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Wild chimpanzee populations in West Africa (Pan troglodytes verus) have dramatically decreased as a direct consequence of anthropogenic activities and infectious diseases. Little information is currently available on the epidemiology, pathogenic significance, and zoonotic potential of protist species in wild chimpanzees. This study investigates the occurrence and genetic diversity of intestinal and blood protists as well as filariae in faecal samples (n = 234) from wild chimpanzees in the Dindefelo Community Nature Reserve, Senegal. PCR-based results revealed the presence of intestinal potential pathogens (Sarcocystis spp.: 11.5%, Giardia duodenalis: 2.1%, Cryptosporidium hominis: 0.9%), protist of uncertain pathogenicity (Blastocystis sp.: 5.6%), and commensal species (Entamoeba dispar: 18.4%, Troglodytella abrassarti: 5.6%). Entamoeba histolytica, Enterocytozoon bieneusi, and Balantioides coli were undetected. Blood protists including Plasmodium malariae (0.4%), Trypanosoma brucei (1.3%), and Mansonella perstans (9.8%) were also identified. Sanger sequencing analyses revealed host-adapted genetic variants within Blastocystis, but other parasitic pathogens (C. hominis, P. malariae, T. brucei, M. perstans) have zoonotic potential, suggesting that cross-species transmission between wild chimpanzees and humans is possible in areas where both species overlap. Additionally, we explored potential interactions between intestinal/blood protist species and seasonality and climate variables. Chimpanzees seem to play a more complex role on the epidemiology of pathogenic and commensal protist and nematode species than initially anticipated.

Simple Summary Little information is currently available on the epidemiology of parasitic and commensal protist species in captive non-human primates (NHP) and their zoonotic potential. This study investigates the occurrence, molecular diversity, and potential transmission dynamics of parasitic and commensal protist species in a zoological garden in southern Spain. The prevalence and genotypes of the main enteric protist species were investigated in faecal samples from NHP, zookeepers and free-living rats by molecular (PCR and sequencing) methods. A high prevalence of the diarrhoea-causing protists Giardia duodenalis and Blastocystis sp. (but not Cryptosporidium spp.) was observed in captive NHP at the Córdoba Zoo Conservation Centre. NHP can harbour zoonotic genotypes of G. duodenalis, Blastocystis sp., and Enterocytozoon bieneusi. Indeed, strong evidence of the occurrence of Blastocystis zoonotic transmission between NHP and their handlers was provided, despite the use of personal protective equipment and the implementation of strict health and safety protocols. Free-living sympatric rats are infected by host-specific species/genotypes of the investigated protists and seem to play a limited role as source of infections to NHP or humans in this setting. The extent of these findings should be confirmed in similar epidemiological surveys targeting other captive NHP populations. Abstract Little information is currently available on the epidemiology of parasitic and commensal protist species in captive non-human primates (NHP) and their zoonotic potential. This study investigates the occurrence, molecular diversity, and potential transmission dynamics of parasitic and commensal protist species in a zoological garden in southern Spain. The prevalence and genotypes of the main enteric protist species were investigated in faecal samples from NHP (n = 51), zookeepers (n = 19) and free-living rats (n = 64) by molecular (PCR and sequencing) methods between 2018 and 2019. The presence of Leishmania spp. was also investigated in tissues from sympatric rats using PCR. Blastocystis sp. (45.1%), Entamoeba dispar (27.5%), Giardia duodenalis (21.6%), Balantioides coli (3.9%), and Enterocytozoon bieneusi (2.0%) (but not Troglodytella spp.) were detected in NHP. Giardia duodenalis (10.5%) and Blastocystis sp. (10.5%) were identified in zookeepers, while Cryptosporidium spp. (45.3%), G. duodenalis (14.1%), and Blastocystis sp. (6.25%) (but not Leishmania spp.) were detected in rats. Blastocystis ST1, ST3, and ST8 and G. duodenalis sub-assemblage AII were identified in NHP, and Blastocystis ST1 in zookeepers. Giardia duodenalis isolates failed to be genotyped in human samples. In rats, four Cryptosporidium (C. muris, C. ratti, and rat genotypes IV and V), one G. duodenalis (assemblage G), and three Blastocystis (ST4) genetic variants were detected. Our results indicate high exposure of NHP to zoonotic protist species. Zoonotic transmission of Blastocysts ST1 was highly suspected between captive NHP and zookeepers.

La diarrea fue la quinta causa de muerte en niños menores de 5 años en el mundo en 2016. Los 6 patógenos entéricos más relevantes causantes de esta condición incluyeron agentes de origen vírico (adenovirus, rotavirus), bacteriano (Campylobacter, Escherichia coli enterotoxigénica, Shigella) y parasitarios (Cryptosporidium). Las infecciones por estos patógenos eran más frecuentes y graves en áreas desfavorecidas de países de renta baja y media caracterizadas por acceso limitado a agua potable, condiciones higiénico-sanitarias inadecuadas y servicios de saneamiento insuficientes. Además de Cryptosporidium, los protozoos Giardia duodenalis y Entamoeba histolytica también contribuyen significativamente a la carga de enfermedad diarreica global, además de estar asociados a desnutrición, retraso del crecimiento y déficit cognitivo en los niños afectados. Otros protistas, como el estramenópilo Blastocystis o el microsporidio Enterocytozoon bieneusi, tienen una patogenicidad incierta o causan infecciones oportunistas en individuos inmunodeprimidos. El papel de los niños asintomáticos en la epidemiología de estos protistas ha sido insuficientemente estudiado tanto en países de renta baja y media como en los de renta alta...

Additional file 4: Table S4. Diversity and frequency of Blastocystis sp. subtypes and 18S alleles identified in the present study.

Los protozoos Giardia duodenalis y Cryptosporidium spp., el estramenopilo Blastocystis sp. y el microsporidio Enterocytozoon bieneusi son algunos de los parásitos entéricos causantes de diarrea más relevantes en salud pública humana. Este estudio epidemiológico molecular investiga la diversidad genética de estos patógenos en una población escolar. El análisis de factores de riesgo o protectores asociados a estas infecciones se presenta en una comunicación independiente. Sí

Additional file 1: Table S1. Oligonucleotides used for the molecular identification and/or characterization of the intestinal protist and helminth parasites investigated in the present study.

Additional file 2: Table S2. Diversity, frequency, and main molecular features of G. duodenalis isolates in swine samples. GenBank accession numbers of representative sequences are provided. Novel genotypes are underlined.