Simian foamy virus transmission from apes to humans, rural Cameroon

Sara Calattini, Edouard Betsem A Betsem, Alain Froment, Philippe Mauclère, Patricia Tortevoye, Christine Schmitt, Richard Njouom, Ali Saib, Antoine Gessain, Sara Calattini, Edouard Betsem A Betsem, Alain Froment, Philippe Mauclère, Patricia Tortevoye, Christine Schmitt, Richard Njouom, Ali Saib, Antoine Gessain

Abstract

Simian virus infections of humans are an increasing public health concern. Simian foamy virus (SFV) infections have been reported in persons occupationally exposed to nonhuman primates and in a few hunters in Cameroon. To better understand this retroviral zoonosis in natural settings, we studied persons who lived in southern Cameroon, near nonhuman primate habitats. First we studied a general population of 1,164 adults; 4 were SFV positive according to serologic and molecular assays. Then we studied 85 persons who reported having been bitten or scratched by nonhuman primates; 7/29 (24.1%) of those who had contact with apes (gorillas or chimpanzees) were SFV positive, compared with only 2/56 (3.6%) of those who had had contact with monkeys. These data demonstrate efficient transmission of SFVs to humans in natural settings in central Africa, specifically following ape bites, and viral persistence in the human host.

Figures

Figure 1
Figure 1
Geographic distribution in Cameroon of the studied populations and the 13 persons infected by simian foamy virus (SFV), according to serologic and molecular results. Red, SFV-positive persons from the hunter study; green, SFV-positive persons from the retrospective study; blue circle, Pygmy area; violet circles, Bantu areas.
Figure 2
Figure 2
A) Western blot (WB) results based on chimpanzee (cpz) simian foamy virus (SFV) antigens. B) WB results based on monkey simian foamy virus antigens originating from participant AG16. C) Example of sero-indeterminate samples (lanes 1–7) and negative samples (lanes 8–13), detected by cpzSFV WB. Last lane (POS cpz), serum from an SFV-positive chimpanzee.
Figure 3
Figure 3
Wounds resulting from bites or scratches from a nonhuman primate. A) Participant no. 801001. B) Participant no. AG16. C) Participant no. 210301.
Figure 4
Figure 4
Immunofluorescence and electron microscopy results. A) Typical multinucleated giant cells with a clear seroreactivity of AG16 antigens, determined by using an immunofluorescence assay with positive anti–foamy virus serum, on BHK-21–infected cells cocultivated with stimulated peripheral blood mononuclear cells. B) Electron microscopy of ultrathin sections from cells infected by AG16 foamy virus.
Figure 5
Figure 5
Semiquantitative PCR for integrase and β-globin genes using AG15 peripheral blood buffy-coat DNA. Lanes 1–7 and 10–16, serial dilutions of the DNA from 500 ng to 0.5 pg; lanes 8 and 17, negative controls; lanes 9 and 18, positive controls; M, 100-bp ladder.

References

    1. Apetrei C, Marx PA. Simian retroviral infections in human beings. Lancet. 2004;364:137–8, author reply 139–40. 10.1016/S0140-6736(04)16620-8
    1. Weiss RA, McMichael AJ. Social and environmental risk factors in the emergence of infectious diseases. Nat Med. 2004;10:S70–6. 10.1038/nm1150
    1. Wolfe ND. Bushmeat hunting, deforestation, and prediction of zoonotic disease emergence. Emerg Infect Dis. 2005;11:1822–7.
    1. Wolfe ND, Prosser TA, Carr JK, Tamoufe U, Mpoudi-Ngole E, Torimiro JN, et al. Exposure to nonhuman primates in rural Cameroon. Emerg Infect Dis. 2004;10:2094–9.
    1. Brooks JI, Rud EW, Pilon RG, Smith JM, Switzer WM, Sandstrom PA. Cross-species retroviral transmission from macaques to human beings. Lancet. 2002;360:387–8. 10.1016/S0140-6736(02)09597-1
    1. Heneine W, Schweizer M, Sandstrom P, Folks T. Human infection with foamy viruses. Curr Top Microbiol Immunol. 2003;277:181–96.
    1. Sandstrom PA, Phan KO, Switzer WM, Fredeking T, Chapman L, Heneine W, et al. Simian foamy virus infection among zoo keepers. Lancet. 2000;355:551–2. 10.1016/S0140-6736(99)05292-7
    1. Heneine W, Switzer WM, Sandstrom P, Brown J, Vedapuri S, Schable CA, et al. Identification of a human population infected with simian foamy viruses. Nat Med. 1998;4:403–7. 10.1038/nm0498-403
    1. Schweizer M, Falcone V, Gange J, Turek R, Neumann-Haefelin D. Simian foamy virus isolated from an accidentally infected human individual. J Virol. 1997;71:4821–4.
    1. Switzer WM, Bhullar V, Shanmugam V, Cong ME, Parekh B, Lerche NW, et al. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J Virol. 2004;78:2780–9. 10.1128/JVI.78.6.2780-2789.2004
    1. Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, et al. Naturally acquired simian retrovirus infections in central African hunters. Lancet. 2004;363:932–7. 10.1016/S0140-6736(04)15787-5
    1. Nerrienet E, Meertens L, Kfutwah A, Foupouapouognigni Y, Gessain A. Molecular epidemiology of simian T-lymphotropic virus (STLV) in wild-caught monkeys and apes from Cameroon: a new STLV-1, related to human T-lymphotropic virus subtype F, in a Cercocebus agilis. J Gen Virol. 2001;82:2973–7.
    1. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397:436–41. 10.1038/17130
    1. Corbet S, Muller-Trutwin MC, Versmisse P, Delarue S, Ayouba A, Lewis J, et al. env sequences of simian immunodeficiency viruses from chimpanzees in Cameroon are strongly related to those of human immunodeficiency virus group N from the same geographic area. J Virol. 2000;74:529–34. 10.1128/JVI.74.1.529-534.2000
    1. Slattery JP, Franchini G, Gessain A. Genomic evolution, patterns of global dissemination, and interspecies transmission of human and simian T-cell leukemia/lymphotropic viruses. Genome Res. 1999;9:525–40.
    1. Calattini S, Nerrienet E, Mauclere P, Georges-Courbot MC, Saib A, Gessain A. Detection and molecular characterization of foamy viruses in Central African chimpanzees of the Pan troglodytes troglodytes and Pan troglodytes vellerosus subspecies. J Med Primatol. 2006;35:59–66. 10.1111/j.1600-0684.2006.00149.x
    1. Calattini S, Nerrienet E, Mauclere PMCG-C, Saib A, Gessain A. Natural simian foamy virus infection in wild-caught gorillas, mandrills and drills from Cameroon and Gabon. J Gen Virol. 2004;85:3313–7. 10.1099/vir.0.80241-0
    1. Calattini S, Wanert F, Thierry B, Schmitt C, Bassot S, Saib A, et al. Modes of transmission and genetic diversity of foamy viruses in a Macaca tonkeana colony. Retrovirology. 2006;3:23. 10.1186/1742-4690-3-23
    1. Broussard SR, Comuzzie AG, Leighton KL, Leland MM, Whitehead EM, Allan JS. Characterization of new simian foamy viruses from African nonhuman primates. Virology. 1997;237:349–59. 10.1006/viro.1997.8797
    1. Herchenroder O, Renne R, Loncar D, Cobb EK, Murthy KK, Schneider J, et al. Isolation, cloning, and sequencing of simian foamy viruses from chimpanzees (SFVcpz): high homology to human foamy virus (HFV). Virology. 1994;201:187–99. 10.1006/viro.1994.1285
    1. McClure MO, Bieniasz PD, Schulz TF, Chrystie IL, Simpson G, Aguzzi A, et al. Isolation of a new foamy retrovirus from orangutans. J Virol. 1994;68:7124–30.
    1. Hussain AI, Shanmugam V, Bhullar VB, Beer BE, Vallet D, Gautier-Hion A, et al. Screening for simian foamy virus infection by using a combined antigen Western blot assay: evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology. 2003;309:248–57. 10.1016/S0042-6822(03)00070-9
    1. Meiering CD, Linial ML. Historical perspective of foamy virus epidemiology and infection. Clin Microbiol Rev. 2001;14:165–76. 10.1128/CMR.14.1.165-176.2001
    1. Saib A. Non-primate foamy viruses. Curr Top Microbiol Immunol. 2003;277:197–211.
    1. Schweizer M, Schleer H, Pietrek M, Liegibel J, Falcone V, Neumann-Haefelin D. Genetic stability of foamy viruses: long-term study in an African green monkey population. J Virol. 1999;73:9256–65.
    1. Tobaly-Tapiero J, Bittoun P, Neves M, Guillemin MC, Lecellier CH, Puvion-Dutilleul F, et al. Isolation and characterization of an equine foamy virus. J Virol. 2000;74:4064–73. 10.1128/JVI.74.9.4064-4073.2000
    1. Switzer WM, Salemi M, Shanmugam V, Gao F, Cong ME, Kuiken C, et al. Ancient co-speciation of simian foamy viruses and primates. Nature. 2005;434:376–80. 10.1038/nature03341
    1. Delebecque F, Suspene R, Calattini S, Casartelli N, Saib A, Froment A, et al. Restriction of foamy viruses by APOBEC cytidine deaminases. J Virol. 2006;80:605–14. 10.1128/JVI.80.2.605-614.2006
    1. Falcone V, Leupold J, Clotten J, Urbanyi E, Herchenroder O, Spatz W, et al. Sites of simian foamy virus persistence in naturally infected African green monkeys: latent provirus is ubiquitous, whereas viral replication is restricted to the oral mucosa. Virology. 1999;257:7–14. 10.1006/viro.1999.9634
    1. Linial M. Why aren't foamy viruses pathogenic? Trends Microbiol. 2000;8:284–9. 10.1016/S0966-842X(00)01763-7
    1. Murray SM, Picker LJ, Axthelm MK, Linial ML. Expanded tissue targets for foamy virus replication with simian immunodeficiency virus-induced immunosuppression. J Virol. 2006;80:663–70. 10.1128/JVI.80.2.663-670.2006
    1. Jones-Engel L, Engel GA, Schillaci MA, Rompis A, Putra A, Suaryana KG, et al. Primate-to-human retroviral transmission in Asia. Emerg Infect Dis. 2005;11:1028–35.
    1. Plancoulaine S, Abel L, Tregouet D, Duprez R, van Beveren M, Tortevoye P, et al. Respective roles of serological status and blood specific antihuman herpesvirus 8 antibody levels in human herpesvirus 8 intrafamilial transmission in a highly endemic area. Cancer Res. 2004;64:8782–7. 10.1158/0008-5472.CAN-04-2000
    1. Gessain A, Mauclere P, Froment A, Biglione M, Le Hesran JY, Tekaia F, et al. Isolation and molecular characterization of a human T-cell lymphotropic virus type II (HTLV-II), subtype B, from a healthy Pygmy living in a remote area of Cameroon: an ancient origin for HTLV-II in Africa. Proc Natl Acad Sci U S A. 1995;92:4041–5. 10.1073/pnas.92.9.4041
    1. Jeannel D, Kourouma K, Fretz C, Zheng YM, Ureta VA, Drame L, et al. Regional differences in human retroviral infections HIV-1, HIV-2, and HTLV-I/II in rural Guinea (west Africa). J Acquir Immune Defic Syndr Hum Retrovirol. 1995;8:315–8. 10.1097/00042560-199503010-00016
    1. Tobaly-Tapiero J, Bittoun P, Saib A. Isolation of foamy viruses from peripheral blood lymphocytes. Methods Mol Biol. 2005;304:125–37.
    1. Schweizer M, Neumann-Haefelin D. Phylogenetic analysis of primate foamy viruses by comparison of pol sequences. Virology. 1995;207:577–82. 10.1006/viro.1995.1120
    1. Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817–8. 10.1093/bioinformatics/14.9.817
    1. Xia X, Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J Hered. 2001;92:371–3. 10.1093/jhered/92.4.371
    1. Engel G, Hungerford LL, Jones-Engel L, Travis D, Eberle R, Fuentes A, et al. Risk assessment: a model for predicting cross-species transmission of simian foamy virus from macaques (M. fascicularis) to humans at a monkey temple in Bali, Indonesia. Am J Primatol. 2006;68:934–48. 10.1002/ajp.20299

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