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Asymptomatic Enterocytozoon bieneusi microsporidiosis in captive mammals

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Abstract

Human microsporidiosis, a serious disease of immunocompetent and immunosuppressed people, can be due to zoonotic transmission of microsporidian spores. A survey utilizing chromotrope 2R stain and fluorescent in situ hybridization techniques for testing feces from 193 captive mammals demonstrated that 3 animals (1.6%) shed Encephalitozoon bieneusi spores. These include two critically endangered species (i.e., black lemurs, Eulemur macaco flavifrons; and Visayan warty pig, Sus cebifrons negrinus) and a threatened species (mongoose lemur, Eulemur mongoz). The concentration of spores varied from 2.7 × 105 to 5.7 × 105/g of feces, and all infections were asymptomatic. The study demonstrates that E. bieneusi spores can originate from captive animals, which is of particular epidemiologic importance because the close containment of zoological gardens can facilitate pathogen spread to other animals and also to people such as zoo personnel and visitors.

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References

  • Ash LR, Orihel TC (1989) Parasites: a guide to laboratory procedures and identification. ASCP Press, Chicago, IL, pp 327

    Google Scholar 

  • 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 118:447–453

    Article  PubMed  Google Scholar 

  • Bretagne S, Foulet F, Alkassoum W, FleuryFeith J, Develoux M (1993) Prevalence of Enterocytozoon bieneusi spores in the stool of AIDS patients and African children not infected by HIV. Bull Soc Pathol Exot 86:351–357

    PubMed  CAS  Google Scholar 

  • Buckholt MA, Lee JH, Tzipori S (2002) Prevalence of Enterocytozoon bieneusi in swine: an 18 month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 68:2595–2599

    Article  PubMed  CAS  Google Scholar 

  • Chalifoux LV, MacKey J, Carville A, Shvetz D, Lin KC, Lackner A, Mansfield KG (1998) Ultrastructural morphology of Enterocytozoon bieneusi in biliary epithelium of rhesus macaques (Macaca mulatta). Vet Pathol 35:292–296

    Article  PubMed  CAS  Google Scholar 

  • Cegielski JP, Ortega YR, McKee S, Madden JF, Gaido L, Schwartz DA, Manji K, Jorgensen AF, Miller SE, Pulipaka UP, Msengi AE, Mwakyusa DH, Sterling CR (1999) Cryptosporidium, Enterocytozoon, and Cyclospora infections in patients in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis 28:314–321

    PubMed  CAS  Google Scholar 

  • Del Aguila C, Lopez-Velez R, Fenoy S, Turrientes C, Cobo J, Navajas R, Visvesvara GS, Croppo GP, DaSilva AJ, Pieniazek NJ (1997) Identification of Enterocytozoon bieneusi spores in respiratory samples from an AIDS patient with a 2 year history of intestinal microsporidiosis. J Clin Microbiol 35:1862–1866

    PubMed  Google Scholar 

  • Del Aguila C, Izquierdo F, Navajas R, Pieniazek NJ, Miro G, Alonso AI, DaSilva AJ, Fenoy S (1999) Enterocytozoon bieneusi in animals: rabbits and dogs as new hosts. J Eukaryot Microbiol 46:8S–9S

    PubMed  Google Scholar 

  • Del Aguila C, Izquierdo F, Haro M, Bernardo R,Rueda C, Andres I, Alonso F, Ponce F, Fenoy S, Henriques N (2004) Zoonotic potential of microsporidiosis in Spain. In: Emergent pathogens in the 21st century: first united workshop on microsporidia from invertebrate and vertebrate hosts, Ceske Budejovice, 12–15 July 2004, pp 200

  • Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke Aa, Loscher T, Gothe R, Rinder H (2001) Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol 39:4495–4499

    Article  PubMed  CAS  Google Scholar 

  • Deplazes P, Mathis A, Muller C, Weber R (1996) Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J Eukaryot Microbiol 43:93S

    PubMed  CAS  Google Scholar 

  • Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, Ravisse P, Modigliani R (1985) Occurrence of a new microsporidian: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. J Protozool 32:250–254

    PubMed  CAS  Google Scholar 

  • Didier ES (2005) Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop 94:61–76

    Article  PubMed  CAS  Google Scholar 

  • Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ (2004) Epidemiology of microsporidiosis: source and modes of transmission. Vet Parasitol 126:145–166

    Article  PubMed  CAS  Google Scholar 

  • Drosten C, Laabs J, Kuhn EM, Schottelius J (2005) Interspecies transmission of Enterocytozoon bieneusi supported by observations in laboratory animals and phylogeny. Med Microbiol Immunol 194:207–209

    Article  PubMed  CAS  Google Scholar 

  • Goodgame R, Stager C, Marcantel B, Alcocer E, Segura AM (1999) Intensity of infection in AIDS-related intestinal microsporidiosis. J Infect Dis 180:929–932

    Article  PubMed  CAS  Google Scholar 

  • Graczyk TK, Cranfield MR (2000) Cryptosporidium serpentis oocysts and microsporidian spores in stools of captive snakes. J Parasitol 86:413–414

    PubMed  CAS  Google Scholar 

  • Graczyk TK, Bosco-Nizeyi J, DaSilva AJ, Moura INS, Pieniazek NJ, Cranfield MR, Lindguist HDA (2002) A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats, Uganda. Parasitol Res 88:926–931

    Article  PubMed  Google Scholar 

  • Graczyk TK, Conn DB, Lucy F, Minchin D, Tamang L, Moura LNS, DaSilva AJ (2004) Human waterborne parasites in zebra mussels (Dreissena polymorpha) from the Shannon River drainage, Ireland. Parasitol Res 93:389–391

    Article  Google Scholar 

  • Guscetti F, Mathis A, Hatt JM, Deplazes P (2003) Overt fatal and chronic subclinical Encephalitozoon cuniculi microsporidiosis in a colony of captive emperor tamarins (Saguinus imperator). J Med Primatol 32:111–119

    PubMed  CAS  Google Scholar 

  • Haro M, Izquiero F, Henriques-Gil N, Alonso AF, Fenoy S, delAquila C (2005) First detection and genotyping of human-associated microsporidia in pigeons form urban parks. Appl Environ Microbiol 71:3153–3157

    Article  PubMed  CAS  Google Scholar 

  • Lobo ML, Teles A, DaCunha MB, Hendriques J, Lourenco AM, Antunes F, Matos O (2003) Microsporidia detection is stools from pets and animals from the zoo in Portugal: a preliminary study. J Eukaryot Microbiol 50(Suppl):581–582

    Article  PubMed  Google Scholar 

  • Lores B, Del Aguila C, Arias C (2002) Enterocytozoon bieneusi (microsporidia) in faecal samples from domestic animals from Galicia, Spain. Mem Inst Oswaldo Cruz 97:941–945

    Article  PubMed  CAS  Google Scholar 

  • Majewska AC, Kasprzak W, Werner A (1997) Prevalence of Cryptosporidium in mammals housed in Poznan zoological garden, Poland. Acta Parasitol 42:195–198

    Google Scholar 

  • Mansfield KG, Carville A, Herbert D, Chalifoux L, Shvetz D, Lin KC, Tzipori S, Lackner AA (1998) Localization of persistent Enterocytozoon bieneusi infection in normal rhesus macaques (Macaca mulatta) to the hepatobiliary tree. J Clin Microbiol 36:2336–2338

    PubMed  CAS  Google Scholar 

  • Mathis A, Breitenmoser AC, Deplazes P(1999) Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite 6:189–193

    PubMed  CAS  Google Scholar 

  • Mungthin M, Suwannasaeng R, Naaglor T, Areekul W, Leelayoo S (2001) Asymptomatic intestinal microsporidiosis in Thai orphans and childcare workers. Trans R Soc Trop Med Hyg 95:304–306

    Article  PubMed  CAS  Google Scholar 

  • Oliver WLR (2004) First (and last?) breeding loan export of Visayan (Negros) warty pigs. Suiform Soundings 4:25–27

    Google Scholar 

  • Pol S, Romana C, Richard S, Carnot F, Dumont JL, Bouche H, Pialox G, Stern M, Pays JF, Bertelot P (1992) Enterocytozoon bieneusi in acquired immunodeficiency syndrome related-sclerosing cholangitis. Gastroenterology 102:1778–1781

    PubMed  CAS  Google Scholar 

  • Pourrut X, Sarfati C, Liguory O, Moyou-Somo R, Derouin F (2002) Search for Enterocytozoon bieneusi infection in wild monkeys in Cameroon. Trans R Soc Trop Med Hyg 96:56–57

    Article  PubMed  CAS  Google Scholar 

  • Reetz J, Rinder H, Thomschke A, Manke H, Schwebs M, Bruderek A (2002) First detection of the microsporidium Enterocytozoon bieneusi in nonmammalian hosts (chickens). Int J Parasitol 32:785–787

    Article  PubMed  Google Scholar 

  • Rinder H, Thomschke A, Dengjel B, Gothe R, Loschner T, Zahler M (2000) Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J Parasitol 86:185–188

    PubMed  CAS  Google Scholar 

  • Santin M, Trout JM, Fayer R (2004) Prevalence of Enterocytozoon bieneusi in postweaned dairy calves in the eastern United States. Parasitol Res 93:287–289

    Article  PubMed  Google Scholar 

  • Santin M, Trout JM, Fayer R (2005) Enterocytozoon bieneusi genotypes in dairy cattle in the eastern United States. Parasitol Res 97:535–538

    Article  PubMed  CAS  Google Scholar 

  • Schwartz DA, Anderson DC, Klumpp SA, McClure HM (1998) Ultrastructure of atypical (teratoid) sporogonial stages of Enterocytozoon bieneusi (Microsporidia) in naturally infected rhesus monkeys (Macacca mulatta). Arch Pathol Lab Med 122:423–429

    PubMed  CAS  Google Scholar 

  • Slodkowicz-Kowalska A, Graczyk TK, Tamang L, Jedrzejewski S, Nowosad A, Zduniak P, Solarczyk P, Girouard AS, Majewska AC (2006) Microsporidia species known to infect humans are present in aquatic birds; implications for transmission via water? Appl Environ Microbiol 72:4540–4544

    Article  PubMed  CAS  Google Scholar 

  • Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, 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 69:4495–4501

    Article  PubMed  CAS  Google Scholar 

  • Sulaiman IM, Fayer R, Yang C, Santin M, Matos O, Xiao L (2004) Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Parasitol Res 92:328–334

    Article  PubMed  Google Scholar 

  • Vesey G, Ashbolt N, Fricker EJ, Deere D, William KL, Veal DA, Dorsch M (1998) The use of a ribosomal RNA targeted oligonucleotide probe for fluorescent labelling of viable Cryptosporidium parvum oocysts. J Appl Microbiol 85:429–440

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Mrs. Ewa Trzesowska, M.Sc., the Poznan Zoological Garden, Poland, for facilitating fecal sample collection. This study was supported by NATO Collaborative Linkage Grant, Brussels, Belgium (grant no. 979765), Johns Hopkins Center in Urban Environmental Health (grant no. P30 ES03819), Alternatives Research & Development Foundation, NOAA Chesapeake Bay Office (grant no. NA04NMF4570426), Procter & Gamble Foundation, The Center for a Livable Future, and the Poznan University of Medical Sciences, Poznan, Poland (grant no. 501-01-03496).

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Authors and Affiliations

  1. Department of Biology and Medical Parasitology, Poznan University of Medical Sciences, 10 Fredry Street, Poznan, 61-701, Poland

    Anna Slodkowicz-Kowalska & Anna C. Majewska

  2. Division of Environmental Health Engineering, Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, MD, 21205, USA

    Thaddeus K. Graczyk & Leena Tamang

  3. Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, MD, 21205, USA

    Thaddeus K. Graczyk & Autumn S. Girouard

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  1. Anna Slodkowicz-Kowalska
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  2. Thaddeus K. Graczyk
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  3. Leena Tamang
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  4. Autumn S. Girouard
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  5. Anna C. Majewska
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Correspondence to Thaddeus K. Graczyk.

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Slodkowicz-Kowalska, A., Graczyk, T.K., Tamang, L. et al. Asymptomatic Enterocytozoon bieneusi microsporidiosis in captive mammals. Parasitol Res 100, 505–509 (2007). https://doi.org/10.1007/s00436-006-0303-z

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  • DOI: https://doi.org/10.1007/s00436-006-0303-z

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