Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon

Abstract

Background Zoonotic diseases are a serious threat to both public health and animal conservation. Most non-human primates (NHP) are facing the threat of forest loss and fragmentation and are increasingly living in closer spatial proximity to humans. Humans are infected with soil-transmitted helminths (STH) at a high prevalence, and bidirectional infection with NHP has been observed. The aim of this study was to determine the prevalence, genetic diversity, distribution and presence of co-infections of STH in free-ranging gorillas, chimpanzees and other NHP species, and to determine the potential role of these NHP as reservoir hosts contributing to the environmental sustenance of zoonotic nematode infections in forested areas of Cameroon and Gabon. Methods A total of 315 faecal samples from six species of NHPs were analysed. We performed PCR amplification, sequencing and maximum likelihood analysis of DNA fragments of the internal transcribed spacer 2 (ITS2) nuclear ribosomal DNA to detect the presence and determine the genetic diversity of Oesophagostomum spp., Necator spp. and Trichuris spp., and of targeted DNA fragments of the internal transcribed spacer 1 (ITS1) to detect the presence of Ascaris spp. Results Necator spp. infections were most common in gorillas (35 of 65 individuals), but also present in chimpanzees (100 of 222 individuals) and in one of four samples from greater spot-nosed monkeys. These clustered with previously described type II and III Necator spp. Gorillas were also the most infected NHP with Oesophagostomum (51/65 individuals), followed by chimpanzees (157/222 individuals), mandrills (8/12 samples) and mangabeys (7/12 samples), with O. stephanostomum being the most prevalent species. Oesophagostomum bifurcum was detected in chimpanzees and a red-capped mangabey, and a non-classified Oesophagostomum species was detected in a mandrill and a red-capped mangabey. In addition, Ternidens deminutus was detected in samples from one chimpanzee and three greater spot-nosed monkeys. A significant relative overabundance of co-infections with Necator and Oesophagostomum was observed in chimpanzees and gorillas. Trichuris sp. was detected at low prevalence in a gorilla, a chimpanzee and a greater spot-nosed monkey. No Ascaris was observed in any of the samples analysed. Conclusions Our results on STH prevalence and genetic diversity in NHP from Cameroon and Gabon corroborate those obtained from other wild NHP populations in other African countries. Future research should focus on better identifying, at a molecular level, the species of Necator and Oesophagostomum infecting NHP and determining how human populations may be affected by increased proximity resulting from encroachment into sylvatic STH reservoir habitats. Graphical Abstract

Novel insight into the genetic diversity of strongylid nematodes infecting South-East and East Asian primates

“…Cryptic species of Oesophagostomum have previously been proposed for nodular worm infections in humans and NHPs in Uganda (Ghai et al ., 2014 ), with high genetic variability of Oesophagostomum spp. observed in African primates (Sirima et al ., 2021 ; Mason et al ., 2022 ). However, although the ITS-2 marker, also used in this study, is ideal for distinguishing between known species for which genetic data exists in repositories, it should be noted that this marker shows high levels of intraspecific variability, which may limit its value in identifying potential cryptic species (Conole et al ., 1999 ; Poissant et al ., 2021 ; Halvarsson and Tydén, 2023 ).…”

Zoonotic helminths – why the challenge remains

“…Smyth (1995) identified two nematodes as emerging zoonoses, Angiostrongylus costaricensis and Oesophagostomum bifurcum . Since then, the zoonotic significance of both parasites has increased and molecular tools have proved invaluable in terms of diagnosis, in the case of A. costaricensis (Rojas et al , 2021) and determining prevalence and genetic diversity of Oesophagostomum (Sirima et al , 2021).…”

A review of Gabonese gorillas and their pathogens: Diversity, transfer and One Health approach to avoid future outbreaks?

“…(E) leopold, Necator americanus, Oesophagostomum stephanostomum, Oesophagostomum spp., Paramphistomum spp., Strongyloides spp., Schistosoma mansoni, Troglodytella abrassarti, Troglodytella gorillae, Troglodytella spp., Goriliophilus thoracatus n.g, Troglodytella gabonensis n.sp., and Prototapirella gorillae n.sp. and several parasites that remain undetermined (Goussard et al, 1983;Imai et al, 1991;Bain et al, 1995;Landsoud-Soukate et al, 1995;Van Zijll Langhout et al, 2010;Hasegawa et al, 2017;Dibakou et al, 2021;Sirima et al, 2021) (Figure 1). Several of its species have been identified in gorillas living in different environments.…”

“…Concerning gastrointestinal parasites and bacteria, although cases of transfer between gorillas and humans in Gabon have not been demonstrated, several studies report cases of infection of captive and wild gorillas with geohelminths [Sch. Mansoni (C ̌ervenáet al, 2016), Necator americanus (Sirima et al, 2021), Cryptosporidium spp (van Zijll Langhout et al, 2010)], and bacteria [S. aureus (Nagel et al, 2013), Chlamydia-Related Bacteria (Klöckner et al, 2016), E. coli (Mbehang Nguema et al, 2021), K. pneumoniae (Mbehang Nguema et al, 2021;Shojaei et al, 2022) known to infect humans. However, for some bacteria like S. aureus, the origin of transfer has not been identified, i.e.…”