Microsporidia – Emergent Pathogens in the Global Food Chain
2016; Elsevier BV; Volume: 32; Issue: 4 Linguagem: Inglês
10.1016/j.pt.2015.12.004
ISSN1471-5007
AutoresGrant D. Stentiford, James J. Becnel, Louis M. Weiss, Patrick J. Keeling, Elizabeth S. Didier, Ben Williams, S. Bjørnson, ML Kent, Mark Freeman, Mark J. F. Brown, Emily R. Troemel, Kristina Roesel, Yuliya Y. Sokolova, Karen F. Snowden, Leellen F. Solter,
Tópico(s)Plant and Fungal Interactions Research
ResumoMicrosporidiosis is an emerging disease in hosts from aquatic and terrestrial biomes. Human infections are often derived from contact with animals and the environment. Common nodes of immune suppression allow opportunistic infection and disease. The animal–human food chain provides a portal for transmission and emergence. Intensification of food production has the potential to drive increased disease prevalence in food plants and animals. Microsporidia are diversely distributed, opportunistic, and density-dependent parasites infecting hosts from almost all known animal taxa. They are frequent in highly managed aquatic and terrestrial hosts, many of which are vulnerable to epizootics, and all of which are crucial for the stability of the animal–human food chain. Mass rearing and changes in global climate may exacerbate disease and more efficient transmission of parasites in stressed or immune-deficient hosts. Further, human microsporidiosis appears to be adventitious and primarily associated with an increasing community of immune-deficient individuals. Taken together, strong evidence exists for an increasing prevalence of microsporidiosis in animals and humans, and for sharing of pathogens across hosts and biomes. Intensification of food production has the potential to drive increased disease prevalence in food plants and animals. Microsporidia are diversely distributed, opportunistic, and density-dependent parasites infecting hosts from almost all known animal taxa. They are frequent in highly managed aquatic and terrestrial hosts, many of which are vulnerable to epizootics, and all of which are crucial for the stability of the animal–human food chain. Mass rearing and changes in global climate may exacerbate disease and more efficient transmission of parasites in stressed or immune-deficient hosts. Further, human microsporidiosis appears to be adventitious and primarily associated with an increasing community of immune-deficient individuals. Taken together, strong evidence exists for an increasing prevalence of microsporidiosis in animals and humans, and for sharing of pathogens across hosts and biomes. In high-income countries, approximately 70% of deaths in people over the age of 70 result from non-communicable or chronic conditions. In low-income countries almost 40% of deaths occur in children under the age of 15 and are generally associated with infectious diseases (e.g., HIV/AIDS, malaria, diarrhea, and tuberculosis). Many of these deaths are caused by pathogens transmitted via food and water supplies [1Gajadhar A.A. et al.Overview of food- and water-borne zoonotic parasites at the farm level.Rev. Sci. Tech. 2006; 25: 595-606Crossref PubMed Google Scholar]. Human food originating from both plants and animals is produced, processed, and marketed in intricately linked systems of primary producers (e.g., corn, cattle, fish), input and service providers (i.e., pesticides, water, veterinary drugs), transporters, processors, wholesalers, retailers, consumers, and end-users of byproducts (e.g., manure). Foodborne diseases comprise a broad range of illnesses caused by ingestion of pathogens, parasites, chemical contaminants, and biotoxins that are either naturally present in food or can contaminate food at different points in the production and preparation process [2WHO First formal meeting of the Foodborne Disease Burden Epidemiology Reference Group (FERG): Implementing Strategy, Setting Priorities and Assigning the Tasks. World Health Organization, 2007Google Scholar]. Many of the 300 species of helminths and over 70 species of protists known to infect humans are transmitted via food and water [3Doyle M.E. Foodborne Parasites. A Review of the Scientific Literature. Food Research Institute, University of Wisconsin–Madison, 2003Google Scholar]. Infectious life stages are acquired by ingesting tissues of infected mammals, fish, or invertebrates, as well as from contaminated food and water supplies or via contaminated fomites or fingers. Although traditionally associated with tropical outbreaks, perceptions of risk in temperate regions are changing following large outbreaks of parasitic infections due to agents such as Toxoplasma gondii [4Centers For Disease Control and Prevention CDC Estimates of Foodborne Illness in the United States. CDC 2011 Estimates: Findings. CDC, 2011Google Scholar] and Cryptosporidium spp. [5MacKenzie W.R. et al.A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply.N. Engl. J. Med. 1994; 331: 161-167Crossref PubMed Scopus (1349) Google Scholar]. Globalized food trade and travel clearly have the potential to increase the risk of imported parasitoses from tropical countries [6Simarro P.P. et al.Human African trypanosomiasis in non-endemic countries (2000 –2010).J. Travel Med. 2012; 19: 44-53Crossref PubMed Scopus (0) Google Scholar]. Microsporidia, although not currently considered to be priority foodborne parasites, have the potential to enter the human food chain through waterborne and foodborne routes, and via exposure to the environment. As such, natural hosts of human infective microsporidia can be part of the human food chain (e.g., [7Slifko T.R. et al.Emerging parasite zoonoses associated with water and food.Int. J. Parasitol. 2000; 30: 1379-1393Crossref PubMed Scopus (0) Google Scholar, 8Sak B. et al.First report of Enterocytozoon bieneusi infection on a pig farm in the Czech Republic.Vet. Parasitol. 2008; 153: 220-224Crossref PubMed Scopus (0) Google Scholar]). In this review we consider members of the phylum Microsporidia as agents of emergent disease in hosts from major global biomes and food production sectors (terrestrial, aquatic) and in human consumers. Further, we combine phylogenetic, ecological and immunological perspectives to propose unifying themes, under a 'One Health' banner, which may explain the emergence of these opportunists. Microsporidia are a hyper-diverse phylum of spore-forming parasites infecting hosts from all major animal taxa in all global biomes (Box 1). The array of hosts is equally diverse, ranging from protists (in some of which Microsporidia are hyperparasites) to vertebrates including humans. Species in almost half the known microsporidian genera infect aquatic hosts, and thousands of these pathogens remain undescribed [9Stentiford G.D. et al.Microsporidia: diverse, dynamic and emergent pathogens in aquatic systems.Trends Parasitol. 2013; 29: 567-578Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Morphological approaches to within-phylum taxonomy have generally been superseded (or at least augmented) by sequence comparisons of the ribosomal rRNA genes (e.g., [10Vossbrinck C.R. Debrunner-Vossbrinck B.A. Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations.Folia Parasitol. 2005; 52: 131-142Crossref PubMed Google Scholar, 11Stentiford G.D. et al.Plastic parasites: extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia.Int. J. Parasitol. 2013; 43: 339-352Crossref PubMed Scopus (0) Google Scholar]). Debate over placement of the Microsporidia within the tree of life has progressed from historical grouping with spore-forming parasites to the current molecular phylogenetics-based view that they are affiliated with the fungi [12Cavalier-Smith T. A 6-kingdom classification and a unified phylogeny.in: Schenk H.E.A. Schwemmler W.S. Endocytobiology II: Intracellular Space as Oligogenetic. Walter de Gruyter, 1983: 1027-1034Google Scholar, 13Keeling P.J. Five things to know about Microsporidia.PLoS Pathog. 2009; 5: e1000489Crossref PubMed Scopus (0) Google Scholar]. Analysis of the first complete microsporidian genome (Encephalitozoon cuniculi) [14Katinka M.D. et al.Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.Nature. 2001; 414: 450-453Crossref PubMed Scopus (690) Google Scholar] confirmed that the previous phylogenies showing a deeper position, and which suggested that the microsporidia were an ancient primitive lineage, was an artifact of long branch attraction [15Thomarat F. et al.Phylogenetic analysis of the complete genome sequence of Encephalitozoon cuniculi supports the fungal origin of microsporidia and reveals a high frequency of fast-evolving genes.J. Mol. Evol. 2004; 59: 780-791Crossref PubMed Scopus (98) Google Scholar], a finding supported by the discovery of highly reduced mitochondria (mitosomes) within the microsporidian cytoplasm [16Williams B.A. et al.A mitochondrial remnant in the microsporidian Trachipleistophora hominis.Nature. 2002; 418: 865-869Crossref PubMed Scopus (280) Google Scholar]. While more recent confirmation of a fungal relationship is now accepted by most, their specific relationships and their branching either within the Fungi (e.g., [17Gill E.E. Fast N.M. Assessing the microsporidia-fungi relationship: Combined phylogenetic analysis of eight genes.Gene. 2006; 375: 103-109Crossref PubMed Scopus (0) Google Scholar]) or outside the group [18Tanabe Y. et al.Are Microsporidia really related to Fungi? A reappraisal based on additional gene sequences from basal fungi.Mycol. Res. 2002; 106: 1380-1391Crossref Scopus (0) Google Scholar, 19Capella-Gutierrez S. et al.Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi.BMC Biol. 2012; 10: 47Crossref PubMed Scopus (0) Google Scholar] are a topic of further debate. Although phylogenetic comparison of known taxa from within the Microsporidia or the Fungi has failed to resolve this issue, the recent discovery (and phylogenetic placement) of three novel lineages, the Cryptomycota [20Jones M.D. et al.Discovery of novel intermediate forms redefines the fungal tree of life.Nature. 2011; 474: 200-203Crossref PubMed Scopus (182) Google Scholar, 21Jones M.D. et al.Validation and justification of the phylum name Cryptomycota phyl. nov.IMA Fungus. 2011; 2: 173-175Crossref PubMed Google Scholar], the aphelids [22Karpov S.A. et al.Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia.Front. Microbiol. 2014; 5: 112Crossref PubMed Scopus (0) Google Scholar, 23Karpov S.A. et al.Obligately phagotrophic aphelids turned out to branch with the earliest-diverging Fungi.Protist. 2013; 164: 195-205Crossref PubMed Scopus (0) Google Scholar], and the genus Mitosporidium [24Haag K.L. et al.Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites.Proc. Natl. Acad. Sci. U.S.A. 2014; 111: 15480-15485Crossref PubMed Scopus (0) Google Scholar] as intermediate between Fungi and the rest of the eukaryotes has re-ignited interest. The Cryptomycota appear to branch at the base of the Fungi and contain the Microsporidia as well as the aforementioned aphelids and Mitosporidium. Discovery of the group is clarifying relationships between the Microsporidia, parasites with intermediate characteristics (such as Mitosporidium), and all other eukaryotes, at the same time revealing how their peculiar infection machinery likely evolved [25Keeling P.J. Phylogenetic place of Microsporidia in the tree of eukaryotes.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 195-202Crossref Scopus (1) Google Scholar].Box 1Microsporidia Form and FunctionMicrosporidia are single-celled, eukaryotic, spore-forming parasites, and both generalist and specialist species are found in invertebrate and vertebrate hosts. There are two main clades of microsporidia: the typical (or advanced) and atypical (or primitive) microsporidia [94Vávra J. Larsson J.I.R. Structure of microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 1-70Crossref Scopus (0) Google Scholar]. The atypical microsporidia are a small group composed of approximately 13 genera and 42 species [95Larsson J.I.R. The primitive microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 605-634Crossref Scopus (1) Google Scholar]. The majority of known microsporidia are of the typical variety, with ∼190 genera and an estimated 1300–1500 species [28Vavra J. Lukes J. Microsporidia and 'the art of living together'.Adv. Parasitol. 2013; 82: 254-319Google Scholar]. This group contains the opportunistic taxa that have simple to complex developmental sequences and life cycles. Spores of the typical microsporidia contain one or two nuclei (the diplokaryon), are most commonly oval or pyriform in shape, and average 2–8 microns in size, but can be as small as 1 micron or as large as 30 microns in length. The spore has a very complex structure that contains the extrusion apparatus for infecting the host cell. The spore wall is composed of two layers: an electron-lucent endospore layer that contains chitin, and an electron-dense exospore that is often layered. The unique infection apparatus is composed of three main parts: a long, thread-like polar filament, a multilayered polaroplast, which is a highly membranous structure that occupies the anterior half of the spore, and a posterior vacuole (Figure I). When the spore is in the appropriate host and environment, the spore germinates and the polar filament is everted to become a hollow tube. The sporoplasm travels through this tube and is inoculated into the cytoplasm of the host cell to begin replication [94Vávra J. Larsson J.I.R. Structure of microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 1-70Crossref Scopus (0) Google Scholar, 96Cali A. Takvorian P. Developmental morphology and life cycles of the microsporidia.in: Weiss L.M. Becnel J.J. Pathogens of Opportunity. Wiley-Blackwell, 2014: 71-133Crossref Google Scholar]. Generalist species of microsporidia have a broad host-range and the ability to infect both invertebrate and vertebrate hosts [28Vavra J. Lukes J. Microsporidia and 'the art of living together'.Adv. Parasitol. 2013; 82: 254-319Google Scholar]. Generalists are often responsible for opportunistic infections in vertebrates. Some notable genera containing species capable of infecting and developing in both arthropod and vertebrate hosts are Anncaliia, Tubulinosema, Trachipleistophora, and Encephalitozoon, although other genera have been implicated by molecular data with species in arthropod and vertebrate hosts (e.g., Enterocytozoon, Endoreticulatus) [29Didier E.S. Khan I.A. The immunology of microsporidiosis in mammals.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 307-325Crossref Google Scholar]. Specialists are restricted to infecting and developing within a narrow range of closely related hosts, or some species require an obligate two-host system with a definitive host and intermediate host (e.g., Amblyospora). Microsporidia are single-celled, eukaryotic, spore-forming parasites, and both generalist and specialist species are found in invertebrate and vertebrate hosts. There are two main clades of microsporidia: the typical (or advanced) and atypical (or primitive) microsporidia [94Vávra J. Larsson J.I.R. Structure of microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 1-70Crossref Scopus (0) Google Scholar]. The atypical microsporidia are a small group composed of approximately 13 genera and 42 species [95Larsson J.I.R. The primitive microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 605-634Crossref Scopus (1) Google Scholar]. The majority of known microsporidia are of the typical variety, with ∼190 genera and an estimated 1300–1500 species [28Vavra J. Lukes J. Microsporidia and 'the art of living together'.Adv. Parasitol. 2013; 82: 254-319Google Scholar]. This group contains the opportunistic taxa that have simple to complex developmental sequences and life cycles. Spores of the typical microsporidia contain one or two nuclei (the diplokaryon), are most commonly oval or pyriform in shape, and average 2–8 microns in size, but can be as small as 1 micron or as large as 30 microns in length. The spore has a very complex structure that contains the extrusion apparatus for infecting the host cell. The spore wall is composed of two layers: an electron-lucent endospore layer that contains chitin, and an electron-dense exospore that is often layered. The unique infection apparatus is composed of three main parts: a long, thread-like polar filament, a multilayered polaroplast, which is a highly membranous structure that occupies the anterior half of the spore, and a posterior vacuole (Figure I). When the spore is in the appropriate host and environment, the spore germinates and the polar filament is everted to become a hollow tube. The sporoplasm travels through this tube and is inoculated into the cytoplasm of the host cell to begin replication [94Vávra J. Larsson J.I.R. Structure of microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 1-70Crossref Scopus (0) Google Scholar, 96Cali A. Takvorian P. Developmental morphology and life cycles of the microsporidia.in: Weiss L.M. Becnel J.J. Pathogens of Opportunity. Wiley-Blackwell, 2014: 71-133Crossref Google Scholar]. Generalist species of microsporidia have a broad host-range and the ability to infect both invertebrate and vertebrate hosts [28Vavra J. Lukes J. Microsporidia and 'the art of living together'.Adv. Parasitol. 2013; 82: 254-319Google Scholar]. Generalists are often responsible for opportunistic infections in vertebrates. Some notable genera containing species capable of infecting and developing in both arthropod and vertebrate hosts are Anncaliia, Tubulinosema, Trachipleistophora, and Encephalitozoon, although other genera have been implicated by molecular data with species in arthropod and vertebrate hosts (e.g., Enterocytozoon, Endoreticulatus) [29Didier E.S. Khan I.A. The immunology of microsporidiosis in mammals.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 307-325Crossref Google Scholar]. Specialists are restricted to infecting and developing within a narrow range of closely related hosts, or some species require an obligate two-host system with a definitive host and intermediate host (e.g., Amblyospora). Based on the descriptive criteria defined by the International Committee of Zoological Nomenclature (ICZN), the phylum Microsporidia currently comprises over 200 genera [26Becnel J.J. et al.Checklist of available generic names for microsporidia with type species and type hosts.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 671-686Crossref Google Scholar]. Phylogenetic analysis (based upon small subunit rRNA partial gene sequence) of 70 of these genera reveals five apparent clades broadly classified into three major groups according to predominant host and environment type, termed the Aquasporidia (clades 1 and 3), the Terresporidia (clades 2 and 4), and the Marinosporidia (clade 5) [27Vossbrinck C.R. et al.Phylogeny of the Microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 203-220Crossref Scopus (0) Google Scholar]. It is noteworthy that most of these clades contain exceptions, likely associated with either the pathogen or even the host switching to a new habitat. Host-switching may be more likely if the microsporidian parasite is a generalist or where hosts move between habitats (e.g., freshwater to marine, or freshwater to terrestrial). In the case of confirmed human-infecting taxa, representatives are observed across the phylum and include the genera Enterocytozoon, Encephalitozoon, and Vittaforma (clade 4, Terresporidia), Anncalia and Tubulinosema (clade 3, Aquasporidia), and Pleistophora (clade 5, Marinosporidia) [27Vossbrinck C.R. et al.Phylogeny of the Microsporidia.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 203-220Crossref Scopus (0) Google Scholar]. Although not inconceivable that Homo sapiens serves as a type host for particular microsporidian taxa, given the spread of human-infecting genera across known clades and the preponderance for infection to occur in immune-compromised patients (see below), it is perhaps more likely that these infections represents zoonotic transfer from hosts inhabiting terrestrial, freshwater, and marine environments. Transfer in this case may relate to direct exposure to type host taxa (e.g., via the food chain) but also by contact with extra-host parasite life-stages in the environment in which they reside. In this respect, the potential for susceptibility of humans to infection by other Microsporidia across the phylum appears to be significant. In nature, microsporidia typically develop a balanced interaction with their host, leading to long-term subclinical infections [28Vavra J. Lukes J. Microsporidia and 'the art of living together'.Adv. Parasitol. 2013; 82: 254-319Google Scholar]. When the immune condition of the host is compromised, infection can lead to overt signs of clinical disease, highlighting the key role of immune competence in mitigating individual- and population-level health effects of microsporidiosis [29Didier E.S. Khan I.A. The immunology of microsporidiosis in mammals.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 307-325Crossref Google Scholar]. Human immune deficiencies can be categorized into primary and secondary types. Primary immune deficiencies (PID) are derived from intrinsic and inherited defects in the immune system. Although PID cases are rare (an estimated 250 000 cases are currently diagnosed in the USA) (Immune Deficiency Foundation; http://primaryimmune.org/about/), microsporidian infections have been occasionally reported in PID patients [30Bednarska M. et al.Occurrence of intestinal microsporidia in immunodeficient patients in Poland.Ann. Agric. Environ. Med. 2014; 21: 244-248Crossref PubMed Google Scholar]. More common are secondary immune deficiencies (SID) which are acquired from an array of causes including chemotherapy and/or radiation treatments for malignancies, immune-suppressive therapies (to prevent transplant rejection), malnutrition, poor sanitation, aging, and infectious diseases such as HIV/AIDS (www.uptodate.com/contents/secondary-immunodeficiency-due-to-underlying-disease-states-environmental-exposures-and-miscellaneous-causes). Prior to the HIV/AIDS pandemic in the mid-1980s, microsporidiosis was rarely reported in human patients [31Sprague V. Nosema connori n. sp., a microsporidian parasite of man.Trans. Am. Microscop. Soc. 1974; 93: 400-403Crossref PubMed Google Scholar]. The pandemic brought to light the opportunistic capability of microsporidia to infect humans and produce disease in virtually all organs [32Desportes I. et al.Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS.J. Protozool. 1985; 32: 250-254Crossref PubMed Google Scholar, 33Orenstein J.M. et al.Disseminated microsporidiosis in AIDS: are any organs spared?.AIDS. 1997; 11: 385-386Crossref PubMed Scopus (0) Google Scholar] (Figure 1). Before common use of anti-retroviral therapies, microsporidiosis was reported in at least 15% (and up to 85%) of HIV/AIDS patients [34Fayer R. Santin-Duran M. Epidemiology of microsporidia in human infections.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 135-164Crossref Scopus (3) Google Scholar]. However, although prevalence declined with improved therapy, an increase in newly diagnosed cases of HIV in people over 50 years of age, coupled with an aging population of patients living with HIV, is leading to so-called HIV-associated non-AIDS (HANA) conditions that accelerate the onset of diseases normally observed in the elderly. These patients show accelerated immune senescence, leaving them susceptible to opportunistic infections, including microsporidia. Reactivation of latent microsporidian infections with age, or with subsequent use of chemotherapy or immune-suppressive treatments, has also been reported [35Sak B. et al.Latent microsporidial infection in immunocompetent individuals – a longitudinal study.PLoS Negl. Trop. Dis. 2011; 5: e1162Crossref PubMed Scopus (0) Google Scholar]. Although at least ten microsporidian genera have been associated with human patients (Table 1), the most frequently detected species is the gut-infecting Enterocytozoon bieneusi in patients with HIV/AIDS, in whom it produces chronic diarrhea [32Desportes I. et al.Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS.J. Protozool. 1985; 32: 250-254Crossref PubMed Google Scholar] (Box 2).Table 1Confirmed Infections of Humans by Members of the Phylum MicrosporidiaConditions of Immune-Deficiency or Immune-SuppressionRefsTaxonHIVTransplantCancerOther Conditions and Risk FactorsAnncaliia (syn. Nosema, Brachiola) algeraeN/raN/r – not recorded.KidneyYesRheumatoid arthritis, ocular infection, steroids, Crohn's disease, diabetes97Cali A. et al.Human vocal cord infection with the microsporidium Anncaliia algerae.J. Eukaryot. Microbiol. 2010; 57: 562-567Crossref PubMed Scopus (22) Google Scholar, 98Watts M.R. et al.Anncaliia algerae microsporidial myositis.Emerg. Infect. Dis. 2014; 20: 185-191Crossref PubMed Scopus (0) Google ScholarAnncaliia (syn. Nosema) connoriN/rN/rN/rAthymic child99Franzen C. et al.Transfer of the members of the genus Brachiola (microsporidia) to the genus Anncaliia based on ultrastructural and molecular data.J. Eukaryot. Microbiol. 2006; 53: 26-35Crossref PubMed Scopus (0) Google Scholar, 100Margileth A.M. et al.Disseminated nosematosis in an immunologically compromised infant.Arch. Pathol. 1973; 95: 145-150PubMed Google ScholarAnncaliia (syn. Brachiola) vesicularumYesN/rN/rN/r99Franzen C. et al.Transfer of the members of the genus Brachiola (microsporidia) to the genus Anncaliia based on ultrastructural and molecular data.J. Eukaryot. Microbiol. 2006; 53: 26-35Crossref PubMed Scopus (0) Google Scholar, 101Cali A. et al.Brachiola vesicularum, n. g., n. sp., a new microsporidium associated with AIDS and myositis.J. Eukaryot. Microbiol. 1998; 45: 240-251Crossref PubMed Google ScholarEncephalitozoon cuniculiYesKidney, bone marrowYesChildren, Primary Immune Deficiency, diabetes, heart disease, ocular infection, steroids29Didier E.S. Khan I.A. The immunology of microsporidiosis in mammals.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 307-325Crossref Google Scholar, 35Sak B. et al.Latent microsporidial infection in immunocompetent individuals – a longitudinal study.PLoS Negl. Trop. Dis. 2011; 5: e1162Crossref PubMed Scopus (0) Google Scholar, 102Hocevar S.N. et al.Microsporidiosis acquired through solid organ transplantation: a public health investigation.Ann. Intern. Med. 2014; 160: 213-220Crossref PubMed Scopus (0) Google Scholar, 103Norhayati M. et al.A preliminary study on the prevalence of intestinal microsporidiosis in patients with and without gastrointestinal symptoms in Malaysia.Trans. R. Soc. Trop. Med. Hyg. 2008; 102: 1274-1278Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 104Orenstein J.M. et al.Fatal pulmonary microsporidiosis due to Encephalitozoon cuniculi following allogeneic bone marrow transplantation for acute myelogenous leukemia.Ultrastruct. Pathol. 2005; 29: 269-276Crossref PubMed Scopus (37) Google Scholar, 105Sharma S. et al.Microsporidial keratitis: need for increased awareness.Surv. Ophthalmol. 2011; 56: 1-22Abstract Full Text Full Text PDF PubMed Scopus (0) Google ScholarEncephalitozoon hellemYesN/rYesOcular infection, steroids106Chabchoub N. et al.Genetic identification of intestinal microsporidia species in immunocompromised patients in Tunisia.Am. J. Trop. Med. Hyg. 2009; 80: 24-27PubMed Google Scholar, 107Didier E.S. et al.Isolation and characterization of a new human microsporidian, Encephalitozoon hellem (n. sp.), from three AIDS patients with keratoconjunctivitis.J. Infect. Dis. 1991; 163: 617-621Crossref PubMed Google Scholar, 108Sharma S. et al.Ocular microsporidiosis.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 403-419Crossref Google ScholarEncephalitozoon intestinalisYesBone marrowYesChildren, ocular infection, steroids29Didier E.S. Khan I.A. The immunology of microsporidiosis in mammals.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 307-325Crossref Google Scholar, 106Chabchoub N. et al.Genetic identification of intestinal microsporidia species in immunocompromised patients in Tunisia.Am. J. Trop. Med. Hyg. 2009; 80: 24-27PubMed Google Scholar, 108Sharma S. et al.Ocular microsporidiosis.in: Weiss L. Becnel J.J. Microsporidia: Pathogens of Opportunity. John Wiley & Sons, 2014: 403-419Crossref Google Scholar, 109Cali A. et al.Septata intestinalis n. g., n. sp., an intestinal microsporidian associated with chronic diarrhea and dissemination in AIDS patients.J. Eukaryot. Microbiol. 1993; 40: 101-112Crossref PubMed Google Scholar, 110Hamamci B. et al.Prevalence of Encephalitozoon intestinalis and Enterocytozoon bieneusi in cancer patients under chemotherapy.Mikrobiyol. Bul. 2015; 49: 105-113Crossref PubMed Google Scholar, 111Jimenez-Gonzalez G.B. et al.Microsporidia in pediatric patients with leukemia or limphoma.Rev. Invest. Clin. 2012; 64: 25-31PubMed Google Scholar, 112Orenstein J.M. et al
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