A review was conducted to examine published works that focus on the complex epidemiology of Enterocytozoon bieneusi infection in humans. Studies on the prevalence of these emerging microsporidian pathogens in humans, in developed and developing countries, the different clinical spectra of E. bieneusi intestinal infection in children, in different settings, and the risk factors associated with E. bieneusi infection have been reviewed. This paper also analyses the impact of the recent application of PCR-based molecular methods for species-specific identification and genotype differentiation has had in increasing the knowledge of the molecular epidemiology of E. bieneusi in humans. The advances in the epidemiology of E. bieneusi, in the last two decades, emphasize the importance of epidemiological control and prevention of E. bieneusi infections, from both the veterinary and human medical perspectives. 1. Introduction Microsporidia are a group of obligate intracellular eukaryotic parasites first identified as the cause of pébrine disease of silkworms in 1857 [1]. Over the past two decades, microsporidia have risen from obscure organisms to well-recognized human pathogens. Several genera and species of microsporidia were found in humans, and diagnosis and clinical management of microsporidiosis cases have improved significantly. Despite these scientific advances, the epidemiology of human microsporidiosis is still unclear. Most of what is now known about human microsporidiosis can be attributed to experience with patients infected with human immunodeficiency virus (HIV). Since 1985 and the first recognition of Enterocytozoon bieneusi as an acquired immunodeficiency syndrome (AIDS)-associated opportunistic pathogen [2], several hundred patients with chronic diarrhea attributed to this organism have been reported. Cases of intestinal microsporidiosis due to E. bieneusi have been increasingly reported in other immunocompromised individuals such as organ transplant recipients, as well as in travelers, children, and elderly [3–12]. Hepatobiliary and pulmonary involvement has also been observed in immunocompromised persons [13–15]. Some reports in humans suggested that this species can produce asymptomatic infections in immunocompromised and immunocompetent individuals [16–20]. In addition, E. bieneusi has been commonly identified in animals, especially mammals [21–32], and water, raising public health concerns about zoonotic and waterborne transmission of microsporidia [33–35]. 2. Prevalence of Enterocytozoon bieneusi in Humans Enterocytozoon bieneusi infections
References
[1]
K. N?geli, “über die neue Krankheit die Seidenraupe unde verwandet Organismen,” Botanische Zeitung, vol. 15, pp. 760–761, 1857.
[2]
I. Desportes, Y. Le Charpentier, A. Galian et al., “Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS,” Journal of Protozoology, vol. 32, no. 2, pp. 250–254, 1985.
[3]
R. T. Bryan and D. A. Schwartz, “Epidemiology of microsporidiosis,” in The Microsporidia and Microsporidiosis, pp. 502–516, American Society For Microbiology, Washington, DC, USA, 1999.
[4]
J. C. Gainzarain, A. Canut, M. Lozano et al., “Detection of Enterocytozoon bieneusi in two human immunodeficiency virus-negative patients with chronic diarrhea by polymerase chain reaction in duodenal biopsy specimens and review,” Clinical Infectious Diseases, vol. 27, no. 2, pp. 394–398, 1998.
[5]
S. Leelayoova, I. Subrungruang, R. Rangsin et al., “Transmission of Enterocytozoon bieneusi genotype A in a Thai orphanage,” American Journal of Tropical Medicine and Hygiene, vol. 73, no. 1, pp. 104–107, 2005.
[6]
R. López-Vélez, M. C. Turrientes, C. Garrón et al., “Microsporidiosis in travelers with diarrhea from the tropics,” Journal of Travel Medicine, vol. 6, no. 4, pp. 223–227, 1999.
[7]
B. Lores, I. López-Miragaya, C. Arias, S. Fenoy, J. Torres, and C. del Aguila, “Intestinal microsporidiosis due to Enterocytozoon bieneusi in elderly human immunodeficiency virus-negative patients from Vigo, Spain,” Clinical Infectious Diseases, vol. 34, no. 7, pp. 918–921, 2002.
[8]
A. Müller, R. Bialek, A. K?mper, G. F?tkenheuer, B. Salzberger, and C. Franzen, “Detection of microsporidia in travelers with diarrhea,” Journal of Clinical Microbiology, vol. 39, no. 4, pp. 1630–1632, 2001.
[9]
M. Mungthin, I. Subrungruang, T. Naaglor, P. Aimpun, W. Areekul, and S. Leelayoova, “Spore shedding pattern of Enterocytozoon bieneusi in asymptomatic children,” Journal of Medical Microbiology, vol. 54, no. 5, pp. 473–476, 2005.
[10]
I. Sobottka, H. Albrecht, J. Schottelius et al., “Self-limited traveller's diarrhea due to a dual infection with Enterocytozoon bieneusi and Cryytosporidium parvum in an immunocompetent HIV-negative child,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 14, no. 10, pp. 919–920, 1995.
[11]
C. A. Wanke, “Enterocytozoon bieneusi infection and diarrheal disease in patients who were not infected with human immunodeficiency virus: case report and review,” Clinical Infectious Diseases, vol. 23, no. 4, pp. 816–818, 1996.
[12]
E. Wichro, D. Hoelzl, R. Krause, G. Bertha, F. Reinthaler, and C. Wenisch, “Microsporidiosis in travel-associated chronic diarrhea in immune-competent patients,” American Journal of Tropical Medicine and Hygiene, vol. 73, no. 2, pp. 285–287, 2005.
[13]
F. Botterel, C. Minozzi, D. Vittecoq, and P. Bourée, “Pulmonary localization of Enterocytozoon bieneusi in an aids patient: case report and review,” Journal of Clinical Microbiology, vol. 40, no. 12, pp. 4800–4801, 2002.
[14]
D. P. Kotler and J. M. Orenstein, “Clinical syndromes associated with microsporidiosis,” Advances in Parasitology, vol. 40, pp. 321–349, 1998.
[15]
M. Sodqi, P. Brazille, G. Gonzalez-Canali, M. Cornet, C. Piketty, and L. Weiss, “Unusual pulmonary Enterocytozoon bieneusi microsporidiosis in an AIDS patient: case report and review,” Scandinavian Journal of Infectious Diseases, vol. 36, no. 3, pp. 230–231, 2004.
[16]
J. M. Orenstein, J. Chiang, W. Steinberg, P. D. Smith, H. Rotterdam, and D. P. Kotler, “Intestinal microsporidiosis as a cause of diarrhea in human immunodeficiency virus-infected patients: a report of 20 cases,” Human Pathology, vol. 21, no. 5, pp. 475–481, 1990.
[17]
C. M. Coyle, M. Wittner, D. P. Kotler et al., “Prevalence of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon (Septata) intestinalis among patients with AIDS-related diarrhea: determination by polymerase chain reaction to the microsporidian small-subunit rRNA gene,” Clinical Infectious Diseases, vol. 23, no. 5, pp. 1002–1006, 1996.
[18]
J. K. Tumwine, A. Kekitiinwa, N. Nabukeera, D. E. Akiyoshi, M. A. Buckholt, and S. Tzipori, “Enterocytozoon bieneusi among children with diarrhea attending Mulago hospital in Uganda,” American Journal of Tropical Medicine and Hygiene, vol. 67, no. 3, pp. 299–303, 2002.
[19]
W. Pagornrat, S. Leelayoova, R. Rangsin, P. Tan-Ariya, T. Naaglor, and M. Mungthin, “Carriage rate of Enterocytozoon bieneusi in an orphanage in Bangkok, Thailand,” Journal of Clinical Microbiology, vol. 47, no. 11, pp. 3739–3741, 2009.
[20]
B. Sak, D. Brady, M. Pelikánová et al., “Unapparent microsporidial infection among immunocompetent humans in the Czech Republic,” Journal of Clinical Microbiology, vol. 49, no. 3, pp. 1064–1070, 2011.
[21]
P. Deplazes, A. Mathis, C. Müller, and R. Weber, “Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs,” Journal of Eukaryotic Microbiology, vol. 43, no. 5, Article ID 93S, 1996.
[22]
K. G. Mansfield, A. Carville, D. Shvetz, J. MacKey, S. Tzipori, and A. A. Lackner, “Identification of an Enterocytozoon bieneusi-like microsporidian parasite in simian-immunodeficiency-virus-inoculated macaques with hepatobiliary disease,” American Journal of Pathology, vol. 150, no. 4, pp. 1395–1405, 1997.
[23]
C. del Aguila, F. Izquierdo, R. Navajas et al., “Enterocytozoon bieneusi in animals: rabbits and dogs as new hosts,” Journal of Eukaryotic Microbiology, vol. 46, no. 5, pp. 8S–9S, 1999.
[24]
I. M. Sulaiman, R. Fayer, A. A. Lal, J. M. Trout, F. W. Schaefer III, and L. Xiao, “Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi,” Applied and Environmental Microbiology, vol. 69, no. 8, pp. 4495–4501, 2003.
[25]
I. M. Sulaiman, R. Fayer, C. Yang, M. Santin, O. Matos, and L. Xiao, “Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential,” Parasitology Research, vol. 92, no. 4, pp. 328–334, 2004.
[26]
M. L. Lobo, L. Xiao, V. Cama, T. Stevens, F. Antunes, and O. Matos, “Genotypes of Enterocytozoon bieneusi in mammals in Portugal,” Journal of Eukaryotic Microbiology, vol. 53, no. 1, pp. S61–S64, 2006.
[27]
N. Abe, I. Kimata, and M. Iseki, “Molecular evidence of Enterocytozoon bieneusi in Japan,” Journal of Veterinary Medical Science, vol. 71, no. 2, pp. 217–219, 2009.
[28]
J. Reetz, K. N?ckler, S. Reckinger, M. M. Vargas, W. Weiske, and A. Broglia, “Identification of Encephalitozoon cuniculi genotype III and two novel genotypes of Enterocytozoon bieneusi in swine,” Parasitology International, vol. 58, no. 3, pp. 285–292, 2009.
[29]
M. Santn, J. A. Cortés Vecino, and R. Fayer, “A zoonotic genotype of Enterocytozoon bieneusi in horses,” Journal of Parasitology, vol. 96, no. 1, pp. 157–161, 2010.
[30]
X. Zhang, Z. Wang, Y. Su et al., “Identification and genotyping of Enterocytozoon bieneusi in China,” Journal of Clinical Microbiology, vol. 49, no. 5, pp. 2006–2008, 2011.
[31]
B. Sak, M. Kvá?, K. Petr?elková et al., “Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission?” Folia Parasitologica, vol. 58, no. 2, pp. 81–86, 2011.
[32]
W. Li, N. M. Kiulia, J. M. Mwenda et al., “Cyclospora papionis, Cryptosporidium hominis, and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya,” Journal of Clinical Microbiology, vol. 49, pp. 4326–4329, 2011.
[33]
L. Cotte, M. Rabodonirina, F. Chapuis et al., “Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection,” Journal of Infectious Diseases, vol. 180, no. 6, pp. 2003–2008, 1999.
[34]
C. Franzen and A. Müller, “Cryptosporidia and microsporidia—waterborne diseases in the immunocompromised host,” Diagnostic Microbiology and Infectious Disease, vol. 34, no. 3, pp. 245–262, 1999.
[35]
H. W. A. Cheng, F. E. Lucy, T. K. Graczyk, M. A. Broaders, and S. E. Mastitsky, “Municipal wastewater treatment plants as removal systems and environmental sources of human-virulent microsporidian spores,” Parasitology Research, vol. 49, no. 12, pp. 4326–4329, 2011.
[36]
D. M. Asmuth, P. C. DeGirolami, M. Federman et al., “Clinical features of microsporidiosis in patients with AIDS,” Clinical Infectious Diseases, vol. 18, no. 5, pp. 819–825, 1994.
[37]
L. Cotte, M. Rabodonirina, M. A. Piens, M. Perreard, M. Mojon, and C. Trepo, “Prevalence of intestinal protozoans in French patients infected with HIV,” Journal of Acquired Immune Deficiency Syndromes, vol. 6, no. 9, pp. 1024–1029, 1993.
[38]
F. M. B. Ferreira, L. Bezerra, M. B. G. Santos, R. M. A. Bernardes, I. Avelino, and M. L. Sampaio Silva, “Intestinal microsporidiosis: a current infection in HIV-seropositive patients in Portugal,” Microbes and Infection, vol. 3, no. 12, pp. 1015–1019, 2001.
[39]
A. S. Field, M. C. Hing, S. T. Milliken, and D. J. Marriott, “Microsporidia in the small intestine of HIV-infected patients. A new diagnostic technique and a new species,” Medical Journal of Australia, vol. 158, no. 6, pp. 390–394, 1993.
[40]
T. Kyaw, A. Curry, V. Edwards-Jones, J. Craske, and B. K. Mandal, “The prevalence of Enterocytozoon bieneusi in acquired immunodeficiency syndrome (AIDS) patients from the north west of England: 1992–1995,” British Journal of Biomedical Science, vol. 54, no. 3, pp. 186–191, 1997.
[41]
J. M. Molina, C. Sarfati, B. Beauvais et al., “Intestinal microsporidiosis in human immunodeficiency virus-infected patients with chronic unexplained diarrhea: prevalence and clinical and biologic features,” Journal of Infectious Diseases, vol. 167, no. 1, pp. 217–221, 1993.
[42]
W. Schmidt, T. Schneider, W. Heise et al., “Mucosal abnormalities in microsporidiosis,” AIDS, vol. 11, no. 13, pp. 1589–1594, 1997.
[43]
I. Sobottka, D. A. Schwartz, J. Schottelius et al., “Prevalence and clinical significance of intestinal microsporidiosis in human immunodeficiency virus-infected patients with and without diarrhea in Germany: a prospective coprodiagnostic study,” Clinical Infectious Diseases, vol. 26, no. 2, pp. 475–480, 1998.
[44]
M. C. Voglino, G. Donelli, P. Rossi et al., “Intestinal microsporidiosis in Italian individuals with AIDS,” Italian Journal of Gastroenterology, vol. 28, no. 7, pp. 381–386, 1996.
[45]
M. L. Lobo, L. Xiao, F. Antunes, and O. Matos, “Microsporidia as emerging pathogens and the implication for public health: a 10-year study on HIV-positive and -negative patients,” International Journal for Parasitology, vol. 42, pp. 197–205, 2012.
[46]
N. Abreu-Acosta, J. Lorenzo-Morales, Y. Leal-Guio et al., “Enterocytozoon bieneusi (microsporidia) in clinical samples from immunocompetent individuals in Tenerife, Canary Islands, Spain,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 99, no. 11, pp. 848–855, 2005.
[47]
O. Alfa Cisse, A. Ouattara, M. Thellier et al., “Evaluation of an immunofluorescent-antibody test using monoclonal antibodies directed against Enterocytozoon bieneusi and Encephalitozoon intestinalis for diagnosis of intestinal microsporidiosis in bamako (Mali),” Journal of Clinical Microbiology, vol. 40, no. 5, pp. 1715–1718, 2002.
[48]
C. Bern, V. Kawai, D. Vargas et al., “The epidemiology of intestinal microsporidiosis in patients with HIV/AIDS in Lima, Peru,” Journal of Infectious Diseases, vol. 191, no. 10, pp. 1658–1664, 2005.
[49]
S. Bretagne, F. Foulet, W. Alkassoum, J. Fleury-Feith, and M. Develoux, “Prevalence of Enterocytozoon bieneusi spores in the stool of AIDS patients and African children not infected by HIV,” Bulletin de la Societe de Pathologie Exotique, vol. 86, no. 5, pp. 351–357, 1993.
[50]
T. Gumbo, S. Sarbah, I. T. Gangaidzo et al., “Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe,” AIDS, vol. 13, no. 7, pp. 819–821, 1999.
[51]
I. Maiga, O. Doumbo, M. Dembele et al., “Human intestinal microsporidiosis in Bamako (Mali): the presence of Enterocytozoon bieneusi in HIV seropositive patients,” Sante, vol. 7, no. 4, pp. 257–262, 1997.
[52]
K. Mohandas, R. Sehgal, A. Sud, and N. Malla, “Prevalence of intestinal parasitic pathogens in HIV-seropositive individuals in Northern India,” Japanese Journal of Infectious Diseases, vol. 55, no. 3, pp. 83–84, 2002.
[53]
S. W. Nkinin, T. Asonganyi, E. S. Didier, and E. S. Kaneshiro, “Microsporidian infection is prevalent in healthy people in Cameroon,” Journal of Clinical Microbiology, vol. 45, no. 9, pp. 2841–2846, 2007.
[54]
A. Samie, C. L. Obi, S. Tzipori, L. M. Weiss, and R. L. Guerrant, “Microsporidiosis in South Africa: PCR detection in stool samples of HIV-positive and HIV-negative individuals and school children in Vhembe district, Limpopo Province,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 101, no. 6, pp. 547–554, 2007.
[55]
C. Sarfati, A. Bourgeois, J. Menotti et al., “Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study,” American Journal of Tropical Medicine and Hygiene, vol. 74, no. 1, pp. 162–164, 2006.
[56]
I. M. Sulaiman, C. Bern, R. Gilman et al., “A Molecular Biologic Study of Enterocytozoon bieneusi in HIV-Infected Patients in Lima, Peru,” Journal of Eukaryotic Microbiology, vol. 50, pp. 591–596, 2003.
[57]
T. Van Gool, E. Luderhoff, K. J. Nathoo, C. F. Kiire, J. Dankert, and P. R. Mason, “High prevalence of Enterocytozoon bieneusi infections among HIV-positive individuals with persistent diarrhoea in Harare, Zimbabwe,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 89, no. 5, pp. 478–480, 1995.
[58]
D. Wanachiwanawin, “Intestinal microsporidiosis in HIV infected patients with chronic diarrhea in Thailand,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 29, no. 4, pp. 767–771, 1998.
[59]
D. Waywa, S. Kongkriengdaj, S. Chaidatch et al., “Protozoan enteric infection in aids related diarrhea in Thailand,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 32, no. 2, pp. 151–155, 2001.
[60]
R. Wumba, B. Longo-Mbenza, M. Mandina et al., “Intestinal parasites infections in hospitalized aids patients in kinshasa, democratic Republic of Congo,” Parasite, vol. 17, no. 4, pp. 321–328, 2010.
[61]
T. Gumbo, I. T. Gangaidzo, S. Sarbah, A. Carville, S. Tzipori, and P. M. Wiest, “Enterocytozoon bieneusi infection in patients without evidence of immunosuppression: two cases from Zimbabwe found to have positive stools by PCR,” Annals of Tropical Medicine and Parasitology, vol. 94, no. 7, pp. 699–702, 2000.
[62]
S. Anane, E. Kaouech, S. Belhadj et al., “Identification of Enterocytozoon bieneusi by PCR in stools of Tunisian immunocompromised patients,” Pathologie Biologie, vol. 59, no. 4, pp. 234–239, 2011.
[63]
S. M. Valperga, S. A. de Jogna Prat, G. J. O. de Valperga et al., “Microsporidian spores in the stool specimens of toddler, with or without diarrhea, from Tucuman, Argentina,” Revista Argentina de Microbiologia, vol. 31, no. 3, pp. 157–164, 1999.
[64]
J. K. Tumwine, A. Kekitiinwa, S. Bakeera-Kitaka et al., “Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus,” American Journal of Tropical Medicine and Hygiene, vol. 73, no. 5, pp. 921–925, 2005.
[65]
D. Wanachiwanawin, K. Chokephaibulkit, P. Lertlaituan, J. Ongrotchanakun, P. Chinabut, and K. Thakerngpol, “Intestinal microsporidiosis in hiv-infected children with diarrhea,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 33, no. 2, pp. 241–245, 2002.
[66]
C. del Aguila, R. Navajas, D. Gurbindo et al., “Microsporidiosis in HIV-positive children in madrid (Spain),” Journal of Eukaryotic Microbiology, vol. 44, no. 6, p. 84, 1997.
[67]
A. B. Ayinmode, O. T. Ojuromi, and L. Xiao, “Molecular Identification of Enterocytozoon bieneusi Isolates from Nigerian Children,” Journal of Parasitology Research, vol. 2011, Article ID 129542, 2 pages, 2011.
[68]
O. T. Ojuromi, F. Izquierdo, S. Fenoy et al., “Identification and characterization of microsporidia from fecal samples of HIV-positive patients from Lagos, Nigeria,” PLoS ONE, vol. 7, no. 4, 2012.
[69]
M. Mungthin, R. Suwannasaeng, T. Naaglor, W. Areekul, and S. Leelayoova, “Asymptomatic intestinal microsporidiosis in Thai orphans and child-care workers,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 95, no. 3, pp. 304–306, 2001.
[70]
C. N. Conteas, O. G. W. Berlin, M. J. Lariviere et al., “Examination of the prevalence and seasonal variation of intestinal microsporidiosis in the stools of persons with chronic diarrhea and human immunodeficiency virus infection,” American Journal of Tropical Medicine and Hygiene, vol. 58, no. 5, pp. 559–561, 1998.
[71]
R. Weber, B. Ledergerber, R. Zbinden et al., “Enteric infections and diarrhea in human virus-infected persons: prospective community-based cohort study,” Archives of Internal Medicine, vol. 159, no. 13, pp. 1473–1480, 1999.
[72]
T. P. R. Bachur, J. M. Vale, I. C. B. C?elho, T. R. B. S. de Queiroz, and C. de Souza Chaves, “Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy,” Brazilian Journal of Infectious Diseases, vol. 12, no. 2, pp. 115–122, 2008.
[73]
C. R. Vossbrinck, J. V. Maddox, and S. Friedman, “Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes,” Nature, vol. 326, no. 6111, pp. 411–414, 1987.
[74]
J. M. Orenstein, W. Zierdt, C. Zierdt, and D. P. Kotler, “Identification of spores of Enterocytozoon bieneusi in stool and duodenal fluid from AIDS patients,” The Lancet, vol. 336, no. 8723, pp. 1127–1128, 1990.
[75]
V. A. Cama, J. Pearson, L. Cabrera et al., “Transmission of Enterocytozoon bieneusi between a child and guinea pigs,” Journal of Clinical Microbiology, vol. 45, no. 8, pp. 2708–2710, 2007.
[76]
A. Espern, F. Morio, M. Miegeville et al., “Molecular study of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among human immunodeficiency virus-infected patients from two geographical areas: Niamey, Niger, and Hanoi, Vietnam,” Journal of Clinical Microbiology, vol. 45, no. 9, pp. 2999–3002, 2007.
[77]
J. P. Cegielski, Y. R. Ortega, S. McKee et al., “Cryptosporidium Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania,” Clinical Infectious Diseases, vol. 28, no. 2, pp. 314–321, 1999.
[78]
D. P. Kotler, A. Francisco, F. Clayton, J. V. Scholes, and J. M. Orenstein, “Small intestinal injury and parasitic diseases in AIDS,” Annals of Internal Medicine, vol. 113, no. 6, pp. 444–449, 1990.
[79]
J. K. Greenson, P. C. Belitsos, J. H. Yardley, and J. G. Bartlett, “AIDS enteropathy: occult enteric infections and duodenal mucosal alterations in chronic diarrhea,” Annals of Internal Medicine, vol. 114, no. 5, pp. 366–372, 1991.
[80]
S. Leelayoova, N. Vithayasai, V. Watanaveeradej et al., “Intestinal microsporidiosis in HIV-infected children with acute and chronic diarrhea,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 32, no. 1, pp. 33–37, 2001.
[81]
S. M. Mor, J. K. Tumwine, E. N. Naumova, G. Ndeezi, and S. Tzipori, “Microsporidiosis and malnutrition in children with persistent diarrhea, Uganda,” Emerging Infectious Diseases, vol. 15, no. 1, pp. 49–52, 2009.
[82]
T. Endeshaw, A. Kebede, J. J. Verweij et al., “Intestinal microsporidiosis in diarrheal patients infected with human immunodeficiency virus-1 in Addis Ababa, Ethiopia,” Japanese Journal of Infectious Diseases, vol. 59, no. 5, pp. 306–310, 2006.
[83]
L. Rabeneck, F. Gyorkey, R. M. Genta, P. Gyorkey, L. W. Foote, and J. M. H. Risser, “The role of Microsporidia in the pathogenesis of HIV-related chronic diarrhea,” Annals of Internal Medicine, vol. 119, no. 9, pp. 895–899, 1993.
[84]
J. E. Clarridge, S. Karkhanis, L. Rabeneck, B. Marino, and L. W. Foote, “Quantitative light microscopic detection of Enterocytozoon bieneusi in stool specimens: a longitudinal study of human immunodeficiency virus-infected microsporidiosis patients,” Journal of Clinical Microbiology, vol. 34, no. 3, pp. 520–523, 1996.
[85]
L. Chacin-Bonilla, A. P. Panunzio, F. M. Monsalve-Castillo, I. E. Parra-Cepeda, and R. Martinez, “Microsporidiosis in Venezuela: prevalence of intestinal microsporidiosis and its contribution to diarrhea in a group of human immunodeficiency virus-infected patients from Zulia State,” American Journal of Tropical Medicine and Hygiene, vol. 74, no. 3, pp. 482–486, 2006.
[86]
K. Dascomb, T. Frazer, R. A. Clark, P. Kissinger, and E. Didier, “Microsporidiosis and HIV,” Journal of Acquired Immune Deficiency Syndromes, vol. 24, no. 3, pp. 290–292, 2000.
[87]
O. I. Sokolova, A. V. Demyanov, L. C. Bowers et al., “Emerging microsporidian infections in Russian HIV-infected patients,” Journal of Clinical Microbiology, vol. 49, no. 6, pp. 2102–2108, 2011.
[88]
J. H. Botero, M. N. Montoya, A. L. Vanegas et al., “Frequency of intestinal microsporidian infections in HIV-positive patients, as diagnosis by quick hot Gram chromotrope staining and PCR,” Biomedica, vol. 24, no. 4, pp. 375–384, 2004.
[89]
P. Brasil, D. B. de Lima, D. D. de Paiva et al., “Clinical and diagnostic aspects of intestinal microsporidiosis in HIV-infected patients with chronic diarrhea in Rio de Janeiro, Brazil,” Revista do Instituto de Medicina Tropical de Sao Paulo, vol. 42, no. 6, pp. 299–304, 2000.
[90]
A. A. Escobedo and F. A. Nú?ez, “Prevalence of intestinal parasites in Cuban acquired immunodeficiency syndrome (AIDS) patients,” Acta Tropica, vol. 72, no. 1, pp. 125–130, 1999.
[91]
E. Bernard, M. Carles, C. Pradier et al., “Chronic diarrhoea in HIV+ patients: role of Enterocytozoon bieneusi,” Presse Medicale, vol. 24, no. 14, pp. 671–674, 1995.
[92]
O. Liguory, C. Sarfati, F. Derouin, and J. M. Molina, “Evidence of different Enterocytozoon bieneusi genotypes in patients with and without human immunodeficiency virus infection,” Journal of Clinical Microbiology, vol. 39, no. 7, pp. 2672–2674, 2001.
[93]
C. Franzen, A. Müller, P. Hegener et al., “Polymerase chain reaction for microsporidian DNA in gastrointestinal biopsy specimens of HIV-infected patients,” AIDS, vol. 10, no. 8, pp. F23–F27, 1996.
[94]
H. Rinder, S. Katzwinkel-Wladarsch, and T. L?scher, “Evidence for the existence of genetically distinct strains of Enterocytozoon bieneusi,” Parasitology Research, vol. 83, no. 7, pp. 670–672, 1997.
[95]
B. Dengjel, M. Zahler, W. Hermanns et al., “Zoonotic potential of Enterocytozoon bieneusi,” Journal of Clinical Microbiology, vol. 39, no. 12, pp. 4495–4499, 2001.
[96]
T. Van Gool, F. Snijders, P. Reiss et al., “Diagnosis of intestinal and disseminated microsporidial infections in patients with HIV by a new rapid fluorescence technique,” Journal of Clinical Pathology, vol. 46, no. 8, pp. 694–699, 1993.
[97]
S. D. Polley, S. Boadi, J. Watson, A. Curry, and P. L. Chiodini, “Detection and species identification of microsporidial infections using SYBR Green real-time PCR,” Journal of Medical Microbiology, vol. 60, no. 4, pp. 459–466, 2011.
[98]
Z. Kucerova, O. I. Sokolova, A. V. Demyanov et al., “Microsporidiosis and cryptosporidiosis in HIV/AIDS patients in St. Petersburg, Russia: serological identification of microsporidia and Cryptosporidium parvum in sera samples from HIV/AIDS patients,” AIDS Research and Human Retroviruses, vol. 27, no. 1, pp. 13–15, 2011.
[99]
J. Breton, E. Bart-Delabesse, S. Biligui et al., “New highly divergent rRNA sequence among biodiverse genotypes of Enterocytozoon bieneusi strains isolated from humans in Gabon and Cameroon,” Journal of Clinical Microbiology, vol. 45, no. 8, pp. 2580–2589, 2007.
[100]
F. Drobniewski, P. Kelly, A. Carew et al., “Human microsporidiosis in African AIDS patients with chronic diarrhea,” Journal of Infectious Diseases, vol. 171, no. 2, pp. 515–516, 1995.
[101]
H. Rinder, S. Katzwinkel-Wladarsch, A. Thomschke, and T. L?scher, “Strain differentiation in microsporidia,” Tokai Journal of Experimental and Clinical Medicine, vol. 23, no. 6, pp. 433–437, 1998.
[102]
W. Saksirisampant, J. Prownebon, P. Saksirisampant, M. Mungthin, S. Siripatanapipong, and S. Leelayoova, “Intestinal parasitic infections: prevalences in HIV/AIDS patients in a Thai AIDS-care centre,” Annals of Tropical Medicine and Parasitology, vol. 103, no. 7, pp. 573–581, 2009.
[103]
N. J. Ryan, G. Sutherland, K. Coughlan et al., “A new trichrome-blue stain for detection of microsporidial species in urine, stool, and nasopharyngeal specimens,” Journal of Clinical Microbiology, vol. 31, no. 12, pp. 3264–3269, 1993.
[104]
S. Katzwinkel-Wladarsch, M. Lieb, W. Heise, T. L?scher, and H. Rinder, “Direct amplification and species determination of microsporidian DNA from stool specimens,” Tropical Medicine and International Health, vol. 1, no. 3, pp. 373–378, 1996.
[105]
S. Coupe, K. Delabre, R. Pouillot, S. Houdart, M. Santillana-Hayat, and F. Derouin, “Detection of Cryptosporidium, Giardia and Enterocytozoon bieneusi in surface water, including recreational areas: a one-year prospective study,” FEMS Immunology and Medical Microbiology, vol. 47, no. 3, pp. 351–359, 2006.
[106]
J. M. Sparfel, C. Sarfati, O. Liguory et al., “Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR,” Journal of Eukaryotic Microbiology, vol. 44, supplement S6, p. 78S, 1997.
[107]
J. A. Thurston-Enriquez, P. Watt, S. E. Dowd, R. Enriquez, I. L. Pepper, and C. P. Gerba, “Detection of protozoan parasites and microsporidia in irrigation waters used for crop production,” Journal of Food Protection, vol. 65, no. 2, pp. 378–382, 2002.
[108]
A. L. Galván, A. M. M. Sánchez, M. A. P. Valentín et al., “First cases of microsporidiosis in transplant recipients in spain and review of the literature,” Journal of Clinical Microbiology, vol. 49, no. 4, pp. 1301–1306, 2011.
[109]
O. Liguory, F. David, C. Sarfati, F. Derouin, and J. M. Molina, “Determination of types of Enterocytozoon bieneusi strains isolated from patients with intestinal microsporidiosis,” Journal of Clinical Microbiology, vol. 36, no. 7, pp. 1882–1885, 1998.
[110]
H. Rinder, B. Dengjel, R. Gothe, and T. Loscher, “Microsporidosis of man: where is the reservoir?” Mitt Osterr Ges Tropenmed Parasitol, vol. 22, pp. 1–6, 2000.
[111]
F. Sadler, N. Peake, R. Borrow, P. L. Rowl, E. G. L. Wilkins, and A. Curry, “Genotyping of Enterocytozoon bieneusi in AIDS patients from the north west of England,” Journal of Infection, vol. 44, no. 1, pp. 39–42, 2002.
[112]
R. J. Ten Hove, L. Van Lieshout, M. B. J. Beadsworth et al., “Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups,” Journal of Eukaryotic Microbiology, vol. 56, no. 4, pp. 388–393, 2009.
[113]
S. Leelayoova, I. Subrungruang, Y. Suputtamongkol, J. Worapong, P. C. Petmitr, and M. Mungthin, “Identification of genotypes of Enterocytozoon bieneusi from stool samples from human immunodeficiency virus-infected patients in Thailand,” Journal of Clinical Microbiology, vol. 44, no. 8, pp. 3001–3004, 2006.
[114]
S. Leelayoova, P. Piyaraj, I. Subrungruang et al., “Genotypic characterization of Enterocytozoon bieneusi in specimens from pigs and humans in a pig farm community in central Thailand,” Journal of Clinical Microbiology, vol. 47, no. 5, pp. 1572–1574, 2009.
[115]
D. Stark, S. van Hal, J. Barratt, J. Ellis, D. Marriott, and J. Harkness, “Limited genetic diversity among genotypes of Enterocytozoon bieneusi strains isolated from HIV-infected patients from Sydney, Australia,” Journal of Medical Microbiology, vol. 58, no. 3, pp. 355–357, 2009.
[116]
N. Abe and I. Kimata, “Molecular survey of Enterocytozoon bieneusi in a Japanese porcine population,” Vector-Borne and Zoonotic Diseases, vol. 10, no. 4, pp. 425–427, 2010.
[117]
D. Ka?i?ková, B. Sak, M. Kvá?, and O. Ditrich, “Sources of potentially infectious human microsporidia: molecular characterisation of microsporidia isolates from exotic birds in the Czech Republic, prevalence study and importance of birds in epidemiology of the human microsporidial infections,” Veterinary Parasitology, vol. 165, no. 1-2, pp. 125–130, 2009.
[118]
L. V. Chalifoux, A. Carville, D. Pauley, B. Thompson, A. A. Lackner, and K. G. Mansfield, “Enterocytozoon bieneusi as a cause of proliferative serositis in simian immunodeficiency virus-infected immunodeficient macaques (Macaca mulatta),” Archives of Pathology and Laboratory Medicine, vol. 124, no. 10, pp. 1480–1484, 2000.
[119]
M. A. Buckholt, J. H. Lee, and S. Tzipori, “Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts,” Applied and Environmental Microbiology, vol. 68, no. 5, pp. 2595–2599, 2002.
[120]
D. K. Jeong, G. Y. Won, B. K. Park et al., “Occurrence and genotypic characteristics of Enterocytozoon bieneusi in pigs with diarrhea,” Parasitology Research, vol. 102, no. 1, pp. 123–128, 2007.
[121]
A. C. Breitenmoser, A. Mathis, E. Bürgi, R. Weber, and P. Deplazes, “High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans,” Parasitology, vol. 118, no. 5, pp. 447–453, 1999.
[122]
M. Santín, J. M. Trout, J. A. C. Vecino, J. P. Dubey, and R. Fayer, “Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates,” Veterinary Parasitology, vol. 141, no. 3-4, pp. 334–339, 2006.
[123]
M. Santín, J. A. Cortés Vecino, and R. Fayer, “Enterocytozoon bieneusi genotypes in dogs in Bogota, Colombia,” American Journal of Tropical Medicine and Hygiene, vol. 79, no. 2, pp. 215–217, 2008.
[124]
J. H. Lee, “Molecular detection of Enterocytozoon bieneusi and identification of a potentially human-pathogenic genotype in milk,” Applied and Environmental Microbiology, vol. 74, no. 5, pp. 1664–1666, 2008.
[125]
M. L. Lobo, L. Xiao, V. Cama, N. Magalh?es, F. Antunes, and O. Matos, “Identification of potentially human-pathogenic Enterocytozoon bieneusi genotypes in various birds,” Applied and Environmental Microbiology, vol. 72, no. 11, pp. 7380–7382, 2006.
[126]
M. Santín, J. M. Trout, and R. Fayer, “Enterocytozoon bieneusi genotypes in dairy cattle in the eastern United States,” Parasitology Research, vol. 97, no. 6, pp. 535–538, 2005.
[127]
B. Sak, M. Kvá?, D. Hanzlíková, and V. Cama, “First report of Enterocytozoon bieneusi infection on a pig farm in the Czech Republic,” Veterinary Parasitology, vol. 153, no. 3-4, pp. 220–224, 2008.
[128]
H. Rinder, A. Thomschke, B. Dengjel, R. Gothe, T. L?scher, and M. Zahler, “Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle,” Journal of Parasitology, vol. 86, no. 1, pp. 185–188, 2000.
[129]
J. H. Lee, “Prevalence and molecular characteristics of Enterocytozoon bieneusi in cattle in Korea,” Parasitology Research, vol. 101, no. 2, pp. 391–396, 2007.
[130]
R. Fayer, M. Santín, and J. M. Trout, “Enterocytozoon bieneusi in mature dairy cattle on farms in the eastern United States,” Parasitology Research, vol. 102, no. 1, pp. 15–20, 2007.
[131]
J. Reetz, H. Rinder, A. Thomschke, H. Manke, M. Schwebs, and A. Bruderek, “First detection of the microsporidium Enterocytozoon bieneusi in non-mammalian hosts (chickens),” International Journal for Parasitology, vol. 32, no. 7, pp. 785–787, 2002.
[132]
F. Izquierdo, J. A. Castro Hermida, S. Fenoy, M. Mezo, M. González-Warleta, and C. D. Aguila, “Detection of microsporidia in drinking water, wastewater and recreational rivers,” Water Research, vol. 45, no. 16, pp. 4837–4843, 2011.
[133]
S. Tzipori, A. Carville, G. Widmer, D. Kotler, K. Mansfield, and A. Lackner, “Transmission and establishment of a persistent infection of Enterocytozoon bieneusi, derived from a human with AIDS, in simian immunodeficiency virus-infected rhesus monkeys,” Journal of Infectious Diseases, vol. 175, no. 4, pp. 1016–1020, 1997.
[134]
L. Xiao, I. Sulaiman, V. Cama, R. H. Gilman, and C. Bern, “Molecular epidemiology of human microsporidiosis caused by Enterocytozoon bieneusi,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 35, no. 1, supplement, pp. 40–47, 2004.
[135]
G. Widmer and D. E. Akiyoshi, “Host-specific segregation of ribosomal nucleotide sequence diversity in the microsporidian Enterocytozoon bieneusi,” Infection, Genetics and Evolution, vol. 10, no. 1, pp. 122–128, 2010.
[136]
N. Henriques-Gil, M. Haro, F. Izquierdo, S. Fenoy, and C. D. águilat, “Phylogenetic approach to the variability of the microsporidian Enterocytozoon bieneusi and its implications for inter- and intrahost transmission,” Applied and Environmental Microbiology, vol. 76, no. 10, pp. 3333–3342, 2010.
[137]
Y. Feng, N. Li, T. Dearen et al., “Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi,” Applied and Environmental Microbiology, vol. 77, no. 14, pp. 4822–4828, 2011.
[138]
M. Santín and R. Fayer, “Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals,” Research in Veterinary Science, vol. 90, no. 3, pp. 363–371, 2011.
[139]
M. G. Müller, J. Kinne, R. K. Schuster, and J. Walochnik, “Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons,” Veterinary Parasitology, vol. 152, no. 1-2, pp. 67–78, 2008.
[140]
A. Carville, K. Mansfield, G. Widmer et al., “Development and application of genetic probes for detection of Enterocytozoon bieneusi in formalin-fixed stools and in intestinal biopsy specimens from infected patients,” Clinical and Diagnostic Laboratory Immunology, vol. 4, no. 4, pp. 405–408, 1997.