Genetic evidence for the role of non-human primates as reservoir hosts for human schistosomiasis

Type Article
Date 2020-09
Language English
Author(s) Kebede Tadesse1, 3, 4, Bech Nicolas2, Allienne Jean-François3, Olivier Rey3, Erko Berhanu4, Boissier Jerome3
Affiliation(s) 1 : Department of Microbiology, Immunology and Parasitology, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia, Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia
2 : Laboratory of Ecologie et Biologie des Interactions (EBI), UMR CNRS 7267, Poitiers University, Poitiers, France
3 : Laboratoire Interactions Hôtes-Pathogènes-Environnements (IHPE), UMR 5244 CNRS, University of Perpignan, IFREMER, Univ. Montpellier, F-66860 Perpignan, France
4 : Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia
Source Plos Neglected Tropical Diseases (1935-2735) (Public Library of Science (PLoS)), 2020-09 , Vol. 14 , N. 9 , P. e0008538 (20p.)
DOI 10.1371/journal.pntd.0008538
WOS© Times Cited 2
Abstract

Background

Schistosomiasis is a chronic parasitic disease, that affects over 207 million people and causes over 200,000 deaths annually, mainly in sub-Saharan Africa. Although many health measures have been carried out to limit parasite transmission, significant numbers of non-human primates such as Chlorocebus aethiops (Ch. aethiops) (vervet) and Papio anubis (baboon) are infected with S. mansoni, notably in Ethiopia, where they are expected to have potentially significant implications for transmission and control efforts.

Objective

 

The objective of this study was to assess and compare the genetic diversity and population structure of S. mansoni isolates from human and non-human primates free-ranging in close proximity to villages in selected endemic areas of Ethiopia.

Methods

 

A cross-sectional study was conducted in three transmission sites: Bochesa, Kime and Fincha. A total of 2,356 S. mansoni miracidia were directly isolated from fecal specimens of 104 hosts (i.e. 60 human hosts and 44 non-human primates). We performed DNA extraction and PCR amplification using fourteen microsatellite loci.

Results

 

At population scale we showed strong genetic structure between the three sample sites. At the definitive host scale, we observed that host factors can shape the genetic composition of parasite infra-populations. First, in male patients, we observed a positive link between parasite genetic diversity and the age of the patients. Second, we observed a difference in genetic diversity which was high in human males, medium in human females and low in non-human primates (NHPs). Finally, whatever the transmission site no genetic structure was observed between human and non-human primates, however, there appears to be little barriers, if any, host specificity of the S. mansoni populations with cross-host infections.

Conclusion

 

Occurrence of infection of a single host with multiple S. mansoni strains and inter- and intra-host genetic variations was observed. Substantial genetic diversity and gene flow across the S. mansoni population occurred at each site and non-human primates likely play a role in local transmission and maintenance of infection. Therefore, public health and wildlife professionals should work together to improve disease control and elimination strategies.

Author summary

 

Schistosomiasis is a chronic disease caused by flukes (trematodes). The definitive host spectrum of schistosomes, whether human, non-human primates (NHPs) or other mammals, is highly dependent on the schistosome species concerned. Genetic diversity and population structure studies of S. mansoni have provided insights into the variation of natural populations. Understanding S. mansoni genetic diversity and population structure of isolates from human and non-human primate hosts living in close proximity showed the occurrence of infection of a single host with multiple S. mansoni strains and inter- and intra-host genetic variations. In this article, the researchers assert the fact that genetic approach reveals that parasites from the three different sites are independent. Thus, we could consider the three sites as geographical replicates showing the influence of NHPs in parasitic transmission in Ethiopia. This study provides insights into the epidemiology, genetic diversity and population structure of S. mansoni in human and non-human primates in Ethiopia, all of which are crucial for the control of schistosomiasis.

Full Text
File Pages Size Access
Publisher's official version 20 1 MB Open access
S1 Table. Natural host spectrum of Schistosoma mansoni. 21 KB Open access
S2 Table. MS Database. 314 KB Open access
S3 Table. Genetic diversity indices (He, Ar, Fis and number of breeders) for each infrapopulation. 29 KB Open access
S4 Table. Results from general linear models examining the association of parasite population genetic indexes (He, Ar, Number of breeders and Fis) with host variables (sex and age). 17 KB Open access
S1 Fig. Population structures of Schistosoma mansoni miracidia using Graphic 'deltaK'. 79 KB Open access
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