Reservoir‐Driven Heterogeneous Distribution of Recorded Human Puumala virus Cases in South‐West Germany

Endemic regions for Puumala virus (PUUV) are located in the most affected federal state Baden‐Wuerttemberg, South‐West Germany, where high numbers of notified human hantavirus disease cases have been occurring for a long time. The distribution of human cases in Baden‐Wuerttemberg is, however, heterogeneous, with a high number of cases recorded during 2012 in four districts (H districts) but a low number or even no cases recorded in four other districts (L districts). Bank vole monitoring during 2012, following a beech (Fagus sylvatica) mast year, resulted in the trapping of 499 bank voles, the host of PUUV. Analyses indicated PUUV prevalences of 7–50% (serological) and 1.8–27.5% (molecular) in seven of eight districts, but an absence of PUUV in one L district. The PUUV prevalence differed significantly between bank voles in H and L districts. In the following year 2013, 161 bank voles were trapped, with reduced bank vole abundance in almost all investigated districts except one. In 2013, no PUUV infections were detected in voles from seven of eight districts. In conclusion, the linear modelling approach indicated that the heterogeneous distribution of human PUUV cases in South‐West Germany was caused by different factors including the abundance of PUUV RNA‐positive bank voles, as well as by the interaction of beech mast and the proportional coverage of beech and oak (Quercus spec.) forest per district. These results can aid developing local public health risk management measures and early warning models.     

Environmental conditions in favour of a hantavirus outbreak in 2015 in Germany?

Bank voles can harbour Puumala virus (PUUV) and vole populations usually peak in years after beech mast. A beech mast occurred in 2014 and a predictive model indicates high vole abundance in 2015. This pattern is similar to the years 2009/2011 when beech mast occurred, bank voles multiplied and human PUUV infections increased a year later. Given similar environmental conditions in 2014/2015, increased risk of human PUUV infections in 2015 is likely. Risk management measures are recommended.     

Different cross-reactivity of human and rodent sera to Tula virus and Puumala virus

Tula virus (TULV) and Puumala virus (PUUV) are hantaviruses carried by the bank vole (Myodes glareolus) and European common vole (Microtus arvalis), respectively. PUUV is a causative agent of hemorrhagic fever with renal syndrome (HFRS), while TULV is thought to be apathogenic to humans. The N-terminal regions of the N proteins from TULV and PUUV were expressed and applied as enzyme-linked immunosorbent assay (ELISA) antigens. Colonized Japanese grass voles (Microtus montebelli) and BALB/c mice were used for experimental inoculation of the vole-borne hantaviruses TULV and PUUV. Voles and mice showed significant antibody production toward both viruses, but these antisera showed little cross-reactivity between TULV and PUUV in the immunofluorescence antibody assay and ELISA. In contrast, sera from patients with HFRS caused by PUUV exhibited high cross-reactivity against the TULV antigen, and sera from a natural rodent reservoir showed moderate cross-reactivity against the heterologous antigen, indicating that the antigenic cross-reactivity between TULV and PUUV differs in sera from rodents and humans.     

Diet shift in bank voles induced by competition from grey‐sided voles?

Grey‐sided voles (Myodes rufocanus) and bank voles (Myodes glareolus) co‐exist in boreal forests in northern Scandinavia. Previous studies suggest that the 2 species interact interspecifically, the grey‐sided vole being the dominant species. We tested the hypothesis that bank voles shift their diet due to competition with the dominant grey‐sided vole by studying stable isotope ratios in both species. Muscle samples were taken from voles in patches of old forest occupied by only bank voles and patches of old forest occupied by both grey‐sided voles and bank voles. We found that: (i) stable isotope ratios of bank voles differed in areas with and without grey‐sided voles; and that (ii) the stable isotope ratios of bank voles were more similar to those of grey‐sided voles in areas where grey‐sided voles were absent. Our data suggests that grey‐sided voles forced bank voles to change their diet due to interspecific competition.     

Disease patterns in field and bank vole populations during a cyclic decline in central Finland

Declining field vole (Microtus agrestis) and bank vole (Clethrionomys glareolus) populations were sampled (117 field voles and 34 bank voles) in south-central Finland during the winter of 1988-89. The last surviving field voles were caught in April and bank voles in February. A subsample (16) of the April field voles were taken live to the laboratory for immunosuppression. The histopathology of the main internal organs and the presence of aerobic bacteria and certain parasites were studied. In the lungs, an increase in lymphoid tissue, probably caused by infections, was the most common finding (52% of all individuals). The prevalences in the voles, in the whole material, of Chrysosporium sp. and Pneumocystis carinii in lungs were 13 and 10% in field voles, and 9 and 0% in bank voles, respectively. Cysts of Taenia mustelae (9 and 27%) were the most common pathological changes in the liver. Enteritis was also rather common (14 and 34%). In field voles the prevalences of Frenkelia sp. in the brain and Sarcocystis sp. in leg muscles were low (both 6%). Bordetella bronchiseptica was commonly (31%) isolated from field vole lungs and Listeria monocytogenes from the intestines (34%). Salmonella spp. could not be found. The dynamics and abundance of inflammations in the lungs and intestines, as well as B. bronchiseptica isolations from the lungs, indicate that obvious epidemics took place in declining vole populations. Of the Luhanka subsample of 16 field voles brought to the laboratory in April, one died of listeriosis, two of Bordetella, and five died for unknown reasons. Even if small mustelids are the driving force in microtine cycles, it is possible that diseases also contribute to the decline.     

Effect of ENSO-driven precipitation on population irruptions of the Yangtze vole Microtus fortis calamorum in the Dongting Lake region of China

The Yangtze vole (Microtus fortis Buechner, 1889) is a small herbivore species that inhabits lake beaches in the Dongting Lake region along the Yangtze River in Southern China. Its population shows strong oscillations during the wet season due to summer precipitation-induced immigration away from the lake into adjacent rice fields. The effect of El Niño-Southern Oscillation-driven precipitation on population abundance and growth of the vole species is not fully understood. We undertook an analysis of the combined data of 4 time series covering 1981–2006 from 4 different sites and a separate analysis on a single time series (1981–2006) from one site. Our results demonstrate that a dual effect of El Niño-Southern Oscillation-driven precipitation on the population abundance of voles is time-dependent: precipitation in the current year has a positive effect, whereas precipitation in the previous year has a negative effect. The dual effect of precipitation on vole population is well explained by the unique interactions among vole population, precipitation water level and the lake beach habitat around Dongting Lake. We found that drier than average weather of the previous year benefited voles because their breeding habitats, lake beaches, were exposed for long stretches of time. Wet weather was found to increase the number of voles inhabiting rice fields because as the water level of the lake rose they were forced from beaches into surrounding rice fields. Summer precipitation in the Dongting Lake region was found to be positively associated with the sea surface temperature (SST) of the eastern tropical Pacific Ocean of the previous year and winter SST and spring SST of the current year. Annual rates of increase in the vole population of the reconstructed time series are negatively associated with the vole abundance and autumn precipitation of the previous year and winter precipitation of the current years. These results suggest that both extrinsic and density-dependent intrinsic factors may affect population dynamics of the Yangtze voles.     

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.     

Puumala Virus Outbreak in Western Thuringia,Germany, 2010: Epidemiology and Strain Identification

In 2010, the highest annual number of human Puumala virus (PUUV) infections was reported in Germany since hantavirus surveillance started in 2001. The increase in annual case numbers was especially marked in western Thuringia. We combined results of case‐based hantavirus surveillance in humans and serological and molecular investigations in the rodent reservoir to describe the epidemiological situation and to identify the putative outbreak strain. A 5‐fold increase in notified hantavirus cases compared to the previous annual maximum was observed in western Thuringia in 2010. Disease incidence varied tremendously within a small geographical area with case patients' places of residence clustering around beech‐dominated broad leaf forest patches. Investigations in the rodent reservoir revealed a novel Puumala virus (PUUV) subtype, which is clearly distinct from strains collected in other PUUV endemic regions of Germany. It can be assumed that in regions in western Thuringia where hantavirus cases occurred in 2010 or previous outbreak years, PUUV has been present in the environment for a long time. Further studies are needed to elucidate the population dynamics and hantavirus prevalence of the rodent reservoir and driving ecological factors.     

Susceptibility to and transmission of H5N1 and H7N1 highly pathogenic avian influenza viruses in bank voles (Myodes glareolus)

The study of influenza type A (IA) infections in wild mammals populations is a critical gap in our knowledge of how IA viruses evolve in novel hosts that could be in close contact with avian reservoir species and other wild animals. The aim of this study was to evaluate the susceptibility to infection, the nasal shedding and the transmissibility of the H7N1 and H5N1 highly pathogenic avian influenza (HPAI) viruses in the bank vole (Myodes glareolus), a wild rodent common throughout Europe and Asia. Two out of 24 H5N1-infected voles displayed evident respiratory distress, while H7N1-infected voles remained asymptomatic. Viable virus was isolated from nasal washes collected from animals infected with both HPAI viruses, and extra-pulmonary infection was confirmed in both experimental groups. Histopathological lesions were evident in the respiratory tract of infected animals, although immunohistochemistry positivity was only detected in lungs and trachea of two H7N1-infected voles. Both HPAI viruses were transmitted by direct contact, and seroconversion was confirmed in 50% and 12.5% of the asymptomatic sentinels in the H7N1 and H5N1 groups, respectively. Interestingly, viable virus was isolated from lungs and nasal washes collected from contact sentinels of both groups. The present study demonstrated that two non-rodent adapted HPAI viruses caused asymptomatic infection in bank voles, which shed high amounts of the viruses and were able to infect contact voles. Further investigations are needed to determine whether bank voles could be involved as silent hosts in the transmission of HPAI viruses to other mammals and domestic poultry.     

Voles and weasels in the boreal Fennoscandian small mammal community: what happens if the least weasel disappears due to climate change?

Climate change, habitat loss and fragmentation are major threats for populations and a challenge for individual behavior, interactions and survival. Predator–prey interactions are modified by climate processes. In the northern latitudes, strong seasonality is changing and the main predicted feature is shortening and instability of winter. Vole populations in the boreal Fennoscandia exhibit multiannual cycles. High amplitude peak numbers of voles and dramatic population lows alternate in 3–5‐year cycles shortening from North to South. One key factor, or driver, promoting the population crash and causing extreme extended lows, is suggested to be predation by the least weasel. We review the arms race between prey voles and weasels through the multiannual density fluctuation, affected by climate change, and especially the changes in the duration and stability of snow cover. For ground‐dwelling small mammals, snow provides thermoregulation and shelter for nest sites, and helps them hide from predators. Predicted increases in the instability of winter forms a major challenge for species with coat color change between brown summer camouflage and white winter coat. One of these is the least weasel, Mustela nivalis nivalis. Increased vulnerability of wrong‐colored weasels to predation affects vole populations and may have dramatic effects on vole dynamics. It may have cascading effects on other small rodent–predator interactions and even on plant–animal interactions and forest dynamics.     

Time series analysis performed on nephropathia epidemica in humans of northern Sweden in relation to bank vole population dynamic and the NAO index

Time series analysis was performed on two data series of human nephropathia epidemica (NE) infections in northern Sweden between the years 1959-1975 and 1985-2006. The analysis confirms that the bank vole (Myodes glareolus), the main reservoir species, shows regular peaks in population density approximately every fourth year. The periodicity in NE cases of the more recent time period (1985-2006) is 2.8-3.3 years and the older period shows a periodicity ranging 3.4-4.2 years, but this is not significantly different from that expected by vole dynamics. A comparison of North Atlantic Oscillation (NAO) index between the two periods reveals higher mean winter NAO index in the period 1985-2006 than in 1959-1975. No difference was found in frequency of the NAO index between the older period (2.8-3.4 years) compared with the recent period (2.4-2.8 years). Cross-correlation revealed a delayed effect by NAO index on vole abundance but a multivariate model showed that NAO index did not explain the variation in NE cases. Vole index was the only factor that contributed significantly to the variation in numbers of NE cases and that no climate effect could be detected. The climate signal from NAO index does not appear to significantly affect the human NE cases and this suggests that the transmission of disease to man is not particularly sensitive to variations in weather factors. The results favour the hypothesis that higher NAO index will not increase the likelihood of virus transmission from voles to man in northern Sweden under present climatic conditions.     

Kinship analysis reveals reproductive success skewed toward overwintered Brandt's voles in semi‐natural enclosures

Age structure and seasonality influence the population fluctuations of small rodents. Age determines body weight and social experience, while seasonality regulates the duration of the breeding season and onset of sexual maturity in newborn offspring. Therefore, reproductive success and skew usually occur in different age groups. Brandt's vole (Lasiopodomys brandtii) is a social, short‐lived and seasonal breeding small rodent with a dramatic seasonal population fluctuation, but reproductive skew is not fully understood in this species. In the present study, we determined kinship in semi‐natural enclosure populations using microsatellite markers based on genotyping, analyzed the reproductive skew between sexes and between overwintered and newborn voles, and monitored variation in male reproductive activity by testing fecal testosterone levels throughout the year. Overwintered voles had the most reproductive success along with a striking increase in the population size in the enclosures, with all biological fathers and 77.8% of biological mothers, which had 100% and 87% of the total offspring, respectively. Compared to overwintered voles, reproductive skews were significantly higher in potential overwintered and newborn parents, implying the possible reproductive suppression of newborn voles by dominant overwintered voles. Moreover, both heavier body weight and higher testosterone levels in overwintered males supported their potential social status in the population. Our study provided new evidence for reproductive skew and differentiation of postnatal gonadal development patterns of different age groups in Brandt's vole.     

Development of transferred xenogeneic vole embryos in mouse uteri

An experimental model to study interspecific pregnancy using voles, Microtus arvalis, and green fluorescent protein gene‐induced transgenic mice is presented. Xenogeneic blastocysts from the vole were transferred into the uteri of pseudopregnant mice along with allogeneic blastocysts from green fluorescent protein gene‐induced transgenic mice. The uteri containing xeno‐allo combined transfers were examined from day 6 to 13 of gestation. Although the vole embryos implanted, the uteri containing vole embryos were smaller compared with those having allogeneic mouse embryos. On day 8, the uteri containing vole embryos hemorrhaged internally and no vole embryo was found in the pregnant uterus after day 11. Allogeneic mouse embryos developed normally despite the presence and abortion of the vole embryos. In uteri implanted with vole embryos, decidua were formed and numerous blood vessels were distributed around the embryo. Maternal blood cells infiltrated into the celomic cavity of the vole embryo through the discontinuous region of trophoblast. Periodic acid‐Schiff‐positive granulated metrial gland cells were remarkably increased in the decidual sites. These findings suggest that a disorder of embryo–maternal interaction might induce the appearance of numerous granulated metrial gland cells and rejection of the embryos.     

模拟条件下布氏田鼠对草原植被的作用1——植被生物量的影响

2007年5-10月在模拟条件下研究了不同密度的布氏田鼠Lasiopodomys brandtii啃食对草原植被生物量、植物补偿生长量的影响。结果表明:1）植被生物量与布氏田鼠密度关系呈现了“低-高-低”的变化趋势;鼠密度每100 m2<5只时,植被生物量呈增加趋势。鼠密度每100 m2为5只时,其植被生物量增长达到最高值,随鼠密度的增加,植被生物量下降。2）植物补偿生长量与布氏田鼠密度相关呈单峰型曲线,鼠密度每100 m2为8只时植被的补偿生长量最高。3）植被生长可承受的鼠密度每100 m2 为4只(折合400只/hm2),鼠密度每100 m2≤4只时刺激植物生长,且可稳定植被群落结构。     

采用布氏田鼠建立动物流感病毒感染模型的试验研究

应用流感病毒A/WSN/33(H1N1),通过人工滴鼻接种的方式感染布氏田鼠,评估其对流感病毒的易感性,并在其易感性较强的基础上,进一步对建立流感病毒感染布氏田鼠疾病动物模型的可能性及其评价指标进行研究。通过对感染的布氏田鼠进行体内病毒分离及鉴定等方法,成功分离到了流感病毒,证实了流感病毒在布氏田鼠组织中的存在。试验结果表明,流感病毒对布氏田鼠具有很强的感染性,其主要侵害的靶器官为肺脏。综合感染布氏田鼠的临床症状及病理变化、体质量变化、死亡率、流感病毒的分离及鉴定等指标,表明成功建立了流感病毒感染布氏田鼠的疾病动物模型。     

Filling the gaps in the Argentinian distribution of orthohantavirus: First finding of Lechiguanas virus in rodents from Corrientes,Argentina

Hantavirus Pulmonary Syndrome (HPS) is an emerging infectious disease caused by orthohantaviruses in the Americas. In Argentina, since 1995, several reservoirs and virus variants have been described, but the northeastern and central endemic zones in the country include an area without human or rodent infections, despite sharing rodent species with areas with that disease. The aim of this study was to search for orthohantavirus in rodent communities that inhabit this area, which borders two endemic areas of HPS. Small rodents were captured in June of 2022 through a total effort of 644 trap nights distributed in five grids located in the Iberá National Park, Corrientes, Northeastern Argentina. All rodents were sexed, weighed, and the species was recorded. Blood samples were extracted to detect ANDV-specific immunoglobulin G (IgG), and to extract the RNA virus. Trimmed sequences were mapped against reference sequences from GenBank. We captured a total of 36 Oligoryzomys flavescens and 15 Oxymycterus rufus. We detected the O. flavescens species infected with Lechiguanas orthohantavirus in the camping area of the National Park. A nucleotide comparison with previously published sequences shows a 98.34% similarity to the virus obtained from a human case of HPS reported in the adjacent Misiones province. This study demonstrated, for the first time, that O. flavescens is a host of the Lechiguanas orthohantavirus in this zone and contributes to closing information gaps on the distribution of orthohantavirus in Argentina. Additionally, the high similarity with the hantavirus found in the human case of Misiones suggests that the reservoir in that province would also be O. flavescens (not previously confirmed). This information permits us to focus on the preventive measurements to protect the human population.     

Yellow-necked mice (Apodemus flavicollis) and bank voles (Myodes glareolus) as zoomonitors of environmental contamination at a polluted area in Slovakia

Background

Free-living wild rodents are often used as zoomonitors of environmental contamination. In the present study, accumulation of cadmium (Cd), copper (Cu), iron (Fe), and zinc (Zn) in critical organs of yellow-necked mice (Apodemus flavicollis) and bank voles (Myodes glareolus) trapped in a polluted area in Nováky, Slovakia was investigated.

Methods

Yellow-necked mice (n = 8) and bank voles (n = 10) were collected using standard theriological methods for wood ecosystems. All animals were adult males in good physical condition. The concentrations of Cd, Cu, Fe, and Zn in the liver, kidney, and bone were determined by atomic absorption spectrophotometry.

Results

The highest concentrations of Cd and Zn were found in the bone of both species while Cu and Fe accumulated mainly in kidney or liver. Significant higher concentrations of Cd and Cu were detected in the liver of bank voles than in yellow-necked mice. Similar significant higher levels of Cd and Zn were found in the bone of bank voles. In contrast, significant higher concentrations of Cu and Fe were present in the kidney of yellow-necked mice.

Conclusions

In the yellow-necked mouse and bank vole, bone seems to accumulate Cd and Zn following prolonged exposure. On the contrary, kidney and liver store Cu and Fe after a long-term environmental exposure. In the present study, bank voles seemed to be more heavy metal loaded zoomonitors than yellow-necked mice.     

Hepatitis E Virus of Subtype 3a in a Pig Farm,South‐Eastern France

Hepatitis E virus (HEV) has emerged during the past decade as a causative agent of autochthonous hepatitis and is a clinical concern in Western developed countries. It has been increasingly recognized that pigs are a major reservoir of HEV of genotypes 3 and 4 worldwide and pig‐derived food items represent a potential source of infections by these viruses in humans. Hepatitis E virus RNA testing was performed here on faeces from rectal swabs sampled in 2012 from 50 3‐month‐old farm pigs from the same farm located in south‐eastern France than in a previous work conducted in 2007. Pig HEV sequences corresponding to genomic fragments of ORF2 and ORF1 genes were obtained after RT‐PCR amplification with in‐house protocols. Hepatitis E virus genotype was determined by phylogenetic analysis. Prevalence was similar to that determined 5 years earlier (68% versus 62%). Two robust phylogenetic clusters of HEV subtypes 3a and 3f were identified, and these sequences obtained in 2012 largely differ compared with those obtained in 2007. Notably, HEV sequences obtained in 2012 from a majority (62%) of the infected pigs belonged to subtype 3a, which was not previously described in France, including not being found in any of humans, pigs or wild boars. Further studies are needed to assess the circulation of HEV‐3a in pigs and humans in this country. In addition, along with previous findings, this study supports the need for increased information to the public on the risk of HEV infection through contacts with pigs or consumption of pig‐derived products in France.