Primates

, Volume 54, Issue 1, pp 89–98 | Cite as

Epidemiological study of zoonoses derived from humans in captive chimpanzees

  • Takanori Kooriyama
  • Michiko Okamoto
  • Tomoyuki Yoshida
  • Toshisada Nishida
  • Toshio Tsubota
  • Akatsuki Saito
  • Masaki Tomonaga
  • Tetsuro Matsuzawa
  • Hirofumi Akari
  • Hidekazu Nishimura
  • Takako Miyabe-Nishiwaki
Original Article

Abstract

Emerging infectious diseases (EIDs) in wildlife are major threats both to human health and to biodiversity conservation. An estimated 71.8 % of zoonotic EID events are caused by pathogens in wildlife and the incidence of such diseases is increasing significantly in humans. In addition, human diseases are starting to infect wildlife, especially non-human primates. The chimpanzee is an endangered species that is threatened by human activity such as deforestation, poaching, and human disease transmission. Recently, several respiratory disease outbreaks that are suspected of having been transmitted by humans have been reported in wild chimpanzees. Therefore, we need to study zoonotic pathogens that can threaten captive chimpanzees in primate research institutes. Serological surveillance is one of several methods used to reveal infection history. We examined serum from 14 captive chimpanzees in Japanese primate research institutes for antibodies against 62 human pathogens and 1 chimpanzee-borne infectious disease. Antibodies tested positive against 29 pathogens at high or low prevalence in the chimpanzees. These results suggest that the proportions of human-borne infections may reflect the chimpanzee’s history, management system in the institute, or regional epidemics. Furthermore, captive chimpanzees are highly susceptible to human pathogens, and their induced antibodies reveal not only their history of infection, but also the possibility of protection against human pathogens.

Keywords

Chimpanzee Serology Captive Human-borne infection 

Supplementary material

10329_2012_320_MOESM1_ESM.pptx (78 kb)
Supplementary material 1 (PPTX 77.8 kb)

References

  1. Bermejo M, Rodriguez-Teijeiro JD, Illera G, Barroso A, Vila C, Walsh PD (2006) Ebola outbreak killed 5000 gorillas. Science 314(5805):1564PubMedCrossRefGoogle Scholar
  2. Bhattarakosol P, Pancharoen C, Mungmee V, Thammaborvorn R, Semboonlor L (2003) Seroprevalence of anti-RSV IgG in Thai children aged 6 months to 5 years. Asian Pac J Allergy Immunol 21(4):269–271PubMedGoogle Scholar
  3. Brack M (1987) Agents transmissible from simians to man. Springer, BerlinCrossRefGoogle Scholar
  4. Clark AG, Glanowski S, Nielsen R, Thomas PD, Kejariwal A, Todd MA, Tanenbaum DM, Civello D, Lu F, Murphy B, Ferriera S, Wang G, Zheng X, White TJ, Sninsky JJ, Adams MD, Cargill M (2003) Inferring nonneutral evolution from human–chimp–mouse orthologous gene trios. Science 302(5652):1960–1963PubMedCrossRefGoogle Scholar
  5. Cohen JI, Moskal T, Shapiro M, Purcell RH (1996) Varicella in chimpanzees. J Med Virol 50:289–292PubMedCrossRefGoogle Scholar
  6. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287(5452):443–449PubMedCrossRefGoogle Scholar
  7. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78(2):103–116PubMedCrossRefGoogle Scholar
  8. De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126CrossRefGoogle Scholar
  9. Dienstag JL, Davenport FM, McCollum RW, Hennessy AV, Klatskin G, Purcell RH (1976) Nonhuman primate-associated viral hepatitis type a: serologic evidence of hepatitis a virus infection. JAMA 236:462–464PubMedCrossRefGoogle Scholar
  10. Ferber D (2000) Primatology. Human diseases threaten great apes. Science 289(5483):1277–1278PubMedCrossRefGoogle Scholar
  11. Gerber P, Pritchett RF, Kieff ED (1976) Antigens and DNA of a chimpanzee agent related to Epstein–Barr virus. J Virol 19:1090–1099PubMedGoogle Scholar
  12. Gerber LR, McCallum H, Lafferty KD, Sabo JL, Dobson A (2005) Exposing extinction risk analysis to pathogens: is disease just another from of density dependence? Ecol Appl 15:1402–1414CrossRefGoogle Scholar
  13. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  14. Gustavssona OEA, Rökenb BO, Serrandera R (1990) An epizootic of whooping cough among chimpanzees in a zoo. Folia Primatol (Basel) 55:45–50CrossRefGoogle Scholar
  15. Hanamura S, Kiyono M, Lukasik-Braum M, Mlengeya T, Fujimoto M, Nakamura M, Nishida T (2008) Chimpanzee deaths at Mahale caused by a flu-like disease. Primates 49(1):77–80PubMedCrossRefGoogle Scholar
  16. Hosaka K (1995) A single flu epidemic killed at least 11 chimps. Pan Afr News 2:3–4Google Scholar
  17. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451(7181):990–993PubMedCrossRefGoogle Scholar
  18. Kaiser J (2003) Conservation biology. Ebola, hunting push ape populations to the brink. Science 300(5617):232Google Scholar
  19. Kalter SS, Heberling RL (1971) Comparative virology of primates. Bacteriol Rev 35:310–364PubMedGoogle Scholar
  20. Kaur T, Singh J, Tong S, Humphrey C, Clevenger D, Tan W, Szekely B, Wang Y, Li Y, Alex Muse E, Kiyono M, Hanamura S, Inoue E, Nakamura M, Huffman MA, Jiang B, Nishida T (2008) Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am J Primatol 70(8):755–765PubMedCrossRefGoogle Scholar
  21. King DA, Peckham C, Waage JK, Brownlie J, Woolhouse ME (2006) Epidemiology. Infectious diseases: preparing for the future. Science 313(5792):1392–1393Google Scholar
  22. Kishi N, Ota H, Maeda H, Obata M, Hayashi H, Takasugi N (1978) A serological study on parainfluenza viruses. Sapporo City Institute of Public Health, Research and Investigation annual report no. 5Google Scholar
  23. Kondgen S, Kuhl H, N’Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, Matz-Rensing K, Schweiger B, Junglen S, Ellerbrok H, Nitsche A, Briese T, Lipkin WI, Pauli G, Boesch C, Leendertz FH (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18(4):260–264PubMedCrossRefGoogle Scholar
  24. Lacoste V, Verschoor EJ, Nerrienet E, Gessain A (2005) A novel homologue of human herpesvirus 6 in chimpanzees. J Gen Virol 86:2135–2140PubMedCrossRefGoogle Scholar
  25. Le Guenno B, Formentry P, Wyers M, Gounon P, Walker F, Boesch C (1995) Isolation and partial characterisation of a new strain of Ebola virus. Lancet 345:1271–1274PubMedCrossRefGoogle Scholar
  26. Luebcke E, Dubovi E, Black D, Ohsawa K, Eberle R (2006) Isolation and characterization of a chimpanzee alpha herpesvirus. J Gen Virol 87(Pt 1):11–19PubMedCrossRefGoogle Scholar
  27. Matsuzawa T (2003) The Ai project: historical and ecological contexts. Anim Cogn 6(4):199–211PubMedCrossRefGoogle Scholar
  28. Matsuzawa T (2006) Sociocognitive development in chimpanzees: a synthesis of laboratory work and field work. I. In: Matsuzawa TT (ed) Cognitive development in chimpanzees. Springer, Tokyo, pp 3–33CrossRefGoogle Scholar
  29. Matsuzawa T, Humle T, Koops K, Biro D, Hayashi M, Sousa C, Mizuno Y, Kato A, Yamakoshi G, Ohashi G, Sugiyama Y, Kourouma M (2004) Wild Chimpanzees at Bossou-Nimba: deaths through a flu-like epidemic in 2003 and the green-corridor project. Primate Res 20:45–55CrossRefGoogle Scholar
  30. McMichael AJ (2004) Environmental and social influences on emerging infectious diseases: past, present and future. Philos Trans R Soc Lond B Biol Sci 359(1447):1049–1058PubMedCrossRefGoogle Scholar
  31. Miyabe-Nishiwaki T, Kaneko A, Nishiwaki K, Watanabe A, Watanabe S, Maeda N, Kumazaki K, Morimoto M, Hirokawa R, Suzuki J, Ito Y, Hayashi M, Tanaka M, Tomonaga M, Matsuzawa T (2010) Tetraparesis resembling acute transverse myelitis in a captive chimpanzee (Pan troglodytes): long-term care and recovery. J Med Primatol 39(5):336–346PubMedCrossRefGoogle Scholar
  32. Morell V (1994) Chimpanzee outbreak heats up search for Ebola origin. Science 268:974–975CrossRefGoogle Scholar
  33. Morens DM, Folkers GK, Fauci AS (2004) The challenge of emerging and re-emerging infectious diseases. Nature 430(6996):242–249PubMedCrossRefGoogle Scholar
  34. Morris JA, Blount RE Jr, Savage RE (1956) Recovery of cytopathogenic agent from chimpanzees with coryza. Proc Soc Exp Biol Med 92(3):544–549PubMedGoogle Scholar
  35. Muehlenbein MP, Ancrenaz M (2009) Vaccination and health status of foreign travelers, and the roles of travel medicine specialists. Great ape health workshop 2009, 21–24 August 2009, Entebbe, UgandaGoogle Scholar
  36. NIH (National Institute of Health, Japan) (2008) The topic of this month, vol 29, No. 3 (No. 337) “Pertussis, Japan, 2005–2007”. Infect Agents Suveil Rep 29:65–66. (http://idsc.nih.go.jp/iasr/29/337/tpc337.html)
  37. NIID (2008) Japanese encephalitis. Department of Virology I, National Institute of Infectious disease, Japan. http://www.nih.go.jp/vir1/NVL/JEVMeeting.htm
  38. Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M, Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primatol 59(3):99–121PubMedCrossRefGoogle Scholar
  39. Nunn CL, Thrall PH, Stewart, Harcour AH (2008) Emerging infectious diseases and animal social system. Evol Ecol 22:519–54Google Scholar
  40. Okamoto M, Sugawara K, Takashita E, Muraki Y, Hongo S, Mizuta K, Itagaki T, Nishimura H, Matsuzaki Y (2010) Development and evaluation of a whole virus-based enzyme-linked immunosorbent assay for the detection of human metapneumovirus antibodies in human sera. J Virol Methods 164(1–2):24–29PubMedCrossRefGoogle Scholar
  41. Patz JA, Daszak P, Tabor GM, Aguirre AA, Pearl M, Epstein J, Wolfe ND, Kilpatrick AM, Foufopoulos J, Molyneux D, Bradley DJ (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112(10):1092–1098PubMedCrossRefGoogle Scholar
  42. Robbins MM, Gray M, Fawcett KA, Nutter FB, Uwingeli P, Mburanumwe I, Kagoda E, Basabose A, Stoinski TS, Cranfield MR, Byamukama J, Spelman LH, Robbins AM (2011) Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One 6(6):e19788PubMedCrossRefGoogle Scholar
  43. Roy S, Vandenberghe LH, Kryazhimskiy S, Grant R, Calcedo R, Yuan X, Keough M, Sandhu A, Wang Q, Medina-Jaszek CA, Plotkin JB, Wilson JM (2009) Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog 5(7):e1000503PubMedCrossRefGoogle Scholar
  44. Ryan SJ, Walsh PD (2011) Consequences of non-intervention for infectious disease in African great apes. PLoS One 6(12):e29030Google Scholar
  45. Sato H, Taya K, Okabe N, Takasaki T, Kurane I (2009) Seroprevalence rate against Japanese encephalitis in domestic pig in Japan. IASR 30:151–152 (Infectious disease surveillance center, National institute of Infectious disease, Japan. http://idsc.nih.go.jp/iasr/30/352/dj3522.html)Google Scholar
  46. Swinkels BW, Geelen JLMC, Wertheim-van Dillen P, van Es AA, van der Noordaa J (1984) Initial characterization of four cytomegalovirus strains isolated from chimpanzees. Arch Virol 82:125–128PubMedCrossRefGoogle Scholar
  47. Tachibana H, Cheng XJ, Kobayashi S, Fujita Y, Udono T (2000) Entamoeba dispar, but not E. histolytica, detected in a colony of chimpanzees in Japan. Parasitol Res 86(7):537–541PubMedCrossRefGoogle Scholar
  48. Takasaka M, Sakakibara I, Mukai R, Suzuki M (1990) An outbreak of nonhuman primate varicella-like herpesvirus infection in the established breeding colony of cynomolgus monkeys. Tsukuba Primate Center News 9:5–11Google Scholar
  49. Taya K, Sato H, Arai T, Kitamoto R, Okabe N (2011) Seroepidemiological survey and vaccination coverage against measles virus 2010: 2010 interim report forecasting survey for infectious disease epidemics. IASR 32:36–39 (Infectious disease surveillance center, National Institute of Infectious disease, Japan. http://idsc.nih.go.jp/iasr/32/372/dj3723.html)
  50. Taylor LH, Latham SM, Woolhouse ME (2001) Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 356(1411):983–989PubMedCrossRefGoogle Scholar
  51. Walsh PD (2009) VaccinApe: protecting wild apes against the disease threat. Great ape health workshop, Entebbe, Uganda, 21–24 AugustGoogle Scholar
  52. Weiss RA, McMichael AJ (2004) Social and environmental risk factors in the emergence of infectious diseases. Nat Med 10(12 Suppl):S70–S76PubMedCrossRefGoogle Scholar
  53. Whitfield J (2003) The law of the jungle. Nature 421(6918):8–9PubMedCrossRefGoogle Scholar
  54. Whittier CA, Nutter FB, Stoskofp MK (2001) Zoonotic disease concerns in primate field settings. The apes: challenges for the 21st century, conference proceedings, May 10–13, 2000. Brookfield Zoo, Brookfield, pp 232–237Google Scholar
  55. Willimzik H-F, Kalter SS, Lester TL, Wigand R (1981) Immunological relationship among adenoviruses of humans, simians, and nonprimates as determined by the neutralization test. Intervirology 15:28–36PubMedCrossRefGoogle Scholar
  56. Wold W (2007) Adenovirus fields virology, vol 2, 5th edn, p 2395Google Scholar
  57. Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36:153–160CrossRefGoogle Scholar
  58. Woolhouse ME, Gowtage-Sequeria S (2005) Host range and emerging and reemerging pathogens. Emerg Infect Dis 11(12):1842–1847PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2012

Authors and Affiliations

  • Takanori Kooriyama
    • 1
    • 2
    • 3
  • Michiko Okamoto
    • 4
    • 5
  • Tomoyuki Yoshida
    • 6
  • Toshisada Nishida
    • 2
  • Toshio Tsubota
    • 3
  • Akatsuki Saito
    • 6
  • Masaki Tomonaga
    • 6
  • Tetsuro Matsuzawa
    • 6
  • Hirofumi Akari
    • 6
  • Hidekazu Nishimura
    • 4
  • Takako Miyabe-Nishiwaki
    • 6
  1. 1.Rakuno Gakuen UniversityEbetsuJapan
  2. 2.Japan Monkey CentreInuyamaJapan
  3. 3.Hokkaido UniversitySapporoJapan
  4. 4.Sendai Medical CenterSendaiJapan
  5. 5.Tohoku UniversitySendaiJapan
  6. 6.Kyoto UniversityInuyamaJapan

Personalised recommendations