Wild micromammal host spectrum of zoonotic eukaryotic parasites in Spain. Occurrence and genetic characterization

Authors: VIOQUE, FATIMA - National Center For Microbiology, The Institute Of Health Carlos Iii; DASHTI, ALEJANDRO - National Center For Microbiology, The Institute Of Health Carlos Iii; Santin-Duran, Monica; RUIZ-FONS, FRANCISCO - National Center For Microbiology, The Institute Of Health Carlos Iii; KOSTER, PAMELA - National Center For Microbiology, The Institute Of Health Carlos Iii; HERNANDEZ-CASTRO, CAROLINA - National Center For Microbiology, The Institute Of Health Carlos Iii; GARCIA, JESUS - University Of Antioquia; BAILO, BEGONA - National Center For Microbiology, The Institute Of Health Carlos Iii; ORTEGA, SHEILA - National Center For Microbiology, The Institute Of Health Carlos Iii; OLEA, PEDRO - Autonomous University Of Madrid; ARCE, FERNANDO - Complutense University Of Madrid (UCM); CHICHARRO, CARMEN - National Center For Microbiology, The Institute Of Health Carlos Iii; NIETO, JAVIER - National Center For Microbiology, The Institute Of Health Carlos Iii; GONZALEZ, FERNANDO - Complutense University Of Madrid (UCM); VINUELA, JAVIER - National Center For Microbiology, The Institute Of Health Carlos Iii; CARMENA, DAVID - National Center For Microbiology, The Institute Of Health Carlos Iii; BARRIOS, 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: 6/22/2022
Publication Date: 6/25/2022
Citation: Vioque, F., Dashti, A., Santin, M., Ruiz-Fons, F., Koster, P.C., Hernandez-Castro, C., Garcia, J.T., Bailo, B., Ortega, S., Olea, P., Arce, F., Chicharro, C., Nieto, J., Gonzalez, F., Vinuela, J., Carmena, D., Barrios, D. 2022. Wild micromammal host spectrum of zoonotic eukaryotic parasites in Spain. Occurrence and genetic characterization. Transboundary and Emerging Diseases. https://doi.org/10.1111/tbed.14643.
DOI: https://doi.org/10.1111/tbed.14643

Interpretive Summary: Micromammals are particularly relevant from a public health perspective because they are potential reservoirs of human infectious pathogens (viruses, bacteria, fungi, and parasites) playing a major role in the spread of zoonotic pathogens to humans. However, limited information is currently available on the epidemiology and potential public health significance of intestinal protists in wild micromammals. Therefore, we examined 490 fecal samples from 11 micromammal species captured in 11 Spanish provinces for the presence of Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, and Blastocystis sp. Additionally, the presence of Leishmania spp. was investigated in spleen samples. All micromammal species investigated harbored at least one parasite, except Apodemus flavicollis, Myodes glareolus, Sorex coronatus and Sciurus vulgaris. Cryptosporidium spp. was the most prevalent species found (3.7%), followed by G. duodenalis (2.8%) and E. bieneusi (2.6%). All samples tested negative for Blastocystis sp. Leishmania infantum was identified in 0.4% of the samples examined. Nucleotide sequence analyses identified for 5 species and 4 genotypes of Cryptosporium, C. andersoni, C. ditrichi, C. muris, C. parvum, C. tyzzeri, rat genotypes CR97, rat genotype W19, vole genotypes V, vole genotype VII (5.9%). For E. bieneusi, two known genotypes, C and Peru11, and a novel genotype (named MouseSpEb1) were detected. None of the G. duodenalis-positive samples could be genotyped at the assemblage level. Molecular data indicate that wild micromammals were mostly infected by rodent-adapted species/genotypes of ptotists pathogens and have a limited role as source of human infections. However, the presence of ruminant-adapted species C. andersoni along with finding wide-range host species C. parvum is indicative of an overlap between domestic/peri-domestic and sylvatic transmission cycles of these agents. This information on intestinal protists and Leishmania in wild micromammals will be useful to other scientists, veterinarians, and public health agencies in understanding taxonomy, epidemiology, zoonotic potential, and public health importance of this infectious pathogens.

Technical Abstract: Micromammals have historically been recognized as highly contentious species in terms of maintenance and transmission of zoonotic pathogens to humans. Limited information is currently available on the epidemiology and potential public health significance of intestinal eukaryotes in wild micromammals. We examined 490 faecal samples, grouped in 155 pools, obtained from 11 micromammal species captured in 11 Spanish provinces for the presence of DNA from Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, and Blastocystis sp. The presence of Leishmania spp. was investigated in individual spleen samples. All micromammal species investigated harboured infections by at least one eukaryotic parasite, except Apodemus flavicollis, Myodes glareolus, Sorex coronatus and Sciurus vulgaris. Cryptosporidium spp. was the most prevalent species found (3.7%, 95% CI: 2.2–5.7), followed by G. duodenalis (2.8%, 95% CI: 1.6–4.6) and E. bieneusi (2.6%, 95% CI: 1.4–4.3). All pooled faecal samples tested negative for Blastocystis sp. Leishmania infantum was identified in 0.41% (95% CI: 0.05–1.46) of the 490 individual spleen samples analysed. Sequences analyses allowed the identification of C. andersoni (5.9%), C. ditrichi (11.7%), C. muris (5.9%), C. parvum (5.9%), C. tyzzeri (5.9%), rat genotypes CR97 (5.9%) and W19 (5.9%), vole genotypes V (11.7%) and VII (5.9%) and Cryptosproridium spp. (35.3%) within Cryptosporidium (n = 17). Known genotypes C (66.7%) and Peru11 (25.0%), and a novel genotype (named MouseSpEb1, 8.3%) were detected within E. bieneusi (n = 12). None of the G. duodenalis-positive samples could be genotyped at the assemblage level. Molecular data indicate that wild micromammals were primarily infected by rodent-adapted species/genotypes of eukaryotic pathogens and have a limited role as source of human infections. The presence of ruminant-adapted species C. andersoni along with finding C. parvum is indicative of an overlap between domestic/peri-domestic and sylvatic transmission cycles of these agents.