Nephropathia Epidemica Caused by Puumala Virus in Bank Voles, Scania, Southern Sweden.

In 2018, a local case of nephropathia epidemica was reported in Scania, southern Sweden, more than 500 km south of the previously known presence of human hantavirus infections in Sweden. Another case emerged in the same area in 2020. To investigate the zoonotic origin of those cases, we trapped rodents in Ballingslöv, Norra Sandby, and Sörby in southern Sweden during 2020‒2021. We found Puumala virus (PUUV) in lung tissues from 9 of 74 Myodes glareolus bank voles by screening tissues using a hantavirus pan-large segment reverse transcription PCR. Genetic analysis revealed that the PUUV strains were distinct from those found in northern Sweden and Denmark and belonged to the Finnish PUUV lineage. Our findings suggest an introduction of PUUV from Finland or Karelia, causing the human PUUV infections in Scania. This discovery emphasizes the need to understand the evolution, cross-species transmission, and disease outcomes of this newly found PUUV variant.

Limits to sustained energy intake. XXXIV. Can the heat dissipation limit (HDL) theory explain reproductive aging?

According to the heat dissipation limit (HDL) theory, reproductive performance is limited by the capacity to dissipate excess heat. We tested the novel hypotheses that (1) the age-related decline in reproductive performance is due to an age-related decrease of heat dissipation capacity and (2) the limiting mechanism is more severe in animals with high metabolic rates. We used bank voles (Myodes glareolus) from lines selected for high swim-induced aerobic metabolic rate, which have also increased basal metabolic rate, and unselected control lines. Adult females from three age classes - young (4 months), middle-aged (9 months) and old (16 months) - were maintained at room temperature (20°C), and half of the lactating females were shaved to increase heat dissipation capacity. Old females from both selection lines had a decreased litter size, mass and growth rate. The peak-lactation average daily metabolic rate was higher in shaved than in unshaved mothers, and this difference was more profound among old than young and middle-aged voles (P=0.02). In females with large litters, milk production tended to be higher in shaved (least squares mean, LSM±s.e.: 73.0±4.74 kJ day-1) than in unshaved voles (61.8±4.78 kJ day-1; P=0.05), but there was no significan"t effect of fur removal on the growth rate [4.47±2.29 g (4 days-1); P=0.45]. The results provide mixed support of the HDL theory and no support for the hypotheses linking the differences in reproductive aging with either a deterioration in thermoregulatory capability or genetically based differences in metabolic rate.

Experimental manipulation of food availability and macroparasite prevalence reveal differential effects on space use in wild rodents.

Research Highlight: Mistrick, J., Veitch, J. S. M., Kitchen, S. M., Clague, S., Newman, B. C., Hall, R. J., Budischak, S. A., Forbes, K. M., & Craft, M. E. (2024). Effects of food supplementation and helminth removal on space use and spatial overlap in wild rodent populations. Journal of Animal Ecology. http://doi.org/10.1111/1365-2656.14067. The spread of pathogens has been of long-standing interest, even before dramatic outbreaks of avian influenza and the coronavirus pandemic spiked broad public interest. However, the dynamics of pathogen spread in wild populations are complex, with multiple effects shaping where animals go (their space use), population density and, more fundamentally, the resultant patterns of contacts (direct or indirect) among individuals. Thus, experimental studies exploring the dynamics of contact under different sets of conditions are needed. In the current field study, Mistrick et al. (2024) used a multifactorial experimental design, manipulating food availability and individual pathogen infection state in wild bank voles (Clethrionomys glareolus). They found that while food availability, individual traits and seasonality can affect how far individual voles moved, the degree of overlap between individual voles remained largely the same despite a high variation in population density-which itself was affected by food availability. These results highlight how biotic and abiotic factors can shape patterns of space use and balance the level of spatial overlap through multiple pathways.

Evolutionary Formation and Distribution of Puumala Virus Genome Variants, Russia.

We analyzed Puumala virus (PUUV) sequences collected from bank voles from different regions of Russia. Phylogenetic analysis revealed PUUV reassortments in areas with the highest hemorrhagic fever with renal syndrome incidence, indicating reassortment might contribute to pathogenic properties of PUUV. Continued surveillance is needed to assess PUUV pathogenicity in Russia.

Zoonotic Virus Seroprevalence among Bank Voles, Poland, 2002-2010.

Bank voles in Poland are reservoirs of zoonotic viruses. To determine seroprevalence of hantavirus, arenavirus, and cowpox virus and factors affecting seroprevalence, we screened for antibodies against these viruses over 9 years. Cowpox virus was most prevalent and affected by extrinsic and intrinsic factors. Long-term and multisite surveillance is crucial.

Variable Protease-Sensitive Prionopathy Transmission to Bank Voles.

Variably protease-sensitive prionopathy (VPSPr), a recently described human sporadic prion disease, features a protease-resistant, disease-related prion protein (resPrPD) displaying 5 fragments reminiscent of Gerstmann-Sträussler-Scheinker disease. Experimental VPSPr transmission to human PrP-expressing transgenic mice, although replication of the VPSPr resPrPD profile succeeded, has been incomplete because of second passage failure. We bioassayed VPSPr in bank voles, which are susceptible to human prion strains. Transmission was complete; first-passage attack rates were 5%-35%, and second-passage rates reached 100% and survival times were 50% shorter. We observed 3 distinct phenotypes and resPrPD profiles; 2 imitated sporadic Creutzfeldt-Jakob disease resPrPD, and 1 resembled Gerstmann-Sträussler-Scheinker disease resPrPD. The first 2 phenotypes may be related to the presence of minor PrPD components in VPSPr. Full VPSPr transmission confirms permissiveness of bank voles to human prions and suggests that bank vole PrP may efficiently reveal an underrepresented native strain but does not replicate the complex VPSPr PrPD profile.

Puumala Virus in Bank Voles, Lithuania.

Little is known about the presence of human pathogenic Puumala virus (PUUV) in Lithuania. We detected this virus in bank voles (Myodes glareolus) in a region of this country in which previously PUUV-seropositive humans were identified. Our results are consistent with heterogeneous distributions of PUUV in other countries in Europe.

Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland.

Parasites are considered to be an important selective force in host evolution but ecological studies of host-parasite systems are usually short-term providing only snap-shots of what may be dynamic systems. We have conducted four surveys of helminths of bank voles at three ecologically similar woodland sites in NE Poland, spaced over a period of 11 years, to assess the relative importance of temporal and spatial effects on helminth infracommunities. Some measures of infracommunity structure maintained relative stability: the rank order of prevalence and abundance of Heligmosomum mixtum, Heligmosomoides glareoli and Mastophorus muris changed little between the four surveys. Other measures changed markedly: dynamic changes were evident in Syphacia petrusewiczi which declined to local extinction, while the capillariid Aonchotheca annulosa first appeared in 2002 and then increased in prevalence and abundance over the remaining three surveys. Some species are therefore dynamic and both introductions and extinctions can be expected in ecological time. At higher taxonomic levels and for derived measures, year and host-age effects and their interactions with site are important. Our surveys emphasize that the site of capture is the major determinant of the species contributing to helminth community structure, providing some predictability in these systems.

Bank voles (Myodes glareolus) and house mice (Mus musculus musculus; M. m. domesticus) in Europe are each parasitized by their own distinct species of Aspiculuris (Nematoda, Oxyurida).

The molecular phylogeny and morphology of the oxyuroid nematode genus Aspiculuris from voles and house mice has been examined. Worms collected from Myodes glareolus in Poland, Eire and the UK are identified as Aspiculuris tianjinensis, previously known only from China, while worms from Mus musculus from a range of locations in Europe and from laboratory mice, all conformed to the description of Aspiculuris tetraptera. Worms from voles and house mice are not closely related and are not derived from each other, with A. tianjinensis being most closely related to Aspiculuris dinniki from snow voles and to an isolate from Microtus longicaudus in the Nearctic. Both A. tianjinensis and A. tetraptera appear to represent recent radiations within their host groups; in voles, this radiation cannot be more than 2 million years old, while in commensal house mice it is likely to be less than 10,000 years old. The potential of Aspiculuris spp. as markers of host evolution is highlighted.

Interrelation of the spatial and genetic structure of tick-borne encephalitis virus, its reservoir host (Myodes glareolus), and its vector (Ixodes ricinus) in a natural focus area.

Tick-borne encephalitis (TBE) virus is considered the medically most important arthropod-borne virus in Europe. Although TBE is endemic throughout central Europe, ticks and rodents determine its maintenance in small, difficult-to-assess, natural foci. We investigated the interrelation between the population genetics of the main TBE virus (TBEV) vector tick (Ixodes ricinus), the most important reservoir host (Myodes glareolus, syn. Clethrionomys glareolus), and TBEV. Rodents and ticks were sampled on 15 sites within an exploratory study area, which has been screened regularly for TBEV occurrence in ticks for more than 10 years. On all 15 sites, ticks and bank voles were sampled, screened for TBEV presence via serology and RT-PCR, and genetically examined. Moreover, TBEV isolates derived from these analyses were sequenced. In long-term TBEV foci bank vole populations show extraordinary genetic constitutions, leading to a particular population structure, whereas ticks revealed a panmictic genetic structure overall sampling sites. Landscape genetics and habitat connectivity modeling (analysis of isolation by resistance) showed no landscape-related barriers explaining the genetic structure of the bank vole populations. The results suggest that bank voles do not simply serve as TBEV reservoirs, but their genetic composition appears to have a significant influence on establishing and maintaining long-term natural TBEV foci, whereas the genetic structure of TBEV's main vector I. ricinus does not play an important role in the sustainability of long-term TBEV foci. A thorough investigation of how and to which extent TBEV and M. glareolus genetics are associated is needed to further unravel the underlying mechanisms.

Balancing selection on the complement system of a wild rodent.

BACKGROUND: Selection pressure exerted by pathogens can influence patterns of genetic diversity in the host. In the immune system especially, numerous genes encode proteins involved in antagonistic interactions with pathogens, paving the way for coevolution that results in increased genetic diversity as a consequence of balancing selection. The complement system is a key component of innate immunity. Many complement proteins interact directly with pathogens, either by recognising pathogen molecules for complement activation, or by serving as targets of pathogen immune evasion mechanisms. Complement genes can therefore be expected to be important targets of pathogen-mediated balancing selection, but analyses of such selection on this part of the immune system have been limited. RESULTS: Using a population sample of whole-genome resequencing data from wild bank voles (n = 31), we estimated the extent of genetic diversity and tested for signatures of balancing selection in multiple complement genes (n = 44). Complement genes showed higher values of standardised ß (a statistic expected to be high under balancing selection) than the genome-wide average of protein coding genes. One complement gene, FCNA, a pattern recognition molecule that interacts directly with pathogens, was found to have a signature of balancing selection, as indicated by the Hudson-Kreitman-Aguadé test (HKA) test. Scans for localised signatures of balancing selection in this gene indicated that the target of balancing selection was found in exonic regions involved in ligand binding. CONCLUSION: The present study adds to the growing evidence that balancing selection may be an important evolutionary force on components of the innate immune system. The identified target in the complement system typifies the expectation that balancing selection acts on genes encoding proteins involved in direct interactions with pathogens.

Discovery of a Novel Coronavirus in Swedish Bank Voles (Myodes glareolus).

The unprecedented pandemic COVID-19, caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), with bats as original reservoirs, has once again highlighted the importance of exploring the interface of wildlife diseases and human health. In this study, we identified a novel Betacoronavirus from bank voles (Myodes glareolus) in Grimsö, Sweden, and this virus is designated as Grimso virus. Repeated detection over three years and an overall prevalence of 3.4% suggest that the virus commonly occurs in bank voles. Furthermore, phylogenetic analyses indicate that the Grimso virus belongs to a highly divergent Embecovirus lineage predominantly associated with bank voles. Given that bank voles are one of the most common rodent species in Sweden and Europe, our findings indicate that Grimso virus might be circulating widely in bank voles and further point out the importance of sentinel surveillance of coronaviruses in wild small mammalian animals, especially in wild rodents.

Seroprevalence and incidence of Puumala orthohantavirus in its bank vole (Myodes glareolus) host population in northeastern France: Between-site and seasonal variability.

Given the difficulty of measuring pathogen transmission in wildlife, epidemiological studies frequently rely on cross-sectional seroprevalence. However, seropositivity indicates only exposure to a pathogen at an unknown time. By allowing to obtain repeated test results from individuals sampled multiple times over an extended period, longitudinal data help reduce this uncertainty. We used capture-mark-recapture data on bank vole (Myodes glareolus) individuals collected at four sites over ten years in northeastern France to investigate the impact of environmental variables on seroprevalence and incidence of Puumala orthohantavirus (PUUV). PUUV causes a chronic infection without apparent symptoms, that may however impair survival of its rodent host in the wild. Viral transmission between rodents may occur through direct contact or via the environment. Principal component analysis was used to deal with multicollinearity among environmental variables. Incidence and seroprevalence were investigated with either generalized estimating equations or Poisson regression models depending on the number of observations for each season. In spring, only the factor site was found to be significant for seroprevalence, while a principal component including meteorological conditions of the previous winter and the normalized difference vegetation index (NDVI) of both the previous winter and spring had a significant effect on incidence. In autumn, only the factor site was significant for incidence, while two principal components, including either the meteorological conditions of the autumn and previous spring or NDVI of the autumn significantly affected seroprevalence. We discuss these results in light of the particular demography of small mammals. We encourage other researchers to investigate the relationships between demographic parameters of wild host populations and the environment, by using both incidence and seroprevalence.

Seroprevalence of Trichinella spp. infection in bank voles (Myodes glareolus) - A long term study.

Rodents play an important role as reservoir hosts of zoonotic diseases. As a component of our long-term programme of monitoring parasitic infections in bank vole populations in three ecologically similar sites in NE Poland, we screened blood samples for signs of a serological response to the presence of Trichinella spp. The overall seroprevalence of Trichinella spp. was 1.52%, but prevalence was largely concentrated in one of our three study sites and confined to the oldest individuals in the study. Seroprevalence of Trichinella spp. did not differ between the sexes. Although a local prevalence of 1.52% may seem low, when this is extrapolated to the national population of bank voles in peak years, perhaps numbering hundreds of millions of animals, the number of infected bank voles on a country wide scale is likely to be huge. Our results suggest that bank voles may be reservoirs of Trichinella spp. However, on the basis of our results we consider their importance as epidemiologically significant hosts for Trichinella spp. to be moderate and their role in this context to require further investigation.

The effect of chlorpyrifos on thermogenic capacity of bank voles selected for increased aerobic exercise metabolism.

Agro-chemicals potentially cause adverse effects in non-target organisms. The rate of animal energy metabolism can influence their susceptibility to pesticides by influencing food consumption, biotransformation and elimination rates of toxicants. We used experimental evolution to study the effects of inherent differences in energy metabolism rate and exposure to the organophosphate insecticide, chlorpyrifos (CPF) on thermogenic capacity in a wild rodent, the bank vole (Myodes = Clethrionomys glareolus). The voles were sampled from four replicate lines selected for high swim-induced aerobic metabolism (A) and four unselected control (C) lines. Thermogenic capacity, measured as the maximum cold-induced rate of oxygen consumption (VO2cold), was higher in the A - than C lines, and it decreased after continuous exposure to CPF via food or after a single dose administered via oral gavage, but only when measured shortly after exposure. VO2cold measured 24 h after repeated exposure was not affected. In addition, gavage with a single dose led to decreased food consumption and loss in body mass. Importantly, the adverse effects of CPF did not differ between the selected and control lines. Therefore, exposure to CPF has adverse effects on thermoregulatory performance and energy balance in this species. The effects are short-lived and their magnitude is not associated with the inherent level of energy metabolism. Even without severe symptoms of poisoning, fitness can be compromised under harsh environmental conditions, such as cold and wet weather.

Temporal trends in the levels of polychlorinated dioxins, -furans, -biphenyls and polybrominated diethyl ethers in bank voles in Northern Finland.

Dioxin-like chemicals and brominated flame retardants are ubiquitous in the environment, despite the introduction of international prohibitions and restrictions. These chemicals do not remain in the vicinity of their source, instead they can be transported over long distances, in fact even to pristine areas in the northern latitudes. However, there have been rather few time series experiments monitoring the trends in the levels of chlorinated and brominated forms of these chemicals in the environment. In this study, the concentrations of polychlorinated dibenzo-p-dioxins and -furans (PCDDs/Fs), polychlorinated biphenyls (PCBs) and polybrominated diethyl ethers (PBDEs) were measured in the liver and muscle of bank voles (Myodes glareolus) caught in a remote area in Finnish Lapland during 1986-2007. Five time points were selected: years 1986, 1992, 1998, 2003 and 2007. The levels of PCDDs/Fs and PCBs declined from 1986 until 2003 in both females and males, but tended to increase again in 2007. The peak levels of the most abundant PBDE congeners (PBDEs 47, 99, 100 and 153) were measured in 1998 and 2003. These results reveal that the levels of dioxin-like chemicals remain high also in rural areas in Lapland, whereas the concentrations of brominated flame retardants decreased and follow the current restriction prohibitions.

First report of Anaplasma phagocytophilum and Babesia microti in rodents in Finland.

Tick-borne diseases pose an increasingly important public health problem in Europe. Rodents are the reservoir host for many tick-transmitted pathogens, including Anaplasma phagocytophilum and Babesia microti, which can cause human granulocytic anaplasmosis and babesiosis, respectively. To estimate the presence of these pathogens in rodents in Finland, we examined blood samples from 151 bank voles (Myodes glareolus) and demonstrate, for the first time, that A. phagocytophilum and B. microti commonly infect bank voles (in 22% and 40% of animals, respectively) in Finland. Sequence analysis of a fragment of 18S rRNA showed that the B. microti strain isolated was identical to the Munich strain, which is considered to be nonzoonotic. The A. phagocytophilum strain (based on a fragment of the msp4 gene) was identical to one found earlier in rodents in the United Kingdom that is transmitted by the tick Ixodes trianguliceps, all the life stages of which feed on small mammals. The infection probability of B. microti in the bank voles was the greater the older the individual was, and males were more often infected than females. A. phagocytophilum infection probability first increased and then decreased with the age of individual without any difference between sexes. While these pathogens presumably pose a limited zoonotic risk to humans in Finland, they might have important interactions with other rodent pathogens and therefore affect infection dynamics of, for example, zoonotic pathogens.

Model-based prediction of nephropathia epidemica outbreaks based on climatological and vegetation data and bank vole population dynamics.

Wildlife-originated zoonotic diseases in general are a major contributor to emerging infectious diseases. Hantaviruses more specifically cause thousands of human disease cases annually worldwide, while understanding and predicting human hantavirus epidemics pose numerous unsolved challenges. Nephropathia epidemica (NE) is a human infection caused by Puumala virus, which is naturally carried and shed by bank voles (Myodes glareolus). The objective of this study was to develop a method that allows model-based predicting 3 months ahead of the occurrence of NE epidemics. Two data sets were utilized to develop and test the models. These data sets were concerned with NE cases in Finland and Belgium. In this study, we selected the most relevant inputs from all the available data for use in a dynamic linear regression (DLR) model. The number of NE cases in Finland were modelled using data from 1996 to 2008. The NE cases were predicted based on the time series data of average monthly air temperature (°C) and bank voles' trapping index using a DLR model. The bank voles' trapping index data were interpolated using a related dynamic harmonic regression model (DHR). Here, the DLR and DHR models used time-varying parameters. Both the DHR and DLR models were based on a unified state-space estimation framework. For the Belgium case, no time series of the bank voles' population dynamics were available. Several studies, however, have suggested that the population of bank voles is related to the variation in seed production of beech and oak trees in Northern Europe. Therefore, the NE occurrence pattern in Belgium was predicted based on a DLR model by using remotely sensed phenology parameters of broad-leaved forests, together with the oak and beech seed categories and average monthly air temperature (°C) using data from 2001 to 2009. Our results suggest that even without any knowledge about hantavirus dynamics in the host population, the time variation in NE outbreaks in Finland could be predicted 3 months ahead with a 34% mean relative prediction error (MRPE). This took into account solely the population dynamics of the carrier species (bank voles). The time series analysis also revealed that climate change, as represented by the vegetation index, changes in forest phenology derived from satellite images and directly measured air temperature, may affect the mechanics of NE transmission. NE outbreaks in Belgium were predicted 3 months ahead with a 40% MRPE, based only on the climatological and vegetation data, in this case, without any knowledge of the bank vole's population dynamics. In this research, we demonstrated that NE outbreaks can be predicted using climate and vegetation data or the bank vole's population dynamics, by using dynamic data-based models with time-varying parameters. Such a predictive modelling approach might be used as a step towards the development of new tools for the prevention of future NE outbreaks.