Influenza coverages in Spain and vaccination-related factors in the subgroup aged 50–64 years

Vaccine 21 (2003) 3550–3555

Influenza coverages in Spain and vaccination-related factors in the subgroup aged 50–64 years Rodrigo Jiménez a,∗ , Amparo Larrauri b , Pilar Carrasco b , Jesús Esteban b , Luis Ignacio Gómez-López c , Ángel Gil b a

b

Unidad de Docencia e Investigación en Medicina Preventiva y Salud Pública, Facultad de Ciencias de la Salud, Universidad Rey Juan Carlos, Avenida de Atenas S/N, Alcorcón, 28402 Madrid, Spain Preventive Medicine and Public Health Teaching and Research Unit, Health Sciences Faculty, Rey Juan Carlos University, Madrid, Spain c Chair of Preventive Medicine, Zaragoza University, Zaragoza, Spain Received 22 November 2002; accepted 19 May 2003

Abstract This study sought to describe influenza vaccination coverages for different Spanish population subgroups, stressing the analysis of vaccination-related factors in subjects aged 50–64 years and estimating the possible beneficial effect of extending universal vaccination to this age group. A total of 6400 surveys, targeting subjects over the age of 16 years and drawn from the 1997 Spanish National Health Survey, were used for study purposes. Influenza coverage was observed to rise significantly with age, and the reason cited by most subjects for seeking vaccination was medical indication. Coverage of the 50–64 age group was 21.6% (95% CI 19.4–23.8) and the variables associated with a greater probability of being vaccination were: residence in towns or cities with <10,000 inhabitants (OR 1.45); monthly income of less than 600 (OR 1.71); and presence of associated chronic disease (OR 3.07.) It is estimated that in Spain, 524,514 (40.7%) persons aged 50–64 years with associated chronic disease receive and 764,218 persons aged 50–64 years with associated chronic disease do not receive influenza vaccine. We conclude that the extremely high number of subjects in the 50–64 age range susceptible to influenza-related complications each year constitutes good grounds for universal vaccination being extended to said age group. © 2003 Elsevier Science Ltd. All rights reserved. Keywords: Influenza; Coverage; Vaccine

1. Introduction To date, influenza continues to be a very important cause of morbidity and mortality in Spain [1]. Annual incidence rates range from 300 to 500 cases per 100,000 population, with a cumulative total of 2–3 million cases per year [1]. This is so despite the influenza vaccination’s proven efficacy in reducing the appearance of the disease in healthy subjects under the age of 65 years and mitigating influenza-related complications, hospitalisations and deaths among subjects aged 65 years and older and/or presenting with underlying medical disorders [2–5]. In Spain, influenza vaccination has been indicated for many years now in subjects above the age of 64 years and in younger subjects with chronic diseases that render ∗ Corresponding author. Tel.: +34-91-488-88-53; fax: +34-91-488-88-48. E-mail address: [email protected] (R. Jim´enez).

sufferers susceptible to influenza-related complications. In all such cases, vaccination is administered free of charge. The end result of any influenza vaccination programme will depends on the efficacy of the vaccine in the respective population subgroups and the accompanying vaccination coverage [6]. Ascertainment of vaccination coverages is an important part of vaccination programmes, since it enables appropriate strategies to be designed for the purpose of achieving designated goals, by furnishing useful data for decision-making and programme management [6,7]. Spanish vaccination coverage studies have essentially targeted the over-64 age group, and have attained values of 50–70% [8–10], which are comparable to those reported from other European countries such as Italy and England [11,12]. These results highlight existing limitations on the attainment of high vaccination rates, meaning in turn that the maximum potential of such interventions has not yet been realised [12–14].

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R. Jim´enez et al. / Vaccine 21 (2003) 3550–3555

The lack of data for other age groups is due to the difficulty of obtaining denominators in respect of persons for whom vaccination would presumably be indicated [15]. In the year 2000, the Advisory Committee on Immunization Practices (ACIP) included subjects aged 50–64 years among its target groups for influenza vaccination, based on the high prevalence of chronic disease in this age range and the fact that “age-based strategies are more successful in increasing vaccine coverage than patient-selection strategies based on medical conditions” [16]. Using the latest, namely the 1997 Spanish National Health Survey for the purpose (Encuesta Nacional de Salud de España 1997—ENS 97) [17], this study therefore set out to describe influenza vaccination coverages for different population subgroups, stressing the analysis of vaccination-related factors in subjects aged 50–64 years, and lastly, estimating the number of unvaccinated persons susceptible to influenza-related complications in this age range and the possible beneficial effect of extending universal vaccination to same.

2. Materials and methods This was a nation-wide cross-sectional descriptive study on influenza vaccination coverage among adults over the age of 16 years in Spain, in 1997. Our study used secondary individualised data drawn from the National Health Survey undertaken by the Spanish Ministry of Health & Consumer Affairs in 1997 [17]. These surveys cover a broad representative sample of the non-institutionalised Spanish population. For study purposes, we used data from 6400 surveys conducted on adults over the age of 16 years. The reply (“yes” or “no”) to the question, “Were you vaccinated against influenza in the last vaccination campaign?” was taken as the dependent variable, while the following were analysed as independent variables: reason for vaccination; perception of state of health, socio-demographic variables (size of town or city, educational level, civil status and monthly income), presence of chronic disease (diabetes, asthma, chronic bronchitis or coronary disease), and lifestyle (smoking, alcohol consumption, obesity and sedentary lifestyle). In a first phase of the analysis, our population sample was divided into the following four age groups: 16–34, 35–49, 50–64, and >64 years. Influenza coverage was assessed by age group, with the prevalence of individuals who had or had not been vaccinated against influenza and the corresponding 95% confidence intervals being estimated by reference to the above independent variables. The second phase entailed an in-depth analysis of factors associated with influenza vaccination in the 50–64 age group. Odds ratios and their 95% confidence intervals were used to assess the association of the study variables with delivery of influenza vaccine to the study sample. To estimate the independent effect of each of the variables on in-

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fluenza vaccine delivery, adjusted odds ratios were obtained by means of multivariate analysis using logistic regression models. The number of Spaniards aged 50–64 years who suffer from one or more health conditions of interest was estimated by multiplying the age- and sex-specific rates by the number of persons in the corresponding age and sex group, as shown in the 1997 census projection furnished by the National Statistics Institute (Instituto Nacional de Estad´ıstica—INE) [18]. This method was described by Russell [15]. Based on this number and using the vaccination coverages, we then estimated the number of subjects who could foreseeably benefit from recommendation that universal vaccination be extended to ages 50–64 years. All analyses were performed using the SPSS version 10.0 statistics software programme. 3. Results The study was based on data from a total of 6337 subjects aged 16 years or over who answered the question as to whether or not they had received influenza vaccine during the latest campaign, a total that represented 99% of the 6400 subjects included in the ENS 97. A breakdown of the study subjects showed that: 48.7% were males (3088), 51.3% were females (3249), and the mean age was 43.9 years (S.D. 18.8). Overall influenza vaccination coverage for the total sample was 17.1% (95% CI 16.2–18). The prevalence of individuals in the study sample who reported receiving influenza vaccine rose significantly (P < 0.001) with age, with coverages of 5.4, 6.7, 21.6, and 51.3% in evidence for the 16–34, 35–49, 50–64, and over-64 age groups, respectively. With regard to subjects’ reasons for seeking vaccination, Table 1 shows medical indication as the reason most cited (68.7%), followed by own initiative (23.6%), occupational reasons and other reasons (7.7%). Distribution of this variable by age group showed a progressive rise with age in the percentage of individuals receiving vaccine as a result of medical indication, whereas own initiative and occupational reasons registered a progressive decline with age among study subjects. Table 2 gives a breakdown of the results of the analysis of influenza vaccination coverage by age group, acTable 1 Reasons for influenza vaccination by age group Age group

Medical indication

Own initiative

Occupational and other reasons

%

95% CI

%

95% CI

%

95% CI

16–34 years 35–49 years 50–64 years >64 years

40.6 54.6 66.1 79.0

32.1–49.1 44.7–64.3 60.6–71.6 75.6–82.4

39.9 32.3 24.4 18.0

31.3–48.3 23.1–41.5 19.4–29.4 14.8–21.2

19.5 13.1 9.5 3.0

12.6–26.4 6.5–19.7 6.1–12.9 1.7–4.5

Total

68.7

65.9–71.5

23.6

21.1–26.1

7.7

6.0–9.2

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Table 2 Influenza coverage by age group, according to perception of state of health and socio-demographic variables 16–34 years

35–49 years

50–64 years

Over-64 years

Total

%

95% CI

%

95% CI

%

95% CI

%

95% CI

%

95% CI

Perception of health Very good or good Fair, poor or very poor

4.9 8.1

4.0–5.8 5.4–10.8

5.8 9.7

4.4–7.2 6.6–12.8

16.7 27.3

14.0–19.4 23.8–30.8

46.1 55.2

41.6–50.6 51.3–59.1

11.5∗ 29.3∗

10.5–12.5 27.3–31.3

Town or city <10000 inhabitants 10–100000 inhabitants >100000 inhabitants

6.1 6.1 4.6

4.0–8.2 4.4–7.8 3.4–5.8

8.5 6.4 6.0

5.6–11.4 4.1–8.7 4.2–7.8

25.4 23.6 17.7

20.8–30.0 19.6–27.6 14.5–20.9

55.2 48.9 50.2

49.8–60.6 43.8–54.0 45.4–55.0

21.2∗ 17.5∗ 14.4∗

19.2–23.2 15.8–19.2 13.1–15.7

5.7 5.6 4.4

4.2–7.2 4.2–7.0 2.5–6.3

6.5 6.6 6.9

4.8–8.2 3.9–9.3 4.0–9.8

21.8 15.0 14.6

19.2–24.4 8.9–21.1 7.5–21.7

52.6 44.6 53.1

49.1–56.1 33.3–55.9 39.1–67.1

20.7∗ 8.5∗ 9.1∗

19.3–22.1 7.1–9.9 7.2–11.0

Monthly income Less than 600 600–1200 1200

7.8 4.3 5.5

5.2–10.4 3.0–5.6 4.1–6.9

5.8 8.6 5.0

3.0–8.6 6.4–10.8 3.2–6.8

26.7 21.9 15.1

22.7–30.7 18.2–25.6 11.5–18.7

51.3 52.4 49.7

47.5–55.1 46.2–58.6 42.7–56.7

28.3∗ 14.3∗ 10.9∗

26.2–30.4 12.9–15.7 9.6–12.2

Married Yes No

4.2 5.9

2.7–5.7 4.8–7.0

6.8 6.6

5.4–8.2 3.7–9.5

22.0 20.1

19.5–24.5 15.0–25.2

53.4 47.8

49.7–57.1 43.0–52.6

19.4∗ 13.8∗

18.1–20.6 12.5–15.1

Total∗

5.4

4.5–6.3

6.7

5.4–8.0

21.6

19.4–23.8

51.3

48.4–54.2

17.1

16.2–18.0

Educational level Halted prior to age 16 years Halted at age 16–19 years Higher education (university and non-university)

∗

P < 0.001.

cording to subjects’ perceived state of health and different socio-demographic variables. Vaccine delivery rose in cases where individuals perceived their health more negatively (29.3% versus 11.5%, P < 0.001), a result which held across all the age groups analysed. As regards the socio-demographic variables, size of town or city was associated with influenza vaccination coverage of the study sample (P < 0.001), inasmuch as towns with fewest inhabitants registered highest vaccination frequencies. Vaccination percentages proved highest among individuals with lowest educational levels, i.e. those whose education had halted prior to age 16 years versus those whose education had halted at ages 16–19 years or who had undergone higher education (P < 0.001). When the distribution of both these socio-demographic variables was analysed by age group, the overall result of the analysis maintained a similar trend, fundamentally in the group of persons aged 50–64 years. Monthly income also showed a statistically significant association with frequency of influenza vaccination, in that the smaller the income of the individual, the greater the vaccination coverage, a trend that remained in evidence when broken down by age group. Civil status was linked to influenza vaccination coverage, insofar as it proved higher among married subjects (P < 0.001). The results yielded by analysis of influenza vaccination coverage by prevalence of chronic disease and lifestyle are shown in Table 3. The frequency of individuals who reported having received vaccine was higher in persons who suffered (45.4%) than in those who did not suffer from chronic dis-

ease (12.9%, P < 0.001), with the prevalence of chronic disease being a determinant of a higher influenza vaccination coverage across all age groups studied. With respect to the influence exerted by lifestyle on influenza vaccine delivery, a higher influenza vaccination coverage was observed for obese versus non-obese individuals (P < 0.001), an effect that was essentially in evidence in the 35–49 and 50–64 age groups. Similarly, influenza vaccination percentages were higher among sedentary versus non-sedentary persons, ex-smokers (25.0%) and non-smokers (20.9%) versus active smokers (8.5%), and lastly, persons who reported that they had not consumed alcohol in the previous 2 weeks versus those who reported that they had. Differences were statistically significant in all cases, with the trends observed in the overall analysis of the study sample being most clearly evident in the 50–64 age group. The analysis performed in the second phase of this study focused on the 1330 persons surveyed who comprised the 50–64 age group, 21.6% of whom (95% CI 19.4–23.8) reported having received influenza vaccine (Table 2). Table 4 sets out the odds ratios, both crude and adjusted by logistic regression, and their 95% confidence intervals, obtained when the association between the study variables and influenza vaccine delivery in this age group is assessed. The multivariate analysis showed that, for the 50–64 age group, the variables associated with a higher probability of having received influenza vaccine were: residence in towns or cities having less than 10,000 inhabitants; a monthly income of less than 600; and—with a strength of association

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Table 3 Influenza coverage by age group, according to presence of associated chronic disease and lifestyle

Presence of chronic Yes No

16–34 years

35–49 years

50–64 years

Over-64 years

Total

%

95% CI

%

95% CI

%

95% CI

%

95% CI

%

95% CI

12.4–29.0 3.9–5.7

15.7 6.3

7.2–24.2 5.0–7.6

40.7 16.7

34.8–46.6 14.4–19.0

60.3 46.5

55.4–65.2 42.9–50.1

45.4∗ 12.9∗

42.0–48.8 11.2–14.6

diseasea 20.7 4.8

Obesity BMI <27 BMI ≥27

5.4 6.7

4.4–6.4 3.8–9.6

5.3 9.6

3.9–6.7 6.8–12.4

19.2 24.5

16.1–22.3 20.9–28.1

51.2 49.2

46.4–56.0 44.0–54.4

12.4∗ 23.0∗

11.4–13.4 20.9–25.1

Sedentary lifestyle Yes No

4.7 5.8

3.3–6.1 4.6–7.0

6.1 7.3

4.3–7.9 5.5–9.1

21.0 22.3

17.9–24.1 19.1–25.5

51.4 51.4

47.4–55.4 47.0–55.8

18.6∗∗ 15.8∗∗

17.2–20.0 14.6–17.0

Tobacco use Active smoker Ex-smoker Non-smoker

4.8 5.7 6.0

3.7–5.9 2.6–8.8 4.6–7.4

5.6 8.5 7.2

3.9–7.3 5.0–12.0 5.1–9.3

17.0 26.4 21.9

12.9–21.1 20.8–32.0 18.9–24.9

38.4 56.7 51.6

29.4–47.4 50.5–62.9 48.0–55.2

8.5∗ 25.0∗ 20.9∗

7.3–9.7 22.2–27.8 19.5–22.3

6.0 7.7

4.4–7.6 5.5–9.9

18.8 24.2

15.7–21.9 21.0–27.4

48.4 53.0

43.3–53.5 49.4–56.6

12.8∗ 21.9∗

11.7–13.9 20.4–23.4

Alcohol consumption in previous 2 weeks Yes 4.9 3.8–6.0 No 6.1 4.6–7.6 a

Coronary disease and/or diabetes and/or asthma/chronic bronchitis. P < 0.001. ∗∗ P < 0.01. ∗

greater than the preceding two—presence of an associated chronic disease, which registered an adjusted odds ratio of 3.07. The ENS 97 estimated the proportion of persons aged 50–64 years who reported that they had some chronic disease (diabetes, asthma, chronic bronchitis or coronary dis-

ease) at 20.6% (95% CI: 18.2–23.0). This proportion, applied to the Spanish population census, enables the denominator to be obtained for the purpose of calculating influenza vaccination coverage among persons at risk of suffering influenza-related complications, some 1,288,732 individuals. Influenza vaccination coverage among the study sample

Table 4 Crude and adjusted odds ratios for factors associated with influenza vaccination in persons aged 50–64 years Variable

Category

Crude OR

95% CI

Adjusted OR

95% CI

Sex

Male Female

1 1.05

– 0.81–1.37

1 1.13

– 0.77–1.66

Town or city

>100000 inhabitants 10001–100000 inhabitants <10000 inhabitants

1 1.44 1.58

– 1.05–1.97 1.14–2.19

1 1.36 1.45

– 0.95–1.93 1.01–2.10

Monthly income

More than 1200 600–1200 Less than 600

1 1.58 2.05

– 0.49–2.17 1.44–2.91

1 1.45 1.71

– 0.98–2.16 1.14–2.56

Presence of chronic diseasea

No Yes

1 3.42

– 2.56–4.58

1 3.07

– 2.18–4.33

Perception of state of health

Very good or good Fair, poor or very poor

1 1.87

– 1.43–2.44

1 1.18

– 0.85–1.61

Obesity

BMI <27 BMI ≥27

1 1.36

– 1.03–1.81

1 1.09

– 0.81–1.48

Tobacco use

Active smoker Non-smoker Ex-smoker

1 1.37 1.76

– 0.98–1.92 1.17–2.64

1 0.90 1.23

– 0.58–1.39 0.79–1.93

Alcohol consumption in previous 2 weeks

Yes No

1 1.38

– 1.06–1.80

1 1.04

– 0.75–1.45

a

Coronary disease and/or diabetes and/or asthma/chronic bronchitis.

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aged 50–64 years suffering from chronic disease was 40.7% (Table 3), which is to say that 524,514 persons aged 50–64 years with chronic disease receive and 764,218 persons aged 50–64 years with chronic disease do not receive influenza vaccine. Assuming that the vaccination coverages attained in the over-64 age group could be attained if universal vaccination were extended to the 50–64 age group, the number of subjects aged 50–64 years with associated diseases who would benefit, would range from 74,746 (where coverage rose from 40.7 to 46.5%, a figure representing coverage among persons over the age of 64 years without chronic disease) to 252,591 persons (where coverage rose from 40.7 to 60.3%, a figure representing coverage among persons over the age of 64 years with chronic disease).

4. Discussion The 1997 National Health Survey has been previously used by Spanish researchers to study different health-related aspects [19,20]. The usefulness of national health surveys for calculating vaccination coverages has been noted by other authors and, indeed, is standard methodology in countries such as the United States [6,21,22]. The very high response rate to the question as to whether subjects had or had not received the influenza vaccine tends to render the existence of any selection bias, which might possibly influence our results, highly unlikely. However, another possible limitation inherent in health surveys is that use of self-reported vaccination data might itself entail a bias. In this connection, a study that compared results yielded by self-reported data against medical records nevertheless showed that self-reporting on influenza vaccination was very sensitive (98%) and moderately specific (71%) [23]. Moreover, another earlier study in Ontario obtained a very high concordance between self-reporting and medical records (κ = 0.92) [24]. The progressive rise in influenza vaccination coverage with age reported by other studies undertaken in Spain, is coherent with: the progressive rise in the prevalence of chronic diseases that indicate the need for vaccination against influenza; and the increase with age in the percentage of individuals receiving vaccine on medical indication [10,17,25]. The higher percentage of subjects who are vaccinated against influenza amongst the population segment having a lower educational and economic level is difficult to explain. One possible reason is the possible confounding effect attributable to “size of town or city”. Spanish residents of smaller-sized towns have a lower educational and economic level than those in the more heavily populated areas [17,8]. Added to this is the fact that the greater proximity and accessibility to health centres in smaller towns may lead to ensuingly higher vaccination coverages there. A study into the use of preventive medical services in the USA reported

influenza coverages of 55% among the urban elderly and 58% among rural residents [26]. The finding that active tobacco use is a negative predictor of influenza vaccination is in line with results reported by other authors [12]. In the USA in 1997, influenza vaccination coverage for subjects under the age of 65 years with associated chronic diseases was below 30% [16]; in our study, coverage for that same year in the 16–64 age range was 32.4%. During the period 1997–2000, vaccination coverage in the USA among the 50–64 age group ranged from 40 to 44% for subjects with, versus 28 to 31% for those without associated diseases [16,27,28]. In our sample, these percentages were 40.7% (95% CI 34.8–46.6) and 16.7% (95% CI 14.4–19), respectively. Such low percentages can be improved, as was shown in Minneapolis, where, thanks to an intensive vaccination programme, vaccination coverage among subjects under the age of 65 years with chronic diseases was 69% in the 1996–1997 influenza season [29]. Our study estimates the proportion of persons aged 50–64 years reporting some chronic disease at 20.6% (95% CI: 18.2–23.0). This prevalence is slightly below that found in the United States (24–32%) [16] and very similar to that described in Alberta (22.8%) [15]. As subjects with diseases susceptible to vaccination, both our and Russell’s studies [15] solely included persons reporting diabetes, asthma, chronic bronchitis or coronary disease, something that probably underestimates the percentage of subjects among whom vaccination would normally be indicated. However, the relative importance of the vaccination-indicator diseases that were not included is proportionally less than those that were included, which would, in turn, possibly mean that the error is not of great magnitude [15] and, in addition, partly serve to explain the differences vis-à-vis the US-based estimates. The conclusion to be drawn from the results of the multivariate analysis for the 50–64 age group is that, while the presence of an associated disease raises the probability of vaccination more than three-fold as against the absence of same, the absolute effectiveness of this recommendation is low inasmuch as it fails to encompass 59.3% of all susceptibles. According to our estimates, anywhere from 74,746 to 252,591 subjects aged 50–64 years with chronic diseases would benefit from the influenza vaccination, were influenza vaccination guidelines to include all subjects in this age range. Logically, this estimate is based on the hypothesis that vaccination coverages would rise to levels attained in the over-64 age group to which this recommendation already applies. Evidence to back this hypothesis is to be found in the results of studies that highlight the limitations of patient-selection strategies based on medical conditions and the greater effectiveness of age-based strategies [16,30]. Further, additional benefits would include a reduction in morbidity, medical visits, absenteeism and use of antibiotics on the part of subjects without associated diseases, plus the

R. Jim´enez et al. / Vaccine 21 (2003) 3550–3555

advantage that could be taken of the fact that it would be at age 50 years when other preventive activities would be initiated [16]. We thus conclude that, while the potential benefit to be gained from amending current influenza vaccination guidelines in Spain and extending universal vaccination to the 50–64 age range is very great, it is nonetheless essential to wait until the results from countries where this recommendation is already being implemented and the economic assessment of same have been received. References [1] Centro Nacional de Epidemiolog´ıa. Area de Vigilancia de la Salud Pública. Servicio de Vigilancia Epidemiológica. Informacion sobre la gripe en España (http://193.146.50.130/ve/ve.htm). [2] Sugaya J, Nerome K, Ishida M, Matsumoto M, Mitamura M, Nirasawa J. Efficacy of inactivated vaccine in preventing antigenically drifted influenza type A and well-matched type B. JAMA 1994; 272:1122–6. [3] Nichol KL, Wuorenma J, Von Sternberg T. Benefits of influenza vaccination for low, intermediate, and high-risk senior citizens. Arch Intern Med 1998;158:1769–76. [4] Demicheli V, Jefferson T, Rivetti D, Deeks J. Prevention and early treatment of influenza in healthy adults. Vaccine 2000;18:957–1030. [5] Govaert TME, Thijs CTMCN, Masurel N, Sprenger MJW, Dinant GJ, Knottnerus JA. Efficacy of influenza vaccination in elderly individuals: a randomized double-blind placebo-controlled trial. JAMA 1994;272:1661–5. [6] Guerin N. Assessing immunization coverage: how and why? Vaccine 1998;16(Suppl):S81–3. [7] LeBaron CW, Chaney M, Baughman AL, Dini EF, Maes E, Dietz V, et al. Impact of measurement and feedback on vaccination coverage in public clinics, 1988–1994. JAMA 1997;277(8):631–5. [8] Sarria A, Timoner J. Determination of influenza vaccination in persons 65 years of age and older. Rev Esp Salud Pública 2002;76(1):17–26. [9] Puig-Barbera J, Ors Zarzoso P, Vilchez Pena C, Lloria Paes F. Impact of various strategies on the rates of flu vaccination in the elderly. Aten Primaria 1999;23(6):339–45. [10] Mulet Pons MJ, Sarrion Ferre MT, Barea Montoro A, Marin Rueda N, Blanquer Gregori JJ, Melchor Penella MA. Evaluation of the completion of influenza vaccination. Aten Primaria 1995;16(7):423– 7. [11] D’Argenio P, Adamo B, Coluccio R, D’Apice A, Ferrara MA, Giugliano F, et al. Influenza vaccination coverage in elderly people, Campania (Italy), 1999. Eur Surveill 2001;6(2):26–30. [12] Nicholson KG, Kent J, Hammersley V. Influenza A among community-dwelling elderly persons in Leicestershire during winter 1993–1994: cigarette smoking as a risk factor and the efficacy of influenza vaccination. Epidemiol Infect 1999;123(1):103–8.

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