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. 1997 Jul;35(7):1862–1866. doi: 10.1128/jcm.35.7.1862-1866.1997

Identification of Enterocytozoon bieneusi spores in respiratory samples from an AIDS patient with a 2-year history of intestinal microsporidiosis.

C del Aguila 1, R Lopez-Velez 1, S Fenoy 1, C Turrientes 1, J Cobo 1, R Navajas 1, G S Visvesvara 1, G P Croppo 1, A J Da Silva 1, N J Pieniazek 1
PMCID: PMC229858  PMID: 9196210

Abstract

Enterocytozoon bieneusi, a microsporidian parasite, has been recognized since 1985 as an agent of intestinal microsporidiosis leading to malabsorption syndrome, diarrhea, and weight loss in AIDS patients. Recently, however, we have identified E. bieneusi spores in the sputum, bronchoalveolar lavage, and stool samples of an AIDS patient with a 2-year history of intestinal microsporidiosis. The spores were characterized by Weber's chromotrope-based staining, immunofluorescence tests, and PCR. No microsporidia were detected in urine samples by the same techniques. PCR was performed with DNAs purified from specimens with E. bieneusi-, Encephalitozoon cuniculi-, Encephalitozoon hellem-, and Encephalitozoon (Septata) intestinalis-specific primers. Treatment with albendazole and loperamide resulted in an improvement of intestinal symptoms, without eradication of the parasite. To our knowledge, this is the second report of the identification of E. bieneusi spores in respiratory and enteric samples obtained from an AIDS patient. Although no pulmonary pathology could be established in either of these cases, it is now clear that E. bieneusi is capable of colonizing the respiratory tract and it is suggested that investigators should be aware of the possibility of finding E. bieneusi spores in respiratory secretions.

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Selected References

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  1. Aldras A. M., Orenstein J. M., Kotler D. P., Shadduck J. A., Didier E. S. Detection of microsporidia by indirect immunofluorescence antibody test using polyclonal and monoclonal antibodies. J Clin Microbiol. 1994 Mar;32(3):608–612. doi: 10.1128/jcm.32.3.608-612.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blanshard C., Ellis D. S., Tovey D. G., Dowell S., Gazzard B. G. Treatment of intestinal microsporidiosis with albendazole in patients with AIDS. AIDS. 1992 Mar;6(3):311–313. doi: 10.1097/00002030-199203000-00009. [DOI] [PubMed] [Google Scholar]
  3. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 51-1993. A 36-year-old man with AIDS, increase in chronic diarrhea, and intermittent fever and chills. N Engl J Med. 1993 Dec 23;329(26):1946–1954. doi: 10.1056/NEJM199312233292609. [DOI] [PubMed] [Google Scholar]
  4. Cox J. C., Hamilton R. C., Attwood H. D. An investigation of the route and progression of Encephalitozoon cuniculi infection in adult rabbits. J Protozool. 1979 May;26(2):260–265. doi: 10.1111/j.1550-7408.1979.tb02776.x. [DOI] [PubMed] [Google Scholar]
  5. Da Silva AJ, Slemenda SB, Visvesvara GS, Schwartz DA, Wilcox CM, Wallace S, Pieniazek NJ. Detection of Septata intestinalis (Microsporidia) Cali et al. 1993 Using Polymerase Chain Reaction Primers Targeting the Small Submit Subunit Ribosomal RNA Coding Region. Mol Diagn. 1997 Mar;2(1):47–52. doi: 10.1054/MODI00200047. [DOI] [PubMed] [Google Scholar]
  6. De Groote M. A., Visvesvara G., Wilson M. L., Pieniazek N. J., Slemenda S. B., daSilva A. J., Leitch G. J., Bryan R. T., Reves R. Polymerase chain reaction and culture confirmation of disseminated Encephalitozoon cuniculi in a patient with AIDS: successful therapy with albendazole. J Infect Dis. 1995 May;171(5):1375–1378. doi: 10.1093/infdis/171.5.1375. [DOI] [PubMed] [Google Scholar]
  7. Didier E. S., Rogers L. B., Brush A. D., Wong S., Traina-Dorge V., Bertucci D. Diagnosis of disseminated microsporidian Encephalitozoon hellem infection by PCR-Southern analysis and successful treatment with albendazole and fumagillin. J Clin Microbiol. 1996 Apr;34(4):947–952. doi: 10.1128/jcm.34.4.947-952.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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. Characterization of Encephalitozoon (Septata) intestinalis isolates cultured from nasal mucosa and bronchoalveolar lavage fluids of two AIDS patients. J Eukaryot Microbiol. 1996 Jan-Feb;43(1):34–43. doi: 10.1111/j.1550-7408.1996.tb02470.x. [DOI] [PubMed] [Google Scholar]
  9. Didier E. S., Vossbrinck C. R., Baker M. D., Rogers L. B., Bertucci D. C., Shadduck J. A. Identification and characterization of three Encephalitozoon cuniculi strains. Parasitology. 1995 Nov;111(Pt 4):411–421. doi: 10.1017/s0031182000065914. [DOI] [PubMed] [Google Scholar]
  10. Dieterich D. T., Lew E. A., Kotler D. P., Poles M. A., Orenstein J. M. Treatment with albendazole for intestinal disease due to Enterocytozoon bieneusi in patients with AIDS. J Infect Dis. 1994 Jan;169(1):178–183. doi: 10.1093/infdis/169.1.178. [DOI] [PubMed] [Google Scholar]
  11. Dore G. J., Marriott D. J., Hing M. C., Harkness J. L., Field A. S. Disseminated microsporidiosis due to Septata intestinalis in nine patients infected with the human immunodeficiency virus: response to therapy with albendazole. Clin Infect Dis. 1995 Jul;21(1):70–76. doi: 10.1093/clinids/21.1.70. [DOI] [PubMed] [Google Scholar]
  12. Hartskeerl R. A., Schuitema A. R., van Gool T., Terpstra W. J. Genetic evidence for the occurrence of extra-intestinal Enterocytozoon bieneusi infections. Nucleic Acids Res. 1993 Aug 25;21(17):4150–4150. doi: 10.1093/nar/21.17.4150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hartskeerl R. A., Van Gool T., Schuitema A. R., Didier E. S., Terpstra W. J. Genetic and immunological characterization of the microsporidian Septata intestinalis Cali, Kotler and Orenstein, 1993: reclassification to Encephalitozoon intestinalis. Parasitology. 1995 Apr;110(Pt 3):277–285. doi: 10.1017/s0031182000080860. [DOI] [PubMed] [Google Scholar]
  14. Lacey C. J., Clarke A. M., Fraser P., Metcalfe T., Bonsor G., Curry A. Chronic microsporidian infection of the nasal mucosae, sinuses and conjunctivae in HIV disease. Genitourin Med. 1992 Jun;68(3):179–181. doi: 10.1136/sti.68.3.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MATSUBAYASHI H., KOIKE T., MIKATA I., TAKEI H., HAGIWARA S. A case of Encephalitozoon-like body infection in man. AMA Arch Pathol. 1959 Feb;67(2):181–187. [PubMed] [Google Scholar]
  16. Molina J. M., Oksenhendler E., Beauvais B., Sarfati C., Jaccard A., Derouin F., Modaï J. Disseminated microsporidiosis due to Septata intestinalis in patients with AIDS: clinical features and response to albendazole therapy. J Infect Dis. 1995 Jan;171(1):245–249. doi: 10.1093/infdis/171.1.245. [DOI] [PubMed] [Google Scholar]
  17. Orenstein J. M. Microsporidiosis in the acquired immunodeficiency syndrome. J Parasitol. 1991 Dec;77(6):843–864. [PubMed] [Google Scholar]
  18. Schwartz D. A., Visvesvara G. S., Diesenhouse M. C., Weber R., Font R. L., Wilson L. A., Corrent G., Serdarevic O. N., Rosberger D. F., Keenen P. C. Pathologic features and immunofluorescent antibody demonstration of ocular microsporidiosis (Encephalitozoon hellem) in seven patients with acquired immunodeficiency syndrome. Am J Ophthalmol. 1993 Mar 15;115(3):285–292. doi: 10.1016/s0002-9394(14)73577-9. [DOI] [PubMed] [Google Scholar]
  19. Velásquez J. N., Carnevale S., Guarnera E. A., Labbé J. H., Chertcoff A., Cabrera M. G., Rodríguez M. I. Detection of the microsporidian parasite Enterocytozoon bieneusi in specimens from patients with AIDS by PCR. J Clin Microbiol. 1996 Dec;34(12):3230–3232. doi: 10.1128/jcm.34.12.3230-3232.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Visvesvara G. S., Leitch G. J., Moura H., Wallace S., Weber R., Bryan R. T. Culture, electron microscopy, and immunoblot studies on a microsporidian parasite isolated from the urine of a patient with AIDS. J Protozool. 1991 Nov-Dec;38(6):105S–111S. [PubMed] [Google Scholar]
  21. 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. 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. 1994 Nov;32(11):2760–2768. doi: 10.1128/jcm.32.11.2760-2768.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Visvesvara G. S., da Silva A. J., Croppo G. P., Pieniazek N. J., Leitch G. J., Ferguson D., de Moura H., Wallace S., Slemenda S. B., Tyrrell I. In vitro culture and serologic and molecular identification of Septata intestinalis isolated from urine of a patient with AIDS. J Clin Microbiol. 1995 Apr;33(4):930–936. doi: 10.1128/jcm.33.4.930-936.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vossbrinck C. R., Baker M. D., Didier E. S., Debrunner-Vossbrinck B. A., Shadduck J. A. Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. J Eukaryot Microbiol. 1993 May-Jun;40(3):354–362. doi: 10.1111/j.1550-7408.1993.tb04928.x. [DOI] [PubMed] [Google Scholar]
  24. Weber R., Bryan R. T., Owen R. L., Wilcox C. M., Gorelkin L., Visvesvara G. S. Improved light-microscopical detection of microsporidia spores in stool and duodenal aspirates. The Enteric Opportunistic Infections Working Group. N Engl J Med. 1992 Jan 16;326(3):161–166. doi: 10.1056/NEJM199201163260304. [DOI] [PubMed] [Google Scholar]
  25. Weber R., Bryan R. T., Schwartz D. A., Owen R. L. Human microsporidial infections. Clin Microbiol Rev. 1994 Oct;7(4):426–461. doi: 10.1128/cmr.7.4.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Weber R., Kuster H., Keller R., Bächi T., Spycher M. A., Briner J., Russi E., Lüthy R. Pulmonary and intestinal microsporidiosis in a patient with the acquired immunodeficiency syndrome. Am Rev Respir Dis. 1992 Dec;146(6):1603–1605. doi: 10.1164/ajrccm/146.6.1603. [DOI] [PubMed] [Google Scholar]
  27. Weber R., Sauer B., Spycher M. A., Deplazes P., Keller R., Ammann R., Briner J., Lüthy R. Detection of Septata intestinalis in stool specimens and coprodiagnostic monitoring of successful treatment with albendazole. Clin Infect Dis. 1994 Aug;19(2):342–345. doi: 10.1093/clinids/19.2.342. [DOI] [PubMed] [Google Scholar]
  28. Zhu X., Wittner M., Tanowitz H. B., Cali A., Weiss L. M. Nucleotide sequence of the small ribosomal RNA of Encephalitozoon cuniculi. Nucleic Acids Res. 1993 Mar 11;21(5):1315–1315. doi: 10.1093/nar/21.5.1315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zhu X., Wittner M., Tanowitz H. B., Kotler D., Cali A., Weiss L. M. Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. J Infect Dis. 1993 Dec;168(6):1570–1575. doi: 10.1093/infdis/168.6.1570. [DOI] [PubMed] [Google Scholar]
  30. da Silva A. J., Schwartz D. A., Visvesvara G. S., de Moura H., Slemenda S. B., Pieniazek N. J. Sensitive PCR diagnosis of Infections by Enterocytozoon bieneusi (microsporidia) using primers based on the region coding for small-subunit rRNA. J Clin Microbiol. 1996 Apr;34(4):986–987. doi: 10.1128/jcm.34.4.986-987.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]

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