Coffey L, Forrester N, Tsetsarkin K, Vasilakis N, Weaver S, 2013. Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease. Future Microbiol 8: 155–176.
Schwartz O, Albert ML, 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8: 491–500.
Sergon K et al. 2004. Seroprevalence of chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. Am J Trop Med Hyg 78: 333–337.
Kumar N, Gopal S, 2010. Reemergence of chikungunya virus in Indian subcontinent. Indian J Virol 21: 8–17.
Kariuki Njenga M, Nderitu L, Ledermann JP, Ndirangu A, Logue C, Kelly CH, Sang RC, Sergon K, Breiman R, Powers AM, 2008. Tracking epidemic chikungunya virus into the Indian Ocean from east Africa. J Gen Virol 89: 2754–2760.
Volk SM et al. 2010. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 84: 6497–6504.
Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S, 2007. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3: e201.
Tsetsarkin KA et al. 2014. Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat Commun 5: 4084.
Vasilakis N, Cardosa J, Hanley KA, Holmes EC, Weaver SC, 2011. Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nat Rev Microbiol 9: 532–541.
Diallo D et al. 2012. Landscape ecology of sylvatic chikungunya virus and mosquito vectors in southeastern Senegal. PLoS Negl Trop Dis 6: e1649.
Powers AM, Brault AC, Tesh RB, Weaver SC, 2002. Re-emergence of chikungunya and o’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 81: 471–479.
Poss M, Biek R, Rodrigo A, 2002. Viruses as evolutionary tools to monitor population dynamics. Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC, eds. Conservation Medicine: Ecological Health in Practice. New York, NY: Oxford University Press, 118–129.
Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA, 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerg Infect Dis 4: 149–158.
Cranfield M, Gaffikin L, Sleeman J, Rooney M, 2002. The mountain gorilla and conservation medicine. Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC, eds. Conservation Medicine: Ecological Health in Practice. New York, NY: Oxford University Press, 282–296.
Jones KE, Patel N, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in human emerging infectious diseases. Nature 451: 990–993.
Leendertz FH, Pauli G, Mätz-Rensing K, Boardman W, Nunn CL, Ellerbrok H, Jenson SA, Junglen S, Boesch C, 2006. Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biol Conserv 131: 325–337.
Diallo M, Thonnon J, Traore-Lamizana M, Fontenille D, 1999. Vectors of chikungunya virus in Senegal: current data and transmission cycles. Am J Trop Med Hyg 60: 281–286.
Jupp PG, McIntosh BM, 1990. Aedes furcifer and other mosquitoes as vectors of Chikungunya virus at Mica, northeastern Transvaal, South Africa. J Am Mosq Control Assoc 6: 415–420.
Chen R, Puri V, Fedorova N, Lin D, Hari KL, Jain R, Rodas JD, Das SR, Shabman RS, Weaver SC, 2016. Comprehensive genome scale phylogenetic study provides new insights on the global expansion of chikungunya virus. J Virol 90: 10600–10611.
Williams MC, Woodall JP, Corbet PS, Gillett JD, 1965. O’nyong-Nyong fever: an epidemic virus disease in east Africa. 8. Virus isolations from Anopheles mosquitoes. Trans R Soc Trop Med Hyg 59: 300–306.
Karabatsos N, 1975. Antigenic relationships of group A arboviruses by plaque reduction neutralization testing. Am J Trop Med Hyg 24: 527–532.
LaBeaud A et al. 2015. High rates of O’nyong nyong and chikungunya virus transmission in coastal Kenya. PLoS Negl Trop Dis 9: e0003436.
Lutomiah J et al. 2013. Abundance, diversity, and distribution of mosquito vectors in selected ecological regions of Kenya: public health implications. J Vector Ecol 38: 134–142.
Rwaguma EB, Lutwama JJ, Sempala SD, Kiwanuka N, Kamugisha J, Okware S, Lanciotti R, Roehrig JT, Gubler DJ, 1997. Emergence of epidemic O’nyong-nyong fever in southwestern Uganda, after an absence of 35 years. Emerg Infect Dis 3: 77.
Hertz J et al. 2012. Chikungunya and dengue fever among hospitalized febrile patients in northern Tanzania. Am J Trop Med Hyg 86: 171–177.
Crump JA et al. 2013. Etiology of severe non-malaria febrile illness in northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis 7: e2324.
Levitt NH, Ramsburg HH, Hasty SE, Repik PM, Cole FE Jr, Lupton HW, 1986. Development of an attenuated strain of chikungunya virus for use in vaccine production. Vaccine 4: 157–162.
Lanciotti RS, Ludwig ML, Rwaguma EB, Lutwama JJ, Kram TM, Karabatsos N, Cropp BC, Miller BR, 1998. Emergence of epidemic O’nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology 252: 258–268.
Ochieng C et al. 2013. Mosquito-borne arbovirus surveillance at selected sites in diverse ecological zones of Kenya; 2007–2012. Virol J 10: 1–10.
Tigoi C, Lwande O, Orindi B, Irura Z, Ongus J, Sang R, 2010. Seroepidemiology of selected arboviruses in febrile patients visiting selected health facilities in the lake/river basin areas of Lake Baringo, Lake Naivasha, and Tana River, Kenya. Vector Borne Zoonotic Dis 15: 124–132.
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Chikungunya virus (CHIKV) is a globally emerging pathogen causing debilitating arthralgia and fever in humans. First identified in Tanzania (1953), this mosquito-borne alphavirus received little further attention until a 2004 re-emergence in Kenya from an unknown source. This outbreak subsequently spread to the Indian Ocean, with adaptation for transmission by a new urban vector. Under the hypothesis that sylvatic progenitor cycles of CHIKV exist in Kenya (as reported in West Africa, between non-human primates (NHPs) and arboreal Aedes spp. mosquitoes), we pursued evidence of enzootic transmission and human spillover events. We initially screened 252 archived NHP sera from Kenya using plaque reduction neutralization tests. Given an overall CHIKV seroprevalence of 13.1% (marginally higher in western Kenya), we sought more recent NHP samples during 2014 from sites in Kakamega County, sampling wild blue monkeys, olive baboons, and red-tailed monkeys (N = 33). We also sampled 34 yellow baboons near Kwale, coastal Kenya. Overall, CHIKV seropositivity in 2014 was 13.4% (9/67). Antibodies reactive against closely related o’nyong-nyong virus (ONNV) occurred; however, neutralization titers were too low to conclude ONNV exposure. Seroprevalence for the flavivirus dengue was also detected (28%), mostly near Kwale, suggesting possible spillback from humans to baboons. CHIKV antibodies in some juvenile and subadult NHPs suggested recent circulation. We conclude that CHIKV is circulating in western Kenya, despite the 2004 human outbreaks only being reported coastally. Further work to understand the enzootic ecology of CHIKV in east Africa is needed to identify sites of human spillover contact where urban transmission may be initiated.
Financial support: This work was financially supported by the UTMB McLaughlin Post-doctoral Fellowship awarded to GE, the UTMB Institute for Human Infections and Immunity, and NIH grant AI120942.
Authors’ addresses: Gillian Eastwood and Scott C. Weaver, Department of Pathology, University of Texas Medical Branch, Galveston, TX, E-mails: gill2g@hotmail.com and sweaver@utmb.edu. Rosemary C. Sang, Arbovirus/VHF Unit, Center for Virus Research, Kenya Medical Research Institute, Nairobi, Kenya, E-mail: rsang@kemri.org. Mathilde Guerbois, University of Texas Medical Branch, Galveston, TX, and Department of Pathology, Center for Tropical Diseases, Institute for Human Infections and Immunity, Galveston, TX, E-mail: maguerbo@utmb.edu. Evans L. N. Taracha, Department of Tropical and Infectious Diseases, Institute of Primate Research, Karen, Kenya, E-mail: evans.taracha@gmail.com.
Coffey L, Forrester N, Tsetsarkin K, Vasilakis N, Weaver S, 2013. Factors shaping the adaptive landscape for arboviruses: implications for the emergence of disease. Future Microbiol 8: 155–176.
Schwartz O, Albert ML, 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8: 491–500.
Sergon K et al. 2004. Seroprevalence of chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. Am J Trop Med Hyg 78: 333–337.
Kumar N, Gopal S, 2010. Reemergence of chikungunya virus in Indian subcontinent. Indian J Virol 21: 8–17.
Kariuki Njenga M, Nderitu L, Ledermann JP, Ndirangu A, Logue C, Kelly CH, Sang RC, Sergon K, Breiman R, Powers AM, 2008. Tracking epidemic chikungunya virus into the Indian Ocean from east Africa. J Gen Virol 89: 2754–2760.
Volk SM et al. 2010. Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 84: 6497–6504.
Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S, 2007. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3: e201.
Tsetsarkin KA et al. 2014. Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat Commun 5: 4084.
Vasilakis N, Cardosa J, Hanley KA, Holmes EC, Weaver SC, 2011. Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nat Rev Microbiol 9: 532–541.
Diallo D et al. 2012. Landscape ecology of sylvatic chikungunya virus and mosquito vectors in southeastern Senegal. PLoS Negl Trop Dis 6: e1649.
Powers AM, Brault AC, Tesh RB, Weaver SC, 2002. Re-emergence of chikungunya and o’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 81: 471–479.
Poss M, Biek R, Rodrigo A, 2002. Viruses as evolutionary tools to monitor population dynamics. Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC, eds. Conservation Medicine: Ecological Health in Practice. New York, NY: Oxford University Press, 118–129.
Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA, 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerg Infect Dis 4: 149–158.
Cranfield M, Gaffikin L, Sleeman J, Rooney M, 2002. The mountain gorilla and conservation medicine. Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC, eds. Conservation Medicine: Ecological Health in Practice. New York, NY: Oxford University Press, 282–296.
Jones KE, Patel N, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P, 2008. Global trends in human emerging infectious diseases. Nature 451: 990–993.
Leendertz FH, Pauli G, Mätz-Rensing K, Boardman W, Nunn CL, Ellerbrok H, Jenson SA, Junglen S, Boesch C, 2006. Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biol Conserv 131: 325–337.
Diallo M, Thonnon J, Traore-Lamizana M, Fontenille D, 1999. Vectors of chikungunya virus in Senegal: current data and transmission cycles. Am J Trop Med Hyg 60: 281–286.
Jupp PG, McIntosh BM, 1990. Aedes furcifer and other mosquitoes as vectors of Chikungunya virus at Mica, northeastern Transvaal, South Africa. J Am Mosq Control Assoc 6: 415–420.
Chen R, Puri V, Fedorova N, Lin D, Hari KL, Jain R, Rodas JD, Das SR, Shabman RS, Weaver SC, 2016. Comprehensive genome scale phylogenetic study provides new insights on the global expansion of chikungunya virus. J Virol 90: 10600–10611.
Williams MC, Woodall JP, Corbet PS, Gillett JD, 1965. O’nyong-Nyong fever: an epidemic virus disease in east Africa. 8. Virus isolations from Anopheles mosquitoes. Trans R Soc Trop Med Hyg 59: 300–306.
Karabatsos N, 1975. Antigenic relationships of group A arboviruses by plaque reduction neutralization testing. Am J Trop Med Hyg 24: 527–532.
LaBeaud A et al. 2015. High rates of O’nyong nyong and chikungunya virus transmission in coastal Kenya. PLoS Negl Trop Dis 9: e0003436.
Lutomiah J et al. 2013. Abundance, diversity, and distribution of mosquito vectors in selected ecological regions of Kenya: public health implications. J Vector Ecol 38: 134–142.
Rwaguma EB, Lutwama JJ, Sempala SD, Kiwanuka N, Kamugisha J, Okware S, Lanciotti R, Roehrig JT, Gubler DJ, 1997. Emergence of epidemic O’nyong-nyong fever in southwestern Uganda, after an absence of 35 years. Emerg Infect Dis 3: 77.
Hertz J et al. 2012. Chikungunya and dengue fever among hospitalized febrile patients in northern Tanzania. Am J Trop Med Hyg 86: 171–177.
Crump JA et al. 2013. Etiology of severe non-malaria febrile illness in northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis 7: e2324.
Levitt NH, Ramsburg HH, Hasty SE, Repik PM, Cole FE Jr, Lupton HW, 1986. Development of an attenuated strain of chikungunya virus for use in vaccine production. Vaccine 4: 157–162.
Lanciotti RS, Ludwig ML, Rwaguma EB, Lutwama JJ, Kram TM, Karabatsos N, Cropp BC, Miller BR, 1998. Emergence of epidemic O’nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology 252: 258–268.
Ochieng C et al. 2013. Mosquito-borne arbovirus surveillance at selected sites in diverse ecological zones of Kenya; 2007–2012. Virol J 10: 1–10.
Tigoi C, Lwande O, Orindi B, Irura Z, Ongus J, Sang R, 2010. Seroepidemiology of selected arboviruses in febrile patients visiting selected health facilities in the lake/river basin areas of Lake Baringo, Lake Naivasha, and Tana River, Kenya. Vector Borne Zoonotic Dis 15: 124–132.
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