Demographic Factors Associated with Hantavirus Infection in Bank Voles (<i>Clethrionomys glareolus</i>)

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

doi:10.3201/eid0809.020037

Cited by 110 publications

(104 citation statements)

References 35 publications

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“…Several hypotheses, not necessarily mutually exclusive, may be suggested to explain the patterns of maturation and survival we have described. In bank voles, the probability of acquiring PUUV infection has been found to increase with a proxy of age (body weight; Verhagen et al, 1986;Olsson et al, 2002). Hence, within the group of reproductively inactive bank voles, PUUV IgG-positive individuals might be older and, consequently, more likely to mature, or to die, in the near future.…”

Section: Discussionmentioning

confidence: 99%

Impact of Puumala Virus Infection on Maturation and Survival in Bank Voles: A Capture-Mark-Recapture Analysis

Tersago

Crespin

Verhagen

et al. 2012

Journal of Wildlife Diseases

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ABSTRACT:Many zoonotic diseases are caused by rodent-borne viruses. Major fluctuations in the transmission of these viruses have been related to large changes in reservoir host population numbers due to external factors. However, the impact of the pathogen itself on the demography of its reservoir host is often overlooked. We investigated the impact of Puumala virus (PUUV) on survival and reproductive maturation probability of its reservoir host, the bank vole (Myodes glareolus). Three years (2004-06) of data from nine independent sites in southern Belgium were collected and analyzed with a capture-mark-recapture (CMR) method that includes statistical correction for the variation in capture probability of voles. A multistate model based on four states of reproductive activity and PUUV immunoglobulin G (IgG) antibody status was used to estimate survival and probability of transition from one reproductive or infection state to another. Although survival estimates for reproductively active voles were similar between infected and noninfected individuals, PUUV infection in reproductively inactive voles decreased mean monthly survival by 14%. PUUV infection was associated with a threefold increase in the probability of reproductive maturation in bank voles. Moreover, the probability of PUUV IgG seroconversion was three times higher for reproductively active voles compared to reproductively inactive voles. Our model indicates that PUUV infection may alter bank vole population dynamics by affecting both survival and maturation in its host. Additional studies, using CMR methodology with shorter time intervals between trapping sessions and possibly a longer duration, are needed to confirm these findings.

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Section: Discussionmentioning

confidence: 99%

Impact of Puumala Virus Infection on Maturation and Survival in Bank Voles: A Capture-Mark-Recapture Analysis

Tersago

Crespin

Verhagen

et al. 2012

Journal of Wildlife Diseases

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“…Differences have commonly been observed in PUUV incidence, with males (Olsson et al, 2002;Deter et al, 2008a) and mature bank voles (for example, Escutenaire et al, 2002) more frequently infected than females and immature ones. Behavioral and physiological characteristics participate in shaping these differences.…”

Section: Intrinsic Factors Shaping Immunoheterogeneitymentioning

confidence: 99%

“…Behavioral and physiological characteristics participate in shaping these differences. Protection of newborns by maternal antibodies and higher risk of exposure for sexually mature voles through fighting, mating or communal nesting (Escutenaire et al, 2002;Olsson et al, 2002) could mediate age-dependent prevalence. Our results suggest that individual variations of immune gene expression could reinforce these differences in the epidemiological roles of particular bank vole groups within natural populations.…”

Section: Intrinsic Factors Shaping Immunoheterogeneitymentioning

confidence: 99%

“…Field surveys and laboratory experiments have indicated that the probability of infection with PUUV differs between individual bank voles, which also differ in their response to PUUV infection (Olsson et al, 2002;Hardestam et al, 2008;Deter et al, 2008b;Guivier et al, 2010a). Polymorphism and variability in the expression of immune genes may determine the ability of the vole to control hantavirus replication (Plyusnin et al, 1997;Makela et al, 2002;Klein et al, 2004;Terajima et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

et al. 2013

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Heterogeneity in environmental conditions helps to maintain genetic and phenotypic diversity in ecosystems. As such, it may explain why the capacity of animals to mount immune responses is highly variable. The quality of habitat patches, in terms of resources, parasitism, predation and habitat fragmentation may, for example, trigger trade-offs ultimately affecting the investment of individuals in various immunological pathways. We described spatial immunoheterogeneity in bank vole populations with respect to landscape features and co-infection. We focused on the consequences of this heterogeneity for the risk of Puumala hantavirus (PUUV) infection. We assessed the expression of the Tnf-a and Mx2 genes and demonstrated a negative correlation between PUUV load and the expression of these immune genes in bank voles. Habitat heterogeneity was partly associated with differences in the expression of these genes. Levels of Mx2 were lower in large forests than in fragmented forests, possibly due to differences in parasite communities. We previously highlighted the positive association between infection with Heligmosomum mixtum and infection with PUUV. We found that Tnf-a was more strongly expressed in voles infected with PUUV than in uninfected voles or in voles co-infected with the nematode H. mixtum and PUUV. H. mixtum may limit the capacity of the vole to develop proinflammatory responses. This effect may increase the risk of PUUV infection and replication in host cells. Overall, our results suggest that close interactions between landscape features, co-infection and immune gene expression may shape PUUV epidemiology.

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“…Also, field surveys and experiments indicate that some variation exists among bank voles in their probability of being infected with PUUV (e.g. Deter et al, 2008a;Olsson et al, 2002). Experimental infections have also shown that infectivity varies among bank voles (Hardestam et al, 2008;.…”

mentioning

confidence: 99%

Associations between MHC genes and Puumala virus infection in Myodes glareolus are detected in wild populations, but not from experimental infection data

Guivier

Galan

Malé

et al. 2010

Journal of General Virology

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We analysed the influence of MHC class II Dqa and Drb genes on Puumala virus (PUUV) infection in bank voles (Myodes glareolus). We considered voles sampled in five European localities or derived from a previous experiment that showed variable infection success of PUUV. The genetic variation observed in the Dqa and Drb genes was assessed by using single-strand conformation polymorphism and pyrosequencing methods, respectively. Patterns were compared with those obtained from 13 microsatellites. We revealed significant genetic differentiation between PUUVseronegative and -seropositive bank voles sampled in wild populations, at the Drb gene only. The absence of genetic differentiation observed at neutral microsatellites confirmed the important role of selective pressures in shaping these Drb patterns. Also, we found no significant associations between infection success and MHC alleles among laboratory-colonized bank voles, which is explained by a loss of genetic variability that occurred during the captivity of these voles.

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

Cited by 110 publications

References 35 publications

Impact of Puumala Virus Infection on Maturation and Survival in Bank Voles: A Capture-Mark-Recapture Analysis

Impact of Puumala Virus Infection on Maturation and Survival in Bank Voles: A Capture-Mark-Recapture Analysis

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

Associations between MHC genes and Puumala virus infection in Myodes glareolus are detected in wild populations, but not from experimental infection data

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