Diarrhoea-causing enteric protist species in intensively and extensively raised pigs ( Sus scrofa domesticus) in Southern Spain. Part II: Association with Hepatitis E virus susceptibility

Authors: RIVERO-JUAREZ, ANTONIO - Universidad De Cordoba; DASHTI, ALEJANDRO - National Center For Microbiology, The Institute Of Health Carlos Iii; Santin-Duran, Monica; KÖSTER, PAMELA - National Center For Microbiology, The Institute Of Health Carlos Iii; LOPEZ-LOPEZ, PEDRO - Universidad De Cordoba; RISALDE, MARIA - Universidad De Cordoba; GARCIA-BOCANEGRA, IGNACIO - Universidad De Cordoba; GOMEZ-VILLAMANDOS, JOSE CARLOS - Universidad De Cordoba; CABALLERO-GOMEZ, JAVIER - Universidad De Cordoba; FRIAS, MARLO - Universidad De Cordoba; BALLO, BEGOÑA - National Center For Microbiology, The Institute Of Health Carlos Iii; ORTEGA, SHEILA - National Center For Microbiology, The Institute Of Health Carlos Iii; MUADICA, 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, DAVED - National Center For Microbiology, The Institute Of Health Carlos Iii

Submitted to: Transboundary and Emerging Diseases
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/17/2021
Publication Date: 11/30/2021
Citation: Rivero-Juarez, A., Dashti, A., Santin, M., Köster, P.C., Lopez-Lopez, P., Risalde, M.A., Garcia-Bocanegra, I., Gomez-Villamandos, J., Caballero-Gomez, J., Frias, M., Ballo, B., Ortega, S., Muadica, A.S., 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 II: Association with Hepatitis E virus susceptibility. Transboundary and Emerging Diseases. https://doi.org/10.1111/tbed.14408.
DOI: https://doi.org/10.1111/tbed.14408

Interpretive Summary: Hepatitis E virus (HEV) is an emerging foodborne pathogen of increasing public health relevance, affecting both human and animal populations. Enteric parasites can infect a wide range of mammals, including humans, supposing an important zoonotic risk. Because both microorganisms share faecal-oral transmission route they may constitute an excellent model to evaluate the interplay between them. Thus, we aim to evaluate the viral-parasite interactions at the enteric interface in swine. We included pigs of two different breeds farming in South Spain under different production systems. We compared the HEV prevalence by the presence of parasites, Giardia duodenalis, Cryptosporidium spp., Balantioides coli, Blastocystis sp., and Enterocytozoon bieneusi in faecal samples. The overall HEV prevalence was 13.1% (62/475, 95% CI: 10.2–16.4). Those pigs infected with Cryptosporidium spp. showed a higher prevalence of HEV (30.8% vs. 12%; p = 0.012). In the same way, animals carrying E. bieneusi seem to have a higher rate of HEV infection (24.2% vs. 12.2%; p = 0.06). According to their location in the gut, animals bearing intracellular parasites (Cryptosporidium spp. and E. bieneusi) showed a higher HEV prevalence than those uninfected (29.6% vs. 12.7%; p = 0.038), meanwhile those carrying extracellular parasites (G. duodenalis, B. coli, and Blastocystis sp.) has a lower likelihood to be infected by HEV than those uninfected (12.1% vs. 23.1%; p = 0.071). Those animals carrying both types of parasites showed a similar prevalence of HEV infection than those exhibiting negative for both (20.8% vs. 26.1%; p = 0.763). In contrast, the HEV prevalence was significantly higher among those animals only bearing intracellular parasites than those bearing only extracellular parasites (50% vs. 9.2%; p = 0.055). Findings provide evidence that intracellular and extracellular parasites could modulate the susceptibility to HEV infection in pigs. Meanwhile, the presence of extracellular parasites shows a protective effect on the risk of HEV acquisition in swine, whereas intracellular parasites seem to have the opposite effect, promoting the HEV infection. This information will be useful to other scientists, veterinarians, and public health agencies in understanding the interplay of HVE and parasites in swine populations and could be useful to evaluate preventive measures against both these microorganisms.

Technical Abstract: Enteropathogenic parasites can infect a wide range of mammals, including humans, supposing an important zoonotic risk. Hepatitis E virus (HEV) is an emerging foodborne pathogen of increasing public health relevance, affecting both human and animal populations. Because both microorganisms share faecal-oral transmission route they may constitute an excellent model to evaluate the interplay between them. Thus, we aim to evaluate the viral-parasite interactions at the enteric interface in swine. We included pigs of two different breeds farming in South Spain under different production systems. We compared the HEV prevalence by the presence of Giardia duodenalis, Cryptosporidium spp., Balantioides coli, Blastocystis sp., and Enterocytozoon bieneusi in faecal samples. The HEV prevalence was 13.1% (62/475, 95% CI: 10.2–16.4). Those pigs infected with Cryptosporidium spp. showed a higher prevalence of HEV (30.8% vs. 12%; p = 0.012). In the same way, animals bearing E. bieneusi seem to have a higher rate of HEV infection (24.2% vs. 12.2%; p = 0.06). According to their location in the gut, animals bearing intracellular enteroparasites (Cryptosporidium spp. and E. bieneusi) showed a higher HEV prevalence than those uninfected (29.6% vs. 12.7%; p = 0.038), meanwhile those carrying extracellular enteroparasites (G. duodenalis, B. coli, and Blastocystis sp.) has a lower likelihood to be infected by HEV than those uninfected (12.1% vs. 23.1%; p = 0.071). Those animals bearing both type of enteroparasites showed a similar prevalence of HEV infection than those exhibiting negative for both (20.8% vs. 26.1%; p = 0.763). In contrast, the HEV prevalence was significantly higher among those animals only bearing intracellular enteroparasites than those bearing only extracellular parasites (50% vs. 9.2%; p = 0.055). Our study provides evidence that intracellular and extracellular enteroparasites modulate the susceptibility to HEV infection in pigs. Meanwhile, the presence of extracellular enteroparasites shows a protective effect on the risk of HEV acquisition in swine, whereas intracellular enteroparasites seems to have the opposite effect, favoring the HEV infection.