Microsporidiosis in mammals

Microbes and Infection

Volumn 2, Issue 6, 2000, Pages 709-720

  Didier, Elizabeth S ^a   Didier, Peter J ^a   Snowden, Karen F ^b   Shadduck, John A ^b  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Emerging infection; Microsporidia; Opportunistic infection; Parasite

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; DISEASE TRANSMISSION; HUMAN; MAMMAL; MICROSPORIDA; MICROSPORIDIOSIS; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; REVIEW; ZOONOSIS;

MAMMALIA; MICROSPORIDIA; PROTOZOA;

EID: 0034116881     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1286-4579(00)00354-3     Document Type: Review

References (98)

1. Wittner M. Historic Perspective on the microsporidia: expanding horizons. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;1-6 Am. Soc. Microbiol, Washington, DC.
2. Wright J.H., Craighead E.M. Infectious motor paralysis in young rabbits. J. Exp. M. 40:1922;135-141.
3. Canning E.U., Lom J. The Microsporidia of Vertebrates. 1986;Academic Press, New York.
4. Didier E.S., Snowden K.F., Shadduck J.A. Biology of microsporidian species infecting mammals. Adv. Parasitol. 48:1998;283-320.
5. Snowden K.F., Didier E.S., Orenstein J.M., Shadduck J.A. Animal models of human microsporidial infections. Lab Anim. Sci. 7:1998;589-592.
6. Weber R., Bryan R.T., Schwartz D.A., Owen R.L. Human microsporidial infections. Clin. Microbiol. Rev. 67:1994;426-461.
7. Matsubayashi H., Koike I., Mikata I., Takei H., Hagiwara S. A case of Encephalitozoon-like infection in man. Arch. Pathol. 3:1959;181-187.
8. Schwartz D.A., Bryan R.T. Microsporidial infections: progress in epidemiology and prevention. Scheld W.M, Craig R.M, Hughes J.M. Emerging Infections. 118:1999;73-98 Am. Soc. Microbiol, Washington DC.
9. Biderre C., Mathis A., Deplazes P., Weber R., Metenier G., Vivares C.P. Molecular karyotype diversity in the microsporidian Encephalitozoon cuniculi. Parasitology. 111:1999;439-445.
10. 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. 29:1995;411-421.
11. Mathis A., Tanner I., Weber R., Deplazes P. Genetic and phenotypic intraspecific variation in the microsporidian Encephalitozoon hellem. Int. J. Parasitol. 45:1999;767-770.
12. Pulparampil N., Graham D., Phalen D., Snowden K. Encephalitozoon hellem in two eclectus parrots (Eclectus roratus): identification from archival tissues. J. Eukaryot. Microbiol. 34:1998;651-655.
13. Black S.S., Steinohrt L.A., Bertucci D.C., Rogers L.B., Didier E.S. Encephalitozoon hellem in budgerigars (Melopsittacus undulatus). Vet. Pathol. 178:1997;189-198.
14. Bornay-Llinares F.J., Da Silva A.J., Moura H., et al. Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 110:1998;820-826.
15. 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. 40:1995;277-285.
16. Cali A., Kotler D.P., Orenstein J.M. Septata intestinalis n. g., n. sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients. J. Eukaryot. Microbiol. 83:1993;101-112.
17. Rinder H., Katzwinkel-Wladarsch S., Loscher T. Evidence for the existence of genetically distinct strains of Enterocytozoon bieneusi. Parasitol. Res. 36:1997;670-672.
18. Liguory O., David F., Sarfati C., Derouin F., Molina J.M. Determination of types of Enterocytozoon bieneusi strains isolated from patients with intestinal microsporidiosis. J. Clin. Microbiol. 118:1998;1882-1885.
19. Breitenmoser A.C., Mathis A., Burgi E., Weber R., Deplazes P. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology. 46:1999;447-453.
20. Del Aguila C., Izquierdo F., Navajas R., Pieniazek N.J., Miro G., Alonso A.I., Da Silva A.J., Fenoy S. Enterocytozoon bieneusi in animals: rabbits and dogs as new hosts. J. Eukaryot. Microbiol. 6:1999;8S-9S.
21. Mathis A., Breitenmoser A.C., Deplazes P. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite. 150:1999;189-193.
22. Mansfield K.G., Carville A., Shvetz D., Mackey J., Tzipori S., Lackner A.A. Identification of an Enterocytozoon bieneusi-like microsporidian parasite in simian-immunodeficiency-virus-inoculated macaques with hepatobiliary disease. Am. J. Pathol. 45:1997;1395-1405.
23. Cali A., Takvorian P.M., Lewin S., Rendel M., Sian C.S., Wittner M., Tanowitz H.B., Keohane E., Weiss L.M. Brachiola vesicularum, n. g., n. sp., a new microsporidium associated with AIDS and myositis. J. Eukaryot. Microbiol. 95:1998;240-251.
24. Margileth A.M., Strano A.J., Chandr R., Neafie R., Blum M., Mc Cully R.M. Disseminated nosematosis in an immunologically compromised infant. Arch. Pathol. 16:1973;145-150.
25. Cali A., Takvorian P. Developmental morphology and life cycles of the microsporidia. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;85-128 Am. Soc. Microbiol, Washington, DC.
26. Chupp G.L., Alroy J., Adelman L.S., Breen J.C., Skolnik P.R. Myositis due to Pleistophora (Microsporidia) in a patient with AIDS. Clin. Infect. Dis. 257:1993;15-21.
27. Doby J.M., Jeannes A., Rault B. Thelohania apodemi n. sp., premiere microsporidie du genre Thelohania observee chex un Mammifere. Compt. Rendus Acad. Sci. 45:1963;248-251.
28. Vavra J., Yachnis A.T., Shadduck J.A., Orenstein J.M. Microsporidia of the genus Trachipleistophora-causative agents of human microsporidiosis: description of Trachipleistophora anthropophthera n. sp. (Protozoa: Microsporidia). J. Eukaryot. Microbiol. 106:1998;273-283.
29. Yachnis A.T., Berg J., Martinez-Salazar A., Bender B.S., Diaz L., Rojiani A.M., Eskin T.A., Orenstein J.M. Disseminated microsporidiosis especially infecting the brain, heart, and kidneys. Report of a newly recognized pansporoblastic species in two symptomatic AIDS patients. Am. J. Clin. Pathol. 34:1996;535-543.
30. Field A.S., Marriott D.J., Milliken S.T., Brew B.J., Canning E.U., Kench J.G., Darveniza P., Harkness J.L. Myositis associated with a newly described microsporidian, Trachipleistophora hominis, in a patient with AIDS. J. Clin. Microbiol. 42:1996;2803-2811.
31. Silveira H., Canning E.U. Vittaforma corneae n. comb. for the human microsporidium Nosema corneum Shadduck, Meccoli, Davis & Font, 1990, based on its ultrastructure in the liver of experimentally infected athymic mice. J. Eukaryot. Microbiol. 162:1995;158-165.
32. Shadduck J.A., Meccoli R.A., Davis R., Font R.L. Isolation of a microsporidian from a human patient. J. Infect. Dis. 73:1990;773-776.
33. Vavra J., Larsson R. Structure of the microsporidia. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;7-84 Am. Soc. Microbiol, Washington, DC.
34. Cavalier-Smith T. A revised six-kingdom system of life. Biol. Rev. Camb. Philos. Soc. 326:1998;203-266.
35. Vossbrinck C.R., Maddox J.V., Friedman S., Debrunner-Vossbrinck B.A., Woese C.R. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature. 5:1987;411-414.
36. Weiss L., Vossbrinck C. Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;129-171 Am. Soc. Microbiol, Washington, DC.
37. Edlind T.D., Li J., Visvesvara G.S., Vodkin M.H., Mc Laughlin G.L., Katiyar S.K. Phylogenetic analysis of beta-tubulin sequences from amitochondrial protozoa. Mol. Phylogenet. Evol. 96:1996;359-367.
38. Hirt R.P., Logsdon J.M. Jr, Healy B., et al. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad. Sci. USA. 46:1999;580-585.
39. Germot A., Philippe H. Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family. J. Eukaryot. Microbiol. 7:1999;116-124.
40. Hirt R.P., Healy B., Vossbrinck C.R., Canning E.U., Embley T.M. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 87:1997;995-998.
41. Germot A., Philippe H., Le Guyader H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial- type HSP70 in Nosema locustae. Mol. Biochem. Parasitol. 8:1997;159-168.
42. Embley T.M., Hirt R.P. Early branching eukaryotes? Curr. Opin. Genet. Dev. 3:1998;624-629.
43. Canning E.U., Hollister W.S. Human infections with microsporidia. Rev. Med. Microbiol. 117:1992;35-42.
44. Shadduck J.A., Orenstein J.M. Comparative pathology of microsporidiosis. Arch. Pathol. Lab M. 32:1993;1215-1219.
45. Desportes I., Le Charpentier Y., Galian A., Bernard F., Cochand-Priollet B., Lavergne A., Ravisse P., Modigliani R. Occurrence of a new microsporidan: Enterocytozoon bieneusi n. g., n. sp., in the enterocytes of a human patient with AIDS. J. Protozool. 37:1985;250-254.
46. Cali A., Owen R.L. Intracellular development of Enterocytozoon, a unique microsporidian found in the intestine of AIDS patients. J. Protozool. 40:1990;145-155.
47. Kotler D.P., Orenstein J.M. Clinical syndromes associated with microsporidiosis. Adv. Parasitol. 45:1998;321-349.
48. Kotler D., Orenstein J.M. Clinical syndromes associated with microsporidiosis. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;258-292 Am. Soc. Microbiol, Washington, DC.
49. Koudela B., Didier E.S., Rogers L.B., Modry D., Kucerova S. Intestinal microsporidiosis in African skink Mabuya perrotetii. Folia Parasitol. (Praha). 23:1998;149-155.
50. Orenstein J.M., Tenner M., Cali A., Kotler D.P. A microsporidian previously undescribed in humans, infecting enterocytes and macrophages, and associated with diarrhea in an acquired immunodeficiency syndrome patient. Hum. Pathol. 89:1992;722-728.
51. Bryan R.T., Schwartz D.A. Epidemiology of microspridiosis. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;502-516 Am. Soc. Microbiol, Washington, DC.
52. Van Gool T., Luderhoff E., Nathoo K.J., Kiire C.F., Dankert J., Mason P.R. High prevalence of Enterocytozoon bieneusi infections among HIV- positive individuals with persistent diarrhoea in Harare, Zimbabwe. Trans. R. Soc. Trop. Med. Hyg. 67:1995;478-480.
53. Gumbo T., Hobbs R.E., Carlyn C., Hall G., Isada C.M. Microsporidia infection in transplant patients. Transplantation. 16:1999;482-484.
54. Hautvast J.L., Tolboom J.J., Derks T.J., Beckers P., Sauerwein R.W. Asymptomatic intestinal microsporidiosis in a human immunodeficiency virus-seronegative, immunocompetent Zambian child. Pediatr. Infect. Dis. J. 92:1997;415-416.
55. Desportes-Livage I., Doumbo O., Pichard E., Hilmarsdottir I., Traore H.A., Maiga I.I., El Fakhry Y., Dolo A. Microsporidiosis in HIV-seronegative patients in Mali. Trans. R. Soc. Trop. Med. Hyg. 24:1998;423-424.
56. Bryan R.T., Weber R., Schwartz D.A. Microsporidiosis in patients who are not infected with human immunodeficiency virus. Clin. Infect. Dis. 26:1997;534-535.
57. Enriquez F.J., Taren D., Cruz-Lopez A., Muramoto M., Palting J.D., Cruz P. Prevalence of intestinal encephalitozoonosis in Mexico. Clin. Infect. Dis. 102 Pt 1:1998;1227-1229.
58. Hollister W.S., Canning E.U., Willcox A. Evidence for widespread occurrence of antibodies to Encephalitozoon cuniculi (Microspora) in man provided by ELISA and other serological tests. Parasitology. 12:1991;33-43.
59. Franzen C., Muller A. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin. Microbiol. Rev. 175:1999;243-285.
60. Didier E.S., Bessinger G.T. Host-parasite relationships in microsporidiosis: animal models and immunology. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;225-257 Am. Soc. Microbiol, Washington, DC.
61. Van Gool T., Vetter J.C., Weinmayr B., Van Dam A., Derouin F., Dankert J. High seroprevalence ofEncephalitozoon species in immunocompetent subjects. J. Infect. Dis. 7:1997;1020-1024.
62. Friedberg D.N., Ritterband D.C. Ocular microsporidiosis. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;293-314 Am. Soc. Microbiol, Washington, DC.
63. Snowden K.F., Shadduck J.A. Microsporidia of higher vertebrates. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;393-419 Am. Soc. Microbiol, Washington, DC.
64. Rastrelli P.D., Didier E.S., Yee R.W. Microsporidial keratitis. Ophthalmol. Clin. N. Am. 58:1994;617-633.
65. Conteas C.N., Berlin O.G., Lariviere M.J., Pandhumas S.S., Speck C.E., Porschen R., Nakaya T. Examination of the prevalence and seasonal variation of intestinal microsporidiosis in the stools of persons with chronic diarrhea and human immunodeficiency virus infection. Am. J. Trop. Med. Hyg. 34:1998;559-561.
66. Franzen C., Muller A. Cryptosporidia and microsporidia - waterborne diseases in the immunocompromised host. Diagn. Microbiol. Infect. Dis. 35:1999;245-262.
67. Dowd S.E., Gerba C.P., Kamper M., Pepper I.L. Evaluation of methodologies including immunofluorescent assay (IFA) and the polymerase chain reaction (PCR) for detection of human pathogenic microsporidia in water. J. Microbiol. Methods. 37:1999;43-52.
68. Dascomb K., Clark R., Aberg J., Pulvirenti J., Hewitt R.G., Kissinger P., Didier E.S. Natural history of intestinal microsporidiosis among patients infected with human immunodeficiency virus. J. Clin. Microbiol. 94:1999;3421-3422.
69. Hollister W.S., Canning E.U. An enzyme-linked immunosorbent assay (ELISA) for detection of antibodies toEncephalitozoon cuniculi and its use in determination of infections in man. Parasitology. 77:1987;209-219.
70. Orenstein J.M. Microsporidiosis in the acquired immunodeficiency syndrome. J. Parasitol. 35:1991;843-864.
71. Weber R., Schwartz D.A., Deplazes P. Laboratory diagnosis of microsporidiosis. Wittner M, Weiss L. The Microsporidia and Microsporidiosis. 1999;315-362 Am. Soc. Microbiol, Washington, DC.
72. Ignatius R., Henschel S., Liesenfeld O., Mansmann U., Schmidt W., Koppe S., Schneider T., Heise W., Futh U., Riecken E.O., Hahn H., Ullrich R. Comparative evaluation of modified trichrome and Uvitex 2B stains for detection of low numbers of microsporidial spores in stool specimens. J. Clin. Microbiol. 33:1997;2266-2269.
73. Didier E.S., Orenstein J.M., Aldras A., Bertucci D., Rogers L.B., Janney F.A. Comparison of three staining methods for detecting microsporidia in fluids. J. Clin. Microbiol. 36:1995;3138-3145.
74. Rinder H., Janitschke K., Aspock H., Da Silva A.J., Deplazes P., Fedorko D.P., Franzen C., Futh U., Hunger F., Lehmacher A., Meyer C.G., Molina J.M., Sandfort J., Weber R., Loscher T. Blinded, externally controlled multicenter evaluation of light microscopy and PCR for detection of microsporidia in stool specimens. The Diagnostic Multicenter Study Group on Microsporidia. J. Clin. Microbiol. 40:1998;1814-1818.
75. Field A.S., Marriott D.J., Hing M.C. The Warthin-Starry stain in the diagnosis of small intestinal microsporidiosis in HIV-infected patients. Folia Parasitol. (Praha). 17:1993;261-266.
76. Lujan H.D., Conrad J.T., Clark C.G., Touz M.C., Delbac F., Vivares C.P., Nash T.E. Detection of microsporidia spore-specific antigens by monoclonal antibodies. Hybridoma. 35:1998;237-243.
77. Enriquez F.J., Ditrich O., Palting J.D., Smith K. Simple diagnosis of Encephalitozoon sp. microsporidial infections by using a panspecific antiexospore monoclonal antibody. J. Clin. Microbiol. 34:1997;724-729.
78. Beckers P.J., Derks G.J., Gool T., Rietveld F.J., Sauerwein R.W. Encephalocytozoon intestinalis-specific monoclonal antibodies for laboratory diagnosis of microsporidiosis. J. Clin. Microbiol. 37:1996;282-285.
79. Accoceberry I., Thellier M., Desportes-Livage I., Achbarou A., Biligui S., Danis M., Datry A. Production of Monoclonal Antibodies Directed against the Microsporidium Enterocytozoon bieneusi. J. Clin. Microbiol. 2:1999;4107-4112.
80. Fedorko D.P., Hijazi Y.M. Application of molecular techniques to the diagnosis of microsporidial infection. Emerg. Infect. Dis. 112:1996;183-191.
81. Sharpstone D., Rowbottom A., Francis N., Tovey G., Ellis D., Barrett M., Gazzard B. Thalidomide: a novel therapy for microsporidiosis. Gastroenterology. 162:1997;1823-1829.
82. Khan I.A., Schwartzman J.D., Kasper L.H., Moretto M. CD8+ CTLs are essential for protective immunity against Encephalitozoon cuniculi infection. J. Immunol. 40:1999;6086-6091.
83. Koudela B., Vitovec J., Kucerova Z., Ditrich O., Travnicek J. The severe combined immunodeficient mouse as a model for Encephalitozoon cuniculi microsporidiosis. Folia Parasitol. (Praha). 40:1993;279-286.
84. Schmidt E.C., Shadduck J.A. Murine encephalitozoonosis model for studying the host-parasite relationship of a chronic infection. Infect. Immun. 133:1983;936-942.
85. Schmidt E.C., Shadduck J.A. Mechanisms of resistance to the intracellular protozoan Encephalitozoon cuniculi in mice. J. Immunol. 17:1984;2712-2719.
86. Didier E.S. Reactive nitrogen intermediates implicated in the inhibition of Encephalitozoon cuniculi (phylum microspora) replication in murine peritoneal macrophages. Parasite Immunol. 67:1995;405-412.
87. Khan I.A., Moretto M. Role of gamma interferon in cellular immune response against murine Encephalitozoon cuniculi infection. Infect. Immun. 18:1999;1887-1893.
88. Achbarou A., Ombrouck C., Gneragbe T., Charlotte F., Renia L., Desportes-Livage I., Mazier D. Experimental model for human intestinal microsporidiosis in interferon gamma receptor knockout mice infected by Encephalitozoon intestinalis. Parasite Immunol. 117:1996;387-392.
89. Enriquez F.J., Wagner G., Fragoso M., Ditrich O. Effects of an anti-exospore monoclonal antibody on microsporidial development in vitro. Parasitology. 169:1998;515-520.
90. 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. 6:1994;178-183.
91. Blanshard C., Ellis D.S., Tovey D.G., Dowell S., Gazzard B.G. Treatment of intestinal microsporidiosis with albendazole in patients with AIDS. AIDS. 13:1992;311-313.
92. Gumbo T., Sarbah S., Gangaidzo I.T., Ortega Y., Sterling C.R., Carville A., Tzipori S., Wiest P.M. Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe. AIDS. 11:1999;819-821.
93. Molina J.M., Goguel J., Sarfati C., Chastang C., Desportes-Livage I., Michiels J.F., Maslo C., Katlama C., Cotte L., Leport C., Raffi F., Derouin F., Modai J. Potential efficacy of fumagillin in intestinal microsporidiosis due to Enterocytozoon bieneusi in patients with HIV infection: results of a drug screening study. The French Microsporidiosis Study Group. AIDS. 177:1997;1603-1610.
94. Coyle C., Kent M., Tanowitz H.B., Wittner M., Weiss L.M. TNP-470 is an effective antimicrosporidial agent. J. Infect. Dis. 41:1998;515-518.
95. Didier E.S. Effects of albendazole, fumagillin, and TNP-470 on microsporidial replication in vitro. Antimicrob. Agents Chemother. 58:1997;1541-1546.
96. Conteas C.N., Berlin O.G., Speck C.E., Pandhumas S.S., Lariviere M.J., Fu C. 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. 351:1998;555-558.
97. Carr A., Marriott D., Field A., Vasak E., Cooper D.A. Treatment of HIV-1-associated microsporidiosis and cryptosporidiosis with combination antiretroviral therapy. Lancet. 11:1998;256-261.
98. Goguel J., Katlama C., Sarfati C., Maslo C., Leport C., Molina J.M. Remission of AIDS-associated intestinal microsporidiosis with highly active antiretroviral therapy. AIDS. 1997;1658-1659.