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High Prevalences and a Wide Genetic Diversity of Simian Retroviruses in Non-human Primate Bushmeat in Rural Areas of the Democratic Republic of Congo

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An Erratum to this article was published on 03 March 2017

Abstract

Like the majority of emerging infectious diseases, HIV and HTLV are of zoonotic origin. Here we assess the risk of cross-species transmissions of their simian counterparts, SIV and STLV, from non-human primates (NHP) to humans in the Democratic Republic of Congo (DRC). A total of 331 samples, derived from NHP bushmeat, were collected as dried blood spots (DBS, n = 283) or as tissue samples (n = 36) at remote forest sites mainly in northern and eastern DRC. SIV antibody prevalences in DBS were estimated with a novel high throughput immunoassay with antigens representing the actual known diversity of HIV/SIV lineages. Antibody-positive samples were confirmed by PCR and sequence analysis. Screening for STLV infection was done with universal primers in tax, and new strains were further characterized in LTR. SIV and STLV infection in tissue samples was done by PCR only. Overall, 5 and 15.4% of NHP bushmeat was infected with SIV and STLV, respectively. A new SIV lineage was identified in Allen’s swamp monkeys (Allenopithecus nigroviridis). Three new STLV-1 subtypes were identified in Allen’s swamp monkeys (Allenopithecus nigroviridis), blue monkeys (Cercopithecus mitis), red-tailed guenons (Cercopithecus ascanius schmidti) and agile mangabeys (Cercocebus agilis). SIV and STLV prevalences varied according to species and geographic region. Our study illustrates clearly, even on a small sample size from a limited number of geographic areas, that our knowledge on the genetic diversity and geographic distribution of simian retroviruses is still limited and that humans continue to be exposed to relative high proportions on infected NHP bushmeat.

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References

  • Aghokeng AF, Ayouba A, Mpoudi-Ngole E, Loul S, Liegeois F, Delaporte E, Peeters M. (2010). Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infect Genet Evol. 2010; 10: 386–396. doi:10.1016/j.meegid.2009.04.014.

    Article  Google Scholar 

  • Ahuka-Mundeke S, Liegeois F, Ayouba A, Foupouapouognini Y, Nerrienet E, Delaporte E, Peeters M. (2010) Full-length genome sequence of a simian immunodeficiency virus (SIV) infecting a captive agile mangabey (Cercocebus agilis) is closely related to SIVrcm infecting wild red-capped mangabeys (Cercocebus torquatus) in Cameroon. J Gen Virol. 91: 2959-64. doi: 10.1099/vir.0.025767-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahuka-Mundeke S, Ayouba A, Mbala-Kingebeni P, Liegeois F, Esteban A, Lunguya-Metila O, Demba D, Bilulu G, Mbenzo-Abokome V, Inogwabini BI, Muyembe-Tamfum JJ, Delaporte E, Peeters M. (2011) Novel multiplexed HIV/simian immunodeficiency virus antibody detection assay. Emerg Infect Dis. 17: 2277-86. doi: 10.3201/eid1712.110783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahuka-Mundeke S, Mbala-Kingebeni P, Liegeois F, Ayouba A, Lunguya-Metila O, Demba D, Bilulu G, Mbenzo-Abokome V, Inogwabini BI, Muyembe-Tamfum JJ, Delaporte E, Peeters M. (2012) Identification and molecular characterization of new simian T cell lymphotropic viruses in nonhuman primates bushmeat from the Democratic Republic of Congo. AIDS Res Hum Retroviruses. 28: 628-35. doi: 10.1089/AID.2011.0211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahuka-Mundeke S, Lunguya-Metila O, Mbenzo-Abokome V, Butel C, Inogwabini B, Omasombo V, Muyembe-Tamfum JJ, Georgiev AV, Muller MN, Ndjango JB, Li Y, Delaporte E, Hahn BH, Peeters M, Ayouba A. (2016) Genetic diversity of STLV-2 and interspecies transmission of STLV-3 in wild-living bonobos. Virus evolution (in press).

  • Ayouba A, Akoua-Koffi C, Calvignac-Spencer S, Esteban A, Locatelli S, Li H, Li Y, Hahn BH, Delaporte E, Leendertz FH, Peeters M. (2013) Evidence for continuing cross-species transmission of SIVsmm to humans: characterization of a new HIV-2 lineage in rural Côte d’Ivoire. AIDS. 27: 2488-91. doi: 10.1097/01.aids.0000432443.22684.50.

    Article  PubMed  Google Scholar 

  • Beer BE, Bailes E, Dapolito G, Campbell BJ, Goeken RM, Axthelm MK, Markham PD, Bernard J, Zagury D, Franchini G, Sharp PM, Hirsch VM. (2000) Patterns of genomic sequence diversity among their simian immunodeficiency viruses suggest that L’Hoest monkeys (Cercopithecus lhoesti) are a natural lentivirus reservoir. J Virol. 74: 3892-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calattini S, Betsem EB, Froment A, Mauclère P, Tortevoye P, Schmitt C, Njouom R, Saib A, Gessain A. (2007) Simian foamy virus transmission from apes to humans, rural Cameroon. Emerg Infect Dis. 13: 1314-1320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvignac-Spencer S, Adjogoua EV, Akoua-Koffi C, Hedemann C, Schubert G, Ellerbrok H, Leendertz SA, Pauli G, Leendertz FH. (2012) Origin of human T-lymphotropic virus type 1 in rural Côte d’Ivoire. Emerg Infect Dis. 18(5): 830-3. doi: 10.3201/eid1805.111663.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Telfier P, Gettie A, Reed P, Zhang L, Ho DD, Marx PA. (1996) Genetic characterization of new West African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. J Virol. 70: 3617-27.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Luckay A, Sodora DL, Telfer P, Reed P, Gettie A, Kanu JM, Sadek RF, Yee J, Ho DD, Zhang L, Marx PA. (1997) Human immunodeficiency virus type 2 (HIV-2) seroprevalence and characterization of a distinct HIV-2 genetic subtype from the natural range of simian immunodeficiency virus-infected sooty mangabeys. J Virol. 71: 3953-60.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clavel F, Guyader M, Guétard D, Sallé M, Montagnier L, Alizon M. (1986) Molecular cloning and polymorphism of the human immune deficiency virus type 2. Nature. 324:691-5.

    Article  CAS  PubMed  Google Scholar 

  • Courgnaud V, Pourrut X, Bibollet-Ruche F, Mpoudi-Ngole E, Bourgeois A, Delaporte E, Peeters M. (2001) Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family. J Virol. 75: 857-66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courgnaud V, Salemi M, Pourrut X, Mpoudi-Ngole E, Abela B, Auzel P, Bibollet-Ruche F, Hahn B, Vandamme AM, Delaporte E, Peeters M. (2002) Characterization of a novel simian immunodeficiency virus with a vpu gene from greater spot-nosed monkeys (Cercopithecus nictitans) provides new insights into simian/human immunodeficiency virus phylogeny. J Virol. 76: 8298-309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Arc M, Ayouba A, Esteban A, Learn GH, Boué V, Liegeois F, Etienne L, Tagg N, Leendertz FH, Boesch C, Madinda NF, Robbins MM, Gray M, Cournil A, Ooms M, Letko M, Simon VA, Sharp PM, Hahn BH, Delaporte E, Ngole E, Peeters M. (2015) Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc Natl Acad Sci U S A. 112: E1343-52. doi: 10.1073/pnas.1502022112.

    Article  PubMed  PubMed Central  Google Scholar 

  • Faria NR, Rambaut A, Suchard MA, Baele G, Bedford T, Ward MJ, Tatem AJ, Sousa JD, Arinaminpathy N, Pépin J, Posada D, Peeters M, Pybus OG, Lemey P. (2014) HIV epidemiology. The early spread and epidemic ignition of HIV-1 in human populations. Science. 346: 56-61. doi: 10.1126/science.1256739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filippone C, Betsem E, Tortevoye P, Cassar O, Bassot S, Froment A, Fontanet A, Gessain A. (2015) A Severe Bite From a Nonhuman Primate Is a Major Risk Factor for HTLV-1 Infection in Hunters From Central Africa. Clin Infect Dis. 60(11):1667-76. doi: 10.1093/cid/civ145.

    Article  PubMed  Google Scholar 

  • Gao F, Yue L, White AT, Pappas PG, Barchue J, Hanson AP, Greene BM, Sharp PM, Shaw GM, Hahn BH. (1992) Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature. 358: 495-499.

    Article  CAS  PubMed  Google Scholar 

  • Gessain A. (2011) Human retrovirus HTLV-1: descriptive and molecular epidemiology, origin, evolution, diagnosis and associated diseases. Bull Soc Pathol Exot. 104(3):167-80. doi: 10.1007/s13149-011-0174-4.

    Article  CAS  PubMed  Google Scholar 

  • Gessain A, Cassar O. (2012) Epidemiological Aspects and World Distribution of HTLV-1 Infection. Front Microbiol. 3:388. doi: 10.3389/fmicb.2012.00388.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gessain A, Rua R, Betsem E, Turpin J, Mahieux R. (2013) HTLV-3/4 and simian foamy retroviruses in humans: discovery, epidemiology, cross-species transmission and molecular virology. Virology. 435: 187-99. doi: 10.1016/j.virol.2012.09.035.

    Article  CAS  PubMed  Google Scholar 

  • Giri A, Markham P, Digilio L, Hurteau G, Gallo RC, Franchini G. (1994) Isolation of a novel simian T-cell lymphotropic virus from Pan paniscus that is distantly related to the human T-cell leukemia/lymphotropic virus types I and II. J Virol. 68: 8392-5.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Groves, C. (2001) Primate taxonomy. Smithsonian Series in Comparative Evolutionary Biology, Smithsonian Institution Press.

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59: 307-21. doi: 10.1093/sysbio/syq010.

    Article  CAS  PubMed  Google Scholar 

  • Hahn BH, Shaw GM, De Cock KM, Sharp PM. (2000) AIDS as a zoonosis: scientific and public health implications. Science 287: 607–614.

  • Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature. 339: 389-392.

    Article  CAS  PubMed  Google Scholar 

  • Kazanji M, Mouinga-Ondémé A, Lekana-Douki-Etenna S, Caron M, Makuwa M, Mahieux R, Gessain A. (2015) Origin of HTLV-1 in hunters of nonhuman primates in Central Africa. J Infect Dis. 211(3): 361-5. doi: 10.1093/infdis/jiu464.

    Article  PubMed  Google Scholar 

  • Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F, Loul S, Ngole EM, Bienvenue Y, Delaporte E, Brookfield JF, Sharp PM, Shaw GM, Peeters M, Hahn BH. (2006) Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 313: 523-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kingdon J. (1997). The Kingdon Field Guide to African Mammals (edited by A. Press).

  • Lauck M, Switzer WM, Sibley SD, Hyeroba D, Tumukunde A, Weny G, Shankar A, Greene JM, Ericsen AJ, Zheng H, Ting N, Chapman CA, Friedrich TC, Goldberg TL, O’Connor DH. (2014a) Discovery and full genome characterization of a new SIV lineage infecting red-tailed guenons (Cercopithecus ascanius schmidti) in Kibale National Park, Uganda. Retrovirology. 11:55. doi:10.1186/1742-4690-11-55.

  • Lauck M, Switzer WM, Sibley SD, Hyeroba D, Tumukunde A, Weny G, Taylor B, Shankar A, Ting N, Chapman CA, Friedrich TC, Goldberg TL, O’Connor DH. (2014b) Discovery and full genome characterization of two highly divergent simian immunodeficiency viruses infecting black-and-white colobus monkeys (Colobus guereza) in Kibale National Park, Uganda. Retrovirology. 10:107. doi:10.1186/1742-4690-10-107.

  • LeBreton M, Switzer WM, Djoko CF, Gillis A, Jia H, Sturgeon MM, Shankar A, Zheng H, Nkeunen G, Tamoufe U, Nana A, Le Doux Diffo J, Tafon B, Kiyang J, Schneider BS, Burke DS, Wolfe ND. (2014) A gorilla reservoir for human T-lymphotropic virus type 4. Emerg Microbes Infect. 3: e7. doi: 10.1038/emi.2014.7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemey P, Pybus OG, Wang B, Saksena NK, Salemi M, Vandamme AM. (2003) Tracing the origin and history of the HIV-2 epidemic. Proc Natl Acad Sci U S A. 100: 6588-92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ndjango JB, Learn GH, Ramirez MA, Keele BF, Bibollet-Ruche F, Liu W, Easlick JL, Decker JM, Rudicell RS, Inogwabini BI, Ahuka-Mundeke S, Leendertz FH, Reynolds V, Muller MN, Chancellor RL, Rundus AS, Simmons N, Worobey M, Shaw GM, Peeters M, Sharp PM, Hahn BH. (2012) Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol 86:10776-91. doi: 10.1128/JVI.01498-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liégeois F, Lafay B, Switzer WM, Locatelli S, Mpoudi-Ngolé E, Loul S, Heneine W, Delaporte E, Peeters M. (2008) Identification and molecular characterization of new STLV-1 and STLV-3 strains in wild-caught nonhuman primates in Cameroon. Virology. 371(2):405-17.

    Article  PubMed  Google Scholar 

  • Liégeois F, Boué V, Mouacha F, Butel C, Ondo BM, Pourrut X, Leroy E, Peeters M, Rouet F. (2012) New STLV-3 strains and a divergent SIVmus strain identified in nonhuman primate bushmeat in Gabon. Retrovirology. 9: 28. doi: 10.1186/1742-4690-9-28.

    Article  PubMed  PubMed Central  Google Scholar 

  • Locatelli S, Peeters M. (2012) Cross-species transmission of simian retroviruses: how and why they could lead to the emergence of new diseases in the human population. AIDS. 26: 659-73. doi: 10.1097/QAD.0b013e328350fb68.

    Article  PubMed  Google Scholar 

  • Lowenstine LJ, Pedersen NC, Higgins J, Pallis KC, Uyeda A, Marx P, Lerche NW, Munn RJ, Gardner MB. (1986) Seroepidemiologic survey of captive Old-World primates for antibodies to human and simian retroviruses, and isolation of a lentivirus from sooty mangabeys (Cercocebus atys). Int J Cancer. 38 (4): 563-74.

    Article  CAS  PubMed  Google Scholar 

  • Mahieux R, Ibrahim F, Mauclere P, Herve V, Michel P, Tekaia F, Chappey C, Garin B, Van Der Ryst E, Guillemain B, Ledru E, Delaporte E, de The G, Gessain A. (1997) Molecular epidemiology of 58 new African human T-cell leukemia virus type 1 (HTLV-1) strains: identification of a new and distinct HTLV-1 molecular subtype in Central Africa and in Pygmies. J Virol. 71: 1317-33.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahieux R, Chappey C, Georges-Courbot MC, Dubreuil G, Mauclere P, Georges A, Gessain A. (1998) Simian T-cell lymphotropic virus type 1 from Mandrillus sphinx as a simian counterpart of human T-cell lymphotropic virus type 1 subtype D. J Virol. 72: 10316-22.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahieux R, Gessain A. (2011) HTLV-3/STLV-3 and HTLV-4 viruses: discovery, epidemiology, serology and molecular aspects. Viruses. 3: 1074-90. doi: 10.3390/v3071074.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meertens L, Rigoulet J, Mauclère P, Van Beveren M, Chen GM, Diop O, Dubreuil G, Georges-Goubot MC, Berthier JL, Lewis J, Gessain A. (2001) Molecular and phylogenetic analyses of 16 novel simian T cell leukemia virus type 1 from Africa: close relationship of STLV-1 from Allenopithecus nigroviridis to HTLV-1 subtype B strains. Virology. 287: 275-85.

    Article  CAS  PubMed  Google Scholar 

  • Peeters M, D’Arc M, Delaporte E. (2014) Origin and diversity of human retroviruses. AIDS Rev. 16: 23–34.

    PubMed  PubMed Central  Google Scholar 

  • Plantier JC, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemée V, Damond F, Robertson DL, Simon F. (2009) A new human immunodeficiency virus derived from gorillas. Nat Med. 15: 871-2. doi: 10.1038/nm.2016.

    Article  CAS  PubMed  Google Scholar 

  • Richard L, Mouinga-Ondémé A, Betsem E, Filippone C, Nerrienet E, Kazanji M, Gessain A. (2016) Zoonotic Transmission of Two New Strains of Human T-lymphotropic Virus Type 4 in Hunters Bitten by a Gorilla in Central Africa. Clin Infect Dis. 63: 800-3. doi: 10.1093/cid/ciw389.

    Article  PubMed  Google Scholar 

  • Santiago ML, Bibollet-Ruche F, Gross-Camp N, Majewski AC, Masozera M, Munanura I, Kaplin BA, Sharp PM, Shaw GM, Hahn BH. (2003) Noninvasive detection of Simian immunodeficiency virus infection in a wild-living L’Hoest’s monkey (Cercopithecus Ihoesti). AIDS Res Hum Retroviruses. 19: 1163-6.

    Article  CAS  PubMed  Google Scholar 

  • Santiago ML, Range F, Keele BF, Li Y, Bailes E, Bibollet-Ruche F, Fruteau C, Noë R, Peeters M, Brookfield JF, Shaw GM, Sharp PM, Hahn BH. (2005) Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d’Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol. 79: 12515-12527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sintasath DM, Wolfe ND, Lebreton M, Jia H, Garcia AD, Le Doux-Diffo J, Tamoufe U, Carr JK, Folks TM, Mpoudi-Ngole E, Burke DS, Heneine W, Switzer WM. (2009) Simian T-lymphotropic virus diversity among nonhuman primates, Cameroon. Emerg Infect Dis. 15(2):175-84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Switzer WM, Tang S, Ahuka-Mundeke S, Shankar A, Hanson DL, Zheng H, Ayouba A, Wolfe ND, LeBreton M, Djoko CF, Tamoufe U, Esteban A, Heneine W, Peeters M, Wright LL, Muyembe-Tamfum JJ, Wemakoy EO, Mulembakani P, Hoff NA, Rimoin AW. (2012) Novel simian foamy virus infections from multiple monkey species in women from the Democratic Republic of Congo. Retrovirology. 9:100. doi: 10.1186/1742-4690-9-100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, and Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution. 30: 2725-2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandamme AM, Liu HF, Van Brussel M, De Meurichy W, Desmyter J, Goubau P. (1996) The presence of a divergent T-lymphotropic virus in a wild-caught pygmy chimpanzee (Pan paniscus) supports an African origin for the human T-lymphotropic/simian T-lymphotropic group of viruses. J Gen Virol. 77: 1089-99.

    Article  CAS  PubMed  Google Scholar 

  • Vandamme AM, Van Laethem K, Liu HF, Van Brussel M, Delaporte E, de Castro Costa CM, Fleischer C, Taylor G, Bertazzoni U, Desmyter J, Goubau P. (1997). Use of a generic polymerase chain reaction assay detecting human T-lymphotropic virus (HTLV) types I, II and divergent simian strains in the evaluation of individuals with indeterminate HTLV serology. J Med Virol. 52: 1-7.

    Article  CAS  PubMed  Google Scholar 

  • van der Kuyl AC, Kuiken CL, Dekker JT, Goudsmit J. (1995) Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences. J Mol Evol 40: 173-180.

    Article  PubMed  Google Scholar 

  • Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y, Ngolle EM, Sharp PM, Shaw GM, Delaporte E, Hahn BH, Peeters M. (2006) Human immunodeficiency viruses: SIV infection in wild gorillas. Nature. 444: 164.

    Article  PubMed  Google Scholar 

  • Van Heuverswyn F, Li Y, Bailes E, Neel C, Lafay B, Keele BF, Shaw KS, Takehisa J, Kraus MH, Loul S, Butel C, Liegeois F, Yangda B, Sharp PM, Mpoudi-Ngole E, Delaporte E, Hahn BH, Peeters M. (2007) Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology. 368: 155-71.

    Article  PubMed  Google Scholar 

  • Wertheim JO, Worobey M. (2009) Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Comput Biol. 5: e1000377. doi: 10.1371/journal.pcbi.1000377.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, Prosser AT, Torimiro JN, Wright A, Mpoudi-Ngole E, McCutchan FE, Birx DL, Folks TM, Burke DS, Heneine W. (2004) Naturally acquired simian retrovirus infections in central African hunters. Lancet. 363: 932-937.

    Article  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci U S A. 102: 7994-7999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, Bunce M, Muyembe JJ, Kabongo JM, Kalengayi RM, Van Marck E, Gilbert MT, Wolinsky SM. (2008) Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature. 455: 661-4. doi: 10.1038/nature07390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worobey M, Telfer P, Souquière S, Hunter M, Coleman CA, Metzger MJ, Reed P, Makuwa M, Hearn G, Honarvar S, Roques P, Apetrei C, Kazanji M, Marx PA. (2010) Island biogeography reveals the deep history of SIV. Science. 329: 1487. doi: 10.1126/science.1193550.

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Wolfe ND, Sintasath DM, Tamoufe U, Lebreton M, Djoko CF, Diffo Jle D, Pike BL, Heneine W, Switzer WM. (2010) Emergence of a novel and highly divergent HTLV-3 in a primate hunter in Cameroon. Virology. 401: 137-45. doi: 10.1016/j.virol.2010.03.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu T, Korber BT, Nahmias AJ, Hooper E, Sharp PM, Ho DD. (1998) An African HIV-1 sequence from 1959 and implications for the origin of the epidemic. Nature. 391: 594-7.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported in part by grants from the National Institute of Health (RO1 AI 50529) and the Agence Nationale de Recherches sur le SIDA (ANRS 12125/12182/12325). We thank the Ministries of Health and Environment and the National Ethic committee from the Democratic Republic of Congo (DRC) for permission to perform this study and all the field staff from DRC. We thank Dr. Mazongo, Dr. Abanda, Dr. Jonnhy and all the local Staff in Equateur and Nord-Kivu Province for their collaboration and participation in this study.

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Authors and Affiliations

  1. UMI 233 TransVIHMI/INSERM1175, Institut de Recherche pour le Développement (IRD), University of Montpellier, 911 Avenue Agropolis, 34394, Montpellier, Cedex 1, France

    Ahuka-Mundeke Steve, Ayouba Ahidjo, Foncelle Caroline, Delaporte Eric & Peeters Martine

  2. Institut National de Recherche Biomédicales, Kinshasa, Democratic Republic of Congo

    Ahuka-Mundeke Steve, Mbala-Kingebeni Placide, Ndimbo-Kumugo Simon-Pierre, Lunguya-Metila Octavie & Muyembe-Tamfum Jean-Jacques

  3. Service de Microbiologie, Cliniques Universitaires de Kinshasa, Kinshasa, Democratic Republic of Congo

    Ahuka-Mundeke Steve, Mbala-Kingebeni Placide, Lunguya-Metila Octavie & Muyembe-Tamfum Jean-Jacques

  4. Institut Supérieur de Techniques Médicales de Walikale, Walikale, Nord Kivu, Democratic Republic of Congo

    Mubonga Mukulumanya

  5. Projet Lac Tumba, WWF, Malebo, Democratic Republic of the Congo

    Mbenzo-Abokome Valentin

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  1. Ahuka-Mundeke Steve
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  10. Delaporte Eric
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Correspondence to Peeters Martine.

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An erratum to this article is available at http://dx.doi.org/10.1007/s10393-017-1223-3.

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Steve, AM., Ahidjo, A., Placide, MK. et al. High Prevalences and a Wide Genetic Diversity of Simian Retroviruses in Non-human Primate Bushmeat in Rural Areas of the Democratic Republic of Congo. EcoHealth 14, 100–114 (2017). https://doi.org/10.1007/s10393-016-1202-0

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