Diarrhoea-causing enteric protist species in intensively and extensively raised pigs (Sus scrofa domesticus) in Southern Spain. Part I: Prevalence, genetic diversity, and zoonotic potential

Authors: DASHTI, ALEJANDRO - National Center For Microbiology, The Institute Of Health Carlos Iii; RIVERO-JUAREZ, ANTONIO - Universidad De Cordoba; Santin-Duran, Monica; George, Nadja; KÖSTER, PAMELA - National Center For Microbiology, The Institute Of Health Carlos Iii; LOPEZ-LOPEZ, PEDRO - Universidad De Cordoba; ROSALDE, MARIA - Universidad De Cordoba; GARCIA-BOCANEGRA, IGNACIO - Universidad De Cordoba; GOMEZ-VILLAMANDOS, JOSE CARLOS - Universidad De Cordoba; CABALLERO-GOMEZ, JAVIER - Universidad De Cordoba; FRIAS, MARIO - Universidad De Cordoba; BAILO, BEGOÑA - National Center For Microbiology, The Institute Of Health Carlos Iii; ORTEGA, SHEILA - National Center For Microbiology, The Institute Of Health Carlos Iii; MAUDICA, ALY - National Center For Microbiology, The Institute Of Health Carlos Iii; CALERO-BERNAL, RAFAEL - Complutense University Of Madrid (UCM); GONZALEZ-BARRIO, DAVID - National Center For Microbiology, The Institute Of Health Carlos Iii; RIVERO, ANTONIO - Universidad De Cordoba; BRIZ, VERONICA - National Center For Microbiology, The Institute Of Health Carlos Iii; CARMENA, DAVID - National Center For Microbiology, The Institute Of Health Carlos Iii

Submitted to: Transboundary and Emerging Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2021
Publication Date: 11/9/2021
Citation: Dashti, A., Rivero-Juarez, A., Santin, M., George, N.S., Köster, P.C., Lopez-Lopez, P., Rosalde, M.A., Garcia-Bocanegra, I., Gomez-Villamandos, J., Caballero-Gomez, J., Frias, M., Bailo, B., Ortega, S., Maudica, A.A., Calero-Bernal, R., Gonzalez-Barrio, D., Rivero, A., Briz, V., Carmena, D. 2021. Diarrhoea-causing enteric protist species in intensively and extensively raised pigs (Sus scrofa domesticus) in Southern Spain. Part I: Prevalence, genetic diversity, and zoonotic potential. Transboundary and Emerging Diseases. https://doi.org/10.1111/tbed.14388.
DOI: https://doi.org/10.1111/tbed.14388

Interpretive Summary: Giardia duodenalis, Cryptosporidium spp., Balantioides coli, Blastocystis sp., and Enterocytozoon bieneusi are among the most frequent enteric parasites infecting pigs globally. However, little information is currently available on the molecular diversity of these protists in swine populations. In this survey, we molecularly assessed the presence of G. duodenalis, Cryptosporidium spp., B. coli, Blastocystis sp., and E. bieneusi in faecal samples from Iberian and Large White pigs raised under intensive and extensive management systems in southern Spain. A total of 151 (31.8%) extensively raised Iberian pigs, 140 (29.5%) intensively raised Iberian pigs, and 184 (38.7%) intensively raised Large White pigs were included in the study. Blastocystis sp. was the agent most prevalently found (47.8%), followed by Balantioides coli (45.5%), G. duodenalis (10.7%), E. bieneusi (6.9%), and Cryptosporidium spp. (5.5%). Molecular characterization revealed the presence of G. duodenalis assemblage E (n = 3), C. scrofarum (61.5%, 16/26), C. suis (38.5%, 10/26), B. coli genotypes A (2/15) and B (13/15), Blastocystis subtypes (ST5: 91.2%, 207/227; ST1: 7.5%, 17/227); ST3: 1.3%, 3/227), and E. bieneusi (EbpA: 66.6%, 22/33; EbpC: 12.1%, 4/33; EbpD: 6.1%, 2/33; O: 6.1%, 2/33; EbpA+EbpD: 3.0%, 1/33; novel genotype PigSpEb2 alone: 3.0%, 1/33; or in combination EbpA+PigSpEb2: 3.0%, 1/33). Prevalence and epidemiological data presented here suggest a widespread exposure to enteroparasites in domestic pig populations irrespective of breed and raising management system. Many of the species/genotype identified have zoonotic potential and might represent a public health concern. This information will be useful to other scientists, veterinarians, and public health agencies in understanding the status of taxonomy, epidemiology, zoonotic potential, and public health importance of enteric parasites in swine populations.

Technical Abstract: The protozoa Giardia duodenalis and Cryptosporidium spp., the ciliate Balantioides coli, the stramenopile Blastocystis sp., and the microsporidia Enterocytozoon bieneusi are among the most frequent protist enteroparasites infecting pigs globally. Whereas G. duodenalis, Cryptosporidium spp. and E. bieneusi are well-recognized diarrhoea-causing pathogens, both Blastocystis sp. and B. coli are commonly regarded as enteroparasites of limited veterinary health relevance. Little information is currently available on the molecular diversity of these protists in swine populations. In this survey, we molecularly assessed the presence of G. duodenalis, Cryptosporidium spp., B. coli, Blastocystis sp., and E. bieneusi in faecal samples from Iberian and Large White pigs raised under intensive and extensive management systems in southern Spain. A total of 151 (31.8%) extensively raised Iberian pigs, 140 (29.5%) intensively raised Iberian pigs, and 184 (38.7%) intensively raised Large White pigs were included in the study. Blastocystis sp. was the agent most prevalently found (47.8%, 95% CI: 43.2–52.4), followed by Balantioides coli (45.5%, 40.9–50.1), G. duodenalis (10.7%, 95% CI: 8.1–13.9), E. bieneusi (6.9%, 95% CI: 4.8–9.6), and Cryptosporidium spp. (5.5%, 95% CI: 3.6–7.9). Sequence analyses revealed the presence of assemblage E (n = 3) within G. duodenalis. Two Cryptosporidium species including C. scrofarum (61.5%, 16/26) and C. suis (38.5%, 10/26) were identified. Genotypes A (2/15) and B (13/15) were found within B. coli. ST5 was the predominant Blastocystis subtype identified (91.2%, 207/227), followed by ST1 (7.5%, 17/227) and ST3 (1.3%, 3/227). Additionally, four known E. bieneusi genotypes (EbpA: 66.6%, 22/33; EbpC: 12.1%, 4/33; EbpD: 6.1%, 2/33; O: 6.1%, 2/33; EbpA+EbpD: 3.0%, 1/33) and one novel genotype (PigSpEb2) alone (PigSpEb2: 3.0%, 1/33) or in combination (EbpA+PigSpEb2: 3.0%, 1/33) were identified. Prevalence and epidemiological data presented here suggest a widespread exposure to protist enteroparasites in domestic pig populations irrespective of breed and raising management system. Many of the species/genotype identified have zoonotic potential and might represent a public health concern.