Contact to Non-human Primates and Risk Factors for Zoonotic Disease Emergence in the Taï Region, Côte d’Ivoire
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Abstract
Elevated exposure levels to non-human primates (NHP) and NHP bushmeat represent major risk factors for zoonotic disease transmission in sub-Saharan Africa. Demography can affect personal nutritional behavior, and thus rates of contact to NHP bushmeat. Here, we analyzed demographic and NHP contact data from 504 participants of differing demographic backgrounds living in proximity to the Taï National Park in Western Côte d’Ivoire (CI) to identify factors impacting the risk of NHP exposure. Overall, participants’ contact rates to NHP were high, and increased along a gradient of bushmeat processing (e.g., 7.7% hunted, but 61.9% consumed monkeys). Contact to monkeys was significantly more frequent than to chimpanzees, most likely a reflection of meat availability and hunting effort. 17.2% of participants reported previous interaction with NHP pets. Generalized linear mixed model analysis revealed significant effects of sex, country of birth or ethnicity on rates of NHP bushmeat contact, with male participants from CI being at particular risk of exposure to NHP. The presence of zoonotic pathogens in humans and NHP in Taï further highlights the risk for zoonotic disease emergence in this region. Our results are relevant for formulating prevention strategies to reduce zoonotic pathogen burden in tropical Africa.
Keywords
bushmeat non-human primates zoonotic pathogen transmission sub-Saharan AfricaNotes
Acknowledgments
We thank all study participants for volunteering to contribute to this work. We also especially thank the sampling team during field investigations (among others Tapé Aimé Fréderic Bozoua, Eric Goueu, Joel Semporé and Dan Driscoll). The hospital at Taï and the Office Ivorien des Parcs et Réserves kindly provided logistic support, and regional health workers aided in sensibilizing the local population for the study. We are grateful towards the national and local health authorities in Côte d’Ivoire for collaborating on this study, as well as the according ethics commission for granting permission for this work. We also thank Kathrin Nowak for help with the figures, Roger Mundry for statistical advice and Christophe Boesch and Roman Wittig for helpful comments on the manuscript. This work was supported by the “Deutsche Forschungsgemeinschaft” (DFG) Grant LE1813/4-1.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Study approval was given by the Ivorian ethics commission (Comité national d’éthique et de la recherche, CNER, permit number 101 10/MSHP/CENR/P).
Informed consent
Informed consent was obtained from all individual participants included in the study.
Supplementary material
References
- Aghokeng AF, Ayouba A, Mpoudi-Ngole E, Loul S, Liegeois F, Delaporte E, and 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. Infection, Genetics and Evolution 10(3):386-396.PubMedPubMedCentralCrossRefGoogle Scholar
- Baayen RH. 2008. Analyzing Linguistic Data: A practical introduction to statistics. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
- Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba NF, Soropogui B, Sow MS, Keïta S, and De Clerck H. 2014. Emergence of Zaire Ebola virus disease in Guinea. New England Journal of Medicine 371(15):1418-1425.PubMedCrossRefGoogle Scholar
- Barr DJ, Levy R, Scheepers C, and Tily HJ. 2013. Random effects structure for confirmatory hypothesis testing: keep it maximal. Journal of Memory and Language 68(3):255-278.CrossRefGoogle Scholar
- Betsem E, Rua R, Tortevoye P, Froment A, and Gessain A. 2011. Frequent and recent human acquisition of simian foamy viruses through apes’ bites in central Africa. PLoS pathogens 7(10):e1002306.PubMedPubMedCentralCrossRefGoogle Scholar
- Beyers RL, Hart JA, Sinclair AR, Grossmann F, Klinkenberg B, and Dino S. 2011. Resource wars and conflict ivory: the impact of civil conflict on elephants in the Democratic Republic of Congo–the case of the Okapi Reserve. PloS one 6(11):e27129.PubMedPubMedCentralCrossRefGoogle Scholar
- Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, and White JS. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24(3):127-135.CrossRefGoogle Scholar
- Calattini S, Betsem EB, Froment A, Mauclere P, Tortevoye P, Schmitt C, Njouom R, Saib A, and Gessain A. 2007. Simian foamy virus transmission from apes to humans, rural Cameroon. Emerging infectious diseases 13(9):1314-1320.PubMedPubMedCentralCrossRefGoogle Scholar
- Calvignac-Spencer S, Adjogoua EV, Akoua-Koffi C, Hedemann C, Schubert G, Ellerbrok H, Leendertz SA, Pauli G, and Leendertz FH. 2012. Origin of human T-lymphotropic virus type 1 in rural Côte d’Ivoire. Emerging infectious diseases 18(5):830-833.PubMedPubMedCentralCrossRefGoogle Scholar
- Campbell G, Kühl H, N’Goran Kouame P, and Boesch C. 2008. Alarming decline of West African chimpanzees in Côte d’Ivoire. Current Biology 18(19):R903-904.PubMedCrossRefGoogle Scholar
- Covey RM, W. Scott 2014. Monkeys in a West African bushmeat market: implications for cercopithecid conservation in eastern Liberia. Tropical Conservation Science 7(1):115-125.Google Scholar
- Daszak P, Cunningham AA, and Hyatt AD. 2000. Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science (New York, NY) 287(5452):443-449.CrossRefGoogle Scholar
- Davies TJ, and Pedersen AB. 2008. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings Biological sciences/The Royal Society 275(1643):1695-1701.PubMedPubMedCentralCrossRefGoogle Scholar
- Dixon MG, and Schafer IJ. 2014. Ebola viral disease outbreak - west Africa, 2014. MMWR Morbidity and mortality weekly report 63(25):548-551.PubMedGoogle Scholar
- Draulans DaVK, Ellen. 2002. The impact of war on forest areas in the Democratic Republic of Congo. Oryx 36(1):35-40.CrossRefGoogle Scholar
- East T, Kümpel NF, Milner-Gulland EJ, and Rowcliffe JM. 2005. Determinants of urban bushmeat consumption in Rio Muni, Equatorial Guinea. Biological Conservation 126(2):206-215.CrossRefGoogle Scholar
- Espinosa S, Branch LC, and Cueva R. 2014. Road Development and the Geography of Hunting by an Amazonian Indigenous Group: Consequences for Wildlife Conservation. PloS one 9(12):e114916.PubMedPubMedCentralCrossRefGoogle Scholar
- Fa JE, Juste J, Burn RW, and Broad G. 2002. Bushmeat consumption and preferences of two ethnic groups in Bioko Island, West Africa. Human Ecology 30(3):397-416.CrossRefGoogle Scholar
- Fa JE, Olivero J, Farfán MÁ, Márquez AL, Duarte J, Nackoney J, Hall A, Dupain J, Seymour S, and Johnson PJ. 2015. Correlates of bushmeat in markets and depletion of wildlife. Conservation Biology.Google Scholar
- Formenty P, Boesch C, Wyers M, Steiner C, Donati F, Dind F, Walker F, and Le Guenno B. 1999. Ebola virus outbreak among wild chimpanzees living in a rain forest of Côte d’Ivoire. The Journal of infectious diseases 179 Suppl 1:S120-126.PubMedCrossRefGoogle Scholar
- Gatherer D. 2014. The 2014 Ebola virus disease outbreak in west Africa. The Journal of general virology.Google Scholar
- Gessain A, Rua R, Betsem E, Turpin J, and Mahieux R. 2013. HTLV-3/4 and simian foamy retroviruses in humans: discovery, epidemiology, cross-species transmission and molecular virology. Virology 435(1):187-199.PubMedCrossRefGoogle Scholar
- Gogarten JF, Akoua-Koffi C, Calvignac-Spencer S, Leendertz SA, Weiss S, Couacy-Hymann E, Kone I, Peeters M, Wittig RM, Boesch C et al.. 2014a. The ecology of primate retroviruses - an assessment of 12 years of retroviral studies in the Tai national park area, Cote dIvoire. Virology 460-461:147-153.PubMedCrossRefGoogle Scholar
- Gogarten JF, Akoua-Koffi C, Calvignac-Spencer S, Leendertz SAJ, Weiss S, Couacy-Hymann E, Koné I, Peeters M, Wittig RM, Boesch C et al.. 2014b. The ecology of primate retroviruses—An assessment of 12 years of retroviral studies in the Taï National Park area, Côte d’Ivoire. Virology 460–461(0):147-153.PubMedCrossRefGoogle Scholar
- Hahn BH, Shaw GM, De Cock KM, and Sharp PM. 2000. AIDS as a zoonosis: scientific and public health implications. Science (New York, NY) 287(5453):607-614.CrossRefGoogle Scholar
- Hoppe-Dominik BK, Hjalmar S., Radl G, and Fischer F. 2011. Long-term monitoring of large rainforest mammals in the Biosphere Reserve of Taï National Park, Côte d’Ivoire. African Journal of Ecology 49: 450-458.CrossRefGoogle Scholar
- International-Crisis-Group (2014) Côte d’Ivoire’s Great West: Key to Reconciliation. Africa Report No. 212. Belgium: International-Crisis-Group.Google Scholar
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, and Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451(7181):990-993.PubMedCrossRefGoogle Scholar
- Junker J, Boesch C, Mundry R, Stephens C, Lormie M, Tweh C, and Kühl HS. 2015. Education and access to fish but not economic development predict chimpanzee and mammal occurrence in West Africa. Biological Conservation 182(0):27-35.CrossRefGoogle Scholar
- Kamins AO, Rowcliffe JM, Ntiamoa-Baidu Y, Cunningham AA, Wood JL, and Restif O. 2014. Characteristics and risk perceptions of Ghanaians potentially exposed to bat-borne zoonoses through bushmeat. EcoHealth 12:104-120.PubMedPubMedCentralCrossRefGoogle Scholar
- Karesh WB, and Noble E. 2009. The bushmeat trade: increased opportunities for transmission of zoonotic disease. The Mount Sinai journal of medicine, New York 76(5):429-434.PubMedCrossRefGoogle Scholar
- Klee SR, Brzuszkiewicz EB, Nattermann H, Brüggemann H, Dupke S, Wollherr A, Franz T, Pauli G, Appel B, Liebl W et al.. 2010. The Genome of a Bacillus Isolate Causing Anthrax in Chimpanzees Combines Chromosomal Properties of B. cereus with B. anthracis Virulence Plasmids. PloS one 5(7):e10986.PubMedPubMedCentralCrossRefGoogle Scholar
- Köndgen S, Kühl H, N’Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, Matz-Rensing K, Schweiger B et al.. 2008. Pandemic human viruses cause decline of endangered great apes. Current Biology 18(4):260-264.PubMedCrossRefGoogle Scholar
- Leendertz FH, Boesch C, Ellerbrok H, Rietschel W, Couacy-Hymann E, and Pauli G. 2004. Non-invasive testing reveals a high prevalence of simian T-lymphotropic virus type 1 antibodies in wild adult chimpanzees of the Tai National Park, Côte d’Ivoire. The Journal of general virology 85(Pt 11):3305-3312.PubMedCrossRefGoogle Scholar
- Leendertz FH, Yumlu S, Pauli G, Boesch C, Couacy-Hymann E, Vigilant L, Junglen S, Schenk S, and Ellerbrok H. 2006. A new Bacillus anthracis found in wild chimpanzees and a gorilla from West and Central Africa. PLoS pathogens 2(1):e8.PubMedPubMedCentralCrossRefGoogle Scholar
- Leendertz SA, Junglen S, Hedemann C, Goffe A, Calvignac S, Boesch C, and Leendertz FH. 2010. High prevalence, coinfection rate, and genetic diversity of retroviruses in wild red colobus monkeys (Piliocolobus badius badius) in Tai National Park, Côte d’Ivoire. Journal of virology 84(15):7427-7436.PubMedPubMedCentralCrossRefGoogle Scholar
- Leroy EM, Rouquet P, Formenty P, Souquière S, Kilbourne A, Froment J-M, Bermejo M, Smit S, Karesh W, Swanepoel R et al.. 2004. Multiple Ebola Virus Transmission Events and Rapid Decline of Central African Wildlife. Science (New York, NY) 303(5656):387-390.CrossRefGoogle 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(6):659-673.CrossRefGoogle Scholar
- Malhi Y, Adu-Bredu S, Asare RA, Lewis SL, and Mayaux P. 2013. African rainforests: past, present and future. Philosophical transactions of the Royal Society of London Series B, Biological sciences 368(1625):20120312.PubMedPubMedCentralCrossRefGoogle Scholar
- Morozov VA, Leendertz FH, Junglen S, Boesch C, Pauli G, and Ellerbrok H. 2009. Frequent foamy virus infection in free-living chimpanzees of the Tai National Park (Côte d’Ivoire). The Journal of general virology 90(Pt 2):500-506.PubMedCrossRefGoogle Scholar
- Mouinga-Ondeme A, Caron M, Nkoghe D, Telfer P, Marx P, Saib A, Leroy E, Gonzalez JP, Gessain A, and Kazanji M. 2012. Cross-species transmission of simian foamy virus to humans in rural Gabon, Central Africa. Journal of virology 86(2):1255-1260.PubMedPubMedCentralCrossRefGoogle Scholar
- Mugisha L, Kücherer C, Ellerbrok H, Junglen S, Opuda-Asibo J, Joseph OO, Pauli G, Leendertz F (2010) Retroviruses in wild-born semi-captive East African sanctuary chimpanzees (Pan troglodytes schweinfurthii). The Open Veterinary Science Journal 4:6-10CrossRefGoogle Scholar
- Ngoran PK, Kouakou CY, Ngoran EK, Konaté S, Herbinger I, Yapi FA, Kuehl H, and Boesch C. 2013. Chimpanzee conservation status in the World Heritage Site Taï National Park, Côte d’Ivoire. International Journal of Innovation and Applied Studies 3(1):326-336.Google Scholar
- N’Goran PK, Boesch C, Mundry R, N’Goran EK, Herbinger I, Yapi FA, and Kuehl HS. 2012. Hunting, law enforcement, and African primate conservation. Conservation Biology 26(3):565-571.PubMedCrossRefGoogle Scholar
- Ndembi N, Kaptue L, and Ido E. 2009. Exposure to SIVmnd-2 in southern Cameroon: public health implications. AIDS reviews 11(3):135-139.PubMedGoogle Scholar
- Paige S, Frost SW, Gibson M, Jones J, Shankar A, Switzer W, Ting N, and Goldberg T. 2014. Beyond Bushmeat: Animal Contact, Injury, and Zoonotic Disease Risk in Western Uganda. EcoHealth 11:534-543.PubMedPubMedCentralCrossRefGoogle Scholar
- Peeters M, Courgnaud V, Abela B, Auzel P, Pourrut X, Bibollet-Ruche F, Loul S, Liegeois F, Butel C, Koulagna D et al.. 2002. Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerging infectious diseases 8(5):451-457.PubMedPubMedCentralCrossRefGoogle Scholar
- Pouliot M, and Treue T. 2013. Rural People’s Reliance on Forests and the Non-Forest Environment in West Africa: Evidence from Ghana and Burkina Faso. World Development 43(0):180-193.CrossRefGoogle Scholar
- Poulsen J, Clark C, Mavah G, and Elkan P. 2009. Bushmeat supply and consumption in a tropical logging concession in northern Congo. Conservation Biology 23(6):1597-1608.PubMedCrossRefGoogle Scholar
- Radonić A, Metzger S, Dabrowski PW, Couacy-Hymann E, Schuenadel L, Kurth A, Mätz-Rensing K, Boesch C, Leendertz FH, and Nitsche A. 2014. Fatal Monkeypox in Wild-Living Sooty Mangabey, Côte d’Ivoire, 2012. Emerging infectious diseases 20(6):1009-1011.PubMedPubMedCentralCrossRefGoogle Scholar
- Refisch JK, Koné I 2005. Impact of Commercial Hunting on Monkey Populations in the Tai region, Côte d’Ivoire. Biotropica 37(1):136-144.CrossRefGoogle Scholar
- Rouquet P, Froment J-M, Bermejo M, Kilbourne A, Karesh WB, Reed P, Kumulungui B, Yaba P, Délicat A, Rollin PE et al.. 2005. Wild Animal Mortality Monitoring and Human Ebola Outbreaks, Gabon and Republic of Congo, 2001–2003. Emerging Infectious Disease 11(2):283.CrossRefGoogle Scholar
- Santiago ML, Range F, Keele BF, Li Y, Bailes E, Bibollet-Ruche F, Fruteau C, Noe R, Peeters M, Brookfield JF et al.. 2005. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Côte d’Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. Journal of virology 79(19):12515-12527.PubMedPubMedCentralCrossRefGoogle Scholar
- Schielzeth H, and Forstmeier W. 2009. Conclusions beyond support: overconfident estimates in mixed models. Behavioral Ecology 20:416-420.PubMedPubMedCentralCrossRefGoogle Scholar
- Sharp PM, and Hahn BH. 2011. Origins of HIV and the AIDS pandemic. Cold Spring Harbor Perspectives in Medicine 1(1):a006841.PubMedPubMedCentralCrossRefGoogle Scholar
- Smith KM, Anthony SJ, Switzer WM, Epstein JH, Seimon T, Jia H, Sanchez MD, Huynh TT, Galland GG, Shapiro SE et al.. 2012. Zoonotic viruses associated with illegally imported wildlife products. PloS one 7(1):e29505.PubMedPubMedCentralCrossRefGoogle Scholar
- Switzer WM, Bhullar V, Shanmugam V, Cong ME, Parekh B, Lerche NW, Yee JL, Ely JJ, Boneva R, Chapman LE et al.. 2004. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. Journal of virology 78(6):2780-2789.PubMedPubMedCentralCrossRefGoogle Scholar
- Switzer WM, Tang S, Ahuka-Mundeke S, Shankar A, Hanson DL, Zheng H, Ayouba A, Wolfe ND, LeBreton M, Djoko CF et al.. 2012. Novel simian foamy virus infections from multiple monkey species in women from the Democratic Republic of Congo. Retrovirology 9(1):100.PubMedPubMedCentralCrossRefGoogle Scholar
- Tranquilli S, Abedi-Lartey M, Abernethy K, Amsini F, Asamoah A, Balangtaa C, Blake S, Bouanga E, Breuer T, and Brncic TM. 2014. Protected Areas in Tropical Africa: Assessing Threats and Conservation Activities. PloS one 9(12):e114154.PubMedPubMedCentralCrossRefGoogle Scholar
- United-Nations-Educational-Scientific-and-Cultural-Organization (2015) Taï National Park. World Heritage List. http://whc.unesco.org/en/list/195/.
- WCF. 2013. Annual report 2013; Activities of the Wild Chimpanzee Foundation for improved conservation of chimpanzees and their habitat in West Africa. Annual report. Available at: http://www.wildchimps.org/.
- Weiss S, Nowak K, Fahr J, Wibbelt G, Mombouli JV, Parra HJ, Wolfe ND, Schneider BS, and Leendertz FH. 2012. Henipavirus-related sequences in fruit bat bushmeat, Republic of Congo. Emerging infectious diseases 18(9):1536-1537.PubMedPubMedCentralCrossRefGoogle Scholar
- WHO-Ebola-Response-Team (2014) Ebola virus disease in West Africa—the first 9 months of the epidemic and forward projections. New England Jorunal of Medicine. 371:1481-1495.CrossRefGoogle Scholar
- Wild-Chimpanzee-Foundation (2013) Annual report 2013; Activities of the Wild Chimpanzee Foundation for improved conservation of chimpanzees and their habitat in West Africa. Annual report. http://www.wildchimps.org/.
- Wilkie DS, Sidle JG, and Boundzanga GC. 1992. Mechanized Logging, Market Hunting, and a Bank Loan in Congo. Conservation Biology 6(4):570-580.CrossRefGoogle Scholar
- Wolfe ND, Prosser TA, Carr JK, Tamoufe U, Mpoudi-Ngole E, Torimiro JN, LeBreton M, McCutchan FE, Birx DL, and Burke DS. 2004a. Exposure to nonhuman primates in rural Cameroon. Emerging infectious diseases 10(12):2094-2099.PubMedPubMedCentralCrossRefGoogle Scholar
- Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, Prosser AT, Torimiro JN, Wright A, Mpoudi-Ngole E et al.. 2004e. Naturally acquired simian retrovirus infections in central African hunters. Lancet 363(9413):932-937.PubMedCrossRefGoogle Scholar
- Wolfe ND, Daszak P, Kilpatrick AM, and Burke DS. 2005a. Bushmeat hunting, deforestation, and prediction of zoonoses emergence. Emerging infectious diseases 11(12):1822-1827.PubMedPubMedCentralCrossRefGoogle Scholar
- Wolfe ND, Heneine W, Carr JK, Garcia AD, Shanmugam V, Tamoufe U, Torimiro JN, Prosser AT, Lebreton M, Mpoudi-Ngole E et al.. 2005d. 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 102(22):7994-7999.PubMedPubMedCentralCrossRefGoogle Scholar
- Wolfe ND, Dunavan CP, and Diamond J. 2007. Origins of major human infectious diseases. Nature 447(7142):279-283.PubMedCrossRefGoogle Scholar
- Wood B, and Marlowe F. 2013. Household and Kin Provisioning by Hadza Men. Hum Nat 24(3):280-317.PubMedCrossRefGoogle Scholar
- Yapi AF, N’Goran KP, Normand E, Herbinger I, Diarrassouba A, Tondossama A, and Boesch C (2011) État du parc national de Tai; rapport de resultats de biomonitoring; Phase VI (Octobre 2010—Mars 2011). In: Wild Chimpanzee Foundation (WCF), and Office Ivoirien des Parcs et Réserves Direction de Zone Sud-Ouest (OIPR/DZSO), editors. État du parc national de Tai; rapport de resultats de biomonitoring.Google Scholar