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Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters.

ABSTRACT: The human T-lymphotropic viruses (HTLVs) types 1 and 2 originated independently and are related to distinct lineages of simian T-lymphotropic viruses (STLV-1 and STLV-2, respectively). These facts, along with the finding that HTLV-1 diversity appears to have resulted from multiple cross-species transmissions of STLV-1, suggest that contact between humans and infected nonhuman primates (NHPs) may result in HTLV emergence. We investigated the diversity of HTLV among central Africans reporting contact with NHP blood and body fluids through hunting, butchering, and keeping primate pets. We show that this population is infected with a wide variety of HTLVs, including two previously unknown retroviruses: HTLV-4 is a member of a phylogenetic lineage that is distinct from all known HTLVs and STLVs; HTLV-3 falls within the phylogenetic diversity of STLV-3, a group not previously seen in humans. We also document human infection with multiple STLV-1-like viruses. These results demonstrate greater HTLV diversity than previously recognized and suggest that NHP exposure contributes to HTLV emergence. Our discovery of unique and divergent HTLVs has implications for HTLV diagnosis, blood screening, and potential disease development in infected persons. The findings also indicate that cross-species transmission is not the rate-limiting step in pandemic retrovirus emergence and suggest that it may be possible to predict and prevent disease emergence by surveillance of populations exposed to animal reservoirs and interventions to decrease risk factors, such as primate hunting.

SUBMITTER: Wolfe ND

PROVIDER: S-EPMC1142377 | biostudies-literature | 2005 May

REPOSITORIES: biostudies-literature

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Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters.

Wolfe Nathan D ND Heneine Walid W Carr Jean K JK Garcia Albert D AD Shanmugam Vedapuri V Tamoufe Ubald U Torimiro Judith N JN Prosser A Tassy AT Lebreton Matthew M Mpoudi-Ngole Eitel E McCutchan Francine E FE Birx Deborah L DL Folks Thomas M TM Burke Donald S DS Switzer William M WM

Proceedings of the National Academy of Sciences of the United States of America 20050523 22

The human T-lymphotropic viruses (HTLVs) types 1 and 2 originated independently and are related to distinct lineages of simian T-lymphotropic viruses (STLV-1 and STLV-2, respectively). These facts, along with the finding that HTLV-1 diversity appears to have resulted from multiple cross-species transmissions of STLV-1, suggest that contact between humans and infected nonhuman primates (NHPs) may result in HTLV emergence. We investigated the diversity of HTLV among central Africans reporting cont ...[more]

PMID: 15911757

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Project description:Simian T-lymphotropic virus 1 (STLV-1) enters human populations through contact with nonhuman primate (NHP) bushmeat. We tested whether differences in the extent of contact with STLV-1-infected NHP bushmeat foster regional differences in prevalence of human T-lymphotropic virus 1 (HTLV-1). Using serological and PCR assays, we screened humans and NHPs at two Sub-Saharan African sites where subsistence hunting was expected to be less (Taï region, Côte d'Ivoire [CIV]) or more (Bandundu region, Democratic Republic of the Congo [DRC]) developed. Only 0.7% of human participants were infected with HTLV-1 in CIV (n = 574), and 1.3% of humans were infected in DRC (n = 302). Two of the Ivorian human virus sequences were closely related to simian counterparts, indicating ongoing zoonotic transmission. Multivariate analysis of human demographic parameters and behavior confirmed that participants from CIV were less often exposed to NHPs than participants from DRC through direct contact, e.g., butchering. At the same time, numbers of STLV-1-infected NHPs were higher in CIV (39%; n = 111) than in DRC (23%; n = 39). We conclude that similar ultimate risks of zoonotic STLV-1 transmission-defined as the product of prevalence in local NHP and human rates of contact to fresh NHP carcasses-contribute to the observed comparable rates of HTLV-1 infection in humans in CIV and DRC. We found that young adult men and mature women are most likely exposed to NHPs at both sites. In view of the continued difficulties in controlling zoonotic disease outbreaks, the identification of such groups at high risk of NHP exposure may guide future prevention efforts.IMPORTANCE Multiple studies report a high risk for zoonotic transmission of blood-borne pathogens like retroviruses through contact with NHPs, and this risk seems to be particularly high in tropical Africa. Here, we reveal high levels of exposure to NHP bushmeat in two regions of Western and Central tropical Africa. We provide evidence for continued zoonotic origin of HTLV-1 in humans at CIV, and we found that young men and mature women represent risk groups for zoonotic transmission of pathogens from NHPs. Identifying such risk groups can contribute to mitigation of not only zoonotic STLV-1 transmission but also transmission of any blood-borne pathogen onto humans in Sub-Saharan Africa.

Project description:Landscapes in many developing countries consist of a heterogeneous matrix of mixed agriculture and forest. Many of the generalist species in this matrix are increasingly traded in the bushmeat markets of West and Central Africa. However, to date there has been little quantification of how the spatial configuration of the landscape influences the urban bushmeat trade over time. As anthropogenic landscapes become the face of rural West Africa, understanding the dynamics of these systems has important implications for conservation and landscape management. The bushmeat production of an area is likely to be defined by landscape characteristics such as habitat disturbance, hunting pressure, level of protection, and distance to market. We explored (SSG, tense) the role of these four characteristics in the spatio-temporal dynamics of the commercial bushmeat trade around the city of Kumasi, Ghana, over 27 years (1978 to 2004). We used geographic information system methods to generate maps delineating the spatial characteristics of the landscapes. These data were combined with spatially explicit market data collected in the main fresh bushmeat market in Kumasi to explore the relationship between trade volume (measured in terms of number of carcasses) and landscape characteristics. Over time, rodents, specifically cane rats (Thryonomys swinderianus), became more abundant in the trade relative to ungulates and the catchment area of the bushmeat market expanded. Areas of intermediate disturbance supplied more bushmeat, but protected areas had no effect. Heavily hunted areas showed significant declines in bushmeat supply over time. Our results highlight the role that low intensity, heterogeneous agricultural landscapes can play in providing ecosystem services, such as bushmeat, and therefore the importance of incorporating bushmeat into ecosystem service mapping exercises. Our results also indicate that even where high bushmeat production is possible, current harvest levels may cause wildlife depletion.

Dataset Information

Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters.

Publications

Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters.

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