Research Article: Nodular Worm Infections in Wild Non-human Primates and Humans Living in the Sebitoli Area (Kibale National Park, Uganda): Do High Spatial Proximity Favor Zoonotic Transmission?

Date Published: October 9, 2015

Publisher: Public Library of Science

Author(s): Marie Cibot, Jacques Guillot, Sophie Lafosse, Céline Bon, Andrew Seguya, Sabrina Krief, Stephen John Davies.

Abstract: BackgroundNodular Oesophagostomum genus nematodes are a major public health concern in some African regions because they can be lethal to humans. Their relatively high prevalence in people has been described in Uganda recently. While non-human primates also harbor Oesophagostomum spp., the epidemiology of this oesophagostomosis and the role of these animals as reservoirs of the infection in Eastern Africa are not yet well documented.Methodology/Principal FindingsThe present study aimed to investigate Oesophagostomum infection in terms of parasite species diversity, prevalence and load in three non-human primates (Pan troglodytes, Papio anubis, Colobus guereza) and humans living in close proximity in a forested area of Sebitoli, Kibale National Park (KNP), Uganda. The molecular phylogenetic analyses provided the first evidence that humans living in the Sebitoli area harbored O. stephanostomum, a common species in free-ranging chimpanzees. Chimpanzees were also infected by O. bifurcum, a common species described in human populations throughout Africa. The recently described Oesophagostomum sp. found in colobine monkeys and humans and which was absent from baboons in the neighboring site of Kanyawara in KNP (10 km from Sebitoli), was only found in baboons. Microscopic analyses revealed that the infection prevalence and parasite load in chimpanzees were significantly lower in Kanyawara than in Sebitoli, an area more impacted by human activities at its borders.Conclusions/SignificanceThree different Oesophagostomum species circulate in humans and non-human primates in the Sebitoli area and our results confirm the presence of a new genotype of Oesophagostomum recently described in Uganda. The high spatiotemporal overlap between humans and chimpanzees in the studied area coupled with the high infection prevalence among chimpanzees represent factors that could increase the risk of transmission for O. stephanostomum between the two primate species. Finally, the importance of local-scale research for zoonosis risk management is important because environmental disturbance and species contact can differ, leading to different parasitological profiles between sites that are close together within the same forest patches.

Partial Text: Emerging zoonotic diseases are a serious threat to public health and animal conservation. This is especially true for apes, whose close phylogenetic relationship with humans increases the risk of zoonotic transmission between them. Although humans have always shared habitats with non-human primates, the dynamics of their relationships are rapidly changing nowadays. Indeed, non-human primate populations suffer from forest loss and fragmentation [1–3] and an increasing number of them live in anthropogenically disturbed habitats such as farmlands, human settlements, fragments of forest, and isolated protected areas [4–6]. As a consequence, people and non-human primates live in increasing spatial proximity to each other [7]. So far, several cases of pathogen transmission have been reported to have occurred between non-human primates and humans; these include the transmission of viruses (e.g. [8–10]), bacteria (e.g. [11–13]) as well as blood-borne parasites (e.g. [14–16]), and intestinal parasites (e.g. [17–21]).

In the present study, microscopic and molecular approaches were used to reveal the prevalence and parasitological load of Oesophagostomum sp. in three non-human primate species and humans living in close proximity in a forested area. Our results provide the first evidence that some humans living in the Sebitoli area are infected by O. stephanostomum, a common species in free-ranging chimpanzees. Moreover, the chimpanzees also harboured O. bifurcum, a species commonly described in humans. Finally, the existence of the new clade Oesophagostomum sp. described in black and white colobus monkeys and humans in Kanyawara (a neighboring site to Sebitoli) by Ghai et al. [18], was confirmed in the Sebitoli region as two baboon fecal samples were infected with it. Microscopy revealed that the infection prevalence and the parasite load were significantly higher in the Sebitoli chimpanzees than in the Kanyawara ones.



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