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Erschienen in: EcoHealth 1/2018

23.01.2018 | Review

Pathogen Transmission from Humans to Great Apes is a Growing Threat to Primate Conservation

verfasst von: Emily Dunay, Kathleen Apakupakul, Stephen Leard, Jamie L. Palmer, Sharon L. Deem

Erschienen in: EcoHealth | Ausgabe 1/2018

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Abstract

All six great ape species are listed as endangered or critically endangered by the IUCN and experiencing decreasing population trends. One of the threats to these non-human primates is the transmission of pathogens from humans. We conducted a literature review on occurrences of pathogen transmission from humans to great apes to highlight this often underappreciated issue. In total, we found 33 individual occurrences of probable or confirmed pathogen transmission from humans to great apes: 23 involved both pathogen and disease transmission, 7 pathogen transmission only, 2 positive antibody titers to zoonotic pathogens, and 1 pathogen transmission with probable disease. Great ape populations were categorized into captive, semi-free-living, and free-living conditions. The majority of occurrences involved chimpanzees (Pan troglodytes) (n = 23) or mountain gorillas (Gorilla beringei beringei) (n = 8). These findings have implications for conservation efforts and management of endangered great ape populations. Future efforts should focus on monitoring and addressing zoonotic pathogen and disease transmission between humans, great ape species, and other taxa to ensure the health of humans, wild and domestic animals, and the ecosystems we share.
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Metadaten
Titel
Pathogen Transmission from Humans to Great Apes is a Growing Threat to Primate Conservation
verfasst von
Emily Dunay
Kathleen Apakupakul
Stephen Leard
Jamie L. Palmer
Sharon L. Deem
Publikationsdatum
23.01.2018
Verlag
Springer US
Erschienen in
EcoHealth / Ausgabe 1/2018
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1306-1

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