Small mammals as carriers of zoonotic bacteria on pig and cattle farms - Prevalence and risk of exposure in an integrative approach.

To prevent foodborne infections from pigs and cattle, the whole food chain must act to minimize the contamination of products, including biosecurity measures which prevent infections via feed and the environment in production farms. Rodents and other small mammals can be reservoirs of and key vectors for transmitting zoonotic bacteria and viruses to farm animals, through direct contact but more often through environmental contamination. In line with One Health concept, we integrated results from a sampling study of small mammals in farm environments and data from a capture-recapture experiment into a probabilistic model which quantifies the degree of environmental exposure of zoonotic bacteria by small mammals to farm premises. We investigated more than 1200 small mammals trapped in and around 38 swine and cattle farm premises in Finland in 2017/2018. Regardless of the farm type, the most common species caught were the yellow-necked mouse (Apodemus flavicollis), bank vole (Clethrionomys glareolus), and house mouse (Mus musculus). Of 554 intestine samples (each pooled from 1 to 10 individuals), 33% were positive for Campylobacter jejuni. Yersinia enterocolitica was detected in 8% of the pooled samples, on 21/38 farm premises. Findings of Salmonella and the Shiga-toxin producing Escherichia coli (STEC) were rare: the pathogens were detected in only single samples from four and six farm premises, respectively. The prevalence of Campylobacter, Salmonella, Yersinia and STEC in small mammal populations was estimated as 26%/13%, 1%/0%, 2%/3%, 1%/1%, respectively, in 2017/2018. The exposure probability within the experimental period of four weeks on farms was 17-60% for Campylobacter and 0-3% for Salmonella. The quantitative model is readily applicable to similar integrative studies. Our results indicate that small mammals increase the risk of exposure to zoonotic bacteria in animal production farms, thus increasing risks also for livestock and human health.

Osteological profiling of femoral diaphysis and neck in aquatic, semiaquatic, and terrestrial carnivores and rodents: effects of body size and locomotor habits.

The increased limb bone density documented previously for aquatic tetrapods has been proposed to be an adaptation to overcome buoyancy during swimming and diving. It can be achieved by increasing the amount of bone deposition or by reducing the amount of bone resorption, leading to cortical thickening, loss of medullary cavity, and compaction of trabecular bone. The present study examined the effects of locomotor habit, body size, and phylogeny on the densitometric, cross-sectional, and biomechanical traits of femoral diaphysis and neck in terrestrial, semiaquatic, and aquatic carnivores, and in terrestrial and semiaquatic rodents (12 species) by using peripheral quantitative computed tomography, three-point bending, and femoral neck loading tests. Groupwise differences were analyzed with the univariate generalized linear model and the multivariate linear discriminant analysis supplemented with hierarchical clustering. While none of the individual features could separate the lifestyles or species adequately, the combinations of multiple features produced very good or excellent classifications and clusterings. In the phocid seals, the aquatic niche allowed for lower femoral bone mineral densities than expected based on the body mass alone. The semiaquatic mammals mostly had high bone mineral densities compared to the terrestrial species, which could be considered an adaptation to overcome buoyancy during swimming and shallow diving. Generally, it seems that different osteological properties at the levels of mineral density and biomechanics could be compatible with the adaptation to aquatic, semiaquatic, or terrestrial niches.

Genomic signatures of climate adaptation in bank voles.

Evidence for divergent selection and adaptive variation across the landscape can provide insight into a species' ability to adapt to different environments. However, despite recent advances in genomics, it remains difficult to detect the footprints of climate-mediated selection in natural populations. Here, we analysed ddRAD sequencing data (21,892 SNPs) in conjunction with geographic climate variation to search for signatures of adaptive differentiation in twelve populations of the bank vole (Clethrionomys glareolus) distributed across Europe. To identify the loci subject to selection associated with climate variation, we applied multiple genotype-environment association methods, two univariate and one multivariate, and controlled for the effect of population structure. In total, we identified 213 candidate loci for adaptation, 74 of which were located within genes. In particular, we identified signatures of selection in candidate genes with functions related to lipid metabolism and the immune system. Using the results of redundancy analysis, we demonstrated that population history and climate have joint effects on the genetic variation in the pan-European metapopulation. Furthermore, by examining only candidate loci, we found that annual mean temperature is an important factor shaping adaptive genetic variation in the bank vole. By combining landscape genomic approaches, our study sheds light on genome-wide adaptive differentiation and the spatial distribution of variants underlying adaptive variation influenced by local climate in bank voles.

Taking the beat of the Arctic: are lemming population cycles changing due to winter climate?

Reports of fading vole and lemming population cycles and persisting low populations in some parts of the Arctic have raised concerns about the spread of these fundamental changes to tundra food web dynamics. By compiling 24 unique time series of lemming population fluctuations across the circumpolar region, we show that virtually all populations displayed alternating periods of cyclic/non-cyclic fluctuations over the past four decades. Cyclic patterns were detected 55% of the time (n = 649 years pooled across sites) with a median periodicity of 3.7 years, and non-cyclic periods were not more frequent in recent years. Overall, there was an indication for a negative effect of warm spells occurring during the snow onset period of the preceding year on lemming abundance. However, winter duration or early winter climatic conditions did not differ on average between cyclic and non-cyclic periods. Analysis of the time series shows that there is presently no Arctic-wide collapse of lemming cycles, even though cycles have been sporadic at most sites during the last decades. Although non-stationary dynamics appears a common feature of lemming populations also in the past, continued warming in early winter may decrease the frequency of periodic irruptions with negative consequences for tundra ecosystems.

Hantavirus Infections among Military Forces.

INTRODUCTION: Hantaviruses cause two kinds of clinical syndromes. Hemorrhagic fever with renal syndrome is caused by Hantaan virus in Asia, Puumala virus (PUUV) and Dobrava virus in Europe, and Seoul virus worldwide. Hantavirus cardiopulmonary syndrome is caused by Sin Nombre virus in North America and Andes virus and related viruses in Latin America. All hantaviruses are carried by rodents and insectivores. Humans are infected via inhaled aerosols of rodent excreta. In the history, there are several epidemics of acute infectious diseases during many wars, which have been suggested or proven to be caused by various hantaviruses. MATERIALS AND METHODS: Literature review of 41 original publications and reviews published between 1943 and 2022 was performed. Among them, 23 publications handle hantavirus infections among military forces, and the rest 17 hantavirus infections themselves. RESULTS: A large epidemic during World War II in 1942 among German and Finnish soldiers in Northern Finland with more than 1,000 patients was most probably caused by PUUV. During Korean War in 1951-1954,∼ 3,200 cases occurred among United Nations soldiers in an epidemic caused by Hantaan virus. During Balkan war from 1991 to 1995, numerous soldiers got ill because of hantavirus infection caused by PUUV and Dobrava virus. Several other reports of cases of various hantavirus infections especially among U.S. soldiers acting in South Korea, Germany, Bosnia, and Kosovo have been described in the literature. CONCLUSIONS: Military maneuvers usually include soil removal, spreading, digging with accompanied dust, and living in field and other harsh conditions, which easily expose soldiers to rodents and their excreta. Therefore, the risks of hantavirus infections in military context are obvious. All military infections have been caused by hantaviruses leading to hemorrhagic fever with renal syndrome.

The impact of wildlife and environmental factors on hantavirus infection in the host and its translation into human risk.

Identifying factors that drive infection dynamics in reservoir host populations is essential in understanding human risk from wildlife-originated zoonoses. We studied zoonotic Puumala orthohantavirus (PUUV) in the host, the bank vole (Myodes glareolus), populations in relation to the host population, rodent and predator community and environment-related factors and whether these processes are translated into human infection incidence. We used 5-year rodent trapping and bank vole PUUV serology data collected from 30 sites located in 24 municipalities in Finland. We found that PUUV seroprevalence in the host was negatively associated with the abundance of red foxes, but this process did not translate into human disease incidence, which showed no association with PUUV seroprevalence. The abundance of weasels, the proportion of juvenile bank voles in the host populations and rodent species diversity were negatively associated with the abundance index of PUUV positive bank voles, which, in turn, showed a positive association with human disease incidence. Our results suggest certain predators, a high proportion of young bank vole individuals, and a diverse rodent community, may reduce PUUV risk for humans through their negative impacts on the abundance of infected bank voles.

Predicting habitat suitability for Ixodes ricinus and Ixodes persulcatus ticks in Finland.

BACKGROUND: Ticks are responsible for transmitting several notable pathogens worldwide. Finland lies in a zone where two human-biting tick species co-occur: Ixodes ricinus and Ixodes persulcatus. Tick densities have increased in boreal regions worldwide during past decades, and tick-borne pathogens have been identified as one of the major threats to public health in the face of climate change. METHODS: We used species distribution modelling techniques to predict the distributions of I. ricinus and I. persulcatus, using aggregated historical data from 2014 to 2020 and new tick occurrence data from 2021. By aiming to fill the gaps in tick occurrence data, we created a new sampling strategy across Finland. We also screened for tick-borne encephalitis virus (TBEV) and Borrelia from the newly collected ticks. Climate, land use and vegetation data, and population densities of the tick hosts were used in various combinations on four data sets to estimate tick species' distributions across mainland Finland with a 1-km resolution. RESULTS: In the 2021 survey, 89 new locations were sampled of which 25 new presences and 63 absences were found for I. ricinus and one new presence and 88 absences for I. persulcatus. A total of 502 ticks were collected and analysed; no ticks were positive for TBEV, while 56 (47%) of the 120 pools, including adult, nymph, and larva pools, were positive for Borrelia (minimum infection rate 11.2%, respectively). Our prediction results demonstrate that two combined predictor data sets based on ensemble mean models yielded the highest predictive accuracy for both I. ricinus (AUC = 0.91, 0.94) and I. persulcatus (AUC = 0.93, 0.96). The suitable habitats for I. ricinus were determined by higher relative humidity, air temperature, precipitation sum, and middle-infrared reflectance levels and higher densities of white-tailed deer, European hare, and red fox. For I. persulcatus, locations with greater precipitation and air temperature and higher white-tailed deer, roe deer, and mountain hare densities were associated with higher occurrence probabilities. Suitable habitats for I. ricinus ranged from southern Finland up to Central Ostrobothnia and North Karelia, excluding areas in Ostrobothnia and Pirkanmaa. For I. persulcatus, suitable areas were located along the western coast from Ostrobothnia to southern Lapland, in North Karelia, North Savo, Kainuu, and areas in Pirkanmaa and Päijät-Häme. CONCLUSIONS: This is the first study conducted in Finland that estimates potential tick species distributions using environmental and host data. Our results can be utilized in vector control strategies, as supporting material in recommendations issued by public health authorities, and as predictor data for modelling the risk for tick-borne diseases.

[Infection outbreak among German and Finish troups in Eastern Lapland during World War II - First description of hantavirus disease in the German language area]. / Infektionsausbruch bei deutschen und finnischen Soldaten während des 2. Weltkriegs im Östlichen Lappland ­ Erstbeschreibung der Hantavirus-Erkrankung im deutschen Sprachraum.

Eight decades ago, a report on "a swamp fever-like disease in German troups in Lapland" was published in this journal. The disease outbreak had occurred in 1942 and affected more than 1000 soldiers at the Finish front. The published, precise analysis of the clinical picture was obviously the first description of hantavirus disease in the German language area. Nowadays, hantavirus disease - in Central and Northern Europe also known as Nephropathia epidemica - is one of the most frequent notifiable virus diseases in Germany and Finland.

Zoonotic Cryptosporidium spp. in Wild Rodents and Shrews.

There has been a significant increase in the number of reported human cryptosporidiosis cases in recent years. The aim of this study is to estimate the prevalence of Cryptosporidium spp. in wild rodents and shrews, and investigate the species and genotype distribution to assess zoonotic risk. Partial 18S rRNA gene nested-PCR reveals that 36.8, 53.9 and 41.9% of mice, voles and shrews are infected with Cryptosporidium species. The highest prevalence occurred in the Microtus agrestis (field vole) and Myodes glareolus (bank vole). Interestingly, bank voles caught in fields were significantly more often Cryptosporidium-positive compared to those caught in forests. The proportion of infected animals increases from over-wintered (spring and summer) to juveniles (autumn) suggesting acquired immunity in older animals. Based on Sanger sequencing and phylogenetic analyses, Apodemus flavicollis (yellow-necked mouse) is commonly infected with zoonotic C. ditrichi. Voles carry multiple different Cryptosporidium sp. and genotypes, some of which are novel. C. andersoni, another zoonotic species, is identified in the Craseomys rufocanus (grey-sided vole). Shrews carry novel shrew genotypes. In conclusion, this study indicates that Cryptosporidium protozoan are present in mouse, vole and shrew populations around Finland and the highest zoonotic risk is associated with C. ditrichi in Apodemus flavicollis and C. andersoni in Craseomys rufocanus. C. parvum, the most common zoonotic species in human infections, was not detected.

The Invasive Bank Vole (Myodes glareolus): A Model System for Studying Parasites and Ecoimmunology during a Biological Invasion.

The primary driver of the observed increase in emerging infectious diseases (EIDs) has been identified as human interaction with wildlife and this increase has emphasized knowledge gaps in wildlife pathogens dynamics. Wild rodent models have proven excellent for studying changes in parasite communities and have been a particular focus of eco-immunological research. Helminth species have been shown to be one of the factors regulating rodent abundance and indirectly affect disease burden through trade-offs between immune pathways. The Myodes glareolus invasion in Ireland is a unique model system to explore the invasion dynamics of helminth species. Studies of the invasive population of M. glareolus in Ireland have revealed a verifiable introduction point and its steady spread. Helminths studies of this invasion have identified enemy release, spillover, spillback and dilution taking place. Longitudinal studies have the potential to demonstrate the interplay between helminth parasite dynamics and both immune adaptation and coinfecting microparasites as M. glareolus become established across Ireland. Using the M. glareolus invasion as a model system and other similar wildlife systems, we can begin to fill the large gap in our knowledge surrounding the area of wildlife pathogen dynamics.

Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe.

The picornavirus named 'Ljungan virus' (LV, species Parechovirus B) has been detected in a dozen small mammal species from across Europe, but detailed information on its genetic diversity and host specificity is lacking. Here, we analyze the evolutionary relationships of LV variants circulating in free-living mammal populations by comparing the phylogenetics of the VP1 region (encoding the capsid protein and associated with LV serotype) and the 3Dpol region (encoding the RNA polymerase) from 24 LV RNA-positive animals and a fragment of the 5' untranslated region (UTR) sequence (used for defining strains) in sympatric small mammals. We define three new VP1 genotypes: two in bank voles (Myodes glareolus) (genotype 8 from Finland, Sweden, France, and Italy, and genotype 9 from France and Italy) and one in field voles (Microtus arvalis) (genotype 7 from Finland). There are several other indications that LV variants are host-specific, at least in parts of their range. Our results suggest that LV evolution is rapid, ongoing and affected by genetic drift, purifying selection, spillover and host evolutionary history. Although recent studies suggest that LV does not have zoonotic potential, its widespread geographical and host distribution in natural populations of well-characterized small mammals could make it useful as a model for studying RNA virus evolution and transmission.

Hantavirus Research in Finland: Highlights and Perspectives.

Finland has the highest incidence of hantavirus infections globally, with a significant impact on public health. The large coverage of boreal forests and the cyclic dynamics of the dominant forest rodent species, the bank vole Myodes glareolus, explain most of this. We review the relationships between Puumala hantavirus (PUUV), its host rodent, and the hantavirus disease, nephropathia epidemica (NE), in Finland. We describe the history of NE and its diagnostic research in Finland, the seasonal and multiannual cyclic dynamics of PUUV in bank voles impacting human epidemiology, and we compare our northern epidemiological patterns with those in temperate Europe. The long survival of PUUV outside the host and the life-long shedding of PUUV by the bank voles are highlighted. In humans, the infection has unique features in pathobiology but rarely long-term consequences. NE is affected by specific host genetics and risk behavior (smoking), and certain biomarkers can predict the outcome. Unlike many other hantaviruses, PUUV causes a relatively mild disease and is rarely fatal. Reinfections do not exist. Antiviral therapy is complicated by the fact that when symptoms appear, the patient already has a generalized infection. Blocking vascular leakage measures counteracting pathobiology, offer a real therapeutic approach.

Geographical Distribution and Genetic Diversity of Bank Vole Hepaciviruses in Europe.

The development of new diagnostic methods resulted in the discovery of novel hepaciviruses in wild populations of the bank vole (Myodes glareolus, syn. Clethrionomys glareolus). The naturally infected voles demonstrate signs of hepatitis similar to those induced by hepatitis C virus (HCV) in humans. The aim of the present research was to investigate the geographical distribution of bank vole-associated hepaciviruses (BvHVs) and their genetic diversity in Europe. Real-time reverse transcription polymerase chain reaction (RT-qPCR) screening revealed BvHV RNA in 442 out of 1838 (24.0%) bank voles from nine European countries and in one of seven northern red-backed voles (Myodes rutilus, syn. Clethrionomys rutilus). BvHV RNA was not found in any other small mammal species (n = 23) tested here. Phylogenetic and isolation-by-distance analyses confirmed the occurrence of both BvHV species (Hepacivirus F and Hepacivirus J) and their sympatric occurrence at several trapping sites in two countries. The broad geographical distribution of BvHVs across Europe was associated with their presence in bank voles of different evolutionary lineages. The extensive geographical distribution and high levels of genetic diversity of BvHVs, as well as the high population fluctuations of bank voles and occasional commensalism in some parts of Europe warrant future studies on the zoonotic potential of BvHVs.

Population cycles and outbreaks of small rodents: ten essential questions we still need to solve.

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.

Why Hantavirus Prevalence Does Not Always Increase With Host Density: Modeling the Role of Host Spatial Behavior and Maternal Antibodies.

For wildlife diseases, one often relies on host density to predict host infection prevalence and the subsequent force of infection to humans in the case of zoonoses. Indeed, if transmission is mainly indirect, i.e., by way of the environment, the force of infection is expected to increase with host density, yet the laborious field data supporting this theoretical claim are often absent. Hantaviruses are among those zoonoses that have been studied extensively over the past decades, as they pose a significant threat to humans. In Europe, the most widespread hantavirus is the Puumala virus (PUUV), which is carried by the bank vole and causes nephropathia epidemica (NE) in humans. Extensive field campaigns have been carried out in Central Finland to shed light on this supposed relationship between bank vole density and PUUV prevalence and to identify other drivers for the infection dynamics. This resulted in the surprising observation that the relationship between bank vole density and PUUV prevalence is not purely monotonic on an annual basis, contrary to what previous models predicted: a higher vole density does not necessary result in a higher infection prevalence, nor in an increased number of humans reported having NE. Here, we advance a novel individual-based spatially-explicit model which takes into account the immunity provided by maternal antibodies and which simulates the spatial behavior of the host, both possible causes for this discrepancy that were not accounted for in previous models. We show that the reduced prevalence in peak years can be attributed to transient immunity, and that the density-dependent spatial vole behavior, i.e., the fact that home ranges are smaller in high density years, plays only a minor role. The applicability of the model is not limited to the study and prediction of PUUV (and NE) occurrence in Europe, as it could be easily adapted to model other rodent-borne diseases, either with indirect or direct transmission.

Zoonotic Viruses in Three Species of Voles from Poland.

Rodents are known to be reservoir hosts for a plethora of zoonotic viruses and therefore play a significant role in the dissemination of these pathogens. We trapped three vole species (Microtus arvalis, Alexandromys oeconomus and Microtus agrestis) in northeastern Poland, all of which are widely distributed species in Europe. Using immunofluorescence assays, we assessed serum samples for the presence of antibodies to hantaviruses, arenaviruses and cowpox viruses (CPXV). We detected antibodies against CPXV and Puumala hantavirus (PUUV), the overall seroprevalence of combined viral infections being 18.2% [10.5-29.3] and mostly attributed to CPXV. We detected only one PUUV/TULV cross-reaction in Microtus arvalis (1.3% [0.1-7.9]), but found similar levels of antibodies against CPXV in all three vole species. There were no significant differences in seroprevalence of CPXV among host species and age categories, nor between the sexes. These results contribute to our understanding of the distribution and abundance of CPXV in voles in Europe, and confirm that CPXV circulates also in Microtus and Alexandromys voles in northeastern Poland.

Geographical Distribution of Ljungan Virus in Small Mammals in Europe.

Ljungan virus (LV), which belongs to the Parechovirus genus in the Picornaviridae family, was first isolated from bank voles (Myodes glareolus) in Sweden in 1998 and proposed as a zoonotic agent. To improve knowledge of the host association and geographical distribution of LV, tissues from 1685 animals belonging to multiple rodent and insectivore species from 12 European countries were screened for LV-RNA using reverse transcriptase (RT)-PCR. In addition, we investigated how the prevalence of LV-RNA in bank voles is associated with various intrinsic and extrinsic factors. We show that LV is widespread geographically, having been detected in at least one host species in nine European countries. Twelve out of 21 species screened were LV-RNA PCR positive, including, for the first time, the red vole (Myodes rutilus) and the root or tundra vole (Alexandromys formerly Microtus oeconomus), as well as in insectivores, including the bicolored white-toothed shrew (Crocidura leucodon) and the Valais shrew (Sorex antinorii). Results indicated that bank voles are the main rodent host for this virus (overall RT-PCR prevalence: 15.2%). Linear modeling of intrinsic and extrinsic factors that could impact LV prevalence showed a concave-down relationship between body mass and LV occurrence, so that subadults had the highest LV positivity, but LV in older animals was less prevalent. Also, LV prevalence was higher in autumn and lower in spring, and the amount of precipitation recorded during the 6 months preceding the trapping date was negatively correlated with the presence of the virus. Phylogenetic analysis on the 185 base pair species-specific sequence of the 5' untranslated region identified high genetic diversity (46.5%) between 80 haplotypes, although no geographical or host-specific patterns of diversity were detected.

High genomic diversity in the bank vole at the northern apex of a range expansion: The role of multiple colonizations and end-glacial refugia.

The history of repeated northern glacial cycling and southern climatic stability has long dominated explanations for how genetic diversity is distributed within temperate species in Eurasia and North America. However, growing evidence indicates the importance of cryptic refugia for northern colonization dynamics. An important geographic region to assess this is Fennoscandia, where recolonization at the end of the last glaciation was restricted to specific routes and temporal windows. We used genomic data to analyse genetic diversity and colonization history of the bank vole (Myodes glareolus) throughout Europe (>800 samples) with Fennoscandia as the northern apex. We inferred that bank voles colonized Fennoscandia multiple times by two different routes; with three separate colonizations via a southern land-bridge route deriving from a "Carpathian" glacial refugium and one via a north-eastern route from an "Eastern" glacial refugium near the Ural Mountains. Clustering of genome-wide SNPs revealed high diversity in Fennoscandia, with eight genomic clusters: three of Carpathian origin and five Eastern. Time estimates revealed that the first of the Carpathian colonizations occurred before the Younger Dryas (YD), meaning that the first colonists survived the YD in Fennoscandia. Results also indicated that introgression between bank and northern red-backed voles (Myodes rutilus) took place in Fennoscandia just after end-glacial colonization. Therefore, multiple colonizations from the same and different cryptic refugia, temporal and spatial separations and interspecific introgression have shaped bank vole genetic variability in Fennoscandia. Together, these processes drive high genetic diversity at the apex of the northern expansion in this emerging model species.