- Email: [email protected]
Influenza and pneumococcal vaccination in Scottish nursing homes: coverage, policies and reasons for receipt and non-receipt of vaccine
Vaccine 20 (2002) 2516–2522
Influenza and pneumococcal vaccination in Scottish nursing homes: coverage, policies and reasons for receipt and non-receipt of vaccine Moe H. Kyaw a,b,∗ , Beverley Wayne b , Eileen M. Holmes a,c , Ian G. Jones b , Harry Campbell a b
a Department of Public Health Sciences, University of Edinburgh, Edinburgh, UK Scottish Centre for Infection and Environmental Health, Clifton House, Clifton Place, Glasgow G3 7LN, UK c Department of Statistics of Statistics and Modelling Science, University of Strathclyde, Glasgow, UK
Received 20 November 2001; received in revised form 25 February 2002; accepted 11 March 2002
Abstract A national survey was carried out to determine the coverage of influenza and pneumococcal vaccines, policies, reasons for receipt, non-receipt of vaccine and strategies to improve vaccine coverage in Scottish nursing homes. Of the 550 nursing homes, 72% (394) participated in the study. Overall coverage was 85% for influenza vaccine in 2001–2002 season and 11% for pneumococcal vaccine in the last 5-year period. Only 6% (23/394) of homes were reported to have a systematic immunization record. The most frequently stated reasons for improved coverage of both vaccines were clear immunization policies (76%), awareness and education for staff and residents (68%), and consent on behalf of the incompetent residents (66%). The presence of vaccination policies was higher for influenza vaccine than pneumococcal vaccine expressed as verbal agreement (27% versus 3%), written policies with set target (24% versus 5%) and written policies without set target (17% versus 2%). Advice from the members of the community health care team was the principal reason for the receipt of both vaccines. The predominant reasons for non-receipt of vaccine were refusal by residents and family members (both vaccines) and lack of advice from general practitioners (pneumococcal vaccine). The substantial disparity in coverage of influenza and pneumococcal vaccine reflects the lack of national recommendations and policies for reimbursements for pneumococcal vaccination. These data suggest that greater efforts are needed to improve prevention behaviors of health care professionals and the public, organized vaccine delivery strategies and systematic vaccination documents to increase influenza and pneumococcal vaccination rates in nursing homes and other long-term care facilities. © 2002 Elsevier Science Ltd. All rights reserved. Keywords: Scottish nursing homes; Influenza and pneumococcal vaccination; Policies
1. Introduction The elderly are at-risk of influenza and pneumococcal disease. Most elderly living in nursing homes have chronic medical conditions [1], and therefore have higher risk of complications and mortality from influenza and pneumococcal disease than the elderly living in the community [2–4]. Outbreaks of influenza and pneumococcal disease have been well documented in nursing homes [5–7]. In addition, data from the US shows that the prevalence of drug resistant pneumococci is increasing in the elderly [8]. Drug resistant pneumococcal strain (serotype 23) has been reported as a cause of an outbreak of pneumococcal disease in a nursing home with low vaccine coverage [6]. Susceptibility to infection and transmission of influenza and pneumococcal disease can be prevented by vaccina∗ Corresponding author. Tel.: +44-141-300-1184; fax: +44-141-300-1170. E-mail address: [email protected] (M.H. Kyaw).
tion [9,10]. Studies show that the estimated effectiveness of influenza vaccine is 43–55% against pneumonia [9] and >42% against influenza-like illness [11] among elderly nursing home residents. Pneumococcal vaccine is 61–75% effective in preventing bacteraemia or meningitis in the elderly [12,13]. The administration of both vaccines is also considered cost-effective in the elderly [14–16]. Despite this evidence, influenza and pneumococcal vaccines are underused in the UK [17,18]. Influenza vaccination is currently targeted to all elderly (aged 65 years and above) and residents in long-term care facilities. However, pneumococcal vaccination is not yet recommended for these groups in the UK [19]. There are limited data on coverage and polices of influenza and pneumococcal vaccinations in UK nursing homes. In addition, little is known of the reasons for receipt and non-receipt of these vaccines in elderly nursing home residents. We therefore report national coverage of and policies for influenza and pneumococcal vaccines together with the factors which may be associated with the use and receipt of both vaccines in Scottish nursing homes. These data
0264-410X/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 2 6 4 - 4 1 0 X ( 0 2 ) 0 0 1 7 7 - 9
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
could help to develop strategies to improve coverage of influenza and pneumococcal vaccines in nursing homes and other long-term care facilities.
2. Methods A list of nursing homes and their addresses was obtained from the Information and Statistics Division (ISD) of the Common Services Agency of the National Health Service (NHS), Scotland. In 2001, there were 550 licensed nursing homes in the whole of Scotland, which provided nursing care primarily to the elderly population. A postal questionnaire was sent to each nursing home on 12 June 2001 with a request for it to be completed by the nurse in charge or care manager. A reminder was posted to non-respondents on 2 August 2001. The questionnaire requested information on the number of residents, the number of general practices looking after residents, the existence of immunization record, the number of residents receiving influenza vaccine or pneumococcal vaccine or both vaccines, vaccination policies, the factors associated with improved vaccine coverage and the reasons for receipt and non-receipt of vaccine, selected from a number of key reasons defined in a pilot study. Information was requested as aggregated format. Therefore, data are completely anonymous and do not identify individual elderly living in each nursing home. Information was entered in DataEase version 4.5 and data analyses were carried out in SPSS version 10 and Stata (Stata Corporation, version 6.0, 1999, College Station, Texas). Since the data are non-normally distributed, non-parametric tests were applied. Mann–Whitney tests were used to compare median coverage where the covariate binary and Kruskal–Wallis tests were used when the covariate had more than two levels.
0.007) although this association was not observed in pneumococcal vaccination rates (P = 0.71). Nursing home with a pneumococcal vaccine policy had significantly higher median coverage rates of this vaccine than those who did not (P = 0.007). However, the presence of an influenza vaccination policy appeared to have no association with influenza vaccine coverage (P = 0.54).
4. Vaccine coverage Although 394 returned the questionnaire, information on vaccine coverage of influenza and pneumococcal vaccinations was provided by 328 homes and 142 homes, respectively. Thus, vaccine coverage was calculated based on the appropriate denominators. Overall vaccine coverage was 85% for enfluenza vaccine in 2001–2002 season and 11% for pneumococcal vaccine in the last 5 years among 13,700 residents. Coverage of influenza and pneumococcal vaccines in residents by nursing home is shown in Table 1. Coverage of influenza vaccine was >70% of residents in 85% of nursing homes. The majority of nursing homes (74%) had less than 5% pneumococcal vaccine coverage among their residents.
5. Factors suggested for improving vaccine coverage The most frequently reported reasons for improving coverage of both vaccines were a clear immunization policy Table 1 Influenza and pneumococcal vaccine coverage among nursing homes which provided information on vaccination Percentage of residents received
3. Results Of the 550 nursing homes, 394 homes (72%) responded to the questionnaire. The mean size of home was 46 residents. The number of general practices looking after residents ranged from 1 to 24 practices per nursing home (mean = 5). A systematic immunization record, which was defined as complete documentation of immunization history, existed in 6% (23/394) of nursing homes. No significant differences in median influenza vaccination rates were found for the following covariates: areas of Scotland by Health Boards (P = 0.37), the presence of systematic immunization record (P = 0.47), the number of GPs per home (<5 GPs = 88% versus >5 GPs = 89%, P = 0.69). Similar results were obtained for the pneumococcal vaccine (P = 0.37, 0.55 and <5 GPs = 0% versus >5 GPs = 0%, P = 0.10, respectively). The number of residents was found to significantly affect the median coverage of influenza vaccination (<30 residents = 89% versus 31–50 residents = 90% versus >51 residents = 85%, P =
2517
Influenza vaccine <40 40–49 50–59 60–69 70–79 80–89 90–99 100 Total Mean Median Pneumococcal vaccine <5 5–9 10–19 20–49 >50 Total Mean Median
No. of nursing homes with vaccine coverage (%) 8 5 12 26 36 86 97 59
(2) (2) (4) (8) (11) (26) (30) (18)
328 (100) – (85) – (88) 105 11 8 6 12
(74) (8) (6) (4) (8)
142 (100) – (11) – (0)
2518
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
Fig. 1. Factors which could improve coverage of influenza and pneumococcal vaccine.
Fig. 2. Policies for vaccination of influenza, pneumococcal and both vaccines.
(76%), awareness and education for staff and residents (68%) and consent on behalf of the incompetent residents (66%) (Fig. 1). Other reported factors associated with vaccinations were organized vaccine programs by nursing staff, active promotion of vaccine, annual review of vaccination status and improved immunization records.
6. Vaccination policies Of the respondents (394 homes), 68% (n = 260), 10% (n = 42) and 10% (n = 42) of nursing homes had one form of vaccination policies for influenza, pneumococcal or both vaccines, respectively. The presence of policies for influenza
Fig. 3. Main reasons for receipt of influenza and pneumococcal vaccine.
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
2519
Fig. 4. Main reasons for non-receipt of influenza and pneumococcal vaccine.
vaccination was higher than pneumococcal vaccination: verbal agreement (27% versus 3%), written policies with set target (24% versus 5%) and written policies without set target (17% versus 2%) (Fig. 2). Over 70% of nursing homes did not provide information on pneumococcal vaccination policies.
7. Main reasons for receipt and non-receipt of vaccine The most reported reasons for receipt of influenza vaccine were advice from community doctors and nurses (72%), nursing home policies and guidelines (57%) and efficacy against respiratory infection (54%) (Fig. 3). Similar reasons were indicated for receiving pneumococcal vaccine (20, 12 and 13%, respectively). The most common reasons for non-receipt of influenza vaccine were refusal by residents (73%), and family members (41%) (Fig. 4). The predominant reasons for non-receipt of pneumococcal vaccine were that it was not recommended by their GPs (19%) and refusals by residents (15%).
8. Discussion Overall, coverage of influenza and pneumococcal vaccine was 85 and 11%, respectively of residents in the present study. No differences in the average number of residents and the presence of immunization policies were documented between nursing homes that took part and did not take part in the survey. This suggests that our results appear to reflect all nursing homes throughout Scotland. Previous surveys in the UK [20] and US [21] showed an increased trend in coverage of influenza vaccine in the elderly over time. In the UK, coverage of influenza vaccine in the elderly nursing home residents was 45% in 1988–1989 [2], 67% in 1991–1992 [22], 77% in 1995 [23] and 89% in 1998–1999 [20]. The
rate of influenza vaccination in the present study exceeded the target level of 65% among recommended groups in Scotland [24]. Nevertheless, about 8% of nursing homes failed to achieve 60–69% coverage of influenza vaccine. The observed high coverage of influenza vaccine is likely to be due to growing awareness of vaccination and changes in national vaccination recommendations and reimbursement policies by the UK Department of Health. Influenza vaccine coverage of above 80% can reduce the transmission of influenza virus in nursing homes by indirect protection (herd immunity) [5,25,26]. Therefore, nursing homes with high vaccine coverage are not only less likely to have outbreaks than those with low vaccine coverage but also more likely to reduce influenza morbidity and mortality. We found that 74% of nursing homes had optimal influenza vaccine coverage of between 80 and 100% of residents. Since the records of influenza and pneumococcal vaccinations were based on nursing home medical/nursing records rather than patient GP records, our results are likely to underestimate the coverage of these vaccines. To our knowledge, this is the first national survey on coverage of pneumococcal vaccine in nursing home residents in the UK. Coverage of pneumococcal vaccine was very low (11%) in the present study. Pneumococcal vaccine coverage was higher in US nursing homes (38%) [27] and in Canadian long-term care facilities (71%) [28] in 1999. Although nursing homes have closed and high-risk populations, which provide ideal conditions for spread of pneumococci, outbreaks of pneumococcal disease have been rarely reported in UK nursing homes. The UK epidemiological studies have shown that the incidence of invasive pneumococcal disease in the elderly, aged 65 years and above, is 21–36 per 100,000 persons [29,30], but rates vary substantially in Europe and North America, ranging from 25 to 90 per 100,000 persons [31]. Case-fatality rates range from 18 to 40% [32–34]. Current 23-valent polysaccharide vaccine included stereotypes caused all reported outbreaks [7,35]. Studies indicate that outbreaks of pneumococcal disease are likely to occur in
2520
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
nursing homes with low vaccine coverage [3,6,36]. These data highlight the importance of pneumococcal vaccination in the elderly nursing home residents in the UK. Therefore, re-evaluation of current vaccination policies is needed in the UK. Our data show that there was a substantial disparity in the coverage of influenza and pneumococcal vaccine. Previous studies in the US and UK indicate that low coverage of pneumococcal vaccine may reflect uncertainty of vaccine effectiveness, misconception about adverse reactions, lack of reimbursements and policies and unclear recommendations [37,38]. In Scotland, GP payment mechanisms similar to influenza vaccination are not yet in place for pneumococcal vaccine and may influence its administration to the elderly and other high-risk groups.
9. Reasons for receipt and non-receipt of vaccines In common with previous surveys [3,39,40], we found that recommendations from community doctors and nurses were the principal reason for being vaccinated. However, in comparison with influenza vaccination, pneumococcal vaccination was more than three-fold less likely to be recommended. Surveys from the UK and US highlighted that between 73 and 91% of nursing homes provided pneumococcal vaccine based on physician discretion [3,40]. Polices for vaccination was reported to be an important factor for receiving influenza and pneumococcal vaccine. Similar to our previous study in general practices and hospital care settings [18,38], the presence of vaccination policies was reported to be an effective means for increasing pneumococcal vaccination rates in nursing homes. In keeping with other reports [3,41], nursing homes in Scotland are less likely to have policies on pneumococcal vaccination than influenza vaccination. We also found that the perceived efficacy of vaccine was an important reason for receipt of vaccines. Influenza vaccination behavior in high-risk patients also showed similar findings [39]. The predominant reason for not receiving influenza or pneumococcal vaccine was due to refusal of vaccine by residents or family members or no specific reason in the present study. Therefore, greater emphasis is needed in increasing awareness of risk of disease and the benefits of vaccination in nursing home residents and their family members.
10. Strategies for vaccination The extension of pneumococcal vaccination policy to residents of long-term care facilities offers the opportunity to vaccinate at the time of annual influenza vaccination. This can undoubtedly enhance the use of pneumococcal vaccine in this at-risk group. In the US, a national objective has been set to achieve coverage of influenza and pneumococcal vaccine in over 90% for residents of long-term care facilities and other high-risk groups for the year 2010 [42].
There is no clear set target for pneumococcal vaccination in the UK. In the present study, only 6% of nursing homes had systematic vaccination records despite half of them expressing the view that these would improve vaccine coverage. Surveys have shown that the determination of pneumococcal vaccination status in individual long-term care residents is difficult and represents a major barrier for pneumococcal vaccination because of misconceptions about the risk of adverse reactions following revaccination [3,43]. The available evidence indicates that second dose of pneumococcal vaccine does not appear to be associated with serious adverse reactions [44,45]. Thus, pneumococcal vaccine could be given to patients with unknown vaccination history [10,46]. Studies in US nursing homes identified that vaccination was low priority among physicians [3,36]. Improved knowledge of adult vaccination in health care professionals may reduce missed opportunities for vaccination during consultations. Difficulty in obtaining consent on behalf of incompetent residents was stated to be one of the important barriers to increased influenza and pneumococcal vaccination rates and this has been noted by others [47]. Data from Canada indicate that obtaining consent for vaccination on admission for current and future years is associated with higher influenza and pneumococcal vaccination rates [28]. Our findings also showed that vaccination programs organized by nursing staff were considered as an effective strategy for enhancing coverage of influenza and pneumococcal vaccine. It has been documented that organized vaccination programs are the most important strategy to improve influenza and pneumococcal vaccination rates [48]. Standing orders for nurses could allow for the easier administration of vaccines in long-term care facilities [49].
11. Conclusions Our results highlight a large gap between influenza and pneumococcal vaccination rates in nursing homes. This is mainly due to lack of national recommendations and reimbursement policies for pneumococcal vaccination. Changes in attitudes, knowledge and practice of healthcare professionals and public together with the implementation of organized vaccine delivery strategies and systematic vaccination records are crucial in improving vaccination rates in nursing home residents and other long-term care facilities. Further studies in understanding of patients and clinicians vaccine preventable behaviors would aid in increasing coverage of these vaccines in high-risk patients.
Acknowledgements The authors would like to thank the staff in nursing homes throughout Scotland for their cooperation in this survey. We
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
are also grateful to the staff at the Scottish Centre for Infection and Environmental Health and the Information and Statistics Division in Scotland, in particular to Kenny McIntyre and Patricia Cassels, for their help in obtaining information and data entry. References [1] Muder RR. Pneumonia in residents of long-term care facilities: epidemiology, etiology, management and prevention. Am J Med 1998;105:319–30. [2] Nicholson K, Baker D, Farquhar A, et al. Acute upper respiratory tract viral illness and influenza immunization in homes for the elderly. Epidemiol Infect 1990;105:609–18. [3] Quick RE, Hoge CW, Hamilton DJ, Whitney C, Borges M, Kobayashi J. Underutilization of pneumococcal vaccine in nursing homes in Washington State: report of serotype-specific outbreak and a survey. Am J Med 1993;94:149–52. [4] Monto A, Ohmit S, Margulies J, et al. Medical practice-based influenza surveillance: viral prevalence and assessment of morbidity. Am J Epidemiol 1995;141:502–6. [5] Arden N, Monto A, Ohmit S. Vaccine use and the risk of outbreaks in a sample of nursing homes during an influenza epidemic. Am J Public Health 1995;85:399–401. [6] Nuorti J, Butler J, Crutcher JM. Outbreak of multidrug-resistant pneumococcal pneumonia and bacteraemia among unvaccinated nursing home residents. N Engl J Med 1998;338:1861–8. [7] Gleich S, Morad Y, Echague R, Miller JR, Kornblum J, Sampson JS, et al. Streptococcus pneumoniae serotype 4 outbreak in a home for the aged: report and review of recent outbreaks. Infect Control Hosp Epidemiol 2000;21:711–7. [8] Butler JC, Cetron MS. Pneumococcal drug resistance: the new special enemy of old age. Clin Infect Dis 1999;28:730–5. [9] Monto AS, Hornbuckle K, Ohmit SE. Influenza vaccine effectiveness among elderly nursing home residents: a cohort study. Am J Epidemiol 2001;154:155–60. [10] MMWR. Prevention of pneumococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR 1997;46:1–24. [11] Ohmit S, Arden N, Monto A. Effectiveness of inactivated influenza vaccine among nursing home residents during an influenza type A (H3N2) epidemic. J Am Geriatr Soc 1999;47:165–71. [12] Shapiro ED, Berg AT, Austrian R, Schroeder D, Parcells V, Margolis A, Adair RK, Clemens JD. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine. N Engl J Med, 1991;325:1453–60. [13] Butler J, Breiman R, Campbell J, Lipman H, Broome C, Facklam R. Pneumococcal polysaccharide vaccine efficacy: an evaluation of current recommendations. JAMA 1993;270:1826–31. [14] Postma M, Baltussen R, Heijnen M, de Berg LT, Jager J. Pharmacoeconomic of influenza vaccination in the elderly: reviewing the available evidence. Drugs Ageing 2000;17:217–27. [15] Nichol K, Baken L, Wuorenma J, Nelson A. The health and economic benefits associated with pneumococcal vaccination of elderly persons with chronic lung disease. Arch Intern Med 1999;159:2437–42. [16] Ament A, Baltussen R, Duru G, et al. The cost effectiveness of pneumococcal vaccination for older people: a study in five western European countries. Clin Infect Dis 2000;31:444–50. [17] McDonald P, Friedman E, Banks A, Anderson R, Carman V. Pneumococcal vaccine campaign based in general practices. BMJ 1997;314:1094–8. [18] Kyaw MH, Wayne B, Chalmers J, Jones IG, Campbell H. Influenza and pneumococcal vaccine distribution and use in primary care and hospital settings in Scotland: coverage, practice and policies. Epidemiol Infect, in press.
2521
[19] Department of Health. Immunisation against infectious disease London: HMSO, 1996. [20] Gupta A, Morris G, Thomas P, Hasan M. Influenza vaccination coverage in old people’s home in Camarthenshire, UK, during the winter of 1998/99. Vaccine 2000;18:2471–5. [21] MMWR. Influenza and pneumococcal vaccination levels among persons aged ≥65 years—United States. MMWR 2001;50:532–7. [22] Evans M, Wilkinson E. How complete is influenza vaccination coverage? A study in 75 nursing and residential home for the elderly people. Br J Clin Pract 1995;45:419–21. [23] Evans M. Monitoring influenza immunisation uptake in nursing homes. Commun Dis Rep 1996;6:R170–2. [24] Chief Medical Officer (CMO). Influenza immunisation. Scottish Executive. Health Department, 2001. [25] Patriarca P, Weber J, Parker R. Risk factors for outbreaks of influenza in nursing homes: a case control study. Am J Epidemiol 1986;124:114–9. [26] Gross P, Rodstein M, LaMontagne J. Epidemiology of acute respiratory illness during an influenza outbreak in a nursing home. Arch Intern Med 1988;148:559–61. [27] Buikema A, Singleton J, Sneller V et al. Influenza and pneumococcal vaccination in nursing homes, US, 1995–1999, In: Abstracts from the 35th National Immunization Conference. Atlanta, Georgia, 2001 [Abstract]. [28] 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? CMAJ 2001;164:1413– 9. [29] Sleeman K, Knox K, George R. Invasive pneumcoccal disease in England and Wales: vaccination implications. J Infect Dis 2001;183:239–46. [30] Kyaw MH, Clarke S, Jones IG, et al. Incidence of invasive pneumococcal disease in Scotland. Epidemiol Infect, in press. [31] Butler JC, Schuchat A. Epidemiology of pneumococcal infections in the elderly. Drugs Aging 1999;15:11–9. [32] Breiman R, Spika J, Navarro V, Darden PM, Darby CP. Pneumococcal bacteremia in Charleston County, South Carolina a decade later. Arch Intern Med 1990;150:1401–5. [33] Plouffe JF, Breiman RF, Facklam RR. Bacteraemia with Streptococcus pneumoniae: implications for therapy and prevention. JAMA 1996;275:194–8. [34] Centers for Disease Control and Prevention. Active Bacterial Core Surveillance (ABCs) Report. Emerging Infections Program Network Streptococcus pneumoniae, 2000 (preliminary). Available at: http:www.cdc.gov/ncidod/dbmd/abcs. Accessed 10 November 2001. [35] Sheppard D, Bartlett K, Lampiris H. Streptococcus pneumoniae transmission in chronic-care facilities: description of an outbreak and review of management strategies. Infect Control Hosp Epidemiol 1998;19:851–3. [36] MMWR. Outbreaks of pneumococcal pneumonia among unvaccinated residents in chronic care facilities—Massachusetts, October 1995, Oklahoma, February 1996, and Maryland, May–June 1996. MMWR 1997;46:60–62. [37] Fedson DS. Pneumococcal vaccination in the United States and 20 other developed countries, 1981–1996. Clin Infect Dis 1998;26:1117– 23. [38] Kyaw MH, Bramley JC, Chalmers J, Jones IG, Campbell H. Pneumococcal vaccination: opinion of general practitioners and hospital doctors in Scotland, 1999–2000. Commun Dis Public Health 2001;4:42–8. [39] Nichol K, Lofgren R, Gapinski J. Influenza vaccination: knowledge, attitudes and behaviour among high-risk outpatients. Arch Intern Med 1992;152:106–10. [40] Kyaw MH, Nguyen-Van-Tam J, Pearson J. Family doctor advice is the main determinant of pneumococcal vaccine uptake. J Epidemiol Community Health 1999;53:589–90.
2522
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
[41] Nichol KL, Grimm MB, Peterson DC. Immunizations in long-term care facilities: policies and practice. J Am Geriatr Soc 1996;44:349– 55. [42] US Department of Health and Human Services. In: Proceedings of Conference on Healthy people 2010 (in two volumes). Washington, DC: US Department of Health and Human Services, 2000. [43] MMWR. Outbreak of pneumococcal pneumonia among unvaccinated residents of a nursing home—New Jersey, April 2001. MMWR 2001;50:707–9. [44] Fine MJ, Smith MA, Carson CA, et al. Efficacy of pneumococcal vaccination in adults: a meta-analysis of randomized controlled trails. Arch Intern Med 1994;154:2666–77. [45] Jackson LA, Benson P, Sneller V-P, Butler JC, Thompson RS, Chen RT, et al. Safety of revaccination with pneumococcal polysaccharide vaccine. JAMA 1999;281:243–8.
[46] Whitney CG, Schaffner W, Butler JC. Rethinking recommendations for use of pneumococcal vaccines in adults. Clin Infect Dis 2001;33:662–75. [47] Russell ML. Influenza vaccination in Alberta long-term care facilities. CMAJ 2001;164:1423–7. [48] Nichol KL. Ten-year durability and success of an organised program to increase influenza and pneumococcal vaccination rates among high-risk adults. Am J Med 1998;105:385–92. [49] MMWR. Adult immunization programs in national strategies: quality standards and guidance for program evaluation and use of standing orders programs to increase adult vaccination rates. MMWR 2000;49:1–28.
Influenza and pneumococcal vaccination in Scottish nursing homes: coverage, policies and reasons for receipt and non-receipt of vaccine Moe H. Kyaw a,b,∗ , Beverley Wayne b , Eileen M. Holmes a,c , Ian G. Jones b , Harry Campbell a b
a Department of Public Health Sciences, University of Edinburgh, Edinburgh, UK Scottish Centre for Infection and Environmental Health, Clifton House, Clifton Place, Glasgow G3 7LN, UK c Department of Statistics of Statistics and Modelling Science, University of Strathclyde, Glasgow, UK
Received 20 November 2001; received in revised form 25 February 2002; accepted 11 March 2002
Abstract A national survey was carried out to determine the coverage of influenza and pneumococcal vaccines, policies, reasons for receipt, non-receipt of vaccine and strategies to improve vaccine coverage in Scottish nursing homes. Of the 550 nursing homes, 72% (394) participated in the study. Overall coverage was 85% for influenza vaccine in 2001–2002 season and 11% for pneumococcal vaccine in the last 5-year period. Only 6% (23/394) of homes were reported to have a systematic immunization record. The most frequently stated reasons for improved coverage of both vaccines were clear immunization policies (76%), awareness and education for staff and residents (68%), and consent on behalf of the incompetent residents (66%). The presence of vaccination policies was higher for influenza vaccine than pneumococcal vaccine expressed as verbal agreement (27% versus 3%), written policies with set target (24% versus 5%) and written policies without set target (17% versus 2%). Advice from the members of the community health care team was the principal reason for the receipt of both vaccines. The predominant reasons for non-receipt of vaccine were refusal by residents and family members (both vaccines) and lack of advice from general practitioners (pneumococcal vaccine). The substantial disparity in coverage of influenza and pneumococcal vaccine reflects the lack of national recommendations and policies for reimbursements for pneumococcal vaccination. These data suggest that greater efforts are needed to improve prevention behaviors of health care professionals and the public, organized vaccine delivery strategies and systematic vaccination documents to increase influenza and pneumococcal vaccination rates in nursing homes and other long-term care facilities. © 2002 Elsevier Science Ltd. All rights reserved. Keywords: Scottish nursing homes; Influenza and pneumococcal vaccination; Policies
1. Introduction The elderly are at-risk of influenza and pneumococcal disease. Most elderly living in nursing homes have chronic medical conditions [1], and therefore have higher risk of complications and mortality from influenza and pneumococcal disease than the elderly living in the community [2–4]. Outbreaks of influenza and pneumococcal disease have been well documented in nursing homes [5–7]. In addition, data from the US shows that the prevalence of drug resistant pneumococci is increasing in the elderly [8]. Drug resistant pneumococcal strain (serotype 23) has been reported as a cause of an outbreak of pneumococcal disease in a nursing home with low vaccine coverage [6]. Susceptibility to infection and transmission of influenza and pneumococcal disease can be prevented by vaccina∗ Corresponding author. Tel.: +44-141-300-1184; fax: +44-141-300-1170. E-mail address: [email protected] (M.H. Kyaw).
tion [9,10]. Studies show that the estimated effectiveness of influenza vaccine is 43–55% against pneumonia [9] and >42% against influenza-like illness [11] among elderly nursing home residents. Pneumococcal vaccine is 61–75% effective in preventing bacteraemia or meningitis in the elderly [12,13]. The administration of both vaccines is also considered cost-effective in the elderly [14–16]. Despite this evidence, influenza and pneumococcal vaccines are underused in the UK [17,18]. Influenza vaccination is currently targeted to all elderly (aged 65 years and above) and residents in long-term care facilities. However, pneumococcal vaccination is not yet recommended for these groups in the UK [19]. There are limited data on coverage and polices of influenza and pneumococcal vaccinations in UK nursing homes. In addition, little is known of the reasons for receipt and non-receipt of these vaccines in elderly nursing home residents. We therefore report national coverage of and policies for influenza and pneumococcal vaccines together with the factors which may be associated with the use and receipt of both vaccines in Scottish nursing homes. These data
0264-410X/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 2 6 4 - 4 1 0 X ( 0 2 ) 0 0 1 7 7 - 9
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
could help to develop strategies to improve coverage of influenza and pneumococcal vaccines in nursing homes and other long-term care facilities.
2. Methods A list of nursing homes and their addresses was obtained from the Information and Statistics Division (ISD) of the Common Services Agency of the National Health Service (NHS), Scotland. In 2001, there were 550 licensed nursing homes in the whole of Scotland, which provided nursing care primarily to the elderly population. A postal questionnaire was sent to each nursing home on 12 June 2001 with a request for it to be completed by the nurse in charge or care manager. A reminder was posted to non-respondents on 2 August 2001. The questionnaire requested information on the number of residents, the number of general practices looking after residents, the existence of immunization record, the number of residents receiving influenza vaccine or pneumococcal vaccine or both vaccines, vaccination policies, the factors associated with improved vaccine coverage and the reasons for receipt and non-receipt of vaccine, selected from a number of key reasons defined in a pilot study. Information was requested as aggregated format. Therefore, data are completely anonymous and do not identify individual elderly living in each nursing home. Information was entered in DataEase version 4.5 and data analyses were carried out in SPSS version 10 and Stata (Stata Corporation, version 6.0, 1999, College Station, Texas). Since the data are non-normally distributed, non-parametric tests were applied. Mann–Whitney tests were used to compare median coverage where the covariate binary and Kruskal–Wallis tests were used when the covariate had more than two levels.
0.007) although this association was not observed in pneumococcal vaccination rates (P = 0.71). Nursing home with a pneumococcal vaccine policy had significantly higher median coverage rates of this vaccine than those who did not (P = 0.007). However, the presence of an influenza vaccination policy appeared to have no association with influenza vaccine coverage (P = 0.54).
4. Vaccine coverage Although 394 returned the questionnaire, information on vaccine coverage of influenza and pneumococcal vaccinations was provided by 328 homes and 142 homes, respectively. Thus, vaccine coverage was calculated based on the appropriate denominators. Overall vaccine coverage was 85% for enfluenza vaccine in 2001–2002 season and 11% for pneumococcal vaccine in the last 5 years among 13,700 residents. Coverage of influenza and pneumococcal vaccines in residents by nursing home is shown in Table 1. Coverage of influenza vaccine was >70% of residents in 85% of nursing homes. The majority of nursing homes (74%) had less than 5% pneumococcal vaccine coverage among their residents.
5. Factors suggested for improving vaccine coverage The most frequently reported reasons for improving coverage of both vaccines were a clear immunization policy Table 1 Influenza and pneumococcal vaccine coverage among nursing homes which provided information on vaccination Percentage of residents received
3. Results Of the 550 nursing homes, 394 homes (72%) responded to the questionnaire. The mean size of home was 46 residents. The number of general practices looking after residents ranged from 1 to 24 practices per nursing home (mean = 5). A systematic immunization record, which was defined as complete documentation of immunization history, existed in 6% (23/394) of nursing homes. No significant differences in median influenza vaccination rates were found for the following covariates: areas of Scotland by Health Boards (P = 0.37), the presence of systematic immunization record (P = 0.47), the number of GPs per home (<5 GPs = 88% versus >5 GPs = 89%, P = 0.69). Similar results were obtained for the pneumococcal vaccine (P = 0.37, 0.55 and <5 GPs = 0% versus >5 GPs = 0%, P = 0.10, respectively). The number of residents was found to significantly affect the median coverage of influenza vaccination (<30 residents = 89% versus 31–50 residents = 90% versus >51 residents = 85%, P =
2517
Influenza vaccine <40 40–49 50–59 60–69 70–79 80–89 90–99 100 Total Mean Median Pneumococcal vaccine <5 5–9 10–19 20–49 >50 Total Mean Median
No. of nursing homes with vaccine coverage (%) 8 5 12 26 36 86 97 59
(2) (2) (4) (8) (11) (26) (30) (18)
328 (100) – (85) – (88) 105 11 8 6 12
(74) (8) (6) (4) (8)
142 (100) – (11) – (0)
2518
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
Fig. 1. Factors which could improve coverage of influenza and pneumococcal vaccine.
Fig. 2. Policies for vaccination of influenza, pneumococcal and both vaccines.
(76%), awareness and education for staff and residents (68%) and consent on behalf of the incompetent residents (66%) (Fig. 1). Other reported factors associated with vaccinations were organized vaccine programs by nursing staff, active promotion of vaccine, annual review of vaccination status and improved immunization records.
6. Vaccination policies Of the respondents (394 homes), 68% (n = 260), 10% (n = 42) and 10% (n = 42) of nursing homes had one form of vaccination policies for influenza, pneumococcal or both vaccines, respectively. The presence of policies for influenza
Fig. 3. Main reasons for receipt of influenza and pneumococcal vaccine.
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
2519
Fig. 4. Main reasons for non-receipt of influenza and pneumococcal vaccine.
vaccination was higher than pneumococcal vaccination: verbal agreement (27% versus 3%), written policies with set target (24% versus 5%) and written policies without set target (17% versus 2%) (Fig. 2). Over 70% of nursing homes did not provide information on pneumococcal vaccination policies.
7. Main reasons for receipt and non-receipt of vaccine The most reported reasons for receipt of influenza vaccine were advice from community doctors and nurses (72%), nursing home policies and guidelines (57%) and efficacy against respiratory infection (54%) (Fig. 3). Similar reasons were indicated for receiving pneumococcal vaccine (20, 12 and 13%, respectively). The most common reasons for non-receipt of influenza vaccine were refusal by residents (73%), and family members (41%) (Fig. 4). The predominant reasons for non-receipt of pneumococcal vaccine were that it was not recommended by their GPs (19%) and refusals by residents (15%).
8. Discussion Overall, coverage of influenza and pneumococcal vaccine was 85 and 11%, respectively of residents in the present study. No differences in the average number of residents and the presence of immunization policies were documented between nursing homes that took part and did not take part in the survey. This suggests that our results appear to reflect all nursing homes throughout Scotland. Previous surveys in the UK [20] and US [21] showed an increased trend in coverage of influenza vaccine in the elderly over time. In the UK, coverage of influenza vaccine in the elderly nursing home residents was 45% in 1988–1989 [2], 67% in 1991–1992 [22], 77% in 1995 [23] and 89% in 1998–1999 [20]. The
rate of influenza vaccination in the present study exceeded the target level of 65% among recommended groups in Scotland [24]. Nevertheless, about 8% of nursing homes failed to achieve 60–69% coverage of influenza vaccine. The observed high coverage of influenza vaccine is likely to be due to growing awareness of vaccination and changes in national vaccination recommendations and reimbursement policies by the UK Department of Health. Influenza vaccine coverage of above 80% can reduce the transmission of influenza virus in nursing homes by indirect protection (herd immunity) [5,25,26]. Therefore, nursing homes with high vaccine coverage are not only less likely to have outbreaks than those with low vaccine coverage but also more likely to reduce influenza morbidity and mortality. We found that 74% of nursing homes had optimal influenza vaccine coverage of between 80 and 100% of residents. Since the records of influenza and pneumococcal vaccinations were based on nursing home medical/nursing records rather than patient GP records, our results are likely to underestimate the coverage of these vaccines. To our knowledge, this is the first national survey on coverage of pneumococcal vaccine in nursing home residents in the UK. Coverage of pneumococcal vaccine was very low (11%) in the present study. Pneumococcal vaccine coverage was higher in US nursing homes (38%) [27] and in Canadian long-term care facilities (71%) [28] in 1999. Although nursing homes have closed and high-risk populations, which provide ideal conditions for spread of pneumococci, outbreaks of pneumococcal disease have been rarely reported in UK nursing homes. The UK epidemiological studies have shown that the incidence of invasive pneumococcal disease in the elderly, aged 65 years and above, is 21–36 per 100,000 persons [29,30], but rates vary substantially in Europe and North America, ranging from 25 to 90 per 100,000 persons [31]. Case-fatality rates range from 18 to 40% [32–34]. Current 23-valent polysaccharide vaccine included stereotypes caused all reported outbreaks [7,35]. Studies indicate that outbreaks of pneumococcal disease are likely to occur in
2520
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
nursing homes with low vaccine coverage [3,6,36]. These data highlight the importance of pneumococcal vaccination in the elderly nursing home residents in the UK. Therefore, re-evaluation of current vaccination policies is needed in the UK. Our data show that there was a substantial disparity in the coverage of influenza and pneumococcal vaccine. Previous studies in the US and UK indicate that low coverage of pneumococcal vaccine may reflect uncertainty of vaccine effectiveness, misconception about adverse reactions, lack of reimbursements and policies and unclear recommendations [37,38]. In Scotland, GP payment mechanisms similar to influenza vaccination are not yet in place for pneumococcal vaccine and may influence its administration to the elderly and other high-risk groups.
9. Reasons for receipt and non-receipt of vaccines In common with previous surveys [3,39,40], we found that recommendations from community doctors and nurses were the principal reason for being vaccinated. However, in comparison with influenza vaccination, pneumococcal vaccination was more than three-fold less likely to be recommended. Surveys from the UK and US highlighted that between 73 and 91% of nursing homes provided pneumococcal vaccine based on physician discretion [3,40]. Polices for vaccination was reported to be an important factor for receiving influenza and pneumococcal vaccine. Similar to our previous study in general practices and hospital care settings [18,38], the presence of vaccination policies was reported to be an effective means for increasing pneumococcal vaccination rates in nursing homes. In keeping with other reports [3,41], nursing homes in Scotland are less likely to have policies on pneumococcal vaccination than influenza vaccination. We also found that the perceived efficacy of vaccine was an important reason for receipt of vaccines. Influenza vaccination behavior in high-risk patients also showed similar findings [39]. The predominant reason for not receiving influenza or pneumococcal vaccine was due to refusal of vaccine by residents or family members or no specific reason in the present study. Therefore, greater emphasis is needed in increasing awareness of risk of disease and the benefits of vaccination in nursing home residents and their family members.
10. Strategies for vaccination The extension of pneumococcal vaccination policy to residents of long-term care facilities offers the opportunity to vaccinate at the time of annual influenza vaccination. This can undoubtedly enhance the use of pneumococcal vaccine in this at-risk group. In the US, a national objective has been set to achieve coverage of influenza and pneumococcal vaccine in over 90% for residents of long-term care facilities and other high-risk groups for the year 2010 [42].
There is no clear set target for pneumococcal vaccination in the UK. In the present study, only 6% of nursing homes had systematic vaccination records despite half of them expressing the view that these would improve vaccine coverage. Surveys have shown that the determination of pneumococcal vaccination status in individual long-term care residents is difficult and represents a major barrier for pneumococcal vaccination because of misconceptions about the risk of adverse reactions following revaccination [3,43]. The available evidence indicates that second dose of pneumococcal vaccine does not appear to be associated with serious adverse reactions [44,45]. Thus, pneumococcal vaccine could be given to patients with unknown vaccination history [10,46]. Studies in US nursing homes identified that vaccination was low priority among physicians [3,36]. Improved knowledge of adult vaccination in health care professionals may reduce missed opportunities for vaccination during consultations. Difficulty in obtaining consent on behalf of incompetent residents was stated to be one of the important barriers to increased influenza and pneumococcal vaccination rates and this has been noted by others [47]. Data from Canada indicate that obtaining consent for vaccination on admission for current and future years is associated with higher influenza and pneumococcal vaccination rates [28]. Our findings also showed that vaccination programs organized by nursing staff were considered as an effective strategy for enhancing coverage of influenza and pneumococcal vaccine. It has been documented that organized vaccination programs are the most important strategy to improve influenza and pneumococcal vaccination rates [48]. Standing orders for nurses could allow for the easier administration of vaccines in long-term care facilities [49].
11. Conclusions Our results highlight a large gap between influenza and pneumococcal vaccination rates in nursing homes. This is mainly due to lack of national recommendations and reimbursement policies for pneumococcal vaccination. Changes in attitudes, knowledge and practice of healthcare professionals and public together with the implementation of organized vaccine delivery strategies and systematic vaccination records are crucial in improving vaccination rates in nursing home residents and other long-term care facilities. Further studies in understanding of patients and clinicians vaccine preventable behaviors would aid in increasing coverage of these vaccines in high-risk patients.
Acknowledgements The authors would like to thank the staff in nursing homes throughout Scotland for their cooperation in this survey. We
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
are also grateful to the staff at the Scottish Centre for Infection and Environmental Health and the Information and Statistics Division in Scotland, in particular to Kenny McIntyre and Patricia Cassels, for their help in obtaining information and data entry. References [1] Muder RR. Pneumonia in residents of long-term care facilities: epidemiology, etiology, management and prevention. Am J Med 1998;105:319–30. [2] Nicholson K, Baker D, Farquhar A, et al. Acute upper respiratory tract viral illness and influenza immunization in homes for the elderly. Epidemiol Infect 1990;105:609–18. [3] Quick RE, Hoge CW, Hamilton DJ, Whitney C, Borges M, Kobayashi J. Underutilization of pneumococcal vaccine in nursing homes in Washington State: report of serotype-specific outbreak and a survey. Am J Med 1993;94:149–52. [4] Monto A, Ohmit S, Margulies J, et al. Medical practice-based influenza surveillance: viral prevalence and assessment of morbidity. Am J Epidemiol 1995;141:502–6. [5] Arden N, Monto A, Ohmit S. Vaccine use and the risk of outbreaks in a sample of nursing homes during an influenza epidemic. Am J Public Health 1995;85:399–401. [6] Nuorti J, Butler J, Crutcher JM. Outbreak of multidrug-resistant pneumococcal pneumonia and bacteraemia among unvaccinated nursing home residents. N Engl J Med 1998;338:1861–8. [7] Gleich S, Morad Y, Echague R, Miller JR, Kornblum J, Sampson JS, et al. Streptococcus pneumoniae serotype 4 outbreak in a home for the aged: report and review of recent outbreaks. Infect Control Hosp Epidemiol 2000;21:711–7. [8] Butler JC, Cetron MS. Pneumococcal drug resistance: the new special enemy of old age. Clin Infect Dis 1999;28:730–5. [9] Monto AS, Hornbuckle K, Ohmit SE. Influenza vaccine effectiveness among elderly nursing home residents: a cohort study. Am J Epidemiol 2001;154:155–60. [10] MMWR. Prevention of pneumococcal disease: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR 1997;46:1–24. [11] Ohmit S, Arden N, Monto A. Effectiveness of inactivated influenza vaccine among nursing home residents during an influenza type A (H3N2) epidemic. J Am Geriatr Soc 1999;47:165–71. [12] Shapiro ED, Berg AT, Austrian R, Schroeder D, Parcells V, Margolis A, Adair RK, Clemens JD. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine. N Engl J Med, 1991;325:1453–60. [13] Butler J, Breiman R, Campbell J, Lipman H, Broome C, Facklam R. Pneumococcal polysaccharide vaccine efficacy: an evaluation of current recommendations. JAMA 1993;270:1826–31. [14] Postma M, Baltussen R, Heijnen M, de Berg LT, Jager J. Pharmacoeconomic of influenza vaccination in the elderly: reviewing the available evidence. Drugs Ageing 2000;17:217–27. [15] Nichol K, Baken L, Wuorenma J, Nelson A. The health and economic benefits associated with pneumococcal vaccination of elderly persons with chronic lung disease. Arch Intern Med 1999;159:2437–42. [16] Ament A, Baltussen R, Duru G, et al. The cost effectiveness of pneumococcal vaccination for older people: a study in five western European countries. Clin Infect Dis 2000;31:444–50. [17] McDonald P, Friedman E, Banks A, Anderson R, Carman V. Pneumococcal vaccine campaign based in general practices. BMJ 1997;314:1094–8. [18] Kyaw MH, Wayne B, Chalmers J, Jones IG, Campbell H. Influenza and pneumococcal vaccine distribution and use in primary care and hospital settings in Scotland: coverage, practice and policies. Epidemiol Infect, in press.
2521
[19] Department of Health. Immunisation against infectious disease London: HMSO, 1996. [20] Gupta A, Morris G, Thomas P, Hasan M. Influenza vaccination coverage in old people’s home in Camarthenshire, UK, during the winter of 1998/99. Vaccine 2000;18:2471–5. [21] MMWR. Influenza and pneumococcal vaccination levels among persons aged ≥65 years—United States. MMWR 2001;50:532–7. [22] Evans M, Wilkinson E. How complete is influenza vaccination coverage? A study in 75 nursing and residential home for the elderly people. Br J Clin Pract 1995;45:419–21. [23] Evans M. Monitoring influenza immunisation uptake in nursing homes. Commun Dis Rep 1996;6:R170–2. [24] Chief Medical Officer (CMO). Influenza immunisation. Scottish Executive. Health Department, 2001. [25] Patriarca P, Weber J, Parker R. Risk factors for outbreaks of influenza in nursing homes: a case control study. Am J Epidemiol 1986;124:114–9. [26] Gross P, Rodstein M, LaMontagne J. Epidemiology of acute respiratory illness during an influenza outbreak in a nursing home. Arch Intern Med 1988;148:559–61. [27] Buikema A, Singleton J, Sneller V et al. Influenza and pneumococcal vaccination in nursing homes, US, 1995–1999, In: Abstracts from the 35th National Immunization Conference. Atlanta, Georgia, 2001 [Abstract]. [28] 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? CMAJ 2001;164:1413– 9. [29] Sleeman K, Knox K, George R. Invasive pneumcoccal disease in England and Wales: vaccination implications. J Infect Dis 2001;183:239–46. [30] Kyaw MH, Clarke S, Jones IG, et al. Incidence of invasive pneumococcal disease in Scotland. Epidemiol Infect, in press. [31] Butler JC, Schuchat A. Epidemiology of pneumococcal infections in the elderly. Drugs Aging 1999;15:11–9. [32] Breiman R, Spika J, Navarro V, Darden PM, Darby CP. Pneumococcal bacteremia in Charleston County, South Carolina a decade later. Arch Intern Med 1990;150:1401–5. [33] Plouffe JF, Breiman RF, Facklam RR. Bacteraemia with Streptococcus pneumoniae: implications for therapy and prevention. JAMA 1996;275:194–8. [34] Centers for Disease Control and Prevention. Active Bacterial Core Surveillance (ABCs) Report. Emerging Infections Program Network Streptococcus pneumoniae, 2000 (preliminary). Available at: http:www.cdc.gov/ncidod/dbmd/abcs. Accessed 10 November 2001. [35] Sheppard D, Bartlett K, Lampiris H. Streptococcus pneumoniae transmission in chronic-care facilities: description of an outbreak and review of management strategies. Infect Control Hosp Epidemiol 1998;19:851–3. [36] MMWR. Outbreaks of pneumococcal pneumonia among unvaccinated residents in chronic care facilities—Massachusetts, October 1995, Oklahoma, February 1996, and Maryland, May–June 1996. MMWR 1997;46:60–62. [37] Fedson DS. Pneumococcal vaccination in the United States and 20 other developed countries, 1981–1996. Clin Infect Dis 1998;26:1117– 23. [38] Kyaw MH, Bramley JC, Chalmers J, Jones IG, Campbell H. Pneumococcal vaccination: opinion of general practitioners and hospital doctors in Scotland, 1999–2000. Commun Dis Public Health 2001;4:42–8. [39] Nichol K, Lofgren R, Gapinski J. Influenza vaccination: knowledge, attitudes and behaviour among high-risk outpatients. Arch Intern Med 1992;152:106–10. [40] Kyaw MH, Nguyen-Van-Tam J, Pearson J. Family doctor advice is the main determinant of pneumococcal vaccine uptake. J Epidemiol Community Health 1999;53:589–90.
2522
M.H. Kyaw et al. / Vaccine 20 (2002) 2516–2522
[41] Nichol KL, Grimm MB, Peterson DC. Immunizations in long-term care facilities: policies and practice. J Am Geriatr Soc 1996;44:349– 55. [42] US Department of Health and Human Services. In: Proceedings of Conference on Healthy people 2010 (in two volumes). Washington, DC: US Department of Health and Human Services, 2000. [43] MMWR. Outbreak of pneumococcal pneumonia among unvaccinated residents of a nursing home—New Jersey, April 2001. MMWR 2001;50:707–9. [44] Fine MJ, Smith MA, Carson CA, et al. Efficacy of pneumococcal vaccination in adults: a meta-analysis of randomized controlled trails. Arch Intern Med 1994;154:2666–77. [45] Jackson LA, Benson P, Sneller V-P, Butler JC, Thompson RS, Chen RT, et al. Safety of revaccination with pneumococcal polysaccharide vaccine. JAMA 1999;281:243–8.
[46] Whitney CG, Schaffner W, Butler JC. Rethinking recommendations for use of pneumococcal vaccines in adults. Clin Infect Dis 2001;33:662–75. [47] Russell ML. Influenza vaccination in Alberta long-term care facilities. CMAJ 2001;164:1423–7. [48] Nichol KL. Ten-year durability and success of an organised program to increase influenza and pneumococcal vaccination rates among high-risk adults. Am J Med 1998;105:385–92. [49] MMWR. Adult immunization programs in national strategies: quality standards and guidance for program evaluation and use of standing orders programs to increase adult vaccination rates. MMWR 2000;49:1–28.