Microsporidiosis: An Emerging and Opportunistic Disease in Humans and Animals
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Published:
Feb 12, 2018
Keywords:
Microsporidiosis Microsporidia Emerging disease Opportunistic disease
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Abstract
Microsporidiosis is an emerging and opportunistic disease in human and a wide range of animals. The disease is caused by Microsporidia, the obligate intracellular parasite which were reclassified from protozoa to fungi. Enterocytozoon bieneusi and Encephalitozoon intestinalisare the most common species cause disease in immunocompromised individuals; however, they were identified in many animals from various areas including Thailand. This review article provides concept knowledge of the disease in humans and animals, the disease transmission, diagnosis and treatment.
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Review Article
References
Anane, S. and Attouchi, H. 2010. Microsporidiosis: epidemiology, clinical data and therapy. Gastroenterol. Clin. Biol. 34(8-9): 450-464.
Anane, S., Kaouech, E., Belhadj, S., Abdelmalek, R., Ammari, L., Ben Othman, T., Bejaoui, M., Ben Chaabane, T., Kallel, K. and Chaker, E. 2011. Identification of Enterocytozoon bieneusi by PCR in stools of Tunisian immunocompromised patients. Pathol. Biol (Paris). 59(4): 234-239.
Bornay-Llinares, F.J., da Silva, A.J., Moura, H., Schwartz, D.A., Visvesvara, G.S., Pieniazek, N.J., Cruz-López, A., Hernández-Jaúregui, P., Guerrero, J. and Enriquez, F.J. 1998. Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 178(3): 820-826.
Breitenmoser, A.C., Mathis, A., Bürgi, E., Weber, R. and Deplazes, P. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology. 118 (Pt 5): 447-453.
Buckholt, M.A., Lee, J.H. and Tzipori, S. 2002. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl. Environ. Microbiol. 68(5): 2595-2599.
Cox, J.C., Hamilton, R.C. and Attwood, H.D. 1979. An investigation of the route and progression of Encephalitozoon cuniculi infection in adult rabbits. J. Protozool. 26(2): 260-265.
Dascomb, K., Frazer, T., Clark, R.A., Kissinger, P. and Didier, E. 2000. Microsporidiosis and HIV. J. Acquir. Immune. Defic. Syndr. 24(3): 290-292.
Graczyk, T.K., Bosco-Nizeyi, J., da Silva, A.J., Moura, I.N., Pieniazek, N.J., Cranfield, M.R. and Lindquist, H.D. 2002. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol Res. 88(10): 926-931.
Hutin, Y.J., Sombardier, M.N., Liguory, O., Sarfati, C., Derouin, F., Modaï, J. and Molina, J.M. 1998. Risk factors for intestinal microsporidiosis in patients with human immunodeficiency virus infection: a case-control study. J. Infect. Dis. 178(3): 904-907.
Jass, A., Matiasek, K., Henke, J., Küchenhoff, H., Hartmann, K. and Fischer, A. 2008. Analysis of cerebrospinal fluid in healthy rabbits and rabbits with clinically suspected encephalito-zoonosis. Vet. Rec. 162(19): 618-622.
Kakrania, R., Joseph, J., Vaddavalli, P.K., Gangopadhyay, N. and Sharma, S. 2006. Microsporidia keratoconjunctivitis in a corneal graft. Eye (Lond). 20(11): 1314-1315.
Künzel, F. and Joachim, A. 2010. Encephalitozoonosis in rabbits. Parasitol. Res. 106(2):299-309.
Leelayoova, S., Piyaraj, P., Subrungruang, I., Pagornrat, W., Naaglor, T., Phumklan, S., Taamasri, P., Suwanasri, J. and Mungthin, M. 2009. Genotypic characterization of Enterocytozoon bieneusi in specimens from pigs and humans in a pig farm community in Central Thailand. J. Clin. Microbiol. 47(5): 1572-1574.
Li, X., Palmer, R., Trout, J.M. and Fayer R. 2003. Infectivity of microsporidia spores storedin water at environmental temperatures. J. Parasitol. 89(1):185-188.
Mathis, A., Weber, R. and Deplazes, P. 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 18(3): 423-445.
Mathis, A., Michel, M., Kuster, H., Müller, C., Weber, R. and Deplazes, P. 1997. Two Encephalitozoon cuniculi strains of human origin are infectious to rabbits. Parasitol. 114 (Pt 1):29-35.
McInnes, E.F. and Stewart, C.G. 1991. The pathology of subclinical infection of Encephalitozoon cuniculi in canine dams producing pups with overt encephalitozoonosis. J. S. Afr. Vet. Assoc. 62(2):51-4.
Mori, H., Mahittikorn, A., Thammasonthijarern, N., Chaisiri, K., Rojekittikhun, W. and Sukthana, Y. 2013a. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Vet. Parasitol. 197(3-4): 696-701.
Mori, H., Mahittikorn, A., Watthanakulpanich, D., Komalamisra, C. and Sukthana, Y. 2013b. Zoonotic potential of Enterocytozoon bieneusi among children in rural communities in Thailand. Parasite. 20:14.
Pan, Y., Wang, S., Liu, X., Li, R., Sun, Y. and Gadahi, J.A. 2015. Seroprevalence of Encephalitozoon cuniculi in Humans and Rabbits in China. Iran. J. Parasitol. 10(2): 290-295.
Prasertbun, R., Mori, H., Pintong, A.R,, Sanyanusin, S., Popruk, S., Komalamisra, C., Changbunjong, T., Buddhirongawatr, R., Sukthana, Y. and Mahittikorn, A. 2017. Zoonotic potential of Enterocytozoon genotypes in humans and pigs in Thailand. Vet. Parasitol. 233:73-79.
Pulparampil, N., Graham, D., Phalen, D. and Snowden, K. 1998. Encephalitozoon hellem in two eclectus parrots (Eclectus roratus): identification from archival tissues. J. Eukaryot. Microbiol. 45(6): 651-655.
Rinder, H. 2004. Transmission of microsporidia to humans: Water-borne, food-borne, air-borne, zoonotic, or anthroponotic? Southeast. Asian. J. Trop. Med. Public. Health. 35 (Suppl1): 54-57
Saigal, K., Sharma, A., Sehgal, R., Sharma, P., Malla, N. and Khurana, S. 2013. Intestinal microsporidiosis in India: a two year study. Parasitol. Int. 62(1): 53-56.
Santín, M. and Fayer, R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res. Vet. Sci. 90(3): 363-371
Shadduck, J.A. and Polley, M.B. 1978. Some factors influencing the in vitro infectivity and replication of Encephalitozoon cuniculi. J. Protozool. 25(4): 491-496.
Snowden, K.F., Logan, K. and Phalen, D.N. 2000. Isolation and characterization of an avian isolate of Encephalitozoon hellem. Parasitol. 121 (Pt 1): 9-14.
Snowden, K.F., Didier, E.S., Orenstein, J.M. and Shadduck, J.A. 1998. Animal models of human microsporidial infections. Lab. Anim. Sci. 48(6): 589-592.
Sulaiman, I.M., Bern, C., Gilman, R., Cama, V., Kawai, V., Vargas, D., Ticona, E., Vivar, A. and Xiao, L. 2003. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. J. Eukaryot. Microbiol. 50 Suppl: 591-596.
Viriyavejakul, P., Nintasen, R., Punsawad, C., Chaisri, U., Punpoowong, B. and Riganti, M. 2009. High prevalence of Microsporidium infection in HIV-infected patients. Southeast Asian J Trop Med Public Health. 40(2): 223-228.
Waller, T. 1979. Sensitivity of Encephalitozoon cuniculi to various temperatures, disinfectants and drugs. Lab. Anim. 13(3): 227-230.
Wanachiwanawin, D., Manatsathit, S., Lertlaituan, P., Thakerngpol, K. and Suwanagool, P. 1998. Intestinal microsporidiosis in HIV infected patients with chronic diarrhea in Thailand. Southeast. Asian. J. Trop. Med. Public. Health. 29(4): 767-771.
Watson, D. R. A., Asmuth, D. and Wanke, C.A. 1996. Environmental risk factors for acquisition of microsporidia in HIV-infected persons. In Proceedings of the 34th Annual Meeting of the Infectious Diseases Society of America, New Orleans, La., p. 67. Infectious Diseases Society of America, New Orleans, La.
Weber, R., Kuster, H., Visvesvara, G.S., Bryan, R.T., Schwartz, D.A. and Lüthy, R. 1993. Disseminated microsporidiosis due to Encephalitozoon hellem: pulmonary colonization, microhematuria, and mild conjunctivitis in a patient with AIDS. Clin. Infect. Dis. 17(3): 415-419.
Wichro, E., Hoelzl, D., Krause, R., Bertha, G., Reinthaler, F. and Wenisch, C. 2005. Microsporidiosis in travel-associated chronic diarrhea in immune-competent patients. Am. J. Trop. Med. Hyg. 73(2): 285-287.
Wumba, R., Longo-Mbenza, B., Menotti, J., Mandina, M., Kintoki, F., Situakibanza, N.H., Kakicha, M.K., Zanga, J., Mbanzulu-Makola, K., Nseka, T., Mukendi, J.P., Kendjo, E., Sala, J. and Thellier, M. 2012. Epidemiology, clinical, immune, and molecular profiles of microsporidiosis and cryptosporidiosis among HIV/AIDS patients. Int. J. Gen. Med. 5: 603-611.
Anane, S., Kaouech, E., Belhadj, S., Abdelmalek, R., Ammari, L., Ben Othman, T., Bejaoui, M., Ben Chaabane, T., Kallel, K. and Chaker, E. 2011. Identification of Enterocytozoon bieneusi by PCR in stools of Tunisian immunocompromised patients. Pathol. Biol (Paris). 59(4): 234-239.
Bornay-Llinares, F.J., da Silva, A.J., Moura, H., Schwartz, D.A., Visvesvara, G.S., Pieniazek, N.J., Cruz-López, A., Hernández-Jaúregui, P., Guerrero, J. and Enriquez, F.J. 1998. Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 178(3): 820-826.
Breitenmoser, A.C., Mathis, A., Bürgi, E., Weber, R. and Deplazes, P. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology. 118 (Pt 5): 447-453.
Buckholt, M.A., Lee, J.H. and Tzipori, S. 2002. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl. Environ. Microbiol. 68(5): 2595-2599.
Cox, J.C., Hamilton, R.C. and Attwood, H.D. 1979. An investigation of the route and progression of Encephalitozoon cuniculi infection in adult rabbits. J. Protozool. 26(2): 260-265.
Dascomb, K., Frazer, T., Clark, R.A., Kissinger, P. and Didier, E. 2000. Microsporidiosis and HIV. J. Acquir. Immune. Defic. Syndr. 24(3): 290-292.
Graczyk, T.K., Bosco-Nizeyi, J., da Silva, A.J., Moura, I.N., Pieniazek, N.J., Cranfield, M.R. and Lindquist, H.D. 2002. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol Res. 88(10): 926-931.
Hutin, Y.J., Sombardier, M.N., Liguory, O., Sarfati, C., Derouin, F., Modaï, J. and Molina, J.M. 1998. Risk factors for intestinal microsporidiosis in patients with human immunodeficiency virus infection: a case-control study. J. Infect. Dis. 178(3): 904-907.
Jass, A., Matiasek, K., Henke, J., Küchenhoff, H., Hartmann, K. and Fischer, A. 2008. Analysis of cerebrospinal fluid in healthy rabbits and rabbits with clinically suspected encephalito-zoonosis. Vet. Rec. 162(19): 618-622.
Kakrania, R., Joseph, J., Vaddavalli, P.K., Gangopadhyay, N. and Sharma, S. 2006. Microsporidia keratoconjunctivitis in a corneal graft. Eye (Lond). 20(11): 1314-1315.
Künzel, F. and Joachim, A. 2010. Encephalitozoonosis in rabbits. Parasitol. Res. 106(2):299-309.
Leelayoova, S., Piyaraj, P., Subrungruang, I., Pagornrat, W., Naaglor, T., Phumklan, S., Taamasri, P., Suwanasri, J. and Mungthin, M. 2009. Genotypic characterization of Enterocytozoon bieneusi in specimens from pigs and humans in a pig farm community in Central Thailand. J. Clin. Microbiol. 47(5): 1572-1574.
Li, X., Palmer, R., Trout, J.M. and Fayer R. 2003. Infectivity of microsporidia spores storedin water at environmental temperatures. J. Parasitol. 89(1):185-188.
Mathis, A., Weber, R. and Deplazes, P. 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 18(3): 423-445.
Mathis, A., Michel, M., Kuster, H., Müller, C., Weber, R. and Deplazes, P. 1997. Two Encephalitozoon cuniculi strains of human origin are infectious to rabbits. Parasitol. 114 (Pt 1):29-35.
McInnes, E.F. and Stewart, C.G. 1991. The pathology of subclinical infection of Encephalitozoon cuniculi in canine dams producing pups with overt encephalitozoonosis. J. S. Afr. Vet. Assoc. 62(2):51-4.
Mori, H., Mahittikorn, A., Thammasonthijarern, N., Chaisiri, K., Rojekittikhun, W. and Sukthana, Y. 2013a. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Vet. Parasitol. 197(3-4): 696-701.
Mori, H., Mahittikorn, A., Watthanakulpanich, D., Komalamisra, C. and Sukthana, Y. 2013b. Zoonotic potential of Enterocytozoon bieneusi among children in rural communities in Thailand. Parasite. 20:14.
Pan, Y., Wang, S., Liu, X., Li, R., Sun, Y. and Gadahi, J.A. 2015. Seroprevalence of Encephalitozoon cuniculi in Humans and Rabbits in China. Iran. J. Parasitol. 10(2): 290-295.
Prasertbun, R., Mori, H., Pintong, A.R,, Sanyanusin, S., Popruk, S., Komalamisra, C., Changbunjong, T., Buddhirongawatr, R., Sukthana, Y. and Mahittikorn, A. 2017. Zoonotic potential of Enterocytozoon genotypes in humans and pigs in Thailand. Vet. Parasitol. 233:73-79.
Pulparampil, N., Graham, D., Phalen, D. and Snowden, K. 1998. Encephalitozoon hellem in two eclectus parrots (Eclectus roratus): identification from archival tissues. J. Eukaryot. Microbiol. 45(6): 651-655.
Rinder, H. 2004. Transmission of microsporidia to humans: Water-borne, food-borne, air-borne, zoonotic, or anthroponotic? Southeast. Asian. J. Trop. Med. Public. Health. 35 (Suppl1): 54-57
Saigal, K., Sharma, A., Sehgal, R., Sharma, P., Malla, N. and Khurana, S. 2013. Intestinal microsporidiosis in India: a two year study. Parasitol. Int. 62(1): 53-56.
Santín, M. and Fayer, R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res. Vet. Sci. 90(3): 363-371
Shadduck, J.A. and Polley, M.B. 1978. Some factors influencing the in vitro infectivity and replication of Encephalitozoon cuniculi. J. Protozool. 25(4): 491-496.
Snowden, K.F., Logan, K. and Phalen, D.N. 2000. Isolation and characterization of an avian isolate of Encephalitozoon hellem. Parasitol. 121 (Pt 1): 9-14.
Snowden, K.F., Didier, E.S., Orenstein, J.M. and Shadduck, J.A. 1998. Animal models of human microsporidial infections. Lab. Anim. Sci. 48(6): 589-592.
Sulaiman, I.M., Bern, C., Gilman, R., Cama, V., Kawai, V., Vargas, D., Ticona, E., Vivar, A. and Xiao, L. 2003. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. J. Eukaryot. Microbiol. 50 Suppl: 591-596.
Viriyavejakul, P., Nintasen, R., Punsawad, C., Chaisri, U., Punpoowong, B. and Riganti, M. 2009. High prevalence of Microsporidium infection in HIV-infected patients. Southeast Asian J Trop Med Public Health. 40(2): 223-228.
Waller, T. 1979. Sensitivity of Encephalitozoon cuniculi to various temperatures, disinfectants and drugs. Lab. Anim. 13(3): 227-230.
Wanachiwanawin, D., Manatsathit, S., Lertlaituan, P., Thakerngpol, K. and Suwanagool, P. 1998. Intestinal microsporidiosis in HIV infected patients with chronic diarrhea in Thailand. Southeast. Asian. J. Trop. Med. Public. Health. 29(4): 767-771.
Watson, D. R. A., Asmuth, D. and Wanke, C.A. 1996. Environmental risk factors for acquisition of microsporidia in HIV-infected persons. In Proceedings of the 34th Annual Meeting of the Infectious Diseases Society of America, New Orleans, La., p. 67. Infectious Diseases Society of America, New Orleans, La.
Weber, R., Kuster, H., Visvesvara, G.S., Bryan, R.T., Schwartz, D.A. and Lüthy, R. 1993. Disseminated microsporidiosis due to Encephalitozoon hellem: pulmonary colonization, microhematuria, and mild conjunctivitis in a patient with AIDS. Clin. Infect. Dis. 17(3): 415-419.
Wichro, E., Hoelzl, D., Krause, R., Bertha, G., Reinthaler, F. and Wenisch, C. 2005. Microsporidiosis in travel-associated chronic diarrhea in immune-competent patients. Am. J. Trop. Med. Hyg. 73(2): 285-287.
Wumba, R., Longo-Mbenza, B., Menotti, J., Mandina, M., Kintoki, F., Situakibanza, N.H., Kakicha, M.K., Zanga, J., Mbanzulu-Makola, K., Nseka, T., Mukendi, J.P., Kendjo, E., Sala, J. and Thellier, M. 2012. Epidemiology, clinical, immune, and molecular profiles of microsporidiosis and cryptosporidiosis among HIV/AIDS patients. Int. J. Gen. Med. 5: 603-611.