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Low coverage and predictors of vaccination uptake against tick-borne encephalitis in Slovenia

Marta Grgič-Vitek, Irena Klavs
DOI: http://dx.doi.org/10.1093/eurpub/ckr018 182-186 First published online: 11 March 2011

Abstract

Background: Although vaccination against tick-borne encephalitis (TBE) was introduced in 1986, Slovenia remains one of the countries with the highest reported incidence rates. For exposed occupationally or during education/training, vaccination is reimbursed by employer or within mandatory health insurance, while others have to pay. Our aim was to obtain the first national estimate of self-reported uptake of vaccination against TBE in a probability sample of the general population aged ≥15 years and identify predictors of self-paid vaccination uptake. Methods: Two questions on vaccination against TBE were added into the 2007 Slovenian version of European Health Interview Survey. We used multivariable logistic regression analysis to identify factors independently associated with self-paid TBE vaccination uptake. Results: The overall self-reported prevalence of TBE vaccination uptake was 12.4%, of which, due to occupational exposure 3.2%, exposure during education/training 2.3% and as military recruits 2.2%. Additional 4.6% individuals reported to be vaccinated due to ‘other reasons’ (self-paid). There were no gender differences among individuals who paid for vaccination (4.5 and 4.8%, respectively). Characteristics independently associated with higher odds for self-paid vaccination against TBE were high income, not being overweight and ever being vaccinated against influenza. Conclusion: To reduce TBE morbidity in Slovenia vaccination coverage of the general population should be increased. Offering vaccination within compulsory health insurance together with intensive vaccination promotion would increase the vaccination coverage and reduce the social inequality in access.

Introduction

Slovenia is one of the countries with the highest reported incidence rates of tick-borne encephalitis (TBE), the most important human flavivirus infection endemic in Europe. During 2000–09, the overall reported rates ranged from 9.8 to 18.6/100 000 population and in the two most affected regions, Gorenjska and Koroška (covered by regional Institutes of Public Health Kranj and Ravne), from 16.2 to 47.1/100 000.1,2 Other countries with several natural foci and high risk TBE areas in Europe include Austria, Czech Republic, Slovakia, Hungary, Germany, Switzerland, Poland, Russia, the Baltic countries, Sweden and Finland. Around 3000 TBE cases are reported annually in Europe excluding Russia, approximately one-tenth of those occur in Slovenia. Latvia was considered the country with the highest TBE incidence rates in the world between 1990 and 2000 (with average incidence rate (1997–2000) being 26.9/100 000 population), since then the number of cases has decreased considerably. During recent years, it is actually Slovenia that has the highest rates.1

Notification of TBE cases is mandatory in Slovenia. Neither TBE surveillance case definition nor definition of TBE endemic area is available. In fact, most of Slovenia is considered TBE endemic area. However, TBE diagnosis established by treating physicians is used for case reporting for surveillance purposes.3

Mandatory vaccination against TBE was introduced in 1986 for occupationally exposed (reimbursed by employers) and in 1990 for students (e.g. of forestry, wood processing), exposed to TBE during training (reimbursed within compulsory health insurance). In addition, since 1991, vaccination against TBE has been recommended for all individuals living in or travelling to endemic areas including children from 1 year of age (paid by vaccinated individuals themselves). During 1993–2003, TBE vaccination was mandatory for all military recruits (reimbursed by the army). Thus the great majority of men born during 1974 to 1984 should have been vaccinated. After 2003, when Slovenian Armed Forces were organized as a fully professional standing army, vaccination against TBE was provided only for professional soldiers and not for whole cohorts of man. Current Slovenian immunization programme recommends three doses of vaccine (0, 1, 9–12 months), followed by the first booster after 3 years and the following boosters every 5 years or every 3 years in elderly individuals (>50 or 60 years of age according to manufacturer's instructions).

Reliable information on vaccination coverage against TBE in endemic countries is scarce.4,5 Available estimates of Slovenian TBE vaccination coverage were based on vaccination data collected annually by the National Institute of Public Health and the number of TBE vaccine doses distributed. The minimal proportion of the population fully protected by vaccination in 2009 was estimated to be ∼5% and was calculated as the total number of third primary doses reported in 2009 and the previous 2 years, plus booster immunizations reported in 2009 and previous 4 years, plus the number of second primary doses reported for 2009. Due to underreporting of performed vaccinations, this is certainly an underestimation. By 2009, a cumulative total of approximately 750 000 TBE vaccine doses had been distributed, a sufficient number for primary vaccination of approximately 250 000 individuals (12.5% of the total population).

To complement available information, our aim was to obtain the first reliable national estimate of self-reported uptake of vaccination against TBE in a probability sample of the Slovenian general population aged ≥15 years and identify factors associated with self-paid TBE vaccination uptake using the data from the 2007 Slovenian version of the European Health Interview Survey (EHIS).

Methods

The overall objective of regularly repeated EHIS, coordinated by Statistical Office of the European Communities on the European Union level, is to collect data on self-reported health status, preventive health practices and lifestyles that are linked to health of EU citizens and to find out how often they use various health-care services.6 In Slovenia, the 2007 EHIS was implemented by the National Institute of Public Health.7

Details of the survey methods have been published previously.6 Briefly, stratified two-stage probability sampling was used. The sampling frame was designed using the list of enumeration areas provided by the Central Population Registry. Within each of the 12 statistical regions of Slovenia, communities were implicitly stratified according to their type and size (six classes). Four hundred and twenty-five primary sampling units were sampled independently from the 12 regions with probability proportional to the size of eligible population, defined as the number of individuals residing in Slovenia aged ≥15 years. From each unit eight individuals aged ≥15 years were selected randomly.

Data were collected during October to December 2007 by means of face-to-face interviews at respondents’ homes using paper questionnaires. Weights were computed to adjust for the differences in survey response between different regions, types and sizes of communities, gender, age groups and education.

Two TBE vaccination related questions were added to the questionnaire: ‘Have you ever been vaccinated against TBE?’ and ‘What was the reason for starting vaccination against TBE?’ Responses offered to the second question were: ‘Due to occupational exposure’, ‘Due to exposure during training programme’, ‘As a military recruit or when in military service’ and ‘Other reasons’. The first three options corresponded to the three Slovenian indications for mandatory vaccination reimbursed by employer or within compulsory health insurance, thus free of charge for the vaccinated individual. The option ‘Other reasons’ captured TBE vaccination requested by and paid by individuals themselves. Everyone who responded ‘Other reason’ was also asked to report the reason.

We conducted analyses using statistical methods for complex survey data (svy commands) to account for stratification, two-stage sampling and weighting using STATA 7.0 statistical software (STATA Corp., College Station, TX, USA). Weighted proportion estimates with 95% confidence intervals (95% CIs) were computed overall and separately for men and women. Univariate analyses of association between self-reported self-paid TBE vaccination uptake and selected explanatory variables were performed by logistic regression to obtain pseudo-maximum likelihood estimates of odds ratios (ORs) together with 95% CI, and results of adjusted Wald tests of significance. Individuals who reported to have been vaccinated due to occupational exposure, exposure during education or training and as military recruits, were excluded from analyses. When the proportions changed systematically, tests for trend were computed by the inclusion of linear terms in the logistic regression model. Variables were included in a series of logistic regression multivariate models if they were associated with the outcome at the significance level of P < 0.1 in univariate analyses. Variables that remained associated with the outcome at the significance level of P < 0.1 were retained in the final model. Records with missing data for any of the variables in the final multivariate logistic regression models were excluded from the final models. Pseudo-maximum likelihood adjusted odds ratios (aORs) with 95% CI for all variables left in the final model and the results of adjusted Wald F-test for significance were computed.

Ethical approval was obtained from the Medical Ethics Committee at the Ministry of Health of the Republic of Slovenia.

Results

Altogether, 2118 individuals (un-weighted count) aged ≥15 years were interviewed. Overall survey response was 68%.7 Two thousand and seventy-five men and women (un-weighted count) reported their TBE vaccination status, resulting in an overall item response of 98%.

The overall self-reported prevalence of TBE vaccination uptake was 12.4% (95% CI: 10.9–14.0%). Of these, due to occupational exposure 3.2% (95% CI: 2.5–4.1%), exposure during education/training 2.3% (95% CI: 1.8–3.1%), and as military recruits 2.2% (95% CI: 1.6–3.0%). Additional 4.6% (95% CI: 3.7–5.7%), 4.5% of men and 4.8% of women, reported to be vaccinated due to ‘other reasons’, all of whom stated they were vaccinated on their own initiative for some preventive reason. Proportions of men and women who reported TBE vaccination uptake according to different reasons and selected socio-demographic characteristics are shown in table 1. The overall vaccination uptake was higher among men than among women [16.5 and 8.4%, respectively; P < 0.001, OR = 2.1 (95% CI: 1.6–2.8)]. Both, men and women with higher education and higher income had higher vaccination uptake (all P < 0.05). There was no evidence for a different uptake between regions. The highest uptake (34.0%) was reported by 25- to 34-year-old men, born during 1973–82.

View this table:
Table 1

Self-reported overall TBE vaccination uptake according to reasons and selected demographic characteristics, 2007, Slovenia

MenWomen
Proportion vaccinatedCountProportion vaccinatedCount
% (95% CI)UWTWT% (95% CI)UWTWT
Overall16.5 (14.2–19.0)96810148.4 (6.9–10.3)11071062
Reimbursement, vaccination reason
    Reimbursed by employer or HIIS12.0 (10.0–14.4)96810143.7 (2.7–5.1)11071062
    Occupational exposure5.4 (4.1–7.1)96810141.1 (0.6–2.2)11071062
    Exposure during education/training2.1 (1.4–3.2)96810142.6 (1.7–3.7)11071062
    Military recruits4.5 (3.3–6.2)968101411071062
    Paid and requested by individual4.5 (3.3–6.0)96810144.8 (3.6–6.2)11071062
Age (years)
    15–2417.3 (12.0–24.3)15914914.1 (9.3–20.9)163139
    25–3434.0 (26.7–42.0)15718911.3 (7.4–16.8)186177
    35–4415.4 (10.5–21.9)1611879.8 (6.1–15.4)171175
    45–5413.5 (9.1–19.6)1791926.6 (3.8–11.3)205183
    55–646.3 (3.4–11.4)1541464.9 (2.5–9.5)154147
    65–749.6 (5.4–16.5)103995.8 (2.9–11.2)126124
    ≥757.7 (3.0–18.3)55535.5 (2.5–11.7)102117
Education
    Elementary school or less11.1 (7.6–16.0)2212096.4 (4.2–9.6)359346
    Secondary16.9 (14.0–20.4)5996527.4 (5.5–9.8)550514
    Higher or more21.9 (15.7–29.6)14815314.6 (10.4–20.2)198202
Income (EUR)
    Low (<1051)8.8 (5.9–12.8)2692875.4 (3.4–8.2)535358
    Medium (1051–2050)22.0 (17.7–27.0)33635210.5 (7.7–14.2)337354
    High (>2050)20.5 (14.0–29.0)11912414.1 (8.6–22.3)115109
Regions (covered by nine regional IPHs)
    Celje13.6 (8.8–20.4)1381627.7 (4.6–12.6)148155
    Nova Gorica11.6 (4.4–27.1)48524.3 (1.0–16.1)5654
    Koper17.0 (10.2–26.8)817011.1 (5.8–20.3)10384
    Kranj22.7 (14.8–33.3)10010711.5 (6.6–19.5)10799
    Ljubljana18.1 (14.0–23.1)2522899.2 (6.8–12.4)329357
    Maribor12.8 (8.3–19.3)1831828.4 (4.5–14.9)177158
    Murska Sobota16.6 (9.4–27.6)69606.3 (2.018.1)8064
    Novo mesto14.5 (6.9–28.1)46511.8 (0.3–11.5)5757
    Ravne24.3 (13.0–40.6)51419.9 (3.4–25.8)5036
  • HIIS, Health Insurance Institute of Slovenia; IPH, Institute of Public Health; UWT, un-weighted count of individuals; WT, weighted count of individuals.

Among men born during 1974–84 (23- to 33-years old in 2007), majority of whom should have been vaccinated against TBE as military recruits, only four cohorts reported vaccination uptake rates of at least 50% (27 years old: 62.5%; 26 years old: 55.6%; 28 and 29 years old: 50.0%).

Table 2 shows the proportions of individuals who reported to have been vaccinated against TBE on their own initiative and paying for vaccination themselves, according to selected demographic and behavioural characteristics. There was no evidence for differences in self-paid TBE vaccination uptake between genders, different age groups and individuals residing in different regions. However, the uptake was higher among those with higher education, higher income, not being overweight and individuals reporting to have ever been vaccinated against influenza.

View this table:
Table 2

Self-reported self-paid TBE vaccination uptake according to demographic and behavioural characteristics (univariate analyses), 2007, Slovenia

Proportion vaccinatedCountOR (95% CI)P-value
% (95% CI)UWTWT
Alla5.0 (4.0–6.2)19141915
Gender
    Female5.0 (3.8–6.5)1064102310.91
    Male5.1 (3.7–6.8)8508921.02 (0.69–1.52)
Age (years)
    15–246.1 (3.8–9.7)28825810.30
    25–346.3 (3.9–10.2)2843011.04 (0.50–2.16)
    35–445.6 (3.5–8.8)3083340.91 (0.45–1.81)
    45–544.9 (2.3–6.6)3603520.63 (0.30–1.35)
    55–643.3 (1.8–6.1)2972860.52 (0.23–1.19)
    65–746.5 (4.0–10.5)2252211.07 (0.51–2.26)
    ≥752.9 (1.3–6.4)1521640.45 (0.17–1.20)
Regions (covered by nine regional IPHs)
    Celje3.8 (2.2–6.4)26429410.46
    Nova Gorica3.8 (0.9–15.1)991011.00 (0.20–4.97)
    Koper4.9 (2.3–9.9)1661401.30 (0.51–3.32)
    Kranj7.4 (4.0–13.3)1831842.03 (0.87–4.76)
    Ljubljana5.4 (3.7–7.9)5365931.44 (0.73–2.87)
    Maribor4.4 (2.5–7.6)3383171.17 (0.53–2.58)
    Murska Sobota4.1 (2.1–8.1)1371141.09 (0.44–2.70)
    Novo mesto2.6 (0.7–9.1)981010.67 (0.16–2.83)
    Ravne9.8 (4.8–19.1)93702.76 (1.07–7.11)
Education
    Elementary or less4.2 (2.8–6.3)55753210.001
    Secondary4.0 (3.0–5.4)104210600.96 (0.55–1.65)
    Higher or more9.6 (6.4–14.0)3153222.41 (1.31–4.42)
Income (EUR)(Pt < 0.01)
    Low (<1051)3.3 (2.1–5.0)59761210.03
    Medium     (1051–2050)5.5 (3.9–7.8)6126101.72 (0.98–3.02)
    High (>2050)8.0 (4.8–13.2)2092082.57 (1.27–5.21)
Body mass index
    Normal/low     (<25.0)6.4 (4.8–8.4)86883610.02
    Overweight/     fat (≥25.0)4.0 (2.9–5.3)100610330.60 (0.40–0.91)
Vaccinated against flu
    No3.5 (2.5–4.9)132113171<0.001
    Yes8.5 (6.4–11.1)5815852.54 (1.61–4.00)
  • a: Individuals who reported to have been vaccinated due to occupational exposure, exposure during education or training and as military recruits were excluded from analyses

  • IPH, Institute of Public Health; UWT, un-weighted count of individuals; WT, weighted count of individuals; P, P-value for test for heterogeneity; Pt, P-value for test for trend

Characteristics independently associated with higher odds for self-paid vaccination against TBE were: (i) higher monthly income [>€2050: adjusted aOR 2.5 (95% CI: 1.3–5.2); €1051–2050: aOR 1.8 (95% CI: 1.0–3.25) in comparison to those with <€1051]; (ii) not being overweight [overweight: aOR 0.6 (95% CI: 0.4–1.0) in comparison to those not] and (iii) ever being vaccinated against influenza [vaccinated: aOR 2.9 (95% CI: 1.7–4.9) in comparison to those not] (table 3).

View this table:
Table 3

Predictors of self-reported self-paid TBE vaccination uptake (univariate and multivariate analyses), 2007, Sloveniaa

Proportion vaccinatedCountOR (95% CI)P-valueaOR (95% CI)P-value
% (95% CI)UWTWT
Income (EUR)Pt = 0.006Pt = 0.006
    Low (<1051)3.3 (2.1–5.0)58059910.0210.03
    Medium (1051–2050)5.6 (4.0–7.9)6015981.76 (1.00–3.13)1.80 (1.00–3.25)
    High (>2050)8.1 (4.8–13.3)2072062.61 (1.28–5.31)2.55 (1.25–5.20)
Overweight
    No (BMI <25)6.4 (4.6–8.8)61159910.0410.06
    Yes (BMI ≥25)3.9 (2.8–5.6)7778040.60 (0.36–0.97)0.62 (0.38–1.01)0.38–1.01
Vaccinated against flu
    No3.3 (2.3–4.9)9569651<0.0011<0.001
    Yes8.6 (6.2–11.7)4324392.72 (1.60–4.60)2.88 (1.69–4.90)
  • a: Individuals who reported to have been vaccinated because of higher risk due to occupational exposure, exposure during education or training and as military recruits were excluded from analyses. An un-weighted count of 1388 individuals without missing values for any of the variables in the model were included in analyses

  • BMI, body mass index; UWT, un-weighted count of individuals; WT, weighted count of individuals; P, P-value for test for heterogeneity; Pt, P-value for test for trend

Discussion

Although vaccination against TBE was introduced in 1986, by 2007, the proportion of the general population aged ≥15 years who reported to have ever been vaccinated against TBE remained rather low (12.4%) and Slovenia remained one of the countries with the highest reported incidence rates of TBE. Due to higher uptake of vaccination among men for reasons of occupational exposure and as military recruits during 1993–2003 which was reimbursed either by employer or the army, the overall uptake was higher among men (16.5%) than among women (8.4%). In contrast, there was no difference in the proportion of men and women who reported to have requested vaccination against TBE themselves and also paid for it (4.5 and 4.8%, respectively). Three predictors for higher uptake of self-paid vaccination against TBE were: having a high income, not being overweight and ever being vaccinated against influenza.

Our results show rather low TBE vaccination uptake, especially in comparison with vaccination rates in Austria where 88% of the total population have a history of TBE vaccination, with 58% being regularly vaccinated within the officially recommended vaccination schedule.4,5 In addition to Austrian data, there is not much published information about vaccination coverage in the general population living in TBE endemic countries of the EU. In Stockholm County in Sweden, ∼12.5% inhabitants had been vaccinated (data from 2001), and more than a cumulative total of one million doses have been distributed by 2007.8,9 The results of the Finbalt survey conducted in Latvia in 2004 showed that 25% of adults 15- to 64-years old reported having received at least one vaccination against TBE.10 TBE vaccination surveys conducted by Growth from Knowledge Group (GfK) in the general population of nine EU endemic countries in 2009, reported rather low rates of vaccination coverage against TBE in all, varying from the lowest of 9% in Lithuania to the highest of 38% in Latvia, except for Austria (86%).11

Our results suggest that self-reported TBE vaccination rates might be slightly higher in the two northern regions Gorenjska and Koroška covered by the regional Institutes of Public Health Kranj and Ravne, although the differences were not statistically significant. In these two regions, also TBE reported incidence rates have been highest. This could indicate some modest behavioural response to the perceived risk of TBE as suggested previously.10

Though vaccination of military recruits was mandatory during 1993–2003, corresponding cohorts of Slovenian men born during 1974–84 (23- to 33-years old at the time of the survey) did not report as high TBE vaccination uptake as expected. The overall vaccination uptake among men 23- to 33-years old at the time of the survey was only 32.8%, which, nevertheless, was several times higher than among women of the same age group (11.2%). This low coverage of mandatory vaccination may reflect the weaknesses in the implementation of our national vaccination programme when resources are not ensured within the compulsory health insurance but covered by employers or the army, or insufficient investment in the logistical aspects of national immunisation programme implementation.

Similar to our results that did not indicate differences in the uptake of self-paid TBE vaccination between men and women no gender differences in the uptake were reported from Latvia.10

Other published studies found similar predictors for TBE vaccination uptake. Not surprisingly, our results showed higher uptake of self-paid TBE vaccination among those with higher income. Similarly, in the general population of Latvia, vaccination was significantly less likely to be reported by people on lowest incomes associated with the lowest level of education.10 Also, in Austrian cross-sectional study among children in an endemic area of Styria, TBE vaccination coverage was lowest in families with four or more children and those with mothers with lowest level of education.12,13 In contrast to our results, this Austrian study also reported about different TBE vaccination uptake between rural and urban areas.13 Also not surprisingly, self-paid vaccination uptake was higher among those not being overweight and those ever vaccinated against seasonal influenza, probably reflecting healthy lifestyle attitudes, general compliance with preventive public health measures and favourable attitude towards vaccination in general.

Though users of complementary and alternative medicine (CAM) often show a lower rate of routine immunizations or influenza vaccination,14–16 Swiss authors found, surprisingly, that TBE vaccination rate was significantly higher in the CAM users than among the non-users.17 Similar to Swiss data, we also found higher TBE vaccination rates in users of homeopathy (25%) and chiropractics (16.7%) in comparison to non-users (12.3%) in both groups of non-users), but these differences were not statistically significant.

Methodological strengths of our survey included the use of reliable general population sampling frame, two stage probability sampling, sufficiently high survey response and weighing the data. The limitations of our survey include validity constraints of self-reported information. Self-reporting of vaccination status has been reported to result in some misclassification bias.18 Unfortunately, TBE awareness was not measured in the survey. As it is one of the most important factors for higher vaccination rates11 it would be reasonable to conduct further research on this topic. The major limitation of our survey was that with only two additional questions that we managed to negotiate to be included into the Slovenian 2007 version of the EHIS, we were not able to capture the information about the vaccination coverage. We were only able to estimate the proportion of individuals who reported to have ever been vaccinated against TBE irrespective of how many doses they had received. Thus, our results only indicate the upper limit of the proportion of the population seeking vaccination and not the proportion of the population fully vaccinated against TBE. Also, our estimate does not include children below 15 years old. Despite these limitations, our results represent the first national estimate of self-reported uptake of vaccination against TBE in a probability sample of the Slovenian general population aged ≥15 years and add to our understanding of social inequalities in access and other predictors of self-paid TBE vaccination uptake.

Since TBE morbidity in Slovenia is substantial and the burden of patients with moderate or severe neurological sequelae which can appear in one-third of patients or even more is high,19–23 it is important to improve vaccination coverage, as this is the only effective approach to TBE prevention. Although in Slovenia relevant surveillance information is not available, it is likely that similar to Austria, over the years TBE has become a disease that is predominantly acquired during leisure activities and is no longer a disease predominant in groups at higher occupational risk.4 Risk group-based approach as currently used in Slovenia does not seem sufficient. As it became obvious very early in Austria, high vaccination coverage of professional groups at risk was not sufficient to substantially reduce the morbidity of TBE. Thus, Austria started mass vaccination campaign already in 1981 and succeeded to increase vaccination coverage of the general population from 6% in 1980 to 86% in 2001, in spite of the fact that only people with occupational risk are vaccinated free of charge, and only part of the costs are covered by health insurance for the rest of the population.4 Thus, it is crucial to understand constraints in more universal access to vaccination and factors associated with vaccination uptake in the general population. To reduce TBE morbidity in Slovenia, vaccination coverage of the general population should be increased. Offering vaccination within mandatory health insurance (free of charge for the vaccinated individuals) together with intensive vaccination promotion for the general population would increase the vaccination coverage and reduce the social inequality in access.

Funding

The implementation of Slovenian version of EHIS was funded by the National Institute of Public Health.

Conflicts of interest: None declared.

Key points

  • The aim was to obtain the first Slovenian national estimate of self-reported uptake of vaccination against TBE and identify predictors of self-paid vaccination uptake among the general population aged ≥15 years.

  • Self-reported prevalence of TBE vaccination uptake was 12.4% overall and 4.6% of the general population paid for vaccination themselves.

  • Characteristics independently associated with higher odds for self-paid vaccination were high income, not being overweight, and ever being vaccinated against influenza.

  • Offering vaccination to the general population within compulsory health insurance together with intensive vaccination promotion would increase the vaccination coverage, reduce the social inequality in access and reduce high TBE morbidity in Slovenia.

References

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