First detection and genotyping of human-associated microsporidia in pigeons from urban parks

Applied and Environmental Microbiology

Volumn 71, Issue 6, 2005, Pages 3153-3157

  Haro, M ^a   Izquierdo, F ^a   Henriques Gil, N ^a   Andres I ^a   Alonso, F ^b   Fenoy, S ^a   Del Aguila C ^a,c  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

^c Facultad de Farmacia   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; DNA; LIVING SYSTEMS STUDIES;

ANIMAL PHYLA; GENOTYPING; MICROSPORIDIA; ZOONOTIC POTENTIAL;

GENETIC ENGINEERING;

PARASITE;

ARTICLE; CONTROLLED STUDY; DNA ISOLATION; ENCEPHALITOZOON INTESTINALIS; ENVIRONMENTAL FACTOR; ENVIRONMENTAL SANITATION; FECES ANALYSIS; GENOTYPE; HIGH RISK POPULATION; HOST PARASITE INTERACTION; HUMAN; MICROSPORIDA; MICROSPORIDIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPPORTUNISTIC INFECTION; PIGEON; SPAIN; URBAN AREA;

ANIMALS; BASE SEQUENCE; BIRD DISEASES; COLUMBIDAE; DNA, INTERGENIC; DNA, PROTOZOAN; ENCEPHALITOZOON; ENTEROCYTOZOON; GENOTYPE; HUMANS; MICROSPORIDIOSIS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SPAIN; URBAN HEALTH; ZOONOSES;

ANIMALIA; COLUMBA; ENCEPHALITOZOON CUNICULI; ENCEPHALITOZOON HELLEM; ENCEPHALITOZOON INTESTINALIS; ENTEROCYTOZOON BIENEUSI; MICROSPORIDIA;

EID: 20444362658     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.6.3153-3157.2005     Document Type: Article

References (61)

1. Akerstedt, J., K. Nordstoga, A. Mathis, E. Smeds, and P. Deplazes. 2002. Fox encephalitozoonosis: isolation of the agent from an outbreak in farmed blue foxes (Alopex lagopus) in Finland and some hitherto unreported pathologic lesions. J. Vet. Med. B Infect. Dis. Vet. Public Health 49:400-405.
2. Ben-Yehuda, A., and M. E. Weksler. 1992. Immune senescence: mechanisms and clinical implications. Cancer Investig. 10:525-531.
3. Black, S. S., L. A. Steinohrt, D. C. Bertucci, L. B. Rogers, and E. S. Didier. 1997. Encephalitozoon hellem in budgerigars (Melopsittacus undulatus). Vet. Pathol. 34:189-198.
4. Bornay-Llinares, F. J., A. J. da Silva, H. Moura, D. A. Schwartz, G. S. Visvesvara, N. J. Pieniazek, A. Cruz-Lopez, P. Hernandez-Jauregui, J. Guerrero, and F. J. Enriquez. 1998. Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 178:820-826.
5. Breitenmoser, A. C., A. Mathis, E. Burgi, R. Weber, and P. Deplazes. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology 118:447-453.
6. Canning, E. U., and J. Lom. 1986. The microsporidia of vertebrates. Academic Press, San Diego, Calif.
7. Carlisle, M. S., K. Snowden, J. Gill, M. Jones, P. O'Donoghue, and P. Prociv. 2002. Microsporidiosis in a Gouldian finch (Erythrura [Chloebia] gouldiae). Aust. Vet. J. 80:41-44.
8. Conteas, C. N., O. G. Berlin, C. E. Speck, S. S. Pandhumas, M. J. Lariviere, and C. Fu. 1998. Modification of the clinical course of intestinal microsporidiosis in acquired immunodeficiency syndrome patients by immune status and anti-human immunodeficiency virus therapy. Am. J. Trop. Med. Hyg. 58:555-558.
9. da Silva, A. J., D. A. Schwartz, G. S. Visvesvara, H. de Moura, S. B. Slemenda, and N. J. Pieniazek. 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.
10. Da Silva, A. J., S. B. Slemenda, G. S. Visvesvara, D. A. Schwartz, C. M. Wilcox, S. Wallace, and N. J. Pieniazek. 1997. Detection of Septata intestinalis (microsporidia) Cali et al. 1993 using polymerase chain reaction primers targeting the small subunit ribosomal RNA coding region. Mol. Diagn. 2:47-52.
11. del Aguila, C., F. Izquierdo, R. Navajas, N. J. Pieniazek, G. Miro, A. I. Alonso, A. J. Da Silva, and S. Fenoy. 1999. Enterocytozoon bieneusi in animals: rabbits and dogs as new hosts. J. Eukaryot. Microbiol. 46:8S-9S.
12. del Aguila, C., R. Lopez-Velez, S. Fenoy, C. Turrientes, J. Cobo, R. Navajas, G. S. Visvesvara, G. P. Croppo, A. J. Da Silva, and N. J. Pieniazek. 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.
13. del Aguila, C., R. Navajas, D. Gurbindo, J. T. Ramos, M. J. Mellado, S. Fenoy, M. A. Munoz Fernandez, M. Subirats, J. Ruiz, and N. J. Pieniazek. 1997. Microsporidiosis in HIV-positive children in Madrid (Spain). J. Eukaryot. Microbiol. 44:84S-85S.
14. Dengjel, B., M. Zahler, W. Hermanns, K. Heinritzi, T. Spillmann, A. Thomschke, T. Loscher, R. Gothe, and H. Rinder. 2001. Zoonotic potential of Enterocytozoon bieneusi. J. Clin. Microbiol. 39:4495-4499.
15. Deplazes, P., A. Mathis, R. Baumgartner, I. Tanner, and R. Weber. 1996. Immunologic and molecular characteristics of Encephalitozoon-like microsporidia isolated from humans and rabbits indicate that Encephalitozoon cuniculi is a zoonotic parasite. Clin. Infect. Dis. 22:557-559.
16. Deplazes, P., A. Mathis, C. Muller, and R. Weber. 1996. Molecular epidemiology of Encephalitozoon cuniculi, and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J. Eukaryot. Microbiol. 43:93S.
17. Deplazes, P., A. Mathis, and R. Weber. 2000. Epidemiology and zoonotic aspects of microsporidia of mammals and birds. Contrib. Microbiol. 6:236-260.
18. Didier, E. S., M. E. Stovall, L. C. Green, P. J. Brindley, K. Sestak, and P. J. Didier. 2004. Epidemiology of microsporidiosis: sources and modes of transmission. Vet. Parasitol. 126:145-166.
19. Didier, E. S., G. S. Visvesvara, M. D. Baker, L. B. Rogers, D. C. Bertucci, M. A. De Groote, and C. R. Vossbrinck. 1996. A microsporidian isolated from an AIDS patient corresponds to Encephalitozoon cuniculi III, originally isolated from domestic dogs. J. Clin. Microbiol. 34:2835-2837.
20. Didier, E. S., C. R. Vossbrinck, M. D. Baker, L. B. Rogers, D. C. Bertucci, and J. A. Shadduck. 1995. Identification and characterization of three Encephalitozoon cuniculi strains. Parasitology 111:411-421.
21. Fayer, R., M. Santin, R. Palmer, and X. Li. 2003. Detection of Encephalitozoon hellem in feces of experimentally infected chickens. J. Eukaryot. Microbiol. 50(Suppl.):574-575.
22. Fayer, R., M. Santin, and J. M. Trout. 2003. First detection of microsporidia in dairy calves in North America. Parasitol. Res. 90:383-386.
23. Graczyk, T. K., J. Bosco-Nizeyi, A. J. da Silva, I. N. Moura, N. J. Pieniazek, M. R. Cranfield, and H. D. Lindquist. 2002. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol. Res. 88:926-931.
24. Gray, M. L., M. Puette, and K. S. Latimer. 1998. Microsporidiosis in a young ostrich (Struthio camelus). Avian Dis. 42:832-836.
25. Gumbo, T., I. T. Gangaidzo, S. Sarbah, A. Carville, S. Tzipori, and P. M. Wiest. 2000. Enterocytozoon bieneusi infection in patients without evidence of immunosuppression: two cases from Zimbabwe found to have positive stools by PCR. Ann. Trop. Med. Parasitol. 94:699-702.
26. Harcourt-Brown, F. M., and H. K. Holloway. 2003. Encephalitozoon cuniculi in pet rabbits. Vet. Rec. 152:427-431.
27. Haro, M., C. Del Aguila, S. Fenoy, and N. Henriques-Gil. 2003. Intraspecies genotype variability of the microsporidian parasite Encephalitozoon hellem. J. Clin. Microbiol. 41:4166-4171.
28. Hollister, W. S., E. U. Canning, and C. L. Anderson. 1996. Identification of microsporidia causing human disease. J. Eukaryot. Microbiol. 43:104S-105S.
29. Katinka, M. D., S. Duprat, E. Cornillot, G. Metenier, F. Thomarat, G. Prensier, V. Barbe, E. Peyretaillade, P. Brottier, P. Wincker, F. Delbac, H. El Alaoui, P. Peyret, W. Saurin, M. Gouy, J. Weissenbach, and C. P. Vivares. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450-453.
30. + CTLs are essential for protective immunity against Encephalitozoon cuniculi infection. J. Immunol. 162:6086-6091.
31. Liguory, O., S. Fournier, C. Sarfati, F. Derouin, and J. M. Molina. 2000. Genetic homology among thirteen Encephalitozoon intestinalis isolates obtained from human immunodeficiency virus-infected patients with intestinal microsporidiosis. J. Clin. Microbiol. 38:2389-2391.
32. Lobo, M. L., A. Teles, M. B. da Cunha, J. Henriques, A. M. Lourenco, F. Antunes, and O. Matos, 2003. Microsporidia detection in stools from pets and animals from the zoo in Portugal: a preliminary study. J. Eukaryot. Microbiol. 50(Suppl.):581-582.
33. Lopez-Velez, R., M. C. Turrientes, C. Garron, P. Montilla, R. Navajas, S. Fenoy, and C. del Aguila. 1999. Microsporidiosis in travelers with diarrhea from the tropics. J. Travel Med. 6:223-227.
34. Lores, B., C. del Aguila, and C. Arias. 2002. Enterocytozoon bieneusi (microsporidia) in faecal samples from domestic animals from Galicia. Spain. Mem. Inst. Oswaldo Cruz 97:941-945.
35. Lores, B., I. Lopez-Miragaya, C. Arias, S. Fenoy, J. Torres, and C. del Aguila. 2002. Intestinal microsporidiosis due to Enterocytozoon bieneusi in elderly human immunodeficiency virus-negative patients from Vigo, Spain. Clin. Infect. Dis. 34:918-921.
36. Mathis, A., A. C. Breitenmoser, and P. Deplazes. 1999. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite 6:189-193.
37. Mathis, A., I. Tanner, R. Weber, and P. Deplazes. 1999. Genetic and phenotypic intraspecific variation in the microsporidian Encephalitozoon hellem. Int. J. Parasitol. 29:767-770.
38. Moura, H., J. L. Da Silva, F. C. Sodre, P. Brasil, K. Wallmo, S. Wahlquist, S. Wallace, G. P. Croppo, and G. S. Visvesvara. 1996. Gram-chromotrope: a new technique that enhances detection of microsporidial spores in clinical samples. J. Eukaryot. Microbiol. 43:94S-95S.
39. Muller, A., R. Bialek, A. Kamper, G. Fatkenheuer, B. Salzberger, and C. Franzen. 2001. Detection of microsporidia in travelers with diarrhea. J. Clin. Microbiol. 39:1630-1632.
40. Myers, R. M., L. H. Elleson, and K. Hayashi. 1997. Detection of DNA variation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Negm, A. Y. 2003. Human pathogenic protozoa in bivalves collected from local markets in Alexandria. J. Egypt Soc. Parasitol. 33:991-998.
42. Pulparampil, N., D. Graham, D. Phalen, and K. Snowden. 1998. Encephalitozoon hellem in two eclectus parrots (Eclectus roratus): identification from archival tissues. J. Eukaryot. Microbiol. 45:651-655.
43. Rabodonirina, M., L. Cotte, S. Radenne, E. Besada, and C. Trepo. 2003. Microsporidiosis and transplantation: a retrospective study of 23 cases. J. Eukaryot. Microbiol. 50(Suppl.):583.
44. Reetz, J., H. Rinder, A. Thomschke, H. Manke, M. Schwehs, and A. Bruderek. 2002. First detection of the microsporidium Enterocytozoon bieneusi in non-mammalian hosts (chickens). Int. J. Parasitol. 32:785-787.
45. Reetz, J., M. Wiedemann, A. Aue, U. Wittstatt, A. Ochs, A. Thomschke, H. Manke, M. Schwebs, and H. Rinder. 2004. Disseminated lethal Encephalitozoon cuniculi (genotype III) infections in cotton-top tamarins (Oedipomidas oedipus)-a case report. Parasitol. Int. 53:29-34.
46. Rinder, H., S. Katzwinkel-Wladarsch, A. Thomschke, and T. Loscher. 1998. Strain differentiation in microsporidia. Tokai J. Exp. Clin. Med. 23:433-437.
47. Rinder, H., A. Thomschke, B. Dengjel, R. Gothe, T. Loscher, and M. Zahler. 2000. Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J. Parasitol. 86:185-188.
48. Snowden, K., and K. Logan. 1999. Molecular identification of Encephalitozoon hellem in an ostrich. Avian Dis. 43:779-782.
49. Snowden, K. F., K. Logan, and D. N. Phalen. 2000. Isolation and characterization of an avian isolate of Encephalitozoon hellem. Parasitology 121:9-14.
50. Sulaiman, I. M., R. Fayer, A. A. Lal, J. M. Trout, F. W. Schaefer III, and L. Xiao. 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.
51. Suter, C., A. Mathis, R. Hoop, and P. Deplazes. 1998. Encephalitozoon hellem infection in a yellow-streaked lory (Chalcopsitta scintillata) imported from Indonesia. Vet. Rec. 143:694-695.
52. Thurston-Enriquez, J. A., P. Watt, S. E. Dowd, R. Enriquez, I. L. Pepper, and C. P. Gerba. 2002. Detection of protozoan parasites and microsporidia in irrigation waters used for crop production. J. Food Prot. 65:378-382.
53. Visvesvara, G. S., M. Belloso, H. Moura, A. J. Da Silva, I. N. Moura, G. J. Leitch, D. A. Schwartz, P. Chevez-Barrios, S. Wallace, N. J. Pieniazek, and J. D. Goosey. 1999. Isolation of Nosema algerae from the cornea of an immunocompetent patient. J. Eukaryot. Microbiol. 46:10S.
54. Visvesvara, G. S., G. J. Leitch, A. J. da Silva, G. P. Croppo, H. Moura, S. Wallace, S. B. Slemenda, D. A. Schwartz, D. Moss, R. T. Bryan, et al. 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.
55. Visvesvara, G. S., G. J. Leitch, H. Moura, S. Wallace, R. Weber, and R. T. Bryan. 1991. Culture, electron microscopy, and immunoblot studies on a microsporidian parasite isolated from the urine of a patient with AIDS. J. Protozool. 38:105S-111S.
56. Weber, R., and R. T. Bryan. 1994. Microsporidial infections in immunodeficient and immunocompetent patients. Clin. Infect. Dis. 19:517-521.
57. Weber, R., R. T. Bryan, R. L. Owen, C. M. Wilcox, L. Gorelkin, and G. S. Visvesvara. 1992. Improved light-microscopical detection of microsporidia spores in stool and duodenal aspirates. N. Engl. J. Med. 326:161-166.
58. Weber, R., R. T. Bryan, D. A. Schwartz, and R. L. Owen. 1994. Human microsporidial infections. Clin. Microbiol. Rev. 7:426-461.
59. Weiss, L. M. 2003. Microsporidia 2003: IWOP-8. J. Eukaryot. Microbiol. 50(Suppl.):566-568.
60. Xiao, L., L. Li, H. Moura, I. Sulaiman, A. A. Lal, S. Gatti, M. Scaglia, E. S. Didier, and G. S. Visvesvara. 2001. Genotyping Encephalitozoon hellem isolates by analysis of the polar tube protein gene. J. Clin. Microbiol. 39:2191-2196.
61. Xiao, L., L. Li, G. S. Visvesvara, H. Moura, E. S. Didier, and A. A. Lal. 2001. Genotyping Encephalitozoon cuniculi by multilocus analyses of genes with repetitive sequences. J. Clin. Microbiol. 39:2248-2253.