Demographic Factors Associated With Hantavirus Infection in Bank Voles (Clethrionomys glareolus)

Gert E. Olsson, Neil White, Clas Ahlm, Fredrik Elgh, Ann-Christin Verlemyr, Per Juto, and R. Thomas Palo


Emerging Infectious Diseases. 2002;8(9) 

In This Article

Abstract and Introduction

The bank vole (Clethrionomys glareolus) is the natural reservoir of Puumala virus (PUUV), a species in the genus Hantavirus. PUUV is the etiologic agent of nephropathia epidemica, a mild form of hemorrhagic fever with renal syndrome. Factors that influence hantavirus transmission within host populations are not well understood. We evaluated a number of factors influencing on the association of increased PUUV infection in bank voles captured in a region in northern Sweden endemic for the virus. Logistic regression showed four factors that together correctly predicted 80% of the model outcome: age, body mass index, population phase during sampling (increase, peak, or decline/low), and gender. This analysis highlights the importance of population demography in the successful circulation of hantavirus. The chance of infection was greatest during the peak of the population cycle, implying that the likelihood of exposure to hantavirus increases with increasing population density.

The hantaviruses belong to the family Bunyaviridae and are the causative agents of hemorrhagic fevers with renal syndrome (HFRS) and hantavirus pulmonary syndrome (HPS) in humans.[1,2] Each distinct form of the virus is closely associated with a single, or possibly a few, rodent species.[3,4] Transmission of hantaviruses to humans occurs mainly through the inhalation of aerosols containing virus excreted from infected rodents; rodent-to-rodent transmission also may occur through biting and social grooming.[5,6,7] Approximately 150,000 human cases of hantavirus infection are reported per year worldwide.[6] Mortality in humans ranges from <0.5% in nephropathia epidemica, a mild form of HFRS,[8,9] to 5% to 10% from other HFRS,[6] and 45% from the more severe HPS.[4]

The only hantavirus isolated in Sweden is the Puumala virus (PUUV) from the bank vole (Clethrionomys glareolus), which serves as the natural reservoir species. The bank vole is the most common and widespread rodent species in northern Sweden. In northern Fennoscandia, density fluctuations may show up to 500-fold changes from peak to decline/low phase during a 3- to 4-year cycle.[10,11,12,13] In northern Sweden, the incidence of nephropathia epidemica in humans reaches an average of 40 serologically confirmed cases per 100,000 inhabitants in rodent peak years; yet up to 80% of human cases may be unrecognized.[14]

The importance of factors assumed to be associated with the occurrence of hantavirus infections in natural rodent host populations is not well understood.[15] Tools need to be developed to model hantavirus transmission in the wild reservoir species to better understand the relationship between the natural circulation of the virus and incidence of the disease in human populations. Among the factors of interest, rodent age and sex are known to distinguish cohorts of high seroprevalence in the wild.[16,17] These two factors represent the elapsed time of possible virus exposure and sex-biased behaviors. We have found,[18] Olsson et al., ms. in prep.) that higher numbers of PUUV-infected bank voles were associated with sites of known human hantavirus exposure in peak years, suggesting an influence of the local environment on subsequent chance of PUUV exposure. Therefore, sampling sites and phase during population cycle were included in our analysis to evaluate the probability of PUUV infection. We also investigated the influence of the body condition of bank voles on their probability of being PUUV seropositive. The models we considered included a measure of body condition because either 1) malnourished bank voles would be more likely to be PUUV infected because of increased susceptibility,[19] or 2) well-nourished bank voles would be more likely to be PUUV seropositive because high-quality habitats support higher or persistent numbers of bank voles,[20] facilitating the spread of the virus.

The aim of our study was to relate and rank characteristics of bank voles, i.e., age, body measurements, and sex, influencing the probability of being PUUV seropositive. Complementary independent variables are sampling sites and sampling events within the population cycle. Determining which of these factors is applicable is essential to the modeling of the spread of hantaviruses within a rodent host population.