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?

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.

Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

“…General taxonomic assignment of 85 ITS-2 haplotypes obtained in this study indicates that the NHPs and humans at Dzanga-Sangha host at least nine genera of strongylid nematodes. The most prevalent genera were Oesophagostomum and Necator, which are common and the most studied strongylid nematodes in NHPs to date (e.g., Cibot et al, 2015;Hasegawa et al, 2017). Other genera found also represented previously identified NHP and human parasites and included: Ternidens, Trichostrongylus, Hyostrongylus, Murshidia and Ancylostoma (e.g., Brooker et al, 2004;Rothman & Bowman, 2003;Cibot et al, 2015;Hasegawa et al, 2017).…”

“…The most prevalent genera were Oesophagostomum and Necator , which are common and the most studied strongylid nematodes in NHPs to date (e.g., Cibot et al, ; Ghai, Chapman, et al, ; Hasegawa et al, ). Other genera found also represented previously identified NHP and human parasites and included: Ternidens , Trichostrongylus , Hyostrongylus, Murshidia and Ancylostoma (e.g., Brooker et al, ; Rothman & Bowman, ; Cibot et al, ; Ghai, Chapman, et al, ; Hasegawa et al, ). Two additional taxa could not been confidently assigned to genera as their ITS‐2 haplotypes did not have close matches in the reference databases and their taxonomic position within strongylids needs to be resolved.…”

“…On the contrary, eight strongylid genera were detected in chimpanzees and gorillas. Oesophagostomum stephanostomum , a common species found in great apes across African (e.g., Cibot et al, ; Ghai, Chapman, et al, ; Krief et al, ; Narat et al, ; Ota et al, ), represented the most abundant strongylid and showed close to 100% prevalence (e.g., OTUs 2, 6, 9). Other taxa found in considerable prevalence in gorillas and chimpanzees but absent in humans included Libyostrongylus (rather Paralibyostrongylus ), Ternidens deminutus , and two unassigned strongylid genera.…”

Molecular characterization of nodule worm in a community of Bornean primates

“…The other two nodule worm species that infect primates are O. stephanostomum and O. aculeatum . The former has been reported to infect chimpanzees ( Pan troglodytes schweinfurthii , Huffman et al, ; Huffman, Gotoh, Turner, Hamai, & Yoshida, , Krief et al, , Kooriyama et al, ) and gorillas ( Gorilla gorilla gorilla, Makouloutou et al, ) in the wild, but also humans in areas where humans, chimpanzees and other nonhuman primates live sympatrically (Cibot et al, ; Ota et al, ). However, O. stephanostomum has not been detected in humans living in close proximity to gorillas in Gabon (Makouloutou et al, ) or bonobos ( Pan paniscus ) in the Democratic Republic of the Congo (Narat et al, ), leading some to suggest that strains with differential capacities to infect humans may exist (Ota et al, ).…”

“…To overcome the limitations of morphological identification, there has been an increase in the use of molecular markers for clinical diagnostics and epidemiological studies, which have resulted in the identification of new lineages/strains within parasite species, showing new levels of diversity and transmission dynamics and suggesting that not all hosts are infected equally. In Uganda, two species of Oesophagostomum and a third uncharacterized and potentially zoonotic lineage have been reported to circulate in nonhuman primate communities and adjacent human populations (Cibot et al, ; Ghai, Chapman, Omeja, Davies, & Goldberg, ). A similar scenario has been documented for Trichuris spp., a whipworm infecting both humans and nonhuman primates in the same community (Ghai, Simons et al, ).…”