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Phylogenetic analysis of genetically distinct Enterocytozoon bieneusi infecting renal transplant recipients

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Abstract

Enterocytozoon bieneusi (E. bieneusi), infecting renal transplant (RT) recipients may be transmitted anthropologically or zoologically. Accordingly, we aimed to a) evaluate genotypes of E. bieneusi ínfecting RT recipients, and b) infer phylogenetic interpretation on transmission of different genotypes among infected hosts. Stool samples of 22 RT recipients infected with microsporidia (identified using modified trichrome staining) were subjected to species identification. All E. bieneusi positive samples were subjected to genotyping. The phylogenetic tree was constructed using Mega 5 software. Of 22 microsporidia infected RT recipients, 21/22 (95.5%) had E. bieneusi. ITS sequences of 21 E. bieneusi were classified into eight genotypes (Ind1 to Ind8). Among them, 4 (Ind5 to Ind8) were novel. Genotypes Ind2, Ind3, Ind4, Ind7 and Ind8 showed close sequence similarity to genotypes reported exclusively from humans. Phylogenetic analysis further supported their anthroponotic transmission. Genotypes Ind1, Ind5 and Ind6 showed close sequence similarity to genotypes reported from both animals and humans. Phylogenetic analysis further supported their zoonotic transmission. Anthroponotic transmission of E. bieneusi was more common among males (11, 100% vs. 7/10, 70%; P = 0.05), presenting with diarrhea (11, 100% vs. 6/10, 60%; P = 0.02) and watery stool (10/11, 91% vs. 5/10, 50%; P = 0.03).

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References

  • Akinbo F.O., Okaka C.E., Omoregie R., Dearen T., Leon E.T., Xiao L. 2012. Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. American Journal of Tropical Medicine and Hygiene, 86, 441–445. DOI: 10.4269/ajtmh.2012.11-0548

    Article  Google Scholar 

  • 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, 2580–2589. DOI: 10.1128/JCM.02554-06

    Article  CAS  Google Scholar 

  • Conteas C.N., Berlin O.G., Ash L.R., Pruthi J.S. 2000. Therapy for human gastrointestinal microsporidiosis. American Journal of Tropical Medicine and Hygiene, 63, 121–127

    Article  CAS  Google Scholar 

  • Dengjel B., Zahler M., Hermanns W., Heinritzi K., Spillmann T., Thomschke A., Loscher T., Gothe R., Rinder H. 2001. Zoonotic potential of Enterocytozoon bieneusi. Journal of Clinical Microbiology, 39, 4495–4499. DOI: 10.1128/JCM.39.12.4495-4499.2001

    Article  CAS  Google Scholar 

  • Didier E.S., Weiss L.M. 2011. Microsporidiosis: not just in AIDS patients. Current Opinion in Infectious Diseases, 24, 490–495. DOI: 10.1097/QCO.0b013e32834aa152

    Article  Google Scholar 

  • Ghoshal U., Khanduja S., Pant P., Prasad K.N., Dhole T.N., Sharma R.K., Ghoshal U.C. 2015. Intestinal microsporidiosis in renal transplant recipients: Prevalence, predictors of occurrence and genetic characterization. Indian Journal of Medical Microbiology, 33, 357–363. DOI: 10.4103/0255-0857.158551

    Article  CAS  Google Scholar 

  • Karp C.L., Auwaerter P.G. 2007. Coinfection with HIV and tropical infectious diseases. II. Helminthic, fungal, bacterial, and viral pathogens. Clinical Infectious Diseases, 45, 1214–1220. DOI: 10.1086/522180

    Article  Google Scholar 

  • 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, 104–107

    Article  Google Scholar 

  • Leelayoova S., Piyaraj P., Subrungruang I., Pagornrat W., Naaglor T., Phumklan S., Taamasri P., Suwanasri J., Mungthin M. 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, 1572–1574. DOI: 10.1128/JCM.00187-09

    Article  Google Scholar 

  • Liguory O., Sarfati C., Derouin F., Molina J.M. 2001. Evidence of different Enterocytozoon bieneusi genotypes in patients with and without human immunodeficiency virus infection. Journal of Clinical Microbiology, 39, 2672–2674. DOI: 10.1128/JCM.39.7.2672-2674.2001

    Article  CAS  Google Scholar 

  • Mathis A., Breitenmoser A.C., Deplazes P. 1999. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite, 6, 189–193. DOI: 10.1051/parasite/1999062189

    Article  CAS  Google Scholar 

  • Mathis A., Weber R., Deplazes P. 2005. Zoonotic potential of the microsporidia. Clinical Microbiology Reviews, 18, 423–445. DOI: 10.1128/CMR.18.3.423-445.2005

    Article  CAS  Google Scholar 

  • Mori H., Mahittikorn A., Thammasonthijarern N., Chaisiri K., Rojekittikhun W., Sukthana Y. 2013. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Veterinary Parasitology, 197, 696–701. DOI: 10.1016/j.vetpar. 2013.07.025

    Article  Google Scholar 

  • Pomares C., Santin M., Miegeville M., Espern A., Albano L., Marty P., Morio F. 2012. A new and highly divergent Enterocytozoon bieneusi genotype isolated from a renal transplant recipient. Journal of Clinical Microbiology, 50, 2176–2178. DOI: 10.1128/JCM.06791-11

    Article  Google Scholar 

  • Raynaud L., Delbac F., Broussolle V., Rabodonirina M., Girault V., Wallon M., Cozon G., Vivares C.P., Peyron F. 1998. Identification of Encephalitozoon intestinalis in travelers with chronic diarrhea by specific PCR amplification. Journal of Clinical Microbiology, 36, 37–40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rinder H., Thomschke A., Dengjel B., Gothe R., Loscher T., Zahler M. 2000. Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. Journal of Parasitology, 86, 185–188. DOI: 10.1645/0022-3395(2000)086[0185:CGRBEB]2.0.CO;2

    Article  CAS  Google Scholar 

  • Santin M., Trout J.M., Vecino J.A., Dubey J.P., Fayer R. 2006. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Veterinary Parasitology, 141, 334–339. DOI: 10.1016/j.vetpar.20 06.06.004

    Article  Google Scholar 

  • Santin M., Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. Journal of Eukaryotic Microbiology, 56, 34–38. DOI: 10.1111/j.1550-7408.2008.00380.x

    Article  CAS  Google Scholar 

  • Santin M., Fayer R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Research in Veterinary Science, 90, 363–371. DOI: 10.1016/j.rvsc.2010.07.014

    Article  Google Scholar 

  • Slodkowicz-Kowalska A., Graczyk T.K., Tamang L., Jedrzejewski S., Nowosad A., Zduniak P., Solarczyk P., Girouard A.S., Majewska A.C. 2006. Microsporidian species known to infect humans are present in aquatic birds: implications for transmission via water? Applied and Environmental Microbiology, 72, 4540–4544. DOI: 10.1128/AEM.02503-05

    Article  CAS  Google Scholar 

  • Sulaiman I.M., Bern C., Gilman R., Cama V., Kawai V., Vargas D., Ticona E., Vivar A., Xiao L. 2003a. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. Journal of Eukaryotic Microbiology, 50 Suppl, 591–596. DOI: 10.1111/j.1550-7408.2003.tb00642.x

    Article  CAS  Google Scholar 

  • Sulaiman I.M., Fayer R., Lal A.A., Trout J.M., Schaefer F.W., Xiao L. 2003b. 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, 4495–4501. DOI: 10.1128/AEM.69.8.4495-4501.2003

    Article  CAS  Google Scholar 

  • ten Hove R.J., Van Lieshout L., Beadsworth M.B., Perez M.A., Spee K., Claas E.C., Verweij J.J. 2009. Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups. Journal of Eukaryotic Microbiology, 56, 388–393. DOI: 10.1111/j.1550-7408.2009. 00393.x

    Article  Google Scholar 

  • Thellier M., Breton J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite, 15, 349–358. DOI: 10.1051/parasite/2008153349

    Article  CAS  Google Scholar 

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Correspondence to Ujjala Ghoshal.

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Khanduja, S., Ghoshal, U. & Ghoshal, U.C. Phylogenetic analysis of genetically distinct Enterocytozoon bieneusi infecting renal transplant recipients. Acta Parasit. 62, 63–68 (2017). https://doi.org/10.1515/ap-2017-0007

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  • DOI: https://doi.org/10.1515/ap-2017-0007

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