Skip to main content

Advertisement

SpringerLink
Log in

Zoonotic Enterobacterial Pathogens Detected in Wild Chimpanzees

  • Short Communication
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Infectious diseases including those acquired through direct or indirect contact with people and livestock threaten the survival of wild great apes. Few studies have reported enterobacterial pathogens in chimpanzees. We used multiplex PCR to screen faeces of chimpanzees sharing a landscape with villagers and livestock in Bulindi, Uganda for Salmonella spp., enterohemorrhagic Escherichia coli (E. coli) and Shigella spp./enteroinvasive E. coli. All three potentially zoonotic pathogens were detected. Individual prevalence ranged between 7 and 20%, with most infections observed in mature male chimpanzees. These preliminary findings suggest detailed investigation of enterobacterial infections in people, primates and livestock in this ecosystem is warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1

References

  • Beisner BA, Balasubramaniam KN, Fernandez K, Heagerty A, Seil SK, Atwill ER, et al. (2016) Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India. Primates 57:459–469

    Article  PubMed  Google Scholar 

  • Beutin L (2006) Emerging enterohaemorrhagic Escherichia coli, causes and effects of the rise of a human pathogen. Journal of Veterinary Medicine Series B 53:299–305

    Article  PubMed  CAS  Google Scholar 

  • Bublitz DC, Wright PC, Rasambainarivo FT, Arrigo‐Nelson SJ, Bodager JR, Gillespie TR (2015) Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance. American Journal of Primatology 77:330–337

    Article  PubMed  Google Scholar 

  • Chapman CA, Gillespie TR, Goldberg TL (2005) Primates and the ecology of their infectious diseases: how will anthropogenic change affect host‐parasite interactions? Evolutionary Anthropology 14:134–144

    Article  Google Scholar 

  • Cibot M, Sabiiti T, McLennan MR (2017) Two cases of chimpanzees interacting with dead animals without food consumption at Bulindi, Hoima District, Uganda. Pan Africa News 24(1):6–8

    Article  Google Scholar 

  • De Nys HM, Madinda NF, Merkel K, Robbins M, Boesch C, Leendertz FH, Calvignac‐Spencer S (2015) A cautionary note on fecal sampling and molecular epidemiology in predatory wild great apes. American Journal of Primatology 77:833–840

    Article  PubMed  Google Scholar 

  • Enurah LU, Uche EMI, Nawathe DR (1988) Fatal shigellosis in a chimpanzee (Pan troglodytes) in the Jos Zoo, Nigeria. Journal of Wildlife Diseases 24:178–179

    Article  PubMed  CAS  Google Scholar 

  • Gilardi KV, Gillespie TR, Leendertz FH, Macfie EJ, Travis DA, Whittier CA, Williamson, EA (2015) Best practice guidelines for health monitoring and disease control in great ape populations. Gland, Switzerland: IUCN SSC Primate Specialist Group

    Book  Google Scholar 

  • Goldberg TL, Gillespie TR, Rwego IB, Estoff EL, Chapman CA (2008) Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerging Infectious Diseases 14:1375–1382

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA (2007) Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation 135:511–517.

    Article  Google Scholar 

  • Hasegawa H, Kalousova B, McLennan MR, Modry D, Profousova-Psenkova I, Shutt-Phillips KA, et al. (2016) Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitology International 65:367–370

    Article  PubMed  Google Scholar 

  • Hasegawa H, Shigyo M, Yanai Y, McLennan MR, Fujita S, Makouloutou P, et al. (2017) Molecular features of hookworm larvae (Necator spp.) raised by coproculture from Ugandan chimpanzees and Gabonese gorillas and humans. Parasitology International 66:12–15

    Article  PubMed  CAS  Google Scholar 

  • Hockings KJ, Anderson JR, Matsuzawa T (2012) Socioecological adaptations by chimpanzees, Pan troglodytes verus, inhabiting an anthropogenically impacted habitat. Animal Behaviour 83:801–810

    Article  Google Scholar 

  • Kaur T, Singh J, Huffman MA, Petrželková KJ, Taylor NS, Xu S, et al. (2011) Campylobacter troglodytis sp. nov., isolated from feces of human-habituated wild chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Applied and Environmental Microbiology 77:2366–2373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, et al. (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. The Lancet 382:209–222

    Article  Google Scholar 

  • Krief S, Vermeulen B, Lafosse S, Kasenene JM, Nieguitsil A, Berthelemy M, et al. (2010) Nodular worm infection in wild chimpanzees in Western Uganda: a risk for human health? PLoS Neglected Tropical Diseases 4:e630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, et al. (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clinical Infectious Diseases 50:882–889

    Article  PubMed  Google Scholar 

  • McLennan MR (2010) Case study of an unusual human–chimpanzee conflict at Bulindi, Uganda. Pan Africa News 17(1):1–4

    Article  Google Scholar 

  • McLennan MR (2013) Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: foraging strategies at the forest–farm interface. International Journal of Primatology 34:585–614

    Article  Google Scholar 

  • McLennan MR, Asiimwe C (2016) Cars kill chimpanzees: case report of a wild chimpanzee killed on a road at Bulindi, Uganda. Primates 57:377–388

    Article  PubMed  Google Scholar 

  • McLennan MR, Hasegawa H, Bardi M, Huffman MA (2017) Gastrointestinal parasite infections and self-medication in wild chimpanzees surviving in degraded forest fragments within an agricultural landscape mosaic in Uganda. PLoS One 12: e0180431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McLennan MR, Huffman MA (2012) High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in “village” chimpanzees at Bulindi, Uganda. American Journal of Primatology 74:642–650

    Article  PubMed  Google Scholar 

  • Nizeyi JB, Rwego IB, Erume J, Kalema GR, Cranfield MR, Graczyk TK (2001) Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. Journal of Wildlife Diseases 37:239–244

    Article  PubMed  CAS  Google Scholar 

  • Nunn C, Altizer SM (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford: Oxford University Press

    Book  Google Scholar 

  • Ocholi RA, Enurah LU, Odeyemi PS (1987) Fatal case of salmonellosis (Salmonella pullorum) in a chimpanzee (Pan troglodytes) in the Jos Zoo. Journal of Wildlife Diseases 23:669–670

    Article  PubMed  CAS  Google Scholar 

  • Ota N, Hasegawa H, McLennan MR, Kooriyama T, Sato H, Pebsworth PA, Huffman MA (2015) Molecular identification of Oesophagostomum spp. from ‘village’ chimpanzees in Uganda and their phylogenetic relationship with those of other primates. Royal Society Open Science 2:150471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rewell RE (1949) Outbreak of Shigella schmitzii infection in men and apes. The Lancet 253(6545):220–221

    Article  Google Scholar 

  • Rwego IB, Isabirye‐Basuta G, Gillespie TR, Goldberg TL (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology 22:1600–1607

    Article  PubMed  Google Scholar 

  • van den Beld M, Reubsaet FAG (2012) Differentiation between Shigella, enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichia coli. European Journal of Clinical Microbiology & Infectious Diseases 31:899–904

    Article  Google Scholar 

Download references

Acknowledgements

This research was approved by the Uganda National Council for Science and Technology, the President’s Office, and the Uganda Wildlife Authority. All applicable institutional and/or national guidelines for the care and use of animals were followed. Sample collection was conducted with assistance from Tom Sabiiti. Matthew McLennan was supported by an Early Career Fellowship from the Leverhulme Trust, UK. Laboratory analysis was supported partly by JSPS Core-to-Core Program (B. Asia-Africa Science Platforms). The manuscript was improved by comments from two anonymous reviewers.

Author information

Authors and Affiliations

  1. Anthropology Centre for Conservation, Environment and Development, Oxford Brookes University, Oxford, OX3 0BP, UK

    Matthew R. McLennan

  2. Bulindi Chimpanzee & Community Project, PO Box 245, Hoima, Uganda

    Matthew R. McLennan

  3. Department of Protozoology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand

    Hirotake Mori, Aongart Mahittikorn & Rapeepun Prasertbun

  4. Department of Pathobiology, School of Veterinary Medicine, Rakuno Gakuen University, Hokkaido, Japan

    Katsuro Hagiwara

  5. Primate Research Institute, Kyoto University, Inuyama, 484, Japan

    Michael A. Huffman

Authors
  1. Matthew R. McLennan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirotake Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aongart Mahittikorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rapeepun Prasertbun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsuro Hagiwara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael A. Huffman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew R. McLennan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McLennan, M.R., Mori, H., Mahittikorn, A. et al. Zoonotic Enterobacterial Pathogens Detected in Wild Chimpanzees. EcoHealth 15, 143–147 (2018). https://doi.org/10.1007/s10393-017-1303-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-017-1303-4

Keywords

Search

Navigation