puumala hantavirus infection

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  • Feb 16, 2020

Differentiation between Puumala hantavirus infection and maternal ...
Differentiation between Puumala hantavirus infection and maternal …

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1Institute of Plant Protection Horticulture and Forestry, Vertebrate Research, Julius Kühn-Institute, Toppheideweg 88, 48161 Muenster, Germany

3Institute Biochemistry and Biology, Animal Ecology, University of Potsdam, Maulbeerallee 1, 14469 Potsdam, Germany

2Institute for Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Südufer 10 17 493 Greifswald-Insel Riems, Germany

1Institute of Plant Protection in Horticulture and Forestry, vertebrate Research, Julius Kühn-Institute, Toppheideweg 88, 48161 Muenster, Germany

2Institute for Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Südufer 10 17 493 Greifswald-Insel Riems, Germany

2Institute for Novel and Emerging Infectious Diseases, Friedrich-Loeffler-Institut, Südufer 10 17 493 Greifswald-Insel Riems, Germany

3Institute Biochemistry and Biology, Animal Ecology, University of Potsdam, Maulbeerallee 1, 14469 Potsdam , Germany

1Instit ute Crop Protection Horticulture and Forestry, Vertebrate Research, Julius Kühn-Institute, Toppheideweg 88, 48161 Muenster, Germany

The data support the findings of this study are available from the corresponding author on request reasonable ,

In Europe, the bank mice (Myodes glareolus) are widely distributed and can transmit the virus Puumala (PUUV) to humans, which causes mild to moderate form of hemorrhagic fever with renal syndrome, called nephropathia epidemica. Revealing the relationship between host and virus dynamics can help prevent the infection of human PUUV in the future. Bank live mice caught three times a year in 2010-2013 in three forest plots in each of the four regions in Germany. Bank estimated population density of mice and collected blood samples to detect specific antibodies PUUV.

We show that fluctuations PUUV seroprevalence depends not only on the multi-annual, but also on the seasonal dynamics of the abundance of rodent host. In addition, PUUV infection may affect the fitness of the host, because individuals seropositive survived better from spring to summer than uninfected mice Bank. the use of individual space is independent of PUUV infection.

Our study provides robust estimates of the relevant pattern and process dynamics and host PUUV rodents in Central Europe, which is very important for the future development of predictive models for human hantavirus infection risk.

Hantaviruses are zoonotic and emerging pathogenic to humans by rodents and other small mammals reservoirs []. Currently, hantaviruses known to occur in two rodent family (Cricetidae and mice), the two families of insects (Soricidae and Talpidae) and in three families of bats (Rhinolophidae, Nycteridae and Vespertilionidae) [,]. All hantaviruses seem to be associated exclusively with one or several closely related species of mammals reservoirs few and largely follows the geographical distribution of the reservoir [,,].

In Europe, five hantaviruses rat-borne (Puumala, Tula, Tatenale, Dobrava-Belgrade, and viruses Seoul) and four insectivore-borne hantaviruses (Seewis, Asikkala, Boginia and virus Nova) have been identified [, ]. According to present knowledge, only a few mouse-borne hantaviruses cause significant disease in humans. Infection occurs through inhalation of aerosolised virus particle, which is poured out through urine, feces or saliva. Hantavirus disease, namely dengue fever with renal syndrome (HFRS), occurred in Eurasia and has been known since the 1930s []. Puumala virus (PUUV) is the most important hantavirus in North, Central and Western Europe [,]. PUUV disease caused in humans is termed nephropatica epidemica (NE), which is a mild to moderate form of HFRS. The disease is mainly characterized by renal dysfunction or renal failure. The main symptoms are fever, headache, backpain and gastrointestinal symptoms []. Far worse hantavirus cardiopulmonary syndrome is limited to the United States [].

The first detection of PUUV in Germany was in 1980 during a military exercise Belgian []. Since 2001, human hantavirus infections have to be reported in Germany and a total of 10 403 cases recorded up to December 2016 (Robert Koch Institute: SurvStat @ RKI 2.0 ,, status Data: 31/12/2016). The geographical distribution of human cases in Germany is heterogeneous, with the majority reported from highly endemic regionsns in the south, west and north-west of Germany [, -]. In the plague years, the number of cases of human NE rises to about 2000 in Germany (SurvStat @ RKI 2.0 ,, status Data: 05/17/2016).

rat bank (Myodes glareolus) are the main, and in Central Europe exclusive, the PUUV reservoir. This species is distributed throughout Germany and in many countries of Europe and Asia. In Central Europe it inhabits forests, mainly deciduous broad-leaved oak (Quercus robur) and beech (Fagus sylvatica) [], but it can also occur on the fence, parks, and urban gardens. In temperate forests, the availability of food for rats bank fluctuate greatly because of the seed harvest beech and other trees, which are triggered by climatic conditions [-]. Beech mast during the year, the Bank rapidly growing rat population reached its peak population densities in the next year [, -]. Previous research showed that in broad leaved forests of Europe, the rat population fluctuates seasonally Bank and the multi-year peak in the summer population and population outbreaks every 4-7 years []. More recent research shows a plague of rats Bank every 2-3 years [] for beech mast shorten the interval []. The increase in the number of human infections associated with peak PUUV rat population Bank [,,,]. However, mice and hantavirus interaction dynamics are much less understood and this may be important for the transmission of hantavirus in the host population ultimately affect the risk of infection in humans. Due to potentially severe course of the disease and a large number of affected people, understanding human PUUV infection is highly relevant for public health management.

We are presenting the results of temporal and spatial replicated live trap rat population studies linking the existence of bank-specific antibodies in mice bank PUUV their population dynamics, use of space and survival. The pattern of population dynamics banks mice served for four, and PUUV dynamics for two people, a geographic region (PUUV almost absent from the 2 areas) in Germany from 2010 to 2013 includes two plague of rats. The results may be relevant to the future development of an early warning system to minimize the risk of hantavirus infection and side effects related to public health in Central Europe.

Rodent monitoring is done in the spring, summer, and autumn 2010-2013 in four fields of study in Germany; West (North Rhine-Westphalia, Billerbeck, 51 ° 59.63’N, 7 ° 18.99’E), south (Baden-Wuerttemberg, Weissach, 48 ° 49.88’N, 8 ° 57.71’E), North (Mecklenburg-Vorpommern, Jeeser , 54 ° 9.75’N, 13 ° 15.55’E), and East (Thuringia, Gotha, 57.38’N 50 °, 10 ° 39.13’E). Habitat surveyed mainly beech forest or deciduous forest mix.

Ugglan some live traps (Grahnab®, Gnosjo, Sweden) baited with apple pellets, mice, rolled oats and beans and curly wood shavings are provided for insulation. On each plot, box traps 49 (7 × 7) at 10 m distance trap set. Pre-bait traps for 3 days and checked twice daily for 2-3 consecutive days, in the morning and afternoon. Thus, each session trap consists of a few (3-7) trapping opportunities. In total, three replicates Woodland plots per study area (region) (0.2 to 2.2 km apart) and trap session sampled. Each rat was captured tagged with passive integrated transponder tags (PIT) (LUX-ident s.r.o.®, Lanskroun, Czech Republic) for the identification of individuals in the nape. Species and sex of the animal morphology is determined and weighed to the nearest gram to 50 g-spring scale (PESOLA AG®, Schindellegi, Switzerland). Blood samples (20-40 ml) was taken from the facial vein or retro-orbital sinus and stored at -20 ° C until analysis PUUV-specific antibodies. After treatment, the animals were released at the point of capture.

Bank assumed the rat population was closed due to immigration, emigration, birth and death are considered a minimum during the period of trapping 3 days. closed population density was estimated using the program DENSITY 5.0 () with a spatial detection model SECR (spatially explicit capture-recapture; []) using maximum likelihood (ML). If the rate of recapture or movement is too limited to estimate the density of compute, the minimum amount is multiplied by extensive live trapping (0.36 ha) is used. Density estimates expressed as individuals per hectare throughout.

The blood is analyzed in immunoglobulin G (IgG) enzyme linkedimmunosorbent assay (ELISA), which uses PUUV yeast-expressed nucleocapsid protein to test for the presence of antibodies in the sample PUUV. The investigation followed a preset protocol [,]. Print reactivity (positive, vague, negative) followed a decision tree described previously []. In a further analysis of the results of a positive or negative explicitly requested, then the faint test results were classified as negative. For each country and season seroprevalences mean ± standard deviation calculated from plots where> 4 samples were obtained.

The minimum distance between traps for trapping sessions divided by the number of recaptures is used as a measure of the space is used to investigate the potential causes and consequences of the infection in mice PUUV Bank []. Animals with the first catch in a trap in the grid margin to avoid the pitfalls incurred edge effect [] and to increase the possibility of including a network of citizens. Individuals arrested only once excluded from the analysis because there is no available information on the motion.

retake the bank mice, which were tested for antibodies specific PUUV in the previous session, can be identified by their respective marks. This allows studying the seroconversion rate and survival in relation to the status PUUV infection. Seroconversion was defined as the occurrence of PUUV-specific antibodies in animals found seronegative during the previous trap.

Annual and seasonal fluctuations in population density and seroprevalence PUUV analyzed by univariate analysis of variance (ANOVA) with subsequent post hoc tests (Tukey HSD). PUUV seroprevalence population density or the dependent variable and the year, the season as well as fixed factors research area. Analyzes were performed using the R software (Version 3.2.5., In 2016, R Core Team, Vienna, Austria). The significance level was α <5%.

The effect of population density in mice bank PUUV-seroprevalence were statistically analyzed using a general linear mixed model (GLMM) with binomial distribution and logit link function (level of significance α <5%) using the software R. PUUV seroprevalence as proportional response variable (variable 2-vector) is generated from the number of mice PUUV Bank seropositivity and the difference between the amount the Bank of mice tested and the number of mice seropositive PUUV bank (= the number of rats PUUV Bank seronegative). population density and density of the previous session (standardized by the z-transform (z = (x – mean) / sd)), either in the interaction with the season (variable factorial), was included as a covariate. Plot nesting in the study area and year is included as a random factor. Furthermore, the effects of random observations added to the account level for overdispersion [], which tested a priori using the packs ‘blmeco’ and function ‘dispersion_glmer’. The number of observations is N = 58 and the best model selected according to the Akaike information criterion (AIC). We use the ‘r.squaredGLMM’ from ‘MuMIn’-packet to estimate the pseudo-R2 for GLMMs (R2 conditional = variance explained by the fixed and random factors) [,].

Individual differences in the use of space was investigated under the premise to be either the cause or the consequence of infection PUUV. To this effect from the minimum mean distance migrated between recaptures PUUV infection status (the use of space = cause) is analyzed by GLMM with binomial distribution and logit link function (level of significance α <5%) using the software R. PUUV infection status is dependent variable and ‘minimum average distance moved’ fixed factor. Plot nesting areas in the study included as a random factor. The number of observations is N = 405.

Furthermore, the effects of the infection status PUUV the minimum distance between the moving average recaptures (space usage = consequences) were analyzed by GLMM with gamma distribution and log link function (level of significance α <5%) using the software R. the dependent variable ‘means the minimum distance moved’ changed by adding 0.1 m for each value to eliminate the zero values. In early models, PUUV infection status, gender, weight, sex and body weight interaction with PUUV infection status, and season included as covariates. Plot nesting areas in the study included as a random factor. The number of observations is N = 405 and the best model selected in accordance with the AIC.

Changes PUUV infection status of recaptures (seroconversion) were analyzed by Chi-square test (χ2). Analyzes were performed using SPSS (IBM SPSS Statistics for Windows, version 22.0, 2013, IBM Corp., Armonk, New York). The significance level was α <5%.

Survival of mice Bank analyzed by GLMM with binomial distribution and logit function link (level of significance α <5%) using the software R (if necessary, install tests hoc performed using multcomp ‘(Tukey contrasts) and ‘lsmeans’ (pairwise comparisons) packet). Survival (factorial variables; yes / no) is the dependent variable and PUUV infection status, gender, weight, sex and body weight interaction with PUUV infection status, and the season is the beginning of certain factors. Plot nesting areas in the study included as a random factor. The number of observations is N = 1263 and the best model selected in accordance with the AIC.

In total 3301 Bank rats trapped during 2010-2013 were roughly evenly between fields of study. population density tends to increase from spring to summer or autumn (Fig.). There were statistically significant differences in population density between the years (ANOVA: F = 34.54, p <0.001) and season (F = 5.83, p = 0.004) but not between the study area (F = 0.50, p = 0.681) , In 2010 and 2012, the population density is significantly higher than in 2011 and 2013 (Tukey HSD: 2010/2011, p <0.001; p = 0.933 2010/2012; 2010/2013 p <0.001; 2011/2012, p <0.001; 2011 / 2013 p = 0.043; 2012/2013, p <0.001). the population density in the summer was significantly higher compared with the spring (p = 0.003) but not for the fall (p = 0.439) or between the spring and autumn (p = 0.095). However, the maximum density observed in the summer of 2010 (61-121 ind / ha) and 2012 (72-82 ind / ha), respectively, which shows the Bank plague rat population. The mice Bank the highest population density is estimated for summer 2010 in the South with an average of 121 ind / ha (Fig.). In the spring of 2011 and 2013 with the lowest population density 1-19 ind / ha (2011) and 0-5 ind / ha (2013).

Population dynamics of rat Bank in Germany from 2010 to 2013. Estimates of population density mean ± standard deviation as individuals per hectare of forest plots with three replications per area of ​​study (N = the total number of trapped mice Bank)

2800 Bank rats were tested for antibodies reactive PUUV which 566 (20%) were seropositive PUUV. Nearly 99% (561 people) from their rat-seropositive PUUV Bank stuck in the South or West. In the North and East Bank only 5 mice tested positive in PUUV IgG ELISA. Therefore, PUUV most likely not present at the location of traps in the North and East, which corresponds to a large-scale study in rats bank of the GDR []. Drewes et al. [] The samples around 1200 mouse snap-stuck from several sites in Germany partly overlaps with the northern and eastern site of the study. All PUUV-negative mice in the IgG ELISA, conventional and real-time RT-PCR. Therefore, positive test results from the two fields of study reported here was most likely due to spillover virus infection associated PUUV Tula (TULV) or false positive reactions in ELISA. Due to the general absence PUUV, North and East are not far included in the analysis of data on prevalence in the rat PUUV Bank.

serological investigation conducted on mice in 1460 the bank of the West and South. The prevalence did not vary between fields of study: (. Photo) (ANOVA F = 2.17, p = 0.145) but significantly different between seasons (F = 4:35, p = 0.017) and the year (F = 19.11, p <0.001 ). Seroprevalences in 2010 and 2012 were significantly higher compared to 2011 and 2013 (Tukey HSD: 2010/2011, p <0.001; p = 0.998 2010/2012; 2010/2013 p <0.001; 2011/2012, p <0.001; p = 2011 / 2013 0,367; 2012/2013, p <0.001). Seroprevalence in the spring were significantly higher than in autumn (p = 0.018) but not for the summer (p = 0.097) or between summer and autumn (p = 0.721). However, the highest prevalence was found in spring 2010 (West: 64 ± 29%, South: 49 ± 32% per plot and trapping session) and 2012 (West: 59 ± 2%, South: 64 ± 40%). In these years, prevalence decreased from spring to summer and from summer to autumn. In 2011 and 2013, the rate PUUV-seropositive individuals in the spring is much lower (<29%), and even zero, compared with the previous year. Over the years, seroprevalence PUUV remained on a low or zero level or slightly increased towards autumn.

PUUV prevalence in a population of two banks rat region in Germany from 2010 to 2013. The average seroprevalence ± standard deviation (%) in the spring, summer and autumn every year an estimated three replications forest plots per area of ​​study. Numerical values ​​per season is the total number of individuals tested of all the plots in each area of ​​study

We do GLMM to test for the effects of population density on the banks mice variance in PUUV seroprevalence in the population. The higher the population density of banks in the session rat traps in the high spring PUUV seroprevalence (p <0.001) (Fig.) (Table). A relation similar but weaker discovered in the summer (p = 0.027), but not in the fall (p = 0.570) (Table) (Fig.). There was no effect of the interaction trap density of the previous session and season on PUUV seroprevalence (p> 0.05; removed from the model). Plot random factor nested in the study area (SA: plot) do not explain the variance in PUUV seroprevalence, but in doing (0.31 ± 0.56; variance ± standard deviation). The best model to explain almost one-third of the variance in PUUV seroprevalence (Rconditional2 = 0.28).

seasonal effects of the rat population density of banks (z-transformed) in PUUV prevalence in the population of the host. Black bars on the x-axis represents the distribution of the value of the population density per trap session

Effects bank population density of rats in the interaction with the season on PUUV prevalence in the population of the host

coefficient parameters general linear mixed model ( GLMM) with binomial distribution

the number of observation = 58 degrees of freedom = 7

Italics indicate significance value of p values ​​(p <0.05)

Analyze the impact of the use of space as a cause of infection in mice Bank PUUV using GLMM did not show a significant effect of the minimum average distance moved PUUV infection status (p = 0.205). Plot random factor nested in the study area (SA: plot) can explain only a small portion of the variance in the probability of infection PUUV (0.01 ± 0.10; variance ± standard deviation) (Table; Figure a.).

The results Model GLMMs investigate the use of space as a cause (a) or consequences (b) infection PUUV in bank mice

Parameter coefficient of general linear mixed model (GLMM) with binomial distribution (a) and the gamma distribution (b)

the number of observations = 405, degrees of freedom = 3 (a) and 4 (b)

the use of Spacebar = average minimum distance migrated between recaptures

Italic indicates a significance value of p values ​​(p <0.05)

Influence plot the use of space as a potential cause of (a) and consequences (b, c) PUUV infection (and sex-c) in mice Bank. use of space mice Bank = minimum average distance moved. A black bar at the x-axis (a) represents the distribution of average individual minimum distance move ‘values ​​

We also do GLMM to test for the effect of infection status PUUV the minimum distance moving average (space usage = consequences). First of all, the election season excluded models, weight and all interactions from further consideration. There is no significant effect of status on the use of space PUUV infection was found (p = 0.378) (Table), although the minimum average distance moved was 11.9% longer for individuals without PUUV-reactive antibody (Fig. B). Men tend to move longer distances than females (p = 0.068) (Fig. C). Plot random factor nested in the study area (SA: plot). Can not explain the difference in the average minimum distance moved

Most people get stuck more than once caught in two (122) and some in three (14) or four (2) trapping session. We recorded a total of 156 recaptures of individuals in several seasons. Typically, reoccupied occurs in the following trap, but in two cases (one in each area of ​​study), the first rat caught in the summer is not recorded in the autumn, but recaptured in the following spring. In the second area of ​​research, women are more often arrested back than males (West: 33/61 = 54%; South: 56/95 = 59%).

Most recaptures remain seronegative (West 44%, South 46%), followed by banks living mice seropositive (West 34% South ;. 34%) (Figure). In the West 11 (18%) of the reoccupy showed seroconversion PUUV. In the South of 16 mice (17%) seroconversion (Fig.). Two rats in the West (1%) and 3 rats in the South (2%) converted from seropositive to seronegative. More females than males remain seronegative (West: 14/27 = 52%; South: 26/44 = 59%) or seropositive (West: 15/21 = 71%; South: 21/32 = 66%). No sexfference in seroconversion (p> 0.05).

The number of mice Bank retakes. Reoccupy per study area (West, South) total and per gender (f female, m male) were divided into recaptures that remain seronegative (neg / neg) or seropositive (postal / zip), seroconversion (neg / post) or seem to have lost antibody (pos / neg)

Most recaptures occurred in 2010 and 2012 (78%). seasonal variations in survival rates (Fig.) reflected fluctuations in the population density of banks rat plague years with a peak in the summer (Fig.). A GLMM conducted to determine the effect of infection status on the survival of mice PUUV Bank. First of all, the model showed survival was significantly lower going from autumn to spring (during the winter) compared to the viability of the year from spring to summer and summer to autumn (spring / summer z = -1.08, p = 0.520; spring / autumn z = -3.43, p = 0.002; summer / autumn z = -2.86, p = 0.011). This is most likely due to trapping interval between seasons (twice as long during the winter). Therefore, a separate GLMMs performed for each season.

The survival rate of mice by PUUV seroprevalence Bank. the average value ± standard deviation per the first fishing season

Models election heavy excluded from further consideration in every season and every interaction in the autumn (Table). From spring to summer, survival was significantly higher for PUUV-seropositive mice (p = 0.044) (Table ;. Figure) but did not differ between the sexes. From summer to autumn, survival was significantly lower for seropositive (post) male (M) compared with seropositive or seronegative (neg) female (F) (negF / posF z = -0.09, p = 1.000 ; negF / Negm z = 0.67, p = 0.903; negF / POSM z = 2.77, p = 0.027; posF / Negm z = 0.63,

p = 0.919; posF / POSM z = 2.64, p = 0.038; Negm / POSM z = 2.38, p = 0.076) (Table ;. Figure b). During the winter (fall to spring), there is no effect of PUUV infection status or sex on survival was found (Table).

seasonal effects of PUUV infection status, sex and their interaction (not in c) on the survival of banks mice

Parameter coefficient of general linear mixed model (GLMM) with binomial distribution

Italic indicates a significance value of p values ​​(p <0.05)

Effect PUUV infection status of individuals on the survival of mice bank of spring (a) to summer and from summer ( b) to fall. significant results shown in Table

processes involved in the transmission of hantavirus have been mostly studied in northern Europe [,,,]. Knowledge of the mechanisms in Central Europe rarely [,, -]. With our latest research, we closed two spatially replicated rat plague bank (2010 and 2012) and two lower phases (2011 and 2013), which is likely to provide robust estimates of the patterns and processes that are relevant.

The dynamics of populations of mice Bank in Central Europe is driven by a beech tree seed crop year [- ,,]. Beech mast such events have recently occurred every 2-3 years [,,], plagues of rats Bank also occur every 2-3 years. 2-3 year cycle has a great influence on the dynamics PUUV in rodent host population and hence the number of infections of human PUUV.

In our study, the prevalence PUUV (reliably detected only in two regions) temporal fluctuate depending on the abundance of the host population. seroprevalences highest were found in 2010 and 2012, when the abundance of host mice peaked (Fig., the chart above) triggered by a pile of beech in 2009 and 2011 [], and coincides with the highest rates of infection PUUV humans ever recorded since the disease became should be reported in 2001 (SurvStat @ RKI 2.0 ,, status Data: 17/05/2016). In banks rat plague years, PUUV prevalence peaked in the spring, when the population consists of old overwintered animals [,]. These animals are most likely to die in the summer, which led in part to a decrease in seroprevalence PUUV, despite the increase in population density [,]. Furthermore, despite the increase in absolute numbers of people infected, PUUV prevalence decreased (Fig.) Shows the transmission rate exceeds the rate of population growth in the peak reproductive phase. Therefore, young children are not infected with the lowering PUUV seroprevalence during the year [,] (see below). Thus, this decline in PUUV seroprevalence observed to continue until the autumn. In 2011 and 2013, when the density of rats Bank collapsed in the West and South, the prevalence also decreased dramatically.

Density-dependence of the virus in rodent host population shown to hantavirus [-]. However, we find also a clear difference in the prevalence PUUV in between seasons. There is a direct density-dependence is strong in the spring. This may be due to the presence of many people overwintered contracted PUUV in the previous year or during the winter and represent the founding population for outbreaks to come, while in the year with a population of spring are smaller (it does not lead to an outbreak), PUUV seroprevalence is much lowered , In summer, when the newborn baby is not infected without maternal antibodies (for details see Kallio et al. []) Sign population, PUUV seroprevalence decreased (juvenile dilution efek- []) and consequently decrease the density dependence, but still significant. In the fall, there was no effect of density and density dependence seems to be diluted during the year may be due to the transmission of more complex scenarios during the reproductive phase based on the reproductive behavior (eg, aggression, territoriality; []). Our data underline the seroprevalence PUUV dependence on seasonal dynamics of density and multi-annual rodent hosts in Central-Europe [,].

sufficient temporal variation and geographical differences in the host and virus detected dynamics indicate that the bank PUUV mouse-human epidemiological system is even more complex than previously thought. Perhaps most striking, PUUV almost none of eastern Germany and northern bank although mice are present [] and fluctuations in abundance are also associated with beech masting []. Bank rats in the North and East and the East belongs to the Carpathian evolutionary lineages, whereas mice in the South and West bank owned Western evolutionary lineages []. The almost complete absence PUUV Bank-seroreactive mice in the study of sites in the North and East is in line with results of previous studies in which rats bank of the north and east Germany was found to be free of PUUV as determined by IgG -ELISA and RT-PCR analysis [ ]. The PUUV presence in eastern and northern Germany caused by PUUV association with Western evolutionary lineages of mice Bank and following the distribution of postglacial recolonization of Germany []. Some mice Bank PUUV-seroreactive found in this study may be the result of spillover infection, most likely by TULV. TULV hantavirus is present only on the rat species more closely related antigenically and PUUV- PUUV and TULV-specific antibodies can not be distinguished by ELISA [,]. However, the spillover of infection appears to only occur rarely (Drewes et al., Unpublished data) [,] and therefore did not affect these results.

Bank Male rats move further away from the Bank female rats [,], which could not be confirmed statistically in our study, although men seem to be more mobile (25.4%, well within the average minimum to move ). men are more active are more susceptible to infection [,], which could lead to the hypothesis that the seroprevalence PUUV positively correlated with the use of space causes the probability of infection increases. However, there was no effect of the use of space as a cause of infection in mice PUUV Bank can be found. Reverse connection of these two parameters (reciprocal effect; []) may indicate the possible sublethal effects on the fitness of the host mice (here presented using space) as a consequence of infection PUUV. However, the effect of infection status PUUV on the use of space can not be detected, which contrasts with previous findings that affect the fitness of the host PUUV infection associated with survival and reproduction [,]. In general, the average minimum distance is shorter move appeared to be associated with a higher probability of infection in mice PUUV bank (Fig. A, b), but it remains unclear whether the infection affects PUUV spatial activity or vice versa. The data generated by the movement of individuals who study recapture a bit raw and more detailed data from the telemetry work is needed to further explain the causes and consequences of the infection in mice host PUUV fitness and behavior.

The proportion of seronegative and -seropositive PUUV- mice or rats with seroconversion associated with previous findings [,]. Seroconversion in our study (17-18%) is smaller than the former results (32%; []). It is most likely the effect of the trap interval, most of the three months in our study and 6 months in Escutenaire et al. [], Reduce the probability of seroconversion in our study. ‘Inverted seroconversion’ from positive to negative in three teens (first capture ≤15 g) likely consequences of the loss of maternal antibodies []. Although the presence of antibodies PUUV-reactive assumed to last a lifetime [], the loss of antibodies in animals retake may indicate clearance of virus [], as discussed also for hantavirus others [], or may be caused by oscillation antibody titer below the detection limit of the ELISA used

women more often recaptured than men. (Male: female = 1: 1.3). The number of arrests of women is higher than men (male: female = 1: 1.2) and can be explained by a strong territorial of women compared to men []. Seroconversion did not differ between the sexes. Therefore, the common assumption that men have a higher risk of infection because of their behavior [,,] or that women may be better off sticking with the subject PUUV infection [] is not supported. Thus, the effect should PUUV on the fitness of mice [] requires further investigation.

reoccupied between trapping sessions more often reflect life on the outbreak of the year when a higher initial population abundance. Survival also followed a seasonal pattern because there is a higher survival at the end of the reproductive phase (summer to autumn) for PUUV seronegative and seropositive catch. survival-winter lows, which is likely effects of trapping interval (during winter twice as long in years) and therefore the survival suit PUUV infection status was analyzed separately for each season. PUUV-seropositive mice survived better from spring to summer, which may indicate a positive effect on the fitness of the host. However, the alternative plausible explanation is the effect of residency. In the spring, especially in the plague years, PUUV increasing prevalence of seropositivity reflected over seronegative mice. PUUV-seropositive animals that survived the most likely local residents, who got infected in the previous year and overwintered. Residents are more likely to be arrested again lead to a better life based recapture than in seronegative. The latter may include temporary or immigrated mice were recaptured less frequently than the population. From summer to autumn, male PUUV-seropositive women survive less well compared to infection status. Again, this power has the effect of residency. In summer, PUUV prevalence declined and seronegative individuals proportionally most likely because of the young mice were not infected. Not only citizens, but also women (territorial; []) were more likely to be recaptured. Thus, men are more likely to disperse, which could lead to reoccupy less (clearly reduced survival). During the winter, there was no effect on survival PUUV infection is found. seasonal survival has not been explored so far. Former studies investigating reports of survival over-winter no effect on survival PUUV infection [,], but see Kallio et al. []. maternal antibodies do not care in our study due to the number of teenagers recaptured with negligible potential maternal antibodies (spring to summer of N = 1, summer to autumn N = 4). Little is known about hantavirus infection sublethal effects on the behavior and fitness of host rodents that may have consequences for the survival and population dynamics. Clarifying the impact could explain the findings are inconsistent us about the relationship status of infection PUUV on survival as shown increased survival with positive results PUUV from spring to summer (probably due to the increased prevalence of PUUV in the spring) and the apparent decline in the survival of men -laki seropositive from summer to autumn. Therefore, further research should be in controlled environments-justified.

Our studies show the patterns and processes that are relevant in PUUV dynamics and host rodent in Central Europe. Seasonal and multi-annual fluctuations in abundance PUUV seroprevalence depending on the host. This knowledge can facilitate the future development of early warning systems to reduce the risk of human hantavirus infection.

Effects PUUV infection in the rodent host space usage and viability could not convince clarified. Further research is needed to test for the possible impact by comparing the behavior and survival between regions endemic and non-endemic.

DR, CI and JJ conceived and designed the study. DR, UMR, CI, SS and JJ collect data, DR, UMR, CI and SS analyzed the samples and DR and CI analyze data. DR, CI, RGU, JAE and JJ interpreted the results and wrote the manuscript. All authors read and approved the final manuscript.

The support of Nastasya G. eel in a mousetrap, from Dorte traders in PUUV ELISA analysis, Dr. Doreen Gabriel in statistical analysis and Alice Kenney in proofreading was friendly recognized.

thatthey The authors declare no competing interests.

The data do not support the findings of this study are available from the corresponding author on request reasonable

All the procedures involving animals do accor ding legislation relevant and with the permission of the federal government (permits South Regierungspräsidium Stuttgart 35-9185.82 / 0261, West :. the state Agency for Nature, the environment and consumer protection of North Rhine-Westphalia 8.87-51.05.20.09.210, North: the state Department of Agriculture, food safety and fisheries Mecklenburg-Vorpommern 7221.3 -030 / 09, East Thuringian state Office for food safety and consumer protection 22-2684-04-15 -107/09).

This study was commissioned and funded by the Environment Agency federal (UBA) in the plans for Environmental Research Ministry of Federal Germany for the Environment, Nature Conservation, Bui lding and Nuclear Safety (BMUB) (Grant No. 3709 41 401 and Grant Number 3713 48.401 for JJ). The work was supported by the Federal Ministry of Education and Research (BMBF) through the National Research Platform for Zoonoses (Network “Rodent-borne pathogens”; Project Number 01KI1018 and 01KI1303, for RGU), the Robert Koch Institute with funding from the German Ministry of Public Health (Grant No. 1362 / 1-924 and 1362 / 1-980 for RGU), the German research Foundation (SPP 1596 ‘ecology and species barriers in developing countries Viral Diseases’, UL 405 / 1-1 for RGU) and EU grants FP7-261504 EDENext (for RGU) and cataloged by the Steering Committee as EDENext EDENext472 (). The contents of this publication are those of the authors and do not necessarily reflect the views of the European Commission.

Daniela Reil and Ulrike M . Rosenfeld contributed equally to this work

Daniela Reil, Phone:

Ulrike M. Rosenfeld, email :: 0049 251 8710642, email ..

Christian Imholt, email: ..

Sabrina Schmidt, e-mail:

Rainer G. Ulrich, email :.

Jana A. Eccard, email:.

Jens Jacob, email:.

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8600 Rockville Pike, Bethesda
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