Patrick Gasqui

Ecological Factors Characterizing the Prevalence of Bacterial Tick-Borne Pathogens in Ixodes ricinus Ticks in Pastures and Woodlands

ABSTRACT Ecological changes are recognized as an important driver behind the emergence of infectious diseases. The prevalence of infection in ticks depends upon ecological factors that are rarely taken into account simultaneously. Our objective was to investigate the influences of forest fragmentation, vegetation, adult tick hosts, and habitat on the infection prevalence of three tick-borne bacteria, Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, and Rickettsia sp. of the spotted fever group, in questing Ixodes ricinus ticks, taking into account tick characteristics. Samples of questing nymphs and adults were taken from 61 pastures and neighboring woodlands in central France. The ticks were tested by PCR of pools of nymphs and individual adults. The individual infection prevalence was modeled using multivariate regression. The highest infection prevalences were found in adult females collected in woodland sites for B. burgdorferi sensu lato and A. phagocytophilum (16.1% and 10.7%, respectively) and in pasture sites for Rickettsia sp. (8.7%). The infection prevalence in nymphs was lower than 6%. B. burgdorferi sensu lato was more prevalent in woodlands than in pastures. Forest fragmentation favored B. burgdorferi sensu lato and A. phagocytophilum prevalence in woodlands, and in pastures, the B. burgdorferi sensu lato prevalence was favored by shrubby vegetation. Both results are probably because large amounts of edges or shrubs increase the abundance of small vertebrates as reservoir hosts. The Rickettsia sp. prevalence was maximal on pasture with medium forest fragmentation. Female ticks were more infected by B. burgdorferi sensu lato than males and nymphs in woodland sites, which suggests an interaction between the ticks and the bacteria. This study confirms the complexity of the tick-borne pathogen ecology. The findings support the importance of small vertebrates as reservoir hosts and make a case for further studies in Europe on the link between the composition of the reservoir host community and the infection prevalence in ticks.

Anthropogenic factors and the risk of highly pathogenic avian influenza H5N1: prospects from a spatial-based model.

Beginning in 2003, highly pathogenic avian influenza (HPAI) H5N1 virus spread across Southeast Asia, causing unprecedented epidemics. Thailand was massively infected in 2004 and 2005 and continues today to experience sporadic outbreaks. While research findings suggest that the spread of HPAI H5N1 is influenced primarily by trade patterns, identifying the anthropogenic risk factors involved remains a challenge. In this study, we investigated which anthropogenic factors played a role in the risk of HPAI in Thailand using outbreak data from the “second wave” of the epidemic (3 July 2004 to 5 May 2005) in the country. We first performed a spatial analysis of the relative risk of HPAI H5N1 at the subdistrict level based on a hierarchical Bayesian model. We observed a strong spatial heterogeneity of the relative risk. We then tested a set of potential risk factors in a multivariable linear model. The results confirmed the role of free-grazing ducks and rice-cropping intensity but showed a weak association with fighting cock density. The results also revealed a set of anthropogenic factors significantly linked with the risk of HPAI. High risk was associated strongly with densely populated areas, short distances to a highway junction, and short distances to large cities. These findings highlight a new explanatory pattern for the risk of HPAI and indicate that, in addition to agro-environmental factors, anthropogenic factors play an important role in the spread of H5N1. To limit the spread of future outbreaks, efforts to control the movement of poultry products must be sustained.

Co-infection of Ticks: The Rule Rather Than the Exception

Introduction Ticks are the most common arthropod vectors of both human and animal diseases in Europe, and the Ixodes ricinus tick species is able to transmit a large number of bacteria, viruses and parasites. Ticks may also be co-infected with several pathogens, with a subsequent high likelihood of co-transmission to humans or animals. However few data exist regarding co-infection prevalences, and these studies only focus on certain well-known pathogens. In addition to pathogens, ticks also carry symbionts that may play important roles in tick biology, and could interfere with pathogen maintenance and transmission. In this study we evaluated the prevalence of 38 pathogens and four symbionts and their co-infection levels as well as possible interactions between pathogens, or between pathogens and symbionts. Methodology/principal findings A total of 267 Ixodes ricinus female specimens were collected in the French Ardennes and analyzed by high-throughput real-time PCR for the presence of 37 pathogens (bacteria and parasites), by rRT-PCR to detect the presence of Tick-Borne encephalitis virus (TBEV) and by nested PCR to detect four symbionts. Possible multipartite interactions between pathogens, or between pathogens and symbionts were statistically evaluated. Among the infected ticks, 45% were co-infected, and carried up to five different pathogens. When adding symbiont prevalences, all ticks were infected by at least one microorganism, and up to eight microorganisms were identified in the same tick. When considering possible interactions between pathogens, the results suggested a strong association between Borrelia garinii and B. afzelii, whereas there were no significant interactions between symbionts and pathogens. Conclusion/significance Our study reveals high pathogen co-infection rates in ticks, raising questions about possible co-transmission of these agents to humans or animals, and their consequences to human and animal health. We also demonstrated high prevalence rates of symbionts co-existing with pathogens, opening new avenues of enquiry regarding their effects on pathogen transmission and vector competence.

Risk factors for highly pathogenic avian influenza (HPAI) H5N1 infection in backyard chicken farms, Thailand

To reduce the risk of highly pathogenic avian influenza (HPAI) H5N1 infection in humans, the pathways by which HPAI is spread in poultry must be determined. Backyard poultry farmers are particularly vulnerable to the threat of HPAI, with both their health and livelihoods at risk. Identifying the risk factors for HPAI infection in backyard farms should allow control measures to be better targeted. To study the risk factors of HPAI H5N1 infection, we carried out a case-control study on backyard chicken farms in Thailand, analyzing 104 case farms and 382 control farms. Data on farming practices and environmental characteristics were analyzed using multivariate logistic regression models. We show that farms where owners bought live chickens from another backyard farm had a higher risk of HPAI H5N1 infection (OR 3.34, 95% CI 1.72-6.47), while those where owners used a disinfectant to clean poultry areas were exposed to lower risk (OR 0.48, 95% CI 0.26-0.87). Our results highlight the important role of the trade of poultry between farms in the transmission of HPAI H5N1, in addition to farming practices and environmental characteristics. Findings from this study may help to tailor prevention measures to the local circumstances of backyard farms in different regions of the world.

Which forest bird species are the main hosts of the tick, Ixodes ricinus, the vector of Borrelia burgdorferi sensu lato, during the breeding season?

Wild birds are important hosts for vector-borne pathogens, especially those borne by ticks. However, few studies have been conducted on the role of different bird species within a community as hosts of vector-borne pathogens. This study addressed individual and species factors that could explain the burden of Ixodes ricinus on forest birds during the reproductive periods of both vectors and hosts. The goal was to identify which bird species contribute the most to the tick population at the community level. Birds were mist-netted on four plots in 2008 and on seven plots in 2009 in two forests (Sénart and Notre Dame, near Paris, France). The dependence of the tick load per bird upon environmental conditions (questing nymph density, year and plot) and on host species traits (species, age, sex, body size, vertical space use, level of innate and acquired immunity) was analysed. Finally, the relative contribution of each bird species to the local dynamics of ticks was estimated, while accounting for their respective abundance. Tick burden differed markedly between bird species and varied according to questing nymph density. Bird species with a high body mass, those that forage low in the vegetation, and those that had a high innate immune response and a high spleen mass were more likely to have a high tick burden. Four species (the Common Blackbird, Turdus merula, the European Robin, Erithacus rubecula, the Song Thrush, Turdus philomelos, and the Winter Wren, Troglodytes troglodytes) hosted more than 90% of the ticks in the local bird community. These species, and particularly T. merula which was host to a high proportion of the nymphs, are likely to contribute significantly to the circulation of pathogens for which they are competent, such as the agent of Lyme borreliosis.

Introduced Siberian chipmunks (Tamias sibiricus barberi) contribute more to lyme borreliosis risk than native reservoir rodents.

The variation of the composition in species of host communities can modify the risk of disease transmission. In particular, the introduction of a new host species can increase health threats by adding a new reservoir and/or by amplifying the circulation of either exotic or native pathogens. Lyme borreliosis is a multi-host vector-borne disease caused by bacteria belonging to the Borrelia burgdorferi sensu lato complex. It is transmitted by the bite of hard ticks, especially Ixodes ricinus in Europe. Previous studies showed that the Siberian chipmunk, Tamias sibiricus barberi, an introduced ground squirrel in the Forest of Sénart (near Paris, France) was highly infested by I. ricinus, and consequently infected by B. burgdorferi sl. An index of the contribution of chipmunks to the density of infected questing nymphs on the vegetation (i.e., the acarological risk for humans) was compared to that of bank voles (Myodes glareolus) and of wood mice (Apodemus sylvaticus), two known native and sympatric competent reservoir hosts. Chipmunks produced nearly 8.5 times more infected questing nymphs than voles and mice. Furthermore, they contribute to a higher diversity of B. burgdorferi sl genospecies (B. afzelii, B. burgdorferi sensu stricto and B. garinii). The contribution of chipmunks varied between years and seasons, according to tick availability. As T. s. barberi must be a competent reservoir, it should amplify B. burgdorferi sl infection, hence increasing the risk of Lyme borreliosis in humans.

Environmental Factors Associated with the Seroprevalence of Toxoplasma gondii in Wild Boars (Sus scrofa), France

Toxoplasma gondii is a protozoan parasite infecting humans and animals. Wild boars Sus scrofa are a potential source of human infection and an appropriate biological model for analyzing T. gondii dynamics in the environment. Here, we aimed to identify environmental factors explaining the seroprevalence of toxoplasmosis in French wild boar populations. Considering 938 individuals sampled from 377 ‘communes’, overall seroprevalence was 23% (95% confidence interval: [22–24]). Using a Poisson regression, we found that the number of seropositive wild boars detected per ‘commune’ was positively associated with the presence of European wildcats (Felis silvestris) and moderate winter temperatures.

The importance of multiparasitism: examining the consequences of co-infections for human and animal health

Most parasites co-occur with other parasites, although the importance of such multiparasitism has only recently been recognised. Co-infections may result when hosts are independently infected by different parasites at the same time or when interactions among parasite species facilitate co-occurrence. Such interactions can have important repercussions on human or animal health because they can alter host susceptibility, infection duration, transmission risks, and clinical symptoms. These interactions may be synergistic or antagonistic and thus produce diverse effects in infected humans and animals. Interactions among parasites strongly influence parasite dynamics and therefore play a major role in structuring parasite populations (both within and among hosts) as well as host populations. However, several methodological challenges remain when it comes to detecting parasite interactions. The goal of this review is to summarise current knowledge on the causes and consequences of multiparasitism and to discuss the different methods and tools that researchers have developed to study the factors that lead to multiparasitism. It also identifies new research directions to pursue.

Local environmental factors characterizing Ixodes ricinus nymph abundance in grazed permanent pastures for cattle

Although Ixodes ricinus ticks are mainly associated with woodland, they are also present in open habitat such as pastures. The distribution of nymphal I. ricinus was monitored by drag sampling the vegetation in May-June 2003 on 61 grazed permanent pastures for cattle located in central France. After selecting explanatory variables from among a set of 155, tick abundance was modelled on the perimeter of the pasture using a negative binomial model that took into account data overdispersion. An abundant tree layer at the perimeter of the pasture associated with a high humidity before sampling greatly enhanced the average number of captured I. ricinus nymphs. The presence of apple or cherry trees around the pasture perimeter, the presence of trees or bushes at the pasture edge, woodland around the pasture and a high number of I. ricinus nymphs in the nearest woodland to the pasture were also favourable to nymph abundance in the pasture. The study highlighted that woodland vegetation associated with humidity and the presence of attractive foraging areas for tick hosts around the pasture played a key role in the abundance of I. ricinus. Finally, the results raised the question of whether and how transfer of ticks between woodland and grazed pastures occurs.

Prevalence of Anaplasma phagocytophilum, Rickettsia sp. and Borrelia burgdorferi sensu lato DNA in Questing Ixodes ricinus Ticks from France

Abstract:  A total of 4701 Ixodes ricinus, collected during the summer of 2003, were analyzed for three pathogens. DNA was detected from the three pathogens. Co‐detection of more than one pathogen was observed.