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Emergence of Unique Primate T-Lymphotropic Viruses Among Central African Bushmeat Hunters

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Emergence of Unique Primate T-Lymphotropic Viruses Among Central African Bushmeat Hunters 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*ʈ, Judith N. Torimiroʈ, A. Tassy Prosser†, Matthew LeBretonʈ, Eitel Mpoudi-Ngoleʈ, Francine E. McCutchan*¶, Deborah L. Birx**, Thomas M. Folks§, Donald S. Burke*†, and William M. Switzer§†† Departments of *Epidemiology, †International Health, and ‡Molecular Microbiology and Immunology, Bloomberg School of Public Health, The Johns Hopkins University, Baltimore, MD 21205; §Laboratory Branch, Division of HIV͞AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA 30333; ¶Henry M. Jackson Foundation, Rockville, MD 20850; ʈArmy Health Research Center, Yaounde, Cameroon; and **Walter Reed Army Institute of Research, Rockville, MD 20850 Edited by John M. Coffin, Tufts University School of Medicine, Boston, and approved April 11, 2005 (received for review March 2, 2005) The human T-lymphotropic viruses (HTLVs) types 1 and 2 origi- There has been no evidence that STLVs cross into people nated independently and are related to distinct lineages of simian occupationally exposed to NHPs in laboratories and primate T-lymphotropic viruses (STLV-1 and STLV-2, respectively). These centers, as has been documented for other primate retroviruses, facts, along with the finding that HTLV-1 diversity appears to have including simian immunodeficiency virus, simian foamy virus resulted from multiple cross-species transmissions of STLV-1, sug- (SFV), and simian type D retrovirus (12–15). Nevertheless, gest that contact between humans and infected nonhuman pri- zoonotic transmission of STLV to human populations naturally mates (NHPs) may result in HTLV emergence. We investigated the exposed to NHPs through hunting or butchering, similar to that diversity of HTLV among central Africans reporting contact with recently reported for SFV in African hunters (16), would be of NHP blood and body fluids through hunting, butchering, and particular public health significance because of the transmissible keeping primate pets. We show that this population is infected and pathogenic nature of this group of viruses among humans. with a wide variety of HTLVs, including two previously unknown Previous studies have not documented evidence of HTLV retroviruses: HTLV-4 is a member of a phylogenetic lineage that is outside the PTLV-1 and PTLV-2 groups (1–9, 17, 18), although distinct from all known HTLVs and STLVs; HTLV-3 falls within the those studies were not focused on persons who reported direct phylogenetic diversity of STLV-3, a group not previously seen in and repeated exposure to the blood and body fluids of NHPs, humans. We also document human infection with multiple STLV- which may increase the likelihood of human infection with 1-like viruses. These results demonstrate greater HTLV diversity zoonotic primate retroviruses (16, 19). than previously recognized and suggest that NHP exposure con- To determine whether previously undescribed HTLVs are tributes to HTLV emergence. Our discovery of unique and diver- present in persons exposed to the blood and body fluids of wild gent HTLVs has implications for HTLV diagnosis, blood screening, primate populations that are infected with STLV-1 and STLV-3 and potential disease development in infected persons. The find- (7, 8), we examined persons from rural villages in southern ings also indicate that cross-species transmission is not the rate- Cameroon located near natural NHP habitats for evidence of limiting step in pandemic retrovirus emergence and suggest that it PTLV infection. This population has been shown to have may be possible to predict and prevent disease emergence by frequent primate exposure risks, including hunting, butchering, surveillance of populations exposed to animal reservoirs and and keeping primate pets (16, 19). interventions to decrease risk factors, such as primate hunting. Materials and Methods retrovirus ͉ zoonosis ͉ simian ͉ exposures ͉ diversity Study Population and Ethical Approvals. Persons living in 11 rural villages in southern Cameroon proximal to forested and nonfor- rimate T-lymphotropic viruses (PTLVs) are deltaretrovi- ested NHP habitats (Fig. 1) were invited to participate in a Pruses composed of three distinct groups (PTLV-1, -2, and community-based HIV prevention campaign designed to provide -3), which by conventional nomenclature are named simian information through the use of Cameroonian educators and coun- T-lymphotropic viruses (STLVs) when found in nonhuman selors and therefore to decrease transmission. Participation in the primates (NHPs) and human T-lymphotropic viruses (HTLVs) study was voluntary. The study protocol was approved by the Johns when found in humans, regardless of suspected zoonotic origin Hopkins Committee for Human Research, the Cameroon National (1–9). PTLV-1 and PTLV-2 include both HTLV-1 and HTLV-2 Ethical Review Board, and the HIV Tri-Services Secondary Re- and their simian analogs (STLV-1 and STLV-2, respectively) view Board. Study participants completed questionnaires designed (1–5), whereas PTLV-3 comprises only simian viruses (6–9). The to determine behaviors that exposed participants to NHPs. Indi- finding that HTLV-1 and HTLV-2 originated independently and viduals were asked to identify and quantify their exposure to a range are related to distinct lineages of STLVs (STLV-1 and STLV-2, of NHPs, which were reliably classified into categories that could be respectively) (1, 2), combined with results showing that HTLV-1 easily distinguished by this population: chimpanzee, gorilla, and diversity appears to have resulted from multiple cross-species monkey. All personal identifiers were removed from questionnaires transmissions of STLV-1 (1–5), suggests that contact between and matching specimens before testing to provide an anonymous, humans and infected NHPs may result in HTLV emergence. unlinked study population. Like HIV, HTLV has spread globally to at least 22 million persons sexually, from mother to child, and by exposure to This paper was submitted directly (Track II) to the PNAS office. contaminated blood through transfusions and injection drug use Abbreviations: HTLV, human T-lymphotropic virus; PTLV, primate T-lymphotropic virus; (1, 10, 11). HTLV-1 causes adult T cell leukemia and HTLV- STLV, simian T-lymphotropic virus; NHPs, nonhuman primates; WB, Western blot; SFV, 1-associated myelopathy͞tropical spastic paraperesis and other simian foamy virus. inflammatory diseases in Ϸ2–5% of those infected (1, 10). Data deposition: The 28 HTLV sequences reported in this paper have been deposited in the HTLV-2 is less pathogenic than HTLV-1 and has been associ- GenBank database (accession nos. AY818406–AY818433). ated with a neurologic disease similar to HTLV-1-associated ††To whom correspondence should be addressed. E-mail: [email protected]. myelopathy͞tropical spastic paraperesis (11). © 2005 by The National Academy of Sciences of the USA 7994–7999 ͉ PNAS ͉ May 31, 2005 ͉ vol. 102 ͉ no. 22 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0501734102 Downloaded by guest on September 24, 2021 designed from conserved PTLV regions. The external and internal tax primers are PTLVTPG [5Ј-T(C͞T)ACCT(G͞ A)GGACCCCATCGATGGACG-3Ј] and PGTAXR1 [5Ј- GAIGA(T͞C)TGIA(C͞G)TAC(T͞C)AAAGATGGCTG-3Ј] and PH2Rrev [5Ј-CCTTATCCCTCGICTCCCCTCCTT-3Ј] and PGTAXR2 [5Ј-TTIGGG(T͞C)AIGGICCGGAAATCAT-3Ј], respectively. The external and internal pol primers are PG- POLF1 [5Ј-C(T͞G)TTAAACCIGA(A͞G)CGCCTCCAGGC- 3Ј] and PGPOLR1 [5Ј-GG(T͞C)(A͞G)TGIA(A͞G)CCA(A͞ G)(A͞G)CIAG(T͞G)GGCCA-3Ј] and PGPOLF2 [5Ј-AC(T͞ C)TGGT(C͞T)(C͞T)(G͞C)(G͞C)A(A͞G)GGCCCTGGAGG- 3Ј] and PGPOLR2 [5Ј-G(A͞G)(T͞C)(A͞G)GGIGTIC- CTTTIGAGACCCA-3Ј], respectively. Additional diagnostic PCR with PTLV-specific primers was performed on specimens with negative results for the generic 222-bp tax fragments. Assays described previously were used for PTLV-1 env and STLV-3 Fig. 1. Map of study sites shown in relation to distribution of lowland forest LTR and HTLV-2 env PCR (6, 21). For HTLV-4 detection, a (green) in central Africa. Sites with evidence of PTLV infection are represented nested PCR assay was developed based on the HTLV-4 tax with colored circles, which correspond to the PTLV(s) found at the site. sequence by using the external primers 1863TF1 (5Ј- CTCCTTCTTTCAGTCCGTGCGGAG-3Ј) and 1863TR1 (5Ј- GGGGTAGTCAGGTTTGGCTGGTAT-3Ј) and the internal Specimen Preparation and Serology. Blood was collected from primers 1863TF2 (5Ј-CCTACCGCAACGGATGTCTTGAAA- participants, transported to a central laboratory, processed into 3Ј) and 1863TR2 (5Ј-TATGGCGCCGGTGTGATGATAAAG- plasma and peripheral blood mononuclear cell aliquots, and 3Ј) and standard conditions to generate a 275-bp fragment. stored at Ϫ80°C. Initial screening for HTLV antibodies in Percentage nucleotide divergence was calculated by using the plasma specimens was performed by using the Vironostika GAP program in the Wisconsin package (Genetics Computer HTLV-1͞2 microelisa system (Organon-Teknika, Durham, NC) according to the manufacturer’s instructions. This enzyme im- Group, Madison, WI) (22). Sequences were aligned by using the munoassay contains purified HTLV-1 and HTLV-2 viral lysates CLUSTAL W program (23); gaps were removed, and distance- and a recombinant HTLV-1 p21 envelope (Env) antigen. Re- based trees were generated by using the Kimura two-parameter active specimens were then tested by a Western blot (WB) test model in conjunction with
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