Prevalence and Genotyping of Microsporidian Parasites in Dogs in Turkey: Zoonotic Concerns.
Encephalitozoon cuniculi
Encephalitozoon intestinalis
Dog
molecular characterization
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:
09 2019
09 2019
Historique:
received:
11
12
2018
revised:
19
02
2019
accepted:
02
03
2019
pubmed:
9
3
2019
medline:
17
6
2020
entrez:
9
3
2019
Statut:
ppublish
Résumé
Microsporidia are opportunistic pathogens that infect a wide range of invertebrates and vertebrates. To assess the potential role of dogs in the transmission of these zoonotic pathogens, a total of 282 fecal samples from dogs in the Central Anatolia Region of Turkey were analyzed by utilizing species specific polymerase chain reaction for the four most frequent human microsporidia. Two microsporidia species were recognized in 41 samples (14.5%). Encephalitozoon intestinalis was detected in 35 samples (12.4%) and it was the most common microsporidium. The second microsporidium, E. cuniculi, was identified in six (2.1%) of the samples. Sequence analysis of the intergenic spacer of the ribosomal ribonucleic acid (RNA) internal transcribed spacer (ITS) gene revealed the presence of three E. intestinalis haplotypes closely associated with each other. No polymorphic region was found among the ITS sequences of E. cuniculi isolates and they were characterized as genotype III. This study provides the first data on the zoonotic microsporidia species from dogs in Turkey.
Banques de données
GENBANK
['KX925857', 'KX925860', 'KX925858', 'KX925859']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
771-777Informations de copyright
© 2019 International Society of Protistologists.
Références
Abu-Akkada, S. S., Ashmawy, K. I. & Dweir, A. W. 2015. First detection of an ignored parasite, Encephalitozoon cuniculi, in different animal hosts in Egypt. Parasitol. Res., 114:843-850.
del Aguila, C., Moura, H., Fenoy, S., Navajas, R., Lopez-Velez, R., Li, L., Xiao, L., Leitch, G. J., da Silva, A., Pieniazek, N. J., Lal, A. A. & Visvesvara, G. S. 2001. In vitro culture, ultrastructure, antigenic, and molecular characterization of Encephalitozoon cuniculi isolated from urine and sputum samples from a Spanish patient with AIDS. J. Clin. Microbiol., 39:1105-1108.
Al-Herrawy, A. Z. & Gad, M. A. 2016. Microsporidial spores in fecal samples of some domesticated animals living in Giza, Egypt. Iran J. Parasitol., 11:195-203.
Cetinkaya, U., Yazar, S., Kuk, S., Sivcan, E., Kaynar, L., Arslan, D. & Sahin, I. 2016. The high prevalence of Encephalitozoon intestinalis in patients receiving chemotherapy and children with growth retardation and the validity of real-time PCR in its diagnosis. Turk. J. Med. Sci., 46:1050-1058.
Cray, C. & Rivas, Y. 2013. Seroprevalence of Encephalitozoon cuniculi in dogs in the United States. J. Parasitol., 99:153-154.
Didier, E. S., Rogers, L. B., Orenstein, J. M., Baker, M. D., Vossbrinck, C. R., Van Gool, T., Hartskeerl, R., Soave, R. & Beaudet, L. M. 1996. Characterization of Encephalitozoon (Septata) intestinalis isolates cultured from nasal mucosa and bronchoalveolar lavage fluids of two AIDS patients. J. Eukaryot. Microbiol., 43:34-43.
Didier, E. S. & Weiss, L. M. 2011. Microsporidiosis: not just in AIDS patients. Curr. Opin. Infect Dis., 24:490.
Franzen, C. & Muller, A. 1999. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin. Microbiol. Rev., 12:243-285.
Furuya, K. 2009. Spore-forming microsporidian encephalitozoon: current understanding of infection and prevention in Japan. Jpn. J. Infect. Dis., 62:413-422.
Galván-Díaz, A. L., Magnet, A., Fenoy, S., Henriques-Gil, N., Haro, M., Gordo, F. P., Miró, G., del Águila, C. & Izquierdo, F. 2014. Microsporidia detection and genotyping study of human pathogenic E. bieneusi in animals from Spain. PLoS ONE, 9:e92289.
García-Torres, I., la Mora-De, D., la Mora, I., Hernández-Alcántara, G., Molina-Ortiz, D., Caballero-Salazar, S., Olivos-García, A., Nava, G., López-Velázquez, G. & Enríquez-Flores, S. 2018. First characterization of a microsporidial triosephosphate isomerase and the biochemical mechanisms of its inactivation to propose a new druggable target. Sci. Rep., 8:8591.
Guindon, S. & Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 52:696-704.
Hamamci, B., Cetinkaya, U., Berk, V., Kaynar, L., Kuk, S. & Yazar, S. 2015. Prevalence of Encephalitozoon intestinalis and Enterocytozoon bieneusi in cancer patients under chemotherapy. Mikrobiyol. Bul., 49:105-113.
Haro, M., Del Aguila, C., Fenoy, S. & Henriques-Gil, N. 2003. Intraspecies genotype variability of the microsporidian parasite Encephalitozoon hellem. J. Clin. Microbiol., 41:4166-4171.
Jamshidi, S. H., Tabrizi, A. S., Bahrami, M. & Momtaz, H. 2012. Microsporidia in household dogs and cats in Iran; a zoonotic concern. Vet. Parasitol., 185:121-123.
Jimenez-Gonzalez, G., Martínez-Gordillo, M. N., Caballero-Salazar, S., Peralta-Abarca, G. E., Cárdenas-Cardoz, R., Arzate-Barbosa, P. & Ponce-Macotela, M. 2012. Microsporidia in pediatric patients with leukemia or limphoma. Rev. Invest. Clin., 64:25-31.
Karaman, U., Daldal, N., Atambay, M. & Colak, C. 2009. The epidemiology of microsporidias in humans (Malatya sample). Turk. J. Med. Sci., 39:281-288.
Karim, M. R., Dong, H., Yu, F., Jian, F., Zhang, L., Wang, R., Zhang, S., Rume, F. I., Ning, C. & Xiao, L. 2014. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J. Clin. Microbiol., 52:3297-3302.
Katzwinkel-Wladarsch, S., Lieb, M., Helse, W., Löscher, T. & Rinder, H. 1996. Direct amplification and species determination of microsporidian DNA from stool specimens. Trop. Med. Int. Health, 1:373-378.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28:1647-1649.
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol., 16:111-120.
Kotková, M., Sak, B., Květoňová, D. & Kváč, M. 2013. Latent microsporidiosis caused by Encephalitozoon cuniculi in immunocompetent hosts: a murine model demonstrating the ineffectiveness of the immune system and treatment with albendazole. PLoS ONE, 8:e60941.
Kumar, S., Stecher, G. & Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 33:1870-1874.
Künzel, F., Peschke, R., Tichy, A. & Joachim, A. 2014. Comparison of an indirect fluorescent antibody test with Western blot for the detection of serum antibodies against Encephalitozoon cuniculi in cats. Parasitol. Res., 113:4457-4462.
Liguory, O., Fournier, S., Sarfati, C., Derouin, F. & Molina, J. M. 2000. Genetic homology among thirteen Encephalitozoon intestinalis isolates obtained from human immunodeficiency virus-infected patients with intestinal microsporidiosis. J. Clin. Microbiol., 38:2389-2391.
Lindsay, D. S., Goodwin, D. G., Zajac, A. M., Corte′s-Vecino, J. A., Gennari, S. M., Rosypal, A. C. & Dubey, J. P. 2009. Serological survey for antibodies to Encephalitozoon cuniculi in ownerless dogs from urban areas of Brazil and Colombia. J. Parasitol., 95:760-763.
Lobo, M. L., Teles, A., da Cunha, M. B., Henriques, J., Lourenco, A. M., Antunes, F. & Matos, O. 2003. Microsporidia detection in stools from pets and animals from the zoo in Portugal: a preliminary study. J. Eukaryot. Microbiol., 50:581-582.
Mathis, A., Weber, R. & Deplazes, P. 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev., 18:423-445.
McInnes, E. F. & Stewart, C. G. 1991. The pathology of subclinical infection of Encephalitozoon cuniculi in canine dams producing pups with overt encephalitozoonosis. J. S. Afr. Vet. Assoc., 62:51-54.
Moretto, M. M., Khan, I. A. & Weiss, L. M. 2012. Gastrointestinal cell mediated immunity and the microsporidia. PLoS Pathog., 8:e1002775.
Nei, M. & Kumar, S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, Oxford.
Piekarska, J., Kicia, M., Wesołowska, M., Kopacz, Ż., Gorczykowski, M., Szczepankiewicz, B., Kváč, M. & Sak, B. 2017. Zoonotic microsporidia in dogs and cats in Poland. Vet. Parasitol., 246:108-111.
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.
Posada, D. 2008. jModel test: phylogenetic model averaging. Mol. Biol. Evol., 25:1253-1256.
Santín, M., Cortés Vecino, J. & Fayer, R. 2008. Enterocytozoon bieneusi genotypes in dogs in Bogota, Colombia. Am. J. Trop. Med. Hyg., 79:215-217.
Santín, M. & Fayer, R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res. Vet. Sci., 90:363-371.
Santín, M., Trout, J. M., Cortés Vecino, J. A., Dubey, J. P. & Fayer, R. 2006. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet. Parasitol., 141:334-339.
Sasaki, M., Yamazaki, A., Haraguchi, A., Tatsumi, M., Ishida, K. & Ikadai, H. 2011. Serological survey of Encephalitozoon cuniculi infection in Japanese dogs. J. Parasitol., 97:167-169.
da Silva, A. J., Sch Wartz, D. A., Visvesvara, G. S., de Moura, H., Slemenda, S. B. & Pieniazek, N. J. 1996. Sensitive PCR diagnosis of Infections by Enterocytozoon bieneusi (microsporidia) using primers based on the region coding for small-subunit rRNA. J. Clin. Microbiol., 34:986-987.
Snowden, K. F., Lewis, B. C., Hoffman, J. & Mansell, J. 2009. Encephalitozoon cuniculi infections in dogs: a case series. J. Am. Anim. Hosp. Assoc., 45:225-231.
Snowden, K. F. & Shadduck, J. A. 1999. Microsporidia in higher vertebrates. In: Wittner, M. (ed.), The Microsporidia and Microsporidiosis. ASM Press, Washington DC. p. 393-417.
Sulaiman, I. M., Bern, C., Gilman, R., Cama, V., Kawai, V., Vargas, D., Ticona, E., Vivar, A. & Xiao, L. 2003. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima. Peru. J. Eukaryot. Microbiol., 50:591-596.
Tamura, K., Steche, G., Peterson, D., Fillipski, A. & Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 30:2725-2729.
Turk, S., Dogruman, A. F., Karaman, U. & Kustimur, S. 2012. Investigation of microsporidia prevalence by different staining methods in cases of diarrhea. Mikrobiyol. Bul., 46:85-92.
Velásquez, J. N., Chertcoff, A. V., Etchart, C., di Risio, C., Sodré, F. C., Cucher, M. A. & Carnevale, S. 2012. First case report of infection caused by Encephalitozoon intestinalis in a domestic cat and a patient with AIDS. Vet. Parasitol., 190:583-586.
Visvesvara, G. S., Leitch, G. J., da Silva, A. J., Croppo, G. P., Moura, H., Wallace, S., Slemenda, S. B., Schwartz, D. A., Moss, D. & Bryan, R. T. 1994. Polyclonal and monoclonal antibody and PCR-amplified small-subunit rRNA identification of a microsporidian, Encephalitozoon hellem, isolated from an AIDS patient with disseminated infection. J. Clin. Microbiol., 32:2760-2768.
Wan, Q., Lin, Y., Mao, Y., Yang, Y., Li, Q., Zhang, S., Jiang, Y., Tao, W. & Li, W. 2016. High prevalence and widespread distribution of zoonotic Enterocytozoon bieneusi genotypes in swine in Northeast China: implications for public health. J. Eukaryot. Microbiol., 63:162-170.
Wang, S. S., Wan, R. J., Fan, X. C., Liu, T. L., Zhang, L. X. & Zhao, G. H. 2018. Prevalence and genotypes of Enterocytozoon bieneusi in China. Acta Trop., 183:142-152.
Weber, R., Bryan, R. T., Schwartz, D. A. & Owen, R. L. 1994. Human microsporidial infections. Clin. Microbiol. Rev., 7:426-461.
Wittne, M. & Weiss, L. M. 1999. The Microsporidia and Microsporidiosis. American Society for Microbiology, Washington, DC.
Xiao, L., Li, L., Moura, H., Sulaiman, I. M., Lal, A. A., Gatti, S., Scaglia, M., Didier, E. S. & Visvesvara, G. S. 2001. Genotyping Encephalitozoon parasites using multilocus analyses of genes with repetitive sequences. J. Eukaryot. Microbiol. Suppl., 48:63-65.
Xu, H., Jin, Y., Wu, W., Li, P., Wang, L., Li, N., Feng, Y. & Xiao, L. 2016. Genotypes of Cryptosporidium spp., Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai, China. Parasit. Vectors., 9:121.