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

Author:

Dashti Alejandro1,Santín Mónica2,Köster Pamela C1,Bailo Begoña1,Ortega Sheila1,Imaña Elena1,Habela Miguel Ángel3,Rivero-Juarez Antonio4,Vicente Joaquin5,Conejero Carles,González-Crespo Carlos,Garrido Cristina,Gassó Diana,Andrea Murillo Diana,Serrano Emmanuel,Mentaberre Gregorio,Torres-Blas Irene,Estruch Josep,Pastor Josep,Ramón López-Olvera Jorge,Escobar-González María,Valldeperes Marta,Mesalles Montse,López Omar,Álvarez Raquel,Cuenca Rafaela,Velarde Roser,Lavín Santiago6,Arnal Maria C7,de Luco Daniel Fernández7,Morrondo Patrocinio8,Armenteros José A9,Balseiro Ana1011,Cardona Guillermo A12,Martínez-Carrasco Carlos13,Ortiz José Antonio14,Calero-Bernal Rafael15,Carmena David161,González-Barrio David1ORCID,

Affiliation:

1. Parasitology Reference and Research Laboratory, Spanish National Centre for Microbiology, Health Institute Carlos III , Majadahonda, Madrid 28220 , Spain

2. Environmental Microbial and Food Safety Laboratory, Agricultural Research Service, United States Department of Agriculture , Beltsville, MD 20705 , USA

3. Department of Animal Health, Veterinary Sciences Faculty, Extremadura University , Caceres 10003 , Spain

4. Infectious Diseases Unit, Maimonides Institute for Biomedical Research (IMIBIC), University Hospital Reina Sofía, University of Córdoba , Córdoba 14004 , Spain

5. SaBio Group, Institute for Game and Wildlife Research, IREC (UCLM-CSIC-JCCM) , Ciudad Real 13005 , Spain

6. Wildlife Ecology & Health Group (WE&H), Wildlife Environmental Pathology Service (SEFaS), Department of Animal Medicine and Surgery, Autonomous University of Barcelona , Bellaterra 08193 , Spain

7. Department of Animal Pathology, Veterinary Faculty, University of Zaragoza , Zaragoza 50013 , Spain

8. INVESAGA Group, Department of Animal Pathology, Faculty of Veterinary, University of Santiago de Compostela , Lugo 27002 , Spain

9. Council of Development, Territory Planning and the Environment of the Principado de Asturias , Oviedo 33005 , Spain

10. Animal Health Department, Veterinary School, University of León , León 24007 , Spain

11. Animal Health Department, Mountain Livestock Institute (CSIC-University of León) , León 24346 , Spain

12. Livestock Laboratory, Regional Government of Álava , Vitoria-Gasteiz 01520 , Spain

13. Animal Health Department, University of Murcia, Regional Campus of International Excellence “Campus Mare Nostrum” , Espinardo, Murcia 30100 , Spain

14. Department of Veterinary and Research, Medianilla S.L. Benalup-Casas Viejas 11179 , Spain

15. SALUVET, Department of Animal Health, Faculty of Veterinary, Complutense University of Madrid , Madrid 28040 , Spain

16. CIBER Infectious Diseases (CIBERINFEC), Health Institute Carlos III , Madrid 28029 , Spain

Abstract

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 are 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 free-ranging (n = 1058) and farmed (n = 324) wild 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. A total of 11 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.

Funder

Carlos III Health Institute

Institute of Cosmos Sciences, University of Barcelona

Ministry of Economy and Competitiveness

Spanish Ministry of Science and Innovation

Publisher

Oxford University Press (OUP)

Subject

Infectious Diseases,General Medicine

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