The Importance of Bank Vole Density and Rainy Winters in Predicting Nephropathia Epidemica Incidence in Northern Sweden

Abstract

Pathogenic hantaviruses (family Bunyaviridae, genus Hantavirus) are rodent-borne viruses causing hemorrhagic fever with renal syndrome (HFRS) in Eurasia. In Europe, there are more than 10,000 yearly cases of nephropathia epidemica (NE), a mild form of HFRS caused by Puumala virus (PUUV). The common and widely distributed bank vole (Myodes glareolus) is the host of PUUV. In this study, we aim to explain and predict NE incidence in boreal Sweden using bank vole densities. We tested whether the number of rainy days in winter contributed to variation in NE incidence. We forecast NE incidence in July 2013–June 2014 using projected autumn vole density, and then considering two climatic scenarios: 1) rain-free winter and 2) winter with many rainy days. Autumn vole density was a strong explanatory variable of NE incidence in boreal Sweden in 1990–2012 (R2 = 79%, p<0.001). Adding the number of rainy winter days improved the model (R2 = 84%, p<0.05). We report for the first time that risk of NE is higher in winters with many rainy days. Rain on snow and ground icing may block vole access to subnivean space. Seeking refuge from adverse conditions and shelter from predators, voles may infest buildings, increasing infection risk. In a rainy winter scenario, we predicted 812 NE cases in boreal Sweden, triple the number of cases predicted in a rain-free winter in 2013/2014. Our model enables identification of high risk years when preparedness in the public health sector is crucial, as a rainy winter would accentuate risk.

Preliminary insights into the genetics of bank vole tolerance to Puumala hantavirus in Sweden

“…We could not use PUUV seroprevalence to assess PUUV‐mediated pressure in the bank vole populations. Indeed, these populations undergo 3‐ to 4‐year population dynamic cycles (Hörnfeldt, ) that lead to strong variations of PUUV distribution at fine spatial and temporal scales (Khalil et al, ). Dense spatiotemporal surveys are therefore required to gain relevant information on PUUV circulation in these bank vole populations (e.g., Khalil et al, , Ecke, Angeler, Magnusson, Khalil, & Hörnfeldt, ).…”

“…Geographic variations in ecoregions are represented with yellow, orange, and green colors. The contact zone between the two mitochondrial lineages of Myodes glareolus is indicated with a black line that lead to strong variations of PUUV distribution at fine spatial and temporal scales (Khalil et al, 2014). Dense spatiotemporal surveys are therefore required to gain relevant information on PUUV circulation in these bank vole populations (e.g., Khalil et al, 2017, Ecke, Angeler, Magnusson, Khalil, & Hörnfeldt, 2017.…”

Spatial and Temporal Epidemiology of Nephropathia Epidemica Incidence and Hantavirus Seroprevalence in Rodent Hosts: Identification of the Main Environmental Factors in Europe

“…Several studies failed to find any association between NE incidence and precipitation measured during different seasons for up to three years prior to the detection of NE cases (Clement et al., ; Linard et al., ; Tersago et al., ; Viel et al., ), despite a monitoring period ranging from three to 15 years (Table ). In contrast, a long‐term study (Khalil et al., with data from 1990 to 2012) found a positive association between the number of rainy days during winter (December–March) and annual NE incidence (from July to June year +1). Zeimes et al.…”

“…Considering only one spatial scale when investigating a biological process, such as PUUV epidemiology, may thus lead to overlook some aspects that link PUUV distributions in humans and rodents with environmental factors. Third, most studies investigated relationships between environmental factors and NE incidence within artificial administrative entities, such as municipalities (Barrios et al., ), cantons (Viel et al., ), counties (Khalil et al., ; Pettersson et al., ; Thomas Palo, ), states (Piechotowski et al., ; Schwarz et al., ) or countries (Clement et al., ; Tersago et al., ) ( n = 14 of 16 articles about NE incidence). Nevertheless, Zeimes et al.…”

Dampening of population cycles in voles affects small mammal community structure, decreases diversity, and increases prevalence of a zoonotic disease

“…Pathogens hosted by small mammals and transmitted to humans include the Puumala virus (PUUV) hosted by the bank vole ( Myodes glareolus Schreber) (Brummer‐Korvenkontio et al., 1980) and causing nephropatia epidemica (NE), a hemorrhagic fever in humans, sometimes leading to kidney failure, and in rare cases to death (Vapalahti et al., 2003). The annual incidence of NE in humans can be explained with high degree (84% of variability) by density of M. glareolus in autumn and the number of rainy days in winter (Khalil, Olsson, et al., 2014). In contrast, the number of PUUV‐infected bank voles and PUUV prevalence (the proportion of infected bank voles) has been shown to be affected by habitat type (Magnusson, Ecke, et al., 2015; Voutilainen et al., 2012).…”