More than a rabbit's tale - Encephalitozoon spp. in wild mammals and birds
Status PubMed-not-MEDLINE Language English Country Great Britain, England Media electronic-ecollection
Document type Journal Article, Review
PubMed
28560162
PubMed Central
PMC5439460
DOI
10.1016/j.ijppaw.2016.01.001
PII: S2213-2244(16)30001-3
Knihovny.cz E-resources
- Keywords
- Encephalitozoon cuniculi, Encephalitozoon intestinalis, Encephalitzoon hellem, Genotype, Reservoir, Zoonosis,
- Publication type
- Journal Article MeSH
- Review MeSH
Within the microsporidian genus Encephalitozoon, three species, Encephalitozoon cuniculi, Encephalitozoon hellem and Encephalitozoon intestinalis have been described. Several orders of the Class Aves (Passeriformes, Psittaciformes, Apodiformes, Ciconiiformis, Gruiformes, Columbiformes, Suliformes, Podicipediformes, Anseriformes, Struthioniformes, Falconiformes) and of the Class Mammalia (Rodentia, Lagomorpha, Primates, Artyodactyla, Soricomorpha, Chiroptera, Carnivora) can become infected. Especially E. cuniculi has a very broad host range while E. hellem is mainly distributed amongst birds. E. intestinalis has so far been detected only sporadically in wild animals. Although genotyping allows the identification of strains with a certain host preference, recent studies have demonstrated that they have no strict host specificity. Accordingly, humans can become infected with any of the four strains of E. cuniculi as well as with E. hellem or E. intestinalis, the latter being the most common. Especially, but not exclusively, immunocompromised people are at risk. Environmental contamination with as well as direct transmission of Encephalitozoon is therefore highly relevant for public health. Moreover, endangered species might be threatened by the spread of pathogens into their habitats. In captivity, clinically overt and often fatal disease seems to occur frequently. In conclusion, Encephalitozoon appears to be common in wild warm-blooded animals and these hosts may present important reservoirs for environmental contamination and maintenance of the pathogens. Similar to domestic animals, asymptomatic infections seem to occur frequently but in captive wild animals severe disease has also been reported. Detailed investigations into the epidemiology and clinical relevance of these microsporidia will permit a full appraisal of their role as pathogens.
See more in PubMed
Abd El Wahab E.W., Easa S.M., Lotfi S.E., El Masry S.A., Kotkat A.M., Shatat H.Z. Risk factors associated with parasitic infection among municipality solid waste workers in an egyptian community. J. Parasitol. 2015 PubMed
Abu-Akkada S.S., Ashmawy K.I., Dweir A.W. First detection of an ignored parasite, Encephalitozoon cuniculi, in different animal hosts in Egypt. Parasitol. Res. 2015;114:843–850. PubMed
Åkerstedt J., Kapel C.M. Survey for Encephalitozoon cuniculi in arctic foxes (Alopex lagopus) in Greenland. J. Wildl. Dis. 2003;39:228–232. PubMed
Åkerstedt J., Nordstoga K., Mathis A., Smeds E., Deplazes 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. Pub. Health. 2002;49:400–405. PubMed
Anver M.N., King N.W., Hunt R.D. Congenital encephalitozoonosis in a squirrel monkey (Saimiri sciureus) Vet. Pathol. 1972;9:475–480. PubMed
Arnesen K., Nordstoga K. Ocular encephalitozoonosis (nosematosis) in blue foxes. polyarteritis nodosa and cataract. Acta Ophthalmol. (Copenh) 1977;55:641–651. PubMed
Asakura T., Nakamura S., Ohta M., Une Y., Furuya K. Genetically unique microsporidian Encephalitozoon cuniculi strain type III isolated from squirrel monkeys. Parasitol. Int. 2006;55:159–162. PubMed
Baneux P.J., Pognan F. In utero transmission of Encephalitozoon cuniculi strain type I in rabbits. Lab. Anim. 2003;37:132–138. PubMed
Bart A., Wentink-Bonnema E.M., Heddema E.R., Buijs J., van Gool T. Frequent occurrence of human-associated microsporidia in fecal droppings of urban pigeons in Amsterdam, the Netherlands. Appl. Environ. Microbiol. 2008;74:7056–7058. PubMed PMC
Barton C.E., Phalen D.N., Snowden K.F. Prevalence of microsporidian spores shed by asymptomatic lovebirds: evidence for a potential emerging zoonosis. J. Avian Med. Surg. 2003;17:197–202.
Bártová E., Marková J., Sedlak K. Prevalence of antibodies to Encephalitozoon cuniculi in European hares (Lepus europaeus) Ann. Agric. Environ. Med. 2015;22:674–676. PubMed
Begon M. Disease: health effects on humans, population effects on rodents. In: Singleton G.R., Hinds L.A., Krebs C.J., Spratt D.M., editors. Rats, Mice and People: Rodent Biology and Management. Australian Centre for International Agricultural Research; Canberra: 2003. pp. 13–19.
Benz P., Maass G., Csokai J., Fuchs-Baumgartinger A., Schwendenwein I., Tichy A., Nell B. Detection of Encephalitozoon cuniculi in the feline cataractous lens. Vet. Ophthalmol. 2011;14(Suppl. 1):37–47. PubMed
Bjerkas I., Nesland J.M. Brain and spinal cord lesions in encephalitozoonosis in the blue fox. Acta Vet. Scand. 1987;28:15–22. PubMed PMC
Black S.S., Steinohrt L.A., Bertucci D.C., Rogers L.B., Didier E.S. Encephalitozoon hellem in budgerigars (Melopsittacus undulatus) Vet. Pathol. 1997;34:189–198. PubMed
Bornay-Llinares F.J., da Silva A.J., Moura H., Schwartz D.A., Visvesvara G.S., Pieniazek N.J., Cruz-Lopez A., Hernandez-Jauregui P., Guerrero J., Enriquez F.J. Immunologic, microscopic, molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 1998;178:820–826. PubMed
Bose H.M., Woodhouse M.A., Powell R. Absence of Encephalitozoon cuniculi antibodies in wild rabbits in England. Vet. Rec. 2015;177:48. PubMed
Brown R.J., Hinkle D.K., Trevethan S.P., Kupper J.L., McKee A.E. Department of the Navy, Naval Aerospace Medical Institute, Naval Aerospace Medical Research Laboratory; 1972. Nosematosis in a Squirrel Monkey (Saimiri sciureus). First Reported Case; pp. 1–8.
Butel C., Mundeke S.A., Drakulovski P., Krasteva D., Ngole E.M., Mallie M., Delaporte E., Peeters M., Locatelli S. Assessment of infections with microsporidia and Cryptosporidium spp. in fecal samples from wild primate populations from Cameroon and Democratic Republic of Congo. Int. J. Primatol. 2015;36:227–243.
Calvo M., Carazo M., Arias M.L., Chaves C., Monge R., Chinchilla M. Prevalence of Cyclospora sp., Cryptosporidium sp, microsporidia and fecal coliform determination in fresh fruit and vegetables consumed in Costa Rica. Arch. Latinoam. Nutr. 2004;54:428–432. PubMed
Carlisle M.S., Snowden K., Gill J., Jones M., O'Donoghue P., Prociv P. Microsporidiosis in a Gouldian finch (Erythrura [chloebia] gouldiae) Aust. Vet. J. 2002;80:41–44. PubMed
Chalupský J., Vavra J., Gaudin J., Vanderwalle P., Arthur C.P., Guenezan M., Launay H. Mise en evidence serologique de la presence d'encephalitozoonose et de toxoplasmose chez le lapin de gareene (Oryctolagus cuniculus) en France. Bull. Soc. Franc Parasitol. 1990;8:91–95. Cited in: Mathis, A., Weber, R., Deplazes, P., 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 18, 423–445.
Childs-Sanford S.E., Garner M.M., Raymond J.T., Didier E.S., Kollias G.V. Disseminated microsporidiosis due to Encephalitozoon hellem in an Egyptian fruit bat (Rousettus aegyptiacus) J. Comp. Pathol. 2006;134:370–373. PubMed
Cotte L., Rabodonirina M., Chapuis F., Bailly F., Bissuel F., Raynal C., Gelas P., Persat F., Piens M.A., Trepo C. Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection. J. Infect. Dis. 1999;180:2003–2008. PubMed
Coupe S., Delabre K., Pouillot R., Houdart S., Santillana-Hayat M., Derouin F. Detection of Cryptosporidium, Giardia and Enterocytozoon bieneusi in surface water, including recreational areas: a one-year prospective study. FEMS Immunol. Med. Microbiol. 2006;47:351–359. PubMed
Cox J.C., Ross J. A serological survey of Encephalitozoon cuniculi infection in the wild rabbit in England and Scotland. Res. Vet. Sci. 1980;28:396. PubMed
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;26:260–265. PubMed
Cox J.C., Pye D., Edmonds J.W., Shepherd R. An investigation of Encephalitozoon cuniculi in the wild rabbit Oryctolagus cuniculus in Victoria, Australia. J. Hyg. (Lond) 1980;84:295–300. PubMed PMC
Cray C., Rivas Y. Seroprevalence of Encephalitozoon cuniculi in dogs in the United States. J. Parasitol. 2013;99:153–154. PubMed
Cutlip R.C., Beall C.W. Encephalitozoonosis in arctic lemmings. Lab. Anim. Sci. 1989;39:331–333. PubMed
Cutlip R.C., Dennis E.D. Retrospective study of diseases in a captive lemming colony. J. Wildl. Dis. 1993;29:620–622. PubMed
Dado D., Izquierdo F., Vera O., Montoya A., Mateo M., Fenoy S., Galvan A.L., Garcia S., Garcia A., Aranguez E., Lopez L., del Aguila C., Miro G. Detection of zoonotic intestinal parasites in public parks of Spain. Potential epidemiological role of microsporidia. Zoonoses Public. Health. 2012;59:23–28. PubMed
Danišová O., Valenčáková A., Stanko M., Luptáková L., Hasajová A. First report of Enterocytozoon bieneusi and Encephalitozoon intestinalis infection of wild mice in Slovakia. Ann. Agric. Environ. Med. 2015;22:251–252. PubMed
Davis M.R., Kinsel M., Wasson K., Boonstra J., Warneke M., Langan J.N. Fatal disseminated encephalitozoonosis in a captive, adult Goeldi's monkey (Callimico goeldii) and subsequent serosurvey of the exposed conspecifics. J. Zoo. Wildl. Med. 2008;39:221–227. PubMed
De Bosschere H., Wang Z., Orlandi P.A. First diagnosis of Encephalitozoon intestinalis and E. hellem in a European brown hare (Lepus europaeus) with kidney lesions. Zoonoses Public. Health. 2007;54:131–134. PubMed
Decraene V., Lebbad M., Botero-Kleiven S., Gustavsson A.M., Löfdahl M. First reported foodborne outbreak associated with microsporidia, Sweden, October 2009. Epidemiol. Infect. 2012;140:519–527. PubMed PMC
Deplazes P., Mathis A., Weber R. Epidemiology and zoonotic aspects of microsporidia of mammals and birds. Contrib. Microbiol. 2000;6:236–260. PubMed
Dickens M.J., Earle K.A., Romero L.M. Initial transference of wild birds to captivity alters stress physiology. Gen. Comp. Endocrinol. 2009;160:76–83. PubMed
Didier E.S. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop. 2005;94:61–76. PubMed
Didier E.S., Weiss L.M. Microsporidiosis: current status. Curr. Opin. Infect. Dis. 2006;19:485–492. PubMed PMC
Didier E.S., Weiss L.M. Microsporidiosis: not just in AIDS patients. Curr. Opin. Infect. Dis. 2011;24:490–495. PubMed PMC
Didier E.S., Stovall M.E., Green L.C., Brindley P.J., Sestak K., Didier P.J. Epidemiology of microsporidiosis: sources and modes of transmission. Vet. Parasitol. 2004;126:145–166. PubMed
Dowd S.E., Gerba C.P., Pepper I.L. Confirmation of the human-pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma corneae in water. Appl. Environ. Microbiol. 1998;64:3332–3335. PubMed PMC
Fournier S., Liguory O., Santillana-Hayat M., Guillot E., Sarfati C., Dumoutier N., Molina J., Derouin F. Detection of microsporidia in surface water: a one-year follow-up study. FEMS Immunol. Med. Microbiol. 2000;29:95–100. PubMed
Fuehrer H.P., Bloschl I., Siehs C., Hassl A. Detection of Toxoplasma gondii, Neospora caninum, Encephalitozoon cuniculi in the brains of common voles (Microtus arvalis) and water voles (Arvicola terrestris) by gene amplification techniques in western Austria (Vorarlberg) Parasitol. Res. 2010;107:469–473. PubMed
Galvan A., Magnet A., Izquierdo F., Fenoy S., Henriques-Gil N., del Aguila C. Variability in minimal genomes: analysis of tandem repeats in the microsporidia Encephalitozoon intestinalis. Infect. Genet. Evol. 2013;20:26–33. PubMed
Galvan-Diaz A.L., Magnet A., Fenoy S., Henriques-Gil N., Haro M., Gordo F.P., Miro G., del Aguila C., Izquierdo F. Microsporidia detection and genotyping study of human pathogenic E. bieneusi in animals from Spain. PLoS One. 2014;9:e92289. PubMed PMC
Garcia L.S. Laboratory identification of the microsporidia. J. Clin. Microbiol. 2002;40:1892–1901. PubMed PMC
Ghosh K., Weiss L.M. Molecular diagnostic tests for microsporidia. Interdiscip. Perspect. Infect. Dis. 2009:926521. PubMed PMC
Goodwin D., Gennari S.M., Howe D.K., Dubey J.P., Zajac A.M., Lindsay D.S. Prevalence of antibodies to Encephalitozoon cuniculi in horses from Brazil. Vet. Parasitol. 2006;142:380–382. PubMed
Graczyk T.K., Bosco-Nizeyi J., da Silva A.J., Moura I.N., Pieniazek N.J., Cranfield M.R., Lindquist H.D. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol. Res. 2002;88:926–931. PubMed
Graczyk T.K., Sunderland D., Rule A.M., da Silva A.J., Moura I.N., Tamang L., Girouard A.S., Schwab K.J., Breysse P.N. Urban feral pigeons (Columba livia) as a source for air- and waterborne contamination with Enterocytozoon bieneusi spores. Appl. Environ. Microbiol. 2007;73:4357–4358. PubMed PMC
Graczyk T.K., Majewska A.C., Schwab K.J. The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol. 2008;24:55–59. PubMed
Groves C.P. Order primates. In: Wilson D.E., Reeder D.M., editors. Mammal Species of the World: a Taxonomic and Geographic Reference. Johns Hopkins University Press; Baltimore: 2005. pp. 111–184.
Guo Y., Alderisio K.A., Yang W., Cama V., Feng Y., Xiao L. Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl. Environ. Microbiol. 2014;80:218–225. PubMed PMC
Guscetti F., Mathis A., Hatt J.M., Deplazes P. Overt fatal and chronic subclinical Encephalitozoon cuniculi microsporidiosis in a colony of captive emperor tamarins (Saguinus imperator) J. Med. Primatol. 2003;32:111–119. PubMed
Halánová M., Valenčáková A., Malčeková B., Kváč M., Sak B., Květoňová D., Bálent P., Čisláková L. Occurrence of microsporidia as emerging pathogens in Slovak Roma children and their impact on public health. Ann. Agric. Environ. Med. 2013;20:695–698. PubMed
Haro M., Del Aguila C., Fenoy S., Henriques-Gil N. Intraspecies genotype variability of the microsporidian parasite Encephalitozoon hellem. J. Clin. Microbiol. 2003;41:4166–4171. PubMed PMC
Haro M., Izquierdo F., Henriques-Gil N., res I., Alonso F., Fenoy S., del Aguila C. First detection and genotyping of human-associated microsporidia in pigeons from urban parks. Appl. Environ. Microbiol. 2005;71:3153–3157. PubMed PMC
Haro M., Del Aguila C., Fenoy S., Henriques-Gil N. Variability in infection efficiency in vitro of different strains of the microsporidian Encephalitozoon hellem. J. Eukaryot. Microbiol. 2006;53:46–48. PubMed
Haro M., Henriques-Gil N., Fenoy S., Izquierdo F., Alonso F., Del Aguila C. Detection and genotyping of Enterocytozoon bieneusi in pigeons. J. Eukaryot. Microbiol. 2006;53(Suppl. 1):S58–S60. PubMed
Hein J., Flock U., Sauter-Louis C., Hartmann K. Encephalitozoon cuniculi in rabbits in Germany: prevalence and sensitivity of antibody testing. Vet. Rec. 2014;174:350. PubMed
Henriksen P. The prevalence of encephalitozoonosis in danish farmed foxes. Nord. Vet. Med. 1986;38:167–172. PubMed
Hersteinsson P., Gunnarsson E., Hjartardóttir S., Skímisson K. Prevalence of Encephalitozoon cuniculi antibodies in terrestrial mammals in Iceland, 1986 to 1989. J. Wildl. Dis. 1993;29:341–344. PubMed
Hinney B., Nell B., Künzel F., Häbich A.C., Joachim A. 25th International Conference of the World Association for the Advancement of Veterinary Parasitology WAAVP 2015; AUG 16-20, 2015; Liverpool, UK. 2015. Encephalitozoonosis-more than a rabbit's parasitosis. 246-246.
Hocevar S.N., Paddock C.D., Spak C.W., Rosenblatt R., Diaz-Luna H., Castillo I., Luna S., Friedman G.C., Antony S., Stoddard R.A., Tiller R.V., Peterson T., Blau D.M., Sriram R.R., da Silva A., de Almeida M., Benedict T., Goldsmith C.S., Zaki S.R., Visvesvara G.S., Kuehnert M.J., Microsporidia Transplant Transmission Investigation Team Microsporidiosis acquired through solid organ transplantation: A public health investigation. Ann. Intern. Med. 2014;160:213–220. PubMed PMC
Hofmannová L., Sak B., Jekl V., Mináriková A., Skorič M., Kváč M. Lethal Encephalitozoon cuniculi genotype III infection in steppe lemmings (Lagurus lagurus) Vet. Parasitol. 2014;205:357–360. PubMed
Hutin Y.J., Sombardier M.N., Liguory O., Sarfati C., Derouin F., Modaï J., Molina J.M. Risk factors for intestinal microsporidiosis in patients with human immunodeficiency virus infection: a case-control study. J. Infect. Dis. 1998;178:904–907. PubMed
Hůrková L., Modrý D. PCR detection of Neospora caninum, Toxoplasma gondii and Encephalitozoon cuniculi in brains of wild carnivores. Vet. Parasitol. 2006;137:150–154. PubMed
Izquierdo F., Castro Hermida J.A., Fenoy S., Mezo M., González-Warleta M., del Aguila C. Detection of microsporidia in drinking water, wastewater and recreational rivers. Water Res. 2011;45:4837–4843. PubMed
Juan-Salles C., Garner M.M., Didier E.S., Serrato S., Acevedo L.D., Ramos-Vara J.A., Nordhausen R.W., Bowers L.C., Paras A. Disseminated encephalitozoonosis in captive, juvenile, cotton-top (Saguinus oedipus) and neonatal emperor (Saguinus imperator) tamarins in North America. Vet. Pathol. 2006;43:438–446. PubMed
Kašičková D., Sak B., Kváč M., Ditrich O. 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. Vet. Parasitol. 2009;165:125–130. PubMed
Keeble E.J., Shaw D.J. Seroprevalence of antibodies to Encephalitozoon cuniculi in domestic rabbits in the United Kingdom. Vet. Rec. 2006;158:539–544. PubMed
Kemp R.L., Kluge J.P. Encephalitozoon sp. in the blue-masked lovebird, Agapornis personata (reichenow): first confirmed report of microsporidan infection in birds. J. Protozool. 1975;22:489–491. PubMed
Kim K., Yoon S., Cheun H.I., Kim J.H., Sim S., Yu J.R. Detection of Encephalitozoon spp. from human diarrheal stool and farm soil samples in Korea. J. Korean Med. Sci. 2015;30:227–232. PubMed PMC
Kotler D.P., Orenstein J. Clinical syndromes associated with microsporidiosis. In: Wittner M., W. L., editors. The Microsporidia and Microsporidiosis. ASM Press; Washington D.C: 1999. pp. 258–292.
Künzel F., Joachim A. Encephalitozoonosis in rabbits. Parasitol. Res. 2010;106:299–309. PubMed
Künzel F., Peschke R., Tichy A., Joachim A. Comparison of an indirect fluorescent antibody test with Western blot for the detection of serum antibodies against Encephalitozoon cuniculi in cats. Parasitol. Res. 2014;113:4457–4462. PubMed
Lallo M.A., Calabria P., Bondan E.F., Milanelo L. Identification of Encephalitozoon and Enterocytozoon (microsporidia) spores in stool and urine samples obtained from free-living South American coatis (Nasua nasua) Appl. Environ. Microbiol. 2012;78:4490–4492. PubMed PMC
Lallo M.A., Calabria P., Milanelo L. Encephalitozoon and Enterocytozoon (microsporidia) spores in stool from pigeons and exotic birds: microsporidia spores in birds. Vet. Parasitol. 2012;190:418–422. PubMed
Lee S.Y., Lee S.S., Lyoo Y.S., Park H.M. DNA detection and genotypic identification of potentially human-pathogenic microsporidia from asymptomatic pet parrots in South Korea as a risk factor for zoonotic emergence. Appl. Environ. Microbiol. 2011;77:8442–8444. PubMed PMC
Levkutová M., Hípiková V., Faitelzon S., Benath G., Paulík S., Levkut M. Prevalence of antibodies to Encephalitozoon cuniculi in horses in the Israel. Ann. Agric. Environ. Med. 2004;11:265–267. PubMed
Li X., Palmer R., Trout J.M., Fayer R. Infectivity of microsporidia spores stored in water at environmental temperatures. J. Parasitol. 2003;89:185–188. PubMed
Lindsay D.S., Goodwin D.G., Zajac A.M., Cortes-Vecino J.A., Gennari S.M., Rosypal A.C., Dubey J.P. Serological survey for antibodies to Encephalitozoon cuniculi in ownerless dogs from urban areas of Brazil and Colombia. J. Parasitol. 2009;95:760–763. PubMed
Lobo M.L., Xiao L., Cama V., Magalhaes N., Antunes F., Matos O. Identification of potentially human-pathogenic Enterocytozoon bieneusi genotypes in various birds. Appl. Environ. Microbiol. 2006;72:7380–7382. PubMed PMC
Malčeková B., Halánová M., Sulínová Z., Molnár L., Ravaszová P., Adam J., Halán M., Valocký I., Baranovič M. Seroprevalence of antibodies to Encephalitozoon cuniculi and Encephalitozoon intestinalis in humans and animals. Res. Vet. Sci. 2010;89:358–361. PubMed
Malčeková B., Valenčáková A., Luptakova L., Molnár L., Ravaszová P., Novotny F. First detection and genotyping of Encephalitozoon cuniculi in a new host species, gyrfalcon (Falco rusticolus) Parasitol. Res. 2011;108:1479–1482. PubMed
Malčeková B., Valenčáková A., Molnár L., Kočišová A. First detection and genotyping of human-associated microsporidia in wild waterfowl of Slovakia. Acta Parasitol. 2013;58:13–17. PubMed
Martino P.E., Montenegro J.L., Preziosi J.A., Venturini C., Bacigalupe D., Stanchi N.O., Bautista E.L. Serological survey of selected pathogens of free-ranging foxes in Southern Argentina, 1998-2001. Rev. Sci. Tech. 2004;23:801–806. PubMed
Mathis A., Tanner I., Weber R., Deplazes P. Genetic and phenotypic intraspecific variation in the microsporidian Encephalitozoon hellem. Int. J. Parasitol. 1999;29:767–770. PubMed
Mathis A., Weber R., Deplazes P. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 2005;18:423–445. PubMed PMC
Mbaya A.W., Aliyu M.M., Ibrahim U.I. The clinico-pathology and mechanisms of trypanosomosis in captive and free-living wild animals: a review. Vet. Res. Commun. 2009;33:793–809. PubMed
McCully R.M., Van Dellen A.F., Basson P.A., Lawrence J. Observations on the pathology of canine microsporidiosis. Onderstepoort J. Vet. Res. 1978;45:75–91. PubMed
Meng X., Zheng J., He X., Jia H., Zhang Y. First characterization in china of Encephalitozoon cuniculi in the blue fox (Alopex lagopus) J. Eukaryot. Microbiol. 2014;61:580–585. PubMed
Meredith A.L., Cleaveland S.C., Brown J., Mahajan A., Shaw D.J. Seroprevalence of Encephalitozoon cuniculi in wild rodents, foxes and domestic cats in three sites in the United Kingdom. Transbound. Emerg. Dis. 2015;62:148–156. PubMed
Mohn S.F. Encephalitozoonosis in the blue fox. comparison between the india-ink immuno-reaction and the indirect fluorescent antibody test in detecting Encephalitozoon cuniculi antibodies. Acta Vet. Scand. 1982;23:99–106. PubMed PMC
Mossallam S.F. Detection of some intestinal protozoa in commercial fresh juices. J. Egypt. Soc. Parasitol. 2010;40:135–149. PubMed
Muller-Doblies U.U., Herzog K., Tanner I., Mathis A., Deplazes P. First isolation and characterisation of Encephalitozoon cuniculi from a free-ranging rat (Rattus norvegicus) Vet. Parasitol. 2002;107:279–285. PubMed
Murphy T.M., Walochnik J., Hassl A., Moriarty J., Mooney J., Toolan D., Sanchez-Miguel C., O'Loughlin A., McAuliffe A. Study on the prevalence of Toxoplasma gondii and Neospora caninum and molecular evidence of Encephalitozoon cuniculi and Encephalitozoon (Septata) intestinalis infections in red foxes (Vulpes vulpes) in rural Ireland. Vet. Parasitol. 2007;146:227–234. PubMed
Musser G., Carleton M. Superfamily Muroidea. In: Wilson D., Reeder D., editors. Mammal Species of the World. Smithsonian Institution Press; Washington, D.C: 2005.
Nell B., Fuchs-Baumgartinger A., Fritsche J., Borer-Germann S., Thyssen C., Hoffmann I., Hinney B. Annual Scientific Meeting of the European College of Veterinary Ophthalmologists, London, UK, May 15–18, 2014. vol. 6. 2014. Distribution of Encephalitozoon cuniculi infections in the cat resulting in ophthlmological symptoms in Europe; p. E24. (Veterinary Ophthalmol.).
Nell B., Csokai J., Fuchs-Baumgartinger A., Maass G. Encephalitozoon cuniculi causes focal anterior cataract and uveitis in dogs. Tierarztl. Prax. Ausg. K. Kleintiere Heimtiere. 2015;43:337–344. PubMed
Nelson J.B. Experimental transmission of a murine microsporidian in Swiss mice. J. Bacteriol. 1967;94:1340–1345. PubMed PMC
Němejc K., Sak B., Květoňová D., Hanzal V., Janiszewski P., Forejtek P., Rajský D., Kotková M., Ravaszová P., McEvoy J., Kváč M. Prevalence and diversity of Encephalitozoon spp. and Enterocytozoon bieneusi in wild boars (Sus scrofa) in central Europe. Parasitol. Res. 2014;113:761–767. PubMed
Persin M., Dousek J. Encephalitozoonosis in farm-bred arctic blue foxes (Alopex lagopus) Vet. Med. (Praha) 1986;31:49–54. PubMed
Phalen D.N., Logan K.S., Snowden K.F. Encephalitozoon hellem infection as the cause of a unilateral chronic keratoconjunctivitis in an umbrella cockatoo (Cacatua alba) Vet. Ophthalmol. 2006;9:59–63. PubMed
Pirestani M., Sadraei J., Forouzandeh M. Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tehran. Iran. Infect. Genet. Evol. 2013;20:495–499. PubMed
Poonacha K.B., William P.D., Stamper R.D. Encephalitozoonosis in a parrot. J. Am. Vet. Med. Assoc. 1985;186:700–702. PubMed
Pulparampil N., Graham D., Phalen D., Snowden K. Encephalitozoon hellem in two Eclectus parrots (Eclectus roratus): Identification from archival tissues. J. Eukaryot. Microbiol. 1998;45:651–655. PubMed
Reetz J. Natural transmission of microsporidia (Encephalitozoon cuniculi) by way of the chicken egg. Tierarztl. Prax. 1994;22:147–150. PubMed
Reetz J., Wiedemann M., Aue A., Wittstatt U., Ochs A., Thomschke A., Manke H., Schwebs M., Rinder H. Disseminated lethal Encephalitozoon cuniculi (genotype III) infections in cotton-top tamarins (Oedipomidas oedipus)–a case report. Parasitol. Int. 2004;53:29–34. PubMed
Ribeiro M.F., Guimaraes A.M. Encephalitozoon-like microsporidia in the ticks amblyomma cajennense and anocentor nitens (acari: Ixodidae) J. Med. Entomol. 1998;35:1029–1033. PubMed
Rinder H. Transmission of microsporidia to humans: water-borne, food-borne, air-borne, zoonotic, or anthroponotic? Southeast Asian J. Trop. Med. Public Health. 2004;35:54–57.
Sak B., Kašičková D., Kváč M., Květoňová D., Ditrich O. Microsporidia in exotic birds: intermittent spore excretion of Encephalitozoon spp. in naturally infected budgerigars (Melopsittacus undulatus) Vet. Parasitol. 2010;168:196–200. PubMed
Sak B., Kváč M., Květoňová D., Albrecht T., Piálek J. The first report on natural Enterocytozoon bieneusi and Encephalitozoon spp. infections in wild east-European house mice (Mus musculus musculus) and west-European house mice (M. m. domesticus) in a hybrid zone across the Czech Republic-Germany border. Vet. Parasitol. 2011;178:246–250. PubMed
Sak B., Kváč M., Petrzelková K., Květoňová D., Pomajbíková K., Mulama M., Kiyang J., Modrý D. Diversity of microsporidia (fungi: microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission? Folia. Parasitol. (Praha) 2011;58:81–86. PubMed
Sak B., Petrželková K.J., Květoňová D., Mynářová A., Shutt K.A., Pomajbíková K., Kalousova B., Modrý D., Benavides J., Todd A., Kváč M. Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga sangha protected areas, Central African Republic. PLoS One. 2013;8:e71840. PubMed PMC
Sak B., Petrželková K.J., Květoňová D., Mynářová A., Pomajbíková K., Modrý D., Cranfield M.R., Mudakikwa A., Kváč M. Diversity of microsporidia, Cryptosporidium and Giardia in mountain gorillas (Gorilla beringei beringei) in volcanoes national park, Rwanda. PLoS One. 2014;9:e109751. PubMed PMC
Sasaki M., Yamazaki A., Haraguchi A., Tatsumi M., Ishida K., Ikadai H. Serological survey of Encephalitozoon cuniculi infection in japanese dogs. J. Parasitol. 2011;97:167–169. PubMed
Scurrell E.J., Holding E., Hopper J., Denk D., Fuchs-Baumgartinger A., Silbermayr K., Nell B. Bilateral lenticular Encephalitozoon cuniculi infection in a snow leopard (panthera uncia) Vet. Ophthalmol. 2015;18(Suppl. 1):143–147. PubMed
Seguel M., Howerth E.W., Ritter J., Paredes E., Colegrove K., Gottdenker N. encephalitozoonosis in 2 South American fur seal (Arctocephalus australis) pups. Vet. Pathol. 2015;52:720–723. PubMed PMC
Seibold H.R., Fussell E.N. Intestinal microsporidiosis in Callicebus moloch. Lab. Anim. Sci. 1973;23:115–118. PubMed
Selman M., Sak B., Kváč M., Farinelli L., Weiss L.M., Corradi N. Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi. Eukaryot. Cell. 2013;12:496–502. PubMed PMC
Shadduck J.A., Watson W.T., Pakes S.P., Cali A. Animal infectivity of Encephalitozoon cuniculi. J. Parasitol. 1979;65:123–129. PubMed
Sinski E. Environmental contamination with protozoan parasite infective stages: biology and risk assessment. Acta Microbiol. Pol. 2003;52(Suppl. l):97–107. PubMed
Snowden K., Logan K. Molecular identification of Encephalitozoon hellem in an ostrich. Avian Dis. 1999;43:779–782. PubMed
Snowden K.F., Logan K., Phalen D.N. Isolation and characterization of an avian isolate of Encephalitozoon hellem. Parasitology. 2000;121(Pt 1):9–14. PubMed
Snowden K., Daft B., Nordhausen R.W. Morphological and molecular characterization of Encephalitozoon hellem in hummingbirds. Avian Pathol. 2001;30:251–255. PubMed
Snowden K.F., Lewis B.C., Hoffman J., Mansell J. Encephalitozoon cuniculi infections in dogs: a case series. J. Am. Anim. Hosp. Assoc. 2009;45:225–231. PubMed
Sokolova O.I., Demyanov A.V., Bowers L.C., Didier E.S., Yakovlev A.V., Skarlato S.O., Sokolova Y.Y. Emerging microsporidian infections in russian HIV-infected patients. J. Clin. Microbiol. 2011;49:2102–2108. PubMed PMC
Suter C., Mathis A., Hoop R., Deplazes P. Encephalitozoon hellem infection in a yellow-streaked lory (Chalcopsitta scintillata) imported from Indonesia. Vet. Rec. 1998;143:694–695. PubMed
Słodkowicz-Kowalska A. Animal reservoirs of human virulent microsporidian species. Wiad. Parazytol. 2009;55:63–65. PubMed
Słodkowicz-Kowalska A., Graczyk T.K., Tamang L., Jedrzejewski S., Nowosad A., Zduniak P., Solarczyk P., Girouard A.S., Majewska A.C. Microsporidian species known to infect humans are present in aquatic birds: implications for transmission via water? Appl. Environ. Microbiol. 2006;72:4540–4544. PubMed PMC
Słodkowicz-Kowalska A., Majewska A.C., Trzesowska E., Skrzypczak L. Occurrence of Encephalitozoon intestinalis in the red ruffed lemur (Varecia rubra) and the ring-tailed lemur (Lemur catta) housed in the Poznan zoological garden, Poland. Ann. Parasitol. 2012;58:49–52. PubMed
Talabani H., Sarfati C., Pillebout E., van Gool T., Derouin F., Menotti J. Disseminated infection with a new genovar of Encephalitozoon cuniculi in a renal transplant recipient. J. Clin. Microbiol. 2010;48:2651–2653. PubMed PMC
Thomas C., Finn M., Twigg L., Deplazes P., Thompson R.C. Microsporidia (Encephalitozoon cuniculi) in wild rabbits in Australia. Aust. Vet. J. 1997;75:808–810. PubMed
Thompson R.C. Parasite zoonoses and wildlife: one health, spillover and human activity. Int. J. Parasitol. 2013;43:1079–1088. PubMed PMC
Tsukada R., Tsuchiyama A., Sasaki M., Park C.H., Fujii Y., Takesue M., Hatai H., Kudo N., Ikadai H. Encephalitozoon infections in rodentia and Soricomorpha in japan. Vet. Parasitol. 2013;198:193–196. PubMed
Tumwine J.K., Kekitiinwa A., Bakeera-Kitaka S., Ndeezi G., Downing R., Feng X., Akiyoshi D.E., Tzipori S. Cryptosporidiosis and microsporidiosis in ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am. J. Trop. Med. Hyg. 2005;73:921–925. PubMed
Valenčáková A., Balent P., Húska M., Novotný F., Luptáková L. First report on Encephalitozoon intestinalis infection of swine in Europe. Acta Vet. Hung. 2006;54:407–411. PubMed
Van Heerden J., Bainbridge N., Burroughs R.E., Kriek N.P. Distemper-like disease and encephalitozoonosis in wild dogs (Lycaon pictus) J. Wildl. Dis. 1989;25:70–75. PubMed
Wagnerová P., Sak B., Květoňová D., Buňatová Z., Civišová H., Maršálek M., Kváč M. Enterocytozoon bieneusi and Encephalitozoon cuniculi in horses kept under different management systems in the Czech Republic. Vet. Parasitol. 2012;190:573–577. PubMed
Wasson K., Peper R.L. Mammalian microsporidiosis. Vet. Pathol. 2000;37:113–128. PubMed
Wilson J.M. Encephalitozoon cuniculi in wild european rabbits and a fox. Res. Vet. Sci. 1979;26:114. Cited in: Mathis, A., Weber, R., Deplazes, P., 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 18, 423–445. PubMed
Wobester G., Schuh J.C. Microsporidal encephalitis in muskrats. J. Wildl. Dis. 1979;15:413–417. PubMed
Xiao L., Li L., Moura H., Sulaiman I., Lal A.A., Gatti S., Scaglia M., Didier E.S., Visvesvara G.S. Genotyping Encephalitozoon hellem isolates by analysis of the polar tube protein gene. J. Clin. Microbiol. 2001;39:2191–2196. PubMed PMC
Yabsley M.J., Jordan C.N., Mitchell S.M., Norton T.M., Lindsay D.S. Seroprevalence of Toxoplasma gondii, Sarcocystis neurona, Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, GA, USA. Vet. Parasitol. 2007;144:28–32. PubMed
Zanet S., Palese V., Trisciuoglio A., Canton Alonso C., Ferroglio E. Encephalitozoon cuniculi, Toxoplasma gondii and Neospora caninum infection in invasive eastern cottontail rabbits Sylvilagus floridanus in northwestern Italy. Vet. Parasitol. 2013;197:682–684. PubMed
Zeman D.H., Baskin G.B. Encephalitozoonosis in squirrel monkeys (Saimiri sciureus) Vet. Pathol. 1985;22:24–31. PubMed
Tick-borne microsporidiosis: ticks as a neglected source of human microsporidian infections?
Biosurveillance of Selected Pathogens with Zoonotic Potential in a Zoo