Zoonotic potential of Enterocytozoon bieneusi among children in rural communities in Thailand

Parasite

and Yaowalark Sukthana²  Chalit Komalamisra¹  Dorn Watthanakulpanich¹  Aongart Mahittikorn²  Hirotake Mori² 

[1] Department of Helminthology, Faculty of Tropical Medicine, Mahidol University,Bangkok,Thailand;Department of Protozoology, Faculty of Tropical Medicine, Mahidol University,Bangkok,Thailand

关键词: Thailand;    children;    Enterocytozoon bieneusi;    zoonosis;    microsporidia;   

Others  :  808616
DOI  :  doi:10.1051/parasite/2013014

 received in 2012-12-23, accepted in 2013-03-30,  发布年份 2013

【 摘 要 】

Enterocytozoon bieneusi is a common opportunistic intestinal pathogen worldwide. Genotype distribution of E. bieneusi differs by geography and host immunity. In order to investigate the prevalence, genotype characteristics, and host specificity of E. bieneusi in the community, we conducted a preliminary cross-sectional study among children in Western and Northern Thailand. Seventy-eight (78) and 102 stool samples were collected; the prevalence of E. bieneusi was 3.8% and 2.9% by nested PCR in Western and Northern Thailand, respectively. Three genotypes were identified: Genotype D predominated, followed by EbpC, and then novel genotype ETMK1. The first two genotypes have zoonotic potential. Analysis of the genetic proximity of the E. bieneusi ITS sequences from our study, compared with those published in genetic databases, showed that all positive samples were classified into Group 1, the largest group consisting of various host specificity. The present study demonstrates the possible zoonotic transmission of E. bieneusi in rural communities in Thailand. A large-scale investigation of both human and animal samples, as well as improvements in the available phylogenetic tools, will be required to elucidate transmission routes of E. bieneusi in this area.

【 授权许可】

   
© H. Mori et al., published by EDP Sciences, 2013

【 参考文献 】

• [1]Abe N, Kimata I. 2010. Molecular survey of Enterocytozoon bieneusi in a Japanese porcine population. Vector Borne and Zoonotic Diseases, 10(4), 425–427.
• [2]Anane S, Attouchi H. 2010. Microsporidiosis: epidemiology, clinical data and therapy. Gastroenterologie Clinique et Biologique, 34(8–9), 450–464. [PubMed]
• [3]Breitenmoser AC, Mathis A, Burgi E, Weber R, Deplazes P. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology, 118(Pt 5), 447–453. [PubMed]
• [4]Breton J, Bart-Delabesse E, Biligui S, Carbone A, Seiller X, Okome-Nkoumou M, Nzamba C, Kombila M, Accoceberry I, Thellier M. 2007. New highly divergent rRNA sequence among biodiverse genotypes of Enterocytozoon bieneusi strains isolated from humans in Gabon and Cameroon. Journal of Clinical Microbiology, 45(8), 2580–2589. [PubMed]
• [5]Buckholt MA, Lee JH, Tzipori S. 2002. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Applied and Environmental Microbiology, 68(5), 2595–2599. [PubMed]
• [6]Cama VA, Pearson J, Cabrera L, Pacheco L, Gilman R, Meyer S, Ortega Y, Xiao L. 2007. Transmission of Enterocytozoon bieneusi between a child and guinea pigs. Journal of Clinical Microbiology, 45(8), 2708–2710. [PubMed]
• [7]Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke A, Löscher T, Gothe R, Rinder H. 2001. Zoonotic potential of Enterocytozoon bieneusi. Journal of Clinical Microbiology, 39(12), 4495–4499. [PubMed]
• [8]Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, Ravisse P, Modigliani R. 1985. Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. Journal of Protozoology, 32(2), 250–254.
• [9]Didier ES. 2005. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Tropica, 94(1), 61–76. [PubMed]
• [10]Didier ES, Weiss LM. 2011. Microsporidiosis: not just in AIDS patients. Current Opinion in Infectious Diseases, 24(5), 490–495. [PubMed]
• [11]Drosten C, Laabs J, Kuhn EM, Schottelius J. 2005. Interspecies transmission of Enterocytozoon bieneusi supported by observations in laboratory animals and phylogeny. Medical Microbiology and Immunology, 194(4), 207–209. [PubMed]
• [12]Dworkin MS, Buskin SE, Davidson AJ, Cohn DL, Morse A, Inungu J, Adams MR, McCombs SB, Jones JL, Moura H, Visvesvara G, Pieniazek NJ, Navin TR. 2007. Prevalence of intestinal microsporidiosis in human immunodeficiency virus-infected patients with diarrhea in major United States cities. Revista do Instituto de Medicina Tropical de Sao Paulo, 49(6), 339–342. [PubMed]
• [13]Espern A, Morio F, Miegeville M, Illa H, Abdoulaye M, Meyssonnier V, Adehossi E, Lejeune A, Cam PD, 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. Journal of Clinical Microbiology, 45(9), 2999–3002. [PubMed]
• [14]Fedorko DP, Nelson NA, Cartwright CP. 1995. Identification of microsporidia in stool specimens by using PCR and restriction endonucleases. Journal of Clinical Microbiology, 33(7), 1739–1741. [PubMed]
• [15]Franzen C, Muller A. 1999. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clinical Microbiology Reviews, 12(2), 243–285. [PubMed]
• [16]Garcia LS. 2002. Laboratory identification of the microsporidia. Journal of Clinical Microbiology, 40(6), 1892–1901. [PubMed]
• [17]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. Applied and Environmental Microbiology, 76(10), 3333–3342. [PubMed]
• [18]Lee JH. 2007. Prevalence and molecular characteristics of Enterocytozoon bieneusi in cattle in Korea. Parasitology Research, 101(2), 391–396. [PubMed]
• [19]Lee JH. 2008. Molecular detection of Enterocytozoon bieneusi and identification of a potentially human-pathogenic genotype in milk. Applied and Environmental Microbiology, 74(5), 1664–1666. [PubMed]
• [20]Leelayoova S, Piyaraj P, Subrungruang I, Pagornrat W, Naaglor T, Phumklan S, Taamasri P, Suwanasri J, Mungthin M, et al. 2009. Genotypic characterization of Enterocytozoon bieneusi in specimens from pigs and humans in a pig farm community in Central Thailand. Journal of Clinical Microbiology, 47(5), 1572–1574. [PubMed]
• [21]Leelayoova S, Subrungruang I, Rangsin R, Chavalitshewinkoon-Petmitr P, Worapong J, Naaglor T, Mungthin M. 2005. Transmission of Enterocytozoon bieneusi genotype a in a Thai orphanage. American Journal of Tropical Medicine and Hygiene, 73(1), 104–107.
• [22]Leelayoova S, Subrungruang I, Suputtamongkol Y, Worapong J, Petmitr PC, Mungthin M. 2006. Identification of genotypes of Enterocytozoon bieneusi from stool samples from human immunodeficiency virus-infected patients in Thailand. Journal of Clinical Microbiology, 44(8), 3001–3004. [PubMed]
• [23]Liguory O, Sarfati C, Derouin F, Molina JM. 2001. Evidence of different Enterocytozoon bieneusi genotypes in patients with and without human immunodeficiency virus infection. Journal of Clinical Microbiology, 39(7), 2672–2674. [PubMed]
• [24]Lobo ML, Xiao L, Cama V, Stevens T, Antunes F, Matos O. 2006. Genotypes of Enterocytozoon bieneusi in mammals in Portugal. Journal of Eukaryotic Microbiology, 53(Suppl 1), S61–S64.
• [25]Mathis A, Breitenmoser AC, Deplazes P. 1999. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite, 6(2), 189–193. [PubMed]
• [26]Muller MG, Kinne J, Schuster RK, Walochnik J. 2008. Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons. Veterinary Parasitology, 152(1–2), 67–78. [PubMed]
• [27]Reetz J, Nockler K, Reckinger S, Vargas MM, Weiske W, Broglia A. 2009. Identification of Encephalitozoon cuniculi genotype III and two novel genotypes of Enterocytozoon bieneusi in swine. Parasitology International, 58(3), 285–292. [PubMed]
• [28]Sak B, Kvac M, Hanzlikova D, Cama V. 2008. First report of Enterocytozoon bieneusi infection on a pig farm in the Czech Republic. Veterinary Parasitology, 153(3–4), 220–224. [PubMed]
• [29]Santin M, Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. Journal of Eukaryotic Microbiology, 56(1), 34–38.
• [30]Santin M, Fayer R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Research in Veterinary Science, 90(3), 363–371. [PubMed]
• [31]Santin M, Trout JM, Fayer R. 2005. Enterocytozoon bieneusi genotypes in dairy cattle in the eastern United States. Parasitology Research, 97(6), 535–538. [PubMed]
• [32]Santin M, Vecino JA, Fayer R. 2010. A zoonotic genotype of Enterocytozoon bieneusi in horses. Journal of Parasitology, 96(1), 157–161.
• [33]Stark D, van Hal S, Barratt J, Ellis J, Marriott D, Harkness J. 2009. Limited genetic diversity among genotypes of Enterocytozoon bieneusi strains isolated from HIV-infected patients from Sydney, Australia. Journal of Medical Microbiology, 58(Pt 3), 355–357. [PubMed]
• [34]Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, 3rd, Xiao L. 2003. Molecular characterization of microsporidia indicates that wild mammals Harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Applied and Environmental Microbiology, 69(8), 4495–4501. [PubMed]
• [35]Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24(8), 1596–1599. [PubMed]
• [36]ten Hove RJ, Van Lieshout L, Beadsworth MB, Perez MA, Spee K, Claas EC, Verweij JJ. 2009. Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups. Journal of Eukaryotic Microbiology, 56(4), 388–393.
• [37]Thellier M, Breton J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite, 15(3), 349–358. [PubMed]
• [38]Tumwine JK, Kekitiinwa A, Nabukeera N, Akiyoshi DE, Buckholt MA, Tzipori S. 2002. Enterocytozoon bieneusi among children with diarrhea attending Mulago Hospital in Uganda. American Journal of Tropical Medicine and Hygiene, 67(3), 299–303.
• [39]van Hal SJ, Muthiah K, Matthews G, Harkness J, Stark D, Cooper D, Marriott D. 2007. Declining incidence of intestinal microsporidiosis and reduction in AIDS-related mortality following introduction of HAART in Sydney, Australia. Transactions of the Royal Society of Tropical Medicine and Hygiene, 101(11), 1096–1100. [PubMed]
• [40]Zhang X, Wang Z, Su Y, Liang X, Sun X, Peng S, Lu H, Jiang N, Yin J, Xiang M, Chen Q. 2011. Identification and genotyping of Enterocytozoon bieneusi in China. Journal of Clinical Microbiology, 49(5), 2006–2008. [PubMed]