The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes

Effects of population fluctuation of the gray-sided vole(Clethrionomys rufocanus) on the prevalence (infection rates) of the parasiteEchinococcus multilocularis in red fox(Vulpes vulpes) populations was investigated from 1985 to 1992 in eastern Hokkaido (Abashiri, Nemuro, and Kushiro area), Japan. This parasite needs two hosts to complete its life cycle; the gray-sided vole as its intermediate host and the red fox as its final host. We found that: (1) Infection rates in foxes depended on the current-year abundance of voles in all three study areas, particularly in Abashiri. (2) In addition to this direct density-dependence, delayed density-dependence between the infection rate and the prior-year abundance of voles was detected in Nemuro and in Kushiro. (3) The regional differences in density-dependence pattern were related to regional differences in the winter food habits of red foxes: in Abashiri the proportion of voles in the fox’s diet greatly decreases in winter, while the proportion remains high in winter in Nemuro and in Kushiro, probably because of shallower snowpack. These results suggest that infection rates in foxes in Abashiri were less influenced by the prior-year prevalence, since the infection cycle might be interrupted in winter, when voles became less important in fox’s diet. In contrast, the state of the prevalence may carry over from year to year in Nemuro and in Kushiro, because red foxes continue to eat a considerable amount of voles throughout year. The regionally contrasted results for the relationship between infection rate in foxes and vole abundance were parallel to the regional difference in fluctuation pattern of vole populations, which are highly variable in Abashiri area, but less variable in Kushiro-Nemuro area. Drastic change in vole populations appears to affect the host-parasite system.     

Life cycles of Echinococcus multilocularis in relation to human infection

The cycle of Echinococcus multilocularus in natural and synanthropic hosts was investigated during 10 yr in an endemic focus of alveolar hydatid disease in the Massif Central of France. The natural cycle, involving red foxes, Vulpes vulpes, and voles, Arvicola terrestris, existed immediately surrounding a village in which human cases of alveolar hydatid disease occurred. Both foxes and free-ranging dogs could serve as the source of infection for the human population.     

Evidence for an increasing presence of Echinococcus multilocularis in foxes in The Netherlands

Echinococcus multilocularis, a tapeworm causing alveolar echinococcosis which is considered a serious zoonosis known to affect humans, appears to be expanding its geographical range in Europe. We studied the emergence of the parasite in the European westernmost edge of its geographical distribution, based on two consecutive parasitological examinations of red foxes (Vulpes vulpes) sampled between 1996 and 2003 in The Netherlands. The average worm count increased from 2.6 worms per fox in the first surveillance to 16.6 worms per fox in the second. Using a mathematical model for a spatially spreading parasite, we found a strong indication that the parasite population is increasing in number and is spreading northward at the speed of 2.7 km per year. The reproduction number (R0), reflecting the parasite's transmission process, is estimated from the surveillance data and it is likely to be more than 1 but not exceeding a value of 4. We analysed a parasite control strategy by estimating the critical fox density for parasite elimination. We conclude that E. multilocularis is an emerging parasite in The Netherlands and thus in the western part of Europe. Control will be very difficult given the current high fox population density.     

Large prey for small cubs - on crucial resources of a boreal red fox population

Many studies of red fox Vulpes vulpes diet have indicated a higher frequency of large prey in the diet of cubs at dens in relation to that of adults From time to time this finding has been questioned as an artifact due to the different types of sampling In this paper I suggest that the observations were correct and reflected optimal behaviour of a central place forager I compared the diet of foxes by analyses of 112 cub scats collected at breeding dens and 168 adult scats collected during the same periods The study was performed in a boreal environment, characterised by cyclically fluctuating vole populations According to theory the diets should converge when voles become plentiful During a year of low, but increasing, vole densities, a significantly higher proportion of large prey was found in the sample from cubs than from adults This was not the case during the peak and the decline year, when the presumably easily available voles appeared frequently in the scats of both cubs and adults I argue that the availability of large prey during the first year of increasing vole densities might determine territory sue and hence also average population density of foxes throughout the whole cycle in boreal foxes     

Dynamics of the Force of Infection: Insights from Echinococcus multilocularis Infection in Foxes

Characterizing the force of infection (FOI) is an essential part of planning cost effective control strategies for zoonotic diseases. Echinococcus multilocularis is the causative agent of alveolar echinococcosis in humans, a serious disease with a high fatality rate and an increasing global spread. Red foxes are high prevalence hosts of E. multilocularis. Through a mathematical modelling approach, using field data collected from in and around the city of Zurich, Switzerland, we find compelling evidence that the FOI is periodic with highly variable amplitude, and, while this amplitude is similar across habitat types, the mean FOI differs markedly between urban and periurban habitats suggesting a considerable risk differential. The FOI, during an annual cycle, ranges from (0.1,0.8) insults (95% CI) in urban habitat in the summer to (9.4, 9.7) (95% CI) in periurban (rural) habitat in winter. Such large temporal and spatial variations in FOI suggest that control strategies are optimal when tailored to local FOI dynamics.     

Epizootiology of Hyalinocysta chapmani (Microsporidia: Thelohaniidae) infections in field populations of Culiseta melanura (Diptera: Culicidae) and Orthocyclops modestus (Copepoda: Cyclopidae): a three-year investigation

The epizootiology, transmission dynamics and survival strategies employed by the microsporidium Hyalinocysta chapmani were examined in field populations of its primary mosquito host, Culiseta melanura and its intermediate copepod host, Orthocyclops modestus over a three-year period in an aquatic subterranean habitat. H. chapmani was enzootic and was maintained in a continuous cycle of horizontal transmission between each host. There were three distinct periods during the summer and fall when developing mosquito larvae acquired infections; each was preceded by or coincident with the detection of infected copepods. Results were corroborated in laboratory bioassays, wherein transmission was achieved in mosquito larvae that were reared in water and sediment samples taken from the site during the same time periods. The highest infection rates, ranging from 60% to 48%, were repeatedly observed during the first six weeks of larval development. These were coincident with the most sustained collections of infected copepods obtained during the year and highest levels of infection achieved in the laboratory transmission studies. The high prevalence rates of lethal infection observed in larval populations of C. melanura at this site are among the highest recorded for any mosquito-parasitic microsporidium and clearly suggest that H. chapmani is an important natural enemy of C. melanura. H. chapmani appears to overwinter in diapausing mosquito larvae but may also persist in copepods. The absence of vertical transmission in the life cycle of H. chapmani and the sole reliance on horizontal transmission via an intermediate host are unique survival strategies not seen among other mosquito-parasitic microsporidia. The epizootiological data suggest that this transmission strategy is a function of the biological attributes of the hosts and the comparatively stable environment in which they inhabit. The subterranean habitat is inundated with water throughout the year; copepods are omnipresent and C. melanura has overlapping broods. The spatial and temporal overlap of both hosts affords abundant opportunity for continuous horizontal transmission and increases the likelihood that H. chapmani will find a target host. It is hypothesized that natural selection has favored the production of meiospores in female host mosquitoes rather than congenital transfer of infection to progeny via ovarian infection as a strategy for achieving greater transmission success.     

A semi-stochastic model of the transmission of Escherichia coli O157 in a typical UK dairy herd: dynamics, sensitivity analysis and intervention/prevention strategies

When modelling the transmission of infection within small populations, it is necessary to consider the possibility of stochastic fade-out of infection. We present a semi-stochastic model for the transmission of a microparasite, in this case Escherichia coli O157, within a multigroup system, namely a typical UK dairy herd. The model includes birth, death, maturation, the dry/lactating cycle and various types of transmission (i.e. direct, pseudovertical (representing direct faecal-oral transmission between dam and calf within the first 48 h) and indirect (via free-living infectious units in the environment)). We present the results of our simulation study alongside data from empirical studies and also compare simulation results with those for the corresponding deterministic model. We then examine the effects of reducing shedding in the food-producing groups on outbreak size and prevalence of infection. A sensitivity analysis of herd prevalence reveals that, for both the deterministic and the semi-stochastic model, the prevalence within the herd is most sensitive to two parameters relating to the weaned group. This supports our previously reported conclusions for the deterministic model, which were based on an analysis of the next-generation matrix. The sensitivity analysis also indicates that herd prevalence is greatly affected by two other parameters relating to the lactating group. We conclude by discussing the possible efficacy of suggested intervention strategies.     

Effective High-Throughput Blood Pooling Strategy before DNA Extraction for Detection of Malaria in Low-Transmission Settings

In the era of (pre) elimination setting, the prevalence of malaria has been decreasing in most of the previously endemic areas. Therefore, effective cost- and time-saving validated pooling strategy is needed for detection of malaria in low transmission settings. In this study, optimal pooling numbers and lowest detection limit were assessed using known density samples prepared systematically, followed by genomic DNA extraction and nested PCR. Pooling strategy that composed of 10 samples in 1 pool, 20 µl in 1 sample, was optimal, and the parasite density as low as 2 p/µl for both falciparum and vivax infection was enough for detection of malaria. This pooling method showed effectiveness for handling of a huge number of samples in low transmission settings (<9% positive rate). The results indicated that pooling of the blood samples before DNA extraction followed by usual nested PCR is useful and effective for detection of malaria in screening of hidden cases in low-transmission settings.     

Inheritance of litter size at birth in farmed arctic foxes (Alopex lagopus, Canidae, Carnivora)

Natural populations of the arctic fox (Alopex lagopus, Canidae, Carnivora) differ drastically in their reproductive strategy. Coastal foxes, which depend on stable food resources, produce litters of moderate size. Inland foxes feed on small rodents, whose populations are characterized by cycling fluctuation. In the years with low food supply, inland fox populations have a very low rate of reproduction. In the years with high food supply, they undergo a population explosion. To gain insight into the genetic basis of the reproductive strategy of this species, we performed complex segregation analysis of the litter size in the extended pedigree of the farmed arctic foxes involving 20,665 interrelated animals. Complex segregation analysis was performed using a mixed model assuming that the trait was under control of a major gene and a large number of additive genetic and random factors. To check the significance of any major gene effect, we used Elston-Stewart transmission probability test. Our analysis demonstrated that the inheritance of this trait can be described within the frameworks of a major gene model with recessive control of low litter size. This model was also supported by the pattern of its familial segregation and by comparison of the distributions observed in the population and that expected under our model. We suggest that a system of balanced polymorphism for litter size in the farmed population might have been established in natural populations of arctic foxes as a result of adaptation to the drastic fluctuations in prey availability.     

Female-biased infection and transmission of the gastrointestinal nematode Trichuris arvicolae infecting the common vole, Microtus arvalis

Previous studies addressing the importance of host gender in parasite transmission have shed light on males as the more important hosts, with the higher transmission potential of males being explained by the fact that they often harbour higher parasite loads than females. However, in some systems females are more heavily infected than males and may be responsible for driving infection under such circumstances. Using a wild population of common voles (Microtus arvalis), we showed that females were more frequently infected by the intestinal nematode Trichuris arvicolae than males (i.e. prevalence based on the presence of eggs in the faeces) and that females were shedding greater numbers of parasite eggs per gram of faeces (EPG) than males. By applying an anthelmintic treatment to either male or female voles, we demonstrated that treating females significantly reduced parasite burdens (i.e. prevalence and EPG) of both male and female hosts, while treating males only reduced parasite burden in males. These findings indicate that in this female-biased infection system females play a more important role than males in driving the dynamics of parasite transmission.     

Pair approximations and the inclusion of indirect transmission: theory and application to between farm transmission of Salmonella

The spatial-temporal dynamics of farm animal diseases depend both on disease specific processes and the underlying contact network between farms. Indirect transmission via free-living bacteria in the environment is an important transmission route and contributes significantly to the dynamics. The pair-wise model has been developed to include both direct transmission and indirect transmission via free stages. The model is compared with stochastic simulations of epidemics on contact networks. The network framework is applied to the investigation of the epidemiological dynamics of between-herd transmission of Salmonella spp. The main results help to explain differences in observed epidemiological patterns and to identify possible causes for different strains of Salmonella developing so much variation in their infection dynamics in UK dairy herds. Numerical results show that shorter infectious period, more persistent immune response and more rapid removal of faeces result in a lower prevalence of infection and a greater tendency for (damped) oscillation. A possible control strategy is consequently suggested. Furthermore, the effect of network structure on long-term dynamics is examined.     

Optimal infection strategies: should macroparasites hedge their bets?

Despite considerable research into the mechanisms that lead to the persistence of parasites, the huge diversity of macroparasite transmission strategies observed both within and among species has yet to be explained. This may be because questions of parasite persistence are typically addressed at the population level, even though observed transmission rates are determined by infection events at the level of the individual parasite. To help overcome this disparity, a simple model is developed to explore the optimal infection strategy for a macroparasite under a range of selection pressures. The model calculates the fitness of the parasite by considering explicitly the probability of the individual infective stages surviving and infecting. The optimal strategy is highly sensitive to the rate of host availability and, considering the parasite's fitness, it is often preferable to have sub-maximal infectivity to maximise survival during periods of host absence. An important finding is that when parasites are faced with unpredictable conditions such as the time of host availability, the optimum strategy may be to produce offspring that differ in their infection strategies. By spreading the risk in this way, known as bet hedging, parasites can increase the chances that at least some of their offspring will infect successfully. This potential for variation in infection strategies has not been considered explicitly before and may have wide reaching implications for current epidemiology theory.     

A role for vector-independent transmission in rodent trypanosome infection?

Within host-pathogen systems where vector-borne transmission is the primary route of infection, little or no attention has been paid to the relative importance of secondary or alternative routes of transmission. Here, by contrast, we report the results from a controlled longitudinal field-scale experiment in which the prevalence of fleas (Siphonaptera) was manipulated and the occurrence and distribution of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in a natural field vole (Microtus agrestis) population was monitored over a 2-year period. A non-systemic insecticide was applied to individual voles within two treatment grids and the prevalences of fleas and of T. microti were monitored on these and on two control grids. Blood samples were taken from all voles and PCR-based methods used to determine infection status. Insecticidal treatment was highly effective at reducing overall flea prevalence and recaptured animals (treated ca. 4 weeks previously) were very rarely infested (ca. 3%, compared with 50-70+% normally). On the other hand, the probability of trypanosome infection was reduced in treated animals on experimental grids to only around one-third of that normally observed. This suggests that direct, as opposed to flea-borne, transmission may not only occur, it may also be of epidemiological importance. The possibility that the importance of such transmission routes may have been underestimated in ‘vector-borne’ infections more generally is discussed.     

Processes leading to a spatial aggregation of Echinococcus multilocularis in its natural intermediate host Microtus arvalis

The small fox tapeworm (Echinococcus multilocularis) shows a heterogeneous spatial distribution in the intermediate host (Microtus arvalis). To identify the ecological processes responsible for this heterogeneity, we developed a spatially explicit simulation model. The model combines individual-based (foxes, Vulpes vulpes) and grid-based (voles) techniques to simulate the infections in both intermediate and definite host. If host populations are homogeneously mixed, the model reproduces field data for parasite prevalence only for a limited number of parameter combinations. As ecological parameters inevitably vary to a certain degree, we discarded the homogeneous mixing model as insufficient to gain insight into the ecology of the fox tapeworm cycle. We analysed five different model scenarios, each focussing on an ecological process that might be responsible for the heterogeneous spatial distribution of E. mulitlocularis in the intermediate host. Field studies revealed that the prevalence ratio between intermediate and definite host remains stable over a wide range of ecological conditions. Thus, by varying the parameters in simulation experiments, we used the robustness of the agreement between field data and model output as quality criterion for the five scenarios. Only one of the five scenarios was found to reproduce the prevalence ratio over a sufficient range of parameter combinations. In the accentuated scenario most tapeworm eggs die due to bad environmental conditions before they cause infections in the intermediate host. This scenario is supported by the known sensitivity of tapeworm eggs to high temperatures and dry conditions. The identified process is likely to lead to a heterogeneous availability of infective eggs and thus to a clumped distribution of infected intermediate hosts. In conclusion, areas with humid conditions and low temperatures must be pointed out as high risk areas for human exposure to E. multilocularis eggs as well.     

Prevalence and geographical distribution of the ear canker mite (Otodectes cynotis) among arctic foxes (Alopex lagopus) in Iceland

Three hundred forty five adult arctic foxes (Alopex lagopus) from all counties in Iceland were examined for excess cerumen and ear canker mites (Otodectes cynotis). Only 13 foxes (4%) from a single county in northwestern Iceland were infested, where the prevalence of otodectiasis was 38%. Whether or not this parasite is new to the arctic fox in Iceland is unknown. If it is recently introduced, possible sources of infestation are farmed silver foxes (Vulpes vulpes), domestic dogs, domestic or feral cats, and arctic foxes from Greenland. It appears that the rate of transmission between adult foxes is low; a more common route of transmission is probably from the mother to her offspring or between vixens breeding in the same dens in subsequent years by contamination of the dens. No correlation was found between the prevalence of mites in foxes and Samson character.     

New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain

Molecular techniques were used to examine the phylogenetic relationships among Hepatozoon species isolated from 13 foxes and 15 opossums from Brazil, and from 15 dogs, 20 foxes, 45 rodents, and 330 domestic cats from Spain. Hemogregarine infection was confirmed by amplification of the 18S rRNA gene and later sequencing. No hemogregarine infections were found in opossums. The prevalence of Hepatozoon in canids ranged from 26.6% (symptomatic domestic dogs) to 90% (Spanish foxes). Four different H. canis genotypes were detected, as well as an H. americanum-related protozoan (97% identical to the USA strain). Two Spanish cats were parasitized by a Hepatozoon species (0.6% prevalence) that showed 96% sequence identity to H. canis. DNA amplification assays performed on Spanish rodents showed 2 bank voles (Clethrionomys glareolus) to be infected by a Hepatozoon species (4.44% prevalence) with 95% sequence identity to Hepatozoon sp. from cats. Phylogenetic analysis showed Hepatozoon to be a monophyletic genus, in which species from carnivorous mammals (Hepatozoon sp. from cats, H. americanum and H. canis) appear as a sister lineage of that of lower vertebrates and rodents. This association suggests that H. americanum evolved in ticks and carnivores (either canids, or felids, or both) rather than in other ectoparasites and other types of mammal.     

Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus)

Toxoplasma gondii is a protozoan parasite that infects humans and animal species worldwide. The relative importance of each potential transmission route in the complex life cycle of this coccidia is largely unknown, due to the lack of studies taking into account all routes simultaneously. In this study, we analyzed the transmission of T. gondii in an urban population of stray cats captured between 1993 and 2004. Analyzing prevalence, our aim was to determine which factors influence transmission in this population. Specific anti-T. gondii IgG antibodies were detected using the modified agglutination test. Firstly, we analyzed the kinetics of antibody titers in cats captured several times, using mixed linear models and correspondence analysis. We showed that antibody titers did not vary significantly with time and that titer 40 was the best threshold to separate individuals into two serological groups. Overall, prevalence was only 18.6%, thus transmission of T. gondii is infrequent in this population. As expected, a highly significant association was detected between age and presence of IgG antibodies. Prevalence was lowest in kittens aged 3-4 months, suggesting that newborn kittens may carry maternal antibodies and that vertical transmission is rare. After taking into account the effect of age, logistic regression showed that antibody carriage was related to factors that possibly related to the survival of oocysts: localization in the study site, origin of the cats, maximal temperatures and rain. Our results suggest that in this population, vertical transmission is rare, low predation limits prevalence, and oocyst survival is a determining factor in the risk of infection. We discuss the more general importance of conditions determining oocyst survival in the life cycle of T. gondii.     

Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species

Spatial structure in the distribution of pathogen infection can influence both epidemiology and host-parasite coevolutionary processes. It may result from the spatial heterogeneity of intrinsic and extrinsic factors, or from the local population dynamics of hosts and parasites. In this study, we investigated the effects of landscape, host dispersal and demography (population abundance and phase of the fluctuation) on the distribution of a gastro-intestinal nematode Trichuris arvicolae in the fossorial water vole Arvicola terrestris sherman. This rodent exhibits outbreaks occurring regularly in Franche-Comté (France). Thirteen out-of-phase populations were studied in autumn 2003. They exhibited highly different T. arvicolae prevalences. The heterogeneity in prevalences was not explained by population structure, landscape or vole abundance, but by the phase of the vole population fluctuations. Populations at the end of the high density phase showed null prevalence whereas populations in increase or outbreak phases exhibited higher prevalences. Population genetic analyses based on microsatellites revealed significant differentiation between vole populations, and higher dispersal rates of young voles compared with old ones. These younger individuals were also infected more frequently than older voles. This suggested a role of host dispersal in the distribution of T. arvicolae. However, there was a strong discrepancy between the spatial patterns of prevalence and of host genetics or demographic phase. Genetic differentiation and differences in demographic phase exhibited significant spatial autocorrelations whereas prevalence did not. We concluded that the distribution of T. arvicolae is influenced by vole dispersal, although this effect might be overwhelmed by local adaptation processes or environmental conditions.     

An SIR pairwise epidemic model with infection age and demography

The demography and infection age play an important role in the spread of slowly progressive diseases. To investigate their effects on the disease spreading, we propose a pairwise epidemic model with infection age and demography on dynamic networks. The basic reproduction number of this model is derived. It is proved that there is a disease-free equilibrium which is globally asymptotically stable if the basic reproduction number is less that unity. Besides, sensitivity analysis is performed and shows that increasing the variance in recovery time and decreasing the variance in infection time can effectively control the diseases. The complex interaction between the death rate and equilibrium prevalence suggests that it is imperative to correctly estimate the parameters of demography in order to assess the disease transmission dynamics accurately. Moreover, numerical simulations show that the endemic equilibrium is globally asymptotically stable.     

Host and pathogen ecology drive the seasonal dynamics of a fungal disease,white-nose syndrome

Seasonal patterns in pathogen transmission can influence the impact of disease on populations and the speed of spatial spread. Increases in host contact rates or births drive seasonal epidemics in some systems, but other factors may occasionally override these influences. White-nose syndrome, caused by the emerging fungal pathogen Pseudogymnoascus destructans, is spreading across North America and threatens several bat species with extinction. We examined patterns and drivers of seasonal transmission of P. destructans by measuring infection prevalence and pathogen loads in six bat species at 30 sites across the eastern United States. Bats became transiently infected in autumn, and transmission spiked in early winter when bats began hibernating. Nearly all bats in six species became infected by late winter when infection intensity peaked. In summer, despite high contact rates and a birth pulse, most bats cleared infections and prevalence dropped to zero. These data suggest the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation. Our study is the first, to the best of our knowledge, to describe the seasonality of transmission in this emerging wildlife disease. The timing of infection and fungal growth resulted in maximal population impacts, but only moderate rates of spatial spread.