The First Report and Molecular Analysis of Enterocytozoon bieneusi from Raccoon (Procyon lotor) in North of Iran.


Journal

The Journal of eukaryotic microbiology
ISSN: 1550-7408
Titre abrégé: J Eukaryot Microbiol
Pays: United States
ID NLM: 9306405

Informations de publication

Date de publication:
05 2020
Historique:
received: 14 08 2019
revised: 21 12 2019
accepted: 06 01 2020
pubmed: 17 1 2020
medline: 16 6 2021
entrez: 17 1 2020
Statut: ppublish

Résumé

Microsporidia are known opportunistic microorganisms and usually transmitted via the fecal-oral route. However, there is no information about human-infecting microsporidia in wildlife in Iran. This study aimed to investigate and analyze human-infecting microsporidia isolated from raccoons in north of Iran. Totally, 30 fecal samples were collected; then, DNA extraction was performed and specific fragments of the SSU rRNA gene of Enterocytozoon bieneusi and Encephalitozoon species were amplified. After amplification and sequencing the ITS, the results were compared to the GenBank database. Phylogenetic trees and network analysis were employed to explore probable relationships. E. bieneusi was the only detected microsporidia among samples. Genotyping showed the genotypes D, E, and RA in 15/18 (83.33%), 1/18 (5.55%), and 2/18 (11.11%) of samples, respectively. Novel genotypes RA1 and RA2 grouped together and apart from other genotypes. E. bieneusi genotypes D and E clustered with the genotypes previously reported from animals, humans, and environmental samples. Network analysis revealed six distinct sequence types among raccoon's isolates. This study demonstrated that E. bieneusi genotype D was the most prevalent microsporidia among raccoons. It seems that wildlife may play a role in dispersion of microsporidia spores.

Identifiants

pubmed: 31943500
doi: 10.1111/jeu.12786
doi:

Substances chimiques

DNA, Fungal 0
DNA, Ribosomal 0

Banques de données

GENBANK
['MN190612', 'MN190613', 'MN190614', 'MN190615', 'MN190616', 'MN190617', 'MN190618', 'MN190619', 'MN190620', 'MN190621', 'MN190622', 'MN190623', 'MN190624', 'MN190625', 'MN190626', 'MN190627', 'MN190628', 'MN190629', 'KU852472']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

359-368

Informations de copyright

© 2020 International Society of Protistologists.

Références

Agholi, M., Hatam, G. R. & Motazedian, M. H. 2013. Microsporidia and coccidia as causes of persistence diarrhea among liver transplant children: incidence rate and species/genotypes. Pediatr. Infect. Dis. J., 32(2):185-187. https://doi.org/10.1097/INF.0b013e318273d95f
Alda, F., Ruiz-López, M. J., García, F. J., Gompper, M. E., Eggert, L. S. & García, J. T. 2013. Genetic evidence for multiple introduction events of raccoons (Procyon lotor) in Spain. Biol. Invas., 15(3):687-698. https://doi.org/10.1007/s10530-012-0318-6
Askari, Z., Mirjalali, H., Mohebali, M., Zarei, Z., Shojaei, S., Rezaeian, T. & Rezaeian, M. 2015. Molecular detection and identification of zoonotic microsporidia spore in fecal samples of some animals with close-contact to human. Iran J. Parasitol., 10(3):381-388.
Bandelt, H. J., Forster, P. & Rohl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol., 16(1):37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Bartoszewicz, M., Okarma, H., Zalewski, A. & Szczęsna, J. 2008. Ecology of the raccoon (Procyon lotor) from western Poland. Ann. Zool. Fenn., 45:291-298. https://doi.org/10.5735/086.045.0409
Beer, K. D., Gargano, J. W., Roberts, V. A., Hill, V. R., Garrison, L. E., Kutty, P. K., Hilborn, E. D., Wade, T. J., Fullerton, K. E. & Yoder, J. S. 2015a. Surveillance for waterborne disease outbreaks associated with drinking water - United States, 2011-2012. MMWR Morb. Mortal. Wkly Rep., 64(31):842-848.
Beer, K. D., Gargano, J. W., Roberts, V. A., Reses, H. E., Hill, V. R., Garrison, L. E., Kutty, P. K., Hilborn, E. D., Wade, T. J., Fullerton, K. E. & Yoder, J. S. 2015b. Outbreaks associated with environmental and undetermined water exposures - United States, 2011-2012. MMWR Morb. Mortal. Wkly Rep., 64(31):849-851.
Beltrán-Beck, B., García, F. J. & Gortázar, C. 2012. Raccoons in Europe: disease hazards due to the establishment of an invasive species. Eur. J. Wildl. Res., 58(1):5-15.
Brown, M. J. F. 2017. Microsporidia: an emerging threat to bumblebees? Trends Parasitol., 33(10):754-762. https://doi.org/10.1016/j.pt.2017.06.001
Clement, M., Posada, D. & Crandall, K. A. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol., 9(10):1657-1659.
Decraene, V., Lebbad, M., Botero-Kleiven, S., Gustavsson, A. M. & Lofdahl, M. 2012. First reported foodborne outbreak associated with microsporidia, Sweden, October 2009. Epidemiol. Infect., 140(3):519-527. https://doi.org/10.1017/s095026881100077x
Delrobaei, M., Jamshidi, S., Shayan, P., Ebrahimzade, E., Ashrafi Tamai, I., Rezaeian, M. & Mirjalali, H. 2019. Molecular detection and genotyping of intestinal microsporidia from stray dogs in Iran. Iran J. Parasitol., 14(1):159-166.
Didier, E. S. & Weiss, L. M. 2006. Microsporidiosis: current status. Curr. Opin. Infect Dis., 19(5):485.
Espern, A., Morio, F., Miegeville, M., Illa, H., Abdoulaye, M., Meyssonnier, V., Adehossi, E., Lejeune, A., Cam, P. D., Besse, B. & Gay-Andrieu, F. 2007. Molecular study of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among human immunodeficiency virus-infected patients from two geographical areas: Niamey, Niger, and Hanoi, Vietnam. J. Clin. Microbiol., 45(9):2999-3002. https://doi.org/10.1128/jcm.00684-07
Farashi, A., Kaboli, M. & Karami, M. 2013. Predicting range expansion of invasive raccoons in northern Iran using ENFA model at two different scales. Ecol. Inform., 15:96-102.
Farashi, A. & Naderi, M. 2017. Predicting invasion risk of raccoon Procyon lotor in Iran using environmental niche models. Landscape Ecol. Eng., 13(2):229-236.
Fayer, R., Santín, M. & Macarisin, D. 2010. Cryptosporidium ubiquitum n. sp. in animals and humans. Vet. Parasitol., 172(1-2):23-32.
Fayer, R. & Santin-Duran, M. 2014. Epidemiology of microsporidia in human infections. In: Weiss, L. M. & Becnel, J. J. (ed.), Microsporidia. p. 135-164. https://doi.org/10.1002/9781118395264.ch3
Feng, Y., Alderisio, K. A., Yang, W., Blancero, L. A., Kuhne, W. G., Nadareski, C. A., Reid, M. & Xiao, L. 2007. Cryptosporidium genotypes in wildlife from a New York watershed. Appl. Environ. Microbiol., 73(20):6475-6483.
Galvan, A. L., Sánchez, A. M., Valentín, M. P., Henriques-Gil, N., Izquierdo, F., Fenoy, S. & Del Aguila, C. 2011. First cases of microsporidiosis in transplant recipients in Spain and review of the literature. J. Clin. Microbiol., 49(4):1301-1306. https://doi.org/10.1128/jcm.01833-10
Guo, Y., Alderisio, K. A., Yang, W., Cama, V., Feng, Y. & Xiao, L. 2014. Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl. Environ. Microbiol., 80(1):218-225. https://doi.org/10.1128/AEM.02997-13
Hasani, Z., Aghdaei, H. A., Balaii, H., Azimirad, M., Mirsamadi, E. S., Mirjalali, H. & Zali, M. R. 2017. The first study on opportunistic intestinal microsporidiosis in IBD patients receiving immunosuppressive medications in Iran. Epidemiol. Infect., 145(10):2095-2099. https://doi.org/10.1017/s0950268817000954
Henriques-Gil, N., Haro, M., Izquierdo, F., Fenoy, S. & del Aguila, C. 2010. Phylogenetic approach to the variability of the microsporidian Enterocytozoon bieneusi and its implications for inter-and intrahost transmission. Appl. Environ. Microbiol., 76(10):3333-3342.
Hu, Y., Feng, Y., Huang, C. & Xiao, L. 2014. Occurrence, source, and human infection potential of Cryptosporidium and Enterocytozoon bieneusi in drinking source water in Shanghai, China, during a pig carcass disposal incident. Environ. Sci. Technol., 48(24):14219-14227.
Huang, X., Zhou, Z., Liu, H., Deng, L., Bi, B., Chai, Y., Zhong, Z., Hu, Y., Fu, H. & Peng, G. 2019. New genotypes and molecular characterization of Enterocytozoon bieneusi in captive black bears in China. Int. J. Parasitol. Parasites Wildl., 10:1-5. https://doi.org/10.1016/j.ijppaw.2019.06.012
Ikeda, T., Asano, M., Matoba, Y. & Abe, G. 2004. Present status of invasive alien raccoon and its impact in Japan. Glob. Environ. Res., 8(2):125-131.
Jamshidi, S., Tabrizi, A. S., Bahrami, M. & Momtaz, H. 2012. Microsporidia in household dogs and cats in Iran; a zoonotic concern. Vet. Parasitol., 185(2-4):121-123. https://doi.org/10.1016/j.vetpar.2011.10.002
Javanmard, E., Mirjalali, H., Niyyati, M., Jalilzadeh, E., Tabaei, S. J., Aghdaei, H. A., Nazemalhosseini-Mojarad, E. & Zali, M. R. 2018. Molecular and phylogenetic evidences of dispersion of human-infecting microsporidia to vegetable farms via irrigation with treated wastewater: one-year follow up. Int. J. Hyg. Environ. Health, 221(4):642-651. https://doi.org/10.1016/j.ijheh.2018.03.007
Kazemi Rad, L. & Mohammadi, H. 2016. Climate change assessment by using lars-wg model in gilan province (Iran). Geog. Environ. Hazard, 4(16):15-20.
Kord-Sarkachi, E., Tavalla, M. & Beiromvand, M. 2018. Molecular diagnosis of microsporidia strains in slaughtered cows of southwest of Iran. J. Parasit. Dis., 42(1):81-86. https://doi.org/10.1007/s12639-017-0969-4
Kresta, A. E., Henke, S. E. & Pence, D. B. 2009. Gastrointestinal helminths in raccoons in Texas. J. Wildl. Dis., 45(1):1-13.
Leigh, J. W. & Bryant, D. 2015. popart: full-feature software for haplotype network construction. Methods Ecol. Evol., 6(9):1110-1116. https://doi.org/10.1111/2041-210x.12410
Lesnianska, K., Perec-Matysiak, A., Hildebrand, J., Bunkowska-Gawlik, K., Pirog, A. & Popiolek, M. 2016. Cryptosporidium spp. and Enterocytozoon bieneusi in introduced raccoons (Procyon lotor)-first evidence from Poland and Germany. Parasitol. Res., 115(12):4535-4541. https://doi.org/10.1007/s00436-016-5245-5
Li, W., Feng, Y. & Santin, M. 2019. Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol., 35(6):436-451. https://doi.org/10.1016/j.pt.2019.04.004
Li, N., Xiao, L., Wang, L., Zhao, S., Zhao, X., Duan, L., Guo, M., Liu, L. & Feng, Y. 2012. Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Neg. Trop. Dis., 6(9):e1809.
Matos, O., Lobo, M. L. & Xiao, L. 2012. Epidemiology of Enterocytozoon bieneusi infection in humans. J. Parasitol. Res., 2012: https://doi.org/10.1155/2012/981424
Mirjalali, H., Mirhendi, H., Meamar, A. R., Mohebali, M., Askari, Z., Mirsamadi, E. S. & Rezaeian, M. 2015. Genotyping and molecular analysis of Enterocytozoon bieneusi isolated from immunocompromised patients in Iran. Infect. Genet. Evol., 36:244-249. https://doi.org/10.1016/j.meegid.2015.09.022
Mirjalali, H., Mohebali, M., Mirhendi, H., Gholami, R., Keshavarz, H., Meamar, A. R. & Rezaeian, M. 2014. Emerging intestinal microsporidia infection in HIV(+)/AIDS patients in Iran: microscopic and molecular detection. Iran J. Parasitol., 9(2):149-154.
Pirestani, M., Sadraei, J. & Forouzandeh, M. 2013. Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tehran, Iran. Infect. Genet. Evol., 20:495-499.
Sadeghi-Dehkordi, Z., Norouzi, E., Rezaeian, H., Nourian, A., Noaman, V. & Sazmand, A. 2019. First insight into Encephalitozoon cuniculi infection in laboratory and pet rabbits in Iran. Comp. Immunol. Microbiol. Infect. Dis., 65:37-40. https://doi.org/10.1016/j.cimid.2019.04.005
Santín, M. & Fayer, R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res. Vet. Sci., 90(3):363-371.
Stentiford, G. D., Becnel, J. J., Weiss, L. M., Keeling, P. J., Didier, E. S., Bjornson, S., Freeman, M. A., Brown, M. J., Roesel, K., Sokolova, Y. & Snowden, K. F. 2016. Microsporidia - emergent pathogens in the global food chain. Trends Parasitol., 32(4):336-348. https://doi.org/10.1016/j.pt.2015.12.004
Stentiford, G. D., Feist, S. W., Stone, D. M., Bateman, K. S. & Dunn, A. M. 2013. Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends Parasitol., 29(11):567-578. https://doi.org/10.1016/j.pt.2013.08.005
Sulaiman, I. M., Fayer, R., Lal, A. A., Trout, J. M., Schaefer 3rd, F. W. & Xiao, L. 2003. Molecular characterization of microsporidia indicates that wild mammals Harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl. Environ. Microbiol., 69(8):4495-4501. https://doi.org/10.1128/aem.69.8.4495-4501.2003
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 30(12):2725-2729. https://doi.org/10.1093/molbev/mst197
Tavalla, M., Kazemi, F., Mardani-Kateki, M. & Abdizadeh, R. 2018a. Molecular diagnosis of Enterocytozoon bieneusi and Encephalitozoon spp. in wild rats of southwest of Iran. Jundishapur J. Microbiol. 11(3):e55961. https://doi.org/10.5812/jjm.55961
Tavalla, M., Mardani-Kateki, M., Abdizadeh, R., Nashibi, R., Rafie, A. & Khademvatan, S. 2017. Molecular identification of Enterocytozoon bieneusi and Encephalitozoon spp. in immunodeficient patients in Ahvaz, Southwest of Iran. Acta Trop., 172:107-112.
Tavalla, M., Mardani-Kateki, M., Abdizadeh, R., Soltani, S. & Saki, J. 2018b. Molecular diagnosis of potentially human pathogenic Enterocytozoon bieneusi and Encephalitozoon species in exotic birds in Southwestern Iran. J. Infect. Public Health, 11(2):192-196. https://doi.org/10.1016/j.jiph.2017.07.028
Thellier, M. & Breton, J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite, 15(3):349-358. https://doi.org/10.1051/parasite/2008153349
Wang, Z. D., Liu, Q., Liu, H. H., Li, S., Zhang, L., Zhao, Y. K. & Zhu, X. Q. 2018. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasit. Vectors, 11(1):28. https://doi.org/10.1186/s13071-017-2558-x
Yazar, S., Koru, O., Hamamci, B., Cetinkaya, U., Karaman, U. & Kuk, S. 2013. Microsporidia and microsporidiosis. Turkiye Parazitol. Derg., 37(2):123-134. https://doi.org/10.5152/tpd.2013.28
Zeveloff, S. I. & Dewitte, E. 2002. Raccoons: a natural history. UBC Press, Vancouver, BC.
Zhang, W., Ren, G., Zhao, W., Yang, Z., Shen, Y., Sun, Y., Liu, A. & Cao, J. 2017. Genotyping of Enterocytozoon bieneusi and subtyping of Blastocystis in cancer patients: relationship to diarrhea and assessment of zoonotic transmission. Front. Microbiol., 8:1835. https://doi.org/10.3389/fmicb.2017.01835
Zhao, W., Zhang, W., Yang, F., Zhang, L., Wang, R., Cao, J., Shen, Y. & Liu, A. 2015. Enterocytozoon bieneusi in dairy cattle in the northeast of china: genetic diversity of its gene and evaluation of zoonotic transmission potential. J. Eukaryot. Microbiol., 62(4):553-560. https://doi.org/10.1111/jeu.12210

Auteurs

Ehsan Javanmard (E)

Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Arabi Street, 1985717413, Chamran Highway, Tehran, Iran.

Sara Nemati (S)

Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Arabi Street, 1985717413, Chamran Highway, Tehran, Iran.

Meysam Sharifdini (M)

Department of Medical Parasitology and Mycology, School of Medicine, Guilan University of Medical Sciences, Tehran Road Km6, Rasht, 3363, Guilan, Iran.

Ali Rostami (A)

Infectious Diseases and Tropical Medicine Research Center, Health Research Institute, Babol University of Medical Sciences, Ganjafrooz Street, 47176-47745, Babol, Mazandaran, Iran.

Hamed Mirjalali (H)

Foodborne and Waterborne Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Arabi Street, 1985717413, Chamran Highway, Tehran, Iran.

Mohammad Reza Zali (MR)

Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Arabi Street, 1985717413, Chamran Highway, Tehran, Iran.

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