Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya

Abstract

Background Gastrointestinal parasites are neglected infections, yet they cause significant burden to animal and human health globally. To date, most studies of gastrointestinal parasites focus on host-parasite systems that involve either a single parasite or a host species. However, when hosts share habitat and resources, they may also cross-transmit generalist gastrointestinal parasites. Here we explore multi-host-parasite interactions in a single ecosystem to understand the infection patterns, especially those linked to livestock-wildlife interfaces and zoonotic risk. Methods We used both coprological methods (flotation and sedimentation; N = 1,138 fecal samples) and molecular identification techniques (rDNA and mtDNA; N = 18 larvae) to identify gastrointestinal parasites in nine sympatric host species (cattle, sheep, goats, wildebeest, Grant’s gazelles, Thomson’s gazelles, impala, vervet monkeys and baboons) in the Amboseli ecosystem, Kenya. Results We found that the host community harbored a diverse community of gastrointestinal helminths, including 22 species and/or morphotypes that were heterogeneously distributed across the hosts. Six zoonotic gastrointestinal helminths were identified: Trichuris spp., Trichostrongylus colubriformis , Enterobius spp. Oesophagostomum bifurcum , Strongyloides stercoralis and Strongyloides fuelleborni . The dominant parasite was Trichuris spp, whose ova occurred in two morphological types. Baboons were co-infected with Strongyloides fuelleborni and S . stercoralis . Conclusions We found that the interface zone shared by wild ungulates, livestock and non-human primates is rich in diversity of gastrointestinal helminths, of which some are extensively shared across the host species. Closely related host species were most likely to be infected by the same parasite species. Several parasites showed genetic sub-structuring according to either geography or host species. Of significance and contrary to expectation, we found that livestock had a higher parasite richness than wild bovids, which is a health risk for both conservation and livestock production. The zoonotic parasites are of public health risk, especially to pastoralist communities living in areas contiguous to wildlife areas. These results expand information on the epidemiology of these parasites and highlights potential zoonotic risk in East African savanna habitats.

Potentially zoonotic gastrointestinal nematodes co-infecting free ranging non-human primates in Kenyan urban centres

“…The diversity of STHs identified in selected Kenyan urban centres highlights the possible reservoir role played by NHPs in helminths urban ecology. The significant diversity of nematodes infecting different species of NHPs within urban and peri-urban centres compliments previous molecular surveys that detected helminths in free-ranging NHPs within remote wildlife habitats in Kenya (Akinyi et al, 2019;Obanda et al, 2019). In STHs endemic countries, re-infection has been observed in half of the children treated for intestinal worms (Jia et al, 2012) a phenomenon attributed to re-infection due to persistence of infective worm stages in the environment.…”

“…isolates from yellow baboon in Kenya (Obanda et al, 2019)which may be as a result of sub structuring according to host species.…”

“…cross-infection and zoonotic potential between human and NHPs. Nematodes in the genus Trichostrongylus are known to infect humans, wild animals, herbivorous animals (Obanda et al, 2019). Primates including humans become infected due to environmental contamination.…”

“…Previous surveys on helminths have focused on NHPs within wildlife reserves and rural forest habitats Akinyi et al, 2019;Obanda et al, 2019) leaving information gap on helminth zoonoses originating from free-ranging NHPs within urban and peri-urban centres. In East Africa, the sharing of habitats between NHPs and humans, such as public parks in major cities or watering points in peri-urban towns, may facilitate the crossspecies transmission of zoonotic STHs.…”

Relationship between the excretion of eggs of parasitic helminths in roe deer and local livestock density

“…Wild and domestic ungulates grazing successively in the same pasture can infect each other through the faecal–oral route with macroparasites that produce free-living stages able to survive in the environment. A recent study in the Amboseli ecosystem (Kenya) showed that wild ungulates and livestock share several GI helminth taxa, suggesting bidirectional exchanges of parasites (Obanda et al ., 2019). However, only a few experimental studies have shown effective successful cross-infection.…”