric population, readmission rates vary widely by diagnosis.¹⁷ A systematic review of interventions to reduce pediatric readmissions found increased impact of discharge interventions in specific populations (asthma, oncology, and NICU).³

Next steps may lie in interventions in targeted populations that function as part of a care continuum bridging the patient from the inpatient to the outpatient setting. A home nurse visit as part of this discharge structure may prove to have more impact on reducing reutilization. One population which accounts for a large proportion of readmissions and where there has been recent focus on discharge transition of care has been children with medical complexity.¹⁸ This group was largely excluded from the H2O trial. Postdischarge home nurse visits in this population have been found to be feasible and address many questions and problems, but the effect on readmission is less clear.¹⁹ Family priorities and preferences related to preparation for discharge, including family engagement, respect for discharge readiness, and goal of returning to normal routines, may be areas on which to focus with future interventions in this population.²⁰ In summary, although widespread postdischarge interventions (home nurse visit⁴ and nurse telephone call⁹) have not been found to be effective, targeting interventions to specific populations by diagnosis or demographic factors may prove to be more effective in reducing pediatric reutilization.

There were several strengths to this study. This qualitative approach allowed us to elucidate potential explanations for the H2O trial results from multiple perspectives. The multidisciplinary composition of our analytic team and the use of an iterative process sparked diverse contributions in a dynamic, ongoing discussion and interpretation of our data.

This study should be considered in the context of several limitations. For families and RNs, there was a time lag between participation in the trial and participation in the qualitative study call or focus group which could lead to difficulty recalling details. Only families who received the intervention could give opinions on their experience of the nurse visit, while families in the control group were asked to hypothesize. Focus groups with hospital medicine physicians and PCPs were purposive samples, and complete demographic information of participants was not collected.

Key stakeholders reflecting on a postdischarge RN visit trial suggested multiple potential explanations for the unexpected increase in reutilization in children randomized to the intervention. Certain participants questioned whether all reutilization events were appropriate or necessary. Others expressed concerns that the H2O intervention lacked context and directed children back to the hospital instead of the PCP. Parents, PCPs, hospital medicine physicians, and RNs all suggested that future transition-focused interventions should enhance postdischarge communication, strengthen connection to the PCP, and be more effectively tailored to the needs of the individual patient and family.

Acknowledgments

Collaborators: H2O Trial Study Group: Joanne Bachus, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Monica L Borell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lenisa V Chang, MA, PhD; Patricia Crawford, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sarah A Ferris, BA, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Judy A Heilman BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Jane C Khoury, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen Lawley, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lynne O’Donnell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Hadley S Sauers-Ford, MPH, Department of Pediatrics, UC Davis Health, Sacramento, California; Anita N Shah, DO, MPH, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lauren G Solan, MD, Med, University of Rochester, Rochester, New York; Heidi J Sucharew, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen P Sullivan, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Christine M White, MD, MAT, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio.

Readmission rates are used as metrics for care quality and reimbursement, with penalties applied to hospitals with higher than expected rates¹ and up to 30% of pediatric readmissions deemed potentially preventable.² There is a paucity of information on how to prevent pediatric readmissions,³ yet pediatric hospitals are tasked with implementing interventions for readmission reduction.

The Hospital to Home Outcomes (H2O) trial was a 2-arm, randomized controlled trial in which patients discharged from hospital medicine and neuroscience services at a single institution were randomized to receive a single home visit from a registered nurse (RN) within 96 hours of discharge.⁴ RNs completed a structured nurse visit designed specifically for the trial. Lists of “red flags” or warning signs associated with common diagnoses were provided to assist RNs in standardizing education about when to seek additional care. The hypothesis was that the postdischarge visits would result in lower reutilization rates (unplanned readmissions, emergency department [ED] visits, and urgent care visits).⁵

Unexpectedly, children randomized to receive the postdischarge nurse visit had higher rates of 30-day unplanned healthcare reutilization, with children randomly assigned to the intervention demonstrating higher odds of 30-day healthcare use (OR 1.33; 95% CI 1.003-1.76).⁴ We sought to understand perspectives on these unanticipated findings by obtaining input from relevant stakeholders. There were 2 goals for the qualitative analysis: first, to understand possible explanations of the increased reutilization finding; second, to elicit suggestions for improving the nurse visit intervention.

We selected an in-depth qualitative approach, using interviews and focus groups to explore underlying explanations for the increase in 30-day unplanned healthcare reutilization among those randomized to receive the postdischarge nurse visit during the H2O trial.⁴ Input was sought from 4 stakeholder groups—parents, primary care physicians (PCPs), hospital medicine physicians, and home care RNs—in an effort to triangulate data sources and elicit rich and diverse opinions. Approval was obtained from the Institutional Review Board prior to conducting the study.

Recruitment
Parents

Because we conducted interviews approximately 1 year after the trial’s conclusion, we purposefully selected families who were enrolled in the latter portion of the H2O trial in order to enhance recall. Beginning with the last families in the study, we sequentially contacted families in reverse order. We contacted 10 families in each of 4 categories (intervention/reutilization, intervention/no reutilization, control/reutilization, control/no reutilization). A total of 3 attempts were made by telephone to contact each family. Participants received a grocery store gift card for participating in the study.

Primary Care Physicians

We conducted focus groups with a purposive sample of physicians recruited from 2 community practices and 1 hospital-­owned practice.

Hospital Medicine Physicians

We conducted focus groups with a purposive sample of physicians from our Division of Hospital Medicine. There was a varying level of knowledge of the original trial; however, none of the participants were collaborators in the trial.

Home Care RNs

We conducted focus groups with a subset of RNs who were involved with trial visits. All RNs were members of the pediatric home care division associated with the hospital with specific training in caring for patients at home.

Data Collection

The study team designed question guides for each stakeholder group (Appendix 1). While questions were tailored for specific stakeholders, all guides included the following topics: benefits and challenges of nurse visits, suggestions for improving the intervention in future trials, and reactions to the trial results (once presented to participants). Only the results of the intention-to-treat (ITT) analysis were shared with stakeholders because ITT is considered the gold standard for trial analysis and allows easy understanding of the results.

A single investigator (A.L.) conducted parental interviews by telephone. Focus groups for PCPs, hospital medicine physicians, and RN groups were held at practice locations in private conference rooms and were conducted by trained moderators (S.N.S., A.L., and H.T.C.). Moderators probed responses to the open-ended questions to delve deeply into issues. The question guides were modified in an iterative fashion to include new concepts raised during interviews or focus groups. All interviews and focus groups were recorded and transcribed verbatim with all identifiable information redacted.

Data Analysis

During multiple cycles of inductive thematic analysis,⁶ we examined, discussed, interpreted, and organized responses to the open-ended questions,^6,7 analyzing each stakeholder group separately. First, transcripts were shared with and reviewed by the entire multidisciplinary team (12 members) which included hospital medicine physicians, PCPs, home care nursing leaders, a nurse scientist, a parent representative, research coordinators, and a qualitative research methodologist. Second, team members convened to discuss overall concepts and ideas and created the preliminary coding frameworks. Third, a smaller subgroup (research coordinator [A.L]., hospital medicine physician [S.R.], parent representative [M.M.], and qualitative research methodologist [S.N.S.]), refined the unique coding framework for each stakeholder group and then independently applied codes to participant comments. This subgroup met regularly to reach consensus about the assigned codes and to further refine the codebooks. The codes were organized into major and minor themes based on recurring patterns in the data and the salience or emphasis given by participants. The subgroup’s work was reviewed and discussed on an ongoing basis by the entire multidisciplinary team. Triangulation of the data was achieved in multiple ways. The preliminary results were shared in several forums, and feedback was solicited and incorporated. Two of 4 members of the subgroup analytic team were not part of the trial planning or data collection, providing a potentially broader perspective. All coding decisions were maintained in an electronic database, and an audit trail was created to document codebook revisions.

A total of 33 parents participated in the interviews (intervention/readmit [8], intervention/no readmit [8], control/readmit [8], and control/no readmit [9]). Although we selected families from all 4 categories, we were not able to explore qualitative differences between these groups because of the relatively low numbers of participants. Parent data was very limited as interviews were brief and “control” parents had not received the intervention. Three focus groups were held with PCPs (7 participants in total), 2 focus groups were held with hospital medicine physicians (12 participants), and 2 focus groups were held with RNs (10 participants).

Goal 1: Explanation of Reutilization Rates

During interviews and focus groups, the results of the H2O trial were discussed, and stakeholders were asked to comment on potential explanations of the findings. 4 major themes and 5 minor themes emerged from analysis of the transcripts (summarized in Table 1).

riddle04770318e_t1.jpg

Theme 1: Appropriateness of Patient Reutilization

Hospital medicine physicians and home care RNs questioned whether the reutilization events were clinically indicated. RNs wondered whether children who reutilized the ED were also readmitted to the hospital; many perceived that if the child was ill enough to be readmitted, then the ED revisit was warranted (Table 2). Parents commented on parental decision-making and changes in clinical status of the child leading to reutilization (Table 2).

riddle04770318e_t2a.jpg

Theme 2: Impact of Red Flags/Warning Sign Instructions on Family’s Reutilization Decisions

riddle04770318e_t2b.jpg

Theme 3: Hospital-Affiliated RNs “Directing Traffic” Back to Hospital

Both physician groups were concerned that, because the study was conducted by hospital-employed nurses, families might have been more likely to reaccess care at the hospital. Thus, the connection with the hospital was strengthened in the H2O model, potentially at the expense of the connection with PCPs. Physicians hypothesized that families might “still feel part of the medical system,” so families would return to the hospital if there was a problem. PCPs emphasized that there may have been straightforward situations that could have been handled appropriately in the outpatient office (Table 2).

Theme 4: Home Visit RNs Had a Low Threshold for Escalating Care

Parents and PCPs hypothesized that RNs are more conservative and, therefore, would have had a low threshold to refer back to the hospital if there were concerns in the home. One parent commented: “I guess, nurses are just by trade accustomed to erring on the side of caution and medical intervention instead of letting time take its course. … They’re more apt to say it’s better off to go to the hospital and have everything be fine” (Table 2).

Minor Themes

Participants also explained reutilization in ways that coalesced into 5 minor themes: (1) families receiving a visit might perceive that their child was sicker; (2) patients in the control group did not reutilize enough; (3) receiving more education on a child’s illness drives reutilization; (4) provider access issues; and (5) variability of RN experience may determine whether escalated care. Supportive quotations found in Appendix 2.

We directly asked parents if they would want a nurse home visit in the future after discussing the results of the study. Almost all of the parents in the intervention group and most of the parents in the control group were in favor of receiving a visit, even knowing that patients who had received a visit were more likely to reutilize care.

Goal 2: Suggestions for Improving Intervention Design

Three major themes and 3 minor themes were related to improving the design of the intervention (Table 1).

Theme 1: Need for Improved Postdischarge Communication

All stakeholder groups highlighted postdischarge communication as an area that could be improved. Parents were frustrated with regard to attempts to connect with inpatient physicians after discharge. PCPs suggested developing pathways for the RN to connect with the primary care office as opposed to the hospital. Hospital medicine physicians discussed a lack of consensus regarding patient ownership following discharge and were uncertain about what types of postdischarge symptoms PCPs would be comfortable managing. RNs described specific situations when they had difficulty contacting a physician to escalate care (Table 3).

riddle04770318e_t3a.jpg

Theme 2: Individualizing Home Visits—One Size Does Not Fit All

All stakeholder groups also encouraged “individualization” of home visits according to patient and family characteristics, diagnosis, and both timing and severity of illness. PCPs recommended visits only for certain diagnoses. Hospital medicine physicians voiced similar sentiments as the PCPs and added that worrisome family dynamics during a hospitalization, such as a lack of engagement with the medical team, might also warrant a visit. RNs suggested visits for those families with more concerns, for example, those with young children or children recovering from an acute respiratory illness (Table 3).

riddle04770318e_t3b.jpg

Theme 3: Providing Context for and Framing of Red Flags

Physicians and nurses suggested providing more context to “red flag” instructions and education. RNs emphasized that some families seemed to benefit from the opportunity to discuss their postdischarge concerns with a medical professional. Others appreciated concrete written instructions that spelled out how to respond in certain situations (Table 3).

Minor Themes

Three minor themes were revealed regarding intervention design improvement (Table 1): (1) streamlining the discharge process; (2) improving the definition of the scope and goal of intervention; and (3) extending inpatient team expertise post discharge. Supportive quotations can be found in Appendix 3.

When stakeholders were asked about why postdischarge RN visits led to increased postdischarge urgent healthcare visits, they questioned the appropriateness of the reutilization events, wondered about the lack of context for the warning signs that nurses provided families as part of the intervention, worried that families were encouraged to return to the hospital because of the ties of the trial to the hospital, and suggested that RNs had a low threshold to refer patients back to the hospital. When asked about how to design an improved nurse visit to better support families, stakeholders emphasized improving communication, individualizing the visit, and providing context around the red-flag discussion, enabling more nuanced instructions about how to respond to specific events.

A synthesis of themes suggests that potential drivers for increased utilization rates may lie in the design and goals of the initial project. The intervention was designed to support families and enhance education after discharge, with components derived from pretrial focus groups with families after a hospital discharge.⁸ The intervention was not designed to divert patients from the ED nor did it enhance access to the PCP. A second trial of the intervention adapted to a phone call also failed to decrease reutilization rates.⁹ Both physician stakeholder groups perceived that the intervention directed traffic back to the hospital because of the intervention design. Coupled with the perception that the red flags may have changed a family’s threshold for seeking care and/or that an RN may be more apt to refer back to care, this failure to push utilization to the primary care office may explain the unexpected trial results. Despite the stakeholders’ perception of enhanced connection back to the hospital as a result of the nurse visit, in analysis of visit referral patterns, a referral was made directly back to the ED in only 4 of the 651 trial visits (Tubbs-Cooley H, Riddle SR, Gold JM, et al.; under review. Pediatric clinical and social concerns identified by home visit nurses in the immediate postdischarge period 2020).

Both H2O trials demonstrated improved recall of red flags by parents who received the intervention, which may be important given the stakeholders’ perspectives that the red flags may not have been contextualized well enough. Yet neither trial demonstrated any differences in postdischarge coping or time to return to normal routine. In interviews with parents, despite the clearly stated results of increased reutilization, intervention parents endorsed a desire for a home visit in the future, raising the possibility that our outcome measures did not capture parents’ priorities adequately.

When asked to recommend design improvements of the intervention, 2 major themes (improvement in communication and individualization of visits) were discussed by all stakeholder groups, providing actionable information to modify or create new interventions. Focus groups with clinicians suggested that communication challenges may have influenced reutilization likelihood during the postdischarge period. RNs expressed uncertainty about who to call with problems or questions at the time of a home visit. This was compounded by difficulty reaching physicians. Both hospital medicine physicians and PCPs identified system challenges including questions of patient ownership, variable PCP practice communication preferences, and difficulty in identifying a partnered staff member (on either end of the inpatient-outpatient continuum) who was familiar with a specific patient. While the communication issues raised may reflect difficulties in our local healthcare system, there is broad evidence of postdischarge communication challenges. In adults, postdischarge communication failures between home health staff and physicians are associated with an increased risk of readmission.¹⁰ The real or perceived lack of communication between inpatient and outpatient providers can add to parental confusion post discharge.¹¹ Although there have been efforts to improve the reliability of communication across this gulf,^12,13 it is not clear whether changes to discharge communication could help to avoid pediatric reutilization events.¹⁴

The theme of individualization of the home nurse visit is consistent with evidence regarding the impact of focusing the intervention on patients with specific diagnoses or demographics. In adults, reduced reutilization associated with postdischarge home nurse visits has been described in specific populations such as patients with heart failure and chronic obstructive pulmonary disease.¹⁵ Impact of home nurse visits on patients within diagnosis-specific populations with certain demographics (such as advanced age) has also been described.¹⁶ In the pediatric population, readmission rates vary widely by diagnosis.¹⁷ A systematic review of interventions to reduce pediatric readmissions found increased impact of discharge interventions in specific populations (asthma, oncology, and NICU).³

Next steps may lie in interventions in targeted populations that function as part of a care continuum bridging the patient from the inpatient to the outpatient setting. A home nurse visit as part of this discharge structure may prove to have more impact on reducing reutilization. One population which accounts for a large proportion of readmissions and where there has been recent focus on discharge transition of care has been children with medical complexity.¹⁸ This group was largely excluded from the H2O trial. Postdischarge home nurse visits in this population have been found to be feasible and address many questions and problems, but the effect on readmission is less clear.¹⁹ Family priorities and preferences related to preparation for discharge, including family engagement, respect for discharge readiness, and goal of returning to normal routines, may be areas on which to focus with future interventions in this population.²⁰ In summary, although widespread postdischarge interventions (home nurse visit⁴ and nurse telephone call⁹) have not been found to be effective, targeting interventions to specific populations by diagnosis or demographic factors may prove to be more effective in reducing pediatric reutilization.

There were several strengths to this study. This qualitative approach allowed us to elucidate potential explanations for the H2O trial results from multiple perspectives. The multidisciplinary composition of our analytic team and the use of an iterative process sparked diverse contributions in a dynamic, ongoing discussion and interpretation of our data.

This study should be considered in the context of several limitations. For families and RNs, there was a time lag between participation in the trial and participation in the qualitative study call or focus group which could lead to difficulty recalling details. Only families who received the intervention could give opinions on their experience of the nurse visit, while families in the control group were asked to hypothesize. Focus groups with hospital medicine physicians and PCPs were purposive samples, and complete demographic information of participants was not collected.

Key stakeholders reflecting on a postdischarge RN visit trial suggested multiple potential explanations for the unexpected increase in reutilization in children randomized to the intervention. Certain participants questioned whether all reutilization events were appropriate or necessary. Others expressed concerns that the H2O intervention lacked context and directed children back to the hospital instead of the PCP. Parents, PCPs, hospital medicine physicians, and RNs all suggested that future transition-focused interventions should enhance postdischarge communication, strengthen connection to the PCP, and be more effectively tailored to the needs of the individual patient and family.

Acknowledgments

Collaborators: H2O Trial Study Group: Joanne Bachus, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Monica L Borell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lenisa V Chang, MA, PhD; Patricia Crawford, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sarah A Ferris, BA, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Judy A Heilman BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Jane C Khoury, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen Lawley, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lynne O’Donnell, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Hadley S Sauers-Ford, MPH, Department of Pediatrics, UC Davis Health, Sacramento, California; Anita N Shah, DO, MPH, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Lauren G Solan, MD, Med, University of Rochester, Rochester, New York; Heidi J Sucharew, PhD, Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Karen P Sullivan, BSN, RN, Department of Patient Services, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Christine M White, MD, MAT, Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio.

The Journal of Hospital Medicine introduced the Choosing Wisely^®: Next Steps in Improving Healthcare Value series in 2015¹ as a companion to the popular Choosing Wisely^®: Things We Do For No Reason^™ series² that was introduced in October in the same year. Both series were created in partnership with the American Board of Internal Medicine Foundation and were designed in the spirit of the Choosing Wisely^® campaign’s mission to “promote conversations between clinicians and patients” in choosing care supported by evidence that minimizes harm, including avoidance of unnecessary treatments and tests.³ The Choosing Wisely^®: Next Steps in Improving Healthcare Value series extends these principles as a forum for manuscripts that focus on translating value-based concepts into daily operations, including systems-level care delivery redesign initiatives, payment model innovations, and analyses of relevant policies or practice trends.

Since its inception, 16 Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscripts have been published, encompassing a wide range of topics such as postacute care transitions,⁴ the role of hospital medicine practice within accountable care organizations (ACOs),⁵ and quality and value at end-of-life.⁶

Few physicians receive health policy training.^7,8 Hospital medicine practitioners are a core component of the workforce, driving change and value-based improvements at almost every inpatient facility across the country. Regardless of their background or experience, hospital medicine practitioners must interface with legislation, regulation, and other policies every day while providing patient care. Intentional, value-based improvements are more likely to succeed if those providing direct patient care understand health policies, particularly the effects of those policies on transactional, point-of-care decisions.

We are pleased to expand the Choosing Wisely^®: Next Steps in Improving Healthcare Value series to include articles exploring health policy implications at the bedside. These articles will use common clinical scenarios to illuminate health policies most germane to hospital medicine practitioners and present applications of the policies as they relate to value at the level of patient–provider interactions. Each article will present a clinical scenario, explain key policy terms, address implications of specific policies in clinical practice, and propose how those policies can be improved (Appendix). Going forward, Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscript titles will include either “Policy in Clinical Practice” or “Improving Healthcare Value” to better establish a connection to the series and distinguish between the two article types.

The first Choosing Wisely^®: Next Steps in Improving Healthcare Value—Implications of Health Policy on Clinical Decision-Making manuscript appears in this issue of the Journal of Hospital Medicine.⁹ As is the current practice for Choosing Wisely^®: Next Steps in Improving Healthcare Value, authors are requested to send series editors a 500-word precis for review to ensure topic suitability before submission of a full manuscript. The precis, as well as any questions pertaining to the new series, can be directed to nextsteps@hospitalmedicine.org.

Acknowledgments

The authors thank the American Board of Internal Medicine Foundation for supporting this series.

The Journal of Hospital Medicine introduced the Choosing Wisely^®: Next Steps in Improving Healthcare Value series in 2015¹ as a companion to the popular Choosing Wisely^®: Things We Do For No Reason^™ series² that was introduced in October in the same year. Both series were created in partnership with the American Board of Internal Medicine Foundation and were designed in the spirit of the Choosing Wisely^® campaign’s mission to “promote conversations between clinicians and patients” in choosing care supported by evidence that minimizes harm, including avoidance of unnecessary treatments and tests.³ The Choosing Wisely^®: Next Steps in Improving Healthcare Value series extends these principles as a forum for manuscripts that focus on translating value-based concepts into daily operations, including systems-level care delivery redesign initiatives, payment model innovations, and analyses of relevant policies or practice trends.

Since its inception, 16 Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscripts have been published, encompassing a wide range of topics such as postacute care transitions,⁴ the role of hospital medicine practice within accountable care organizations (ACOs),⁵ and quality and value at end-of-life.⁶

Few physicians receive health policy training.^7,8 Hospital medicine practitioners are a core component of the workforce, driving change and value-based improvements at almost every inpatient facility across the country. Regardless of their background or experience, hospital medicine practitioners must interface with legislation, regulation, and other policies every day while providing patient care. Intentional, value-based improvements are more likely to succeed if those providing direct patient care understand health policies, particularly the effects of those policies on transactional, point-of-care decisions.

We are pleased to expand the Choosing Wisely^®: Next Steps in Improving Healthcare Value series to include articles exploring health policy implications at the bedside. These articles will use common clinical scenarios to illuminate health policies most germane to hospital medicine practitioners and present applications of the policies as they relate to value at the level of patient–provider interactions. Each article will present a clinical scenario, explain key policy terms, address implications of specific policies in clinical practice, and propose how those policies can be improved (Appendix). Going forward, Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscript titles will include either “Policy in Clinical Practice” or “Improving Healthcare Value” to better establish a connection to the series and distinguish between the two article types.

The first Choosing Wisely^®: Next Steps in Improving Healthcare Value—Implications of Health Policy on Clinical Decision-Making manuscript appears in this issue of the Journal of Hospital Medicine.⁹ As is the current practice for Choosing Wisely^®: Next Steps in Improving Healthcare Value, authors are requested to send series editors a 500-word precis for review to ensure topic suitability before submission of a full manuscript. The precis, as well as any questions pertaining to the new series, can be directed to nextsteps@hospitalmedicine.org.

Acknowledgments

The authors thank the American Board of Internal Medicine Foundation for supporting this series.

The Journal of Hospital Medicine introduced the Choosing Wisely^®: Next Steps in Improving Healthcare Value series in 2015¹ as a companion to the popular Choosing Wisely^®: Things We Do For No Reason^™ series² that was introduced in October in the same year. Both series were created in partnership with the American Board of Internal Medicine Foundation and were designed in the spirit of the Choosing Wisely^® campaign’s mission to “promote conversations between clinicians and patients” in choosing care supported by evidence that minimizes harm, including avoidance of unnecessary treatments and tests.³ The Choosing Wisely^®: Next Steps in Improving Healthcare Value series extends these principles as a forum for manuscripts that focus on translating value-based concepts into daily operations, including systems-level care delivery redesign initiatives, payment model innovations, and analyses of relevant policies or practice trends.

Since its inception, 16 Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscripts have been published, encompassing a wide range of topics such as postacute care transitions,⁴ the role of hospital medicine practice within accountable care organizations (ACOs),⁵ and quality and value at end-of-life.⁶

Few physicians receive health policy training.^7,8 Hospital medicine practitioners are a core component of the workforce, driving change and value-based improvements at almost every inpatient facility across the country. Regardless of their background or experience, hospital medicine practitioners must interface with legislation, regulation, and other policies every day while providing patient care. Intentional, value-based improvements are more likely to succeed if those providing direct patient care understand health policies, particularly the effects of those policies on transactional, point-of-care decisions.

We are pleased to expand the Choosing Wisely^®: Next Steps in Improving Healthcare Value series to include articles exploring health policy implications at the bedside. These articles will use common clinical scenarios to illuminate health policies most germane to hospital medicine practitioners and present applications of the policies as they relate to value at the level of patient–provider interactions. Each article will present a clinical scenario, explain key policy terms, address implications of specific policies in clinical practice, and propose how those policies can be improved (Appendix). Going forward, Choosing Wisely^®: Next Steps in Improving Healthcare Value manuscript titles will include either “Policy in Clinical Practice” or “Improving Healthcare Value” to better establish a connection to the series and distinguish between the two article types.

The first Choosing Wisely^®: Next Steps in Improving Healthcare Value—Implications of Health Policy on Clinical Decision-Making manuscript appears in this issue of the Journal of Hospital Medicine.⁹ As is the current practice for Choosing Wisely^®: Next Steps in Improving Healthcare Value, authors are requested to send series editors a 500-word precis for review to ensure topic suitability before submission of a full manuscript. The precis, as well as any questions pertaining to the new series, can be directed to nextsteps@hospitalmedicine.org.

Acknowledgments

The authors thank the American Board of Internal Medicine Foundation for supporting this series.

Cervical lymphadenitis is a common superficial neck infection in childhood. While most children with cervical lymphadenitis recover with antibiotic therapy, a subset can develop an abscess that may require surgical drainage. Radiologic imaging, most commonly ultrasound or computed tomography (CT), is often performed to identify such an abscess.^1-3 However, no national standards exist to guide clinician decision making around imaging in this population. In the absence of evidence-based guidelines, variability in frequency, timing, and modality of imaging likely exists in children hospitalized with cervical lymphadenitis.

As demonstrated for several other common pediatric conditions,^4,5 variability in imaging practices may contribute to overutilization of resources in children with cervical lymphadenitis. In particular, routinely conducting imaging on presentation may constitute overuse, as children with cervical lymphadenitis who present with less than 72 hours of neck swelling rarely undergo surgical drainage within the first 24 hours of hospitalization.^1,6,7 Imaging performed on presentation is often repeated later during hospitalization, particularly if the patient has not improved with antibiotic therapy. The net result may be unnecessary, redundant radiologic studies. Furthermore, serious complications such as bacteremia, extension of infection into the retropharyngeal space, or involvement of the airway or vasculature rarely occur in children with cervical lymphadenitis.^6,8 In this context, deferring initial imaging in this population is unlikely to lead to adverse outcomes and may reduce radiation exposure.

The overall objectives of this study are to describe hospital-level variation in imaging practices for pediatric cervical lymphadenitis and to examine the association between early imaging and outcomes in this population.

Study Design and Data Source

We conducted a multicenter, cross-sectional study using the Pediatric Health Information Systems (PHIS) database, which contains administrative and billing data from 49 geographically diverse children’s hospitals across the United States (US) affiliated with the Children’s Hospital Association (Lenexa, Kansas). PHIS includes data on patient demographics, discharge diagnoses, and procedures using the International Classification of Diseases, 9th (ICD-9) and 10th Revision (ICD-10) diagnosis codes, as well as daily billed resource utilization for laboratory tests, imaging studies, and medications. Encrypted medical record numbers permit longitudinal identification of children across multiple visits to the same hospital. Use of de-identified PHIS data was deemed to be nonhuman subjects research; our approach to validation of ICD codes using local electronic medical record review was reviewed and approved by the Cincinnati Children’s Hospital Medical Center Institutional Review Board.

Study Population

Our study team developed an algorithm to identify children with cervical lymphadenitis and minimize misclassification using PHIS (Appendix A). All children with lymphadenitis-related ICD-9 and ICD-10 discharge diagnosis codes were eligible for inclusion. Codes were validated at a single center via electronic medical record review; clinician-documented discharge diagnosis of cervical lymphadenitis or the presence of fever and unilateral or asymmetrical neck swelling with overlying skin changes was used as the reference standard. We then excluded children who did not receive antibiotics, children who received radiologic imaging not involving the head or neck (which suggested noncervical lymphadenitis or other illness), and children who had discharge diagnosis codes for other specified conditions that are sometimes associated with enlarged cervical lymph nodes but warrant different evaluation or treatment (eg, Kawasaki disease, retropharyngeal abscess, and dental abscess; Appendix A). Our final algorithm yielded a positive predictive value of 87.5% (95% CI: 79.2%-93.4%) when ICD-9 codes were considered, and 95.1% (95% CI: 88.9%-98.4%) when ICD-10 codes were considered (Appendix A).

This algorithm was subsequently applied to the PHIS database. Children ages two months to 18 years hospitalized at participating PHIS institutions between July 2013 and December 2017 with a diagnosis of cervical lymphadenitis as per the algorithm (Appendix A) were eligible for inclusion. For children with multiple eligible admissions during the study period, we only included the first hospitalization. Children with complex chronic condition diagnosis codes⁹ were excluded as their clinical complexity could influence decisions around timing and modality of diagnostic imaging. In addition, we excluded children who did not have an emergency department (ED) visit associated with their hospitalization. This step was intended to exclude children who were transferred from another institution, as imaging performed at outside institutions prior to transfer is not available in PHIS. To avoid overinflating hospital-level variation in the setting of a small sample size, we also excluded all children admitted to the five hospitals with fewer than 50 cases of cervical lymphadenitis during the study period. Our final cohort consisted of 44 PHIS hospitals.

Measures of Interest

To examine hospital-level variation in imaging practices, we measured the proportion of children at each hospital who underwent any neck imaging study, CT or ultrasound imaging, early imaging, and multiple imaging studies within a single hospitalization. Neck imaging was defined as the presence of a billing code for ultrasound, CT, or magnetic resonance imaging (MRI) study of the neck (Appendix B). Early imaging was defined as neck imaging conducted on day 0 of hospitalization (ie, calendar day of admission and ending at midnight). Multiple imaging studies were defined as the receipt of more than one imaging study, regardless of timing or modality. We also measured the proportion of children by hospital who received surgical drainage, defined by the presence of procedure codes for incision and drainage of abscess of the neck (Appendix B).

In examining patient-level association between early imaging and clinical outcomes, our primary outcome of interest was the receipt of multiple imaging studies. Secondary outcomes included rates of surgical drainage, length of stay (in hospital days), and rates of lymphadenitis-related hospital readmission within 30 days of index discharge.

Covariates

Baseline demographic characteristics included age, gender, race/ethnicity, and insurance type. We measured ED visits associated with lymphadenitis-related diagnosis codes in the 30 days prior to admission as a proxy measure for illness duration prior to presentation. To approximate illness severity, we included the following covariates: rates of intensive care unit admission on presentation, rates of receipt of intravenous (IV) analgesia (Appendix B) on hospital days prior to surgical drainage, and rates of receipt of broad-spectrum antibiotics on day 0 or 1 of hospitalization. Broad-spectrum antibiotics (Appendix B) were defined by an independent three-person review of available antibiotic codes (SD, SSS, and JT); differences were resolved by group consensus.

Analysis

Categorical variables were described using frequencies and percentages, while continuous data were described using median and interquartile range. We described hospital-level variation in imaging practices by calculating and comparing the proportion of children at each hospital who underwent any neck imaging study, CT imaging, ultrasound imaging, early imaging, multiple imaging studies, and surgical drainage.

Patient-level demographics and clinical characteristics were compared across groups using chi-square test. To examine the association between early imaging and outcomes, we used generalized linear or logistic mixed effects models to control for patient demographic characteristics and clinical markers of illness duration and severity, with a random effect for hospital to account for clustering. Patient demographics in the model defined a priori included age, race/ethnicity, and insurance type; clinical characteristics included prior ED visit for lymphadenitis, initial intensive care unit (ICU) admission, use of IV analgesia, and use of broad-spectrum antibiotics on day 0 or 1 of hospitalization. To assess the potential for misclassification related to the availability of calendar day but not time of imaging in PHIS, we conducted a secondary analysis to examine the patient-level association between early imaging and outcomes using an alternative definition for early imaging (defined as imaging conducted on day 0 or day 1 of hospitalization).

desai04071120e_f1.jpg

We identified 19,785 PHIS hospitalizations with lymphadenitis-related discharge diagnosis codes between July 1, 2013 and December 31, 2017. Applying our algorithm and exclusion criteria, we assembled a cohort of 10,014 children hospitalized with cervical lymphadenitis (Figure 1). Two-thirds of the children in our cohort were <4 years old, 42% were non-Hispanic white, and 63% had a government payor (Table 1). Neck imaging (ultrasound, CT, or MRI) was conducted in 8,103 (81%) children. CT imaging was performed in 4,097 (41%) of children, and early imaging was conducted in 6,111 (61%) of children with cervical lymphadenitis.

We noted hospital-level variation in rates of any neck imaging (median: 82.1%, interquartile range [IQR]: 77.7%-85.5%, full range: 68.7%-93.1%), CT imaging (median: 42.3%, IQR: 26.7%-55.2%, full range: 12.0%-81.5%), early imaging (median: 64.4%, IQR: 59.8%-68.4%, full range: 13.8%-76.9%), and multiple imaging studies (median: 23.7%, IQR: 18.6%-28.9%, full range: 1.2%-40.7%; Figure 2). Rates of surgical drainage also varied by hospital (median: 35.1%, IQR: 31.3%-42.0%, full range: 17.1%-54.5%).

desai04071120e_f2.jpg

desai04071120e_t1.jpg

desai04071120e_t2.jpg

In this large multicenter study of children with cervical lymphadenitis, we found variation in imaging practices across 44 US children’s hospitals. Children with cervical lymphadenitis who underwent early imaging were more likely to receive multiple imaging studies during a single hospitalization than those who did not receive early imaging. At the patient level, early imaging was also associated with higher rates of surgical drainage, more frequent 30-day readmission, and longer lengths of stay.

To our knowledge, imaging practices in the population of children hospitalized with cervical lymphadenitis have not been previously characterized in the US; one study from Atlanta, Georgia, describes imaging practices in all children evaluated in the ED.¹ Single-center studies of children hospitalized with cervical lymphadenitis have been previously conducted in Canada⁶ and New Zealand,⁸ in which 42%-51% of children received imaging. In our study, most (81%) children hospitalized with lymphadenitis received some form of imaging, with 61% of all children receiving early imaging. Furthermore, 41% received CT imaging, as compared with 8%-10% of children in the aforementioned studies from Canada and New Zealand.^6,8 This finding is consistent with a pattern of imaging overuse in the US, which has amongst the highest utilization rates globally for advanced imaging such as CT and MRI.^10,11 Identifying opportunities to safely reduce routine imaging, particularly CT imaging, in this population could decrease unnecessary radiation exposure without compromising outcomes.

We also noted variability in imaging practices across PHIS hospitals. Some of this variability may be partially explained by differences in the patient population or illness severity across hospitals. However, given the absence of evidence-based best practices for children with cervical lymphadenitis, clinicians may rely on anecdotal experience or local practice culture to guide their decision making,¹² leading to variability in frequency, timing, and modality of imaging.

At the patient level, we found that children who received early imaging were more likely to receive multiple imaging studies. This finding supports our hypothesis that clinicians often order a second imaging study when the initial imaging study does not clearly demonstrate an abscess, and the child subsequently fails to demonstrate clear improvement after 24-48 hours of antibiotics.

Furthermore, early imaging was associated with overall increased utilization in our cohort, including increased likelihood of surgical drainage, 30-day readmission for lymphadenitis, as well as longer lengths of stay. Confounding may be one explanation for this finding. For instance, clinicians may pursue early imaging in children who present with longer duration of symptoms or more severe illness on presentation, as these factors may be associated with abscess formation.^1,6,7 These clinical covariates are not available in PHIS. Thus, we used prior ED visits for lymphadenitis to approximate illness duration, and initial admission to ICU, receipt of IV analgesia, and receipt of broad-spectrum antibiotics to approximate illness severity in an attempt to mitigate confounding. However, our proxy measures may not appropriately estimate illness duration and severity. For instance, children who had urgent care or outpatient visits for lymphadenitis would not be captured using the proxy of prior ED visit for lymphadenitis. Similarly, use of broad-spectrum antibiotics and IV analgesia may be influenced by provider or institutional preference rather than illness severity. Thus, residual confounding may exist despite adjusting for these measures.

On the other hand, it is also possible that a proportion of children with a small fluid collection on imaging may have improved with antibiotics alone. There is a growing body of evidence in children with other head and neck infections (eg, retropharyngeal abscess and orbital cellulitis with periosteal abscess)^13-15 that suggests that children with small abscesses often improve with antibiotic therapy alone. In children with cervical lymphadenitis who have small or developing abscesses identified via routine imaging on presentation, clinicians may be driven to pursue a surgical intervention with uncertain benefit. Deferring routine imaging in this population may provide an opportunity to improve the value of care in children with lymphadenitis without adversely affecting outcomes.

Upon closer examination of readmissions, children who received early imaging during index hospitalization were more likely to have a 30-day readmission when only evaluating the subset of patients who did not receive surgical drainage during the index admission. This suggests that readmissions are less likely attributable to surgical complications and more likely a reflection of the natural history of lymphadenitis in which a subset of patients eventually develop an abscess. Further supporting this, 61% of children who had a 30-day readmission for lymphadenitis underwent surgical drainage during readmission. Given that lymphadenitis is a slow-brewing infection in which serious complications are rare, patients who demonstrate gradual clinical improvement do not need to remain hospitalized and serially imaged to identify a possible abscess. Outpatient expectant management and readmission as needed for drainage may be an acceptable approach.

This study has several limitations given our use of an administrative database. Children with lymphadenitis may have been misclassified as these patients were identified using discharge diagnosis codes. To mitigate this potential misclassification, we conducted a structured validation process and found that the included codes had high positive predictive values (Appendix A). This validation process was conducted at a single hospital, and coding may vary across hospitals. To approximate sensitivity, we also sampled children without our included codes but with neck imaging and antibiotic use, and found that rates of cervical lymphadenitis were very low among children without our included diagnosis codes.

Furthermore, we were unable to measure the exact time of imaging study in PHIS; we used imaging conducted on hospital day 0 as a proxy measure for imaging conducted within the first 24 hours of presentation. With this definition, some children who had early imaging were likely misclassified as not having received early imaging. For example, a patient who arrived in the ED at 9 pm on day 0 of admission and had a neck ultrasound performed at 1 am would be classified as having had an imaging study on day 1 of hospitalization even though the imaging study was conducted within 4 hours of presentation. Using an alternative definition of early imaging as imaging conducted on hospital day 0 and day 1, we found a much higher adjusted OR for multiple imaging studies, with similar associations for secondary outcomes. As such, our definition of early imaging as day 0 likely biases the results toward the null; the true increase in likelihood of multiple imaging for those who receive early imaging is probably greater than our conservative estimation.

Additionally, there may be a subset of children who underwent imaging prior to presentation at the PHIS hospital ED for further workup and admission. Imaging conducted outside a PHIS hospital was not captured in this database. Similarly, children who had a readmission at a different hospital than their index admission would not be captured using PHIS. Finally, PHIS captures data from children’s hospitals; practices at these hospitals may not be generalizable to practices in the community hospital setting.

In conclusion, we found that imaging practices in children hospitalized with cervical lymphadenitis were widely variable across hospitals. Children receiving early imaging had more resource utilization and intervention when compared with children who did not receive early imaging. Our findings may represent a cascade effect, in which routinely conducted early imaging prompts clinicians to pursue more testing and interventions in this population. Future studies should obtain more detailed patient level covariates to further characterize clinical factors that may impact decisions around imaging and clinical outcomes for children with cervical lymphadenitis.

Acknowledgments

The authors would like to acknowledge the following investigators for their contributions to data interpretation and review of the final manuscript: Angela Choe MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Margaret Rush MD, Children’s National Medical Center, Washington, DC; Ryosuke Takei MD, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; Wallis Molchen DO, Texas Children’s Hospital, Houston, Texas; Stephanie Royer Moss MD, Cleveland Clinic, Cleveland, Ohio; Rebecca Dang, MD, Lucile Packard Children’s Hospital Stanford, Palo Alto, California; Joy Solano MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas; Nathaniel P. Goodrich MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Ngozi Eboh MD, Texas Tech University Health Sciences Center, Dallas, Texas; Ashley Jenkins MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Rebecca Steuart MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sonya Tang Girdwood MD, PhD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Alissa McInerney MD, Maria Fareri Children’s Hospital at Westchester Medical Center, Valhalla, New York; Sumeet Banker MD, MPH, New York Presbyterian Morgan Stanley Children’s Hospital, New York, New York; Corrie McDaniel DO, Seattle Children’s Hospital, Seattle, Washington; Christiane Lenzen MD, Rady Children’s Hospital, San Diego, California; Aleisha Nabower MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Waheeda Samady MD, Ann & Robert H. Lurie Children’s Hospital, Chicago, Illinois; Jennifer Chen MD, Rady Children’s Hospital, San Diego, California; Marquita Genies MD, MPH, John’s Hopkins Children’s Center, Baltimore, Maryland; Justin Lockwood MD, Children’s Hospital Colorado, Aurora, Colorado; David Synhorst MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas.

Cervical lymphadenitis is a common superficial neck infection in childhood. While most children with cervical lymphadenitis recover with antibiotic therapy, a subset can develop an abscess that may require surgical drainage. Radiologic imaging, most commonly ultrasound or computed tomography (CT), is often performed to identify such an abscess.^1-3 However, no national standards exist to guide clinician decision making around imaging in this population. In the absence of evidence-based guidelines, variability in frequency, timing, and modality of imaging likely exists in children hospitalized with cervical lymphadenitis.

As demonstrated for several other common pediatric conditions,^4,5 variability in imaging practices may contribute to overutilization of resources in children with cervical lymphadenitis. In particular, routinely conducting imaging on presentation may constitute overuse, as children with cervical lymphadenitis who present with less than 72 hours of neck swelling rarely undergo surgical drainage within the first 24 hours of hospitalization.^1,6,7 Imaging performed on presentation is often repeated later during hospitalization, particularly if the patient has not improved with antibiotic therapy. The net result may be unnecessary, redundant radiologic studies. Furthermore, serious complications such as bacteremia, extension of infection into the retropharyngeal space, or involvement of the airway or vasculature rarely occur in children with cervical lymphadenitis.^6,8 In this context, deferring initial imaging in this population is unlikely to lead to adverse outcomes and may reduce radiation exposure.

The overall objectives of this study are to describe hospital-level variation in imaging practices for pediatric cervical lymphadenitis and to examine the association between early imaging and outcomes in this population.

Study Design and Data Source

We conducted a multicenter, cross-sectional study using the Pediatric Health Information Systems (PHIS) database, which contains administrative and billing data from 49 geographically diverse children’s hospitals across the United States (US) affiliated with the Children’s Hospital Association (Lenexa, Kansas). PHIS includes data on patient demographics, discharge diagnoses, and procedures using the International Classification of Diseases, 9th (ICD-9) and 10th Revision (ICD-10) diagnosis codes, as well as daily billed resource utilization for laboratory tests, imaging studies, and medications. Encrypted medical record numbers permit longitudinal identification of children across multiple visits to the same hospital. Use of de-identified PHIS data was deemed to be nonhuman subjects research; our approach to validation of ICD codes using local electronic medical record review was reviewed and approved by the Cincinnati Children’s Hospital Medical Center Institutional Review Board.

Study Population

Our study team developed an algorithm to identify children with cervical lymphadenitis and minimize misclassification using PHIS (Appendix A). All children with lymphadenitis-related ICD-9 and ICD-10 discharge diagnosis codes were eligible for inclusion. Codes were validated at a single center via electronic medical record review; clinician-documented discharge diagnosis of cervical lymphadenitis or the presence of fever and unilateral or asymmetrical neck swelling with overlying skin changes was used as the reference standard. We then excluded children who did not receive antibiotics, children who received radiologic imaging not involving the head or neck (which suggested noncervical lymphadenitis or other illness), and children who had discharge diagnosis codes for other specified conditions that are sometimes associated with enlarged cervical lymph nodes but warrant different evaluation or treatment (eg, Kawasaki disease, retropharyngeal abscess, and dental abscess; Appendix A). Our final algorithm yielded a positive predictive value of 87.5% (95% CI: 79.2%-93.4%) when ICD-9 codes were considered, and 95.1% (95% CI: 88.9%-98.4%) when ICD-10 codes were considered (Appendix A).

This algorithm was subsequently applied to the PHIS database. Children ages two months to 18 years hospitalized at participating PHIS institutions between July 2013 and December 2017 with a diagnosis of cervical lymphadenitis as per the algorithm (Appendix A) were eligible for inclusion. For children with multiple eligible admissions during the study period, we only included the first hospitalization. Children with complex chronic condition diagnosis codes⁹ were excluded as their clinical complexity could influence decisions around timing and modality of diagnostic imaging. In addition, we excluded children who did not have an emergency department (ED) visit associated with their hospitalization. This step was intended to exclude children who were transferred from another institution, as imaging performed at outside institutions prior to transfer is not available in PHIS. To avoid overinflating hospital-level variation in the setting of a small sample size, we also excluded all children admitted to the five hospitals with fewer than 50 cases of cervical lymphadenitis during the study period. Our final cohort consisted of 44 PHIS hospitals.

Measures of Interest

To examine hospital-level variation in imaging practices, we measured the proportion of children at each hospital who underwent any neck imaging study, CT or ultrasound imaging, early imaging, and multiple imaging studies within a single hospitalization. Neck imaging was defined as the presence of a billing code for ultrasound, CT, or magnetic resonance imaging (MRI) study of the neck (Appendix B). Early imaging was defined as neck imaging conducted on day 0 of hospitalization (ie, calendar day of admission and ending at midnight). Multiple imaging studies were defined as the receipt of more than one imaging study, regardless of timing or modality. We also measured the proportion of children by hospital who received surgical drainage, defined by the presence of procedure codes for incision and drainage of abscess of the neck (Appendix B).

In examining patient-level association between early imaging and clinical outcomes, our primary outcome of interest was the receipt of multiple imaging studies. Secondary outcomes included rates of surgical drainage, length of stay (in hospital days), and rates of lymphadenitis-related hospital readmission within 30 days of index discharge.

Covariates

Baseline demographic characteristics included age, gender, race/ethnicity, and insurance type. We measured ED visits associated with lymphadenitis-related diagnosis codes in the 30 days prior to admission as a proxy measure for illness duration prior to presentation. To approximate illness severity, we included the following covariates: rates of intensive care unit admission on presentation, rates of receipt of intravenous (IV) analgesia (Appendix B) on hospital days prior to surgical drainage, and rates of receipt of broad-spectrum antibiotics on day 0 or 1 of hospitalization. Broad-spectrum antibiotics (Appendix B) were defined by an independent three-person review of available antibiotic codes (SD, SSS, and JT); differences were resolved by group consensus.

Analysis

Categorical variables were described using frequencies and percentages, while continuous data were described using median and interquartile range. We described hospital-level variation in imaging practices by calculating and comparing the proportion of children at each hospital who underwent any neck imaging study, CT imaging, ultrasound imaging, early imaging, multiple imaging studies, and surgical drainage.

Patient-level demographics and clinical characteristics were compared across groups using chi-square test. To examine the association between early imaging and outcomes, we used generalized linear or logistic mixed effects models to control for patient demographic characteristics and clinical markers of illness duration and severity, with a random effect for hospital to account for clustering. Patient demographics in the model defined a priori included age, race/ethnicity, and insurance type; clinical characteristics included prior ED visit for lymphadenitis, initial intensive care unit (ICU) admission, use of IV analgesia, and use of broad-spectrum antibiotics on day 0 or 1 of hospitalization. To assess the potential for misclassification related to the availability of calendar day but not time of imaging in PHIS, we conducted a secondary analysis to examine the patient-level association between early imaging and outcomes using an alternative definition for early imaging (defined as imaging conducted on day 0 or day 1 of hospitalization).

desai04071120e_f1.jpg

We identified 19,785 PHIS hospitalizations with lymphadenitis-related discharge diagnosis codes between July 1, 2013 and December 31, 2017. Applying our algorithm and exclusion criteria, we assembled a cohort of 10,014 children hospitalized with cervical lymphadenitis (Figure 1). Two-thirds of the children in our cohort were <4 years old, 42% were non-Hispanic white, and 63% had a government payor (Table 1). Neck imaging (ultrasound, CT, or MRI) was conducted in 8,103 (81%) children. CT imaging was performed in 4,097 (41%) of children, and early imaging was conducted in 6,111 (61%) of children with cervical lymphadenitis.

We noted hospital-level variation in rates of any neck imaging (median: 82.1%, interquartile range [IQR]: 77.7%-85.5%, full range: 68.7%-93.1%), CT imaging (median: 42.3%, IQR: 26.7%-55.2%, full range: 12.0%-81.5%), early imaging (median: 64.4%, IQR: 59.8%-68.4%, full range: 13.8%-76.9%), and multiple imaging studies (median: 23.7%, IQR: 18.6%-28.9%, full range: 1.2%-40.7%; Figure 2). Rates of surgical drainage also varied by hospital (median: 35.1%, IQR: 31.3%-42.0%, full range: 17.1%-54.5%).

desai04071120e_f2.jpg

desai04071120e_t1.jpg

desai04071120e_t2.jpg

In this large multicenter study of children with cervical lymphadenitis, we found variation in imaging practices across 44 US children’s hospitals. Children with cervical lymphadenitis who underwent early imaging were more likely to receive multiple imaging studies during a single hospitalization than those who did not receive early imaging. At the patient level, early imaging was also associated with higher rates of surgical drainage, more frequent 30-day readmission, and longer lengths of stay.

To our knowledge, imaging practices in the population of children hospitalized with cervical lymphadenitis have not been previously characterized in the US; one study from Atlanta, Georgia, describes imaging practices in all children evaluated in the ED.¹ Single-center studies of children hospitalized with cervical lymphadenitis have been previously conducted in Canada⁶ and New Zealand,⁸ in which 42%-51% of children received imaging. In our study, most (81%) children hospitalized with lymphadenitis received some form of imaging, with 61% of all children receiving early imaging. Furthermore, 41% received CT imaging, as compared with 8%-10% of children in the aforementioned studies from Canada and New Zealand.^6,8 This finding is consistent with a pattern of imaging overuse in the US, which has amongst the highest utilization rates globally for advanced imaging such as CT and MRI.^10,11 Identifying opportunities to safely reduce routine imaging, particularly CT imaging, in this population could decrease unnecessary radiation exposure without compromising outcomes.

We also noted variability in imaging practices across PHIS hospitals. Some of this variability may be partially explained by differences in the patient population or illness severity across hospitals. However, given the absence of evidence-based best practices for children with cervical lymphadenitis, clinicians may rely on anecdotal experience or local practice culture to guide their decision making,¹² leading to variability in frequency, timing, and modality of imaging.

At the patient level, we found that children who received early imaging were more likely to receive multiple imaging studies. This finding supports our hypothesis that clinicians often order a second imaging study when the initial imaging study does not clearly demonstrate an abscess, and the child subsequently fails to demonstrate clear improvement after 24-48 hours of antibiotics.

Furthermore, early imaging was associated with overall increased utilization in our cohort, including increased likelihood of surgical drainage, 30-day readmission for lymphadenitis, as well as longer lengths of stay. Confounding may be one explanation for this finding. For instance, clinicians may pursue early imaging in children who present with longer duration of symptoms or more severe illness on presentation, as these factors may be associated with abscess formation.^1,6,7 These clinical covariates are not available in PHIS. Thus, we used prior ED visits for lymphadenitis to approximate illness duration, and initial admission to ICU, receipt of IV analgesia, and receipt of broad-spectrum antibiotics to approximate illness severity in an attempt to mitigate confounding. However, our proxy measures may not appropriately estimate illness duration and severity. For instance, children who had urgent care or outpatient visits for lymphadenitis would not be captured using the proxy of prior ED visit for lymphadenitis. Similarly, use of broad-spectrum antibiotics and IV analgesia may be influenced by provider or institutional preference rather than illness severity. Thus, residual confounding may exist despite adjusting for these measures.

On the other hand, it is also possible that a proportion of children with a small fluid collection on imaging may have improved with antibiotics alone. There is a growing body of evidence in children with other head and neck infections (eg, retropharyngeal abscess and orbital cellulitis with periosteal abscess)^13-15 that suggests that children with small abscesses often improve with antibiotic therapy alone. In children with cervical lymphadenitis who have small or developing abscesses identified via routine imaging on presentation, clinicians may be driven to pursue a surgical intervention with uncertain benefit. Deferring routine imaging in this population may provide an opportunity to improve the value of care in children with lymphadenitis without adversely affecting outcomes.

Upon closer examination of readmissions, children who received early imaging during index hospitalization were more likely to have a 30-day readmission when only evaluating the subset of patients who did not receive surgical drainage during the index admission. This suggests that readmissions are less likely attributable to surgical complications and more likely a reflection of the natural history of lymphadenitis in which a subset of patients eventually develop an abscess. Further supporting this, 61% of children who had a 30-day readmission for lymphadenitis underwent surgical drainage during readmission. Given that lymphadenitis is a slow-brewing infection in which serious complications are rare, patients who demonstrate gradual clinical improvement do not need to remain hospitalized and serially imaged to identify a possible abscess. Outpatient expectant management and readmission as needed for drainage may be an acceptable approach.

This study has several limitations given our use of an administrative database. Children with lymphadenitis may have been misclassified as these patients were identified using discharge diagnosis codes. To mitigate this potential misclassification, we conducted a structured validation process and found that the included codes had high positive predictive values (Appendix A). This validation process was conducted at a single hospital, and coding may vary across hospitals. To approximate sensitivity, we also sampled children without our included codes but with neck imaging and antibiotic use, and found that rates of cervical lymphadenitis were very low among children without our included diagnosis codes.

Furthermore, we were unable to measure the exact time of imaging study in PHIS; we used imaging conducted on hospital day 0 as a proxy measure for imaging conducted within the first 24 hours of presentation. With this definition, some children who had early imaging were likely misclassified as not having received early imaging. For example, a patient who arrived in the ED at 9 pm on day 0 of admission and had a neck ultrasound performed at 1 am would be classified as having had an imaging study on day 1 of hospitalization even though the imaging study was conducted within 4 hours of presentation. Using an alternative definition of early imaging as imaging conducted on hospital day 0 and day 1, we found a much higher adjusted OR for multiple imaging studies, with similar associations for secondary outcomes. As such, our definition of early imaging as day 0 likely biases the results toward the null; the true increase in likelihood of multiple imaging for those who receive early imaging is probably greater than our conservative estimation.

Additionally, there may be a subset of children who underwent imaging prior to presentation at the PHIS hospital ED for further workup and admission. Imaging conducted outside a PHIS hospital was not captured in this database. Similarly, children who had a readmission at a different hospital than their index admission would not be captured using PHIS. Finally, PHIS captures data from children’s hospitals; practices at these hospitals may not be generalizable to practices in the community hospital setting.

In conclusion, we found that imaging practices in children hospitalized with cervical lymphadenitis were widely variable across hospitals. Children receiving early imaging had more resource utilization and intervention when compared with children who did not receive early imaging. Our findings may represent a cascade effect, in which routinely conducted early imaging prompts clinicians to pursue more testing and interventions in this population. Future studies should obtain more detailed patient level covariates to further characterize clinical factors that may impact decisions around imaging and clinical outcomes for children with cervical lymphadenitis.

Acknowledgments

The authors would like to acknowledge the following investigators for their contributions to data interpretation and review of the final manuscript: Angela Choe MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Margaret Rush MD, Children’s National Medical Center, Washington, DC; Ryosuke Takei MD, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; Wallis Molchen DO, Texas Children’s Hospital, Houston, Texas; Stephanie Royer Moss MD, Cleveland Clinic, Cleveland, Ohio; Rebecca Dang, MD, Lucile Packard Children’s Hospital Stanford, Palo Alto, California; Joy Solano MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas; Nathaniel P. Goodrich MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Ngozi Eboh MD, Texas Tech University Health Sciences Center, Dallas, Texas; Ashley Jenkins MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Rebecca Steuart MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sonya Tang Girdwood MD, PhD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Alissa McInerney MD, Maria Fareri Children’s Hospital at Westchester Medical Center, Valhalla, New York; Sumeet Banker MD, MPH, New York Presbyterian Morgan Stanley Children’s Hospital, New York, New York; Corrie McDaniel DO, Seattle Children’s Hospital, Seattle, Washington; Christiane Lenzen MD, Rady Children’s Hospital, San Diego, California; Aleisha Nabower MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Waheeda Samady MD, Ann & Robert H. Lurie Children’s Hospital, Chicago, Illinois; Jennifer Chen MD, Rady Children’s Hospital, San Diego, California; Marquita Genies MD, MPH, John’s Hopkins Children’s Center, Baltimore, Maryland; Justin Lockwood MD, Children’s Hospital Colorado, Aurora, Colorado; David Synhorst MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas.

Cervical lymphadenitis is a common superficial neck infection in childhood. While most children with cervical lymphadenitis recover with antibiotic therapy, a subset can develop an abscess that may require surgical drainage. Radiologic imaging, most commonly ultrasound or computed tomography (CT), is often performed to identify such an abscess.^1-3 However, no national standards exist to guide clinician decision making around imaging in this population. In the absence of evidence-based guidelines, variability in frequency, timing, and modality of imaging likely exists in children hospitalized with cervical lymphadenitis.

As demonstrated for several other common pediatric conditions,^4,5 variability in imaging practices may contribute to overutilization of resources in children with cervical lymphadenitis. In particular, routinely conducting imaging on presentation may constitute overuse, as children with cervical lymphadenitis who present with less than 72 hours of neck swelling rarely undergo surgical drainage within the first 24 hours of hospitalization.^1,6,7 Imaging performed on presentation is often repeated later during hospitalization, particularly if the patient has not improved with antibiotic therapy. The net result may be unnecessary, redundant radiologic studies. Furthermore, serious complications such as bacteremia, extension of infection into the retropharyngeal space, or involvement of the airway or vasculature rarely occur in children with cervical lymphadenitis.^6,8 In this context, deferring initial imaging in this population is unlikely to lead to adverse outcomes and may reduce radiation exposure.

The overall objectives of this study are to describe hospital-level variation in imaging practices for pediatric cervical lymphadenitis and to examine the association between early imaging and outcomes in this population.

Study Design and Data Source

We conducted a multicenter, cross-sectional study using the Pediatric Health Information Systems (PHIS) database, which contains administrative and billing data from 49 geographically diverse children’s hospitals across the United States (US) affiliated with the Children’s Hospital Association (Lenexa, Kansas). PHIS includes data on patient demographics, discharge diagnoses, and procedures using the International Classification of Diseases, 9th (ICD-9) and 10th Revision (ICD-10) diagnosis codes, as well as daily billed resource utilization for laboratory tests, imaging studies, and medications. Encrypted medical record numbers permit longitudinal identification of children across multiple visits to the same hospital. Use of de-identified PHIS data was deemed to be nonhuman subjects research; our approach to validation of ICD codes using local electronic medical record review was reviewed and approved by the Cincinnati Children’s Hospital Medical Center Institutional Review Board.

Study Population

Our study team developed an algorithm to identify children with cervical lymphadenitis and minimize misclassification using PHIS (Appendix A). All children with lymphadenitis-related ICD-9 and ICD-10 discharge diagnosis codes were eligible for inclusion. Codes were validated at a single center via electronic medical record review; clinician-documented discharge diagnosis of cervical lymphadenitis or the presence of fever and unilateral or asymmetrical neck swelling with overlying skin changes was used as the reference standard. We then excluded children who did not receive antibiotics, children who received radiologic imaging not involving the head or neck (which suggested noncervical lymphadenitis or other illness), and children who had discharge diagnosis codes for other specified conditions that are sometimes associated with enlarged cervical lymph nodes but warrant different evaluation or treatment (eg, Kawasaki disease, retropharyngeal abscess, and dental abscess; Appendix A). Our final algorithm yielded a positive predictive value of 87.5% (95% CI: 79.2%-93.4%) when ICD-9 codes were considered, and 95.1% (95% CI: 88.9%-98.4%) when ICD-10 codes were considered (Appendix A).

This algorithm was subsequently applied to the PHIS database. Children ages two months to 18 years hospitalized at participating PHIS institutions between July 2013 and December 2017 with a diagnosis of cervical lymphadenitis as per the algorithm (Appendix A) were eligible for inclusion. For children with multiple eligible admissions during the study period, we only included the first hospitalization. Children with complex chronic condition diagnosis codes⁹ were excluded as their clinical complexity could influence decisions around timing and modality of diagnostic imaging. In addition, we excluded children who did not have an emergency department (ED) visit associated with their hospitalization. This step was intended to exclude children who were transferred from another institution, as imaging performed at outside institutions prior to transfer is not available in PHIS. To avoid overinflating hospital-level variation in the setting of a small sample size, we also excluded all children admitted to the five hospitals with fewer than 50 cases of cervical lymphadenitis during the study period. Our final cohort consisted of 44 PHIS hospitals.

Measures of Interest

To examine hospital-level variation in imaging practices, we measured the proportion of children at each hospital who underwent any neck imaging study, CT or ultrasound imaging, early imaging, and multiple imaging studies within a single hospitalization. Neck imaging was defined as the presence of a billing code for ultrasound, CT, or magnetic resonance imaging (MRI) study of the neck (Appendix B). Early imaging was defined as neck imaging conducted on day 0 of hospitalization (ie, calendar day of admission and ending at midnight). Multiple imaging studies were defined as the receipt of more than one imaging study, regardless of timing or modality. We also measured the proportion of children by hospital who received surgical drainage, defined by the presence of procedure codes for incision and drainage of abscess of the neck (Appendix B).

In examining patient-level association between early imaging and clinical outcomes, our primary outcome of interest was the receipt of multiple imaging studies. Secondary outcomes included rates of surgical drainage, length of stay (in hospital days), and rates of lymphadenitis-related hospital readmission within 30 days of index discharge.

Covariates

Baseline demographic characteristics included age, gender, race/ethnicity, and insurance type. We measured ED visits associated with lymphadenitis-related diagnosis codes in the 30 days prior to admission as a proxy measure for illness duration prior to presentation. To approximate illness severity, we included the following covariates: rates of intensive care unit admission on presentation, rates of receipt of intravenous (IV) analgesia (Appendix B) on hospital days prior to surgical drainage, and rates of receipt of broad-spectrum antibiotics on day 0 or 1 of hospitalization. Broad-spectrum antibiotics (Appendix B) were defined by an independent three-person review of available antibiotic codes (SD, SSS, and JT); differences were resolved by group consensus.

Analysis

Categorical variables were described using frequencies and percentages, while continuous data were described using median and interquartile range. We described hospital-level variation in imaging practices by calculating and comparing the proportion of children at each hospital who underwent any neck imaging study, CT imaging, ultrasound imaging, early imaging, multiple imaging studies, and surgical drainage.

Patient-level demographics and clinical characteristics were compared across groups using chi-square test. To examine the association between early imaging and outcomes, we used generalized linear or logistic mixed effects models to control for patient demographic characteristics and clinical markers of illness duration and severity, with a random effect for hospital to account for clustering. Patient demographics in the model defined a priori included age, race/ethnicity, and insurance type; clinical characteristics included prior ED visit for lymphadenitis, initial intensive care unit (ICU) admission, use of IV analgesia, and use of broad-spectrum antibiotics on day 0 or 1 of hospitalization. To assess the potential for misclassification related to the availability of calendar day but not time of imaging in PHIS, we conducted a secondary analysis to examine the patient-level association between early imaging and outcomes using an alternative definition for early imaging (defined as imaging conducted on day 0 or day 1 of hospitalization).

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We identified 19,785 PHIS hospitalizations with lymphadenitis-related discharge diagnosis codes between July 1, 2013 and December 31, 2017. Applying our algorithm and exclusion criteria, we assembled a cohort of 10,014 children hospitalized with cervical lymphadenitis (Figure 1). Two-thirds of the children in our cohort were <4 years old, 42% were non-Hispanic white, and 63% had a government payor (Table 1). Neck imaging (ultrasound, CT, or MRI) was conducted in 8,103 (81%) children. CT imaging was performed in 4,097 (41%) of children, and early imaging was conducted in 6,111 (61%) of children with cervical lymphadenitis.

We noted hospital-level variation in rates of any neck imaging (median: 82.1%, interquartile range [IQR]: 77.7%-85.5%, full range: 68.7%-93.1%), CT imaging (median: 42.3%, IQR: 26.7%-55.2%, full range: 12.0%-81.5%), early imaging (median: 64.4%, IQR: 59.8%-68.4%, full range: 13.8%-76.9%), and multiple imaging studies (median: 23.7%, IQR: 18.6%-28.9%, full range: 1.2%-40.7%; Figure 2). Rates of surgical drainage also varied by hospital (median: 35.1%, IQR: 31.3%-42.0%, full range: 17.1%-54.5%).

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In this large multicenter study of children with cervical lymphadenitis, we found variation in imaging practices across 44 US children’s hospitals. Children with cervical lymphadenitis who underwent early imaging were more likely to receive multiple imaging studies during a single hospitalization than those who did not receive early imaging. At the patient level, early imaging was also associated with higher rates of surgical drainage, more frequent 30-day readmission, and longer lengths of stay.

To our knowledge, imaging practices in the population of children hospitalized with cervical lymphadenitis have not been previously characterized in the US; one study from Atlanta, Georgia, describes imaging practices in all children evaluated in the ED.¹ Single-center studies of children hospitalized with cervical lymphadenitis have been previously conducted in Canada⁶ and New Zealand,⁸ in which 42%-51% of children received imaging. In our study, most (81%) children hospitalized with lymphadenitis received some form of imaging, with 61% of all children receiving early imaging. Furthermore, 41% received CT imaging, as compared with 8%-10% of children in the aforementioned studies from Canada and New Zealand.^6,8 This finding is consistent with a pattern of imaging overuse in the US, which has amongst the highest utilization rates globally for advanced imaging such as CT and MRI.^10,11 Identifying opportunities to safely reduce routine imaging, particularly CT imaging, in this population could decrease unnecessary radiation exposure without compromising outcomes.

We also noted variability in imaging practices across PHIS hospitals. Some of this variability may be partially explained by differences in the patient population or illness severity across hospitals. However, given the absence of evidence-based best practices for children with cervical lymphadenitis, clinicians may rely on anecdotal experience or local practice culture to guide their decision making,¹² leading to variability in frequency, timing, and modality of imaging.

At the patient level, we found that children who received early imaging were more likely to receive multiple imaging studies. This finding supports our hypothesis that clinicians often order a second imaging study when the initial imaging study does not clearly demonstrate an abscess, and the child subsequently fails to demonstrate clear improvement after 24-48 hours of antibiotics.

Furthermore, early imaging was associated with overall increased utilization in our cohort, including increased likelihood of surgical drainage, 30-day readmission for lymphadenitis, as well as longer lengths of stay. Confounding may be one explanation for this finding. For instance, clinicians may pursue early imaging in children who present with longer duration of symptoms or more severe illness on presentation, as these factors may be associated with abscess formation.^1,6,7 These clinical covariates are not available in PHIS. Thus, we used prior ED visits for lymphadenitis to approximate illness duration, and initial admission to ICU, receipt of IV analgesia, and receipt of broad-spectrum antibiotics to approximate illness severity in an attempt to mitigate confounding. However, our proxy measures may not appropriately estimate illness duration and severity. For instance, children who had urgent care or outpatient visits for lymphadenitis would not be captured using the proxy of prior ED visit for lymphadenitis. Similarly, use of broad-spectrum antibiotics and IV analgesia may be influenced by provider or institutional preference rather than illness severity. Thus, residual confounding may exist despite adjusting for these measures.

On the other hand, it is also possible that a proportion of children with a small fluid collection on imaging may have improved with antibiotics alone. There is a growing body of evidence in children with other head and neck infections (eg, retropharyngeal abscess and orbital cellulitis with periosteal abscess)^13-15 that suggests that children with small abscesses often improve with antibiotic therapy alone. In children with cervical lymphadenitis who have small or developing abscesses identified via routine imaging on presentation, clinicians may be driven to pursue a surgical intervention with uncertain benefit. Deferring routine imaging in this population may provide an opportunity to improve the value of care in children with lymphadenitis without adversely affecting outcomes.

Upon closer examination of readmissions, children who received early imaging during index hospitalization were more likely to have a 30-day readmission when only evaluating the subset of patients who did not receive surgical drainage during the index admission. This suggests that readmissions are less likely attributable to surgical complications and more likely a reflection of the natural history of lymphadenitis in which a subset of patients eventually develop an abscess. Further supporting this, 61% of children who had a 30-day readmission for lymphadenitis underwent surgical drainage during readmission. Given that lymphadenitis is a slow-brewing infection in which serious complications are rare, patients who demonstrate gradual clinical improvement do not need to remain hospitalized and serially imaged to identify a possible abscess. Outpatient expectant management and readmission as needed for drainage may be an acceptable approach.

This study has several limitations given our use of an administrative database. Children with lymphadenitis may have been misclassified as these patients were identified using discharge diagnosis codes. To mitigate this potential misclassification, we conducted a structured validation process and found that the included codes had high positive predictive values (Appendix A). This validation process was conducted at a single hospital, and coding may vary across hospitals. To approximate sensitivity, we also sampled children without our included codes but with neck imaging and antibiotic use, and found that rates of cervical lymphadenitis were very low among children without our included diagnosis codes.

Furthermore, we were unable to measure the exact time of imaging study in PHIS; we used imaging conducted on hospital day 0 as a proxy measure for imaging conducted within the first 24 hours of presentation. With this definition, some children who had early imaging were likely misclassified as not having received early imaging. For example, a patient who arrived in the ED at 9 pm on day 0 of admission and had a neck ultrasound performed at 1 am would be classified as having had an imaging study on day 1 of hospitalization even though the imaging study was conducted within 4 hours of presentation. Using an alternative definition of early imaging as imaging conducted on hospital day 0 and day 1, we found a much higher adjusted OR for multiple imaging studies, with similar associations for secondary outcomes. As such, our definition of early imaging as day 0 likely biases the results toward the null; the true increase in likelihood of multiple imaging for those who receive early imaging is probably greater than our conservative estimation.

Additionally, there may be a subset of children who underwent imaging prior to presentation at the PHIS hospital ED for further workup and admission. Imaging conducted outside a PHIS hospital was not captured in this database. Similarly, children who had a readmission at a different hospital than their index admission would not be captured using PHIS. Finally, PHIS captures data from children’s hospitals; practices at these hospitals may not be generalizable to practices in the community hospital setting.

In conclusion, we found that imaging practices in children hospitalized with cervical lymphadenitis were widely variable across hospitals. Children receiving early imaging had more resource utilization and intervention when compared with children who did not receive early imaging. Our findings may represent a cascade effect, in which routinely conducted early imaging prompts clinicians to pursue more testing and interventions in this population. Future studies should obtain more detailed patient level covariates to further characterize clinical factors that may impact decisions around imaging and clinical outcomes for children with cervical lymphadenitis.

Acknowledgments

The authors would like to acknowledge the following investigators for their contributions to data interpretation and review of the final manuscript: Angela Choe MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Margaret Rush MD, Children’s National Medical Center, Washington, DC; Ryosuke Takei MD, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; Wallis Molchen DO, Texas Children’s Hospital, Houston, Texas; Stephanie Royer Moss MD, Cleveland Clinic, Cleveland, Ohio; Rebecca Dang, MD, Lucile Packard Children’s Hospital Stanford, Palo Alto, California; Joy Solano MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas; Nathaniel P. Goodrich MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Ngozi Eboh MD, Texas Tech University Health Sciences Center, Dallas, Texas; Ashley Jenkins MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Rebecca Steuart MD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Sonya Tang Girdwood MD, PhD, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; Alissa McInerney MD, Maria Fareri Children’s Hospital at Westchester Medical Center, Valhalla, New York; Sumeet Banker MD, MPH, New York Presbyterian Morgan Stanley Children’s Hospital, New York, New York; Corrie McDaniel DO, Seattle Children’s Hospital, Seattle, Washington; Christiane Lenzen MD, Rady Children’s Hospital, San Diego, California; Aleisha Nabower MD, Children’s Hospital & Medical Center, Omaha, Nebraska; Waheeda Samady MD, Ann & Robert H. Lurie Children’s Hospital, Chicago, Illinois; Jennifer Chen MD, Rady Children’s Hospital, San Diego, California; Marquita Genies MD, MPH, John’s Hopkins Children’s Center, Baltimore, Maryland; Justin Lockwood MD, Children’s Hospital Colorado, Aurora, Colorado; David Synhorst MD, Children’s Mercy Hospital Kansas, Overland Park, Kansas.

Neurologic impairment (NI) encompasses static and progressive diseases of the central and/or peripheral nervous systems that result in functional and intellectual impairments.¹ While a variety of neurologic diseases are responsible for NI (eg, hypoxic-ischemic encephalopathy, muscular dystrophy), consequences of these diseases extend beyond neurologic manifestations.¹ These children are at an increased risk for aspiration of oral and gastric contents given their common comorbidities of dysphagia, gastroesophageal reflux, impaired cough, and respiratory muscle weakness.² While aspiration may manifest as a self-resolving pneumonitis, the presence of oral or enteric bacteria in aspirated material may result in the development of bacterial pneumonia. Children with NI hospitalized with aspiration pneumonia have higher complication rates, longer and costlier hospitalizations, and higher readmission rates when compared with children with nonaspiration pneumonia.³

While pediatric aspiration pneumonia is commonly attributed to anaerobic bacteria, this is largely based on extrapolation from epidemiologic studies that were conducted in past decades.^4-8 A single randomized controlled trial found that penicillin and clindamycin, antimicrobials with similar antimicrobial activity against anaerobes, to be equally effective.⁹ However, the recent literature emphasizes the polymicrobial nature of aspiration pneumonia in adults, with the common isolation of Gram-negative enteric bacteria.¹⁰ Further, while Pseudomonas aeruginosa is often identified in respiratory cultures from children with NI and chronic respiratory insufficiency,^11,12 the significance of P. aeruginosa in lower airways remains unclear.

We designed this study to compare hospital outcomes associated with the most commonly prescribed empiric antimicrobial therapies for aspiration pneumonia in children with NI.

Study Design and Data Source

This multicenter, retrospective cohort study used the Pediatric Health Information System (PHIS) database. PHIS, an administrative database of 50 not-for-profit tertiary care pediatric hospitals, contains data regarding patient demographics, diagnoses and procedures, and daily billed resource utilization, including laboratory and imaging studies. Data quality and reliability are assured through the Children’s Hospital Association (CHA; Lenexa, Kansas) and participating hospitals. Due to incomplete data through the study period and data quality issues, six hospitals were excluded.

Inclusion Criteria

Children 1-18 years of age who were discharged between July 1, 2007 and June 30, 2015 were included if they had a NI diagnosis,¹ a principal diagnosis indicative of aspiration pneumonia (507.x),^3,13,14 and received antibiotics in the first two calendar days of admission. NI was determined using previously defined International Classification of Diseases, Ninth Revision-Clinical Modification (ICD-9-CM) diagnosis codes.¹ We only included children who received antibiotics in the first two calendar days of admission to minimize the likelihood of including children admitted for other reasons who acquired aspiration pneumonia after hospitalization. For children with multiple hospitalizations, one admission was randomly selected for inclusion to minimize weighting results toward repeat visits.

Exclusion Criteria

Children transferred from another hospital were excluded as records from their initial presentation, including treatment and outcomes, were not available. We also excluded children with tracheostomy^15,16 or chronic ventilator dependence,¹⁷ those with a diagnosis of human immunodeficiency virus or tuberculosis, and children who received chemotherapy during hospitalization given expected differences in etiology, treatment, and outcomes.¹⁸

Exposure

The primary exposure was antibiotic therapy received in the first two days of admission. Antibiotics were classified by their antimicrobial spectra of activity as defined by The Sanford Guide to Antimicrobial Therapy¹⁹ against the most commonly recognized pathogens of aspiration pneumonia: anaerobes, Gram-negatives, and P. aeruginosa (Appendix Table 1).^10,20 For example, penicillin G and clindamycin were among the antibiotics classified as providing anaerobic coverage alone, whereas ceftriaxone was classified as providing Gram-negative coverage alone and ampicillin-sulbactam or as combination therapy with clindamycin and ceftriaxone were classified as providing anaerobic and Gram-negative coverage. Piperacillin-tazobactam and meropenem were classified as providing anaerobic, Gram-negative, and P. aeruginosa coverage. We excluded antibiotics that do not provide coverage against anaerobes, Gram-negative, or P. aeruginosa (eg, ampicillin, azithromycin) or that provide coverage against Gram-negative and P. aeruginosa, but not anaerobes (eg, cefepime, tobramycin), as these therapies were prescribed for <5% of the cohort. We chose not to examine the coverage for Streptococcus pneumonia or Staphylococcus aureus as antibiotics included in this analysis covered these bacteria for 99.9% of our cohort.

Outcomes included acute respiratory failure during hospitalization, intensive care unit (ICU) transfer, and hospital length of stay (LOS). Acute respiratory failure during hospitalization was defined as the presence of Clinical Transaction Classification (CTC) or ICD-9 procedure code for noninvasive or invasive mechanical ventilation on day two or later of hospitalization, with or without the need for respiratory support on day 0 or day 1 (Appendix Table 2). Given the variability in hospital policies that may drive ICU admission criteria for complex patients, our outcome of ICU transfer was defined as the requirement for ICU level care on day two or later of hospitalization without ICU admission. Acute respiratory failure and ICU care occurring within the first two hospital days were not classified as outcomes because these early events likely reflect illness severity at presentation rather than outcomes attributable to treatment failure; these were included as markers of severity in the models.

Patient Demographics and Clinical Characteristics

Demographic and clinical characteristics that might influence antibiotic choice and/or hospital outcomes were assessed. Clinical characteristics included complex chronic conditions,^21-23 medical technology assistance,²⁴ performance of diagnostic testing, and markers of severe illness on presentation. Diagnostic testing included bacterial cultures (blood, respiratory, urine) and chest radiograph performance in the first two days of hospitalization. Results of diagnostic testing are not available in the PHIS. Illness severity on presentation included acute respiratory failure, pleural drainage, receipt of vasoactive agents, and transfusion of blood products in the first two days of hospitalization (Appendix Table 2).^17,25,26

Continuous data were described with median and interquartile ranges (IQR) due to nonnormal distribution. Categorical data were described with frequencies and percentages. Patient demographics, clinical characteristics, and hospital outcomes were stratified by empiric antimicrobial coverage and compared using chi-square and Kruskal–Wallis tests as appropriate.

Generalized linear mixed-effects models with random hospital intercepts were derived to assess the independent effect of antimicrobial spectra of activity on outcomes of acute respiratory failure, ICU transfer, and LOS while adjusting for important differences in demographic and clinical characteristics. LOS had a nonnormal distribution. Thus, we used an exponential distribution. Covariates were chosen a priori given the clinical and biological relevance to exposure and outcomes—age, presence of complex chronic condition diagnoses, the number of complex chronic conditions, technology dependence, the performance of diagnostic tests on presentation, and illness severity on presentation. ICU admission was included as a covariate in acute respiratory failure and LOS outcome models. The results of the model for acute respiratory failure and ICU transfer are presented as adjusted odds ratios (OR) with a 95% CI. LOS results are presented as adjusted rate ratios (RR) with 95% CI.

All analyses were performed with SAS 9.3 (SAS Institute, Cary, North Carolina). P values <.05 were considered statistically significant. Cincinnati Children’s Hospital Medical Center Institutional Review Board considered this deidentified dataset study as not human subjects research.

Study Cohort

At the 44 hospitals included, 4,812 children with NI hospitalized with the diagnosis of aspiration pneumonia met the eligibility criteria. However, 79 received antibiotics with the spectra of activity not examined, leaving 4,733 children in our final analysis (Appendix Figure). Demographic and clinical characteristics of the study cohort are shown in Table 1. Median age was five years (interquartile range [IQR]: 2-11 years). Most subjects were male (53.9%), non-Hispanic white (47.9%), and publicly insured (63.6%). There was a slight variation in the distribution of admissions across seasons (spring 31.6%, summer 19.2%, fall 21.3%, and winter 27.9%). One-third of children had four or more comorbid CCCs (complex chronic conditions; 34.2%). The three most common nonneurologic CCC diagnosis categories were gastrointestinal (63.1%), congenital and/or genetic defects (36.9%), and respiratory (8.9%). Assistance with medical technologies was also common (82%)—particularly gastrointestinal (63.1%) and neurologic/neuromuscular (9.8%) technologies. The vast majority of children (92.5%) had either a chest radiograph (90.5%), respiratory viral study (33.7%), or respiratory culture (10.0%) obtained on presentation. A minority required noninvasive or invasive respiratory support (25.4%), vasoactive agents (8.9%), blood products (1.2%), or pleural drainage (0.3%) in the first two hospital days.

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Spectrum of Antimicrobial Coverage

Most children (57.9%) received anaerobic and Gram-negative coverage; 16.2% received anaerobic, Gram-negative and P. aeruginosa coverage; 15.3% received anaerobic coverage alone; and 10.6% received Gram-negative coverage alone. Empiric antimicrobial coverage varied substantially across hospitals: anaerobic coverage was prescribed for 0%-44% of patients; Gram-negative coverage was prescribed for 3%-26% of patients; anaerobic and Gram-negative coverage was prescribed for 25%-90% of patients; and anaerobic, Gram-negative, and P. aeruginosa coverage was prescribed for 0%-65% of patients (Figure 1).

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Outcomes

Acute Respiratory Failure

One-quarter (25.4%) of patients had acute respiratory failure on presentation; 22.5% required respiratory support (continued from presentation or were new) on day two or later of hospitalization (Table 2). In the adjusted analysis, children receiving Gram-negative coverage alone had two-fold greater odds (OR 2.15, 95% CI: 1.41-3.27) and children receiving anaerobic and Gram-negative coverage had 1.6-fold greater odds (OR 1.65, 95% CI: 1.19-2.28), of respiratory failure during hospitalization compared with those receiving anaerobic coverage alone (Figure 2). Odds of respiratory failure during hospitalization did not significantly differ for children receiving anaerobic, Gram-negative, and P. aeruginosa coverage compared with those receiving anaerobic coverage alone.

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ICU Transfer

Nearly thirty percent (29.0%) of children required ICU admission, with an additional 3.8% requiring ICU transfer following admission (Table 2). In the multivariable analysis, the odds of an ICU transfer were greater for children receiving Gram-negative coverage alone (OR 1.80, 95% CI: 1.03-3.14) compared with those receiving anaerobic coverage alone. There was no statistical difference in ICU transfer for those receiving anaerobic and Gram-negative coverage (with or without P. aeruginosa coverage) compared with those receiving anaerobic coverage alone (Figure 2).

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Length of Stay

Median hospital LOS for the total cohort was five days (IQR: 3-9 days; Table 2). In the multivariable analysis, children receiving Gram-negative coverage alone had a longer LOS (RR 1.28; 95% CI: 1.16-1.41) compared with those receiving anaerobic coverage alone, whereas children receiving anaerobic, Gram-negative, and P. aeruginosa coverage had a shorter LOS (RR 0.83; 95% CI: 0.76-0.90) than those receiving anaerobic coverage alone (Figure 2). There was no statistical difference in the LOS between children receiving anaerobic and Gram-negative coverage and those receiving anaerobic coverage alone.

In this multicenter study of children with NI hospitalized with aspiration pneumonia, we found substantial variation in empiric antimicrobial coverage for children with aspiration pneumonia. When comparing outcomes across groups, children who received anaerobic and Gram-negative coverage had outcomes similar to children who received anaerobic therapy alone. However, children who did not receive anaerobic coverage (ie, Gram-negative coverage alone) had worse outcomes, most notably a greater than two-fold increase in the odds of experiencing acute respiratory failure during hospitalization when compared with children receiving anaerobic therapy. These findings support prior literature that has highlighted the importance of anaerobic therapy in the treatment of aspiration pneumonia. The benefit of antibiotics targeting Gram-negative organisms, in addition to anaerobes, remains uncertain.

The variability in empiric antimicrobial coverage likely reflects the paucity of available information on oral and/or enteric bacteria required to identify them as causative organisms in aspiration pneumonia. In part, this problem is due to the difficulty in obtaining adequate sputum for culture from pediatric patients.²⁷ While it may be more feasible to obtain tracheal aspirates for respiratory culture in children with a tracheostomy, interpretation of culture results remains challenging because the lower airways of children with tracheostomy are commonly colonized with bacterial pathogens.²⁸ Thus, physicians are often left to choose empiric antimicrobial coverage with inadequate supporting evidence.²⁹ Although the polymicrobial nature of aspiration pneumonia is well recognized in adult and pediatric literature,^10,30 it is less clear which organisms are of pathological significance and require treatment.

The treatment standard for aspiration pneumonia has long included anaerobic therapy.²⁹ The worse outcomes of children not receiving anaerobic therapy (ie, Gram-negative coverage alone) compared with children who received anaerobic therapy support the continued importance of anaerobic therapy in the treatment of aspiration pneumonia for hospitalized children with NI. The role of antibiotics covering Gram-negative organisms is less clear. Recent studies suggest the role of anaerobes is overemphasized in the etiology and treatment of aspiration pneumonia.^10,29,31-38 Multiple studies on aspiration pneumonia bacteriology in hospitalized adults have demonstrated a predominance of Gram-negative organisms (ranging from 37%-71% of isolates identified on respiratory culture) and a relative scarcity of anaerobes (ranging from 0%-16% of isolates).^31-37 A prospective study of 50 children hospitalized with clinical and radiographic evidence of pneumonia with known aspiration risk (eg, neuromuscular disease or dysphagia) found that ~80% of 163 bacterial isolates were Gram-negative.³⁸ However, this study included repeat cultures from the same children, and thus, may overestimate the prevalence of Gram-negative organisms. In our study, children who received both anaerobic and Gram-negative therapy had no differences in ICU transfer or LOS but did experience higher odds of acute respiratory failure. As these results may be due to unmeasured confounding, future studies should further explore the necessity of Gram-negative coverage in addition to anaerobic coverage in this population.

While these recent studies may seem to suggest that anaerobic coverage is not necessary for aspiration pneumonia, there are important limitations worth noting. First, these studies used a variety of sampling techniques. While organisms grown from samples obtained via bronchoalveolar lavage^31-34,36 are likely pathogenic, those grown from tracheal or oral samples obtained via percutaneous transtracheal aspiration,³⁴ a protected specimen brush,^34,36,37 or expectorated sputum^35,38 may not represent lower airway organisms. Second, anaerobic cultures were not obtained in all studies.^31,34,38 Anaerobic organisms are difficult to isolate using traditional clinical specimen collection techniques and aerobic culture media.¹⁸ Furthermore, anaerobes are not easily recovered from lung infections after the receipt of antibiotic therapy.³⁹ Details regarding pretreatment, which are largely lacking from these studies, are necessary to interpret the relative scarcity of anaerobes on respiratory culture. Finally, caution should be taken when extrapolating the results of studies focused on the etiology and treatment of aspiration pneumonia in elderly adults to children. Our results, particularly in the context of the limitation of these more recent studies, suggest that the role of anaerobes has been underestimated.

Recent studies examining populations of children with cerebral palsy and/or tracheostomy have emphasized the high rates of carriage and infection rates with Gram-negative and drug-resistant bacteria; in particular, P. aeruginosa accounts for 50%-72% of pathogenic bacteria.^11,12,38,40These studies note the generally poor outcomes of children with P. aeruginosa—including multiple and longer hospitalizations, frequent readmissions, and the increased severity of pneumonia, including the need for ICU admission, pleural effusions, the need for intubation, and mortality.^{11,12,38,40,41} In our study, nearly 35% of children who received anaerobic, Gram-negative, and P. aeruginosa coverage experienced acute respiratory failure during hospitalization compared with 20% of children who received other therapies. While these results might seem to suggest that broader spectrum therapy is harmful, they must be interpreted in the context of important population differences; children who received a combination of anaerobic, Gram-negative, and P. aeruginosa coverage had greater medical complexity and greater severity of illness on presentation. Such factors may provide the reason for the appropriate prescription of antipseudomonal antibiotics (eg, history of tracheostomy colonization or infection, long-term care facility resident).⁴² When we controlled for population differences, children who received antipseudomonal therapy had a significantly shorter LOS and no differences in outcomes of acute respiratory failure or ICU transfer compared with those receiving anaerobic therapy alone. This result suggests that worse outcomes were associated with antipseudomonal therapy on unadjusted analyses resulting from underlying medical complexity and illness severity rather than from colonization or infection with P. aeruginosa.

Our multicenter observational study has several limitations. We used diagnosis codes to identify patients with aspiration pneumonia. As validated clinical criteria for the diagnosis of aspiration pneumonia do not exist, clinicians may assign a diagnosis of and treatment for aspiration pneumonia by subjective suspicion based on a child’s severe NI or illness severity on presentation leading to selection bias. Although administrative data are not able to verify pneumonia type with absolute certainty, we previously demonstrated that the differences in the outcomes of children with aspiration and nonaspiration pneumonia diagnosis codes persist after accounting for the complexity that might influence the diagnosis.³It is also possible that the diagnosis of aspiration pneumonia was not made upon admission for a subset of patients leading to misclassification of exposure. Some children may have had aspiration pneumonia on admission but were not assigned that diagnosis or treated for presumed aspiration pneumonia until later in the hospital course as they demonstrated treatment failure or clinical worsening. It is also possible that some children had an aspiration event during hospitalization that developed into aspiration pneumonia. We attempted to adjust for medical complexity and illness severity through multivariable adjustment based on the diagnosis and procedure codes, as well as the laboratory testing performed. However, unmeasured or residual confounding may remain as administrative data are not equipped to distinguish detailed functional status (eg, ability to cough, chest wall strength) or illness severity (eg, respiratory distress) that might influence antibiotic selection and/or outcomes.

Frthermore, we were unable to account for laboratory, microbiology, or radiology test results, and other management practices (eg, frequency of airway clearance, previous antimicrobial therapy) that may influence outcomes. Future studies should certainly include an examination of the concordance of the antibiotics prescribed with causative organisms, as this undoubtedly affects patient outcomes. Other outcomes are important to examine (eg, time to return to respiratory baseline), but we were unable to do so, given the lack of clinical detail in our database. We randomly selected a single hospitalization for children with multiple admissions; alternative methods could have different results. Although children with NI predominately use children’s hospitals,¹ results may not be generalizable.

These findings support prior literature that has highlighted the important role anaerobic therapy plays in the treatment of aspiration pneumonia in children with NI. In light of the limitations of our study design, we believe that rigorous clinical trials comparing anaerobic with anaerobic and Gram-negative therapy are an important and necessary next step to determine the optimal treatment for aspiration pneumonia in this population.

Disclosures

The authors do not have any financial relationships relevant to this article to disclose.

Funding

Dr. Thomson was supported by the Agency for Healthcare Research and Quality (AHRQ) under award number K08HS025138. Dr. Ambroggio was supported by the National Institute for Allergy and Infectious Diseases (NIAID) under award number K01AI125413. The content is solely the responsibility of the authors and does not necessarily represent the official views of the AHRQ or NIAID.

Neurologic impairment (NI) encompasses static and progressive diseases of the central and/or peripheral nervous systems that result in functional and intellectual impairments.¹ While a variety of neurologic diseases are responsible for NI (eg, hypoxic-ischemic encephalopathy, muscular dystrophy), consequences of these diseases extend beyond neurologic manifestations.¹ These children are at an increased risk for aspiration of oral and gastric contents given their common comorbidities of dysphagia, gastroesophageal reflux, impaired cough, and respiratory muscle weakness.² While aspiration may manifest as a self-resolving pneumonitis, the presence of oral or enteric bacteria in aspirated material may result in the development of bacterial pneumonia. Children with NI hospitalized with aspiration pneumonia have higher complication rates, longer and costlier hospitalizations, and higher readmission rates when compared with children with nonaspiration pneumonia.³

While pediatric aspiration pneumonia is commonly attributed to anaerobic bacteria, this is largely based on extrapolation from epidemiologic studies that were conducted in past decades.^4-8 A single randomized controlled trial found that penicillin and clindamycin, antimicrobials with similar antimicrobial activity against anaerobes, to be equally effective.⁹ However, the recent literature emphasizes the polymicrobial nature of aspiration pneumonia in adults, with the common isolation of Gram-negative enteric bacteria.¹⁰ Further, while Pseudomonas aeruginosa is often identified in respiratory cultures from children with NI and chronic respiratory insufficiency,^11,12 the significance of P. aeruginosa in lower airways remains unclear.

We designed this study to compare hospital outcomes associated with the most commonly prescribed empiric antimicrobial therapies for aspiration pneumonia in children with NI.

Study Design and Data Source

This multicenter, retrospective cohort study used the Pediatric Health Information System (PHIS) database. PHIS, an administrative database of 50 not-for-profit tertiary care pediatric hospitals, contains data regarding patient demographics, diagnoses and procedures, and daily billed resource utilization, including laboratory and imaging studies. Data quality and reliability are assured through the Children’s Hospital Association (CHA; Lenexa, Kansas) and participating hospitals. Due to incomplete data through the study period and data quality issues, six hospitals were excluded.

Inclusion Criteria

Children 1-18 years of age who were discharged between July 1, 2007 and June 30, 2015 were included if they had a NI diagnosis,¹ a principal diagnosis indicative of aspiration pneumonia (507.x),^3,13,14 and received antibiotics in the first two calendar days of admission. NI was determined using previously defined International Classification of Diseases, Ninth Revision-Clinical Modification (ICD-9-CM) diagnosis codes.¹ We only included children who received antibiotics in the first two calendar days of admission to minimize the likelihood of including children admitted for other reasons who acquired aspiration pneumonia after hospitalization. For children with multiple hospitalizations, one admission was randomly selected for inclusion to minimize weighting results toward repeat visits.

Exclusion Criteria

Children transferred from another hospital were excluded as records from their initial presentation, including treatment and outcomes, were not available. We also excluded children with tracheostomy^15,16 or chronic ventilator dependence,¹⁷ those with a diagnosis of human immunodeficiency virus or tuberculosis, and children who received chemotherapy during hospitalization given expected differences in etiology, treatment, and outcomes.¹⁸

Exposure

The primary exposure was antibiotic therapy received in the first two days of admission. Antibiotics were classified by their antimicrobial spectra of activity as defined by The Sanford Guide to Antimicrobial Therapy¹⁹ against the most commonly recognized pathogens of aspiration pneumonia: anaerobes, Gram-negatives, and P. aeruginosa (Appendix Table 1).^10,20 For example, penicillin G and clindamycin were among the antibiotics classified as providing anaerobic coverage alone, whereas ceftriaxone was classified as providing Gram-negative coverage alone and ampicillin-sulbactam or as combination therapy with clindamycin and ceftriaxone were classified as providing anaerobic and Gram-negative coverage. Piperacillin-tazobactam and meropenem were classified as providing anaerobic, Gram-negative, and P. aeruginosa coverage. We excluded antibiotics that do not provide coverage against anaerobes, Gram-negative, or P. aeruginosa (eg, ampicillin, azithromycin) or that provide coverage against Gram-negative and P. aeruginosa, but not anaerobes (eg, cefepime, tobramycin), as these therapies were prescribed for <5% of the cohort. We chose not to examine the coverage for Streptococcus pneumonia or Staphylococcus aureus as antibiotics included in this analysis covered these bacteria for 99.9% of our cohort.

Outcomes included acute respiratory failure during hospitalization, intensive care unit (ICU) transfer, and hospital length of stay (LOS). Acute respiratory failure during hospitalization was defined as the presence of Clinical Transaction Classification (CTC) or ICD-9 procedure code for noninvasive or invasive mechanical ventilation on day two or later of hospitalization, with or without the need for respiratory support on day 0 or day 1 (Appendix Table 2). Given the variability in hospital policies that may drive ICU admission criteria for complex patients, our outcome of ICU transfer was defined as the requirement for ICU level care on day two or later of hospitalization without ICU admission. Acute respiratory failure and ICU care occurring within the first two hospital days were not classified as outcomes because these early events likely reflect illness severity at presentation rather than outcomes attributable to treatment failure; these were included as markers of severity in the models.

Patient Demographics and Clinical Characteristics

Demographic and clinical characteristics that might influence antibiotic choice and/or hospital outcomes were assessed. Clinical characteristics included complex chronic conditions,^21-23 medical technology assistance,²⁴ performance of diagnostic testing, and markers of severe illness on presentation. Diagnostic testing included bacterial cultures (blood, respiratory, urine) and chest radiograph performance in the first two days of hospitalization. Results of diagnostic testing are not available in the PHIS. Illness severity on presentation included acute respiratory failure, pleural drainage, receipt of vasoactive agents, and transfusion of blood products in the first two days of hospitalization (Appendix Table 2).^17,25,26

Continuous data were described with median and interquartile ranges (IQR) due to nonnormal distribution. Categorical data were described with frequencies and percentages. Patient demographics, clinical characteristics, and hospital outcomes were stratified by empiric antimicrobial coverage and compared using chi-square and Kruskal–Wallis tests as appropriate.

Generalized linear mixed-effects models with random hospital intercepts were derived to assess the independent effect of antimicrobial spectra of activity on outcomes of acute respiratory failure, ICU transfer, and LOS while adjusting for important differences in demographic and clinical characteristics. LOS had a nonnormal distribution. Thus, we used an exponential distribution. Covariates were chosen a priori given the clinical and biological relevance to exposure and outcomes—age, presence of complex chronic condition diagnoses, the number of complex chronic conditions, technology dependence, the performance of diagnostic tests on presentation, and illness severity on presentation. ICU admission was included as a covariate in acute respiratory failure and LOS outcome models. The results of the model for acute respiratory failure and ICU transfer are presented as adjusted odds ratios (OR) with a 95% CI. LOS results are presented as adjusted rate ratios (RR) with 95% CI.

All analyses were performed with SAS 9.3 (SAS Institute, Cary, North Carolina). P values <.05 were considered statistically significant. Cincinnati Children’s Hospital Medical Center Institutional Review Board considered this deidentified dataset study as not human subjects research.

Study Cohort

At the 44 hospitals included, 4,812 children with NI hospitalized with the diagnosis of aspiration pneumonia met the eligibility criteria. However, 79 received antibiotics with the spectra of activity not examined, leaving 4,733 children in our final analysis (Appendix Figure). Demographic and clinical characteristics of the study cohort are shown in Table 1. Median age was five years (interquartile range [IQR]: 2-11 years). Most subjects were male (53.9%), non-Hispanic white (47.9%), and publicly insured (63.6%). There was a slight variation in the distribution of admissions across seasons (spring 31.6%, summer 19.2%, fall 21.3%, and winter 27.9%). One-third of children had four or more comorbid CCCs (complex chronic conditions; 34.2%). The three most common nonneurologic CCC diagnosis categories were gastrointestinal (63.1%), congenital and/or genetic defects (36.9%), and respiratory (8.9%). Assistance with medical technologies was also common (82%)—particularly gastrointestinal (63.1%) and neurologic/neuromuscular (9.8%) technologies. The vast majority of children (92.5%) had either a chest radiograph (90.5%), respiratory viral study (33.7%), or respiratory culture (10.0%) obtained on presentation. A minority required noninvasive or invasive respiratory support (25.4%), vasoactive agents (8.9%), blood products (1.2%), or pleural drainage (0.3%) in the first two hospital days.

thomson02831120e_t1.jpg

Spectrum of Antimicrobial Coverage

Most children (57.9%) received anaerobic and Gram-negative coverage; 16.2% received anaerobic, Gram-negative and P. aeruginosa coverage; 15.3% received anaerobic coverage alone; and 10.6% received Gram-negative coverage alone. Empiric antimicrobial coverage varied substantially across hospitals: anaerobic coverage was prescribed for 0%-44% of patients; Gram-negative coverage was prescribed for 3%-26% of patients; anaerobic and Gram-negative coverage was prescribed for 25%-90% of patients; and anaerobic, Gram-negative, and P. aeruginosa coverage was prescribed for 0%-65% of patients (Figure 1).

thomson02831120e_f1.jpg

Outcomes

Acute Respiratory Failure

One-quarter (25.4%) of patients had acute respiratory failure on presentation; 22.5% required respiratory support (continued from presentation or were new) on day two or later of hospitalization (Table 2). In the adjusted analysis, children receiving Gram-negative coverage alone had two-fold greater odds (OR 2.15, 95% CI: 1.41-3.27) and children receiving anaerobic and Gram-negative coverage had 1.6-fold greater odds (OR 1.65, 95% CI: 1.19-2.28), of respiratory failure during hospitalization compared with those receiving anaerobic coverage alone (Figure 2). Odds of respiratory failure during hospitalization did not significantly differ for children receiving anaerobic, Gram-negative, and P. aeruginosa coverage compared with those receiving anaerobic coverage alone.

thomson02831120e_t2.jpg

ICU Transfer

Nearly thirty percent (29.0%) of children required ICU admission, with an additional 3.8% requiring ICU transfer following admission (Table 2). In the multivariable analysis, the odds of an ICU transfer were greater for children receiving Gram-negative coverage alone (OR 1.80, 95% CI: 1.03-3.14) compared with those receiving anaerobic coverage alone. There was no statistical difference in ICU transfer for those receiving anaerobic and Gram-negative coverage (with or without P. aeruginosa coverage) compared with those receiving anaerobic coverage alone (Figure 2).

thomson02831120e_f2.jpg

Length of Stay

Median hospital LOS for the total cohort was five days (IQR: 3-9 days; Table 2). In the multivariable analysis, children receiving Gram-negative coverage alone had a longer LOS (RR 1.28; 95% CI: 1.16-1.41) compared with those receiving anaerobic coverage alone, whereas children receiving anaerobic, Gram-negative, and P. aeruginosa coverage had a shorter LOS (RR 0.83; 95% CI: 0.76-0.90) than those receiving anaerobic coverage alone (Figure 2). There was no statistical difference in the LOS between children receiving anaerobic and Gram-negative coverage and those receiving anaerobic coverage alone.

In this multicenter study of children with NI hospitalized with aspiration pneumonia, we found substantial variation in empiric antimicrobial coverage for children with aspiration pneumonia. When comparing outcomes across groups, children who received anaerobic and Gram-negative coverage had outcomes similar to children who received anaerobic therapy alone. However, children who did not receive anaerobic coverage (ie, Gram-negative coverage alone) had worse outcomes, most notably a greater than two-fold increase in the odds of experiencing acute respiratory failure during hospitalization when compared with children receiving anaerobic therapy. These findings support prior literature that has highlighted the importance of anaerobic therapy in the treatment of aspiration pneumonia. The benefit of antibiotics targeting Gram-negative organisms, in addition to anaerobes, remains uncertain.

The variability in empiric antimicrobial coverage likely reflects the paucity of available information on oral and/or enteric bacteria required to identify them as causative organisms in aspiration pneumonia. In part, this problem is due to the difficulty in obtaining adequate sputum for culture from pediatric patients.²⁷ While it may be more feasible to obtain tracheal aspirates for respiratory culture in children with a tracheostomy, interpretation of culture results remains challenging because the lower airways of children with tracheostomy are commonly colonized with bacterial pathogens.²⁸ Thus, physicians are often left to choose empiric antimicrobial coverage with inadequate supporting evidence.²⁹ Although the polymicrobial nature of aspiration pneumonia is well recognized in adult and pediatric literature,^10,30 it is less clear which organisms are of pathological significance and require treatment.

The treatment standard for aspiration pneumonia has long included anaerobic therapy.²⁹ The worse outcomes of children not receiving anaerobic therapy (ie, Gram-negative coverage alone) compared with children who received anaerobic therapy support the continued importance of anaerobic therapy in the treatment of aspiration pneumonia for hospitalized children with NI. The role of antibiotics covering Gram-negative organisms is less clear. Recent studies suggest the role of anaerobes is overemphasized in the etiology and treatment of aspiration pneumonia.^10,29,31-38 Multiple studies on aspiration pneumonia bacteriology in hospitalized adults have demonstrated a predominance of Gram-negative organisms (ranging from 37%-71% of isolates identified on respiratory culture) and a relative scarcity of anaerobes (ranging from 0%-16% of isolates).^31-37 A prospective study of 50 children hospitalized with clinical and radiographic evidence of pneumonia with known aspiration risk (eg, neuromuscular disease or dysphagia) found that ~80% of 163 bacterial isolates were Gram-negative.³⁸ However, this study included repeat cultures from the same children, and thus, may overestimate the prevalence of Gram-negative organisms. In our study, children who received both anaerobic and Gram-negative therapy had no differences in ICU transfer or LOS but did experience higher odds of acute respiratory failure. As these results may be due to unmeasured confounding, future studies should further explore the necessity of Gram-negative coverage in addition to anaerobic coverage in this population.

While these recent studies may seem to suggest that anaerobic coverage is not necessary for aspiration pneumonia, there are important limitations worth noting. First, these studies used a variety of sampling techniques. While organisms grown from samples obtained via bronchoalveolar lavage^31-34,36 are likely pathogenic, those grown from tracheal or oral samples obtained via percutaneous transtracheal aspiration,³⁴ a protected specimen brush,^34,36,37 or expectorated sputum^35,38 may not represent lower airway organisms. Second, anaerobic cultures were not obtained in all studies.^31,34,38 Anaerobic organisms are difficult to isolate using traditional clinical specimen collection techniques and aerobic culture media.¹⁸ Furthermore, anaerobes are not easily recovered from lung infections after the receipt of antibiotic therapy.³⁹ Details regarding pretreatment, which are largely lacking from these studies, are necessary to interpret the relative scarcity of anaerobes on respiratory culture. Finally, caution should be taken when extrapolating the results of studies focused on the etiology and treatment of aspiration pneumonia in elderly adults to children. Our results, particularly in the context of the limitation of these more recent studies, suggest that the role of anaerobes has been underestimated.

Recent studies examining populations of children with cerebral palsy and/or tracheostomy have emphasized the high rates of carriage and infection rates with Gram-negative and drug-resistant bacteria; in particular, P. aeruginosa accounts for 50%-72% of pathogenic bacteria.^11,12,38,40These studies note the generally poor outcomes of children with P. aeruginosa—including multiple and longer hospitalizations, frequent readmissions, and the increased severity of pneumonia, including the need for ICU admission, pleural effusions, the need for intubation, and mortality.^{11,12,38,40,41} In our study, nearly 35% of children who received anaerobic, Gram-negative, and P. aeruginosa coverage experienced acute respiratory failure during hospitalization compared with 20% of children who received other therapies. While these results might seem to suggest that broader spectrum therapy is harmful, they must be interpreted in the context of important population differences; children who received a combination of anaerobic, Gram-negative, and P. aeruginosa coverage had greater medical complexity and greater severity of illness on presentation. Such factors may provide the reason for the appropriate prescription of antipseudomonal antibiotics (eg, history of tracheostomy colonization or infection, long-term care facility resident).⁴² When we controlled for population differences, children who received antipseudomonal therapy had a significantly shorter LOS and no differences in outcomes of acute respiratory failure or ICU transfer compared with those receiving anaerobic therapy alone. This result suggests that worse outcomes were associated with antipseudomonal therapy on unadjusted analyses resulting from underlying medical complexity and illness severity rather than from colonization or infection with P. aeruginosa.

Our multicenter observational study has several limitations. We used diagnosis codes to identify patients with aspiration pneumonia. As validated clinical criteria for the diagnosis of aspiration pneumonia do not exist, clinicians may assign a diagnosis of and treatment for aspiration pneumonia by subjective suspicion based on a child’s severe NI or illness severity on presentation leading to selection bias. Although administrative data are not able to verify pneumonia type with absolute certainty, we previously demonstrated that the differences in the outcomes of children with aspiration and nonaspiration pneumonia diagnosis codes persist after accounting for the complexity that might influence the diagnosis.³It is also possible that the diagnosis of aspiration pneumonia was not made upon admission for a subset of patients leading to misclassification of exposure. Some children may have had aspiration pneumonia on admission but were not assigned that diagnosis or treated for presumed aspiration pneumonia until later in the hospital course as they demonstrated treatment failure or clinical worsening. It is also possible that some children had an aspiration event during hospitalization that developed into aspiration pneumonia. We attempted to adjust for medical complexity and illness severity through multivariable adjustment based on the diagnosis and procedure codes, as well as the laboratory testing performed. However, unmeasured or residual confounding may remain as administrative data are not equipped to distinguish detailed functional status (eg, ability to cough, chest wall strength) or illness severity (eg, respiratory distress) that might influence antibiotic selection and/or outcomes.

Frthermore, we were unable to account for laboratory, microbiology, or radiology test results, and other management practices (eg, frequency of airway clearance, previous antimicrobial therapy) that may influence outcomes. Future studies should certainly include an examination of the concordance of the antibiotics prescribed with causative organisms, as this undoubtedly affects patient outcomes. Other outcomes are important to examine (eg, time to return to respiratory baseline), but we were unable to do so, given the lack of clinical detail in our database. We randomly selected a single hospitalization for children with multiple admissions; alternative methods could have different results. Although children with NI predominately use children’s hospitals,¹ results may not be generalizable.

These findings support prior literature that has highlighted the important role anaerobic therapy plays in the treatment of aspiration pneumonia in children with NI. In light of the limitations of our study design, we believe that rigorous clinical trials comparing anaerobic with anaerobic and Gram-negative therapy are an important and necessary next step to determine the optimal treatment for aspiration pneumonia in this population.

Disclosures

The authors do not have any financial relationships relevant to this article to disclose.

Funding

Dr. Thomson was supported by the Agency for Healthcare Research and Quality (AHRQ) under award number K08HS025138. Dr. Ambroggio was supported by the National Institute for Allergy and Infectious Diseases (NIAID) under award number K01AI125413. The content is solely the responsibility of the authors and does not necessarily represent the official views of the AHRQ or NIAID.

Neurologic impairment (NI) encompasses static and progressive diseases of the central and/or peripheral nervous systems that result in functional and intellectual impairments.¹ While a variety of neurologic diseases are responsible for NI (eg, hypoxic-ischemic encephalopathy, muscular dystrophy), consequences of these diseases extend beyond neurologic manifestations.¹ These children are at an increased risk for aspiration of oral and gastric contents given their common comorbidities of dysphagia, gastroesophageal reflux, impaired cough, and respiratory muscle weakness.² While aspiration may manifest as a self-resolving pneumonitis, the presence of oral or enteric bacteria in aspirated material may result in the development of bacterial pneumonia. Children with NI hospitalized with aspiration pneumonia have higher complication rates, longer and costlier hospitalizations, and higher readmission rates when compared with children with nonaspiration pneumonia.³

While pediatric aspiration pneumonia is commonly attributed to anaerobic bacteria, this is largely based on extrapolation from epidemiologic studies that were conducted in past decades.^4-8 A single randomized controlled trial found that penicillin and clindamycin, antimicrobials with similar antimicrobial activity against anaerobes, to be equally effective.⁹ However, the recent literature emphasizes the polymicrobial nature of aspiration pneumonia in adults, with the common isolation of Gram-negative enteric bacteria.¹⁰ Further, while Pseudomonas aeruginosa is often identified in respiratory cultures from children with NI and chronic respiratory insufficiency,^11,12 the significance of P. aeruginosa in lower airways remains unclear.

We designed this study to compare hospital outcomes associated with the most commonly prescribed empiric antimicrobial therapies for aspiration pneumonia in children with NI.

Study Design and Data Source

This multicenter, retrospective cohort study used the Pediatric Health Information System (PHIS) database. PHIS, an administrative database of 50 not-for-profit tertiary care pediatric hospitals, contains data regarding patient demographics, diagnoses and procedures, and daily billed resource utilization, including laboratory and imaging studies. Data quality and reliability are assured through the Children’s Hospital Association (CHA; Lenexa, Kansas) and participating hospitals. Due to incomplete data through the study period and data quality issues, six hospitals were excluded.

Inclusion Criteria

Children 1-18 years of age who were discharged between July 1, 2007 and June 30, 2015 were included if they had a NI diagnosis,¹ a principal diagnosis indicative of aspiration pneumonia (507.x),^3,13,14 and received antibiotics in the first two calendar days of admission. NI was determined using previously defined International Classification of Diseases, Ninth Revision-Clinical Modification (ICD-9-CM) diagnosis codes.¹ We only included children who received antibiotics in the first two calendar days of admission to minimize the likelihood of including children admitted for other reasons who acquired aspiration pneumonia after hospitalization. For children with multiple hospitalizations, one admission was randomly selected for inclusion to minimize weighting results toward repeat visits.

Exclusion Criteria

Children transferred from another hospital were excluded as records from their initial presentation, including treatment and outcomes, were not available. We also excluded children with tracheostomy^15,16 or chronic ventilator dependence,¹⁷ those with a diagnosis of human immunodeficiency virus or tuberculosis, and children who received chemotherapy during hospitalization given expected differences in etiology, treatment, and outcomes.¹⁸

Exposure

The primary exposure was antibiotic therapy received in the first two days of admission. Antibiotics were classified by their antimicrobial spectra of activity as defined by The Sanford Guide to Antimicrobial Therapy¹⁹ against the most commonly recognized pathogens of aspiration pneumonia: anaerobes, Gram-negatives, and P. aeruginosa (Appendix Table 1).^10,20 For example, penicillin G and clindamycin were among the antibiotics classified as providing anaerobic coverage alone, whereas ceftriaxone was classified as providing Gram-negative coverage alone and ampicillin-sulbactam or as combination therapy with clindamycin and ceftriaxone were classified as providing anaerobic and Gram-negative coverage. Piperacillin-tazobactam and meropenem were classified as providing anaerobic, Gram-negative, and P. aeruginosa coverage. We excluded antibiotics that do not provide coverage against anaerobes, Gram-negative, or P. aeruginosa (eg, ampicillin, azithromycin) or that provide coverage against Gram-negative and P. aeruginosa, but not anaerobes (eg, cefepime, tobramycin), as these therapies were prescribed for <5% of the cohort. We chose not to examine the coverage for Streptococcus pneumonia or Staphylococcus aureus as antibiotics included in this analysis covered these bacteria for 99.9% of our cohort.

Outcomes included acute respiratory failure during hospitalization, intensive care unit (ICU) transfer, and hospital length of stay (LOS). Acute respiratory failure during hospitalization was defined as the presence of Clinical Transaction Classification (CTC) or ICD-9 procedure code for noninvasive or invasive mechanical ventilation on day two or later of hospitalization, with or without the need for respiratory support on day 0 or day 1 (Appendix Table 2). Given the variability in hospital policies that may drive ICU admission criteria for complex patients, our outcome of ICU transfer was defined as the requirement for ICU level care on day two or later of hospitalization without ICU admission. Acute respiratory failure and ICU care occurring within the first two hospital days were not classified as outcomes because these early events likely reflect illness severity at presentation rather than outcomes attributable to treatment failure; these were included as markers of severity in the models.

Patient Demographics and Clinical Characteristics

Demographic and clinical characteristics that might influence antibiotic choice and/or hospital outcomes were assessed. Clinical characteristics included complex chronic conditions,^21-23 medical technology assistance,²⁴ performance of diagnostic testing, and markers of severe illness on presentation. Diagnostic testing included bacterial cultures (blood, respiratory, urine) and chest radiograph performance in the first two days of hospitalization. Results of diagnostic testing are not available in the PHIS. Illness severity on presentation included acute respiratory failure, pleural drainage, receipt of vasoactive agents, and transfusion of blood products in the first two days of hospitalization (Appendix Table 2).^17,25,26

Continuous data were described with median and interquartile ranges (IQR) due to nonnormal distribution. Categorical data were described with frequencies and percentages. Patient demographics, clinical characteristics, and hospital outcomes were stratified by empiric antimicrobial coverage and compared using chi-square and Kruskal–Wallis tests as appropriate.

Generalized linear mixed-effects models with random hospital intercepts were derived to assess the independent effect of antimicrobial spectra of activity on outcomes of acute respiratory failure, ICU transfer, and LOS while adjusting for important differences in demographic and clinical characteristics. LOS had a nonnormal distribution. Thus, we used an exponential distribution. Covariates were chosen a priori given the clinical and biological relevance to exposure and outcomes—age, presence of complex chronic condition diagnoses, the number of complex chronic conditions, technology dependence, the performance of diagnostic tests on presentation, and illness severity on presentation. ICU admission was included as a covariate in acute respiratory failure and LOS outcome models. The results of the model for acute respiratory failure and ICU transfer are presented as adjusted odds ratios (OR) with a 95% CI. LOS results are presented as adjusted rate ratios (RR) with 95% CI.

All analyses were performed with SAS 9.3 (SAS Institute, Cary, North Carolina). P values <.05 were considered statistically significant. Cincinnati Children’s Hospital Medical Center Institutional Review Board considered this deidentified dataset study as not human subjects research.

Study Cohort

At the 44 hospitals included, 4,812 children with NI hospitalized with the diagnosis of aspiration pneumonia met the eligibility criteria. However, 79 received antibiotics with the spectra of activity not examined, leaving 4,733 children in our final analysis (Appendix Figure). Demographic and clinical characteristics of the study cohort are shown in Table 1. Median age was five years (interquartile range [IQR]: 2-11 years). Most subjects were male (53.9%), non-Hispanic white (47.9%), and publicly insured (63.6%). There was a slight variation in the distribution of admissions across seasons (spring 31.6%, summer 19.2%, fall 21.3%, and winter 27.9%). One-third of children had four or more comorbid CCCs (complex chronic conditions; 34.2%). The three most common nonneurologic CCC diagnosis categories were gastrointestinal (63.1%), congenital and/or genetic defects (36.9%), and respiratory (8.9%). Assistance with medical technologies was also common (82%)—particularly gastrointestinal (63.1%) and neurologic/neuromuscular (9.8%) technologies. The vast majority of children (92.5%) had either a chest radiograph (90.5%), respiratory viral study (33.7%), or respiratory culture (10.0%) obtained on presentation. A minority required noninvasive or invasive respiratory support (25.4%), vasoactive agents (8.9%), blood products (1.2%), or pleural drainage (0.3%) in the first two hospital days.

thomson02831120e_t1.jpg

Spectrum of Antimicrobial Coverage

Most children (57.9%) received anaerobic and Gram-negative coverage; 16.2% received anaerobic, Gram-negative and P. aeruginosa coverage; 15.3% received anaerobic coverage alone; and 10.6% received Gram-negative coverage alone. Empiric antimicrobial coverage varied substantially across hospitals: anaerobic coverage was prescribed for 0%-44% of patients; Gram-negative coverage was prescribed for 3%-26% of patients; anaerobic and Gram-negative coverage was prescribed for 25%-90% of patients; and anaerobic, Gram-negative, and P. aeruginosa coverage was prescribed for 0%-65% of patients (Figure 1).

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Outcomes

Acute Respiratory Failure

One-quarter (25.4%) of patients had acute respiratory failure on presentation; 22.5% required respiratory support (continued from presentation or were new) on day two or later of hospitalization (Table 2). In the adjusted analysis, children receiving Gram-negative coverage alone had two-fold greater odds (OR 2.15, 95% CI: 1.41-3.27) and children receiving anaerobic and Gram-negative coverage had 1.6-fold greater odds (OR 1.65, 95% CI: 1.19-2.28), of respiratory failure during hospitalization compared with those receiving anaerobic coverage alone (Figure 2). Odds of respiratory failure during hospitalization did not significantly differ for children receiving anaerobic, Gram-negative, and P. aeruginosa coverage compared with those receiving anaerobic coverage alone.

thomson02831120e_t2.jpg

ICU Transfer

Nearly thirty percent (29.0%) of children required ICU admission, with an additional 3.8% requiring ICU transfer following admission (Table 2). In the multivariable analysis, the odds of an ICU transfer were greater for children receiving Gram-negative coverage alone (OR 1.80, 95% CI: 1.03-3.14) compared with those receiving anaerobic coverage alone. There was no statistical difference in ICU transfer for those receiving anaerobic and Gram-negative coverage (with or without P. aeruginosa coverage) compared with those receiving anaerobic coverage alone (Figure 2).

thomson02831120e_f2.jpg

Length of Stay

Median hospital LOS for the total cohort was five days (IQR: 3-9 days; Table 2). In the multivariable analysis, children receiving Gram-negative coverage alone had a longer LOS (RR 1.28; 95% CI: 1.16-1.41) compared with those receiving anaerobic coverage alone, whereas children receiving anaerobic, Gram-negative, and P. aeruginosa coverage had a shorter LOS (RR 0.83; 95% CI: 0.76-0.90) than those receiving anaerobic coverage alone (Figure 2). There was no statistical difference in the LOS between children receiving anaerobic and Gram-negative coverage and those receiving anaerobic coverage alone.

In this multicenter study of children with NI hospitalized with aspiration pneumonia, we found substantial variation in empiric antimicrobial coverage for children with aspiration pneumonia. When comparing outcomes across groups, children who received anaerobic and Gram-negative coverage had outcomes similar to children who received anaerobic therapy alone. However, children who did not receive anaerobic coverage (ie, Gram-negative coverage alone) had worse outcomes, most notably a greater than two-fold increase in the odds of experiencing acute respiratory failure during hospitalization when compared with children receiving anaerobic therapy. These findings support prior literature that has highlighted the importance of anaerobic therapy in the treatment of aspiration pneumonia. The benefit of antibiotics targeting Gram-negative organisms, in addition to anaerobes, remains uncertain.

The variability in empiric antimicrobial coverage likely reflects the paucity of available information on oral and/or enteric bacteria required to identify them as causative organisms in aspiration pneumonia. In part, this problem is due to the difficulty in obtaining adequate sputum for culture from pediatric patients.²⁷ While it may be more feasible to obtain tracheal aspirates for respiratory culture in children with a tracheostomy, interpretation of culture results remains challenging because the lower airways of children with tracheostomy are commonly colonized with bacterial pathogens.²⁸ Thus, physicians are often left to choose empiric antimicrobial coverage with inadequate supporting evidence.²⁹ Although the polymicrobial nature of aspiration pneumonia is well recognized in adult and pediatric literature,^10,30 it is less clear which organisms are of pathological significance and require treatment.

The treatment standard for aspiration pneumonia has long included anaerobic therapy.²⁹ The worse outcomes of children not receiving anaerobic therapy (ie, Gram-negative coverage alone) compared with children who received anaerobic therapy support the continued importance of anaerobic therapy in the treatment of aspiration pneumonia for hospitalized children with NI. The role of antibiotics covering Gram-negative organisms is less clear. Recent studies suggest the role of anaerobes is overemphasized in the etiology and treatment of aspiration pneumonia.^10,29,31-38 Multiple studies on aspiration pneumonia bacteriology in hospitalized adults have demonstrated a predominance of Gram-negative organisms (ranging from 37%-71% of isolates identified on respiratory culture) and a relative scarcity of anaerobes (ranging from 0%-16% of isolates).^31-37 A prospective study of 50 children hospitalized with clinical and radiographic evidence of pneumonia with known aspiration risk (eg, neuromuscular disease or dysphagia) found that ~80% of 163 bacterial isolates were Gram-negative.³⁸ However, this study included repeat cultures from the same children, and thus, may overestimate the prevalence of Gram-negative organisms. In our study, children who received both anaerobic and Gram-negative therapy had no differences in ICU transfer or LOS but did experience higher odds of acute respiratory failure. As these results may be due to unmeasured confounding, future studies should further explore the necessity of Gram-negative coverage in addition to anaerobic coverage in this population.

While these recent studies may seem to suggest that anaerobic coverage is not necessary for aspiration pneumonia, there are important limitations worth noting. First, these studies used a variety of sampling techniques. While organisms grown from samples obtained via bronchoalveolar lavage^31-34,36 are likely pathogenic, those grown from tracheal or oral samples obtained via percutaneous transtracheal aspiration,³⁴ a protected specimen brush,^34,36,37 or expectorated sputum^35,38 may not represent lower airway organisms. Second, anaerobic cultures were not obtained in all studies.^31,34,38 Anaerobic organisms are difficult to isolate using traditional clinical specimen collection techniques and aerobic culture media.¹⁸ Furthermore, anaerobes are not easily recovered from lung infections after the receipt of antibiotic therapy.³⁹ Details regarding pretreatment, which are largely lacking from these studies, are necessary to interpret the relative scarcity of anaerobes on respiratory culture. Finally, caution should be taken when extrapolating the results of studies focused on the etiology and treatment of aspiration pneumonia in elderly adults to children. Our results, particularly in the context of the limitation of these more recent studies, suggest that the role of anaerobes has been underestimated.

Recent studies examining populations of children with cerebral palsy and/or tracheostomy have emphasized the high rates of carriage and infection rates with Gram-negative and drug-resistant bacteria; in particular, P. aeruginosa accounts for 50%-72% of pathogenic bacteria.^11,12,38,40These studies note the generally poor outcomes of children with P. aeruginosa—including multiple and longer hospitalizations, frequent readmissions, and the increased severity of pneumonia, including the need for ICU admission, pleural effusions, the need for intubation, and mortality.^{11,12,38,40,41} In our study, nearly 35% of children who received anaerobic, Gram-negative, and P. aeruginosa coverage experienced acute respiratory failure during hospitalization compared with 20% of children who received other therapies. While these results might seem to suggest that broader spectrum therapy is harmful, they must be interpreted in the context of important population differences; children who received a combination of anaerobic, Gram-negative, and P. aeruginosa coverage had greater medical complexity and greater severity of illness on presentation. Such factors may provide the reason for the appropriate prescription of antipseudomonal antibiotics (eg, history of tracheostomy colonization or infection, long-term care facility resident).⁴² When we controlled for population differences, children who received antipseudomonal therapy had a significantly shorter LOS and no differences in outcomes of acute respiratory failure or ICU transfer compared with those receiving anaerobic therapy alone. This result suggests that worse outcomes were associated with antipseudomonal therapy on unadjusted analyses resulting from underlying medical complexity and illness severity rather than from colonization or infection with P. aeruginosa.

Our multicenter observational study has several limitations. We used diagnosis codes to identify patients with aspiration pneumonia. As validated clinical criteria for the diagnosis of aspiration pneumonia do not exist, clinicians may assign a diagnosis of and treatment for aspiration pneumonia by subjective suspicion based on a child’s severe NI or illness severity on presentation leading to selection bias. Although administrative data are not able to verify pneumonia type with absolute certainty, we previously demonstrated that the differences in the outcomes of children with aspiration and nonaspiration pneumonia diagnosis codes persist after accounting for the complexity that might influence the diagnosis.³It is also possible that the diagnosis of aspiration pneumonia was not made upon admission for a subset of patients leading to misclassification of exposure. Some children may have had aspiration pneumonia on admission but were not assigned that diagnosis or treated for presumed aspiration pneumonia until later in the hospital course as they demonstrated treatment failure or clinical worsening. It is also possible that some children had an aspiration event during hospitalization that developed into aspiration pneumonia. We attempted to adjust for medical complexity and illness severity through multivariable adjustment based on the diagnosis and procedure codes, as well as the laboratory testing performed. However, unmeasured or residual confounding may remain as administrative data are not equipped to distinguish detailed functional status (eg, ability to cough, chest wall strength) or illness severity (eg, respiratory distress) that might influence antibiotic selection and/or outcomes.

Frthermore, we were unable to account for laboratory, microbiology, or radiology test results, and other management practices (eg, frequency of airway clearance, previous antimicrobial therapy) that may influence outcomes. Future studies should certainly include an examination of the concordance of the antibiotics prescribed with causative organisms, as this undoubtedly affects patient outcomes. Other outcomes are important to examine (eg, time to return to respiratory baseline), but we were unable to do so, given the lack of clinical detail in our database. We randomly selected a single hospitalization for children with multiple admissions; alternative methods could have different results. Although children with NI predominately use children’s hospitals,¹ results may not be generalizable.

These findings support prior literature that has highlighted the important role anaerobic therapy plays in the treatment of aspiration pneumonia in children with NI. In light of the limitations of our study design, we believe that rigorous clinical trials comparing anaerobic with anaerobic and Gram-negative therapy are an important and necessary next step to determine the optimal treatment for aspiration pneumonia in this population.

Disclosures

The authors do not have any financial relationships relevant to this article to disclose.

Funding

Dr. Thomson was supported by the Agency for Healthcare Research and Quality (AHRQ) under award number K08HS025138. Dr. Ambroggio was supported by the National Institute for Allergy and Infectious Diseases (NIAID) under award number K01AI125413. The content is solely the responsibility of the authors and does not necessarily represent the official views of the AHRQ or NIAID.

Polypharmacy, the practice of taking multiple medications to manage health conditions, is common for children. Many children today have a higher burden chronic illness and an increasing number of pharmaceuticals—often delivered in various doses throughout the day. Polypharmacy has been linked to a variety of pediatric and adult outcomes, including medication errors and readmission.^1-3 Consequently, the Society of Hospital Medicine recognizes polypharmacy as a risk factor for readmission for adult populations.⁴ These adverse outcomes are related to both the human elements of polypharmacy (eg, cognitive burden, adherence) and the pharmacologic elements, including drug–drug interactions. For many children, the safety implications of polypharmacy may be more consequential due to the reliance of multiple caregivers to administer medications, which requires additional coordination to ensure that medications are administered and not duplicated. Dual administration of the same medication by both parents is the most common reason for pediatric calls to Poison Control Centers.⁵ Yet, there is a paucity of research in this area, with most of the pediatric literature focusing on the outpatient setting and specific populations, including epilepsy and mental health.^6-8

How providers, patients, and families translate medication lists to counts of medications—and hence the burden of polypharmacy—is not clearly or consistently described. Often in studies of polypharmacy, researchers utilize medication claims data to count the number of medications a patient has filled from the pharmacy. However, in routine clinical practice, clinicians rarely have access to medication claims and thus rely on patient or family report, which may or may not match the list of medications in the patients’ medical records.

Therefore, linking polypharmacy research to the pragmatic complexities of clinical care requires greater clarity and consistent application of concepts. At hospital discharge, families receive a list of medications to take, including home medications to resume as well as newly prescribed medications. However, not all medications are equally essential to patients’ care regarding importance of administration (eg, hydrocortisone ointment versus an anticonvulsant medication). Patients, parents, and caregivers are ultimately responsible for determining which medications to prioritize and administer.

Although there is no standard numerical definition for how to identify polypharmacy, five medications is commonly considered the threshold for polypharmacy.⁹ A recent review of the pediatric polypharmacy literature suggested a lower threshold, with any two concurrent medications for at least a day.⁷ Yet, the best approach to “count” medications at hospital discharge is unclear. The simplest method is to tally the number of medications listed in the discharge summary. However, medications are sometimes listed twice due to different dosages administered at different times. Frequently, medications are prescribed on an as-needed basis; these medications could be administered routinely or very infrequently (eg, epinephrine for anaphylaxis). Over-the-counter medications are also sometimes included in discharge summaries and consideration should be given as to whether these medications count toward measures of polypharmacy. Over-the-counter medications would not be counted by a polypharmacy measure that relies on claims data if those medications are not paid by the insurer.

We sought consensus on how to count discharge medications through a series of informal interviews with hospitalists, nurses, and parents. We asked the seemingly simple question, “How many medications is this child on?” across a variety of scenarios (Figure). For panel A, all stakeholders agreed that this medication list includes two medications. All other scenarios elicited disagreement. For panel B, many people responded three medications, but others (often physicians) counted only clindamycin and therefore responded one medication.

jhm014080506_f1.jpg

Disclosures

Dr. Auger has nothing to disclose. Dr. Shah is the Editor-in-Chief of the Journal of Hospital Medicine. Dr. Davis has nothing to disclose. Dr. Brady reports grants from Agency for Healthcare Research and Quality, outside the submitted work.

Funding

This project is supported by a grant from the Agency for Healthcare Research and Quality (1K08HS204735-01A1).

Polypharmacy, the practice of taking multiple medications to manage health conditions, is common for children. Many children today have a higher burden chronic illness and an increasing number of pharmaceuticals—often delivered in various doses throughout the day. Polypharmacy has been linked to a variety of pediatric and adult outcomes, including medication errors and readmission.^1-3 Consequently, the Society of Hospital Medicine recognizes polypharmacy as a risk factor for readmission for adult populations.⁴ These adverse outcomes are related to both the human elements of polypharmacy (eg, cognitive burden, adherence) and the pharmacologic elements, including drug–drug interactions. For many children, the safety implications of polypharmacy may be more consequential due to the reliance of multiple caregivers to administer medications, which requires additional coordination to ensure that medications are administered and not duplicated. Dual administration of the same medication by both parents is the most common reason for pediatric calls to Poison Control Centers.⁵ Yet, there is a paucity of research in this area, with most of the pediatric literature focusing on the outpatient setting and specific populations, including epilepsy and mental health.^6-8

How providers, patients, and families translate medication lists to counts of medications—and hence the burden of polypharmacy—is not clearly or consistently described. Often in studies of polypharmacy, researchers utilize medication claims data to count the number of medications a patient has filled from the pharmacy. However, in routine clinical practice, clinicians rarely have access to medication claims and thus rely on patient or family report, which may or may not match the list of medications in the patients’ medical records.

Therefore, linking polypharmacy research to the pragmatic complexities of clinical care requires greater clarity and consistent application of concepts. At hospital discharge, families receive a list of medications to take, including home medications to resume as well as newly prescribed medications. However, not all medications are equally essential to patients’ care regarding importance of administration (eg, hydrocortisone ointment versus an anticonvulsant medication). Patients, parents, and caregivers are ultimately responsible for determining which medications to prioritize and administer.

Although there is no standard numerical definition for how to identify polypharmacy, five medications is commonly considered the threshold for polypharmacy.⁹ A recent review of the pediatric polypharmacy literature suggested a lower threshold, with any two concurrent medications for at least a day.⁷ Yet, the best approach to “count” medications at hospital discharge is unclear. The simplest method is to tally the number of medications listed in the discharge summary. However, medications are sometimes listed twice due to different dosages administered at different times. Frequently, medications are prescribed on an as-needed basis; these medications could be administered routinely or very infrequently (eg, epinephrine for anaphylaxis). Over-the-counter medications are also sometimes included in discharge summaries and consideration should be given as to whether these medications count toward measures of polypharmacy. Over-the-counter medications would not be counted by a polypharmacy measure that relies on claims data if those medications are not paid by the insurer.

We sought consensus on how to count discharge medications through a series of informal interviews with hospitalists, nurses, and parents. We asked the seemingly simple question, “How many medications is this child on?” across a variety of scenarios (Figure). For panel A, all stakeholders agreed that this medication list includes two medications. All other scenarios elicited disagreement. For panel B, many people responded three medications, but others (often physicians) counted only clindamycin and therefore responded one medication.

jhm014080506_f1.jpg

Disclosures

Dr. Auger has nothing to disclose. Dr. Shah is the Editor-in-Chief of the Journal of Hospital Medicine. Dr. Davis has nothing to disclose. Dr. Brady reports grants from Agency for Healthcare Research and Quality, outside the submitted work.

Funding

This project is supported by a grant from the Agency for Healthcare Research and Quality (1K08HS204735-01A1).

Polypharmacy, the practice of taking multiple medications to manage health conditions, is common for children. Many children today have a higher burden chronic illness and an increasing number of pharmaceuticals—often delivered in various doses throughout the day. Polypharmacy has been linked to a variety of pediatric and adult outcomes, including medication errors and readmission.^1-3 Consequently, the Society of Hospital Medicine recognizes polypharmacy as a risk factor for readmission for adult populations.⁴ These adverse outcomes are related to both the human elements of polypharmacy (eg, cognitive burden, adherence) and the pharmacologic elements, including drug–drug interactions. For many children, the safety implications of polypharmacy may be more consequential due to the reliance of multiple caregivers to administer medications, which requires additional coordination to ensure that medications are administered and not duplicated. Dual administration of the same medication by both parents is the most common reason for pediatric calls to Poison Control Centers.⁵ Yet, there is a paucity of research in this area, with most of the pediatric literature focusing on the outpatient setting and specific populations, including epilepsy and mental health.^6-8

How providers, patients, and families translate medication lists to counts of medications—and hence the burden of polypharmacy—is not clearly or consistently described. Often in studies of polypharmacy, researchers utilize medication claims data to count the number of medications a patient has filled from the pharmacy. However, in routine clinical practice, clinicians rarely have access to medication claims and thus rely on patient or family report, which may or may not match the list of medications in the patients’ medical records.

Therefore, linking polypharmacy research to the pragmatic complexities of clinical care requires greater clarity and consistent application of concepts. At hospital discharge, families receive a list of medications to take, including home medications to resume as well as newly prescribed medications. However, not all medications are equally essential to patients’ care regarding importance of administration (eg, hydrocortisone ointment versus an anticonvulsant medication). Patients, parents, and caregivers are ultimately responsible for determining which medications to prioritize and administer.

Although there is no standard numerical definition for how to identify polypharmacy, five medications is commonly considered the threshold for polypharmacy.⁹ A recent review of the pediatric polypharmacy literature suggested a lower threshold, with any two concurrent medications for at least a day.⁷ Yet, the best approach to “count” medications at hospital discharge is unclear. The simplest method is to tally the number of medications listed in the discharge summary. However, medications are sometimes listed twice due to different dosages administered at different times. Frequently, medications are prescribed on an as-needed basis; these medications could be administered routinely or very infrequently (eg, epinephrine for anaphylaxis). Over-the-counter medications are also sometimes included in discharge summaries and consideration should be given as to whether these medications count toward measures of polypharmacy. Over-the-counter medications would not be counted by a polypharmacy measure that relies on claims data if those medications are not paid by the insurer.

We sought consensus on how to count discharge medications through a series of informal interviews with hospitalists, nurses, and parents. We asked the seemingly simple question, “How many medications is this child on?” across a variety of scenarios (Figure). For panel A, all stakeholders agreed that this medication list includes two medications. All other scenarios elicited disagreement. For panel B, many people responded three medications, but others (often physicians) counted only clindamycin and therefore responded one medication.

jhm014080506_f1.jpg

Disclosures

Dr. Auger has nothing to disclose. Dr. Shah is the Editor-in-Chief of the Journal of Hospital Medicine. Dr. Davis has nothing to disclose. Dr. Brady reports grants from Agency for Healthcare Research and Quality, outside the submitted work.

Funding

This project is supported by a grant from the Agency for Healthcare Research and Quality (1K08HS204735-01A1).