Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts – a field study in a high altitude lake

Understanding transmission is a critical prerequisite for predicting disease dynamics and impacts on host populations. It is well established that Batrachochytrium dendrobatidis (Bd), the amphibian fungal pathogen responsible for chytridiomycosis, can be transmitted directly, through physical contact with an infected host. However, indirect pathways of transmission remain poorly investigated. We conducted a five‐week long field infection experiment at a high altitude mountain lake in the French Pyrenees to investigate Bd transmission pathways in larval midwife toads Alytes obstetricans. Uninfected naïve tadpoles were co‐housed either with infected tadpoles (direct and indirect transmission) or with uninfected ones (indirect transmission only). We found that physical contact with an infected host is not necessary for initial infection with Bd and that all tadpoles became infected after only four weeks. However, physical contact with infected tadpoles led to a faster spread within a tadpole group and resulted in higher Bd loads and subsequently higher mortality. Our findings clearly demonstrate that in A. obstetricans, Bd can quickly spread in a population even without physical contact. Our experiment therefore stresses the importance of indirect transmission of Bd zoospores in infected lakes for disease dynamics, especially when a reservoir species such as A. obstetricans is present.     

Evidence for Transmission of Bluetongue Virus Serotype 26 through Direct Contact

The aim of this study was to assess the mechanisms of transmission of bluetongue virus serotype 26 (BTV-26) in goats. A previous study, which investigated the pathogenicity and infection kinetics of BTV-26 in goats, unexpectedly revealed that one control goat may have been infected through a direct contact transmission route. To investigate the transmission mechanisms of BTV-26 in more detail an experimental infection study was carried out in which three goats were infected with BTV-26, three goats were kept uninfected, but were housed in direct contact with the infected goats, and an additional four goats were kept in indirect contact separated from infected goats by metal gates. This barrier allowed the goats to have occasional face-to-face contact in the same airspace, but feeding, watering, sampling and environmental cleaning was carried out separately. The three experimentally infected goats did not show clinical signs of BTV, however high levels of viral RNA were detected and virus was isolated from their blood. At 21 dpi viral RNA was detected in, and virus was isolated from the blood of the three direct contact goats, which also seroconverted. The four indirect barrier contact goats remained uninfected throughout the duration of the experiment. In order to assess replication in a laboratory model species of Culicoides biting midge, more than 300 Culicoides sonorensis were fed a BTV-26 spiked blood meal and incubated for 7 days. The dissemination of BTV-26 in individual C. sonorensis was inferred from the quantity of virus RNA and indicated that none of the insects processed at day 7 possessed transmissible infections. This study shows that BTV-26 is easily transmitted through direct contact transmission between goats, and the strain does not seem to replicate in C. sonorensis midges using standard incubation conditions.     

Human Exposure to Particulate Matter Potentially Contaminated with Sin Nombre Virus

The most common mechanism for human exposure to hantaviruses throughout North America is inhalation of virally contaminated particulates. However, risk factors associated with exposure to particulates potentially contaminated with hantaviruses are generally not well understood. In North America, Sin Nombre virus (SNV) is the most common hantavirus that infects humans, causing hantavirus pulmonary syndrome, which has a significant mortality rate (approximately 35%). We investigated human exposure to particulate matter and evaluated the effects of season, location (sylvan and peridomestic environment), and activity (walking and sweeping) on generation of particulates at the breathing zone (1.5 m above the ground). We found greater volumes of small inhalable particulates during the spring and summer compared to the fall and winter seasons and greater volumes of small inhalable particulates produced in peridomestic, compared to sylvan, environments. Also, greater volumes of particulates were generated at the breathing zone while walking compared to sweeping. Results suggest that more aerosolized particles were generated during the spring and summer months. Our findings suggest that simply moving around in buildings is a significant source of human exposure to particulates, potentially contaminated with SNV, during spring and summer seasons. These findings could be advanced by investigation of what particle sizes SNV is most likely to attach to, and where in the respiratory tract humans become infected.     

A multi-structured epidemic problem with direct and indirect transmission in heterogeneous environments

In this work, we analyse a deterministic epidemic mathematical model motivated by the propagation of a hantavirus (Puumala hantavirus) within a bank vole population (Clethrionomys glareolus). The host population is split into juvenile and adult individuals. A heterogeneous spatial chronological age and infection age structure is considered, and also indirect transmission via the environment. Maturation rates for juvenile individuals are adult density-dependent. For the reaction–diffusion systems with age structures derived, we give global existence, uniqueness and global boundedness results. A model with transmission to humans is also studied here.     

Decrease of memory retention in a parasitic wasp: an effect of host manipulation by Wolbachia?

Several factors, such as cold exposure, aging, the number of experiences and viral infection, have been shown to affect learning ability in different organisms. Wolbachia has been found worldwide as an arthropod parasite/mutualist symbiont in a wide range of species, including insects. Differing effects have been identified on physiology and behavior by Wolbachia. However, the effect of Wolbachia infection on the learning ability of their host had never previously been studied. The current study carried out to compare learning ability and memory duration in 2 strains of the parasitoid Trichogramma brassicae: 1 uninfected and 1 infected by Wolbachia. Both strains were able to associate the novel odors with the reward of an oviposition into a host egg. However, the percentage of females that responded to the experimental design and displayed an ability to learn in these conditions was higher in the uninfected strain. Memory duration was longer in uninfected wasps (23.8 and 21.4 h after conditioning with peppermint and lemon, respectively) than in infected wasps (18.9 and 16.2 h after conditioning with peppermint and lemon, respectively). Memory retention increased in response to the number of conditioning sessions in both strains, but memory retention was always shorter in the infected wasps than in the uninfected ones. Wolbachia infection may select for reduced memory retention because shorter memory induces infected wasps to disperse in new environments and avoid competition with uninfected wasps by forgetting cues related to previously visited environments, thus increasing transmission of Wolbachia in new environments.     

Ecology of rodent-associated hantaviruses in the Southern Cone of South America: Argentina, Chile, Paraguay, and Uruguay

Thirteen hantavirus genotypes, associated with at least 12 sigmodontine reservoir rodents, have been recognized in the four countries that represent the Southern Cone of South America. Host-virus relationships are not as well defined as in North America; several Southern Cone hantaviruses appear to share a common host and some viruses do not occur throughout the range of their host. Although hantavirus-host relationships in the Southern Cone are less strictly concordant with the single-host-single-virus pattern reported elsewhere, recent studies suggest that much of the ambiguity may result from an incomplete understanding of host and hantavirus systematics. Although some Southern Cone host species are habitat generalists, some sympatric species are habitat specialists, helping to explain how some strict host-virus pairings may be maintained. In some cases, host population densities were higher in peridomestic habitats and prevalence of hantavirus infection was higher in host populations in peridomestic habitats. Seasonal and multiyear patterns in climate and human disturbance affect host population densities, prevalence of infection, and disease risk to humans. Unusually high hantavirus antibody prevalence in indigenous human populations may be associated with frequent and close contact with host rodents. Ongoing studies are improving our understanding of hantavirus-host ecology and providing tools that may predict human risk.     

Puumala hantavirus infection alters the odour attractiveness of its reservoir host

The random-mixing assumptions of many parasite-transmission models are challenged if healthy individuals can alter their behaviour to reduce their risk of infection. Some pathogens reduce the attractiveness of their hosts’ excretions, for example, potentially altering contact rates and thus the predicted force of infection for pathogens transmissible by contact with excretions. For bank voles (Myodes glareolus), contact with contaminated urine is an important route of transmission for Puumala hantavirus (PUUV); however, it is not known whether PUUV infection changes the voles’ urinary odours or their attractiveness. Here, we use a Y-maze to test whether PUUV infection alters the attractiveness of male bank voles’ urine. We presented wild-caught PUUV-free male and female bank voles with PUUV-infected conspecific urine, uninfected urine and a water control, and measured the relative and absolute latency to first visit, number of visits, and total time bank voles spent investigating each treatment over 30 min. PUUV infection significantly altered the bank voles’ initial response to conspecific urine, with fewer visits and less time spent close to infected urine relative to uninfected urine, and less total time spent near the infected urine than the uninfected urine or control. These strong preferences weakened over the 30-min trial, however, partly due to a general decline in male activity, and there were no absolute differences between the treatments overall. This suggests that PUUV infection does change the attractiveness of bank vole urine to conspecifics, and we discuss the implications of these results for random-mixing assumptions.     

Parasite‐induced Changes in the Anti‐predator Behavior of a Cricket Intermediate Host

Many parasites with complex life cycles are known to modify their host phenotype to enhance transmission from the intermediate host to the definitive host. Several earlier studies explored these effects in acanthocephalan and trematode parasites, especially in aquatic ecosystems; however, much less is known about parasite‐mediated alterations of host behavior in terrestrial systems involving nematodes. Here, we address this gap by investigating a trophically transmitted nematode (Pterygodermatites peromysci) that uses a camel cricket (Ceuthophilus pallidipes) as the intermediate host before transmission to the final host, the white‐footed mouse (Peromyscus leucopus). In a laboratory experiment, we quantified the anti‐predatory responses of the cricket intermediate host using simulated predator cues. Results showed a decrease in jumping performance among infected crickets as compared with uninfected crickets, specifically in terms of frequency of jumps and jumping distance. Additionally, the relationship between parasite load and frequency of jumps is negatively correlated with the intensity of infection. These behavioral modifications are likely to increase vulnerability to predation by the definitive host. An analysis of the age‐intensity pattern of infection in natural cricket populations appears to support this hypothesis: parasites accumulate with age, peak at an intermediate age class before the intensity of infection decreases in older age groups. We suggest that older, heavily infected crickets are preferentially removed from the population by predators because of increased vulnerability. These results show that cricket intermediate hosts infected with P. peromysci have diminished jumping performance, which is likely to impair their anti‐predatory behavior and potentially facilitate parasite transmission.     

Predators reduce Batrachochytrium dendrobatidis infection loads in their prey

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Deer mouse movements in peridomestic and sylvan settings in relation to Sin Nombre virus antibody prevalence

Prevalence of antibody to Sin Nombre virus (SNV) has been found to be nearly twice as high in deer mice (Peromyscus maniculatus) in peridomestic settings as in sylvan settings in two studies in Montana and one in New Mexico. We investigated whether this difference may be related to a difference in deer mouse movements in the two settings. We used radiotelemetry to determine home range size and length of movement for 22 sylvan (1991-1992) and 40 peridomestic deer mice (1995-1999). We also determined the percentage of locations inside versus outside of buildings for peridomestic mice. Though variable, average home range size for female deer mice was significantly smaller for peridomestic deer mice than for sylvan deer mice. The smaller home range in peridomestic settings may concentrate shed SNV, and protection from solar ultraviolet radiation inside buildings may increase environmental persistence of SNV. Both these factors could lead to increased SNV exposure of deer mice within peridomestic populations and result in higher antibody prevalence. Peridomestic deer mice moved between buildings and outside areas, which is evidence that SNV can be transmitted between peridomestic and sylvan populations.     

Genetic management of infectious diseases: a heterogeneous epidemio-genetic model illustrated with S. aureus mastitis

Given that individuals are genetically heterogeneous in their degree of resistance to infection, a model is proposed to formulate appropriate choices that will limit the spread of an infectious disease. The model is illustrated with data on S. aureus mastitis and is based on parameters characterizing the spread of the disease (contact rate, probability of infection after contact, and rate of recovery after infection), the demography (replacement and culling rates) and the genetic composition (degree of relationship and heritability of the disease trait) of the animal population. To decrease infection pressure, it is possible to apply non-genetic procedures that increase the culling (e.g., culling of chronically infected cows) and recovery (e.g., antibiotic therapy) rates of infected cows. But the contribution of the paper is to show that genetic management of infectious disease is also theoretically possible as a control measure complementary to non-genetic actions. Indeed, the probability for an uninfected individual to become infected after contact with an infected one is partially related to their degree of kinship: the more closely they are related, the more likely they are to share identical genes like those associated to the non-resistance to infection. Different prospective genetic management procedures are proposed to decrease the contact rate between infected and uninfected relatives and keep the number of secondary cases generated by one infected animal below 1.     

Ecology,Wolbachia infection frequency and mode of reproduction in the parasitoid wasp Tetrastichus coeruleus (Hymenoptera: Eulophidae)

Whereas sexual reproduction may facilitate adaptation to complex environments with many biotic interactions, simplified environments are expected to favour asexual reproduction. In agreement with this, recent studies on invertebrates have shown a prevalence of asexual species in agricultural (simplified) but not in natural (complex) environments. We investigated whether the same correlation between reproductive mode and habitat can be found in different populations within one species. The parasitoid wasp Tetrastichus coeruleus forms an ideal model to test this question, since it occurs both in natural and agricultural environments. Further, we investigated whether Wolbachia infection caused parthenogenesis in female‐biased populations. In contrast to the general pattern, in Dutch and French natural areas, we found Wolbachia‐infected, highly female‐biased populations that reproduce parthenogenetically. In contrast, populations on Dutch agricultural fields were not infected with Wolbachia, showed higher frequencies of males and reproduced sexually. However, we also found a female‐only, Wolbachia‐infected population on agricultural fields in north‐eastern United States. All Wolbachia‐infected populations were infected with the same Wolbachia strain. At this moment, we do not have a convincing explanation for this deviation from the general pattern of ecology and reproductive mode. It may be that asparagus agricultural fields differ from other crop fields in ways that favour sexual reproduction. Alternatively, Wolbachia may manipulate life history traits in its host, resulting in different fitness pay‐offs in different habitats. The fixation of Wolbachia in the United States populations (where the species was introduced) may be due to founder effect and lack of uninfected, sexual source populations.     

An optimal control problem for ovine brucellosis with culling

A mathematical model is used to study the dynamics of ovine brucellosis when transmitted directly from infected individual, through contact with a contaminated environment or vertically through mother to child. The model developed by Aïnseba et al. [A model for ovine brucellosis incorporating direct and indirect transmission, J. Biol. Dyn. 4 (2010), pp. 2–11. Available at http://www.math.u-bordeaux1.fr/～pmagal100p/papers/BBM-JBD09.pdf. Accessed 3 July 2012] was modified to include culling and then used to determine important parameters in the spread of human brucellosis using sensitivity analysis. An optimal control analysis was performed on the model to determine the best way to control such as a disease in the population. Three time-dependent controls to prevent exposure, cull the infected and reduce environmental transmission were used to set up to minimize infection at a minimum cost.     

Sex‐dependent infection causes nonadditive effects on kissing bug fecundity

The influence of parasites on host reproduction has been widely studied in natural and experimental conditions. Most studies, however, have evaluated the parasite impact on female hosts only, neglecting the contribution of males for host reproduction. This omission is unfortunate as sex‐dependent infection may have important implications for host–parasite associations. Here, we evaluate for the first time the independent and nonindependent effects of gender infection on host reproductive success using the kissing bug Mepraia spinolai and the protozoan Trypanosoma cruzi as model system. We set up four crossing treatments including the following: (1) both genders infected, (2) both genders uninfected, (3) males infected—females uninfected, and (4) males uninfected—females infected, using fecundity measures as response variables. Interactive effects of infection between sexes were prevalent. Uninfected females produced more and heavier eggs when crossed with uninfected than infected males. Uninfected males, in turn, sired more eggs and nymphs when crossed with uninfected than infected females. Unexpectedly, infected males sired more nymphs when crossed with infected than uninfected females. These results can be explained by the effect of parasitism on host body size. As infection reduced size in both genders, infection on one sex only creates body size mismatches and mating constraints that are not present in pairs with the same infection status. Our results indicate the fitness impact of parasitism was contingent on the infection status of genders and mediated by body size. As the fecundity impact of parasitism cannot be estimated independently for each gender, inferences based only on female host infection run the risk of providing biased estimates of parasite‐mediated impact on host reproduction.     

Microparasite transmission to <Emphasis Type="Italic">Daphnia magna</Emphasis> decreases in the presence of conspecifics

Single parasite species often have a range of different hosts which vary in their ability to sustain the parasite. When foraging for food, alternative hosts with similar feeding modes may compete for the infective stages of trophically transmitted parasites. If some of the infective stages end up in unsuitable hosts, transmission of the parasite to the focal host is decreased. I studied whether the presence of conspecifics alters the probability of an uninfected susceptible recipient Daphnia becoming infected by a microparasite and if this effect depends on whether the added conspecifics themselves are susceptible or resistant to infection. The presence of both susceptible and resistant conspecifics decreased the probability of infection in recipients. This effect was dependent on the density of the conspecifics but was not found to be related to their size. In addition, when Daphnia were placed in medium derived from crowded Daphnia populations, the probability of infection in recipients decreased as compared to that in standard medium. This implies that decreases in transmission probability are not caused by dilution of spores through food competition only, but also by indirect interference mediated through infochemicals released by Daphnia. Since Daphnia have been found to respond to crowding by decreasing their filtering rate, the decrease in transmission is probably caused by decreased intake of spores in crowded conditions. The presence of conspecifics can thus decrease microparasite transmission in Daphnia which may have important consequences for epidemiology and evolution of Daphnia parasites.     

Direct Transmission of a Hemoflagellate,Cryptobia salmositica (Kinetoplastida: Bodonina) Between Rainbow Trout Under Laboratory Conditions1

Transmission of Cryptobia salmositica occurred when infected and uninfected rainbow trout were held in the same tank. In tanks where infected and uninfected fish were allowed to mix freely, 67–80% of the uninfected fish acquired detectable infections by the 27th week. None of the control fish in another tank was infected. In another tank where the infected and uninfected fish were separated by a wire screen, 9 of 20 uninfected fish acquired detectable infections by the 22nd week. This is the first demonstration of direct transmission of a hemoflagellate via the water medium in aquatic vertebrates. Cryptobia salmositica was found in the mucus on the body surface of 9 of 10 fish examined 6 weeks after infection. These parasites were infective and some of them were morphologically similar to those in the blood or peritoneal fluid. It is suggested that the vascular species of Cryptobia were originally ectoparasitic on fishes and that these ectoparasitic species were descended from the free-living Procryptobia.     

Transmission Ecology of Sin Nombre Hantavirus in Naturally Infected North American Deermouse Populations in Outdoor Enclosures

Sin Nombre hantavirus (SNV), hosted by the North American deermouse (Peromyscus maniculatus), causes hantavirus pulmonary syndrome (HPS) in North America. Most transmission studies in the host were conducted under artificial conditions, or extrapolated information from mark-recapture data. Previous studies using experimentally infected deermice were unable to demonstrate SNV transmission. We explored SNV transmission in outdoor enclosures using naturally infected deermice. Deermice acquiring SNV in enclosures had detectable viral RNA in blood throughout the acute phase of infection and acquired significantly more new wounds (indicating aggressive encounters) than uninfected deermice. Naturally-infected wild deermice had a highly variable antibody response to infection, and levels of viral RNA sustained in blood varied as much as 100-fold, even in individuals infected with identical strains of virus. Deermice that infected other susceptible individuals tended to have a higher viral RNA load than those that did not infect other deermice. Our study is a first step in exploring the transmission ecology of SNV infection in deermice and provides new knowledge about the factors contributing to the increase of the prevalence of a zoonotic pathogen in its reservoir host and to changes in the risk of HPS to human populations. The techniques pioneered in this study have implications for a wide range of zoonotic disease studies.     

Trypanosoma cruzi-infected Rhodnius prolixus endure increased predation facilitating parasite transmission to mammal hosts

Triatomine bugs aggregate with conspecifics inside shelters during daylight hours. At dusk, they leave their refuges searching for hosts on which to blood feed. After finding a host, triatomines face the threat of being killed, because hosts often prey on them. As it is known that many parasites induce the predation of intermediate hosts to promote transmission, and that ingestion of Trypanosoma cruzi-infected bugs represents a very effective means for mammal infection, we hypothesized that trypanosomes induce infected bugs to take increased risk, and, as a consequence, be predated when approaching a host. Therefore, we evaluated whether the predation risk and predation rates endured by Rhodnius prolixus increase when infected with T. cruzi. Assays were performed in square glass arenas offering one central refuge to infected and uninfected 5^th instar nymphs. A caged mouse was introduced in each arena after a three-day acclimation interval to activate sheltered insects and induce them to approach it. As hypothesized, a significantly higher proportion of infected insects was predated when compared with uninfected ones (36% and 19%, respectively). Indeed, T. cruzi-infected bugs took higher risk (Approximation Index = 0.642) when compared with healthy ones (Approximation Index = 0.302) and remained outside the shelters when the host was removed from the arena. Our results show that infection by T. cruzi induces bugs to assume higher risk and endure higher predation rates. We reveal a hitherto unknown trypanosome-vector interaction process that increases infected bug predation, promoting increased rates of robust oral transmission. The significant consequences of the mechanism revealed here make it a fundamental component for the resilient maintenance of sylvatic, peridomestic and domestic cycles.     

Distinct Mechanisms Trigger Apoptosis in Human Immunodeficiency Virus Type 1-Infected and in Uninfected Bystander T Lymphocytes

Apoptosis is a main feature of AIDS pathogenesis and is thought to play a role in the progressive decrease of CD4⁺ T lymphocytes in infected individuals. To determine whether apoptosis occurs in infected and/or in uninfected peripheral blood T lymphocytes, we have used a recombinant human immunodeficiency virus type 1 (HIV-1) infectious clone expressing the green fluorescent protein (GFP). Using flow cytometry, we have determined the incidence of apoptosis by either terminal transferase dUTP nick end labeling or annexin-V assays in different cell subpopulations, i.e., in CD4⁺ or CD8⁺ T cells that were GFP positive or negative. After HIV-1 infection of purified peripheral blood lymphocytes, we observed that apoptosis occurred mostly in infected CD4⁺ peripheral blood lymphocytes. Remarkably, the presence of monocyte-derived macrophages in the culture increased dramatically the apoptosis of uninfected bystander T lymphocytes, while apoptosis in HIV-infected T lymphocytes was not changed. We therefore demonstrate that HIV-induced apoptosis results from at least two distinct mechanisms: (i) direct apoptosis in HIV-infected CD4⁺ T lymphocytes and (ii) indirect apoptosis in uninfected T cells mediated by antigen-presenting cells.     

Emergence of hantaviral disease in the southwestern United States.

Hantaviruses are parasites of small mammals, predominantly peridomestic and commensal rodents. They have a worldwide distribution. Hantavirus-related illness occurs in rural areas where humans come into contact with rodents. In most cases human infection is manifested by one of a variety of acute illnesses involving hemorrhagic fever and renal disease. In May 1993, a cluster of patients with an acute pulmonary disease with high mortality was noted in the Four Corners region of the southwestern United States. Serologic and genetic studies indicated that the etiologic agent was a novel hantavirus. The uncertainty engendered by the emergence of a new disease with high mortality forced a rapid response by state and federal agencies and by the University of New Mexico Medical Center, Albuquerque, where most patients from this region were referred. Considerable progress has been made in identifying infected cases on clinical and laboratory grounds and in ensuring that appropriate supportive care is made available to patients as soon as they are suspected of having hantaviral infection. Cases of hantavirus pulmonary syndrome--both new and retrospectively diagnosed--are still being recognized throughout the western United States. Many important questions remain unanswered.