infection control & hospital epidemiology
october 2015, vol. 36, no. 10
concise communication
Influenza Vaccination in Patients With Cancer: Factors Associated With Vaccination Practices for Patients and Their Household Members Ella J. Ariza-Heredia, MD; Jacques Azzi, MD; Dimpy P. Shah, MD, PhD; Lior Nesher, MD; Shashank S. Ghantoji, MD; Lamprinos Michailidis, MD; Lisa Marsh, RN; Roy F. Chemaly, MD, MPH, FACP, FIDSA
Presented in part: IDWeek 2014; Philadelphia, PA; October 8-12, 2014 (Poster 1120). Infect. Control Hosp. Epidemiol. 2 01 5 ;3 6( 10 ): 1 23 9 –1 2 41
Influenza infection causes serious illness and death in patients with cancer. However, immunization with annual flu vaccine is low. We demonstrated that a recommendation by the patient’s oncologist was the strongest predictor of vaccination not only for patients but also for their households, underscoring the importance of a well-informed provider. Patients with cancer experience greater morbidity and mortality of influenza infections than the general population.1 Annual inactivated influenza vaccination is recommended for immunocompromised patients who are at least 6 months old and for their family members by the Centers for Disease Control and Prevention and the Infectious Diseases Society of America.2 Unfortunately, low vaccination coverage (9%–40%) has been reported in patients with cancer and stem cell transplant.3,4 With the aim of understanding the barriers that prevent wide vaccination uptake among cancer patients and their household, we evaluated the influenza vaccination practices at a tertiary cancer center.
m e th o d s Patients 18 years or older who had influenza infection confirmed in our microbiology laboratory were contacted by telephone and asked to provide verbal consent to participate in this observational study. In addition, a waiver of consent to obtain available data from the patients’ medical records in case the patient and/or a designated person could not be contacted in 2 different attempts was requested. The study was approved by our institutional review board. The telephone survey included questions about the influenza vaccine, whether the vaccine was recommended by their provider, the main reason for the patient not receiving the vaccine when that was the case, household members’ vaccination status,
and the reasons for household members not undergoing vaccination when that was the case (Online Appendix A). Demographic information, including age, sex, race, spoken language, marital status, type of insurance, religion, previous influenza vaccination, and place of residency (urban versus rural), was obtained. Data on vaccine eligibility for the nonvaccinated patients according to guidelines,2,5 type and status of malignancy, stem-cell transplant, comorbidities, received chemotherapy, clinical variables, treatment, and outcomes were also collected. The influenza vaccination status of the patients and household members represented the main predictive variable in this study. Descriptive statistics were used to summarize the demographic and clinical characteristics of participants. A bivariate analysis was conducted to compare factors predictive of vaccination in the vaccinated and nonvaccinated participants. These characteristics were compared using a χ2 test or Fisher exact test for categorical variables and t test or Wilcoxon rank sum test for continuous variables to identify their associations with outcome. Univariable and multivariable logistic regression analyses were used to calculate the odds ratios and 95% CIs for the effect of the patient and household member vaccination status on the outcomes of interest. A 2-sided P level of .05 was considered statistically significant.
resul ts We identified 154 eligible patients with laboratory-confirmed influenza. One hundred eight patients consented verbally to participate in the survey, for a response rate of 70%. We also included vaccination rates in 12 patients from medical records. The survey showed that 52 (43%) of the 120 patients received the flu vaccine, and 64 (53%) did not. Four patients (3%) did not remember whether they had undergone vaccination, and they were excluded from the analysis. We determined that 39 patients (61%) of the nonvaccinated patients had been eligible to receive the influenza vaccine by current recommendations.2,5 Recommendation by a healthcare provider was the strongest predictor of vaccination. Patients whose oncologists recommended the vaccine were more likely to have been vaccinated than were those who did not receive such recommendation (crude odds ratio, 6.96 [95% CI, 2.92-16.55]; P < .001). Furthermore, age older than 50 years was also a significant predictor of vaccination (crude odds ratio, 2.39 [95% CI, 1.09–5.25]; P = .029) (Table 1). In terms of sociodemographic factors, we describe a trend of more frequent vaccination in white and Asian patients than in Hispanic and African Americans patients, although it was not statistically significant (P = .19). There was no association between vaccination status and the other demographic and clinical variables (Table 1). Of the 64 patients who did not receive the influenza vaccine and who responded to our survey, the main reason cited for
1240 infection control & hospital epidemiology
table 1.
october 2015, vol. 36, no. 10
Influenza Vaccination Status in Patients with Cancer: Characteristics y and Underlying Medical Conditions
Characteristic Median age at flu diagnosis ≤ 50 years > 50 years Sex Male Female Race/ethnicity White Black Hispanic Asian Smoking statusa Never Former/Current Underlying condition Hematological malignancy Solid tumor HCT Cancer statusb Active Remission Physician recommendation of vaccinationc No Yes
Unvaccinated (N = 64)
Vaccinated (N = 52)
Crude odds ratio for receiving vaccination (95% CI)
P value
30 (47) 34 (53)
14 (27) 38 (73)
1 [Reference] 2.39 (1.09–5.25)
.029
41 (64) 23 (36)
30 (58) 22 (42)
1 [Reference] 1.31 (0.62–2.77)
.484
34 (53) 12 (19) 15 (23) 3 (5)
33 (63) 5 (10) 6 (12) 8 (15)
1 [Reference] 0.43 (0.14–1.35) 0.41 (0.14–1.19) 2.75 (0.67–11.26)
.149 .102 .160
36 (56) 27 (42)
35 (67) 16 (31)
1 [Reference] 0.61 (0.28–1.32)
.21
20 (31) 12 (19) 32 (50)
13 (25) 8 (15) 31(60)
1 [Reference] 1.03 (0.33–3.19) 1.49 (0.63–3.51)
.965 .361
43 (67) 20 (31)
29 (56) 21 (40)
1 [Reference] 1.56 (0.72–3.37)
.261
43 (67) 17 (27)
12 (23) 33 (63)
1 [Reference] 6.96 (2.92–16.55)
< .001
NOTE. Data are no. (%) of patients unless otherwise indicated. HCT, hematopoietic stem cell transplantation. Bold indicates statistically significant values (p < .005). a Data was available for 114 patients for smoking status. b Data was available for 113 patients for cancer status. c Data was available for 105 patients for physician recommendations.
nonvaccination was the recommendation against it by the patient’s oncologist (56 [88%]). Information on influenza vaccination of household members for 88 patients was analyzed. Full household vaccination occurred in 38 (43%) of the households. A healthcare provider’s recommendation against vaccination was also among the most common reasons behind the lack of vaccination (Figure 1). Notably, 16 household members (18%) had flu-like illness around the time patients were diagnosed with influenza infection. Vaccination status did not have a significant effect on hospital admission, progression to pneumonia, or mortality. In multivariable analysis, patients who experienced progression to pneumonia were more likely to be neutropenic, to be older, and to have not received oseltamivir early in the course (all, P < .05)
d is c u s s i o n
figure 1. Primary reasons for not undergoing influenza vaccination. A, Patients’ answers; B, Household members’ answers.
Vaccination as a public health intervention has been shown to lessen or eliminate the burden of many infectious diseases. Proper understanding of the barriers to appropriate influenza vaccination coverage is essential for designing future improvement strategies to increase compliance.6 Therefore,
influenza vaccine in cancer patients
we sought to determine factors associated with decisions regarding influenza vaccination in a cohort of cancer patients diagnosed with influenza and their household members. In our cohort, healthcare provider’s recommendation was the most significant determining factor for immunization for the patients. Literature on influenza vaccination in general population and other immunocompromised populations7 supports the importance of the role of the physician in vaccination decisions, and this is not an exception in oncological patients, resulting in our study in an approximately 7-fold greater likelihood of vaccination when patients receive a recommendations by their provider. Furthermore, 61% of the nonvaccinated patients met criteria for vaccination, underscoring how providers should be well informed of current recommendations and the benefits of influenza vaccination in patients with cancer. This study also highlights the unrecognized effect of the oncologists’ recommendations on household vaccination. Because immunocompromised patients are at greater risk for complications from influenza than the general population, providing an indirect protective effect via herd immunity (cocooning) by vaccination of family members becomes a crucial aspect of reducing their risk of infection.8 Furthermore, we found that patients older than 50 years were more likely to have received the influenza vaccine than were younger patients, probably related to the perception of being at higher risk of complications at older age. Different from other studies, concerns about vaccine side effects or effectiveness were not identified as significant barriers to vaccination in patients with cancer.9,10 Lastly, the lack of protection of the influenza vaccine on severity of illness in this specific cohort of patients should be interpreted with caution owing to the design of our study that identified only patients who had influenza infection, which systematically underestimates the effectiveness of the vaccine. Our study had a number of limitations because this was a single-institution study of patients with influenza, which may limit the generalizability of the results. In addition, we had to rely on patient reports to obtain data on the recommendations for influenza vaccination. Such reports are subject to patients’ interpretation of physician recommendations. In conclusion, physician attitudes and recommendations play major roles in the influenza vaccination decisions of cancer patients and their household members. One targeted intervention should be to strengthen the recommendation of physicians, especially oncologists, encouraging their participation in promoting influenza vaccination of both patients and their family members.
a ck n ow le d g m e n t s We acknowledge Michael Worley, Scientific Publications, and especially our patients at MD Anderson Cancer Center who were willing to participate in our survey. Financial support. None reported.
1241
Potential conflicts of interest. R. F. C. reports that he has received research funding from Gilead, GlaxoSmithKline, ADMA Biologics, Ansun Biopharma, and Roche. All other authors report no conflicts of interest relevant to this article. Affiliation: Department of Infectious Diseases, Infection Control and Employee Health, University of Texas MD Anderson Cancer Center, Houston, Texas. Address correspondence to Ella J. Ariza-Heredia, MD, Department of Infectious Diseases, Infection Control and Employee Health, Unit 1460, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030 ([email protected]). Received April 23, 2015; accepted: June 1, 2015; electronically published July 1, 2015 © 2015 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2015/3610-0017. DOI: 10.1017/ice.2015.150
supplementary materials To view Supplementary Materials for this article, please visit http://dx.doi.org/10.1017/ice.2015.150
ref e ren ces 1. Kunisaki KM, Janoff EN. Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 2009;9: 493–504. 2. Rubin LG, Levin MJ, Ljungman P, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis 2014;58 309–318. 3. Pedrazzoli P, Baldanti F, Donatelli I, et al. Vaccination for seasonal influenza in patients with cancer: recommendations of the Italian Society of Medical Oncology (AIOM). Ann Oncol 2014;25:1243–1247. 4. Ariza-Heredia EJ, Gulbis AM, Stolar KR, et al. Vaccination guidelines after hematopoietic stem cell transplantation: practitioners’ knowledge, attitudes, and gap between guidelines and clinical practice. Transpl Infect Dis 2014;16:878–886. 5. Fiore AE, Shay DK, Broder K, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) 2008 MMWR Recomm Rep 2008;57:1–60. 6. Dexter LJ, Teare MD, Dexter M, Siriwardena AN, Read RC. Strategies to increase influenza vaccination rates: outcomes of a nationwide cross-sectional survey of UK general practice. BMJ Open 2012:2 pii:e000851. 7. Loulergue P, Mir O, Alexandre J, Ropert S, Goldwasser F, Launay O. Low influenza vaccination rate among patients receiving chemotherapy for cancer. Ann Oncol 2008;19:1658. 8. Fine P, Eames K, Heymann DL. “Herd immunity”: a rough guide. Clin Infect Dis 2011;52:911–916. 9. Zimmerman RK, Santibanez TA, Janosky JE, et al. What affects influenza vaccination rates among older patients? An analysis from inner-city, suburban, rural, and Veterans Affairs practices. Am J Med 2003;114:31–38. 10. Earle CC. Influenza vaccination in elderly patients with advanced colorectal cancer. J Clin Oncol 2003;21:1161–1166.
october 2015, vol. 36, no. 10
concise communication
Influenza Vaccination in Patients With Cancer: Factors Associated With Vaccination Practices for Patients and Their Household Members Ella J. Ariza-Heredia, MD; Jacques Azzi, MD; Dimpy P. Shah, MD, PhD; Lior Nesher, MD; Shashank S. Ghantoji, MD; Lamprinos Michailidis, MD; Lisa Marsh, RN; Roy F. Chemaly, MD, MPH, FACP, FIDSA
Presented in part: IDWeek 2014; Philadelphia, PA; October 8-12, 2014 (Poster 1120). Infect. Control Hosp. Epidemiol. 2 01 5 ;3 6( 10 ): 1 23 9 –1 2 41
Influenza infection causes serious illness and death in patients with cancer. However, immunization with annual flu vaccine is low. We demonstrated that a recommendation by the patient’s oncologist was the strongest predictor of vaccination not only for patients but also for their households, underscoring the importance of a well-informed provider. Patients with cancer experience greater morbidity and mortality of influenza infections than the general population.1 Annual inactivated influenza vaccination is recommended for immunocompromised patients who are at least 6 months old and for their family members by the Centers for Disease Control and Prevention and the Infectious Diseases Society of America.2 Unfortunately, low vaccination coverage (9%–40%) has been reported in patients with cancer and stem cell transplant.3,4 With the aim of understanding the barriers that prevent wide vaccination uptake among cancer patients and their household, we evaluated the influenza vaccination practices at a tertiary cancer center.
m e th o d s Patients 18 years or older who had influenza infection confirmed in our microbiology laboratory were contacted by telephone and asked to provide verbal consent to participate in this observational study. In addition, a waiver of consent to obtain available data from the patients’ medical records in case the patient and/or a designated person could not be contacted in 2 different attempts was requested. The study was approved by our institutional review board. The telephone survey included questions about the influenza vaccine, whether the vaccine was recommended by their provider, the main reason for the patient not receiving the vaccine when that was the case, household members’ vaccination status,
and the reasons for household members not undergoing vaccination when that was the case (Online Appendix A). Demographic information, including age, sex, race, spoken language, marital status, type of insurance, religion, previous influenza vaccination, and place of residency (urban versus rural), was obtained. Data on vaccine eligibility for the nonvaccinated patients according to guidelines,2,5 type and status of malignancy, stem-cell transplant, comorbidities, received chemotherapy, clinical variables, treatment, and outcomes were also collected. The influenza vaccination status of the patients and household members represented the main predictive variable in this study. Descriptive statistics were used to summarize the demographic and clinical characteristics of participants. A bivariate analysis was conducted to compare factors predictive of vaccination in the vaccinated and nonvaccinated participants. These characteristics were compared using a χ2 test or Fisher exact test for categorical variables and t test or Wilcoxon rank sum test for continuous variables to identify their associations with outcome. Univariable and multivariable logistic regression analyses were used to calculate the odds ratios and 95% CIs for the effect of the patient and household member vaccination status on the outcomes of interest. A 2-sided P level of .05 was considered statistically significant.
resul ts We identified 154 eligible patients with laboratory-confirmed influenza. One hundred eight patients consented verbally to participate in the survey, for a response rate of 70%. We also included vaccination rates in 12 patients from medical records. The survey showed that 52 (43%) of the 120 patients received the flu vaccine, and 64 (53%) did not. Four patients (3%) did not remember whether they had undergone vaccination, and they were excluded from the analysis. We determined that 39 patients (61%) of the nonvaccinated patients had been eligible to receive the influenza vaccine by current recommendations.2,5 Recommendation by a healthcare provider was the strongest predictor of vaccination. Patients whose oncologists recommended the vaccine were more likely to have been vaccinated than were those who did not receive such recommendation (crude odds ratio, 6.96 [95% CI, 2.92-16.55]; P < .001). Furthermore, age older than 50 years was also a significant predictor of vaccination (crude odds ratio, 2.39 [95% CI, 1.09–5.25]; P = .029) (Table 1). In terms of sociodemographic factors, we describe a trend of more frequent vaccination in white and Asian patients than in Hispanic and African Americans patients, although it was not statistically significant (P = .19). There was no association between vaccination status and the other demographic and clinical variables (Table 1). Of the 64 patients who did not receive the influenza vaccine and who responded to our survey, the main reason cited for
1240 infection control & hospital epidemiology
table 1.
october 2015, vol. 36, no. 10
Influenza Vaccination Status in Patients with Cancer: Characteristics y and Underlying Medical Conditions
Characteristic Median age at flu diagnosis ≤ 50 years > 50 years Sex Male Female Race/ethnicity White Black Hispanic Asian Smoking statusa Never Former/Current Underlying condition Hematological malignancy Solid tumor HCT Cancer statusb Active Remission Physician recommendation of vaccinationc No Yes
Unvaccinated (N = 64)
Vaccinated (N = 52)
Crude odds ratio for receiving vaccination (95% CI)
P value
30 (47) 34 (53)
14 (27) 38 (73)
1 [Reference] 2.39 (1.09–5.25)
.029
41 (64) 23 (36)
30 (58) 22 (42)
1 [Reference] 1.31 (0.62–2.77)
.484
34 (53) 12 (19) 15 (23) 3 (5)
33 (63) 5 (10) 6 (12) 8 (15)
1 [Reference] 0.43 (0.14–1.35) 0.41 (0.14–1.19) 2.75 (0.67–11.26)
.149 .102 .160
36 (56) 27 (42)
35 (67) 16 (31)
1 [Reference] 0.61 (0.28–1.32)
.21
20 (31) 12 (19) 32 (50)
13 (25) 8 (15) 31(60)
1 [Reference] 1.03 (0.33–3.19) 1.49 (0.63–3.51)
.965 .361
43 (67) 20 (31)
29 (56) 21 (40)
1 [Reference] 1.56 (0.72–3.37)
.261
43 (67) 17 (27)
12 (23) 33 (63)
1 [Reference] 6.96 (2.92–16.55)
< .001
NOTE. Data are no. (%) of patients unless otherwise indicated. HCT, hematopoietic stem cell transplantation. Bold indicates statistically significant values (p < .005). a Data was available for 114 patients for smoking status. b Data was available for 113 patients for cancer status. c Data was available for 105 patients for physician recommendations.
nonvaccination was the recommendation against it by the patient’s oncologist (56 [88%]). Information on influenza vaccination of household members for 88 patients was analyzed. Full household vaccination occurred in 38 (43%) of the households. A healthcare provider’s recommendation against vaccination was also among the most common reasons behind the lack of vaccination (Figure 1). Notably, 16 household members (18%) had flu-like illness around the time patients were diagnosed with influenza infection. Vaccination status did not have a significant effect on hospital admission, progression to pneumonia, or mortality. In multivariable analysis, patients who experienced progression to pneumonia were more likely to be neutropenic, to be older, and to have not received oseltamivir early in the course (all, P < .05)
d is c u s s i o n
figure 1. Primary reasons for not undergoing influenza vaccination. A, Patients’ answers; B, Household members’ answers.
Vaccination as a public health intervention has been shown to lessen or eliminate the burden of many infectious diseases. Proper understanding of the barriers to appropriate influenza vaccination coverage is essential for designing future improvement strategies to increase compliance.6 Therefore,
influenza vaccine in cancer patients
we sought to determine factors associated with decisions regarding influenza vaccination in a cohort of cancer patients diagnosed with influenza and their household members. In our cohort, healthcare provider’s recommendation was the most significant determining factor for immunization for the patients. Literature on influenza vaccination in general population and other immunocompromised populations7 supports the importance of the role of the physician in vaccination decisions, and this is not an exception in oncological patients, resulting in our study in an approximately 7-fold greater likelihood of vaccination when patients receive a recommendations by their provider. Furthermore, 61% of the nonvaccinated patients met criteria for vaccination, underscoring how providers should be well informed of current recommendations and the benefits of influenza vaccination in patients with cancer. This study also highlights the unrecognized effect of the oncologists’ recommendations on household vaccination. Because immunocompromised patients are at greater risk for complications from influenza than the general population, providing an indirect protective effect via herd immunity (cocooning) by vaccination of family members becomes a crucial aspect of reducing their risk of infection.8 Furthermore, we found that patients older than 50 years were more likely to have received the influenza vaccine than were younger patients, probably related to the perception of being at higher risk of complications at older age. Different from other studies, concerns about vaccine side effects or effectiveness were not identified as significant barriers to vaccination in patients with cancer.9,10 Lastly, the lack of protection of the influenza vaccine on severity of illness in this specific cohort of patients should be interpreted with caution owing to the design of our study that identified only patients who had influenza infection, which systematically underestimates the effectiveness of the vaccine. Our study had a number of limitations because this was a single-institution study of patients with influenza, which may limit the generalizability of the results. In addition, we had to rely on patient reports to obtain data on the recommendations for influenza vaccination. Such reports are subject to patients’ interpretation of physician recommendations. In conclusion, physician attitudes and recommendations play major roles in the influenza vaccination decisions of cancer patients and their household members. One targeted intervention should be to strengthen the recommendation of physicians, especially oncologists, encouraging their participation in promoting influenza vaccination of both patients and their family members.
a ck n ow le d g m e n t s We acknowledge Michael Worley, Scientific Publications, and especially our patients at MD Anderson Cancer Center who were willing to participate in our survey. Financial support. None reported.
1241
Potential conflicts of interest. R. F. C. reports that he has received research funding from Gilead, GlaxoSmithKline, ADMA Biologics, Ansun Biopharma, and Roche. All other authors report no conflicts of interest relevant to this article. Affiliation: Department of Infectious Diseases, Infection Control and Employee Health, University of Texas MD Anderson Cancer Center, Houston, Texas. Address correspondence to Ella J. Ariza-Heredia, MD, Department of Infectious Diseases, Infection Control and Employee Health, Unit 1460, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030 ([email protected]). Received April 23, 2015; accepted: June 1, 2015; electronically published July 1, 2015 © 2015 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2015/3610-0017. DOI: 10.1017/ice.2015.150
supplementary materials To view Supplementary Materials for this article, please visit http://dx.doi.org/10.1017/ice.2015.150
ref e ren ces 1. Kunisaki KM, Janoff EN. Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 2009;9: 493–504. 2. Rubin LG, Levin MJ, Ljungman P, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis 2014;58 309–318. 3. Pedrazzoli P, Baldanti F, Donatelli I, et al. Vaccination for seasonal influenza in patients with cancer: recommendations of the Italian Society of Medical Oncology (AIOM). Ann Oncol 2014;25:1243–1247. 4. Ariza-Heredia EJ, Gulbis AM, Stolar KR, et al. Vaccination guidelines after hematopoietic stem cell transplantation: practitioners’ knowledge, attitudes, and gap between guidelines and clinical practice. Transpl Infect Dis 2014;16:878–886. 5. Fiore AE, Shay DK, Broder K, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) 2008 MMWR Recomm Rep 2008;57:1–60. 6. Dexter LJ, Teare MD, Dexter M, Siriwardena AN, Read RC. Strategies to increase influenza vaccination rates: outcomes of a nationwide cross-sectional survey of UK general practice. BMJ Open 2012:2 pii:e000851. 7. Loulergue P, Mir O, Alexandre J, Ropert S, Goldwasser F, Launay O. Low influenza vaccination rate among patients receiving chemotherapy for cancer. Ann Oncol 2008;19:1658. 8. Fine P, Eames K, Heymann DL. “Herd immunity”: a rough guide. Clin Infect Dis 2011;52:911–916. 9. Zimmerman RK, Santibanez TA, Janosky JE, et al. What affects influenza vaccination rates among older patients? An analysis from inner-city, suburban, rural, and Veterans Affairs practices. Am J Med 2003;114:31–38. 10. Earle CC. Influenza vaccination in elderly patients with advanced colorectal cancer. J Clin Oncol 2003;21:1161–1166.
