A national case-control study identifies human socio-economic status and activities as risk factors for tick-borne encephalitis in Poland

PLoS ONE. 2012 Sept; 7(9): e45511

Pawel Stefanoff,1 Magdalena Rosinska,1 Steven Samuels,2 Dennis J White,2,3 Dale L Morse,4 Sarah E Randolph.5

 

  1. Department of Epidemiology, National Institute of Public Health – National Institute of Hygiene, Warsaw, Poland
  2. State University of New York at Albany, School of Public Health, Rensselaer, NY
  3. New York State Department of Health, Albany, NY
  4. National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
  5. Department of Zoology, University of Oxford, Oxford, United Kingdom

 

Abstract

Background:  Tick-borne encephalitis (TBE) is endemic to Europe and medically highly significant. This study, focused on Poland, is the first to identify individual risk factors for TBE symptomatic infection.

Methods and Findings: In a nation-wide population-based case-control study, of the 351 TBE cases reported to local health departments in Poland in 2009, 178 were included in the analysis. For controls, of 2704 subjects (matched to cases by age, sex, district of residence) selected at random from the national population register, two were interviewed for each case and a total of 327 were suitable for the analysis. Questionnaires yielded information on potential exposure to ticks during the six weeks (maximum incubation period) preceding disease onset in each case. Independent associations between disease and socio-economic factors and occupational or recreational exposure were assessed by conditional logistic regression, stratified according to residence in known endemic and non-endemic areas. Adjusted population attributable fractions (PAF) were computed for significant variables. In endemic areas, highest TBE risk was associated with spending >10 hours/week in mixed forests and harvesting forest foods (adjusted odds ratio 19.19 [95% CI: 1.72 – 214.32]; PAF 0.127 [0.064-0.193]), being unemployed (11.51 [2.84-46.59]; 0.109 [0.046-0.174]), or employed as a forester (8.96 [1.58-50.77]; 0.053 [0.011-0.100]) or manual worker (5.39 [2.21-13.16]; 0.202 [0.090-0.282]). Other activities (swimming, camping and travel to non-endemic regions) reduced risk. Outside TBE endemic areas, risk was greater for those who spent >10 hours/week on recreation in mixed forests (5.34 [1.28-22.38]; 0.191 [0.065-0.304]) and visited known TBE endemic areas (7.18 [1.90-27.08]; 0.058 [-0.007-0.144]), while secondary education reduced risk.

Conclusions: These socio-economic factors and associated human activities identified as risk factors for symptomatic TBE in Poland are consistent with results from previous correlational studies across eastern Europe, and allow public health interventions to be targeted at particularly vulnerable sections of the population.

 

Supplement:

Background:  Many diseases are caused by microbes that circulate naturally amongst wildlife hosts; humans are infected accidentally through contact with infected agents.  Vector-borne pathogens, spread from host to host by blood-sucking insects or ticks, are prime examples.  Many of these so-called ‘zoonoses’ have increased in distribution and incidence in recent decades, and the search for causes typically depends on identifying correlations between changing patterns of infection and environmental factors, in both time and space.  Correlations at this population level are the first indication of a causal relationship, but can never prove causality.  Instead, epidemiological analytical studies enable direct estimation of the association between exposure and disease in the affected populations, allowing inferences on causal associations.  The “gold standard” of analytical epidemiology, experimental studies, are not allowed due to ethical constraints.  Also, population-based cohort studies are logistically non-realistic due to the enormous sample sizes necessary to detect sufficient numbers of tick-borne disease cases.  As a feasible alternative, during 2009 we performed a large, population-based case-control investigation of one of the most significant tick-borne diseases in Europe, tick-borne encephalitis (TBE) caused by a virus transmitted by the ubiquitous and abundant tick Ixodes ricinus.  This disease is untreatable, has an approximately 1% case fatality rate, and also causes long-term severe neurological symptoms in 30-50% of patients.

The study:  Incidence has been rising steadily in western Europe over recent decades, and is particularly high in central and eastern Europe especially since the early 1990s.  In Poland there are typically 200-300 symptomatic TBE cases per year, with the majority occurring in the northeast of the country.  We showed that for the 350 cases in 2009, highest risk was related to specific recreational, occupational and socio-economic factors.  Specifically, in endemic areas, people who spent 10 or more hours per week in mixed deciduous and coniferous forests harvesting forest foods (edible fungi and berries), or those employed as foresters or in low paid unspecialized manual work, had significantly higher risk of infection.  Similarly, for people who lived outside recognized endemic regions, those who visited endemic areas or spent 10 hours or more per week on recreation in mixed forests also had a raised risk of infection.

 

 

Sarah Randolph-1

Sarah Randolph-2

Left: Ixodes ricinus tick questing for a host.  Right: Odds ratios for significant risk factors for contracting symptomatic tick-borne encephalitis, Poland, January-December 2009.  Notice the interaction between time spent in mixed forest and collecting forest foods.

 

Significance of results:  The results of this case-control study are entirely consistent with those of previous correlational studies in central and eastern Europe, and add weight to the conclusion that the sudden increase in incidence there in the early 1990s was an unintended consequence of the collapse of communism and the shift to a market economy.  Both the rise in wealth and the rise in unemployment and poverty resulted in greater exposure of people to infected ticks in forests.  In the former case there was more opportunity for leisure and outdoor recreation, while in the latter case people relied more on harvesting forest foods both for their own consumption and for trading on newly available national and international markets.  The epidemiological consequences of poverty are likely to be more extreme because of more limited opportunities for avoidance through changes in behaviour, and self-protection through effective but costly vaccination.  These conclusions can help to direct public health interventions by targeting those sections of the population that are at greatest risk but are least able to afford to take ameliorative action themselves.

 

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