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

Jean-François Allienne,Nicolas Bech,Rey Olivier,Berhanu Erko,Tadesse Kebede,Jerome Boissier

doi:10.1371/journal.pntd.0008538

Abstract

BackgroundSchistosomiasis 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.ObjectiveThe 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.MethodsA 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.ResultsAt 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.ConclusionOccurrence 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.

Highlights

Schistosomiasis remains one of the most prevalent and debilitating helminthic infections in the world
Genetic diversity of Schistosoma mansoni from human and non-human primates genetic diversity which was high in human males, medium in human females and low in non-human primates (NHPs)
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

Summary

Introduction

Schistosomiasis remains one of the most prevalent and debilitating helminthic infections in the world. More than 207 million people are infected, and over 600 million people are at risk of infection [1] These parasites have a complex life cycle with freshwater snail intermediate hosts and vertebrate definitive hosts. With 59% and 24% of the species inventoried, the majority of non-human S. mansoni definitive hosts are rodents and primates, respectively. Large-scale control programs are mainly based on morbidity control through a mass-drug chemotherapy program using a single drug treatment [3]. Despite their important role in the transmission of the parasite, the reservoir hosts are currently excluded from control programs in Africa. Many health measures have been carried out to limit parasite transmission, significant numbers of nonhuman 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.

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Results

Conclusion