Abstract
It is now well established that the human immunodeficiency viruses, HIV-1 and HIV-2, are the results of cross-species transmissions of simian immunodeficiency viruses (SIV) naturally infecting nonhuman primates in sub-Saharan Africa. SIVs are found in many African primates, and humans continue to be exposed to these viruses by hunting and handling primate bushmeat. Sooty mangabeys (Cercocebus atys) and western red colobus (Piliocolobus badius badius) are infected with SIV at a high rate in the Taï Forest, Côte d’Ivoire. We investigated the SIV infection and prevalence in 6 other monkey species living in the Taï Forest using noninvasive methods. We collected 127 fecal samples from 2 colobus species (Colobus polykomos and Procolobus verus) and 4 guenon species (C. diana, C. campbelli, C. petaurista, and C. nictitans). We tested these samples for HIV cross-reactive antibodies and performed reverse transcriptase-polymerase chain reactions (RT-PCR) targeting the gag, pol, and env regions of the SIV genome. We screened 16 human microsatellites for use in individual discrimination and identified 4–6 informative markers per species. Serological analysis of 112 samples yielded negative (n = 86) or uninterpretable (n = 26) results. PCR analysis on 74 samples confirmed the negative results. These results may reflect either the limited number of individuals sampled or a low prevalence of infection. Further research is needed to improve the sensitivity of noninvasive methods for SIV detection.
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Aghokeng, A. F., Liu, W., Bibollet-Ruche, F., Loul, S., Mpoudi-Ngole, E., Laurent, C., et al. (2006). Widely varying SIV prevalence rates in naturally infected primate species from Cameroon. Virology, 345(1), 174–189.
Aghokeng, A. F., Bailes, E., Loul, S., Courgnaud, V., Mpoudi-Ngole, E., Sharp, P. M., et al. (2007). Full-length sequence analysis of SIVmus in wild populations of mustached monkeys (Cercopithecus cephus) from Cameroon provides evidence for two co-circulating SIVmus lineages. Virology, 360(2), 407–418.
Aghokeng, A. F., Ayouba, A., Mpoudi-Ngole, E., Loul, S., Liegeois, F., Delaporte, E., et al. (2009). Extensive survey on the prevalence and genetic diversity of SIVs in primate bushmeat provides insights into risks for potential new cross-species transmissions. Infection, Genetics and Evolution, 10(3), 386–396.
Allen, M., Engstrom, A. S., Meyers, S., Handt, O., Saldeen, T., von Haeseler, A., et al. (1998). Mitochondrial DNA sequencing of shed hairs and saliva on robbery caps: sensitivity and matching probabilities. Journal of Forensic Science, 43(3), 453–464.
Bailes, E., Gao, F., Bibollet-Ruche, F., Courgnaud, V., Peeters, M., Marx, P. A., et al. (2003). Hybrid origin of SIV in chimpanzees. Science, 300(5626), 1713.
Bonhomme, M., Blancher, A., & Crouau-Roy, B. (2005). Multiplexed microsatellites for rapid identification and characterization of individuals and populations of Cercopithecidae. American Journal of Primatology, 67(3), 385–391.
Bradley, B. J., & Vigilant, L. (2002). False alleles derived from microbial DNA poses a potential source of error in microsatellite genotyping of DNA from faeces. Molecular Ecology Notes, 2, 602–605.
Bshary, R. (2001). Diana monkeys, Cercopithecus diana, adapt their anti-predator response behaviour to human hunting strategies. Behavioral Ecology and Sociobiology, 50, 251–256.
Buzzard, P., & Eckardt, W. (2007). The social system of the guenons. In W. S. McGraw, K. Zuberbühler, & R. Noë (Eds.), Monkeys of the Taï Forest (pp. 51–71). Cambridge: Cambridge University Press.
Caspary, H. U., Koné, I., Prouot, C., & De Pauw, M. (2001). La chasse et la filière viande de brousse dans l’espace Taï, Côte-d’Ivoire. Tropenbos Côte-d’Ivoire. Séries 2, 170 pp.
Clewley, J. P., Lewis, J. C., Brown, D. W., & Gadsby, E. L. (1998). A novel simian immunodeficiency virus (SIVdrl) pol sequence from the drill monkey, Mandrillus leucophaeus. Journal of Virology, 72(12), 10305–10309.
Coote, T., & Bruford, M. W. (1996). Human microsatellites applicable for analysis of genetic variation in apes and Old World monkeys. The Journal of Heredity, 87(5), 406–410.
Courgnaud, V., Pourrut, X., Bibollet-Ruche, F., Mpoudi-Ngole, E., Bourgeois, A., Delaporte, E., et al. (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. Journal of Virology, 75(2), 857–866.
Courgnaud, V., Abela, B., Pourrut, X., Mpoudi-Ngole, E., Loul, S., Delaporte, E., et al. (2003). Identification of a new simian immunodeficiency virus lineage with a vpu gene present among different cercopithecus monkeys (C. mona, C. cephus, and C. nictitans) from Cameroon. Journal of Virology, 77(23), 12523–12534.
Courgnaud, V., Formenty, P., Akoua-Koffi, C., Noe, R., Boesch, C., Delaporte, E., et al. (2003). Partial molecular characterization of two simian immunodeficiency viruses (SIV) from African colobids: SIVwrc from Western red colobus (Piliocolobus badius) and SIVolc from olive colobus (Procolobus verus). Journal of Virology, 77(1), 744–748.
Gagneux, P., Boesch, C., & Woodruff, D. S. (1997). Microsatellite scoring errors associated with noninvasive genotyping based on nuclear DNA amplified from shed hair. Molecular Ecology, 6(9), 861–868.
Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., et al. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature, 397(6718), 436–441.
Goossens, B., Latour, S., Vidal, C., Jamart, A., Ancrenaz, M., & Bruford, M. W. (2000). Twenty new microsatellite loci for use with hair and faecal samples in the chimpanzee (Pan troglodytes troglodytes). Folia Primatologica, 71(3), 177–180.
Hahn, B. H., Shaw, G. M., De Cock, K. M., & Sharp, P. M. (2000). AIDS as a zoonosis: scientific and public health implications. Science, 287(5453), 607–614.
Hirsch, V. M., Olmsted, R. A., Murphey-Corb, M., Purcell, R. H., & Johnson, P. R. (1989). An African primate lentivirus (SIVsm) closely related to HIV-2. Nature, 339(6223), 389–392.
Keele, B. F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M. L., et al. (2006). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science, 313(5786), 523–526.
Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., et al. (2009). Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature, 460(7254), 515–519.
Korstjens, A. H. (2001). Ph.D. thesis, Utrecht University, Utrecht.
Leendertz, S. A., Junglen, S., Hedemann, C., Goffe, A., Calvignac, S., Boesch, C., et al. (2010). High prevalence, co-infection rate and genetic diversity of retroviruses in wild red colobus monkeys (Piliocolobus badius badius) in Tai National Park, Cote d’Ivoire. Journal of Virology, 84(15), 7427–7436.
Liégeois, F., Lafay, B., Formenty, P., Locatelli, S., Courgnaud, V., Delaporte, E., et al. (2009). Full-length genome characterization of a novel simian immunodeficiency virus lineage (SIVolc) from olive colobus (Procolobus verus) and new SIVwrcPbb strains from western red colobus (Piliocolobus badius badius) from the Taï Forest in Ivory Coast. Journal of Virology, 83(1), 428–439.
Ling, B., Santiago, M. L., Meleth, S., Gormus, B., McClure, H. M., Apetrei, C., et al. (2003). Noninvasive detection of new simian immunodeficiency virus lineages in captive sooty mangabeys: ability to amplify virion RNA from fecal samples correlates with viral load in plasma. Journal of Virology, 77(3), 2214–2226.
Locatelli, S., Lafay, B., Liegeois, F., Ting, N., Delaporte, E., & Peeters, M. (2008). Full molecular characterisation of a simian immunodeficiency virus, SIVwrc-pbt from Temminck’s red colobus (Piliocolobus badius temminckii) from Abuko Nature Reserve, The Gambia. Virology, 376(1), 90–100.
Locatelli, S., Liegeois, F., Lafay, B., Roeder, A. D., Bruford, M. W., Formenty, P., et al. (2008). Prevalence and genetic diversity of simian immunodeficiency virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Taï Forest, Côte d’Ivoire. Infection, Genetics and Evolution, 8(1), 1–14.
McGraw, W. S., Zuberbühler, K., & Noë, R. (2007). Monkeys of the Taï Forest: An African primate community. Cambridge: Cambridge University Press.
Morin, P. A., Mahboubi, P., Wedel, S., & Rogers, J. (1998). Rapid screening and comparison of human microsatellite markers in baboons: allele size is conserved, but allele number is not. Genomics, 53(1), 12–20.
Navidi, W., Arnheim, N., & Waterman, M. S. (1992). A multiple-tubes approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. American Journal of Human Genetics, 50, 347–359.
Neel, C., Etienne, L., Li, Y., Takehisa, J., Rudicell, R. S., Bass, I. N., et al. (2009). Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. Journal of Virology, 84(3), 1464–1476.
Peeters, M., Honore, C., Huet, T., Bedjabaga, L., Ossari, S., Bussi, P., et al. (1989). Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS, 3(10), 625–630.
Peeters, M., Courgnaud, V., Abela, B., Auzel, P., Pourrut, X., Bibollet-Ruche, F., et al. (2002). Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerging Infectious Diseases, 8(5), 451–457.
Plantier, J. C., Leoz, M., Dickerson, J. E., De Oliveira, F., Cordonnier, F., Lemée, V., et al. (2009). A new human immunodeficiency virus derived from gorillas. Nature Medicine, 15(8), 871–872.
Prince, A. M., Brotman, B., Lee, D. H., Andrus, L., Valinsky, J., & Marx, P. (2002). Lack of evidence for HIV type 1–related SIVcpz infection in captive and wild chimpanzees (Pan troglodytes verus) in West Africa. AIDS Research and Human Retroviruses, 18(9), 657–660.
Raymond, M., & Rousset, F. (1995). Genepop (version 1.2), population genetics software for exact tests and ecumenicism. The Journal of Heredity, 86, 248–249.
Refisch, J., & Koné, I. (2005). Impact of commercial hunting on monkey populations in the Taï region, Côte d’Ivoire. Biotropica, 37(1), 136–144.
Salemi, M., De Oliveira, T., Courgnaud, V., Moulton, V., Holland, B., Cassol, S., et al. (2003). Mosaic genomes of the six major primate lentivirus lineages revealed by phylogenetic analyses. Journal of Virology, 77(13), 7202–7213.
Santiago, M. L., Rodenburg, C. M., Kamenya, S., Bibollet-Ruche, F., Gao, F., Bailes, E., et al. (2002). SIVcpz in wild chimpanzees. Science, 295(5554), 465.
Santiago, M. L., Lukasik, M., Kamenya, S., Li, Y., Bibollet-Ruche, F., Bailes, E., et al. (2003). Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). Journal of Virology, 77(13), 7545–7562.
Santiago, M. L., Range, F., Keele, B. F., Li, Y., Bailes, E., Bibollet-Ruche, F., et al. (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. Journal of Virology, 79(19), 12515–12527.
Smith, K. L., Alberts, CS. C., Bayes, M. K., Bruford, M. W., Altmann, J., & Ober, C. (2000). Cross-species amplification, non-invasive genotyping, and non-Mendelian inheritance of human STRPs in Savannah baboons. American Journal of Primatology, 51(4), 219–227.
Souquiere, S., Bibollet-Ruche, F., Robertson, D. L., Makuwa, M., Apetrei, C., Onanga, R., et al. (2001). Wild Mandrillus sphinx are carriers of two types of lentivirus. Journal of Virology, 75(15), 7086–7096.
Stoorvogel, J. J. (1993). Gross inputs and outputs of nutrients in undisturbed forest, Taï Area, Côte d’Ivoire. Veenman Drukkers: Wageningen.
Switzer, W. M., Parekh, B., Shanmugam, V., Bhullar, V., Phillips, S., Ely, J. J., et al. (2005). The epidemiology of simian immunodeficiency virus infection in a large number of wild- and captive-born chimpanzees: evidence for a recent introduction following chimpanzee divergence. AIDS Research and Human Retroviruses, 21(5), 335–342.
Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., et al. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research, 24(16), 3189–3194.
Takehisa, J., Harada, Y., Ndembi, N., Mboudjeka, I., Taniguchi, Y., Ngansop, C., et al. (2001). Natural infection of wild-born mandrills (Mandrillus sphinx) with two different types of simian immunodeficiency virus. AIDS Research and Human Retroviruses, 17(12), 1143–1154.
van de Woude, S., & Apetrei, C. (2006). Going wild: lessons from naturally occurring T-lymphotropic lentiviruses. Clinical Microbiology Reviews, 19(4), 728–762.
Van Heuverswyn, F., & Peeters, M. (2007). The origins of HIV and implications for the global epidemic. Current Infectious Disease Reports, 9(4), 338–346.
Van Heuverswyn, F., Li, Y., Neel, C., Bailes, E., Keele, B. F., Liu, W., et al. (2006). Human immunodeficiency viruses: SIV infection in wild gorillas. Nature, 444(7116), 164.
Van Heuverswyn, F., Li, Y., Bailes, E., Neel, C., Lafay, B., Keele, B. F., et al. (2007a). Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology, 368(1), 155–171.
Van Heuverswyn, F., Li, Y., Bailes, E., Neel, C., Lafay, B., Keele, B. F., et al. (2007b). Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology.
Vigilant, L. (1999). An evaluation of techniques for the extraction and amplification of DNA from naturally shed hairs. Biological Chemistry, 380(11), 1329–31.
Withmore, T. C. (1990). An introduction to tropical rain forests. Oxford: Clarendon.
Acknowledgments
We thank the Ministère d’Enseignement Supérieur et Recherche Scientifique, the Ministère d’Agriculture et Ressources Animales, the Centre Suisse de Recherche Scientifiques(CSRS) in Abidjan, the P.A.C.P.N.T., and the Centre de Recherche en Ecologie in Côte d’Ivoire for support and permission to conduct research in the Taï National Park. We thank the Taï Monkey Project and in particular F. Bélé, C. Benetton, and B. Diero for helping in sample collection; C. Butel, F. Van Heuverswyn, N. Vidal, A. Aghokeng, and F. Liégeois for technical advice and help in the laboratory in Montpellier; F. Leendertz and J. Refisch for involvement in the early phase of the project; and M. Tanner and J. Zinsstag for critical support outside the field. We also thank the journal editor J. M. Setchell and 3 anonymous reviewers for their useful comments on earlier versions of the manuscript. The virology section of this study was financially supported by the Institut de Recherche pour le Développement (IRD), the Agence Nationale de Recherches pour le SIDA (ANRS) and by the National Institute of Health (R01AI50529). Sabrina Locatelli was supported by grants from the Commission for Research Partnerships with Developing Countries (KFPE), Bern; the Messerli foundation, Zürich; and the Guggenheim-Schnurr Foundation, Basel.
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Locatelli, S., Roeder, A.D., Bruford, M.W. et al. Lack of Evidence of Simian Immunodeficiency Virus Infection Among Nonhuman Primates in Taï National Park, Côte d’Ivoire: Limitations of Noninvasive Methods and SIV Diagnostic Tools for Studies of Primate Retroviruses. Int J Primatol 32, 288–307 (2011). https://doi.org/10.1007/s10764-010-9466-7
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DOI: https://doi.org/10.1007/s10764-010-9466-7