Zoonotic Enterocytozoon bieneusi genotypes in free-ranging and farmed wild ungulates in Spain

Authors: DASHTI, ALEJANDRO - Health Research Institute Of The San Carlos Clinical Hospital; Santin, Monica; KOSTER, PAMELA - Health Research Institute Of The San Carlos Clinical Hospital; BALLO, BEGONA - Health Research Institute Of The San Carlos Clinical Hospital; ORTEGA, SHEILA - Health Research Institute Of The San Carlos Clinical Hospital; IMANA, ELANA - Health Research Institute Of The San Carlos Clinical Hospital; HABELA, MIGUEL - Universidad De Extremadura; RIVERO-JUAREZ, ANTONIO - University Of Cordoba; VICENTE, JOAQUIN - Collaborator; WE&H, GROUP - Autonomous University Of Barcelona; ARNAL, MARIA - University Of Zaragoza; MORRONDO, PATROCINIO - University Of Santiago De Compostela; ARMENTEROS, JOSE - Collaborator; BALSEIRO, ANA - University Of Leon; CARDONA, GUILLERMO - Collaborator; MARTINEZ, CARRASCO - Universidad De Murcia; ORTIZ, JOSE - Collaborator; CALERO-BERNAL, RAFAEL - Complutense University Of Madrid (UCM); GONZALEZ-BARRIO, DAVID - Health Research Institute Of The San Carlos Clinical Hospital; CARMENA, DAVID - Health Research Institute Of The San Carlos Clinical Hospital

Submitted to: Medical Mycology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2022
Publication Date: 9/12/2022
Citation: Dashti, A., Santin, M., Koster, P.C., Ballo, B., Ortega, S., Imana, E., Habela, M.A., Rivero-Juarez, A., Vicente, J., We&H, G., Arnal, M.C., Morrondo, P., Armenteros, J.A., Balseiro, A., Cardona, G.A., Martinez, C., Ortiz, J.A., Calero-Bernal, R., Gonzalez-Barrio, D., Carmena, D. 2022. Zoonotic Enterocytozoon bieneusi genotypes in free-ranging and farmed wild ungulates in Spain. Medical Mycology. 60(9). Article myac070. https://doi.org/10.1093/mmy/myac070.
DOI: https://doi.org/10.1093/mmy/myac070

Interpretive Summary: The fungi-related intracellular parasite Enterocytozoon bieneusi is a public and veterinary health concern globally. Although its presence and genetic diversity is relatively well documented in humans and domestic animals, little information is available from wildlife in general. Here we demonstrated that E. bieneusi was present in wild boars as well as in wild and farmed red deer in Spain. They were infected with genetic variants of the parasite potentially able to infect humans, posing a public health risk that should not be underestimated. Data presented here expand our current knowledge on the epidemiology, host range, and molecular diversity of E. bieneusi that will be useful to other scientists, veterinarians, and public health agencies in understanding zoonotic potential and public health importance of this infectious pathogen.

Technical Abstract: Microsporidia comprises a diverse group of obligate, intracellular, and spore-forming parasites that infect a wide range of animals. Among them, Enterocytozoon bieneusi is the most frequently reported species in humans and other mammals and birds. Data on the epidemiology of E. bieneusi in wildlife is limited. Hence, E. bieneusi was investigated in eight wild ungulate species present in Spain (genera Ammotragus, Capra, Capreolus, Cervus, Dama, Ovis, Rupicapra, and Sus) by molecular methods. Faecal samples were collected from wild (n = 1058) and farmed (n = 324) ungulates from five Spanish bioregions. The parasite was detected only in red deer (10.4%, 68/653) and wild boar (0.8%, 3/359). Enterocytozoon bieneusi infections were more common in farmed (19.4%, 63/324) than in wild (1.5%, 5/329) red deer. Eleven genotypes were identified in red deer, eight known (BEB6, BEB17, EbCar2, HLJD-V, MWC_d1, S5, Type IV, and Wildboar3) and three novel (DeerSpEb1, DeerSpEb2, and DeerSpEb3) genotypes. Mixed genotype infections were detected in 15.9% of farmed red deer. Two genotypes were identified in wild boar, a known (Wildboar3) and a novel (WildboarSpEb1) genotypes. All genotypes identified belonged to E. bieneusi zoonotic Groups 1 and 2. This study provides the most comprehensive epidemiological study of E. bieneusi in Spanish ungulates to date, representing the first evidence of the parasite in wild red deer populations worldwide. Spanish wild boars and red deer are reservoir of zoonotic genotypes of E. bieneusi and might play an underestimated role in the transmission of this microsporidian species to humans and other animals.