Behavioral, Physiologic, and Habitat Influences on the Dynamics of Puumala virus Infection in Bank Voles

Sophie Escutenaire, Patrice Chalon, Florence De Jaegere, Lucie Karelle-Bui, Georges Mees, Bernard Brochier, Francine Rozenfeld, and Paul-Pierre Pastoret


Emerging Infectious Diseases. 2002;8(9) 

In This Article

Abstract and Introduction

Populations of bank voles (Clethrionomys glareolus) were monitored during a 4-year study in southern Belgium to assess the influence of agonistic behavior, reproductive status, mobility, and distribution of the rodents on the dynamics of Puumala virus (abbreviation: PUUV; genus: Hantavirus) infection. Concordance was high between data from serologic testing and results of viral RNA detection. Wounds resulting from biting or scratching were observed mainly in adult rodents. Hantavirus infection in adults was associated with wounds in the fall, i.e., at the end of the breeding season, but not in spring. In addition, sexually active animals were significantly more often wounded and positive for infection. Hantavirus infection was associated with higher mobility in juvenile and subadult males. Seroconversions observed 6 months apart also occurred more frequently in animals that had moved longer distances from their original capture point. During nonepidemic years, the distribution of infection was patchy, and positive foci were mainly located in dense ground vegetation.

Hantaviruses (family Bunyaviridae) are rodent-borne zoonotic agents responsible for human diseases called hemorrhagic fever with renal syndrome (HFRS) in Europe and Asia and hantavirus pulmonary syndrome (HPS) in the Americas.[1,2] Viral transmission occurs through inhalation of aerosols from the urine, saliva, or feces of infected rodents and possibly through biting.[3,4,5] Hantavirus infection persists in reservoir species apparently without causing clinical signs.[6] In experimentally infected rodents, the virus is distributed in different organs (including lungs, kidneys, intestines, and salivary glands) and elicits the production of antibodies that may be detected lifelong, while the viremia is generally transient.[4,7,8] In the wild, adult rodents are generally more often infected than younger animals. The age-dependent prevalence may result from protection of newborns by maternal antibodies and from higher risk of infection for sexually mature rodents through fighting, mating, or communal nesting.[9,10,11,12] In Europe, Puumala virus (PUUV), which causes a mild form of HFRS in humans, is carried by bank voles (Clethrionomys glareolus).[13] No data are available on the dynamics of PUUV infection in bank vole populations according to behavioral patterns. Most seroconversions recorded in a capture-mark-recapture (CMR) study of PUUV transmission occurred during the breeding season and in sexually mature voles, with a prevalence bias in favor of mature males.[10] Aggressive encounters in adults and the occupation of exclusive territories by breeding females are characteristic of the breeding season in bank voles.[14,15,16]

We studied the influence of aggressive behavior, reproductive status, and mobility of bank voles on the prevalence of PUUV infection. Along with behavioral and physiologic factors, we studied the influence of habitat on bank vole distribution. Two HFRS outbreaks were reported in Belgium in 1996 (224 cases) and in 1999 (124 cases).[17,18] Our survey was conducted from 1996 to 1999 in southern Belgium, where most patients had been reported during the epidemic years. In our trapping sites, rodent population densities were the highest in 1996 and 1999, as was the prevalence of PUUV infection, with 41 (19.2%) of 213 and 259 (39.3%) of 659, respectively, of bank voles positive;[19] S. Escutenaire, unpub. data).