Influenza Vaccination of Healthcare Workers: a Literature Review of Attitudes and Beliefs

F. Hofmann, C. Ferracin, G. Marsh, R. Dumas

Abstract

Background: Influenza vaccination coverage among healthcare workers (HCW) is insufficient despite health authority recommendations in many countries. Numerous vaccination campaigns encouraging HCW to be vaccinated have met with resistance. We reviewed published influenza vaccination programs in healthcare settings to understand the reasons for their success and failure, as well as the attitudes and beliefs of HCW.

Methods: Relevant articles published up to June 2004 were identified in the MEDLINE/Pubmed database.

Results: Thirty-two studies performed between 1985 and 2002 reported vaccination rates of 2.1–82%. Vaccination campaigns including easy access to free vaccine and an educational program tended to obtain the highest uptake, particularly in the USA. Yet, even this type of campaign was not always successful. Two main barriers to satisfactory vaccine uptake were consistently reported: (1) misperception of influenza, its risks, the role of HCW in its transmission to patients, and the importance and risks of vaccination (2) lack of (or perceived lack of) conveniently available vaccine.

Conclusion: To overcome these barriers and increase uptake, vaccination campaigns must be carefully designed and implemented taking account of the specific needs at each healthcare institution.

Infection 2006; 34: 142–147
DOI 10.1007/s15010-006-5109-5

Introduction

Many institutions recommend that healthcare workers (HCW) be routinely vaccinated against influenza to reduce the occupational risk of infection [1], and to prevent the transmission of influenza virus to patients at risk of secondary complications and death. The latter reason is the one stated in most national recommendations. Influenza vaccination of HCW has been recommended by the United States Centers for Disease Control and Prevention (CDC) since the early 1980’s, and since at least 2000 in 12 European countries [2, 3]. Numerous international vaccination programs have subsequently tried to encourage HCW to be vaccinated, but have met with surprising resistance. Individual programs have been the subject of a number of articles and letters to journals. Here we review the published reasons for success and failure of vaccination programs, and the attitudes and beliefs of HCW. With this understanding we attempt to provide some helpful insights for future programs.

Healthcare workers are particularly exposed to influenza infection as they are exposed in both the general community (household contacts, public transport etc.) and the workplace. Close proximity to patients, and a constant flow of visitors and co-workers may increase the infection risk. Up to 25% of non-immunized HCW develop influenza during the winter [4]. Attack rates may be even higher as infected HCW may also be asymptomatic. In a study of 518 HCW during the winter of 1993–1994, 23% had serologically proved of infection, of whom 59% did not remember having influenza and 28% did not remember having any respiratory infection [5]. HCW show a high work-commitment and often continue looking after patients despite being infected with influenza [6]. The average incubation period is 2 days. Adults are infectious from the day before symptoms start and up to 5 days afterwards. The infection is regarded as nosocomial if symptoms start at least 2–3 days after hospitalization. Case reports include extended care facilities for the elderly, renal transplant and oncology units, neonatal intensive care and pediatrics [7, 8]. Persons cared for in these settings are at high complication- risk and personnel are often undervaccinated [9, 10]. In acute-care facilities and geriatric hospitals, the median mortality rate during influenza outbreaks has been put at 16%, but may be as high as 60% in transplant or intensive care units [7]. Unfortunately, the risks of influenza are not well perceived by all HCW [11]. For example 44% of homeopathic but only 2% of allopathic physicians consider influenza vaccination unnecessary for adults, children or even for risk groups [12]. Thus HCW are more likely to get influenza and to pass it on, with more significant consequences than for any other worker-group.

One simple definition for the term “HCW” is all medical and non-medical personnel in contact with patients [13]. The CDC holds this view, including non-remunerated and/ or temporary staff, as well as persons exposed to human samples. This definition includes diverse roles with varying exposure levels to the virus and contact with the patients: physicians, nurses, physiotherapists, dieticians, religious workers, cleaning, kitchen and laboratory personnel. The Canadian National Advisory Committee on Immunization (NACI) adopts a narrower, and possibly more pragmatic approach by targeting personnel involved in direct patient care [14]. For this group, the NACI considers annual influenza vaccination to be essential component of the standard of care for the protection of patients and states that, in absence of contraindications, refusal of these HCW to be immunized against influenza implies failure in their duty of care.

Methods

Relevant articles published up to June 2004 were identified (MEDLINE/Pubmed database) using keywords related to influenza immunization and the perception and coverage among HCW. The reference lists of the retrieved articles were reviewed to identify additional articles.

Results

Thirty-two primary publications reporting influenza vaccination coverage among HCW between 1985 and 2002 were identified, including 25 addressing the attitudes of HCW towards influenza vaccination [6, 11, 15–44].

Vaccination Coverage

The 32 publications can be divided into four classes: (1) 16 reported coverage in health care units in which a vaccination campaign accompanied the season and influenza vaccine was provided free of charge, (2) one reported the result of a vaccination campaign, but did not specify whether vaccine was provided free of charge, (3) in seven cases, vaccine was provided free of charge but no specific campaign was reported, and (4) eight publications reported coverage, but provided no details of any campaign or free vaccine (Figure 1).

Vaccination rates varied from 2.1% to 82% (Figure 1) [6, 41]. In the US studies, coverage rates in hospitals with free vaccine (with or without an informational campaign) were higher than in hospitals without free vaccine or campaigns, and tended to be higher than in Europe. In the five Canadian reports with vaccination rates between 35% and 51% no clear benefit of either free vaccine or a vaccination campaign was observed, with the exception of one study [31].

Healthcare Workers’ Attitudes

The 25 studies that addressed how HCW view influenza vaccination mostly used anonymous closed-question questionnaires to understand the motivations of HCW in getting vaccinated, and the reasons for refusal. The most recurrent ideas are presented in tables 1 and 2. The percentage range represents the minimum and maximum values reported in the publications that addressed each idea.

Discussion

Many national/international recommendations include HCW as a priority group for annual influenza vaccination [1–3, 14, 45] without defining a minimum coverage rate for this population. Uptake rates of ~ 50% have been associated with a ~ 40% reduction of total winter mortality of elderly patients in long-term care [46, 47]. The Canadian NACI sets a minimum rate of 90% of all “eligible recipients” of influenza vaccine [14]. The WHO and ACIP state coverage rates of 50–90% for the elderly population and 60% for high-risk adults, but none for HCW [2, 48]. Current HCW influenza vaccination coverage is far below these figures: 38% in 2002 in the USA [2], 26–61% in Canada [14], and 12–25% in Europe [49]. Strategies to increase coverage are clearly necessary.

The six US programs with the highest uptake rates can be considered successful as they attained uptake rates in excess of the 2002 national average (38%), surpassing 60% in four cases [16, 22–24, 26, 41]. All included free vaccine, and five (including all four with uptake > 60%) an educational component. Although the details of these successful campaigns differed, many features were similar including three key phases: notification, education, and vaccination. Notification was characterized by the communication of key messages through various media: individual invitations sent with pay slip, e-mail messages, memos, and posters in well-traveled areas. Education included staff in-service sessions, conferences, and educational films. Vaccination was characterized by readily accessible free vaccine using mobile vaccination carts and “walk-in” vaccination clinics. Interestingly, the highest coverage was obtained by a US program including festive vaccination sessions with educational games, free refreshments and participation in a lottery for vaccinees [41].

Yet even this type of extensive program does not guarantee success. One such program during the 1995–1996 season in the USA, achieved an uptake of only 21% [17]. However, when HCW were questioned on their reasons for refusing vaccination and when these concerns were addressed during the following campaign, coverage was increased to 38%. Similarly, Swiss HCW were questioned on their attitudes regarding influenza and vaccination and their answers were used to design interventions to improve coverage [30]. This worked, as coverage increased from 10% (1995–1996) to 26–37% (1996–1997). More recently, a significant increase of vaccination rates among the staff of 25 German hospitals over 5 years was achieved using posters in the wards and common areas, combined with active support from hospital management [50].

Figure 1. Healthcare worker influenza vaccination rates in 32 publications classed by region and by whether vaccine was provided free of charge and whether vaccination was actively promoted through an information campaign.

Only one European study had an uptake of > 50% [31]. In this hospital, free vaccination was actively promoted and frequently available at immunization clinics. Campaign advertisements in the monthly hospital newsletter included local epidemiological data, and the rational and benefits of vaccination. Coverage in the European studies was generally lower than in the USA, paralleling the difference in national rates between the two regions [2, 49]. One British campaign reported success with a rate of just 4.5%, since this was double that of the previous year [34]. Cultural and political issues have been evoked to explain these differences [33], however other factors may be involved:

Ease of access to vaccination: In a UK study, vaccine was free, but personnel had to consult their general practitioner to obtain it [40].

Influenza education: Two programs advertised vaccination (notice board announcements, e-mails etc), but no educational component was included [32, 43]. In two other cases, the information/educational campaigns were insufficient [35] or poorly adapted to the target audience [34]. In the first case HCW remained largely unaware of the vaccine-availability. In the second, physicians deemed the information insufficiently scientific and inappropriately relayed by non-medical managers.

Coverage differed between physicians and nurses: US physicians had higher coverage than US nurses [24], while in the UK the opposite was true [43]. Educational differences between these professions may impact uptake by influencing beliefs and attitudes. But it is also possible that these groups simply respond differently to different campaign-types. This is suggested by researchers stressing the need of separate strategies for separate groups: easily accessible vaccination for physicians, and education for non-physicians [22].

Education programs should address the most frequent anti-vaccination ideas. A perceived lack of vaccine efficacy was a frequent dissuasion. Yet the efficacy of influenza vaccines among adults is 70–90% against confirmed influenza when the vaccine strains match the circulating strains [51]. Immunization has been shown to significantly reduce influenza like and, upper respiratory illnesses and sick leave for influenza in HCW and other healthy working adults [52–54].

Although “to protect oneself” was the main idea encouraging immunization, this is not the primary intention of most recommendations. By targeting HCW, recommendations seek to protect patients or frail elderly persons in care [2, 14, 45]. The fact that “to protect one’s patients” was a key motivation, suggests that some HCW understand this. However, the recurrent “not at risk”, “doubt that influenza is a serious disease” and “inefficacy of the vaccine” answers indicate that not all HCW fully recognize their role in spreading influenza to their patients or the possible consequences.

A main barrier was the fear of adverse reactions. Therefore, campaigns should include factual information about possible reactions and their incidence. As with any vaccine, reactions do occur after vaccination: mainly local inflammatory reactions that are generally mild and short lived. Less frequently (< 15% of recipients) fever, myalgia, arthralgia or headache can occur [45, 51]. Influenza vaccines are generally considered to be safe [45].

Other barriers to vaccination concerned the ease of access to vaccine and the fear of injections. While the former can be overcome by careful planning, communication and the use of mobile vaccination carts, the latter can only be overcome by demonstrating that the benefits of vaccination outweigh their fears or by ultimately mandating vaccination.

In conclusion, despite recommendations for annual influenza vaccination, HCW are insufficiently vaccinated, due to two hurdles: a misperception of influenza, its risks, the role HCW play in its transmission, and the importance and risks of vaccination and a lack (or perceived lack) of accessible free vaccine. Several vaccination programs have successfully overcome these hurdles. While others have failed, possibly due to their suboptimal content or conduct. Those responsible for influenza vaccination programs might consider adopting an iterative approach to improving coverage. By integrating a survey of HCW beliefs and attitudes as a routine and integral part of a campaign, the answers collected can be used to refine the next season’s campaign.

Influenza vaccination campaigns will only be effective in the long run if HCW understand their role in influenza-transmission and prevention, and if vaccination is free and convenient. Concerted efforts are required to attain these goals and fulfill recommendations.

Acknowledgements

The authors thank Jeremy P. Grierson PhD for editorial assistance.

References

1. Directive 2000/54/EC of the European Parliament and of the Council of 18 September 2000 on the protection of workers from risks related to exposure to biological agents at work. Official Journal of the European Communities 2000.
2. Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB: Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2004; 53(RR-6): 1–40.
3. van Essen GA, Palache AM, Forleo E, Fedson DS: Influenza vaccination in 2000: recommendations and vaccine use in 50 developed and rapidly developing countries. Vaccine 2003; 21: 1780–1785, doi: 10.1016/S0264-410X(03)00072-0.
4. Odelin MF, Pozzetto B, Aymard M, Defayolle M, Jolly-Million J: Role of influenza vaccination in the elderly during an epidemic of A/H1N1 virus in 1988-1989: clinical and serological data. Gerontology 1993; 39: 109–116.
5. Elder AG, O’Donnell B, McCruden EA, Symington IS, Carman WF: Incidence and recall of influenza in a cohort of Glasgow health-care workers during the 1993-4 epidemic: results of serum testing and questionnaire. Br Med J 1996; 313: 1241–1242.
6. Weingarten S, Riedinger M, Bolton LB, Miles P, Ault M: Barriers to influenza vaccine acceptance. A survey of physicians and nurses. Am J Infect Control 1989; 17: 202–207.
7. Salgado CD, Farr BM, Hall KK, Hayden FG: Influenza in the acute hospital setting. Lancet Infect Dis 2002; 2: 145–155.
8. Stott DJ, Kerr G, Carman WF: Nosocomial transmission of influenza. Occup Med 2002; 52: 249–253.
9. Guy RJ, Di Natale R, Kelly HA, Lambert SB, Tobin S, Robinson PM, Tallis G, Hampson AW: Influenza outbreaks in aged-care facilities: staff vaccination and the emerging use of antiviral therapy. Med J Aust 2004; 180: 640–642.
10. 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: 918–922.
11. Beguin C, Boland B, Ninane J: Health care workers: vectors of influenza virus? Low vaccination rate among hospital health care workers. Am J Med Qual 1998; 13: 223–227.
12. Lehrke P, Nuebling M, Hofmann F, Stoessel U: Attitudes of homoeopathic physicians towards vaccination. Vaccine 2001; 19: 4859–4864.
13. Dash GP, Fauerbach L, Pfeiffer J, Soule B, Bartley J, Barnard BM, Lundstrom T, Andrus M: APIC position paper: improving health care worker influenza immunization rates. Am J Infect Control 2004; 32: 123–125, doi: 10.1016/j.ajic.2004.03.001.
14. Orr P: An Advisory Committee Statement (ACS). National Advisory Committee on Immunization (NACI). Statement on influenza vaccination for the 2004–2005 season. Can Commun Dis Rep 2004; 30: 1–32.
15. Stevenson CG, McArthur MA, Naus M, Abraham E, McGeer AJ: Prevention of influenza and pneumococcal pneumonia in Canadian long-term care facilities: how are we doing? Can Med Assoc J 2001; 164: 1413–1419.
16. Ohrt CK, McKinney WP: Achieving compliance with influenza immunization of medical house staff and students. A randomized controlled trial. J Am Med Assoc 1992; 267: 1377–1380.
17. Begue RE, Gee SQ: Improving influenza immunization among healthcare workers. Infect Control Hosp Epidemiol 1998; 19: 518–520.
18. Christian MA: Influenza and hepatitis B vaccine acceptance: a survey of health care workers. Am J Infect Control 1991; 19: 177–184.
19. Heimberger T, Chang HG, Shaikh M, Crotty L, Morse D, Birkhead G: Knowledge and attitudes of healthcare workers about influenza: why are they not getting vaccinated? Infect Control Hosp Epidemiol 1995; 16: 412–415.
20. Lester RT, McGeer A, Tomlinson G, Detsky AS: Use of, effectiveness of, and attitudes regarding influenza vaccine among house staff. Infect Control Hosp Epidemiol 2003; 24: 839–844.
21. Manuel DG, Henry B, Hockin J, Naus M: Health behavior associated with influenza vaccination among healthcare workers in long-term-care facilities. Infect Control Hosp Epidemiol 2002; 23: 609–614.
22. Martinello RA, Jones L, Topal JE: Correlation between healthcare workers’ knowledge of influenza vaccine and vaccine receipt. Infect Control Hosp Epidemiol 2003; 24: 845–847.
23. Nafziger DA, Herwaldt LA: Attitudes of internal medicine residents regarding influenza vaccination. Infect Control Hosp Epidemiol 1994; 15: 32–35.
24. Nichol KL, Hauge M: Influenza vaccination of healthcare workers. Infect Control Hosp Epidemiol 1997; 18: 189–194.
25. Pachucki CT, Lentino JR, Jackson GG: Attitudes and behavior of health care personnel regarding the use and efficacy of influenza vaccine. J Infect Dis 1985; 151: 1170–1171.
26. Thomas DR, Winsted B, Koontz C: Improving neglected influenza vaccination among healthcare workers in long-term care. J Am Geriatr Soc 1993; 41: 928–930.
27. Watanakunakorn C, Ellis G, Gemmel D: Attitude of healthcare personnel regarding influenza immunization. Infect Control Hosp Epidemiol 1993; 14: 17–20.
28. Yassi A, Murdzak C, Cheang M, Tran N, Aoki FY: Influenza immunization: knowledge, attitude and behaviour of health care workers. Can J Infect Control 1994; 9: 103–108.
29. Ballada D, Biasio LR, Cascio G, D’Alessandro D, Donatelli I, Fara GM, Pozzi T, Profeta ML, Squarcione S, Riccò D, Todisco T, Vacca F: Attitudes and behavior of health care personnel regarding influenza vaccination. Eur J Epidemiol 1994; 10: 63–68.
30. Harbarth S, Siegrist CA, Schira JC, Wunderli W, Pittet D: Influenza immunization: improving compliance of healthcare workers. Infect Control Hosp Epidemiol 1998; 19: 337–342.
31. Heininger U, Bachler M, Schaad UB: Attitudes of pediatricians regarding influenza self-immunization: a survey in a Swiss university children’s hospital. Pediatr Infect Dis J 2003; 22: 391–394.
32. O’Rorke C, Bourke W, Bedford D, Howell F: Uptake of influenza vaccine by healthcare workers in an acute hospital in Ireland. Ir Med J 2003; 96(7): 207–209.
33. Qureshi AM, Hughes NJ, Murphy E, Primrose WR: Factors influencing uptake of influenza vaccination among hospital-based health care workers. Occup Med 2004; 54: 197–201.
34. Smedley J, Palmer C, Baird J, Barker M: A survey of the delivery and uptake of influenza vaccine among health care workers. Occup Med 2002; 52: 271–276.
35. Stephenson I, Roper JP, Nicholson KG: Healthcare workers and their attitudes to influenza vaccination. Commun Dis Public Health 2002; 5: 247–252.
36. Habib S, Rishpon S, Rubin L: Influenza vaccination among healthcare workers. Isr Med Assoc J 2000; 2: 899–901.
37. Halliday L, Thomson JA, Roberts L, Bowen S, Mead C: Influenza vaccination of staff in aged care facilities in the ACT: how can we improve the uptake of influenza vaccine? Aust N Z J Public Health 2003; 27: 70–75.
38. Murray SB, Skull SA: Poor health care worker vaccination coverage and knowledge of vaccination recommendations in a tertiary Australia hospital. Aust N Z J Public Health 2002; 26: 65–68.
39. Doebbeling BN, Edmond MB, Davis CS, Woodin JR, Zeitler RR: Influenza vaccination of health care workers: evaluation of factors that are important in acceptance. Prev Med 1997; 26: 68–77.
40. Dey P, Halder S, Collins S, Benons L, Woodman C: Promoting uptake of influenza vaccination among health care workers: a randomized controlled trial. J Public Health Med 2001; 23: 346–348.
41. Hall KL, Holmes SS, Evans ME: Increasing hospital employee participation in an influenza vaccine program. Am J Infect Control 1998; 26: 367–368.
42. Baron G, De Wals P, Milord F: Vaccination practices of Quebec family physicians. Influenza vaccination status and professional practices for influenza vaccination. Can Fam Physician 2001; 47: 2261–2266.
43. Harrison J, Abbott P: Vaccination against influenza: UK health care workers not on-message. Occup Med 2002; 52: 277–279.
44. Akinosi B, Ramaiah S, Pugh RN: Survey of NHS staff attitudes to influenza immunisation. Commun Dis Public Health 2002; 5: 132–133.
45. Influenza vaccines: Recommendations for the use of inactivated influenza vaccines and other preventive measures. Wkly Epidemiol Rec 2000; 75: 281–288.
46. Potter J, Stott DJ, Roberts MA, Elder AG, O’Donnell B, Knight PV, Carman WF: Influenza vaccination of health care workers in long-term-care hospitals reduces the mortality of elderly patients. J Infect Dis 1997; 175: 1–6.
47. Carman WF, Elder AG, Wallace LA, McAulay K, Walker A, Murry GD, Stott DJ: Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: a randomised controlled trial. Lancet 2000; 355: 93–97.
48. Prevention and control of influenza pandemics and annual epidemics. Fifty-Sixth World Health Assembly, WHA56.19, Agenda Item 14.14, 2005.
49. Kroneman M, Paget WJ, van Essen GA: Influenza vaccination in Europe: an inventory of strategies to reach target populations and optimise vaccination uptake. Euro Surveill 2003; 8: 130–138.
50. Hallauer JF, Neuschaefer-Rube N: Influenza vaccination of hospital staff in Germany: a five-year survey on vaccination coverage and policies: identified deficits in influenza immunisation campaigns for hospital employees. Soz Praventivmed 2005; 50: 38–44.
51. Fukuda K, Levandowski RA, Bridges CB, Cox NJ: Inactivated Influenza Vaccines. In: Plotkin SA, Orenstein WA (eds): Vaccines, 4th edn. Saunders, Philadelphia, PA, 2004, pp 339–370.
52. Wilde JA, McMillan JA, Serwint J, Butta J, O’Riordan MA, Steinhoff MC: Effectiveness of influenza vaccine in health care professionals: a randomized trial. J Am Med Assoc 1999; 281: 908–913.
53. Nichol KL, Lind A, Margolis KL, Murdoch M, McFadden R, Hauge M, Magnan S, Drake M: The effectiveness of vaccination against influenza in healthy, working adults. N Engl J Med 1995; 333: 889–893.
54. Saxen H, Virtanen M: Randomized, placebo-controlled double blind study on the efficacy of influenza immunization on absenteeism of health care workers. Pediatr Infect Dis J 1999; 18: 779–783.

---

F. Hofmann (corresponding author)
Bergische Universität Wuppertal, Fachbereich D – Abteilung Sicherheitstechnik, FG Arbeitsphysiologie, Arbeitsmedizin und Infektionsschutz, Gaußstr. 20, 42097 Wuppertal, Germany;
Phone: (+49/202) 439-2069, Fax: -2068, e-mail: fhofmann@uni-wuppertal.de
C. Ferracin, G. Marsh, R. Dumas
Medical Affairs, sanofi pasteur, Lyon, France

Received: July 27, 2005 • Revision accepted: December 13, 2005