American Journal of Infection Control 42 (2014) 649-52
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Understanding health care personnel’s attitudes toward mandatory influenza vaccination Reda A. Awali MD, MPH a, *, Preethy S. Samuel PhD b, Bharat Marwaha MD a, Nazir Ahmad MD a, Puneet Gupta MBBS a, Vinod Kumar MBBS a, Joseph Ellsworth BS a, Elaine Flanagan BSN, MSA a, Mark Upfal MD c, Jim Russell RN, BSN c, Carol Kaplan BS a, Keith S. Kaye MD, MPH a, Teena Chopra MD, MPH a a
Division of Infectious Diseases, Detroit Medical Center/Wayne State University, Detroit, MI Department of Health Care Sciences, Wayne State University, Detroit, MI c Occupational Health Services, Detroit Medical Center, Detroit, MI b
Key Words: Pro-mandate attitude Leadership Web-based questionnaire Ethical
Background: This study investigated the factors influencing influenza vaccination rates among health care personnel (HCP) and explored HCP’s attitudes toward a policy of mandatory vaccination. Methods: In September 2012, a 33-item Web-based questionnaire was administered to 3,054 HCP employed at a tertiary care hospital in metropolitan Detroit. Results: There was a significant increase in the rate of influenza vaccination, from 80% in the 2010-2011 influenza season (before the mandated influenza vaccine) to 93% in 2011-2012 (after the mandate) (P < .0001). Logistic regression showed that HCP with a history of previous influenza vaccination were 7 times more likely than their peers without this history to receive the vaccine in 2011-2012. A promandate attitude toward influenza vaccination was a significant predictor of receiving the vaccine after adjusting for demographics, history of previous vaccination, awareness of the hospital’s mandatory vaccination policy, and patient contact while providing care (P ¼ .01). Conclusions: The increased rate of influenza vaccination among HCP was driven by both an awareness of the mandatory policy and a pro-mandate attitude toward vaccination. The findings of this study call for better education of HCP on the influenza vaccine along with enforcement of a mandatory vaccination policy. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Influenza vaccination is associated with reduced influenzarelated morbidity and mortality in health care personnel (HCP).1-4 More importantly, vaccinating HCP against influenza reduces the risk of the related disease and subsequent mortality among patients in health care facilities.5,6 A review of the literature identified 2 critical factors contributing to HCP’s adherence to influenza vaccination: HCP’s recognition of their role in transmitting the influenza virus to patients, and HCP’s knowledge of the benefits and risks of influenza vaccination.7 The US Advisory Committee on Immunization Practices first endorsed influenza vaccination for all HCP in 1984.8,9 Since then, advocacy for influenza vaccination of HCP has grown with increased
* Address correspondence to Reda A. Awali, MD, MPH, Division of Infectious Diseases, Detroit Medical Center and Wayne State University School of Medicine, University Health Center, 4201 St Antoine, Suite 2B, Detroit, MI 48201. E-mail address: [email protected] (R.A. Awali). Conflict of interest: None to report.
recognition of the ethical and practical justification for the vaccine. In attempts to improve the nationwide rate of influenza vaccination, professional societies and public health authorities have implemented educational programs, used incentives, encouraged greater leadership support, and provided free and easily accessible vaccine for all HCP.10-14 Despite these herculean efforts, however, the rate of influenza vaccination among HCP remains low (44%-60%).14-17 In the United States, mandatory influenza vaccination of HCP was first instituted at Seattle’s Virginia Mason Medical Center in 2004.18 In 2005, Bronson Methodist Hospital in Kalamazoo became the first hospital in Michigan to implement a mandatory influenza vaccination program for its HCP.19 In the 2009-2010 influenza season, the influenza vaccination coverage rate among HCP at our institution was 45.4%. During the next season (2010-2011), the institutional vaccination policy was not strictly mandatory; however, all unvaccinated employees were required to wear masks when within 6 feet of all patient contacts. Influenza vaccination for all HCP became mandatory in
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.02.025
650
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
the 2011-2012 season. The present study was conducted to investigate the factors influencing vaccination among HCP, and to explore their attitudes toward the mandatory vaccination policy. METHODS Study context and design In September 2012, a cross-sectional survey research study was conducted at an urban tertiary care hospital in the metropolitan Detroit area to assess the impact of implementation of a mandatory HCP influenza vaccination policy. The Institutional Review Board of Wayne State University approved the study protocol. The mandatory vaccination policy adopted in 2011-2012 specified that all HCP be vaccinated against influenza each year when the vaccine becomes available and no later than the annual deadline established by the hospital’s Vaccination Planning Committee. Vaccination is a condition of employment for all HCP, including contracted, clinical, and nonclinical personnel. HCP who fail to obtain the vaccine receive a written warning with a suspension of at least 3 days, and are expected to be compliant by the end of the suspension period. HCP who fail to comply with the policy by the end of the suspension are immediately terminated. Exemptions for medical, religious, or other reasons are reviewed and validated by the hospital Occupational Health Services (OHS). HCP who are deemed exempt or are not vaccinated are required to wear a mask whenever within 6 feet of patients during influenza season or are reassigned from high-risk units, such as intensive care units or protective environment patient care areas, to low-risk units. The OHS and HCP’s direct supervisors or managers are responsible for ensuring compliance with this policy. The new mandatory vaccination policy was communicated to all HCP through their managers, the hospital’s Web site, and e-mail. For this study, a 33-item Web-based questionnaire was delivered by e-mail to all HCP after they were informed about the policy with educational materials about the vaccine and before any reports by the OHS regarding failure of compliance. Responses to the survey, including vaccination refusal, were obtained from all HCP irrespective of whether they were later deemed exempt or were suspended or terminated. At 1 week after the survey was transmitted, a follow-up e-mail reminder was sent to those who had not yet responded. The questionnaire elicited data on the following: respondent’s demographic information, job title, and duration and location of employment at the hospital (part 1); availability and cost of influenza vaccine at the work site, vaccination status, and vaccinerelated side effects in the 2011-2012 and 2010-2011 influenza seasons (part 2); and reasons for acceptance or refusal of vaccination, knowledge of the hospital’s mandatory vaccination policy, and attitudes toward mandatory vaccination (part 3). Four statements were used to evaluate HCP’s attitudes toward the mandated vaccination: (1) “It is the ethical responsibility of all HCP to take the flu shot”; (2) “It is unethical for HCP to not be vaccinated against flu, as they can endanger the lives of their very sick patients by unintentionally transmitting the influenza virus”; (3) “It is unethical to mandate all HCP to take the flu shot”; and (4) “The flu shot should be mandated next year.” The degree of agreement with each statement was rated on a 5-point Likert scale (1, strongly disagree; 2, disagree; 3, neutral; 4, agree; and 5, strongly agree), except for the third statement, which was reverse-coded. Data analysis The c2 test was used to compare the rates of influenza vaccination in 2010-2011 and 2011-2012, and to compare HCP’s attitudes
regarding the vaccination mandate. HCP who strongly agreed or agreed with any of the 4 attitudinal statements were coded as “promandate” (ie, advocating mandatory influenza vaccination), whereas those who strongly disagreed, disagreed, or were neutral to all of the statements were considered “anti-mandate.” Bivariate logistic regression was performed to examine the differences between vaccinated and nonvaccinated HCP in terms of sociodemographic variables, history of vaccination, accessibility to the vaccine, direct patient contact, knowledge of the hospital’s vaccination mandate, and attitudes toward mandatory vaccination. Multivariate logistic regression, using backward selection of variables, was performed to identify the independent predictors of vaccination among HCP. Factors found to be statistically significant (P < .05) predictors of HCP vaccination in the bivariate analysis were included in the final model. Data were analyzed using SPSS version 21 (IBM, Armonk, NY). RESULTS Sociodemographic data The survey was completed by 3,054 HCP, for a response rate of 32%. The majority of respondents were aged 36-65 years (75%), non-Hispanic white (66%), female (86%), working as a nurse (33%), and at the current job for >10 years (51%). Vaccination coverage and reasons for vaccination refusal The vaccination coverage rate increased significantly from 80% before institution of the mandatory vaccination policy in 2010-2011 to 93% after the institution of the policy in 2011-2012 (P < .0001). The rate of influenza vaccination refusal among HCP was 4.8% in 2011-2012. The top 3 reasons cited for vaccination refusal were concerns about potential side effects (63.5%), medical conditions (33%), and religious concerns (17%) (Fig 1). The proportion of respondents citing concerns about side effects as a reason for vaccination refusal was higher in African American HCP compared with non-Hispanic white HCP (P < .0001) and in HCP with a an associate degree or lower educational level compared with those with a bachelors degree or higher (P ¼ .004). Predictors of vaccination There were no reported differences between vaccinated and unvaccinated HCP in terms of age, health-care profession, duration of work, presence of a chronic disease, and access to free vaccine. Male, non-Hispanic white, and HCP with higher educational levels were more likely to receive the vaccine (Table 1). HCP who were vaccinated in 2010-2011 were almost 12 times more likely to be vaccinated in 2011-2012 (P < .0001). A pro-mandate attitude was reported by 79% of HCP who received the vaccine, compared with 56% of unvaccinated HCP (P < .0001). HCP who learned about vaccination risks and benefits through their institution’s milieu, such as information from coworkers or the hospital’s Web site, were more likely to get the vaccine compared with HCP who relied on information from their primary care physicians or media sources (Table 1). Other factors positively associated with receipt of vaccination included previous history of influenza-related side effects (P < .0001), providing direct patient care (P < .0001), working in the pediatrics department (P ¼ .043), and knowledge of the hospital’s mandatory vaccination policy (P ¼ .002) (Table 1). HCP who strongly agreed/agreed with any of the 4 attitudinal statements were more likely to receive the influenza vaccine compared with those who disagreed or were neutral (Table 2).
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
651
Table 2 Comparing HCP attitudes toward mandating vaccination by history of vaccination in 2011-2012 Response variable: agree/strongly agree, n (%)
Statement
Fig 1. Reasons for HCP’s refusal of influenza vaccination 2011-2012. Many respondents reported multiple reasons for vaccination refusal. Table 1 Predictors of vaccination among HCPs in 2011-2012
Characteristic
Vaccinated Unvaccinated HCPs HCPs (n ¼ 2,794), (n ¼ 227), n (%) n (%)
Age 35 y 611 (22) >35 y 2,179 (78) Race African American 661 (24) Non-Hispanic white 1,874 (67) Other 248 (9) Sex Female 2,363 (85) Male 408 (15) Education Associate degree or 1,243 (45) less Bachelors degree 935 (34) Masters degree or 595 (21.5) higher Health-care profession Physician 57 (2) Nurse 804 (34) Administrative 730 (31) Technician 328 (14) Other 456 (19) Duration of work 10 y 1,353 (49) >10 y 1,404 (51) Access to free vaccine 2,595 (98) Working in pediatrics 544 (20) department Previous side effects 1905 (68) (2010-2011) Previous vaccination 2,338 (84) (2010-2011) Chronic disease 559 (20) Providing direct patient 1,816 (66) care Learning about vaccination from Family and friends 36 (1.4) Family physician 148 (6) Media 194 (7) Hospital coworkers 1,414 (53) and Web site Other 869 (33) Knowledge of the nature 1,734 (65) of mandatory policy Pro-mandate attitude 2,103 (79)
49 (22) 176 (78)
1. It is the ethical responsibility of all HCPs to receive the flu shot. 2. It is unethical for HCPs to not be vaccinated against flu, because they could endanger the lives of their very sick patients by unintentionally transmitting the influenza virus. 3. It is unethical to mandate that all HCPs receive the flu shot.* 4. The flu shot should be mandated next year.
Vaccinated HCPs (n ¼ 2,794), n (%)
Unvaccinated HCPs (n ¼ 227), n (%)
P value
1,722 (64)
60 (30)
< .0001
1,659 (62)
73 (37)
< .0001
1,207 (45)
127 (64)
< .0001
1,480 (55)
36 (18)
< .0001
*Responses to statement 3 were reverse-coded.
OR
95% CI
P value
Table 3 Regression model predicting factors associated with vaccination of HCPs against influenza, 2011-2012 Characteristic
0.99 0.71-1.38
.96
105 (47) 98 (44) 20 (9)
3.00 2.27-4.05 1.97 1.19-3.25
< .0001 .008
207 (92) 19 (8)
1.88 1.16-3.04
.01
64 (29) 25 (11)
1.55 1.14-2.12 2.53 1.63-3.92
.006 < .0001
4 39 67 27 37
(2) (22) (38.5) (15.5) (21)
1.45 0.76 0.85 0.86
122 102 175 32
(54.5) (45.5) (97) (14)
1.24 0.94-1.63 1.78 0.75-4.21 1.50 1.01-2.19
.12 .19 .043
4.17 3.14-5.56
< .0001
Race African American Non-Hispanic white Other Previous side effects (2010-2011) Previous vaccination (2010-2011) Providing direct care to patients Knowledge of the nature of mandatory policy Pro-mandate attitude
b
SE
OR
95% CI
P value
0.78 0.21 0.81 1.92 0.70 0.60 0.48
0.18 0.31 0.17 0.18 0.17 0.17 0.18
1.00 2.20 1.23 2.24 7.00 2.02 1.81 1.60
1.55-3.10 0.68-2.24 1.60-3.14 5.0-10.0 1.44-2.82 1.30-2.53 1.12-2.31
< .0001 .50 < .0001 < .0001 < .0001 .001 .01
132 (60)
77 (34) 71 (32) 36 (16) 104 (46)
0.50-4.19 0.27-2.17 0.30-2.53 0.30-2.52
.50 .61 .77 .79
11.70 8.68-15.80 < .0001 1.33 0.92-1.92 2.26 1.72-2.97
.13 < .0001
(3) (16) (13) (33)
0.66 0.24-1.83 1.08 0.39-3.00 3.07 1.17-8.08
.43 .88 .023
69 (36) 107 (54)
1.75 0.66-4.60 1.58 1.19-2.12
.26 .002
111 (56)
2.94 2.19-3.96
< .0001
5 31 25 64
On multivariate logistic regression, the strongest predictor positively associated with vaccination in 2011-2012 was previous vaccination in 2010-2011 (P < .0001) (Table 3). Other variables
independently associated with vaccination compared with nonvaccination included non-Hispanic white race (P < .0001), previous side effects of vaccination (P < .0001), providing direct patient care (P < .001), knowledge of the hospital’s mandate policy (P ¼ .001), and a pro-mandate attitude (P ¼ .01) (Table 3). DISCUSSION Our data demonstrate higher rates of influenza vaccination among HCP after the implementation of a mandatory vaccination policy. This finding is consistent with recent studies reporting substantial increases in influenza vaccination rates among HCP in facilities that instituted a mandated vaccination policy.20-22 A pro-mandate attitude of HCP was significantly associated with receipt of influenza vaccination even after controlling for demographics and potential confounders. Even though 68% of vaccinated HCP reported vaccine-related side effects in 2010-2011, the vaccination rate increased significantly from 2010-2011 to 20112012. The significant increase in vaccination coverage might have been driven by the pro-mandate attitude exhibited by the HCP at our hospital. Higher rates of vaccination have been documented in many health care facilities that implemented well-organized educational programs focusing on the vaccine benefits and side effects.23-26 Surprisingly, a history of vaccine-related side effects was associated with increased likelihood of receiving the influenza vaccine. This finding is in contrast to the results of a previous study conducted in the general population, in which concerns regarding vaccine-related side effects were associated with a low rate of intention to be vaccinated.27 Only HCP were included in the present study, however, and concerns regarding patient safety might have outweighed concerns about vaccine side effects.
652
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
The most common reason for refusing influenza vaccine in the present study was an overall concern about side effects, which is in agreement with previous studies that identified fear of side effects as the main reason for vaccine refusal.28-32 It has been postulated that fear of side effects among HCP might be attributed to misconceptions and poor knowledge of the vaccine’s benefits and safety.33,34 Given that 53% of the vaccinated HCP at our hospital were influenced by their coworkers and the hospital’s Web site in learning about the risks and benefits of influenza vaccination, we believe that implementation of immunization educational programs, in combination with strong support from leadership, can help reduce misperceptions about vaccination and achieve optimal vaccine coverage. HCP who provided direct patient care were more willing to be vaccinated. This is consistent with recent studies identifying patient protection as one of the top reasons for receiving the influenza vaccine.35 Despite the strengths of this descriptive study, we acknowledge some limitations. First, our Web-based survey had a low response rate of 32%; however, average response rates of 11% have been reported in the literature and rates as low as 2% have been reported in Web-based survey studies.36 Second, the study’s cross-sectional design and the lack of evidence of a temporal relationship between predictors and outcomes may call a cause-and-effect relationship into question. Moreover, the survey was based on voluntary, selfreported data, which might have led to social desirability and selection bias. Third, the 2011-2012 seasonal influenza vaccination received much publicity, which might have contributed to the increased rate of vaccination in our HCP. Regardless of these limitations, however, the annual increase in the rate of influenza vaccination and continuing high vaccination coverage point to an overall positive attitude of HCP toward the vaccination mandate. The reluctance of some HCP at our hospital to receive the influenza vaccine despite the mandatory vaccination policy most likely reflects misperceptions and poor knowledge of the benefits and risks of the vaccine. Well-organized influenza vaccine education campaigns aimed at educating HCP about the benefits, emphasizing patient protection as an overriding responsibility, can help overcome HCP’s attitudinal barriers. Such efforts can lead to positive perceptions regarding the benefits of vaccination, replace negative attitudes with accurate knowledge about vaccination, and thereby change HCP’s intentions into actual behaviors. Further studies are needed to probe the longitudinal effect of mandating influenza vaccination and assess the benefits of vaccine-related educational programs. References 1. Advisory Committee on Immunization Practices. Centers for Disease Control and Prevention. Immunization of health-care personnel: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2011;60(RR-7):1-45. 2. Hayward AC, Harling R, Wetten S, Johnson AM, Munro S, Smedley J, et al. Effectiveness of an influenza vaccine programme for care home staff to prevent death, morbidity, and health service use among residents: cluster randomised controlled trial. BMJ 2006;333:1241. 3. Lemaitre M, Meret T, Rothan-Tondeur M, Belmin J, Lejonc JL, Luquel L, et al. Effect of influenza vaccination of nursing home staff on mortality of residents: a cluster-randomized trial. J Am Geriatr Soc 2009;57:1580-6. 4. Carman WF, Elder AG, Wallace LA, McAulay K, Walker A, Murray GD, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: a randomised controlled trial. Lancet 2000;355:93-7. 5. Potter J, Stott DJ, Roberts MA, Elder AG, O’Donnell B, Knight PV, et al. Influenza vaccination of health care workers in long-term-care hospitals reduces the mortality of elderly patients. J Infect Dis 1997;175:1-6. 6. Salgado CD, Giannetta ET, Hayden FG, Farr BM. Preventing nosocomial influenza by improving the vaccine acceptance rate of clinicians. Infect Control Hosp Epidemiol 2004;25:923-8. 7. Hofmann F, Ferracin C, Marsh G, Dumas R. Influenza vaccination of healthcare workers: a literature review of attitudes and beliefs. Infection 2006;34:142-7.
8. Centers for Disease Control and Prevention. Prevention and control of influenza. MMWR Morb Mortal Wkly Rep 1984;33:253-60. 9. Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008; 57(RR-7):1-60. 10. Pearson ML, Bridges CB, Harper SA. Influenza vaccination of health-care personnel: recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55(RR-2):1-16. 11. McArthur MA, Simor AE, Campbell B, McGeer A. Influenza vaccination in longterm-care facilities: structuring programs for success. Infect Control Hosp Epidemiol 1999;20:499-503. 12. Lugo NR. Will carrots or sticks raise influenza immunization rates of health care personnel? Am J Infect Control 2007;35:1-6. 13. Harbarth S, Siegrist CA, Schira JC, Wunderli W, Pittet D. Influenza immunization: improving compliance of healthcare workers. Infect Control Hosp Epidemiol 1998;19:337-42. 14. Bryant KA, Stover B, Cain L, Levine GL, Siegel J, Jarvis WR. Improving influenza immunization rates among healthcare workers caring for high-risk pediatric patients. Infect Control Hosp Epidemiol 2004;25:912-7. 15. Fiore AE, Shay DK, Haber P, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2007. MMWR Recomm Rep 2007;56(RR-6):1-54. 16. Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58(RR-8):1-52. 17. Sartor C, Tissot-Dupont H, Zandotti C, Martin F, Roques P, Drancourt M. Use of a mobile cart influenza program for vaccination of hospital employees. Infect Control Hosp Epidemiol 2004;25:918-22. 18. Wynia MK. Mandating vaccination: what counts as a “mandate” in public health and when should they be used? Am J Bioeth 2007;7:2-6. 19. Stewart AM, Rosenbaum S. Vaccinating the health-care workforce: state law vs. institutional requirements. Public Health Rep 2010;125:615-8. 20. Rakita RM, Hagar BA, Crome P, Lammert JK. Mandatory influenza vaccination of healthcare workers: a 5-year study. Infect Control Hosp Epidemiol 2010;31: 881-8. 21. Bernstein HH, Starke JR. American Academy of Pediatrics, Committee on Infectious D. Policy statement: recommendation for mandatory influenza immunization of all health care personnel. Pediatrics 2010;126:809-15. 22. Babcock HM, Gemeinhart N, Jones M, Dunagan WC, Woeltje KF. Mandatory influenza vaccination of health care workers: translating policy to practice. Clin Infect Dis 2010;50:459-64. 23. de Juanes JR, Garcia de Codes A, Arrazola MP, Jaen F, Sanz MI, Gonzalez A. Influenza vaccination coverage among hospital personnel over three consecutive vaccination campaigns (2001-2002 to 2003-2004). Vaccine 2007;25:201-4. 24. Saluja I, Theakston KD, Kaczorowski J. Influenza vaccination rate among emergency department personnel: a survey of four teaching hospitals. CJEM 2005;7:17-21. 25. Trivalle C, Okenge E, Hamon B, Taillandier J, Falissard B. Factors that influence influenza vaccination among healthcare workers in a French geriatric hospital. Infect Control Hosp Epidemiol 2006;27:1278-80. 26. Dunais B, Saccomano C, Mousnier A, Roure MC, Dellamonica P, Roger PM. Influenza vaccination: impact of an intervention campaign targeting hospital staff. Infect Control Hosp Epidemiol 2006;27:529-31. 27. Renner B, Reuter T. Predicting vaccination using numerical and affective risk perceptions: the case of A/H1N1 influenza. Vaccine 2012;30:7019-26. 28. Barriere J, Vanjak D, Kriegel I, Otto J, Peyrade F, Estève M, et al. Acceptance of the 2009 A(H1N1) influenza vaccine among hospital workers in two French cancer centers. Vaccine 2010;28:7030-4. 29. To KW, Lee S, Chan TO, Lee SS. Exploring determinants of acceptance of the pandemic influenza A (H1N1) 2009 vaccination in nurses. Am J Infect Control 2010;38:623-30. 30. Ferguson CD, Ferguson TE, Golledge J, McBride WJ. Pandemic influenza vaccination: will the health care system take its own medicine? Aust J Rural Health 2010;18:137-42. 31. Seale H, Kaur R, Wang Q, Yang P, Zhang Y, Wang X, et al. Acceptance of a vaccine against pandemic influenza A (H1N1) virus amongst healthcare workers in Beijing, China. Vaccine 2011;29:1605-10. 32. Rachiotis G, Mouchtouri VA, Kremastinou J, Gourgoulianis K, Hadjichristodoulou C. Low acceptance of vaccination against the 2009 pandemic influenza A(H1N1) among healthcare workers in Greece. Euro Surveill 2010;15:19486. 33. Christini AB, Shutt KA, Byers KE. Influenza vaccination rates and motivators among healthcare worker groups. Infect Control Hosp Epidemiol 2007;28: 171-7. 34. Bautista D, Vila B, Uso R, Tellez M, Zanon V. Predisposing, reinforcing, and enabling factors influencing influenza vaccination acceptance among healthcare workers. Infect Control Hosp Epidemiol 2006;27:73-7. 35. Hakim H, Gaur AH, McCullers JA. Motivating factors for high rates of influenza vaccination among healthcare workers. Vaccine 2011;29:5963-9. 36. Petchenik J, Watermolen DJ. A cautionary note on using the Internet to survey recent hunter education graduates. Hum Dimens Wildlife 2011;16:216-8.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Understanding health care personnel’s attitudes toward mandatory influenza vaccination Reda A. Awali MD, MPH a, *, Preethy S. Samuel PhD b, Bharat Marwaha MD a, Nazir Ahmad MD a, Puneet Gupta MBBS a, Vinod Kumar MBBS a, Joseph Ellsworth BS a, Elaine Flanagan BSN, MSA a, Mark Upfal MD c, Jim Russell RN, BSN c, Carol Kaplan BS a, Keith S. Kaye MD, MPH a, Teena Chopra MD, MPH a a
Division of Infectious Diseases, Detroit Medical Center/Wayne State University, Detroit, MI Department of Health Care Sciences, Wayne State University, Detroit, MI c Occupational Health Services, Detroit Medical Center, Detroit, MI b
Key Words: Pro-mandate attitude Leadership Web-based questionnaire Ethical
Background: This study investigated the factors influencing influenza vaccination rates among health care personnel (HCP) and explored HCP’s attitudes toward a policy of mandatory vaccination. Methods: In September 2012, a 33-item Web-based questionnaire was administered to 3,054 HCP employed at a tertiary care hospital in metropolitan Detroit. Results: There was a significant increase in the rate of influenza vaccination, from 80% in the 2010-2011 influenza season (before the mandated influenza vaccine) to 93% in 2011-2012 (after the mandate) (P < .0001). Logistic regression showed that HCP with a history of previous influenza vaccination were 7 times more likely than their peers without this history to receive the vaccine in 2011-2012. A promandate attitude toward influenza vaccination was a significant predictor of receiving the vaccine after adjusting for demographics, history of previous vaccination, awareness of the hospital’s mandatory vaccination policy, and patient contact while providing care (P ¼ .01). Conclusions: The increased rate of influenza vaccination among HCP was driven by both an awareness of the mandatory policy and a pro-mandate attitude toward vaccination. The findings of this study call for better education of HCP on the influenza vaccine along with enforcement of a mandatory vaccination policy. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Influenza vaccination is associated with reduced influenzarelated morbidity and mortality in health care personnel (HCP).1-4 More importantly, vaccinating HCP against influenza reduces the risk of the related disease and subsequent mortality among patients in health care facilities.5,6 A review of the literature identified 2 critical factors contributing to HCP’s adherence to influenza vaccination: HCP’s recognition of their role in transmitting the influenza virus to patients, and HCP’s knowledge of the benefits and risks of influenza vaccination.7 The US Advisory Committee on Immunization Practices first endorsed influenza vaccination for all HCP in 1984.8,9 Since then, advocacy for influenza vaccination of HCP has grown with increased
* Address correspondence to Reda A. Awali, MD, MPH, Division of Infectious Diseases, Detroit Medical Center and Wayne State University School of Medicine, University Health Center, 4201 St Antoine, Suite 2B, Detroit, MI 48201. E-mail address: [email protected] (R.A. Awali). Conflict of interest: None to report.
recognition of the ethical and practical justification for the vaccine. In attempts to improve the nationwide rate of influenza vaccination, professional societies and public health authorities have implemented educational programs, used incentives, encouraged greater leadership support, and provided free and easily accessible vaccine for all HCP.10-14 Despite these herculean efforts, however, the rate of influenza vaccination among HCP remains low (44%-60%).14-17 In the United States, mandatory influenza vaccination of HCP was first instituted at Seattle’s Virginia Mason Medical Center in 2004.18 In 2005, Bronson Methodist Hospital in Kalamazoo became the first hospital in Michigan to implement a mandatory influenza vaccination program for its HCP.19 In the 2009-2010 influenza season, the influenza vaccination coverage rate among HCP at our institution was 45.4%. During the next season (2010-2011), the institutional vaccination policy was not strictly mandatory; however, all unvaccinated employees were required to wear masks when within 6 feet of all patient contacts. Influenza vaccination for all HCP became mandatory in
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.02.025
650
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
the 2011-2012 season. The present study was conducted to investigate the factors influencing vaccination among HCP, and to explore their attitudes toward the mandatory vaccination policy. METHODS Study context and design In September 2012, a cross-sectional survey research study was conducted at an urban tertiary care hospital in the metropolitan Detroit area to assess the impact of implementation of a mandatory HCP influenza vaccination policy. The Institutional Review Board of Wayne State University approved the study protocol. The mandatory vaccination policy adopted in 2011-2012 specified that all HCP be vaccinated against influenza each year when the vaccine becomes available and no later than the annual deadline established by the hospital’s Vaccination Planning Committee. Vaccination is a condition of employment for all HCP, including contracted, clinical, and nonclinical personnel. HCP who fail to obtain the vaccine receive a written warning with a suspension of at least 3 days, and are expected to be compliant by the end of the suspension period. HCP who fail to comply with the policy by the end of the suspension are immediately terminated. Exemptions for medical, religious, or other reasons are reviewed and validated by the hospital Occupational Health Services (OHS). HCP who are deemed exempt or are not vaccinated are required to wear a mask whenever within 6 feet of patients during influenza season or are reassigned from high-risk units, such as intensive care units or protective environment patient care areas, to low-risk units. The OHS and HCP’s direct supervisors or managers are responsible for ensuring compliance with this policy. The new mandatory vaccination policy was communicated to all HCP through their managers, the hospital’s Web site, and e-mail. For this study, a 33-item Web-based questionnaire was delivered by e-mail to all HCP after they were informed about the policy with educational materials about the vaccine and before any reports by the OHS regarding failure of compliance. Responses to the survey, including vaccination refusal, were obtained from all HCP irrespective of whether they were later deemed exempt or were suspended or terminated. At 1 week after the survey was transmitted, a follow-up e-mail reminder was sent to those who had not yet responded. The questionnaire elicited data on the following: respondent’s demographic information, job title, and duration and location of employment at the hospital (part 1); availability and cost of influenza vaccine at the work site, vaccination status, and vaccinerelated side effects in the 2011-2012 and 2010-2011 influenza seasons (part 2); and reasons for acceptance or refusal of vaccination, knowledge of the hospital’s mandatory vaccination policy, and attitudes toward mandatory vaccination (part 3). Four statements were used to evaluate HCP’s attitudes toward the mandated vaccination: (1) “It is the ethical responsibility of all HCP to take the flu shot”; (2) “It is unethical for HCP to not be vaccinated against flu, as they can endanger the lives of their very sick patients by unintentionally transmitting the influenza virus”; (3) “It is unethical to mandate all HCP to take the flu shot”; and (4) “The flu shot should be mandated next year.” The degree of agreement with each statement was rated on a 5-point Likert scale (1, strongly disagree; 2, disagree; 3, neutral; 4, agree; and 5, strongly agree), except for the third statement, which was reverse-coded. Data analysis The c2 test was used to compare the rates of influenza vaccination in 2010-2011 and 2011-2012, and to compare HCP’s attitudes
regarding the vaccination mandate. HCP who strongly agreed or agreed with any of the 4 attitudinal statements were coded as “promandate” (ie, advocating mandatory influenza vaccination), whereas those who strongly disagreed, disagreed, or were neutral to all of the statements were considered “anti-mandate.” Bivariate logistic regression was performed to examine the differences between vaccinated and nonvaccinated HCP in terms of sociodemographic variables, history of vaccination, accessibility to the vaccine, direct patient contact, knowledge of the hospital’s vaccination mandate, and attitudes toward mandatory vaccination. Multivariate logistic regression, using backward selection of variables, was performed to identify the independent predictors of vaccination among HCP. Factors found to be statistically significant (P < .05) predictors of HCP vaccination in the bivariate analysis were included in the final model. Data were analyzed using SPSS version 21 (IBM, Armonk, NY). RESULTS Sociodemographic data The survey was completed by 3,054 HCP, for a response rate of 32%. The majority of respondents were aged 36-65 years (75%), non-Hispanic white (66%), female (86%), working as a nurse (33%), and at the current job for >10 years (51%). Vaccination coverage and reasons for vaccination refusal The vaccination coverage rate increased significantly from 80% before institution of the mandatory vaccination policy in 2010-2011 to 93% after the institution of the policy in 2011-2012 (P < .0001). The rate of influenza vaccination refusal among HCP was 4.8% in 2011-2012. The top 3 reasons cited for vaccination refusal were concerns about potential side effects (63.5%), medical conditions (33%), and religious concerns (17%) (Fig 1). The proportion of respondents citing concerns about side effects as a reason for vaccination refusal was higher in African American HCP compared with non-Hispanic white HCP (P < .0001) and in HCP with a an associate degree or lower educational level compared with those with a bachelors degree or higher (P ¼ .004). Predictors of vaccination There were no reported differences between vaccinated and unvaccinated HCP in terms of age, health-care profession, duration of work, presence of a chronic disease, and access to free vaccine. Male, non-Hispanic white, and HCP with higher educational levels were more likely to receive the vaccine (Table 1). HCP who were vaccinated in 2010-2011 were almost 12 times more likely to be vaccinated in 2011-2012 (P < .0001). A pro-mandate attitude was reported by 79% of HCP who received the vaccine, compared with 56% of unvaccinated HCP (P < .0001). HCP who learned about vaccination risks and benefits through their institution’s milieu, such as information from coworkers or the hospital’s Web site, were more likely to get the vaccine compared with HCP who relied on information from their primary care physicians or media sources (Table 1). Other factors positively associated with receipt of vaccination included previous history of influenza-related side effects (P < .0001), providing direct patient care (P < .0001), working in the pediatrics department (P ¼ .043), and knowledge of the hospital’s mandatory vaccination policy (P ¼ .002) (Table 1). HCP who strongly agreed/agreed with any of the 4 attitudinal statements were more likely to receive the influenza vaccine compared with those who disagreed or were neutral (Table 2).
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
651
Table 2 Comparing HCP attitudes toward mandating vaccination by history of vaccination in 2011-2012 Response variable: agree/strongly agree, n (%)
Statement
Fig 1. Reasons for HCP’s refusal of influenza vaccination 2011-2012. Many respondents reported multiple reasons for vaccination refusal. Table 1 Predictors of vaccination among HCPs in 2011-2012
Characteristic
Vaccinated Unvaccinated HCPs HCPs (n ¼ 2,794), (n ¼ 227), n (%) n (%)
Age 35 y 611 (22) >35 y 2,179 (78) Race African American 661 (24) Non-Hispanic white 1,874 (67) Other 248 (9) Sex Female 2,363 (85) Male 408 (15) Education Associate degree or 1,243 (45) less Bachelors degree 935 (34) Masters degree or 595 (21.5) higher Health-care profession Physician 57 (2) Nurse 804 (34) Administrative 730 (31) Technician 328 (14) Other 456 (19) Duration of work 10 y 1,353 (49) >10 y 1,404 (51) Access to free vaccine 2,595 (98) Working in pediatrics 544 (20) department Previous side effects 1905 (68) (2010-2011) Previous vaccination 2,338 (84) (2010-2011) Chronic disease 559 (20) Providing direct patient 1,816 (66) care Learning about vaccination from Family and friends 36 (1.4) Family physician 148 (6) Media 194 (7) Hospital coworkers 1,414 (53) and Web site Other 869 (33) Knowledge of the nature 1,734 (65) of mandatory policy Pro-mandate attitude 2,103 (79)
49 (22) 176 (78)
1. It is the ethical responsibility of all HCPs to receive the flu shot. 2. It is unethical for HCPs to not be vaccinated against flu, because they could endanger the lives of their very sick patients by unintentionally transmitting the influenza virus. 3. It is unethical to mandate that all HCPs receive the flu shot.* 4. The flu shot should be mandated next year.
Vaccinated HCPs (n ¼ 2,794), n (%)
Unvaccinated HCPs (n ¼ 227), n (%)
P value
1,722 (64)
60 (30)
< .0001
1,659 (62)
73 (37)
< .0001
1,207 (45)
127 (64)
< .0001
1,480 (55)
36 (18)
< .0001
*Responses to statement 3 were reverse-coded.
OR
95% CI
P value
Table 3 Regression model predicting factors associated with vaccination of HCPs against influenza, 2011-2012 Characteristic
0.99 0.71-1.38
.96
105 (47) 98 (44) 20 (9)
3.00 2.27-4.05 1.97 1.19-3.25
< .0001 .008
207 (92) 19 (8)
1.88 1.16-3.04
.01
64 (29) 25 (11)
1.55 1.14-2.12 2.53 1.63-3.92
.006 < .0001
4 39 67 27 37
(2) (22) (38.5) (15.5) (21)
1.45 0.76 0.85 0.86
122 102 175 32
(54.5) (45.5) (97) (14)
1.24 0.94-1.63 1.78 0.75-4.21 1.50 1.01-2.19
.12 .19 .043
4.17 3.14-5.56
< .0001
Race African American Non-Hispanic white Other Previous side effects (2010-2011) Previous vaccination (2010-2011) Providing direct care to patients Knowledge of the nature of mandatory policy Pro-mandate attitude
b
SE
OR
95% CI
P value
0.78 0.21 0.81 1.92 0.70 0.60 0.48
0.18 0.31 0.17 0.18 0.17 0.17 0.18
1.00 2.20 1.23 2.24 7.00 2.02 1.81 1.60
1.55-3.10 0.68-2.24 1.60-3.14 5.0-10.0 1.44-2.82 1.30-2.53 1.12-2.31
< .0001 .50 < .0001 < .0001 < .0001 .001 .01
132 (60)
77 (34) 71 (32) 36 (16) 104 (46)
0.50-4.19 0.27-2.17 0.30-2.53 0.30-2.52
.50 .61 .77 .79
11.70 8.68-15.80 < .0001 1.33 0.92-1.92 2.26 1.72-2.97
.13 < .0001
(3) (16) (13) (33)
0.66 0.24-1.83 1.08 0.39-3.00 3.07 1.17-8.08
.43 .88 .023
69 (36) 107 (54)
1.75 0.66-4.60 1.58 1.19-2.12
.26 .002
111 (56)
2.94 2.19-3.96
< .0001
5 31 25 64
On multivariate logistic regression, the strongest predictor positively associated with vaccination in 2011-2012 was previous vaccination in 2010-2011 (P < .0001) (Table 3). Other variables
independently associated with vaccination compared with nonvaccination included non-Hispanic white race (P < .0001), previous side effects of vaccination (P < .0001), providing direct patient care (P < .001), knowledge of the hospital’s mandate policy (P ¼ .001), and a pro-mandate attitude (P ¼ .01) (Table 3). DISCUSSION Our data demonstrate higher rates of influenza vaccination among HCP after the implementation of a mandatory vaccination policy. This finding is consistent with recent studies reporting substantial increases in influenza vaccination rates among HCP in facilities that instituted a mandated vaccination policy.20-22 A pro-mandate attitude of HCP was significantly associated with receipt of influenza vaccination even after controlling for demographics and potential confounders. Even though 68% of vaccinated HCP reported vaccine-related side effects in 2010-2011, the vaccination rate increased significantly from 2010-2011 to 20112012. The significant increase in vaccination coverage might have been driven by the pro-mandate attitude exhibited by the HCP at our hospital. Higher rates of vaccination have been documented in many health care facilities that implemented well-organized educational programs focusing on the vaccine benefits and side effects.23-26 Surprisingly, a history of vaccine-related side effects was associated with increased likelihood of receiving the influenza vaccine. This finding is in contrast to the results of a previous study conducted in the general population, in which concerns regarding vaccine-related side effects were associated with a low rate of intention to be vaccinated.27 Only HCP were included in the present study, however, and concerns regarding patient safety might have outweighed concerns about vaccine side effects.
652
R.A. Awali et al. / American Journal of Infection Control 42 (2014) 649-52
The most common reason for refusing influenza vaccine in the present study was an overall concern about side effects, which is in agreement with previous studies that identified fear of side effects as the main reason for vaccine refusal.28-32 It has been postulated that fear of side effects among HCP might be attributed to misconceptions and poor knowledge of the vaccine’s benefits and safety.33,34 Given that 53% of the vaccinated HCP at our hospital were influenced by their coworkers and the hospital’s Web site in learning about the risks and benefits of influenza vaccination, we believe that implementation of immunization educational programs, in combination with strong support from leadership, can help reduce misperceptions about vaccination and achieve optimal vaccine coverage. HCP who provided direct patient care were more willing to be vaccinated. This is consistent with recent studies identifying patient protection as one of the top reasons for receiving the influenza vaccine.35 Despite the strengths of this descriptive study, we acknowledge some limitations. First, our Web-based survey had a low response rate of 32%; however, average response rates of 11% have been reported in the literature and rates as low as 2% have been reported in Web-based survey studies.36 Second, the study’s cross-sectional design and the lack of evidence of a temporal relationship between predictors and outcomes may call a cause-and-effect relationship into question. Moreover, the survey was based on voluntary, selfreported data, which might have led to social desirability and selection bias. Third, the 2011-2012 seasonal influenza vaccination received much publicity, which might have contributed to the increased rate of vaccination in our HCP. Regardless of these limitations, however, the annual increase in the rate of influenza vaccination and continuing high vaccination coverage point to an overall positive attitude of HCP toward the vaccination mandate. The reluctance of some HCP at our hospital to receive the influenza vaccine despite the mandatory vaccination policy most likely reflects misperceptions and poor knowledge of the benefits and risks of the vaccine. Well-organized influenza vaccine education campaigns aimed at educating HCP about the benefits, emphasizing patient protection as an overriding responsibility, can help overcome HCP’s attitudinal barriers. Such efforts can lead to positive perceptions regarding the benefits of vaccination, replace negative attitudes with accurate knowledge about vaccination, and thereby change HCP’s intentions into actual behaviors. Further studies are needed to probe the longitudinal effect of mandating influenza vaccination and assess the benefits of vaccine-related educational programs. References 1. Advisory Committee on Immunization Practices. Centers for Disease Control and Prevention. Immunization of health-care personnel: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2011;60(RR-7):1-45. 2. Hayward AC, Harling R, Wetten S, Johnson AM, Munro S, Smedley J, et al. Effectiveness of an influenza vaccine programme for care home staff to prevent death, morbidity, and health service use among residents: cluster randomised controlled trial. BMJ 2006;333:1241. 3. Lemaitre M, Meret T, Rothan-Tondeur M, Belmin J, Lejonc JL, Luquel L, et al. Effect of influenza vaccination of nursing home staff on mortality of residents: a cluster-randomized trial. J Am Geriatr Soc 2009;57:1580-6. 4. Carman WF, Elder AG, Wallace LA, McAulay K, Walker A, Murray GD, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: a randomised controlled trial. Lancet 2000;355:93-7. 5. Potter J, Stott DJ, Roberts MA, Elder AG, O’Donnell B, Knight PV, et al. Influenza vaccination of health care workers in long-term-care hospitals reduces the mortality of elderly patients. J Infect Dis 1997;175:1-6. 6. Salgado CD, Giannetta ET, Hayden FG, Farr BM. Preventing nosocomial influenza by improving the vaccine acceptance rate of clinicians. Infect Control Hosp Epidemiol 2004;25:923-8. 7. Hofmann F, Ferracin C, Marsh G, Dumas R. Influenza vaccination of healthcare workers: a literature review of attitudes and beliefs. Infection 2006;34:142-7.
8. Centers for Disease Control and Prevention. Prevention and control of influenza. MMWR Morb Mortal Wkly Rep 1984;33:253-60. 9. Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008; 57(RR-7):1-60. 10. Pearson ML, Bridges CB, Harper SA. Influenza vaccination of health-care personnel: recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55(RR-2):1-16. 11. McArthur MA, Simor AE, Campbell B, McGeer A. Influenza vaccination in longterm-care facilities: structuring programs for success. Infect Control Hosp Epidemiol 1999;20:499-503. 12. Lugo NR. Will carrots or sticks raise influenza immunization rates of health care personnel? Am J Infect Control 2007;35:1-6. 13. Harbarth S, Siegrist CA, Schira JC, Wunderli W, Pittet D. Influenza immunization: improving compliance of healthcare workers. Infect Control Hosp Epidemiol 1998;19:337-42. 14. Bryant KA, Stover B, Cain L, Levine GL, Siegel J, Jarvis WR. Improving influenza immunization rates among healthcare workers caring for high-risk pediatric patients. Infect Control Hosp Epidemiol 2004;25:912-7. 15. Fiore AE, Shay DK, Haber P, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2007. MMWR Recomm Rep 2007;56(RR-6):1-54. 16. Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58(RR-8):1-52. 17. Sartor C, Tissot-Dupont H, Zandotti C, Martin F, Roques P, Drancourt M. Use of a mobile cart influenza program for vaccination of hospital employees. Infect Control Hosp Epidemiol 2004;25:918-22. 18. Wynia MK. Mandating vaccination: what counts as a “mandate” in public health and when should they be used? Am J Bioeth 2007;7:2-6. 19. Stewart AM, Rosenbaum S. Vaccinating the health-care workforce: state law vs. institutional requirements. Public Health Rep 2010;125:615-8. 20. Rakita RM, Hagar BA, Crome P, Lammert JK. Mandatory influenza vaccination of healthcare workers: a 5-year study. Infect Control Hosp Epidemiol 2010;31: 881-8. 21. Bernstein HH, Starke JR. American Academy of Pediatrics, Committee on Infectious D. Policy statement: recommendation for mandatory influenza immunization of all health care personnel. Pediatrics 2010;126:809-15. 22. Babcock HM, Gemeinhart N, Jones M, Dunagan WC, Woeltje KF. Mandatory influenza vaccination of health care workers: translating policy to practice. Clin Infect Dis 2010;50:459-64. 23. de Juanes JR, Garcia de Codes A, Arrazola MP, Jaen F, Sanz MI, Gonzalez A. Influenza vaccination coverage among hospital personnel over three consecutive vaccination campaigns (2001-2002 to 2003-2004). Vaccine 2007;25:201-4. 24. Saluja I, Theakston KD, Kaczorowski J. Influenza vaccination rate among emergency department personnel: a survey of four teaching hospitals. CJEM 2005;7:17-21. 25. Trivalle C, Okenge E, Hamon B, Taillandier J, Falissard B. Factors that influence influenza vaccination among healthcare workers in a French geriatric hospital. Infect Control Hosp Epidemiol 2006;27:1278-80. 26. Dunais B, Saccomano C, Mousnier A, Roure MC, Dellamonica P, Roger PM. Influenza vaccination: impact of an intervention campaign targeting hospital staff. Infect Control Hosp Epidemiol 2006;27:529-31. 27. Renner B, Reuter T. Predicting vaccination using numerical and affective risk perceptions: the case of A/H1N1 influenza. Vaccine 2012;30:7019-26. 28. Barriere J, Vanjak D, Kriegel I, Otto J, Peyrade F, Estève M, et al. Acceptance of the 2009 A(H1N1) influenza vaccine among hospital workers in two French cancer centers. Vaccine 2010;28:7030-4. 29. To KW, Lee S, Chan TO, Lee SS. Exploring determinants of acceptance of the pandemic influenza A (H1N1) 2009 vaccination in nurses. Am J Infect Control 2010;38:623-30. 30. Ferguson CD, Ferguson TE, Golledge J, McBride WJ. Pandemic influenza vaccination: will the health care system take its own medicine? Aust J Rural Health 2010;18:137-42. 31. Seale H, Kaur R, Wang Q, Yang P, Zhang Y, Wang X, et al. Acceptance of a vaccine against pandemic influenza A (H1N1) virus amongst healthcare workers in Beijing, China. Vaccine 2011;29:1605-10. 32. Rachiotis G, Mouchtouri VA, Kremastinou J, Gourgoulianis K, Hadjichristodoulou C. Low acceptance of vaccination against the 2009 pandemic influenza A(H1N1) among healthcare workers in Greece. Euro Surveill 2010;15:19486. 33. Christini AB, Shutt KA, Byers KE. Influenza vaccination rates and motivators among healthcare worker groups. Infect Control Hosp Epidemiol 2007;28: 171-7. 34. Bautista D, Vila B, Uso R, Tellez M, Zanon V. Predisposing, reinforcing, and enabling factors influencing influenza vaccination acceptance among healthcare workers. Infect Control Hosp Epidemiol 2006;27:73-7. 35. Hakim H, Gaur AH, McCullers JA. Motivating factors for high rates of influenza vaccination among healthcare workers. Vaccine 2011;29:5963-9. 36. Petchenik J, Watermolen DJ. A cautionary note on using the Internet to survey recent hunter education graduates. Hum Dimens Wildlife 2011;16:216-8.
