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Care-Seeking Behavior for Upper Respiratory Infections

BACKGROUND: Many recent efforts to reduce unnecessary medical services have targeted care of upper respiratory infections (URIs). We tested whether patients who seek care very early in their illness differ from those who seek care later and whether they might require a different approach to care.

METHODS: We surveyed by telephone 257 adult patients and 249 parents of child patients who called or visited one of 3 primary care clinics within 10 days (adults) or 14 days (parents) of the onset of uncomplicated URI symptoms. Those who contacted the clinic within the first 2 days of illness were compared with those who made contact later.

RESULTS: Although 28% of adults and 41% of parents contacted their clinic within the first 2 days of symptom onset, we found very few differences in the characteristics of the caller or patient between those who called early and later. The illnesses of those who called early were not more severe, and they did not have different beliefs, histories, approaches to medical care, or needs. The only clinician-relevant difference was that adult patients calling in the first 2 days had a greater desire to rule out complications (84.7% vs 64.1% calling in 3-5 days and 70.6% calling after 5 days of illness, P .05).

CONCLUSIONS: Those who seek medical care very early for a URI do not appear to be different in clinically important ways. If we are going to reduce overuse of medical care and antibiotics for URIs, clinical trials of more effective and efficient strategies are needed to encourage home care and self-management.

Rising health care costs (especially for medications) and a growing concern that unnecessary antibiotic use is creating troublesome bacterial resistance patterns have triggered increasing attention to upper respiratory infection (URI) care.1 URIs are the most frequent reason for office visits and antibiotic use, and at least 50% of patient visits with the diagnosis of URI, cold, or bronchitis include the writing of antibiotic prescriptions.1-2 Also, there is reason to believe that antibiotic use for URI symptoms has increased during the past 2 decades, despite increasing public health efforts to the contrary.3

Much of the expanding literature on URI patients is descriptive, attempting to provide understanding of their expectations and the relationship of various characteristics to antibiotic use for this illness.4-12 Because of the belief that it is patients who create most of the visits and antibiotic use, most studies of URI care address patients’ perceptions, attitudes, and satisfaction.2,4-12 Some studies, however, have shown that the physician’s perception that a patient expects antibiotics is the strongest predictor of prescriptions, even though that perception is not always correct.4-5 This literature suggests that once patients with URIs appear in the clinic it is likely that they will leave with an antibiotic prescription, either because the clinician feels that the illness might be helped by antibiotics or because he or she believes that the patient will be unhappy if antibiotics are not provided. Miller and colleagues13 obtained physician questionnaires for patients with a suspected infection as the reason for the visit. They found that physicians responded to their perception that patients wanted an antibiotic only when the physicians were uncertain about the need for it. When they were fairly certain that an antibiotic was either needed or not needed, perceived patient demand was rarely a factor. Patient satisfaction does not appear to be related to the receipt of antibiotics even when they are expected.5-6

Patients who call or come in within the first few days of the onset of their illness constitute a particularly troubling subgroup of patients for most clinicians. Because it is usually difficult for a clinician to predict whether patients with early URI symptoms are going to encounter complications, it is hard for the clinician to avoid assuming that these patients are either sicker or unusually desirous of a test or treatment. In the absence of any studies of this subgroup, it is possible that those making early contact are particularly likely to receive antibiotics. They will continue to frustrate clinicians and to confound health care system efforts to reduce unnecessary visits and treatments.

To understand the local failure of the implementation of a URI clinical guideline targeted at reducing unnecessary patient visits and antibiotic prescriptions, we conducted a study of the characteristics of patients who seek care for URI symptoms.14 A study of that guideline’s implementation had demonstrated that only 13% of primary care patients with respiratory symptoms were eligible for guideline care, and that subgroup did not show a decrease in clinic visits, antibiotic use, or care costs after guideline implementation.15

 

 

Our study provided an opportunity to better understand the adult patient or parent who seeks care particularly early in the course of the illness. Our research question was: Are those patients or parents who make contact with their care providers particularly early in the course of the illness different from those who make contact later in any way that should affect the way in which they are approached by clinicians or nurses? We hypothesized that the illnesses of these patients are different or that they have different reasons for seeking care from those who present later in the course of the illness. We felt that if clinicians understood these differences, perhaps they could help these patients more effectively, and care systems could reduce unnecessary services and antibiotic usage.

Methods

To test these hypotheses we conducted a telephone survey of cross-sectional samples of adults or parents of children seeking care for URI symptoms at one of 3 diverse primary care clinics in the Minneapolis/St. Paul region of Minnesota: a primary care site for a large multispecialty group practice in an affluent suburb, a staff-model health maintenance organization clinic in a blue-collar suburb, and a medium-sized primary care medical group in a nearby town.

To be included in the sample, adults had to be from 18 to 64 years old or parents of children aged 3 months to 17 years. The patients needed to have a runny nose, cough, or sore throat and to have called or visited the clinic within 14 days (adults) or 10 days (parents) of the onset of symptoms during the study period (March 1, 1997, to May 1, 1997). The subjects were excluded if they reported poor general health, ear pain or infection, or did not speak English. Eligible people were identified from each clinic’s logs of walk-in visits, scheduled appointments, or calls to get advice.

A telephone interview was conducted between 48 and 96 hours after the initial contact with the clinic. Patient selection continued until at least 80 adults and 80 parents of children had participated from each site. The interview consisted of 88 questions devised by study investigators and revised after interviews with 20 patients. Additional pretesting was done with the first 15 patients identified in one clinic. A second 15-item follow-up interview was conducted with the subset of participants who had initially made contact with the clinic within 7 days (adults) or 5 days (parents) of the onset of symptoms. This follow-up interview was made on day 14 (adults) or day 10 (parents) of symptom onset to assess the episode of illness more completely.

Because the dependent variable of interest was the number of days between the onset of illness and the patient’s contact with the clinic, subjects were divided into 3 approximately equal groups. Because contact in the first 2 days of illness may be the most difficult for clinicians to understand and because McIsaac and coworkers16 showed that adults with URI symptoms for more than 2 days were 2.7 times more likely to visit the physician than those sick for 1 to 2 days, the members of this group were designated as the early callers. These callers were compared with those who waited to contact their clinic until between 3 and 5 days or after 5 days of symptoms (who constitute the other 2 groups). Because nearly all subjects had made both a call and a visit (usually within a very short period of time), it was not possible to clearly separate the response into these 2 groups in the analysis.

Descriptive statistics were examined separately for each of the study variables for adult patients and parents. We used the chi-square test of association to compare categorical variables for the 3 illness duration subgroups within each age group.

Results

Interviews were completed with 257 adult patients and 249 parents of child patients (with completion rates of those who met the selection criteria of 94% and 90%, respectively). The sample size for each subgroup by duration of illness and the demographic characteristics of these individuals are listed in Table 1.

Twenty-eight percent of the adult patients and 41% of the child patients had been ill only 1 to 2 days at the time of their first contact with the health care system. None of the characteristics listed in Table 1 differed significantly among these groups, except that parents calling within 2 days of their child’s illness were somewhat less likely to have a college education than parents calling later.

Table 2 illustrates that early callers (in the first 2 days) did not have symptoms that were more frequent or severe than the other groups. In fact, children in this group were less likely to have a cough or green nasal drainage than those in the groups that made contact later (after 3 or more days). Fever, however, was less frequent in both adults and children of parents who sought care after 5 days.

 

 

Adult patients and parents who contacted the clinic early were not more likely to report being unsure that the symptoms represented a cold or being unsure how to treat the symptoms than those coming in after the first 2 days. There was also no greater likelihood that either adults or parents in the early calling group would report a history of any of the following: colds lasting longer; colds being complicated by sinusitis, otitis, or streptococcal infections; seeing a physician for a cold or being told by a physician to be seen; or receiving antibiotics for cold symptoms. Parents (but not adult patients) who made contact early, however, were significantly more likely to report a history of having recovered faster with an antibiotic prescription in the past (42% vs 22% and 23%, P=.01).

The only other differences among these 3 groups were in what they were seeking from the contact and whether they felt that the cold had lasted too long. Adult patients (but not parents) who sought care early were more likely to be worried about complications, while those who appeared later were more likely to want antibiotics and relief (Table 3).

Both adult patients and parents who made contact later were more likely to feel that the cold had lasted too long. For adult patients, 87% of groups that made contact later—but only 46% of those who made contact early—felt that the illness had been going on too long (P=.001). This finding was similar for parents of sick children but to a lesser degree (78% vs 58%, P=.01).

There were no differences in knowledge or beliefs about colds among these 3 groups for either adult patients or parents. Although more than 80% of all groups believed viruses cause colds, 50% believed bacteria also can cause them, and 80% agreed that getting tired and rundown causes colds. Eighty-five percent thought that colds resolve on their own, but 97% thought that rest helps, 66% felt that steam or Vitamin C helps, and nearly half believed in the value of chicken soup.

Finally, early callers were no more likely than those who came in later to report attitudes toward medical care or satisfaction with the visit that might affect their timing of medical care use. Thus, the duration of illness had no effect on respondent reactions to any of the following statements: (1) I will do just about anything to avoid going to the doctor; (2) when I am sick, I try not to let others know; (3) I usually go to the doctor as soon as I start to feel bad; (4) I have paid for my health insurance, so I might as well use it; (5) overall, I liked the manner in which my/my child’s problem was handled; (6) I trust the advice I was given for this illness; and (7) I would recommend this clinic to family or friends for an illness like this.

What about antibiotic use? Although 65% of patients received antibiotics within the 14-day observation period of our study, there was no relationship between receipt of antibiotics and the duration of symptoms at the time of first contact.

Discussion

Contrary to our original hypotheses and the expectations of many clinicians, symptomatic adults and parents of symptomatic children who seek medical assistance soon after the development of URI symptoms do not appear to be different in any important way from those making contact later. They do not have different demographic characteristics, beliefs about colds, or past experiences that might lead them to seek this very early contact. They are also not more likely to have different health status or to have different or more severe symptoms than those seeking care later in their illness (except for a somewhat greater frequency of fever). Although they are more likely to be concerned about complications, they are not any more likely to be unsure about the diagnosis or treatment and do not seem to want anything from the health care system that is different from those making contact later. Specifically, they are not any more likely to want antibiotics for their illness and are not more likely to receive them, despite the fact that parents who call or visit in the first 2 days are twice as likely to report that their child recovered more quickly with antibiotics in the past. Finally, they do not report attitudes toward medical care or satisfaction with the care of this illness that are any different from those who make later contact.

Because nearly one third of adult patients and two fifths of the parents of child patients seek care too early for the clinician to be very confident about the course of the illness, what is it that leads them to this action? There may be some reason that was not addressed in our survey, or the respondents may not feel comfortable admitting to their reasons in an interview sponsored by the health system. It seems more likely, however, that they are simply somewhat more eager to bring health problems to medical attention. The evidence-based guideline that led to our study suggests that almost all the patients in any of the groups we compared are seeking care too early.17

 

 

The overall rate at which antibiotics were prescribed for these patients (65%) is similar to that reported by most other studies.1,4-5 One of the principal aims of the guideline that led to our study was reduction of unnecessary antibiotic use, along with encouragement for initial telephone care instead of office visits for uncomplicated cases.17 The guideline also recommended contact only under these conditions: worsening or new symptoms after the first 3 to 5 days and lack of improvement after 7 to 10 days (children) or 14 days (adults).

However, an impact study of that guideline’s implementation by O’Connor and colleagues15 found that patients who received telephone advice were 50% more likely to come in for an office visit after guideline implementation than before. Also, although antibiotic use at initial contact for the diagnosis of a URI fell from 24% to 16%, the likelihood of receiving an antibiotic during a 21-day follow-up period actually rose after the implementation of the guideline. O’Connor and coworkers concluded that the failure of the guideline implementation to achieve its aims was the result of conflict with patient expectations and desires. Because only those adult patients with illnesses of more than 5 days’ duration reported desires for antibiotic prescriptions at a rate as high as that for actual use, patient desires do not seem to be the only driver of antibiotic use.

Limitations

Our analysis is limited by its inability to separate those who called from those who visited, although the usual concurrence of those events makes any such study difficult. It is also limited in that it is focused entirely on patient responses to a telephone survey, with no additional information about the illness diagnoses, care, or outcomes from chart audits.

Conclusions

There were no obvious explanations in our survey results for the decision by a sizable minority of those seeking medical attention for URI symptoms to do so very soon after the onset of their symptoms. Clinicians will need to elicit and address the chief concerns and needs of each patient they see, regardless of the timing of that contact. It is possible that providing more general information to potential patients about the nature and care of URIs will help health care systems delay or reduce the perceived need of these patients for such contacts, but that remains to be proved. It is time for researchers to move into trials of various intervention strategies that may reduce both unnecessary visits and the associated antibiotic use.

Acknowledgments

Our project was supported by a grant from the Institute for Clinical Systems Improvement, Minneapolis, Minnesota. We are also grateful to the clinic staff who cooperated with our need to identify patients making contact for their URI symptoms.

References

1. Gonzales R, Steiner JF, Sande MA. Antibiotic prescribing for adults with colds, upper respiratory tract infections, and bronchitis by ambulatory care physicians. JAMA 1997;278:901-04.

2. Schappert SM. National ambulatory medical care survey, 1991 summary. Vital and health statistics series 13. No. 116. Hyattsville, Md: National Center for Health Statistics; 1994.

3. Metlay JP, Stafford RS, Singer DE. National trends in the use of antibiotics by primary care physicians for adult patients with cough. Arch Intern Med 1998;158:1813-18.

4. Britten N, Ukoumunne O. The influence of patients’ hopes of receiving a prescription on doctors’ perceptions and the decision to prescribe: a questionnaire survey. BMJ 1997;315:1506-10.

5. Hamm RM, Hicks RJ, Bemben DA. Antibiotics and respiratory infections: are patients more satisfied when expectations are met? J Fam Pract 1996;43:56-62.

6. Cowan PF. Patient satisfaction with an office visit for the common cold. J Fam Pract 1987;24:412-13.

7. Mainous AG,, III, Zoorob RJ, Oler MJ, Haynes DM. Patient knowledge of upper respiratory infections: implications for antibiotic expectations and unnecessary utilization. J Fam Pract 1997;45:75-83.

8. Wyke S, Hewison J, Russell IT. Respiratory illness in children: what makes parents decide to consult? Br J Gen Pract 1990;40:226-29.

9. Macfarlane J, Holmes W, Macfarlane R, Britten N. Influence of patients’ expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study. BMJ 1997;315:1211-14.

10. Holmes WF, Macfarlane JT, Macfarlane RM, Lewis S. The influence of antibiotics and other factors on reconsultation for acute lower respiratory tract illness in primary care. Br J Gen Pract 1997;47:815-18.

11. Bergh KD. The patient’s differential diagnosis: unpredictable concerns in visits for acute cough. J Fam Pract 1998;46:153-58.

12. Brett AS, Mathieu AE. Perceptions and behaviors of patients with upper respiratory tract infection. J Fam Pract 1982;15:277-79.

13. Miller E, MacKeigan LD, Rosser W, Marshman J. Effects of perceived patient demand on prescribing anti-infective drugs. Can Med Assoc J 1999;161:139-42.

14. Braun BL, Fowles JB, Solberg LI, Kind E, Healey M, Anderson R. Patient beliefs about the characteristics, causes, and care of the common cold. J Fam Pract 2000;49:153-56.

15. O’Connor PJ, Amundson G, Christianson J. Performance failure of an evidence-based upper respiratory infection clinical guideline. J Fam Pract 1999;48:690-97.

16. McIsaac WJ, Levine N, Goel V. Visits by adults to family physicians for the common cold. J Fam Pract 1998;47:366-69.

17. ICSI. Health care guidelines: products of ongoing quality improvement. Vol. 2. Bloomington Minn: Institute for Clinical Systems Integration; 1997.

Author and Disclosure Information

Leif I. Solberg, MD
Barbara L. , PhD
Jinnet Briggs Fowles, PhD
Elizabeth A. Kind, MS, RN
Renner S. Anderson, MD
Margaret L. Healey, PhD
Minneapolis, Minnesota
Submitted, revised, April 16, 2000.
From HealthPartners Research Foundation/HealthPartners (L.I.S.) and the Institute for Research and Education, HealthSystem Minnesota (B.L.B., J.B.F., E.A.K., R.S.A., M.L.H.). Reprint requests should be addressed to Leif I. Solberg, MD, Associate Medical Director for Care Improvement Research, HealthPartners/HealthPartners Research Foundation, 8100 34th Ave South, P.O. Box 1524, Minneapolis, MN 55440-1524. E-mail: leif.i.solberg@healthpartners.com.

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The Journal of Family Practice - 49(10)
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915-920
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,Respiratory tract infectionsantibioticsguidelinesprimary care. (J Fam Pract 2000; 49:915-920)
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Author and Disclosure Information

Leif I. Solberg, MD
Barbara L. , PhD
Jinnet Briggs Fowles, PhD
Elizabeth A. Kind, MS, RN
Renner S. Anderson, MD
Margaret L. Healey, PhD
Minneapolis, Minnesota
Submitted, revised, April 16, 2000.
From HealthPartners Research Foundation/HealthPartners (L.I.S.) and the Institute for Research and Education, HealthSystem Minnesota (B.L.B., J.B.F., E.A.K., R.S.A., M.L.H.). Reprint requests should be addressed to Leif I. Solberg, MD, Associate Medical Director for Care Improvement Research, HealthPartners/HealthPartners Research Foundation, 8100 34th Ave South, P.O. Box 1524, Minneapolis, MN 55440-1524. E-mail: leif.i.solberg@healthpartners.com.

Author and Disclosure Information

Leif I. Solberg, MD
Barbara L. , PhD
Jinnet Briggs Fowles, PhD
Elizabeth A. Kind, MS, RN
Renner S. Anderson, MD
Margaret L. Healey, PhD
Minneapolis, Minnesota
Submitted, revised, April 16, 2000.
From HealthPartners Research Foundation/HealthPartners (L.I.S.) and the Institute for Research and Education, HealthSystem Minnesota (B.L.B., J.B.F., E.A.K., R.S.A., M.L.H.). Reprint requests should be addressed to Leif I. Solberg, MD, Associate Medical Director for Care Improvement Research, HealthPartners/HealthPartners Research Foundation, 8100 34th Ave South, P.O. Box 1524, Minneapolis, MN 55440-1524. E-mail: leif.i.solberg@healthpartners.com.

BACKGROUND: Many recent efforts to reduce unnecessary medical services have targeted care of upper respiratory infections (URIs). We tested whether patients who seek care very early in their illness differ from those who seek care later and whether they might require a different approach to care.

METHODS: We surveyed by telephone 257 adult patients and 249 parents of child patients who called or visited one of 3 primary care clinics within 10 days (adults) or 14 days (parents) of the onset of uncomplicated URI symptoms. Those who contacted the clinic within the first 2 days of illness were compared with those who made contact later.

RESULTS: Although 28% of adults and 41% of parents contacted their clinic within the first 2 days of symptom onset, we found very few differences in the characteristics of the caller or patient between those who called early and later. The illnesses of those who called early were not more severe, and they did not have different beliefs, histories, approaches to medical care, or needs. The only clinician-relevant difference was that adult patients calling in the first 2 days had a greater desire to rule out complications (84.7% vs 64.1% calling in 3-5 days and 70.6% calling after 5 days of illness, P .05).

CONCLUSIONS: Those who seek medical care very early for a URI do not appear to be different in clinically important ways. If we are going to reduce overuse of medical care and antibiotics for URIs, clinical trials of more effective and efficient strategies are needed to encourage home care and self-management.

Rising health care costs (especially for medications) and a growing concern that unnecessary antibiotic use is creating troublesome bacterial resistance patterns have triggered increasing attention to upper respiratory infection (URI) care.1 URIs are the most frequent reason for office visits and antibiotic use, and at least 50% of patient visits with the diagnosis of URI, cold, or bronchitis include the writing of antibiotic prescriptions.1-2 Also, there is reason to believe that antibiotic use for URI symptoms has increased during the past 2 decades, despite increasing public health efforts to the contrary.3

Much of the expanding literature on URI patients is descriptive, attempting to provide understanding of their expectations and the relationship of various characteristics to antibiotic use for this illness.4-12 Because of the belief that it is patients who create most of the visits and antibiotic use, most studies of URI care address patients’ perceptions, attitudes, and satisfaction.2,4-12 Some studies, however, have shown that the physician’s perception that a patient expects antibiotics is the strongest predictor of prescriptions, even though that perception is not always correct.4-5 This literature suggests that once patients with URIs appear in the clinic it is likely that they will leave with an antibiotic prescription, either because the clinician feels that the illness might be helped by antibiotics or because he or she believes that the patient will be unhappy if antibiotics are not provided. Miller and colleagues13 obtained physician questionnaires for patients with a suspected infection as the reason for the visit. They found that physicians responded to their perception that patients wanted an antibiotic only when the physicians were uncertain about the need for it. When they were fairly certain that an antibiotic was either needed or not needed, perceived patient demand was rarely a factor. Patient satisfaction does not appear to be related to the receipt of antibiotics even when they are expected.5-6

Patients who call or come in within the first few days of the onset of their illness constitute a particularly troubling subgroup of patients for most clinicians. Because it is usually difficult for a clinician to predict whether patients with early URI symptoms are going to encounter complications, it is hard for the clinician to avoid assuming that these patients are either sicker or unusually desirous of a test or treatment. In the absence of any studies of this subgroup, it is possible that those making early contact are particularly likely to receive antibiotics. They will continue to frustrate clinicians and to confound health care system efforts to reduce unnecessary visits and treatments.

To understand the local failure of the implementation of a URI clinical guideline targeted at reducing unnecessary patient visits and antibiotic prescriptions, we conducted a study of the characteristics of patients who seek care for URI symptoms.14 A study of that guideline’s implementation had demonstrated that only 13% of primary care patients with respiratory symptoms were eligible for guideline care, and that subgroup did not show a decrease in clinic visits, antibiotic use, or care costs after guideline implementation.15

 

 

Our study provided an opportunity to better understand the adult patient or parent who seeks care particularly early in the course of the illness. Our research question was: Are those patients or parents who make contact with their care providers particularly early in the course of the illness different from those who make contact later in any way that should affect the way in which they are approached by clinicians or nurses? We hypothesized that the illnesses of these patients are different or that they have different reasons for seeking care from those who present later in the course of the illness. We felt that if clinicians understood these differences, perhaps they could help these patients more effectively, and care systems could reduce unnecessary services and antibiotic usage.

Methods

To test these hypotheses we conducted a telephone survey of cross-sectional samples of adults or parents of children seeking care for URI symptoms at one of 3 diverse primary care clinics in the Minneapolis/St. Paul region of Minnesota: a primary care site for a large multispecialty group practice in an affluent suburb, a staff-model health maintenance organization clinic in a blue-collar suburb, and a medium-sized primary care medical group in a nearby town.

To be included in the sample, adults had to be from 18 to 64 years old or parents of children aged 3 months to 17 years. The patients needed to have a runny nose, cough, or sore throat and to have called or visited the clinic within 14 days (adults) or 10 days (parents) of the onset of symptoms during the study period (March 1, 1997, to May 1, 1997). The subjects were excluded if they reported poor general health, ear pain or infection, or did not speak English. Eligible people were identified from each clinic’s logs of walk-in visits, scheduled appointments, or calls to get advice.

A telephone interview was conducted between 48 and 96 hours after the initial contact with the clinic. Patient selection continued until at least 80 adults and 80 parents of children had participated from each site. The interview consisted of 88 questions devised by study investigators and revised after interviews with 20 patients. Additional pretesting was done with the first 15 patients identified in one clinic. A second 15-item follow-up interview was conducted with the subset of participants who had initially made contact with the clinic within 7 days (adults) or 5 days (parents) of the onset of symptoms. This follow-up interview was made on day 14 (adults) or day 10 (parents) of symptom onset to assess the episode of illness more completely.

Because the dependent variable of interest was the number of days between the onset of illness and the patient’s contact with the clinic, subjects were divided into 3 approximately equal groups. Because contact in the first 2 days of illness may be the most difficult for clinicians to understand and because McIsaac and coworkers16 showed that adults with URI symptoms for more than 2 days were 2.7 times more likely to visit the physician than those sick for 1 to 2 days, the members of this group were designated as the early callers. These callers were compared with those who waited to contact their clinic until between 3 and 5 days or after 5 days of symptoms (who constitute the other 2 groups). Because nearly all subjects had made both a call and a visit (usually within a very short period of time), it was not possible to clearly separate the response into these 2 groups in the analysis.

Descriptive statistics were examined separately for each of the study variables for adult patients and parents. We used the chi-square test of association to compare categorical variables for the 3 illness duration subgroups within each age group.

Results

Interviews were completed with 257 adult patients and 249 parents of child patients (with completion rates of those who met the selection criteria of 94% and 90%, respectively). The sample size for each subgroup by duration of illness and the demographic characteristics of these individuals are listed in Table 1.

Twenty-eight percent of the adult patients and 41% of the child patients had been ill only 1 to 2 days at the time of their first contact with the health care system. None of the characteristics listed in Table 1 differed significantly among these groups, except that parents calling within 2 days of their child’s illness were somewhat less likely to have a college education than parents calling later.

Table 2 illustrates that early callers (in the first 2 days) did not have symptoms that were more frequent or severe than the other groups. In fact, children in this group were less likely to have a cough or green nasal drainage than those in the groups that made contact later (after 3 or more days). Fever, however, was less frequent in both adults and children of parents who sought care after 5 days.

 

 

Adult patients and parents who contacted the clinic early were not more likely to report being unsure that the symptoms represented a cold or being unsure how to treat the symptoms than those coming in after the first 2 days. There was also no greater likelihood that either adults or parents in the early calling group would report a history of any of the following: colds lasting longer; colds being complicated by sinusitis, otitis, or streptococcal infections; seeing a physician for a cold or being told by a physician to be seen; or receiving antibiotics for cold symptoms. Parents (but not adult patients) who made contact early, however, were significantly more likely to report a history of having recovered faster with an antibiotic prescription in the past (42% vs 22% and 23%, P=.01).

The only other differences among these 3 groups were in what they were seeking from the contact and whether they felt that the cold had lasted too long. Adult patients (but not parents) who sought care early were more likely to be worried about complications, while those who appeared later were more likely to want antibiotics and relief (Table 3).

Both adult patients and parents who made contact later were more likely to feel that the cold had lasted too long. For adult patients, 87% of groups that made contact later—but only 46% of those who made contact early—felt that the illness had been going on too long (P=.001). This finding was similar for parents of sick children but to a lesser degree (78% vs 58%, P=.01).

There were no differences in knowledge or beliefs about colds among these 3 groups for either adult patients or parents. Although more than 80% of all groups believed viruses cause colds, 50% believed bacteria also can cause them, and 80% agreed that getting tired and rundown causes colds. Eighty-five percent thought that colds resolve on their own, but 97% thought that rest helps, 66% felt that steam or Vitamin C helps, and nearly half believed in the value of chicken soup.

Finally, early callers were no more likely than those who came in later to report attitudes toward medical care or satisfaction with the visit that might affect their timing of medical care use. Thus, the duration of illness had no effect on respondent reactions to any of the following statements: (1) I will do just about anything to avoid going to the doctor; (2) when I am sick, I try not to let others know; (3) I usually go to the doctor as soon as I start to feel bad; (4) I have paid for my health insurance, so I might as well use it; (5) overall, I liked the manner in which my/my child’s problem was handled; (6) I trust the advice I was given for this illness; and (7) I would recommend this clinic to family or friends for an illness like this.

What about antibiotic use? Although 65% of patients received antibiotics within the 14-day observation period of our study, there was no relationship between receipt of antibiotics and the duration of symptoms at the time of first contact.

Discussion

Contrary to our original hypotheses and the expectations of many clinicians, symptomatic adults and parents of symptomatic children who seek medical assistance soon after the development of URI symptoms do not appear to be different in any important way from those making contact later. They do not have different demographic characteristics, beliefs about colds, or past experiences that might lead them to seek this very early contact. They are also not more likely to have different health status or to have different or more severe symptoms than those seeking care later in their illness (except for a somewhat greater frequency of fever). Although they are more likely to be concerned about complications, they are not any more likely to be unsure about the diagnosis or treatment and do not seem to want anything from the health care system that is different from those making contact later. Specifically, they are not any more likely to want antibiotics for their illness and are not more likely to receive them, despite the fact that parents who call or visit in the first 2 days are twice as likely to report that their child recovered more quickly with antibiotics in the past. Finally, they do not report attitudes toward medical care or satisfaction with the care of this illness that are any different from those who make later contact.

Because nearly one third of adult patients and two fifths of the parents of child patients seek care too early for the clinician to be very confident about the course of the illness, what is it that leads them to this action? There may be some reason that was not addressed in our survey, or the respondents may not feel comfortable admitting to their reasons in an interview sponsored by the health system. It seems more likely, however, that they are simply somewhat more eager to bring health problems to medical attention. The evidence-based guideline that led to our study suggests that almost all the patients in any of the groups we compared are seeking care too early.17

 

 

The overall rate at which antibiotics were prescribed for these patients (65%) is similar to that reported by most other studies.1,4-5 One of the principal aims of the guideline that led to our study was reduction of unnecessary antibiotic use, along with encouragement for initial telephone care instead of office visits for uncomplicated cases.17 The guideline also recommended contact only under these conditions: worsening or new symptoms after the first 3 to 5 days and lack of improvement after 7 to 10 days (children) or 14 days (adults).

However, an impact study of that guideline’s implementation by O’Connor and colleagues15 found that patients who received telephone advice were 50% more likely to come in for an office visit after guideline implementation than before. Also, although antibiotic use at initial contact for the diagnosis of a URI fell from 24% to 16%, the likelihood of receiving an antibiotic during a 21-day follow-up period actually rose after the implementation of the guideline. O’Connor and coworkers concluded that the failure of the guideline implementation to achieve its aims was the result of conflict with patient expectations and desires. Because only those adult patients with illnesses of more than 5 days’ duration reported desires for antibiotic prescriptions at a rate as high as that for actual use, patient desires do not seem to be the only driver of antibiotic use.

Limitations

Our analysis is limited by its inability to separate those who called from those who visited, although the usual concurrence of those events makes any such study difficult. It is also limited in that it is focused entirely on patient responses to a telephone survey, with no additional information about the illness diagnoses, care, or outcomes from chart audits.

Conclusions

There were no obvious explanations in our survey results for the decision by a sizable minority of those seeking medical attention for URI symptoms to do so very soon after the onset of their symptoms. Clinicians will need to elicit and address the chief concerns and needs of each patient they see, regardless of the timing of that contact. It is possible that providing more general information to potential patients about the nature and care of URIs will help health care systems delay or reduce the perceived need of these patients for such contacts, but that remains to be proved. It is time for researchers to move into trials of various intervention strategies that may reduce both unnecessary visits and the associated antibiotic use.

Acknowledgments

Our project was supported by a grant from the Institute for Clinical Systems Improvement, Minneapolis, Minnesota. We are also grateful to the clinic staff who cooperated with our need to identify patients making contact for their URI symptoms.

BACKGROUND: Many recent efforts to reduce unnecessary medical services have targeted care of upper respiratory infections (URIs). We tested whether patients who seek care very early in their illness differ from those who seek care later and whether they might require a different approach to care.

METHODS: We surveyed by telephone 257 adult patients and 249 parents of child patients who called or visited one of 3 primary care clinics within 10 days (adults) or 14 days (parents) of the onset of uncomplicated URI symptoms. Those who contacted the clinic within the first 2 days of illness were compared with those who made contact later.

RESULTS: Although 28% of adults and 41% of parents contacted their clinic within the first 2 days of symptom onset, we found very few differences in the characteristics of the caller or patient between those who called early and later. The illnesses of those who called early were not more severe, and they did not have different beliefs, histories, approaches to medical care, or needs. The only clinician-relevant difference was that adult patients calling in the first 2 days had a greater desire to rule out complications (84.7% vs 64.1% calling in 3-5 days and 70.6% calling after 5 days of illness, P .05).

CONCLUSIONS: Those who seek medical care very early for a URI do not appear to be different in clinically important ways. If we are going to reduce overuse of medical care and antibiotics for URIs, clinical trials of more effective and efficient strategies are needed to encourage home care and self-management.

Rising health care costs (especially for medications) and a growing concern that unnecessary antibiotic use is creating troublesome bacterial resistance patterns have triggered increasing attention to upper respiratory infection (URI) care.1 URIs are the most frequent reason for office visits and antibiotic use, and at least 50% of patient visits with the diagnosis of URI, cold, or bronchitis include the writing of antibiotic prescriptions.1-2 Also, there is reason to believe that antibiotic use for URI symptoms has increased during the past 2 decades, despite increasing public health efforts to the contrary.3

Much of the expanding literature on URI patients is descriptive, attempting to provide understanding of their expectations and the relationship of various characteristics to antibiotic use for this illness.4-12 Because of the belief that it is patients who create most of the visits and antibiotic use, most studies of URI care address patients’ perceptions, attitudes, and satisfaction.2,4-12 Some studies, however, have shown that the physician’s perception that a patient expects antibiotics is the strongest predictor of prescriptions, even though that perception is not always correct.4-5 This literature suggests that once patients with URIs appear in the clinic it is likely that they will leave with an antibiotic prescription, either because the clinician feels that the illness might be helped by antibiotics or because he or she believes that the patient will be unhappy if antibiotics are not provided. Miller and colleagues13 obtained physician questionnaires for patients with a suspected infection as the reason for the visit. They found that physicians responded to their perception that patients wanted an antibiotic only when the physicians were uncertain about the need for it. When they were fairly certain that an antibiotic was either needed or not needed, perceived patient demand was rarely a factor. Patient satisfaction does not appear to be related to the receipt of antibiotics even when they are expected.5-6

Patients who call or come in within the first few days of the onset of their illness constitute a particularly troubling subgroup of patients for most clinicians. Because it is usually difficult for a clinician to predict whether patients with early URI symptoms are going to encounter complications, it is hard for the clinician to avoid assuming that these patients are either sicker or unusually desirous of a test or treatment. In the absence of any studies of this subgroup, it is possible that those making early contact are particularly likely to receive antibiotics. They will continue to frustrate clinicians and to confound health care system efforts to reduce unnecessary visits and treatments.

To understand the local failure of the implementation of a URI clinical guideline targeted at reducing unnecessary patient visits and antibiotic prescriptions, we conducted a study of the characteristics of patients who seek care for URI symptoms.14 A study of that guideline’s implementation had demonstrated that only 13% of primary care patients with respiratory symptoms were eligible for guideline care, and that subgroup did not show a decrease in clinic visits, antibiotic use, or care costs after guideline implementation.15

 

 

Our study provided an opportunity to better understand the adult patient or parent who seeks care particularly early in the course of the illness. Our research question was: Are those patients or parents who make contact with their care providers particularly early in the course of the illness different from those who make contact later in any way that should affect the way in which they are approached by clinicians or nurses? We hypothesized that the illnesses of these patients are different or that they have different reasons for seeking care from those who present later in the course of the illness. We felt that if clinicians understood these differences, perhaps they could help these patients more effectively, and care systems could reduce unnecessary services and antibiotic usage.

Methods

To test these hypotheses we conducted a telephone survey of cross-sectional samples of adults or parents of children seeking care for URI symptoms at one of 3 diverse primary care clinics in the Minneapolis/St. Paul region of Minnesota: a primary care site for a large multispecialty group practice in an affluent suburb, a staff-model health maintenance organization clinic in a blue-collar suburb, and a medium-sized primary care medical group in a nearby town.

To be included in the sample, adults had to be from 18 to 64 years old or parents of children aged 3 months to 17 years. The patients needed to have a runny nose, cough, or sore throat and to have called or visited the clinic within 14 days (adults) or 10 days (parents) of the onset of symptoms during the study period (March 1, 1997, to May 1, 1997). The subjects were excluded if they reported poor general health, ear pain or infection, or did not speak English. Eligible people were identified from each clinic’s logs of walk-in visits, scheduled appointments, or calls to get advice.

A telephone interview was conducted between 48 and 96 hours after the initial contact with the clinic. Patient selection continued until at least 80 adults and 80 parents of children had participated from each site. The interview consisted of 88 questions devised by study investigators and revised after interviews with 20 patients. Additional pretesting was done with the first 15 patients identified in one clinic. A second 15-item follow-up interview was conducted with the subset of participants who had initially made contact with the clinic within 7 days (adults) or 5 days (parents) of the onset of symptoms. This follow-up interview was made on day 14 (adults) or day 10 (parents) of symptom onset to assess the episode of illness more completely.

Because the dependent variable of interest was the number of days between the onset of illness and the patient’s contact with the clinic, subjects were divided into 3 approximately equal groups. Because contact in the first 2 days of illness may be the most difficult for clinicians to understand and because McIsaac and coworkers16 showed that adults with URI symptoms for more than 2 days were 2.7 times more likely to visit the physician than those sick for 1 to 2 days, the members of this group were designated as the early callers. These callers were compared with those who waited to contact their clinic until between 3 and 5 days or after 5 days of symptoms (who constitute the other 2 groups). Because nearly all subjects had made both a call and a visit (usually within a very short period of time), it was not possible to clearly separate the response into these 2 groups in the analysis.

Descriptive statistics were examined separately for each of the study variables for adult patients and parents. We used the chi-square test of association to compare categorical variables for the 3 illness duration subgroups within each age group.

Results

Interviews were completed with 257 adult patients and 249 parents of child patients (with completion rates of those who met the selection criteria of 94% and 90%, respectively). The sample size for each subgroup by duration of illness and the demographic characteristics of these individuals are listed in Table 1.

Twenty-eight percent of the adult patients and 41% of the child patients had been ill only 1 to 2 days at the time of their first contact with the health care system. None of the characteristics listed in Table 1 differed significantly among these groups, except that parents calling within 2 days of their child’s illness were somewhat less likely to have a college education than parents calling later.

Table 2 illustrates that early callers (in the first 2 days) did not have symptoms that were more frequent or severe than the other groups. In fact, children in this group were less likely to have a cough or green nasal drainage than those in the groups that made contact later (after 3 or more days). Fever, however, was less frequent in both adults and children of parents who sought care after 5 days.

 

 

Adult patients and parents who contacted the clinic early were not more likely to report being unsure that the symptoms represented a cold or being unsure how to treat the symptoms than those coming in after the first 2 days. There was also no greater likelihood that either adults or parents in the early calling group would report a history of any of the following: colds lasting longer; colds being complicated by sinusitis, otitis, or streptococcal infections; seeing a physician for a cold or being told by a physician to be seen; or receiving antibiotics for cold symptoms. Parents (but not adult patients) who made contact early, however, were significantly more likely to report a history of having recovered faster with an antibiotic prescription in the past (42% vs 22% and 23%, P=.01).

The only other differences among these 3 groups were in what they were seeking from the contact and whether they felt that the cold had lasted too long. Adult patients (but not parents) who sought care early were more likely to be worried about complications, while those who appeared later were more likely to want antibiotics and relief (Table 3).

Both adult patients and parents who made contact later were more likely to feel that the cold had lasted too long. For adult patients, 87% of groups that made contact later—but only 46% of those who made contact early—felt that the illness had been going on too long (P=.001). This finding was similar for parents of sick children but to a lesser degree (78% vs 58%, P=.01).

There were no differences in knowledge or beliefs about colds among these 3 groups for either adult patients or parents. Although more than 80% of all groups believed viruses cause colds, 50% believed bacteria also can cause them, and 80% agreed that getting tired and rundown causes colds. Eighty-five percent thought that colds resolve on their own, but 97% thought that rest helps, 66% felt that steam or Vitamin C helps, and nearly half believed in the value of chicken soup.

Finally, early callers were no more likely than those who came in later to report attitudes toward medical care or satisfaction with the visit that might affect their timing of medical care use. Thus, the duration of illness had no effect on respondent reactions to any of the following statements: (1) I will do just about anything to avoid going to the doctor; (2) when I am sick, I try not to let others know; (3) I usually go to the doctor as soon as I start to feel bad; (4) I have paid for my health insurance, so I might as well use it; (5) overall, I liked the manner in which my/my child’s problem was handled; (6) I trust the advice I was given for this illness; and (7) I would recommend this clinic to family or friends for an illness like this.

What about antibiotic use? Although 65% of patients received antibiotics within the 14-day observation period of our study, there was no relationship between receipt of antibiotics and the duration of symptoms at the time of first contact.

Discussion

Contrary to our original hypotheses and the expectations of many clinicians, symptomatic adults and parents of symptomatic children who seek medical assistance soon after the development of URI symptoms do not appear to be different in any important way from those making contact later. They do not have different demographic characteristics, beliefs about colds, or past experiences that might lead them to seek this very early contact. They are also not more likely to have different health status or to have different or more severe symptoms than those seeking care later in their illness (except for a somewhat greater frequency of fever). Although they are more likely to be concerned about complications, they are not any more likely to be unsure about the diagnosis or treatment and do not seem to want anything from the health care system that is different from those making contact later. Specifically, they are not any more likely to want antibiotics for their illness and are not more likely to receive them, despite the fact that parents who call or visit in the first 2 days are twice as likely to report that their child recovered more quickly with antibiotics in the past. Finally, they do not report attitudes toward medical care or satisfaction with the care of this illness that are any different from those who make later contact.

Because nearly one third of adult patients and two fifths of the parents of child patients seek care too early for the clinician to be very confident about the course of the illness, what is it that leads them to this action? There may be some reason that was not addressed in our survey, or the respondents may not feel comfortable admitting to their reasons in an interview sponsored by the health system. It seems more likely, however, that they are simply somewhat more eager to bring health problems to medical attention. The evidence-based guideline that led to our study suggests that almost all the patients in any of the groups we compared are seeking care too early.17

 

 

The overall rate at which antibiotics were prescribed for these patients (65%) is similar to that reported by most other studies.1,4-5 One of the principal aims of the guideline that led to our study was reduction of unnecessary antibiotic use, along with encouragement for initial telephone care instead of office visits for uncomplicated cases.17 The guideline also recommended contact only under these conditions: worsening or new symptoms after the first 3 to 5 days and lack of improvement after 7 to 10 days (children) or 14 days (adults).

However, an impact study of that guideline’s implementation by O’Connor and colleagues15 found that patients who received telephone advice were 50% more likely to come in for an office visit after guideline implementation than before. Also, although antibiotic use at initial contact for the diagnosis of a URI fell from 24% to 16%, the likelihood of receiving an antibiotic during a 21-day follow-up period actually rose after the implementation of the guideline. O’Connor and coworkers concluded that the failure of the guideline implementation to achieve its aims was the result of conflict with patient expectations and desires. Because only those adult patients with illnesses of more than 5 days’ duration reported desires for antibiotic prescriptions at a rate as high as that for actual use, patient desires do not seem to be the only driver of antibiotic use.

Limitations

Our analysis is limited by its inability to separate those who called from those who visited, although the usual concurrence of those events makes any such study difficult. It is also limited in that it is focused entirely on patient responses to a telephone survey, with no additional information about the illness diagnoses, care, or outcomes from chart audits.

Conclusions

There were no obvious explanations in our survey results for the decision by a sizable minority of those seeking medical attention for URI symptoms to do so very soon after the onset of their symptoms. Clinicians will need to elicit and address the chief concerns and needs of each patient they see, regardless of the timing of that contact. It is possible that providing more general information to potential patients about the nature and care of URIs will help health care systems delay or reduce the perceived need of these patients for such contacts, but that remains to be proved. It is time for researchers to move into trials of various intervention strategies that may reduce both unnecessary visits and the associated antibiotic use.

Acknowledgments

Our project was supported by a grant from the Institute for Clinical Systems Improvement, Minneapolis, Minnesota. We are also grateful to the clinic staff who cooperated with our need to identify patients making contact for their URI symptoms.

References

1. Gonzales R, Steiner JF, Sande MA. Antibiotic prescribing for adults with colds, upper respiratory tract infections, and bronchitis by ambulatory care physicians. JAMA 1997;278:901-04.

2. Schappert SM. National ambulatory medical care survey, 1991 summary. Vital and health statistics series 13. No. 116. Hyattsville, Md: National Center for Health Statistics; 1994.

3. Metlay JP, Stafford RS, Singer DE. National trends in the use of antibiotics by primary care physicians for adult patients with cough. Arch Intern Med 1998;158:1813-18.

4. Britten N, Ukoumunne O. The influence of patients’ hopes of receiving a prescription on doctors’ perceptions and the decision to prescribe: a questionnaire survey. BMJ 1997;315:1506-10.

5. Hamm RM, Hicks RJ, Bemben DA. Antibiotics and respiratory infections: are patients more satisfied when expectations are met? J Fam Pract 1996;43:56-62.

6. Cowan PF. Patient satisfaction with an office visit for the common cold. J Fam Pract 1987;24:412-13.

7. Mainous AG,, III, Zoorob RJ, Oler MJ, Haynes DM. Patient knowledge of upper respiratory infections: implications for antibiotic expectations and unnecessary utilization. J Fam Pract 1997;45:75-83.

8. Wyke S, Hewison J, Russell IT. Respiratory illness in children: what makes parents decide to consult? Br J Gen Pract 1990;40:226-29.

9. Macfarlane J, Holmes W, Macfarlane R, Britten N. Influence of patients’ expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study. BMJ 1997;315:1211-14.

10. Holmes WF, Macfarlane JT, Macfarlane RM, Lewis S. The influence of antibiotics and other factors on reconsultation for acute lower respiratory tract illness in primary care. Br J Gen Pract 1997;47:815-18.

11. Bergh KD. The patient’s differential diagnosis: unpredictable concerns in visits for acute cough. J Fam Pract 1998;46:153-58.

12. Brett AS, Mathieu AE. Perceptions and behaviors of patients with upper respiratory tract infection. J Fam Pract 1982;15:277-79.

13. Miller E, MacKeigan LD, Rosser W, Marshman J. Effects of perceived patient demand on prescribing anti-infective drugs. Can Med Assoc J 1999;161:139-42.

14. Braun BL, Fowles JB, Solberg LI, Kind E, Healey M, Anderson R. Patient beliefs about the characteristics, causes, and care of the common cold. J Fam Pract 2000;49:153-56.

15. O’Connor PJ, Amundson G, Christianson J. Performance failure of an evidence-based upper respiratory infection clinical guideline. J Fam Pract 1999;48:690-97.

16. McIsaac WJ, Levine N, Goel V. Visits by adults to family physicians for the common cold. J Fam Pract 1998;47:366-69.

17. ICSI. Health care guidelines: products of ongoing quality improvement. Vol. 2. Bloomington Minn: Institute for Clinical Systems Integration; 1997.

References

1. Gonzales R, Steiner JF, Sande MA. Antibiotic prescribing for adults with colds, upper respiratory tract infections, and bronchitis by ambulatory care physicians. JAMA 1997;278:901-04.

2. Schappert SM. National ambulatory medical care survey, 1991 summary. Vital and health statistics series 13. No. 116. Hyattsville, Md: National Center for Health Statistics; 1994.

3. Metlay JP, Stafford RS, Singer DE. National trends in the use of antibiotics by primary care physicians for adult patients with cough. Arch Intern Med 1998;158:1813-18.

4. Britten N, Ukoumunne O. The influence of patients’ hopes of receiving a prescription on doctors’ perceptions and the decision to prescribe: a questionnaire survey. BMJ 1997;315:1506-10.

5. Hamm RM, Hicks RJ, Bemben DA. Antibiotics and respiratory infections: are patients more satisfied when expectations are met? J Fam Pract 1996;43:56-62.

6. Cowan PF. Patient satisfaction with an office visit for the common cold. J Fam Pract 1987;24:412-13.

7. Mainous AG,, III, Zoorob RJ, Oler MJ, Haynes DM. Patient knowledge of upper respiratory infections: implications for antibiotic expectations and unnecessary utilization. J Fam Pract 1997;45:75-83.

8. Wyke S, Hewison J, Russell IT. Respiratory illness in children: what makes parents decide to consult? Br J Gen Pract 1990;40:226-29.

9. Macfarlane J, Holmes W, Macfarlane R, Britten N. Influence of patients’ expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study. BMJ 1997;315:1211-14.

10. Holmes WF, Macfarlane JT, Macfarlane RM, Lewis S. The influence of antibiotics and other factors on reconsultation for acute lower respiratory tract illness in primary care. Br J Gen Pract 1997;47:815-18.

11. Bergh KD. The patient’s differential diagnosis: unpredictable concerns in visits for acute cough. J Fam Pract 1998;46:153-58.

12. Brett AS, Mathieu AE. Perceptions and behaviors of patients with upper respiratory tract infection. J Fam Pract 1982;15:277-79.

13. Miller E, MacKeigan LD, Rosser W, Marshman J. Effects of perceived patient demand on prescribing anti-infective drugs. Can Med Assoc J 1999;161:139-42.

14. Braun BL, Fowles JB, Solberg LI, Kind E, Healey M, Anderson R. Patient beliefs about the characteristics, causes, and care of the common cold. J Fam Pract 2000;49:153-56.

15. O’Connor PJ, Amundson G, Christianson J. Performance failure of an evidence-based upper respiratory infection clinical guideline. J Fam Pract 1999;48:690-97.

16. McIsaac WJ, Levine N, Goel V. Visits by adults to family physicians for the common cold. J Fam Pract 1998;47:366-69.

17. ICSI. Health care guidelines: products of ongoing quality improvement. Vol. 2. Bloomington Minn: Institute for Clinical Systems Integration; 1997.

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