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Original research
Benjamin H. Chin-Yeea, Katherine Monkman MDa, Zafar Hussain MD, FRCP(C)a and Leonard A. Minuk MD, FRCP(C)
Background
Patients with hematologic malignancies are at increased risk of influenza and its complications. Despite current health recommendations and evidence favoring influenza vaccination, vaccination rates remain low in cancer patients.
Objective
The purpose of this study was to determine which factors influenced vaccination rates.
Methods
During the 2009–2010 pandemic H1N1 and seasonal influenza season, we surveyed patients with hematologic malignancies in a Canadian cancer center. Of the patients participating in our study (n = 129), 66% and 57% received the H1N1 pandemic influenza and seasonal influenza vaccines, respectively.
Results
A number of reasons for vaccination refusal were reported, most relating to general skepticism about the safety and efficacy of vaccination. Physician advice was also a factor influencing vaccination rates in patients. The vaccination rate for seasonal influenza was 39% in patients <65 years old, significantly lower than the rate of 73% reported for patients aged ≥65 years (P < 0.0001).
Conclusion
Future education programs should target younger patient populations and health-care workers, focusing on vaccine safety and efficacy in the high-risk cancer population.
Despite the annual development of effective influenza vaccines, influenza remains a significant cause of morbidity and mortality in Canada. In the 2009–2010 influenza season, approximately 40,000 Canadians were infected with seasonal influenza or the pandemic H1N1 influenza virus,1 and influenza has been estimated to cause 4,000–8,000 deaths in Canada each year.2 It is estimated that a severe influenza pandemic could result in a 1% reduction in annual gross domestic product in Canada.3
Patients with hematologic malignancies are known to be at increased risk of influenza and its complications, with estimated mortality rates in the range 5%–27%.[4], [5], [6], [7] and [8] Evidence for the efficacy of the influenza vaccine is limited and contradictory, and many assume that immunocompromised patients will not be able to generate a protective antibody response. Nonetheless, current evidence favors vaccination.9 Pollyea et al10 reported that eight of 15 trials on the efficacy of vaccination in patients with hematologic malignancies concluded that vaccination was beneficial. Both the Centers for Disease Control and Prevention (CDC) and the Public Health Agency of Canada (PHAC) advised that all immunocompromised patients, including those with cancer, receive both the seasonal influenza vaccine and the pandemic H1N1 influenza vaccine in the 2009–2010 influenza season.[11] and [12]
Despite these recommendations, rates of influenza vaccination remain low for the general population and cancer patients in Canada, with rates reported at 40% and 65% respectively.[13] and [14] A recent study by Yee et al15 reported similarly low influenza vaccination rates of 58% in cancer patients in the United States. Vaccination has long been a controversial public health issue, and many people choose not to be vaccinated due to fears that vaccines may not be safe and effective.[16], [17] and [18] Lack of physician recommendation has also been cited as a significant factor in the decision to decline vaccination.16
In this study, we sought to determine what percentage of patients being treated for hematologic malignancies in an Ontario, Canada, cancer center received the H1N1 pandemic influenza vaccine in the 2009–2010 influenza season and to explore the barriers to vaccination in this high-risk population. We also collected information on the percentage of patients who received the seasonal influenza vaccine. It was general practice for physicians at this center to recommend influenza vaccination in accordance with the PHAC recommendations.
Methods
Patients being treated for hematologic malignancies at the London Regional Cancer Program (London, Canada) were invited to complete a survey regarding influenza vaccination (Appendix). The London Regional Cancer Program is a tertiary care center providing specialized cancer care to a population base of 1.2 million in southwestern Ontario. The survey was administered to patients eligible to participate in another study assessing antibody levels pre- and postvaccination with the H1N1 pandemic vaccine. Eligible patients were 18 years or older and being treated or followed for hematological malignancies at the London Regional Cancer Program who attended an appointment between October 28 and November 19, 2009, and returned for a follow-up visit between January 5 and March 26, 2010 (n = 151). Patients were asked if they had received the pandemic H1N1 influenza vaccine and the seasonal influenza vaccine during the 2009–2010 influenza season. Those who had declined vaccination were asked to describe the reasons for their choice. The survey provided a list of six possible reasons for declining vaccination and gave patients the option of writing in their own responses.
The results of the study were analyzed using InStat 3 software (GraphPad, La Jolla, CA). The Mann-Whitney U-test was used to compare continuous variables, and Fisher's exact test was used to compare proportions. The study was approved by the University of Western Ontario's Institutional Research Ethics Board (IRB 16627E).
Results
Of the 151 patients invited to participate, 129 completed the survey, yielding a response rate of 85%. Patient characteristics are shown in Table 1. The respondents ranged in age from 19 to 86 years, 56% were male and 44% were female, and patients aged 65 years or older comprised 52% of the study population. The mean age of the patient group was 62.7 ± 14.8 years. Overall 119 patients (92%) had received chemotherapy at some time during their illness, with 96 patients (76%) actively receiving chemotherapy, defined as treatment within the past 3 months. Diagnoses included acute leukemia, chronic lymphocytic leukemia, chronic myeloid leukemia, lymphoma, multiple myeloma, myelodysplastic syndromes, and myeloproliferative neoplasms.
Of the 129 patients surveyed, 85 (66%) reported that they had received the H1N1 pandemic influenza vaccine during the 2009–2010 influenza season. Fifty-seven percent had received the seasonal influenza vaccine, and 50% had received both the seasonal and the H1N1 vaccines. Of the 44 patients who did not receive the H1N1 vaccine, only three planned to receive it. Eight of the 56 patients not vaccinated with the seasonal influenza vaccine planned to receive it.
There were no significant differences in mean age, percentage of patients over 65 years old, gender, or chemotherapy status between patients who received the H1N1 vaccine and those who declined it (Table 1). The mean age of patients who received the seasonal influenza vaccine was significantly higher than that of those who did not (67.8 ±12.1 vs. 56.1 ± 15.5 years, P < 0.0001), and a significantly higher percentage of patients in the vaccinated group were over the age of 65 (67% vs. 33%, P < 0.0001).
Patient-reported reasons for not receiving the H1N1 vaccine are shown in Figure 1. The two most common reasons for declining vaccination were beliefs that “the vaccine is dangerous because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). The belief that vaccination was dangerous or not effective because of the patient's medical condition represented 16% and 12% of responses, respectively. Six percent responded that receiving the vaccine would have been too inconvenient. No patients reported concerns about pain at the injection site as a reason for avoiding vaccination. In the category of “other,” responses fell into four broad categories: “physician advised against vaccination” (8%), “vaccination is unnecessary” (8%), “previous bad experience from vaccine” (4%), and “vaccine will make me sick” (4%).
Discussion
Our study found that 66% of patients being treated for hematological malignancies at a southwestern Ontario cancer center received the H1N1 vaccine during the 2009–2010 influenza season. This was higher than the rate of H1N1 vaccination in the general Canadian population, which was reported as 41%.14 Canadian cancer patients have been previously shown to have higher rates of participation in vaccination programs. In 2005, 64% of Canadians with cancer received the seasonal influenza vaccine compared with 34% of the overall population.13 This trend may be driven in part by the higher average age of patients receiving cancer treatment as adults 65 years of age or older comprised 52% of the respondents in our study.
Worldwide, Canada ranks among the highest countries in vaccination coverage. The United Kingdom reported a vaccination rate of 28.7% during the 2007–2008 influenza season, which was at the time one of the highest in Europe.19 Other European countries, including Germany, Italy, and France, showed vaccination rates similar to that of the United Kingdom. In all of these countries vaccination coverage increased with age. The United States has vaccination rates most similar to those of Canada, estimated at 40% in the overall population and 68% in the population ≥65 years old during the 2009–2010 influenza season.20
Higher vaccination rates have been reported in the elderly compared to younger adult population,[13] and [14] and our findings prove to be consistent with this reported trend. In this study, the group vaccinated with the seasonal influenza vaccine had a mean age of 67.8 ± 12.1 years compared with the unvaccinated group aged 56.1 ± 15.5 years (P < 0.0001). Interestingly, there was no significant difference in mean age between the vaccinated and unvaccinated groups for the H1N1 pandemic influenza vaccine (P > 0.05). This was not entirely unexpected since public health campaigns during the 2009–2010 influenza season focused on the younger age group due to their increased susceptibility to severe H1N1 disease. Nonetheless, there was a trend toward an increased mean age for those who received the vaccine (64.0 ± 12.5 years) compared to those who did not (60.4 ± 18.4 years), and it is possible that statistical significance was not reached due to the small sample size. Our study reported an alarmingly low 39% vaccination rate for seasonal influenza in cancer patients <65, suggesting that the PHAC's message is not adequately reaching this potentially at-risk group.
Reasons for refusal of vaccination have been well described in previous studies.[16], [17], [18], [21], [22], [23], [24], [25] and [26] We found that the most common reasons for refusal of vaccination by cancer patients were very similar to those reported in healthy individuals. Specifically, concerns about the safety and efficacy of vaccines in general were more common than concerns related to cancer or chemotherapy. The most common reasons for refusal of vaccination were “I think the vaccine will be dangerous for people in general because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). Despite the publicity, 8% of unvaccinated patients responded that they did not feel that H1N1 influenza was a significant threat. In this study, the belief that the vaccine was dangerous because of lack of testing or a previous medical condition was responsible for 13% of patients not receiving the vaccine. Five percent of patients elected not to be vaccinated because of questions of efficacy. The H1N1 vaccine is an adjuvant with AsO3, which may cause more vaccine reactions, while the seasonal influenza vaccine is not an adjuvant. It is possible that the presence of adjuvant contributed to some patients' safety concerns, though we did not specifically ask if the adjuvant influenced their decision.
Physician advice may have played a significant role in patients' decisions to vaccinate. Eight percent of patients who did not receive the vaccine reported that they were not vaccinated due to advice from a physician. It is our routine institutional policy to recommend vaccination for all cancer patients irrespective of underlying diagnosis or treatment regimen. We do not, however, provide standardized written information to patients or referring physicians, so some patients may have been advised against vaccination by other physicians. Some primary care physicians might not have been familiar with the current PHAC recommendations or the recent literature suggesting the vaccine's potential benefits in this group. Public health campaigns should therefore seek to educate physicians as well as patients regarding the safety and efficacy of the influenza vaccine for cancer patients.
Conclusion
We found that rates of H1N1 and seasonal influenza vaccination in a southwestern Ontario cancer center were higher than those reported for the general population. Nevertheless, despite a large public health education campaign, a significant number of patients declined vaccination due to fear that it would not be safe or effective or due to a belief that vaccination was not necessary. Although the rate of seasonal influenza vaccination was high for those ≥65 years old, it was poor for those aged <65 years, despite vaccination being recommended for all adults with chronic medical conditions. Future education programs should target younger patient populations and health-care workers and focus on vaccine safety and efficacy in immunocompromised patients as well as in other high-risk groups.
References1
1 Public Health Agency of Canada, FluWatch http://www.phac-aspc.gc.ca/fluwatch/09-10/w28_10/index-eng.php Accessed August 5, 2010.
2 Public Health Agency of Canada, Influenza http://www.phac-aspc.gc.ca/influenza/index-eng.php Accessed August 5, 2010.
3 S. James and T. Sargent, The Economic Impact of an Influenza Pandemic, Department of Finance Canada, Ottawa (2006), p. 90.
4 R.F. Chemaly, S. Ghosh, G.P. Bodey, N. Rohatgi, A. Safdar, M.J. Keating, R.E. Champlin, E.A. Aguilera, J.J. Tarrand and I.I. Raad, Respiratory viral infections in adults with hematologic malignancies and human stem cell transplantation recipients: a retrospective study at a major cancer center, Medicine 85 (5) (2006), pp. 278–287. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (66)
5 H.M. Yousuf, J. Englund, R. Couch, K. Rolston, M. Luna, J. Goodrich, V. Lewis, N.Q. Mirza, M. Andreeff, C. Koller, L. Elting, G.P. Bodey and E. Whimbey, Influenza among hospitalized adults with leukemia, Clin Infect Dis 24 (6) (1997), pp. 1095–1099. View Record in Scopus | Cited By in Scopus (55)
6 C.D. Cooksley, E.B. Avritscher, B.N. Bekele, K.V. Rolston, J.M. Geraci and L.S. Elting, Epidemiology and outcomes of serious influenza-related infections in the cancer population, Cancer 104 (3) (2005), pp. 618–628. View Record in Scopus | Cited By in Scopus (24)
7 L.S. Elting, E. Whimbey, W. Lo, R. Couch, M. Andreeff and G.P. Bodey, Epidemiology of influenza A virus infection in patients with acute or chronic leukemia, Support Care Cancer 3 (3) (1995), pp. 198–202. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (32)
8 E. Whimbey, L.S. Elting, R.B. Couch, W. Lo, L. Williams, R.E. Champlin and G.P. Bodey, Influenza A virus infections among hospitalized adult bone marrow transplant recipients, Bone Marrow Transplant 13 (4) (1994), pp. 437–440. View Record in Scopus | Cited By in Scopus (110)
9 M. Tiseo, B. Calatafimi, L. Ferri, A. Menardi and A. Ardizzoni, Efficacy and safety of influenza vaccination during chemotherapy treatment, J Support Oncol 8 (6) (2010), pp. 271–272. Article | 
10 D.A. Pollyea, J.M. Brown and S.J. Horning, Utility of influenza vaccination for oncology patients, J Clin Oncol 28 (14) (2010), pp. 2481–2490. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (8)
11 Public Health Agency of Canada, Guidance Document on the Use of Pandemic Influenza A (H1N1) 2009: Inactivated Monovalent Vaccine, Public Health Agency of Canada, Ottawa (2009).
12 Centers for Disease Control, 2009 H1N1 Vaccination Recommendations http://www.cdc.gov/h1n1flu/vaccination/acip.htm Accessed August 5, 2010.
13 J.C. Kwong, L.C. Rosella and H. Johansen, Trends in influenza vaccination in Canada, 1996/1997 to 2005, Health Rep 18 (4) (2007), pp. 9–19. View Record in Scopus | Cited By in Scopus (14)
14 Statistics Canda, Canadian Community Health Survey: H1N1 Vaccinations http://www.statcan.gc.ca/daily-quotidien/100719/dq100719b-eng.htm Accessed August 5, 2010.
15 S.S. Yee, P.R. Dutta, L.J. Solin, N. Vapiwala and G.D. Kao, Lack of compliance with national vaccination guidelines in oncology patients receiving radiation therapy, J Support Oncol 8 (1) (2010), pp. 28–34. View Record in Scopus | Cited By in Scopus (2)
16 P. Loulergue, O. Mir, J. Alexandre, S. Ropert, F. Goldwasser and O. Launay, Low influenza vaccination rate among patients receiving chemotherapy for cancer, Ann Oncol 19 (9) (2008), p. 1658. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (10)
17 R.K. Zimmerman, T.A. Santibanez, J.E. Janosky, M.J. Fine, M. Raymund, S.A. Wilson, I.J. Bardella, A.R. Medsger and M.P. Nowalk, What affects influenza vaccination rates among older patients?: An analysis from inner-city, suburban, rural, and Veterans Affairs practices, Am J Med 114 (1) (2003), pp. 31–38. Article |
18 M.W. Mah, N.A. Hagen, K. Pauling-Shepard, J.S. Hawthorne, M. Mysak, T. Lye and T.J. Louie, Understanding influenza vaccination attitudes at a Canadian cancer center, Am J Infect Control 33 (4) (2005), pp. 243–250. Article |
19 P.R. Blank, M. Schwenkglenks and T.D. Szucs, Vaccination coverage rates in eleven European countries during two consecutive influenza seasons, J Infect 58 (6) (2009), pp. 446–458. Article |
20 Centers for Disease Control and Prevention, Interim Results: State-Specific Seasonal Influenza Vaccination Coverage—United States, August 2009–January 2010, MMWR Morb Mortal Wkly Rep 59 (16) (2010), pp. 477–484.
21 X. Dedoukou, G. Nikolopoulos, A. Maragos, S. Giannoulidou and H.C. Maltezou, Attitudes towards vaccination against seasonal influenza of health-care workers in primary health-care settings in Greece, Vaccine 28 (37) (2010), pp. 5931–5933. Article |
22 J.N. Kent, C.S. Lea, X. Fang, L.F. Novick and J. Morgan, Seasonal influenza vaccination coverage among local health department personnel in North Carolina, 2007–2008, Am J Prev Med 39 (1) (2010), pp. 74–77. Article |
23 M. Madjid, A. Alfred, A. Sahai, J.L. Conyers and S.W. Casscells, Factors contributing to suboptimal vaccination against influenza: results of a nationwide telephone survey of persons with cardiovascular disease, Tex Heart Inst J 36 (6) (2009), pp. 546–552. View Record in Scopus | Cited By in Scopus (5)
24 K.W. To, S. Lee, T.O. Chan and S.S. Lee, Exploring determinants of acceptance of the pandemic influenza A (H1N1) 2009 vaccination in nurses, Am J Infect Control 38 (8) (2010), pp. 623–630. Article |
25 S.D. Torun and F. Torun, Vaccination against pandemic influenza A/H1N1 among healthcare workers and reasons for refusing vaccination in Istanbul in last pandemic alert phase, Vaccine 28 (35) (2010), pp. 5703–5710. Article |
26 S. Vírseda, M.A. Restrepo, E. Arranz, P. Magán-Tapia, M. Fernández-Ruiz, A.G. de la Cámara, J.M. Aguado and F. López-Medrano, Seasonal and pandemic A (H1N1) 2009 influenza vaccination coverage and attitudes among health-care workers in a Spanish university hospital, Vaccine 28 (30) (2010), pp. 4751–4757. Article |
Appendix
Questionnaire
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
_________________________________________
5) If you are not planning to get the H1N1 vaccine, what best describes your reason for not getting vaccinated? Please circle one.
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
8) If you are not planning to get the seasonal flu vaccine, what best describes your reason for not getting vaccinated? Please circle one.
_____________________________________
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.
Original research
Benjamin H. Chin-Yeea, Katherine Monkman MDa, Zafar Hussain MD, FRCP(C)a and Leonard A. Minuk MD, FRCP(C)
Background
Patients with hematologic malignancies are at increased risk of influenza and its complications. Despite current health recommendations and evidence favoring influenza vaccination, vaccination rates remain low in cancer patients.
Objective
The purpose of this study was to determine which factors influenced vaccination rates.
Methods
During the 2009–2010 pandemic H1N1 and seasonal influenza season, we surveyed patients with hematologic malignancies in a Canadian cancer center. Of the patients participating in our study (n = 129), 66% and 57% received the H1N1 pandemic influenza and seasonal influenza vaccines, respectively.
Results
A number of reasons for vaccination refusal were reported, most relating to general skepticism about the safety and efficacy of vaccination. Physician advice was also a factor influencing vaccination rates in patients. The vaccination rate for seasonal influenza was 39% in patients <65 years old, significantly lower than the rate of 73% reported for patients aged ≥65 years (P < 0.0001).
Conclusion
Future education programs should target younger patient populations and health-care workers, focusing on vaccine safety and efficacy in the high-risk cancer population.
Despite the annual development of effective influenza vaccines, influenza remains a significant cause of morbidity and mortality in Canada. In the 2009–2010 influenza season, approximately 40,000 Canadians were infected with seasonal influenza or the pandemic H1N1 influenza virus,1 and influenza has been estimated to cause 4,000–8,000 deaths in Canada each year.2 It is estimated that a severe influenza pandemic could result in a 1% reduction in annual gross domestic product in Canada.3
Patients with hematologic malignancies are known to be at increased risk of influenza and its complications, with estimated mortality rates in the range 5%–27%.[4], [5], [6], [7] and [8] Evidence for the efficacy of the influenza vaccine is limited and contradictory, and many assume that immunocompromised patients will not be able to generate a protective antibody response. Nonetheless, current evidence favors vaccination.9 Pollyea et al10 reported that eight of 15 trials on the efficacy of vaccination in patients with hematologic malignancies concluded that vaccination was beneficial. Both the Centers for Disease Control and Prevention (CDC) and the Public Health Agency of Canada (PHAC) advised that all immunocompromised patients, including those with cancer, receive both the seasonal influenza vaccine and the pandemic H1N1 influenza vaccine in the 2009–2010 influenza season.[11] and [12]
Despite these recommendations, rates of influenza vaccination remain low for the general population and cancer patients in Canada, with rates reported at 40% and 65% respectively.[13] and [14] A recent study by Yee et al15 reported similarly low influenza vaccination rates of 58% in cancer patients in the United States. Vaccination has long been a controversial public health issue, and many people choose not to be vaccinated due to fears that vaccines may not be safe and effective.[16], [17] and [18] Lack of physician recommendation has also been cited as a significant factor in the decision to decline vaccination.16
In this study, we sought to determine what percentage of patients being treated for hematologic malignancies in an Ontario, Canada, cancer center received the H1N1 pandemic influenza vaccine in the 2009–2010 influenza season and to explore the barriers to vaccination in this high-risk population. We also collected information on the percentage of patients who received the seasonal influenza vaccine. It was general practice for physicians at this center to recommend influenza vaccination in accordance with the PHAC recommendations.
Methods
Patients being treated for hematologic malignancies at the London Regional Cancer Program (London, Canada) were invited to complete a survey regarding influenza vaccination (Appendix). The London Regional Cancer Program is a tertiary care center providing specialized cancer care to a population base of 1.2 million in southwestern Ontario. The survey was administered to patients eligible to participate in another study assessing antibody levels pre- and postvaccination with the H1N1 pandemic vaccine. Eligible patients were 18 years or older and being treated or followed for hematological malignancies at the London Regional Cancer Program who attended an appointment between October 28 and November 19, 2009, and returned for a follow-up visit between January 5 and March 26, 2010 (n = 151). Patients were asked if they had received the pandemic H1N1 influenza vaccine and the seasonal influenza vaccine during the 2009–2010 influenza season. Those who had declined vaccination were asked to describe the reasons for their choice. The survey provided a list of six possible reasons for declining vaccination and gave patients the option of writing in their own responses.
The results of the study were analyzed using InStat 3 software (GraphPad, La Jolla, CA). The Mann-Whitney U-test was used to compare continuous variables, and Fisher's exact test was used to compare proportions. The study was approved by the University of Western Ontario's Institutional Research Ethics Board (IRB 16627E).
Results
Of the 151 patients invited to participate, 129 completed the survey, yielding a response rate of 85%. Patient characteristics are shown in Table 1. The respondents ranged in age from 19 to 86 years, 56% were male and 44% were female, and patients aged 65 years or older comprised 52% of the study population. The mean age of the patient group was 62.7 ± 14.8 years. Overall 119 patients (92%) had received chemotherapy at some time during their illness, with 96 patients (76%) actively receiving chemotherapy, defined as treatment within the past 3 months. Diagnoses included acute leukemia, chronic lymphocytic leukemia, chronic myeloid leukemia, lymphoma, multiple myeloma, myelodysplastic syndromes, and myeloproliferative neoplasms.
Of the 129 patients surveyed, 85 (66%) reported that they had received the H1N1 pandemic influenza vaccine during the 2009–2010 influenza season. Fifty-seven percent had received the seasonal influenza vaccine, and 50% had received both the seasonal and the H1N1 vaccines. Of the 44 patients who did not receive the H1N1 vaccine, only three planned to receive it. Eight of the 56 patients not vaccinated with the seasonal influenza vaccine planned to receive it.
There were no significant differences in mean age, percentage of patients over 65 years old, gender, or chemotherapy status between patients who received the H1N1 vaccine and those who declined it (Table 1). The mean age of patients who received the seasonal influenza vaccine was significantly higher than that of those who did not (67.8 ±12.1 vs. 56.1 ± 15.5 years, P < 0.0001), and a significantly higher percentage of patients in the vaccinated group were over the age of 65 (67% vs. 33%, P < 0.0001).
Patient-reported reasons for not receiving the H1N1 vaccine are shown in Figure 1. The two most common reasons for declining vaccination were beliefs that “the vaccine is dangerous because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). The belief that vaccination was dangerous or not effective because of the patient's medical condition represented 16% and 12% of responses, respectively. Six percent responded that receiving the vaccine would have been too inconvenient. No patients reported concerns about pain at the injection site as a reason for avoiding vaccination. In the category of “other,” responses fell into four broad categories: “physician advised against vaccination” (8%), “vaccination is unnecessary” (8%), “previous bad experience from vaccine” (4%), and “vaccine will make me sick” (4%).
Discussion
Our study found that 66% of patients being treated for hematological malignancies at a southwestern Ontario cancer center received the H1N1 vaccine during the 2009–2010 influenza season. This was higher than the rate of H1N1 vaccination in the general Canadian population, which was reported as 41%.14 Canadian cancer patients have been previously shown to have higher rates of participation in vaccination programs. In 2005, 64% of Canadians with cancer received the seasonal influenza vaccine compared with 34% of the overall population.13 This trend may be driven in part by the higher average age of patients receiving cancer treatment as adults 65 years of age or older comprised 52% of the respondents in our study.
Worldwide, Canada ranks among the highest countries in vaccination coverage. The United Kingdom reported a vaccination rate of 28.7% during the 2007–2008 influenza season, which was at the time one of the highest in Europe.19 Other European countries, including Germany, Italy, and France, showed vaccination rates similar to that of the United Kingdom. In all of these countries vaccination coverage increased with age. The United States has vaccination rates most similar to those of Canada, estimated at 40% in the overall population and 68% in the population ≥65 years old during the 2009–2010 influenza season.20
Higher vaccination rates have been reported in the elderly compared to younger adult population,[13] and [14] and our findings prove to be consistent with this reported trend. In this study, the group vaccinated with the seasonal influenza vaccine had a mean age of 67.8 ± 12.1 years compared with the unvaccinated group aged 56.1 ± 15.5 years (P < 0.0001). Interestingly, there was no significant difference in mean age between the vaccinated and unvaccinated groups for the H1N1 pandemic influenza vaccine (P > 0.05). This was not entirely unexpected since public health campaigns during the 2009–2010 influenza season focused on the younger age group due to their increased susceptibility to severe H1N1 disease. Nonetheless, there was a trend toward an increased mean age for those who received the vaccine (64.0 ± 12.5 years) compared to those who did not (60.4 ± 18.4 years), and it is possible that statistical significance was not reached due to the small sample size. Our study reported an alarmingly low 39% vaccination rate for seasonal influenza in cancer patients <65, suggesting that the PHAC's message is not adequately reaching this potentially at-risk group.
Reasons for refusal of vaccination have been well described in previous studies.[16], [17], [18], [21], [22], [23], [24], [25] and [26] We found that the most common reasons for refusal of vaccination by cancer patients were very similar to those reported in healthy individuals. Specifically, concerns about the safety and efficacy of vaccines in general were more common than concerns related to cancer or chemotherapy. The most common reasons for refusal of vaccination were “I think the vaccine will be dangerous for people in general because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). Despite the publicity, 8% of unvaccinated patients responded that they did not feel that H1N1 influenza was a significant threat. In this study, the belief that the vaccine was dangerous because of lack of testing or a previous medical condition was responsible for 13% of patients not receiving the vaccine. Five percent of patients elected not to be vaccinated because of questions of efficacy. The H1N1 vaccine is an adjuvant with AsO3, which may cause more vaccine reactions, while the seasonal influenza vaccine is not an adjuvant. It is possible that the presence of adjuvant contributed to some patients' safety concerns, though we did not specifically ask if the adjuvant influenced their decision.
Physician advice may have played a significant role in patients' decisions to vaccinate. Eight percent of patients who did not receive the vaccine reported that they were not vaccinated due to advice from a physician. It is our routine institutional policy to recommend vaccination for all cancer patients irrespective of underlying diagnosis or treatment regimen. We do not, however, provide standardized written information to patients or referring physicians, so some patients may have been advised against vaccination by other physicians. Some primary care physicians might not have been familiar with the current PHAC recommendations or the recent literature suggesting the vaccine's potential benefits in this group. Public health campaigns should therefore seek to educate physicians as well as patients regarding the safety and efficacy of the influenza vaccine for cancer patients.
Conclusion
We found that rates of H1N1 and seasonal influenza vaccination in a southwestern Ontario cancer center were higher than those reported for the general population. Nevertheless, despite a large public health education campaign, a significant number of patients declined vaccination due to fear that it would not be safe or effective or due to a belief that vaccination was not necessary. Although the rate of seasonal influenza vaccination was high for those ≥65 years old, it was poor for those aged <65 years, despite vaccination being recommended for all adults with chronic medical conditions. Future education programs should target younger patient populations and health-care workers and focus on vaccine safety and efficacy in immunocompromised patients as well as in other high-risk groups.
References1
1 Public Health Agency of Canada, FluWatch http://www.phac-aspc.gc.ca/fluwatch/09-10/w28_10/index-eng.php Accessed August 5, 2010.
2 Public Health Agency of Canada, Influenza http://www.phac-aspc.gc.ca/influenza/index-eng.php Accessed August 5, 2010.
3 S. James and T. Sargent, The Economic Impact of an Influenza Pandemic, Department of Finance Canada, Ottawa (2006), p. 90.
4 R.F. Chemaly, S. Ghosh, G.P. Bodey, N. Rohatgi, A. Safdar, M.J. Keating, R.E. Champlin, E.A. Aguilera, J.J. Tarrand and I.I. Raad, Respiratory viral infections in adults with hematologic malignancies and human stem cell transplantation recipients: a retrospective study at a major cancer center, Medicine 85 (5) (2006), pp. 278–287. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (66)
5 H.M. Yousuf, J. Englund, R. Couch, K. Rolston, M. Luna, J. Goodrich, V. Lewis, N.Q. Mirza, M. Andreeff, C. Koller, L. Elting, G.P. Bodey and E. Whimbey, Influenza among hospitalized adults with leukemia, Clin Infect Dis 24 (6) (1997), pp. 1095–1099. View Record in Scopus | Cited By in Scopus (55)
6 C.D. Cooksley, E.B. Avritscher, B.N. Bekele, K.V. Rolston, J.M. Geraci and L.S. Elting, Epidemiology and outcomes of serious influenza-related infections in the cancer population, Cancer 104 (3) (2005), pp. 618–628. View Record in Scopus | Cited By in Scopus (24)
7 L.S. Elting, E. Whimbey, W. Lo, R. Couch, M. Andreeff and G.P. Bodey, Epidemiology of influenza A virus infection in patients with acute or chronic leukemia, Support Care Cancer 3 (3) (1995), pp. 198–202. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (32)
8 E. Whimbey, L.S. Elting, R.B. Couch, W. Lo, L. Williams, R.E. Champlin and G.P. Bodey, Influenza A virus infections among hospitalized adult bone marrow transplant recipients, Bone Marrow Transplant 13 (4) (1994), pp. 437–440. View Record in Scopus | Cited By in Scopus (110)
9 M. Tiseo, B. Calatafimi, L. Ferri, A. Menardi and A. Ardizzoni, Efficacy and safety of influenza vaccination during chemotherapy treatment, J Support Oncol 8 (6) (2010), pp. 271–272. Article |
10 D.A. Pollyea, J.M. Brown and S.J. Horning, Utility of influenza vaccination for oncology patients, J Clin Oncol 28 (14) (2010), pp. 2481–2490. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (8)
11 Public Health Agency of Canada, Guidance Document on the Use of Pandemic Influenza A (H1N1) 2009: Inactivated Monovalent Vaccine, Public Health Agency of Canada, Ottawa (2009).
12 Centers for Disease Control, 2009 H1N1 Vaccination Recommendations http://www.cdc.gov/h1n1flu/vaccination/acip.htm Accessed August 5, 2010.
13 J.C. Kwong, L.C. Rosella and H. Johansen, Trends in influenza vaccination in Canada, 1996/1997 to 2005, Health Rep 18 (4) (2007), pp. 9–19. View Record in Scopus | Cited By in Scopus (14)
14 Statistics Canda, Canadian Community Health Survey: H1N1 Vaccinations http://www.statcan.gc.ca/daily-quotidien/100719/dq100719b-eng.htm Accessed August 5, 2010.
15 S.S. Yee, P.R. Dutta, L.J. Solin, N. Vapiwala and G.D. Kao, Lack of compliance with national vaccination guidelines in oncology patients receiving radiation therapy, J Support Oncol 8 (1) (2010), pp. 28–34. View Record in Scopus | Cited By in Scopus (2)
16 P. Loulergue, O. Mir, J. Alexandre, S. Ropert, F. Goldwasser and O. Launay, Low influenza vaccination rate among patients receiving chemotherapy for cancer, Ann Oncol 19 (9) (2008), p. 1658. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (10)
17 R.K. Zimmerman, T.A. Santibanez, J.E. Janosky, M.J. Fine, M. Raymund, S.A. Wilson, I.J. Bardella, A.R. Medsger and M.P. Nowalk, What affects influenza vaccination rates among older patients?: An analysis from inner-city, suburban, rural, and Veterans Affairs practices, Am J Med 114 (1) (2003), pp. 31–38. Article |
18 M.W. Mah, N.A. Hagen, K. Pauling-Shepard, J.S. Hawthorne, M. Mysak, T. Lye and T.J. Louie, Understanding influenza vaccination attitudes at a Canadian cancer center, Am J Infect Control 33 (4) (2005), pp. 243–250. Article |
19 P.R. Blank, M. Schwenkglenks and T.D. Szucs, Vaccination coverage rates in eleven European countries during two consecutive influenza seasons, J Infect 58 (6) (2009), pp. 446–458. Article |
20 Centers for Disease Control and Prevention, Interim Results: State-Specific Seasonal Influenza Vaccination Coverage—United States, August 2009–January 2010, MMWR Morb Mortal Wkly Rep 59 (16) (2010), pp. 477–484.
21 X. Dedoukou, G. Nikolopoulos, A. Maragos, S. Giannoulidou and H.C. Maltezou, Attitudes towards vaccination against seasonal influenza of health-care workers in primary health-care settings in Greece, Vaccine 28 (37) (2010), pp. 5931–5933. Article |
22 J.N. Kent, C.S. Lea, X. Fang, L.F. Novick and J. Morgan, Seasonal influenza vaccination coverage among local health department personnel in North Carolina, 2007–2008, Am J Prev Med 39 (1) (2010), pp. 74–77. Article |
23 M. Madjid, A. Alfred, A. Sahai, J.L. Conyers and S.W. Casscells, Factors contributing to suboptimal vaccination against influenza: results of a nationwide telephone survey of persons with cardiovascular disease, Tex Heart Inst J 36 (6) (2009), pp. 546–552. View Record in Scopus | Cited By in Scopus (5)
24 K.W. To, S. Lee, T.O. Chan and S.S. Lee, Exploring determinants of acceptance of the pandemic influenza A (H1N1) 2009 vaccination in nurses, Am J Infect Control 38 (8) (2010), pp. 623–630. Article |
25 S.D. Torun and F. Torun, Vaccination against pandemic influenza A/H1N1 among healthcare workers and reasons for refusing vaccination in Istanbul in last pandemic alert phase, Vaccine 28 (35) (2010), pp. 5703–5710. Article |
26 S. Vírseda, M.A. Restrepo, E. Arranz, P. Magán-Tapia, M. Fernández-Ruiz, A.G. de la Cámara, J.M. Aguado and F. López-Medrano, Seasonal and pandemic A (H1N1) 2009 influenza vaccination coverage and attitudes among health-care workers in a Spanish university hospital, Vaccine 28 (30) (2010), pp. 4751–4757. Article |
Appendix
Questionnaire
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
_________________________________________
5) If you are not planning to get the H1N1 vaccine, what best describes your reason for not getting vaccinated? Please circle one.
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
8) If you are not planning to get the seasonal flu vaccine, what best describes your reason for not getting vaccinated? Please circle one.
_____________________________________
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.
Original research
Benjamin H. Chin-Yeea, Katherine Monkman MDa, Zafar Hussain MD, FRCP(C)a and Leonard A. Minuk MD, FRCP(C)
Background
Patients with hematologic malignancies are at increased risk of influenza and its complications. Despite current health recommendations and evidence favoring influenza vaccination, vaccination rates remain low in cancer patients.
Objective
The purpose of this study was to determine which factors influenced vaccination rates.
Methods
During the 2009–2010 pandemic H1N1 and seasonal influenza season, we surveyed patients with hematologic malignancies in a Canadian cancer center. Of the patients participating in our study (n = 129), 66% and 57% received the H1N1 pandemic influenza and seasonal influenza vaccines, respectively.
Results
A number of reasons for vaccination refusal were reported, most relating to general skepticism about the safety and efficacy of vaccination. Physician advice was also a factor influencing vaccination rates in patients. The vaccination rate for seasonal influenza was 39% in patients <65 years old, significantly lower than the rate of 73% reported for patients aged ≥65 years (P < 0.0001).
Conclusion
Future education programs should target younger patient populations and health-care workers, focusing on vaccine safety and efficacy in the high-risk cancer population.
Despite the annual development of effective influenza vaccines, influenza remains a significant cause of morbidity and mortality in Canada. In the 2009–2010 influenza season, approximately 40,000 Canadians were infected with seasonal influenza or the pandemic H1N1 influenza virus,1 and influenza has been estimated to cause 4,000–8,000 deaths in Canada each year.2 It is estimated that a severe influenza pandemic could result in a 1% reduction in annual gross domestic product in Canada.3
Patients with hematologic malignancies are known to be at increased risk of influenza and its complications, with estimated mortality rates in the range 5%–27%.[4], [5], [6], [7] and [8] Evidence for the efficacy of the influenza vaccine is limited and contradictory, and many assume that immunocompromised patients will not be able to generate a protective antibody response. Nonetheless, current evidence favors vaccination.9 Pollyea et al10 reported that eight of 15 trials on the efficacy of vaccination in patients with hematologic malignancies concluded that vaccination was beneficial. Both the Centers for Disease Control and Prevention (CDC) and the Public Health Agency of Canada (PHAC) advised that all immunocompromised patients, including those with cancer, receive both the seasonal influenza vaccine and the pandemic H1N1 influenza vaccine in the 2009–2010 influenza season.[11] and [12]
Despite these recommendations, rates of influenza vaccination remain low for the general population and cancer patients in Canada, with rates reported at 40% and 65% respectively.[13] and [14] A recent study by Yee et al15 reported similarly low influenza vaccination rates of 58% in cancer patients in the United States. Vaccination has long been a controversial public health issue, and many people choose not to be vaccinated due to fears that vaccines may not be safe and effective.[16], [17] and [18] Lack of physician recommendation has also been cited as a significant factor in the decision to decline vaccination.16
In this study, we sought to determine what percentage of patients being treated for hematologic malignancies in an Ontario, Canada, cancer center received the H1N1 pandemic influenza vaccine in the 2009–2010 influenza season and to explore the barriers to vaccination in this high-risk population. We also collected information on the percentage of patients who received the seasonal influenza vaccine. It was general practice for physicians at this center to recommend influenza vaccination in accordance with the PHAC recommendations.
Methods
Patients being treated for hematologic malignancies at the London Regional Cancer Program (London, Canada) were invited to complete a survey regarding influenza vaccination (Appendix). The London Regional Cancer Program is a tertiary care center providing specialized cancer care to a population base of 1.2 million in southwestern Ontario. The survey was administered to patients eligible to participate in another study assessing antibody levels pre- and postvaccination with the H1N1 pandemic vaccine. Eligible patients were 18 years or older and being treated or followed for hematological malignancies at the London Regional Cancer Program who attended an appointment between October 28 and November 19, 2009, and returned for a follow-up visit between January 5 and March 26, 2010 (n = 151). Patients were asked if they had received the pandemic H1N1 influenza vaccine and the seasonal influenza vaccine during the 2009–2010 influenza season. Those who had declined vaccination were asked to describe the reasons for their choice. The survey provided a list of six possible reasons for declining vaccination and gave patients the option of writing in their own responses.
The results of the study were analyzed using InStat 3 software (GraphPad, La Jolla, CA). The Mann-Whitney U-test was used to compare continuous variables, and Fisher's exact test was used to compare proportions. The study was approved by the University of Western Ontario's Institutional Research Ethics Board (IRB 16627E).
Results
Of the 151 patients invited to participate, 129 completed the survey, yielding a response rate of 85%. Patient characteristics are shown in Table 1. The respondents ranged in age from 19 to 86 years, 56% were male and 44% were female, and patients aged 65 years or older comprised 52% of the study population. The mean age of the patient group was 62.7 ± 14.8 years. Overall 119 patients (92%) had received chemotherapy at some time during their illness, with 96 patients (76%) actively receiving chemotherapy, defined as treatment within the past 3 months. Diagnoses included acute leukemia, chronic lymphocytic leukemia, chronic myeloid leukemia, lymphoma, multiple myeloma, myelodysplastic syndromes, and myeloproliferative neoplasms.
Of the 129 patients surveyed, 85 (66%) reported that they had received the H1N1 pandemic influenza vaccine during the 2009–2010 influenza season. Fifty-seven percent had received the seasonal influenza vaccine, and 50% had received both the seasonal and the H1N1 vaccines. Of the 44 patients who did not receive the H1N1 vaccine, only three planned to receive it. Eight of the 56 patients not vaccinated with the seasonal influenza vaccine planned to receive it.
There were no significant differences in mean age, percentage of patients over 65 years old, gender, or chemotherapy status between patients who received the H1N1 vaccine and those who declined it (Table 1). The mean age of patients who received the seasonal influenza vaccine was significantly higher than that of those who did not (67.8 ±12.1 vs. 56.1 ± 15.5 years, P < 0.0001), and a significantly higher percentage of patients in the vaccinated group were over the age of 65 (67% vs. 33%, P < 0.0001).
Patient-reported reasons for not receiving the H1N1 vaccine are shown in Figure 1. The two most common reasons for declining vaccination were beliefs that “the vaccine is dangerous because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). The belief that vaccination was dangerous or not effective because of the patient's medical condition represented 16% and 12% of responses, respectively. Six percent responded that receiving the vaccine would have been too inconvenient. No patients reported concerns about pain at the injection site as a reason for avoiding vaccination. In the category of “other,” responses fell into four broad categories: “physician advised against vaccination” (8%), “vaccination is unnecessary” (8%), “previous bad experience from vaccine” (4%), and “vaccine will make me sick” (4%).
Discussion
Our study found that 66% of patients being treated for hematological malignancies at a southwestern Ontario cancer center received the H1N1 vaccine during the 2009–2010 influenza season. This was higher than the rate of H1N1 vaccination in the general Canadian population, which was reported as 41%.14 Canadian cancer patients have been previously shown to have higher rates of participation in vaccination programs. In 2005, 64% of Canadians with cancer received the seasonal influenza vaccine compared with 34% of the overall population.13 This trend may be driven in part by the higher average age of patients receiving cancer treatment as adults 65 years of age or older comprised 52% of the respondents in our study.
Worldwide, Canada ranks among the highest countries in vaccination coverage. The United Kingdom reported a vaccination rate of 28.7% during the 2007–2008 influenza season, which was at the time one of the highest in Europe.19 Other European countries, including Germany, Italy, and France, showed vaccination rates similar to that of the United Kingdom. In all of these countries vaccination coverage increased with age. The United States has vaccination rates most similar to those of Canada, estimated at 40% in the overall population and 68% in the population ≥65 years old during the 2009–2010 influenza season.20
Higher vaccination rates have been reported in the elderly compared to younger adult population,[13] and [14] and our findings prove to be consistent with this reported trend. In this study, the group vaccinated with the seasonal influenza vaccine had a mean age of 67.8 ± 12.1 years compared with the unvaccinated group aged 56.1 ± 15.5 years (P < 0.0001). Interestingly, there was no significant difference in mean age between the vaccinated and unvaccinated groups for the H1N1 pandemic influenza vaccine (P > 0.05). This was not entirely unexpected since public health campaigns during the 2009–2010 influenza season focused on the younger age group due to their increased susceptibility to severe H1N1 disease. Nonetheless, there was a trend toward an increased mean age for those who received the vaccine (64.0 ± 12.5 years) compared to those who did not (60.4 ± 18.4 years), and it is possible that statistical significance was not reached due to the small sample size. Our study reported an alarmingly low 39% vaccination rate for seasonal influenza in cancer patients <65, suggesting that the PHAC's message is not adequately reaching this potentially at-risk group.
Reasons for refusal of vaccination have been well described in previous studies.[16], [17], [18], [21], [22], [23], [24], [25] and [26] We found that the most common reasons for refusal of vaccination by cancer patients were very similar to those reported in healthy individuals. Specifically, concerns about the safety and efficacy of vaccines in general were more common than concerns related to cancer or chemotherapy. The most common reasons for refusal of vaccination were “I think the vaccine will be dangerous for people in general because of lack of testing” (22%) and “I don't believe in vaccination in general” (18%). Despite the publicity, 8% of unvaccinated patients responded that they did not feel that H1N1 influenza was a significant threat. In this study, the belief that the vaccine was dangerous because of lack of testing or a previous medical condition was responsible for 13% of patients not receiving the vaccine. Five percent of patients elected not to be vaccinated because of questions of efficacy. The H1N1 vaccine is an adjuvant with AsO3, which may cause more vaccine reactions, while the seasonal influenza vaccine is not an adjuvant. It is possible that the presence of adjuvant contributed to some patients' safety concerns, though we did not specifically ask if the adjuvant influenced their decision.
Physician advice may have played a significant role in patients' decisions to vaccinate. Eight percent of patients who did not receive the vaccine reported that they were not vaccinated due to advice from a physician. It is our routine institutional policy to recommend vaccination for all cancer patients irrespective of underlying diagnosis or treatment regimen. We do not, however, provide standardized written information to patients or referring physicians, so some patients may have been advised against vaccination by other physicians. Some primary care physicians might not have been familiar with the current PHAC recommendations or the recent literature suggesting the vaccine's potential benefits in this group. Public health campaigns should therefore seek to educate physicians as well as patients regarding the safety and efficacy of the influenza vaccine for cancer patients.
Conclusion
We found that rates of H1N1 and seasonal influenza vaccination in a southwestern Ontario cancer center were higher than those reported for the general population. Nevertheless, despite a large public health education campaign, a significant number of patients declined vaccination due to fear that it would not be safe or effective or due to a belief that vaccination was not necessary. Although the rate of seasonal influenza vaccination was high for those ≥65 years old, it was poor for those aged <65 years, despite vaccination being recommended for all adults with chronic medical conditions. Future education programs should target younger patient populations and health-care workers and focus on vaccine safety and efficacy in immunocompromised patients as well as in other high-risk groups.
References1
1 Public Health Agency of Canada, FluWatch http://www.phac-aspc.gc.ca/fluwatch/09-10/w28_10/index-eng.php Accessed August 5, 2010.
2 Public Health Agency of Canada, Influenza http://www.phac-aspc.gc.ca/influenza/index-eng.php Accessed August 5, 2010.
3 S. James and T. Sargent, The Economic Impact of an Influenza Pandemic, Department of Finance Canada, Ottawa (2006), p. 90.
4 R.F. Chemaly, S. Ghosh, G.P. Bodey, N. Rohatgi, A. Safdar, M.J. Keating, R.E. Champlin, E.A. Aguilera, J.J. Tarrand and I.I. Raad, Respiratory viral infections in adults with hematologic malignancies and human stem cell transplantation recipients: a retrospective study at a major cancer center, Medicine 85 (5) (2006), pp. 278–287. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (66)
5 H.M. Yousuf, J. Englund, R. Couch, K. Rolston, M. Luna, J. Goodrich, V. Lewis, N.Q. Mirza, M. Andreeff, C. Koller, L. Elting, G.P. Bodey and E. Whimbey, Influenza among hospitalized adults with leukemia, Clin Infect Dis 24 (6) (1997), pp. 1095–1099. View Record in Scopus | Cited By in Scopus (55)
6 C.D. Cooksley, E.B. Avritscher, B.N. Bekele, K.V. Rolston, J.M. Geraci and L.S. Elting, Epidemiology and outcomes of serious influenza-related infections in the cancer population, Cancer 104 (3) (2005), pp. 618–628. View Record in Scopus | Cited By in Scopus (24)
7 L.S. Elting, E. Whimbey, W. Lo, R. Couch, M. Andreeff and G.P. Bodey, Epidemiology of influenza A virus infection in patients with acute or chronic leukemia, Support Care Cancer 3 (3) (1995), pp. 198–202. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (32)
8 E. Whimbey, L.S. Elting, R.B. Couch, W. Lo, L. Williams, R.E. Champlin and G.P. Bodey, Influenza A virus infections among hospitalized adult bone marrow transplant recipients, Bone Marrow Transplant 13 (4) (1994), pp. 437–440. View Record in Scopus | Cited By in Scopus (110)
9 M. Tiseo, B. Calatafimi, L. Ferri, A. Menardi and A. Ardizzoni, Efficacy and safety of influenza vaccination during chemotherapy treatment, J Support Oncol 8 (6) (2010), pp. 271–272. Article |
10 D.A. Pollyea, J.M. Brown and S.J. Horning, Utility of influenza vaccination for oncology patients, J Clin Oncol 28 (14) (2010), pp. 2481–2490. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (8)
11 Public Health Agency of Canada, Guidance Document on the Use of Pandemic Influenza A (H1N1) 2009: Inactivated Monovalent Vaccine, Public Health Agency of Canada, Ottawa (2009).
12 Centers for Disease Control, 2009 H1N1 Vaccination Recommendations http://www.cdc.gov/h1n1flu/vaccination/acip.htm Accessed August 5, 2010.
13 J.C. Kwong, L.C. Rosella and H. Johansen, Trends in influenza vaccination in Canada, 1996/1997 to 2005, Health Rep 18 (4) (2007), pp. 9–19. View Record in Scopus | Cited By in Scopus (14)
14 Statistics Canda, Canadian Community Health Survey: H1N1 Vaccinations http://www.statcan.gc.ca/daily-quotidien/100719/dq100719b-eng.htm Accessed August 5, 2010.
15 S.S. Yee, P.R. Dutta, L.J. Solin, N. Vapiwala and G.D. Kao, Lack of compliance with national vaccination guidelines in oncology patients receiving radiation therapy, J Support Oncol 8 (1) (2010), pp. 28–34. View Record in Scopus | Cited By in Scopus (2)
16 P. Loulergue, O. Mir, J. Alexandre, S. Ropert, F. Goldwasser and O. Launay, Low influenza vaccination rate among patients receiving chemotherapy for cancer, Ann Oncol 19 (9) (2008), p. 1658. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (10)
17 R.K. Zimmerman, T.A. Santibanez, J.E. Janosky, M.J. Fine, M. Raymund, S.A. Wilson, I.J. Bardella, A.R. Medsger and M.P. Nowalk, What affects influenza vaccination rates among older patients?: An analysis from inner-city, suburban, rural, and Veterans Affairs practices, Am J Med 114 (1) (2003), pp. 31–38. Article |
18 M.W. Mah, N.A. Hagen, K. Pauling-Shepard, J.S. Hawthorne, M. Mysak, T. Lye and T.J. Louie, Understanding influenza vaccination attitudes at a Canadian cancer center, Am J Infect Control 33 (4) (2005), pp. 243–250. Article |
19 P.R. Blank, M. Schwenkglenks and T.D. Szucs, Vaccination coverage rates in eleven European countries during two consecutive influenza seasons, J Infect 58 (6) (2009), pp. 446–458. Article |
20 Centers for Disease Control and Prevention, Interim Results: State-Specific Seasonal Influenza Vaccination Coverage—United States, August 2009–January 2010, MMWR Morb Mortal Wkly Rep 59 (16) (2010), pp. 477–484.
21 X. Dedoukou, G. Nikolopoulos, A. Maragos, S. Giannoulidou and H.C. Maltezou, Attitudes towards vaccination against seasonal influenza of health-care workers in primary health-care settings in Greece, Vaccine 28 (37) (2010), pp. 5931–5933. Article |
22 J.N. Kent, C.S. Lea, X. Fang, L.F. Novick and J. Morgan, Seasonal influenza vaccination coverage among local health department personnel in North Carolina, 2007–2008, Am J Prev Med 39 (1) (2010), pp. 74–77. Article |
23 M. Madjid, A. Alfred, A. Sahai, J.L. Conyers and S.W. Casscells, Factors contributing to suboptimal vaccination against influenza: results of a nationwide telephone survey of persons with cardiovascular disease, Tex Heart Inst J 36 (6) (2009), pp. 546–552. View Record in Scopus | Cited By in Scopus (5)
24 K.W. To, S. Lee, T.O. Chan and S.S. Lee, Exploring determinants of acceptance of the pandemic influenza A (H1N1) 2009 vaccination in nurses, Am J Infect Control 38 (8) (2010), pp. 623–630. Article |
25 S.D. Torun and F. Torun, Vaccination against pandemic influenza A/H1N1 among healthcare workers and reasons for refusing vaccination in Istanbul in last pandemic alert phase, Vaccine 28 (35) (2010), pp. 5703–5710. Article |
26 S. Vírseda, M.A. Restrepo, E. Arranz, P. Magán-Tapia, M. Fernández-Ruiz, A.G. de la Cámara, J.M. Aguado and F. López-Medrano, Seasonal and pandemic A (H1N1) 2009 influenza vaccination coverage and attitudes among health-care workers in a Spanish university hospital, Vaccine 28 (30) (2010), pp. 4751–4757. Article |
Appendix
Questionnaire
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
_________________________________________
5) If you are not planning to get the H1N1 vaccine, what best describes your reason for not getting vaccinated? Please circle one.
- a) I do not think it will be effective for me because of my medical condition
b) I am concerned it might be dangerous for me because of my medical condition
c) I am concerned it might be dangerous for people in general because not enough testing has been done
d) Receiving the vaccination would be too inconvenient (long lineups, etc.)
8) If you are not planning to get the seasonal flu vaccine, what best describes your reason for not getting vaccinated? Please circle one.
_____________________________________
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.