Nodule Worm Infection in Humans and Wild Primates in Uganda: Cryptic Species in a Newly Identified Region of Human Transmission

Abstract

Introduction

Soil-transmitted helminths (STHs) are a major health concern in tropical and sub-tropical countries. Oesophagostomum infection is considered endemic to West Africa but has also been identified in Uganda, East Africa, among primates (including humans). However, the taxonomy and ecology of Oesophagostomum in Uganda have not been studied, except for in chimpanzees ( Pan troglodytes), which are infected by both O. bifurcum and O. stephanostomum.

Methods and Findings

We studied Oesophagostomum in Uganda in a community of non-human primates that live in close proximity to humans. Prevalence estimates based on microscopy were lower than those based on polymerase chain reaction (PCR), indicating greater sensitivity of PCR. Prevalence varied among host species, with humans and red colobus ( Procolobus rufomitratus) infected at lowest prevalence (25% and 41% by PCR, respectively), and chimpanzees, olive baboons ( Papio anubis), and l'hoest monkeys ( Cercopithecus lhoesti) infected at highest prevalence (100% by PCR in all three species). Phylogenetic regression showed that primates travelling further and in smaller groups are at greatest risk of infection. Molecular phylogenetic analyses revealed three cryptic clades of Oesophagostomum that were not distinguishable based on morphological characteristics of their eggs. Of these, the clade with the greatest host range had not previously been described genetically. This novel clade infects humans, as well as five other species of primates.

Conclusions

Multiple cryptic forms of Oesophagostomum circulate in the people and primates of western Uganda, and parasite clades differ in host range and cross-species transmission potential. Our results expand knowledge about human Oesophagostomum infection beyond the West African countries of Togo and Ghana, where the parasite is a known public health concern. Oesophagostomum infection in humans may be common throughout Sub-Saharan Africa, and the transmission of this neglected STH among primates, including zoonotic transmission, may vary among host communities depending on their location and ecology.

Author Summary

Nodule worms infect the gastrointestinal tracts of a number of mammalian species, including humans and other primates. This study sought to identify the species of nodule worms causing infections within and around an East African national park in Uganda where monkeys and apes co-occur and overlap with people. Some primates, particularly those traversing large distances in small groups, were most susceptible to nodule worm infection. Additionally, molecular analyses identified three separate groups of nodule worm that could not be distinguished based on microscopic examination of their eggs. One of these groups was found in humans as well as other primates and had not previously been genetically characterized. These results suggest that certain types of nodule worm may be restricted to particular hosts, while others may be transmitted among primates, including humans. Nodule worms are currently thought to be a human health concern only in some West African countries. This research suggests that nodule worms have a broader geographic impact in humans than previously appreciated.