Intestinal Protists in Captive Non-human Primates and Their Handlers in Six European Zoological Gardens. Molecular Evidence of Zoonotic Transmission.

Pamela C Köster,María T Abelló-Poveda,Begoña Bailo,Tobias Knauf-Witzens,David Carmena,Eva Martínez-Nevado,David González-Barrio,Aly S Muadica,Elena Imaña,Bertille Marquet,Francisco Ponce-Gordo,Annika Weigold,Jean-Pascal Guéry,Rafael Calero-Bernal,Hugo Fernández-Bellon,Andrea González,Manuel De La Riva-Fraga,Alejandro Dashti

doi:10.3389/fvets.2021.819887

Pamela C Köster, María T Abelló-Poveda + Show 16 more

Open Access

https://doi.org/10.3389/fvets.2021.819887

Copy DOI

Abstract

We assessed the occurrence, genetic diversity, and zoonotic potential of four protozoan (Cryptosporidium spp., Entamoeba histolytica, Entamoeba dispar, Giardia duodenalis), one stramenopile (Blastocystis sp.), one microsporidia (Enterocytozoon bieneusi), and two ciliate (Balantioides coli, Troglodytella abrassarti) intestinal parasite or commensal protist species in captive non-human primates (NHP) and their zookeepers from six European zoological gardens in France (n = 1), Germany (n = 1), and Spain (n = 4). Faecal samples from NHP (n = 454) belonging to 63 species within 35 genera and humans (n = 70) were collected at two sampling periods in each participating institution between October 2018-August 2021. Detection and species identification was accomplished by PCR and Sanger sequencing of the ssu rRNA and/or ITS genes. Sub-genotyping analyses using specific markers were conducted on isolates positive for G. duodenalis (gdh, bg, tpi) and Cryptosporidium spp. (gp60). Overall, 41.0% (186/454) and 30.0% (21/70) of the faecal samples of NHP and human origin tested positive for at least one intestinal protist species, respectively. In NHP, Blastocystis sp. was the most prevalent protist species found (20.3%), followed by G. duodenalis (18.1%), E. dispar (7.9%), B. coli and T. abrassarti (1.5% each), and Cryptosporidium spp. and E. bieneusi (0.9% each). Occurrence rates varied largely among NHP host species, sampling periods, and zoological institutions. The predominant protist species found in humans was Blastocystis sp. (25.7%), followed by Cryptosporidium spp. (2.9%), E. dispar (1.4%), and G. duodenalis (1.4%). Sequencing of PCR-positive amplicons in human and/or NHP confirmed the presence of Cryptosporidium in six isolates (C. hominis: 66.7%, C. parvum: 33.3%), G. duodenalis in 18 isolates (assemblage A: 16.7%, assemblage B: 83.3%), Blastocystis in 110 isolates (ST1:38.2%, ST2:11.8%, ST3: 18.2%, ST4: 9.1%, ST5: 17.3%, ST8: 2.7%, ST13: 0.9%), and E. bieneusi in four isolates (CM18: 75.0%, Type IV: 25.0%). Zoonotic transmission events involving Blastocystis ST1–ST4 were identified in four zoological institutions. Zoonotic transmission of C. hominis was highly suspected, but not fully demonstrated, in one of them. Monitoring of intestinal protist species might be useful for assessing health status of captive NHP and their zookeepers, and to identify transmission pathways of faecal-orally transmitted pathogens.

Highlights

Diarrhoea is one of the leading problems requiring veterinary care in captive non-human primates (NHP)
The entodiniomorphid ciliate T. abrassarti is thought to participate in colonic fermentation of fibre during digestion, so changes in diet may determine its abundance in the intestinal tract of captive NHP [9]
We identified Blastocystis sp. as the most prevalent protist species found (20.3%, range: 1.2–40.9%), followed by G. duodenalis (18.1%, range: 9.5–29.1%), E. dispar (7.9%, range: 0.0– 26.6%), B. coli (1.5%, 0.0–7.5%), T. abrassarti (1.5%, 0.0–15.2%), Cryptosporidium spp. (0.9%, 0.0–3.5%), and E. bieneusi (0.9%, 0.0–2.4%)

Summary

Introduction

Diarrhoea is one of the leading problems requiring veterinary care in captive non-human primates (NHP). Gastrointestinal manifestations may arise as consequence of nutritional changes, stress and/or infection by viral, bacterial and parasitic pathogens [1]. Among the latter, the protozoa Entamoeba histolytica, Giardia duodenalis Some protist species, such as Entamoeba dispar or the ape-restricted Troglodytella abrassarti, are non-pathogenic commensals. The entodiniomorphid ciliate T. abrassarti is thought to participate in colonic fermentation of fibre during digestion, so changes in diet may determine its abundance in the intestinal tract of captive NHP [9]. Transmission is primarily through the faecal-oral route via direct contact with infected hosts (or their faecal material), or indirect through the ingestion of contaminated water or food

Objectives

Methods

Results

Conclusion