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

Nathan D. Wolfe, Walid Heneine, Jean K. Carr, Albert D. Garcia, Vedapuri Shanmugam, Ubald Tamoufe, Judith N. Torimiro, A. Tassy Prosser, Matthew LeBreton, Eitel Mpoudi-Ngole, Francine E. McCutchan, Deborah L. Birx, Thomas M. Folks, Donald S. Burke, William M. Switzer

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)7994-7999
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume102
Issue number22
DOIs
StatePublished - May 31 2005

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Primates
Viruses
Simian T-lymphotropic virus 1
Human T-lymphotropic virus 1
Retroviridae
Simian T-lymphotropic virus 2
Simian T-lymphotropic virus 3
Human T-lymphotropic virus 3
Population Surveillance
Human T-lymphotropic virus 2
Pets
Body Fluids
Pandemics

Keywords

  • Diversity
  • Exposures
  • Retrovirus
  • Simian
  • Zoonosis

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. / Wolfe, Nathan D.; Heneine, Walid; Carr, Jean K.; Garcia, Albert D.; Shanmugam, Vedapuri; Tamoufe, Ubald; Torimiro, Judith N.; Prosser, A. Tassy; LeBreton, Matthew; Mpoudi-Ngole, Eitel; McCutchan, Francine E.; Birx, Deborah L.; Folks, Thomas M.; Burke, Donald S.; Switzer, William M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, No. 22, 31.05.2005, p. 7994-7999.

Research output: Contribution to journalArticle

Wolfe, ND, Heneine, W, Carr, JK, Garcia, AD, Shanmugam, V, Tamoufe, U, Torimiro, JN, Prosser, AT, LeBreton, M, Mpoudi-Ngole, E, McCutchan, FE, Birx, DL, Folks, TM, Burke, DS & Switzer, WM 2005, 'Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters', Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 22, pp. 7994-7999. https://doi.org/10.1073/pnas.0501734102
Wolfe, Nathan D. ; Heneine, Walid ; Carr, Jean K. ; Garcia, Albert D. ; Shanmugam, Vedapuri ; Tamoufe, Ubald ; Torimiro, Judith N. ; Prosser, A. Tassy ; LeBreton, Matthew ; Mpoudi-Ngole, Eitel ; McCutchan, Francine E. ; Birx, Deborah L. ; Folks, Thomas M. ; Burke, Donald S. ; Switzer, William M. / Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. In: Proceedings of the National Academy of Sciences of the United States of America. 2005 ; Vol. 102, No. 22. pp. 7994-7999.
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AU - Shanmugam, Vedapuri

AU - Tamoufe, Ubald

AU - Torimiro, Judith N.

AU - Prosser, A. Tassy

AU - LeBreton, Matthew

AU - Mpoudi-Ngole, Eitel

AU - McCutchan, Francine E.

AU - Birx, Deborah L.

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AU - Burke, Donald S.

AU - Switzer, William M.

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N2 - 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.

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