Identifying Transmission Cycles at the Human-Animal Interface: The Role of Animal Reservoirs in Maintaining Gambiense Human African Trypanosomiasis

Many infections can be transmitted between animals and humans. The epidemiological roles of different species can vary from important reservoirs to dead-end hosts. Here, we present a method to identify transmission cycles in different combinations of species from field data. We used this method to synthesise epidemiological and ecological data from Bipindi, Cameroon, a historical focus of gambiense Human African Trypanosomiasis (HAT, sleeping sickness), a disease that has often been considered to be maintained mainly by humans. We estimated the basic reproduction number of gambiense HAT in Bipindi and evaluated the potential for transmission in the absence of human cases. We found that under the assumption of random mixing between vectors and hosts, gambiense HAT could not be maintained in this focus without the contribution of animals. This result remains robust under extensive sensitivity analysis. When using the distributions of species among habitats to estimate the amount of mixing between those species, we found indications for an independent transmission cycle in wild animals. Stochastic simulation of the system confirmed that unless vectors moved between species very rarely, reintroduction would usually occur shortly after elimination of the infection from human populations. This suggests that elimination strategies may have to be reconsidered as targeting human cases alone would be insufficient for control, and reintroduction from animal reservoirs would remain a threat. Our approach is broadly applicable and could reveal animal reservoirs critical to the control of other infectious diseases.     

New tools for the study of animal trypanosomiasis in the Sudan: model-building of dangerous epidemiological passage by remote sensing geographic information systems

Recent studies in a rangeland area of Burkina Faso showed that riparian tsetse flies (Glossina tachinoides and G. palpalis gambiensis) were found along the main rivers, but depending on their location, they had different hosts and were not infected by the same trypanosomoses. There were different epidemiological situations within a distance of a few kilometres, and local assessment of the trypanosome risk thus called for a global approach taking account of the environmental and human factors involved in the interfaces between hosts and vectors. Various types of information concerning entomology, parasitology, ecology, land occupation and animal production systems were fed into a Geographical Information System. High spatial resolution remote sensing tools and original modelling methods were used to detect the valley landscapes most favourable to tsetse flies, and describe land use by herds. The impact of trypanosomes appeared to depend largely on animal movements, watering practices and the degree of contact with riparian tsetse flies. Linking these types of information revealed the most dangerous sites in epidemiological terms, which in this case represented some 18% of the network initially surveyed.     

Vector preference and host defense against infection interact to determine disease dynamics

Vector preference based on host infection status has long been recognized for its importance in disease dynamics. Prior theoretical work has assumed that all hosts are uniformly susceptible to the pathogen. Here we investigated disease dynamics when this assumption is relaxed using a series of vector–host epidemiological compartment models with variable levels of host resistance or tolerance to infection – collectively termed defense. In our models, vectors cannot acquire the infection from resistant hosts but can acquire from tolerant hosts. Specifically, we investigated the interacting effects of vector preference and host defense in a series of single‐ and two‐patch models. Results indicate that resistant host types generally reduce disease prevalence and pathogen spillover, independent of vector preference. The epidemiological consequences of host tolerance, however, depended on vector preference. When vectors preferred diseased hosts, tolerance reduced incidence compared to susceptible hosts; when vectors avoided diseased hosts, tolerance enhanced disease prevalence. Finally, a variation of the model that included preference‐based vector patch leaving rates suggests that both resistance and tolerance can promote pathogen spillover if vectors prefer diseased hosts, because of increased vector dispersal into susceptible patches. Collectively, we found complex, context‐dependent effects of vector preference and host defense on disease dynamics. In the context of management programs for vector‐borne diseases, managers should consider both the precise form of host defense present in a population, breed, or cultivar, as well as vector feeding behavior.     

Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens

Several floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.     

Estimating Contact Process Saturation in Sylvatic Transmission of Trypanosoma cruzi in the United States

Although it has been known for nearly a century that strains of Trypanosoma cruzi, the etiological agent for Chagas'' disease, are enzootic in the southern U.S., much remains unknown about the dynamics of its transmission in the sylvatic cycles that maintain it, including the relative importance of different transmission routes. Mathematical models can fill in gaps where field and lab data are difficult to collect, but they need as inputs the values of certain key demographic and epidemiological quantities which parametrize the models. In particular, they determine whether saturation occurs in the contact processes that communicate the infection between the two populations. Concentrating on raccoons, opossums, and woodrats as hosts in Texas and the southeastern U.S., and the vectors Triatoma sanguisuga and Triatoma gerstaeckeri, we use an exhaustive literature review to derive estimates for fundamental parameters, and use simple mathematical models to illustrate a method for estimating infection rates indirectly based on prevalence data. Results are used to draw conclusions about saturation and which population density drives each of the two contact-based infection processes (stercorarian/bloodborne and oral). Analysis suggests that the vector feeding process associated with stercorarian transmission to hosts and bloodborne transmission to vectors is limited by the population density of vectors when dealing with woodrats, but by that of hosts when dealing with raccoons and opossums, while the predation of hosts on vectors which drives oral transmission to hosts is limited by the population density of hosts. Confidence in these conclusions is limited by a severe paucity of data underlying associated parameter estimates, but the approaches developed here can also be applied to the study of other vector-borne infections.     

Multiscale analysis for a vector-borne epidemic model

Traditional studies about disease dynamics have focused on global stability issues, due to their epidemiological importance. We study a classical SIR-SI model for arboviruses in two different directions: we begin by describing an alternative proof of previously known global stability results by using only a Lyapunov approach. In the sequel, we take a different view and we argue that vectors and hosts can have very distinctive intrinsic time-scales, and that such distinctiveness extends to the disease dynamics. Under these hypothesis, we show that two asymptotic regimes naturally appear: the fast host dynamics and the fast vector dynamics. The former regime yields, at leading order, a SIR model for the hosts, but with a rational incidence rate. In this case, the vector disappears from the model, and the dynamics is similar to a directly contagious disease. The latter yields a SI model for the vectors, with the hosts disappearing from the model. Numerical results show the performance of the approximation, and a rigorous proof validates the reduced models.     

New tools for epidemiology: a space odyssey

Geographical Information Systems (GIS) facilitate access to epidemiological data through visualization and may be consulted for the development of mathematical models and analysis by spatial statistics. Variables such as land-cover, land-use, elevations, surface temperatures, rainfall etc. emanating from earth-observing satellites, complement GIS as this information allows the analysis of disease distribution based on environmental characteristics. The strength of this approach issues from the specific environmental requirements of those causative infectious agents, which depend on intermediate hosts for their transmission. The distribution of these diseases is restricted, both by the environmental requirements of their intermediate hosts/vectors and by the ambient temperature inside these hosts, which effectively govern the speed of maturation of the parasite. This paper discusses the current capabilities with regard to satellite data collection in terms of resolution (spatial, temporal and spectral) of the sensor instruments on board drawing attention to the utility of computer-based models of the Earth for epidemiological research. Virtual globes, available from Google and other commercial firms, are superior to conventional maps as they do not only show geographical and man-made features, but also allow instant import of data-sets of specific interest, e.g. environmental parameters, demographic information etc., from the Internet.     

Spatial trypanosomosis management: from data-layers to decision making

The use of geographical information systems (GIS) in the management of African animal trypanosomosis in sub-Saharan Africa offers potential in assisting decisions on allocation of resources, prioritization of control areas, and planning and management of field operations. Here, Guy Hendrickx and colleagues review approaches being used to develop reliable data-layers and to incorporate these data into GIS models. They argue that techniques should be further refined to produce more-detailed data layers and to include a dynamic element, a problem rarely addressed until now.     

High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex pipiens)

Avian malaria studies have taken a prominent place in different aspects of evolutionary ecology. Despite a recent interest in the role of vectors within the complex interaction system of the malaria parasite, they have largely been ignored in most epidemiological studies. Epidemiology of the disease is however strongly related to the vector's ecology and behaviour, and there is a need for basic investigations to obtain a better picture of the natural associations between Plasmodium lineages, vector species and bird hosts. The aim of the present study was to identify the mosquito species involved in the transmission of the haemosporidian parasites Plasmodium spp. in two wild populations of breeding great tits (Parus major) in western Switzerland. Additionally, we compared Plasmodium lineages, based on mitochondrial DNA cytochrome b sequences, between the vertebrate and dipteran hosts, and evaluated the prevalence of the parasite in the mosquito populations. Plasmodium spp. were detected in Culex pipiens only, with an overall 6.6% prevalence. Among the six cytochrome b lineages of Plasmodium identified in the mosquitoes, three were also present in great tits. The results provide evidence for the first time that C. pipiens can act as a natural vector of avian malaria in Europe and yield baseline data for future research on the epidemiology of avian malaria in European countries.     

Some general aspects of the distribution and epidemiology of bovine trypanosomosis in southern Africa

Bovine trypanosomosis occurs in vast areas of southern Africa. Its epidemiology and impact on cattle production is determined largely by the level of interaction between tsetse and cattle. Four situations can be distinguished. First, areas where cattle are absent. Second, zones where cattle have been introduced in game areas but where game is still abundant and constitutes the major source of food for tsetse. Third, areas where, often because of human interference, the density of game animals is low and cattle constitute the main source of food and finally, areas where cattle occur at the edge of tsetse-infested zones. In southern Africa, the impact of the disease on cattle production varies according to the epidemiological circumstances. The disease has an epidemic character with significant impacts on production in areas where cattle have been introduced recently or along the interface between tsetse-infested game areas and tsetse-free cultivated areas. Bovine trypanosomosis has an endemic character, with little impact on production, in areas where tsetse mainly feed on cattle and where the invasion of tsetse is low. Options for the control of bovine trypanosomosis will vary according to the epidemiological circumstance. In particular, the control of tsetse with insecticide-treated cattle will only be effective when a large proportion of feeds are taken from cattle over a large area and when the invasion of tsetse can be reduced sufficiently.     

Colorado animal‐based plague surveillance systems: relationships between targeted animal species and prediction efficacy of areas at risk for humans

Human plague risks (Yersinia pestis infection) are greatest when epizootics cause high mortality among this bacterium's natural rodent hosts. Therefore, health departments in plague‐endemic areas commonly establish animal‐based surveillance programs to monitor Y. pestis infection among plague hosts and vectors. The primary objectives of our study were to determine whether passive animal‐based plague surveillance samples collected in Colorado from 1991 to 2005 were sampled from high human plague risk areas and whether these samples provided information useful for predicting human plague case locations. By comparing locations of plague‐positive animal samples with a previously constructed GIS‐based plague risk model, we determined that the majority of plague‐positive Gunnison's prairie dogs (100%) and non‐prairie dog sciurids (85.82%), and moderately high percentages of sigmodontine rodents (71.4%), domestic cats (69.3%), coyotes (62.9%), and domestic dogs (62.5%) were recovered within 1 km of the nearest area posing high peridomestic risk to humans. In contrast, the majority of white‐tailed prairie dog (66.7%), leporid (cottontailed and jack rabbits) (71.4%), and black‐tailed prairie dog (93.0%) samples originated more than 1 km from the nearest human risk habitat. Plague‐positive animals or their fleas were rarely (one of 19 cases) collected within 2 km of a case exposure site during the 24 months preceding the dates of illness onset for these cases. Low spatial accuracy for identifying epizootic activity prior to human plague cases suggested that other mammalian species or their fleas are likely more important sources of human infection in high plague risk areas. To address this issue, epidemiological observations and multi‐locus variable number tandem repeat analyses (MLVA) were used to preliminarily identify chipmunks as an under‐sampled, but potentially important, species for human plague risk in Colorado.     

Spatio-temporal distribution of tsetse and other biting flies in the Mouhoun River basin, Burkina Faso

In the Mouhoun River basin, Burkina Faso, the main vectors of African animal trypanosomoses are Glossina palpalis gambiensis Vanderplank and Glossina tachinoides Westwood (Diptera: Glossinidae), both of which are riverine tsetse species. The aim of our study was to understand the impact of landscape anthropogenic changes on the seasonal dynamics of vectors and associated trypanosomosis risk. Three sites were selected on the basis of the level of disturbance of tsetse habitats and predominant tsetse species: disturbed (Boromo, for G. tachinoides) and half-disturbed (Douroula for G. tachinoides and Kadomba for G. p. gambiensis). At each of these sites, seasonal variations in the apparent densities of tsetse and mechanical vectors and tsetse infection rates were monitored over 17 months. Tsetse densities differed significantly between sites and seasons. Of 5613 captured tsetse, 1897 were dissected; 34 of these were found to be infected with trypanosomes. The most frequent infection was Trypanosoma vivax (1.4%), followed by Trypanosoma congolense (0.3%) and Trypanosoma brucei (0.05%). The mean physiological age of 703 tsetse females was investigated to better characterize the transmission risk. Despite the environmental changes, it appeared that tsetse lived long enough to transmit trypanosomes, especially in half-disturbed landscapes. A total of 3021 other biting flies from 15 species (mainly Tabanidae and Stomoxyinae) were also caught: their densities also differed significantly among sites and seasons. Their relative importance regarding trypanosome transmission is discussed; the trypanosomosis risk in cattle was similar at all sites despite very low tsetse densities (but high mechanical vector densities) in one of them.     

Molecular detection of Megatrypanum trypanosomes in tabanid flies

Trypanosomes of the subgenus Megatrypanum have been isolated from many mammalian hosts around the world. They are usually non-pathogenic, although they may confuse the parasitological diagnosis of trypanosomosis. Additionally, Trypanosoma theileri has been associated with disease in cattle. Megatrypanum trypanosomes are considered to be transmitted by different arthropods, including tabanids. However, little is known about the potential vectors of Megatrypanum trypanosomes in different parts of the world. The present study reports on the detection of Megatrypanum trypanosomes in Heamatopota pluvialis, Tabanus bromius, Tabanus maculicornis and Tabanus distinguendus in Poland. It also discusses the possible role of these tabanids in the transmission of Megatrypanum trypanosomes.     

An emerging hemorrhagic fever in China caused by a novel bunyavirus SFTSV

Severe fever with thrombocytopenia syndrome(SFTS) is an emerging hemorrhagic fever in rural areas of China and is caused by a new bunyavirus,SFTSV,named after the disease.The transmission vectors and animal hosts of SFTSV are unclear.Ticks are the most likely transmission vectors and domestic animals,including goats,dogs,and cattle,are potential amplifying hosts of SFTSV.The clinical symptoms of SFTS are nonspecific,but major symptoms include fever,gastrointestinal symptoms,myalgia,dizziness,joint pain,chills,and regional lymphadenopathy.The most common abnormalities in laboratory test results are thrombocytopenia(95%),leukocytopenia(86%),and elevated levels of serum alanine aminotransferase,aspartate aminotransferase,creatine kinase,and lactate dehydrogenase.The fatality rate for SFTS is 12% on average,and the annual incidence of the disease is approximately five per 100000 of the rural population.     

Human activities and American trypanosomiasis. Review of the literature

Trypanosoma cruzi, the causative agent of American trypanosomiasis (Chagas disease) is a parasite of wild mammals of Americas. It has been further transmitted to man through an insect vector belonging to the Reduviidae family. In the context of an ecoepidemiological study of this vector borne anthropozoonosis, a medical anthropological overview tries, by using data from literature, to clarify the different ways human activities play on the disease epidemiological cycle. The everyday human activities support domiciliation of triatomine bugs. But, the human intervention in the natural environment disturbs strongly the ecology of the vectors or hosts and leads to a new structuring of the natural foci of the disease with its displacement toward the human environment. The way society or individuals manage the disease plays also an important role. Some human activities, as building dwelling structures, have been well studied, but some others, such as the real impact of the human modes of production, are less known. A medical anthropology study of the role of human activities on the foci of Chagas disease is still needed.     

Mechanisms of arthropod transmission of plant and animal viruses.

A majority of the plant-infecting viruses and many of the animal-infecting viruses are dependent upon arthropod vectors for transmission between hosts and/or as alternative hosts. The viruses have evolved specific associations with their vectors, and we are beginning to understand the underlying mechanisms that regulate the virus transmission process. A majority of plant viruses are carried on the cuticle lining of a vector's mouthparts or foregut. This initially appeared to be simple mechanical contamination, but it is now known to be a biologically complex interaction between specific virus proteins and as yet unidentified vector cuticle-associated compounds. Numerous other plant viruses and the majority of animal viruses are carried within the body of the vector. These viruses have evolved specific mechanisms to enable them to be transported through multiple tissues and to evade vector defenses. In response, vector species have evolved so that not all individuals within a species are susceptible to virus infection or can serve as a competent vector. Not only are the virus components of the transmission process being identified, but also the genetic and physiological components of the vectors which determine their ability to be used successfully by the virus are being elucidated. The mechanisms of arthropod-virus associations are many and complex, but common themes are beginning to emerge which may allow the development of novel strategies to ultimately control epidemics caused by arthropod-borne viruses.     

Development of a pHrodo-Based Assay for the Assessment of In Vitro and In Vivo Erythrophagocytosis during Experimental Trypanosomosis

Extracellular trypanosomes can cause a wide range of diseases and pathological complications in a broad range of mammalian hosts. One common feature of trypanosomosis is the occurrence of anemia, caused by an imbalance between erythropoiesis and red blood cell clearance of aging erythrocytes. In murine models for T. brucei trypanosomosis, anemia is marked by a very sudden non-hemolytic loss of RBCs during the first-peak parasitemia control, followed by a short recovery phase and the subsequent gradual occurrence of an ever-increasing level of anemia. Using a newly developed quantitative pHrodo based in vitro erythrophagocytosis assay, combined with FACS-based ex vivo and in vivo results, we show that activated liver monocytic cells and neutrophils as well as activated splenic macrophages are the main cells involved in the occurrence of the early-stage acute anemia. In addition, we show that trypanosomosis itself leads to a rapid alteration of RBC membrane stability, priming the cells for accelerated phagocytosis.     

Molecular crosstalks in Leishmania-sandfly-host relationships

Sandflies (Diptera: Phlebotominael are vectors of Leishmania parasites, causative agents of important human and animal diseases with diverse manifestations. This review summarizes present knowledge about the vectorial part of Leishmania life cycle and parasite transmission to the vertebrate host. Particularly, it focuses on molecules that determine the establishment of parasite infection in sandfly midgut. It describes the concept of specific versus permissive sandfly vectors, explains the epidemiological consequences of broad susceptibility of permissive sandflies and demonstrates that genetic exchange may positively affect Leishmania fitness in the vector. Last but not least, the review describes recent knowledge about circulating antibodies produced by hosts in response to sandfly bites. Studies on specificity and kinetics of antibody response revealed that anti-saliva IgG could be used as a marker of host exposure to sandflies, i.e. as a useful tool for evaluation of vector control.     

Ecological interactions in the transmission of the leishmaniases

Epidemiological studies on the leishmaniases are disclosing a multiplicity of Leishmania species infecting a wide range of wild mammalian hosts, from marsupials to monkeys. In the primitive, silvatic habitat these parasites are transmitted by an equally wide variety of phlebotomine sandfly species (Diptera: Psychodidae: Phlebotominae). Transmission is not haphazard, however, and available evidence points to the existence of environmental barriers that normally limit the different Leishmania species to specific sandfly vectors, transmitting to certain mammalian species, within distinct ecotopes. In this situation, humans may become infected by a variety of leishmanial parasites when intruding into the different enzootics, if the sandfly vectors are anthropophilic. Many are not, however, and their parasites rarely, if ever, make contact with the human host. Natural or man-made ecological changes may result in modification of the epidemiological pattern of leishmaniasis, leading to either a reduction or an increase in the human disease.     

Trypanosoma vivax Infections: Pushing Ahead with Mouse Models for the Study of Nagana. I. Parasitological,Hematological and Pathological Parameters

African trypanosomiasis is a severe parasitic disease that affects both humans and livestock. Several different species may cause animal trypanosomosis and although Trypanosoma vivax (sub-genus Duttonella) is currently responsible for the vast majority of debilitating cases causing great economic hardship in West Africa and South America, little is known about its biology and interaction with its hosts. Relatively speaking, T. vivax has been more than neglected despite an urgent need to develop efficient control strategies. Some pioneering rodent models were developed to circumvent the difficulties of working with livestock, but disappointedly were for the most part discontinued decades ago. To gain more insight into the biology of T. vivax, its interactions with the host and consequently its pathogenesis, we have developed a number of reproducible murine models using a parasite isolate that is infectious for rodents. Firstly, we analyzed the parasitical characteristics of the infection using inbred and outbred mouse strains to compare the impact of host genetic background on the infection and on survival rates. Hematological studies showed that the infection gave rise to severe anemia, and histopathological investigations in various organs showed multifocal inflammatory infiltrates associated with extramedullary hematopoiesis in the liver, and cerebral edema. The models developed are consistent with field observations and pave the way for subsequent in-depth studies into the pathogenesis of T. vivax - trypanosomosis.