Occurrence of zoonotic Enterocytozoon bieneusi in cats in Brazil

Ocorrência de Enterocytozoon bieneusi zoonótico em gatos no Brasil

Jamille Batista Faria Prado Carlos Alberto do Nascimento Ramos Vagner Ricardo da Silva Fiuza Veronica Jorge Babo Terra About the authors

Abstract

Enterocytozoon bieneusi is an opportunistic intestinal pathogen that infects humans and a wide variety of animals worldwide. Our aim in this study was to investigate the occurrence of E. bieneusi in a domestic cat population in Campo Grande, Mato Grosso do Sul, Brazil. Sixty fecal samples from diarrheic cats were subjected to polymerase chain reaction (PCR) and the amplicons were sequenced for identification. E. bieneusi was detected in two samples (3.3%), both identified as genotype D. This genotype has already been reported in animals and humans and is considered a zoonotic genotype. Our findings represent the first report of E. bieneusi in domestic cats in Brazil, reinforcing the importance of identifying this agent as a source of infection in animals and humans.

Keywords:
Microsporidia; zoonosis; felines; diagnosis; PCR

Resumo

Enterocytozoon bieneusi é um patógeno intestinal oportunista que infecta humanos e uma variedade de animais em todo o mundo. O objetivo no presente estudo foi investigar a ocorrência de E. bieneusi em uma população de gatos domésticos em Campo Grande, Mato Grosso do Sul, Brasil. Sessenta amostras fecais de gatos diarréicos foram submetidas a reação em cadeia da polimerase (PCR) e os produtos de amplificação foram sequenciados para identificação molecular. E. bieneusi foi detectado em duas amostras (3,3%), ambos identificados como genótipo D. Esse genótipo tem sido relatado em animais e humanos e é considerado um genótipo zoonótico. Nossos resultados representam a primeira descrição de E. bieneusi em gatos domésticos no Brasil, reforçando a importância desse agente como fonte de infecção para animais e humanos.

Palavras-chave:
Microsporídeo; zoonose; felinos; diagnóstico; PCR

Introduction

Microsporidia are obligate intracellular fungi. Currently between 1300 and 1500 different species have already been described, infecting a wide variety of invertebrate and vertebrate hosts, including humans ( VÁVRA & LUKEŠ, 2013 Vávra J, Lukeš J. Microsporidia and ‘The Art of Living Together’. In: Rollinson D. Advances in parasitology. United States of America: Academic Press; 2013. p. 253-319. ; SANTÍN, 2015 Santín M. Enterocytozoon bieneusi. In: Xiao L, Ryan U, Feng Y. Biology of foodborne parasites. United States of America: CRC Press; 2015. p. 149-174. ). However, only 17 species are known to be pathogenic to humans, among which Enterocytozoon bieneusi is considered the most common disease-causing species ( FAYER & SANTÍN, 2014 Fayer R, Santín M. Epidemiology of Microsporidia in human infections. In: Weiss LM, Becnel JJ. Microsporidia: pathogens of opportunity. 1st ed. Hoboken: John Wiley & Sons, Inc. 2014. p. 135-164. http://dx.doi.org/10.1002/9781118395264.ch3.
http://dx.doi.org/10.1002/9781118395264...
; MATHIS et al., 2005 Mathis A, Weber R, Deplazes P. Zoonotic potential of the microsporidia. Clin Microbiol Rev 2005; 18(3): 423-445. http://dx.doi.org/10.1128/CMR.18.3.423-445.2005. PMid:16020683.
http://dx.doi.org/10.1128/CMR.18.3.423-...
). It is an opportunistic pathogen, which infects mainly immunocompromised individuals whose CD4+ cell counts are lower than 100 cels/mm3 ( ESPERN et al., 2007 Espern A, Morio F, Miegeville M, Illa H, Abdoulaye M, Meyssonnier V, 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. J Clin Microbiol 2007; 45(9): 2999-3002. http://dx.doi.org/10.1128/JCM.00684-07. PMid:17634305.
http://dx.doi.org/10.1128/JCM.00684-07 ...
), causing clinical signs of chronic diarrhea associated with abdominal pain, fever and weight loss ( AKINBO et al., 2012 Akinbo FO, Omoregie R, Xiao L, Dearen T, Leon ET, Okaka CE. Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. Am J Trop Med Hyg 2012; 86(3): 441-445. http://dx.doi.org/10.4269/ajtmh.2012.11-0548. PMid:22403314.
http://dx.doi.org/10.4269/ajtmh.2012.11...
; BRASIL et al., 2000 Brasil P, Lima DB, Paiva DD, Lobo MS, Sodré FC, Silva SP, et al. Clinical and diagnostic aspects of intestinal microsporidiosis in HIV-infected patients with chronic diarrhea in Rio de Janeiro, Brazil. Rev Inst Med Trop São Paulo 2000; 42(6): 299-304. http://dx.doi.org/10.1590/S0036-46652000000600001. PMid:11136515.
http://dx.doi.org/10.1590/S0036-4665200...
). Transmission occurs through the fecal-oral route by the accidental ingestion of spores eliminated within feces from infected animals or humans or by the ingestion of contaminated water and/or food ( SANTÍN, 2015 Santín M. Enterocytozoon bieneusi. In: Xiao L, Ryan U, Feng Y. Biology of foodborne parasites. United States of America: CRC Press; 2015. p. 149-174. ).

E. bieneusi was first identified in 1985 in enterocytes from an HIV positive human ( DESPORTES et al., 1985 Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, 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(2): 250-254. http://dx.doi.org/10.1111/j.1550-7408.1985.tb03046.x. PMid:4009510.
http://dx.doi.org/10.1111/j.1550-7408.1...
). In animals, E. bieneusi was first reported in pig feces in 1996 ( DEPLAZES et al., 1996 Deplazes P, Mathis A, Muller C, Weber R. Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J Eukaryot Microbiol 1996; 43(5): 93S. http://dx.doi.org/10.1111/j.1550-7408.1996.tb05018.x. PMid:8822883.
http://dx.doi.org/10.1111/j.1550-7408.1...
), and since then it has been detected in the feces and intestinal tissue of 236 different animal species ( MATHIS et al., 2005 Mathis A, Weber R, Deplazes P. Zoonotic potential of the microsporidia. Clin Microbiol Rev 2005; 18(3): 423-445. http://dx.doi.org/10.1128/CMR.18.3.423-445.2005. PMid:16020683.
http://dx.doi.org/10.1128/CMR.18.3.423-...
; SANTÍN & FAYER, 2011 Santín M, Fayer R. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci 2011; 90(3): 363-371. http://dx.doi.org/10.1016/j.rvsc.2010.07.014. PMid:20699192.
http://dx.doi.org/10.1016/j.rvsc.2010.0...
; WANG et al., 2018 Wang SS, Wang RJ, Fan XC, Liu TL, Zhang LX, Zhao GH. Prevalence and genotypes of Enterocytozoon bieneusi in China. Acta Trop 2018; 183: 142-152. http://dx.doi.org/10.1016/j.actatropica.2018.04.017. PMid:29660311.
http://dx.doi.org/10.1016/j.actatropica...
). Information about the occurrence of E. bieneusi in cats is scanty; a few studies have been conducted in Asian and European countries, and a single study in South America. Most of these studies have identified zoonotic E. bieneusi genotypes, which includes cats as dispersing agents and a potential source of infection in humans. Given the absence of studies on E. bieneusi in cats in Brazil, the purpose of our research was to investigate the occurrence of E. bieneusi in diarrheic domestic cats in the city of Campo Grande, state of Mato Grosso do Sul, mid west Brazil.

Material and Methods

Samples

This study was approved by the Ethics Committee on Animal Use of the Federal University of Mato Grosso do Sul (Protocol no. 787/2016).

Fecal samples from 60 diarrheic cats were carefully collected from the ground immediately after defecation, between September 2016 and May 2017. The fecal samples were collected in private residences and veterinary clinics. The cats ages varied from 45 days to 17 years old. All the samples (approximately 8 grams each) were placed in clean containers and immediately sent for processing at the laboratory of molecular biology at veterinary hospital facilities. Aliquots of the samples (approximately 1g) were transferred to 1.5 mL polypropylene tubes containing 500 μL of 0.9% sterile saline solution, and stored at -20 °C until DNA extraction. The classification of feces as diarrheic was based on a scoring system presented by Queen et al. (2012) Queen EV, Marks SL, Farver TB. Prevalence of Selected bacterial and parasitic agents in feces from diarrheic and healthy control cats from Northern California. J Vet Intern Med 2012; 26(1): 54-60. http://dx.doi.org/10.1111/j.1939-1676.2011.00843.x. PMid:22182203.
http://dx.doi.org/10.1111/j.1939-1676.2...
, in which score 1 was considered very firm, score 2 was considered well-formed, score 3 was considered soft-formed, and score 4 was considered watery. Only specimens with scores 3 or 4 were included in the diarrheic group.

DNA extraction

Three hundred microliters of the fecal suspensions stored in microtubes were centrifuged (10,000 x g for 10 minutes). After discarding the supernatant, the pellet was suspended in 500 μL of 20% SDS (Sodium Dodecyl Sulfate), and 10 μL of Proteinase K (20 mg/mL) were added. The suspension was homogenized in a vortex mixer and incubated at 65 °C for 10 minutes. Then, 400 μL of chloroform was added and the suspension was vortexed again, after which 300 μL of protein precipitation solution (5M potassium acetate, 11% glacial acetic acid) was added. The microtubes were centrifuged (10,000 x g for 10 minutes) and the supernatant transferred to a new 1.5 mL microtube. One mL of ethanol was then added for DNA precipitation. After another centrifugation step (10,000 x g for 5 minutes), the supernatant was discarded and the pellet washed with 1 mL of 70% ethanol. The samples were centrifuged for 2 min (10,000 x g ), and the pellets were allowed to dry at room temperature. Then, 100 μL of nuclease free water was added for DNA elution. An analysis of the material in an BioPhotometer Plus spectrophotometer (Eppendorf) indicated that all the samples showed a DNA concentration equal to or greater than 25 ng/μL and a ratio of 260/280nm equal to or greater than 1.75.

PCR and sequencing

The molecular identification of E. bieneusi was performed using a nested protocol, as described by Buckholt et al. (2002) Buckholt MA, Lee JH, Tzipori S. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 2002; 68(5): 2595-2599. http://dx.doi.org/10.1128/AEM.68.5.2595-2599.2002. PMid:11976142.
http://dx.doi.org/10.1128/AEM.68.5.2595...
. The primers for the first PCR were EBITS3 (5' GGT CAT AGG GAT GAA GAG 3') and EBITS4 (5' TCG AGT TCT TTC GCG CTC 3'). The second reaction was performed with the primers EBITS1 (5' GCT CTG AAT ATC TAT GGC T 3') and EBITS2.4 (5' ATC GCC GAC GGA TCC AAG TG 3'), amplifying a 392bp DNA fragment comprising part of the internal transcribed spacer (ITS) region of the E. bieneusi rRNA gene. Reactions were performed in a final volume of 25 μL containing 1.5 mM MgCl2, 50 mM KCl, 20 mM Tris-HCl (pH 9.0), 0.2 mM dNTPs, 1 μM of each primer, and 2.5 U of Taq DNA polymerase (Ludwig Biotec). The conditions for the first reaction was 94 °C for 3 min, followed by 35 cycles of denaturation at 94 °C for 30s, annealing at 57 °C for 30s, and extension at 72 °C for 40s, followed by a final extension at 72 °C for 10 min. The procedure for the second reaction was similar to the first, except the annealing temperature (55 °C), and the number of PCR cycles (30 cycles). E. bieneusi positive controls obtained from cattle from a previous study conducted in Brazil (FIUZA et al., 2016b Fiuza VRS, Lopes CW, Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 2016b; 216: 46-51. http://dx.doi.org/10.1016/j.vetpar.2015.12.008. PMid:26801594.
http://dx.doi.org/10.1016/j.vetpar.2015...
), as well as negative controls (ultra-pure water), were included in all the reactions.

Amplification products were visualized in agarose gel (2%) stained with GelRed® (Biotium) under ultraviolet light after gel electrophoresis. Positive samples were purified using CleanSweep® PCR Purification (Applied Biosystems), following the manufacturer’s protocol, and were sequenced in both directions by the Sanger method ( SANGER et al., 1977 Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977; 74(12): 5463-5467. http://dx.doi.org/10.1073/pnas.74.12.5463. PMid:271968.
http://dx.doi.org/10.1073/pnas.74.12.54...
). The resulting sequences were aligned with reference sequences downloaded from GenBank using the MEGA v. 7 program ( KUMAR et al., 2016 Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33(7): 1870-1874. http://dx.doi.org/10.1093/molbev/msw054. PMid:27004904.
http://dx.doi.org/10.1093/molbev/msw054...
) for genotype identification.

Results

Positive E. bieneusi PCR amplifications were observed in 2 (3.3%) of the 60 fecal samples. The samples came from a 3-month-old and a 5-year-old cat living in two different households. Both PCR products were successfully purified and sequenced, and presented 100% similarity with genotype D. The nucleotide sequences obtained in the present study were deposited in the GenBank database under accession nos. MH161409 and MH161410.

Discussion

This is the first report of presence of E. bieneusi in domestic cats in Brazil. Indeed, E. bieneusi was previously identified through PCR in feces from cats in Asia: China ( KARIM et al., 2014a Karim MR, Dong H, Yu F, Jian F, Zhang L, Wang R, et al. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J Clin Microbiol 2014a; 52(9): 3297-3302. http://dx.doi.org/10.1128/JCM.01352-14. PMid:24989604.
http://dx.doi.org/10.1128/JCM.01352-14 ...
; LI et al., 2015 Li W, Li Y, Song M, Lu Y, Yang J, Tao W, et al. Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Vet Parasitol 2015; 208(3-4): 125-134. http://dx.doi.org/10.1016/j.vetpar.2015.01.014. PMid:25665462.
http://dx.doi.org/10.1016/j.vetpar.2015...
; XU et al., 2016b Xu H, Jin Y, Wu W, Li P, Wang L, Li N, et al. Genotypes of Cryptosporidium spp., Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai, China. Parasit Vectors 2016b; 9(1): 121. http://dx.doi.org/10.1186/s13071-016-1409-5. PMid:26932267.
http://dx.doi.org/10.1186/s13071-016-14...
), Japan ( ABE et al., 2009 Abe N, Kimata I, Iseki M. Molecular evidence of Enterocytozoon bieneusi in Japan. J Vet Med Sci 2009; 71(2): 217-219. http://dx.doi.org/10.1292/jvms.71.217. PMid:19262036.
http://dx.doi.org/10.1292/jvms.71.217 ...
), Iran ( JAMSHIDI et al., 2012 Jamshidi S, Tabrizi AS, Bahrami M, Momtaz H. Microsporidia in household dogs and cats in Iran; a zoonotic concern. Vet Parasitol 2012; 185(2-4): 121-123. http://dx.doi.org/10.1016/j.vetpar.2011.10.002. PMid:22035849.
http://dx.doi.org/10.1016/j.vetpar.2011...
) and Thailand ( MORI et al., 2013 Mori H, Mahittikorn A, Thammasonthijarern N, Chaisiri K, Rojekittikhun W, Sukthana Y. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Vet Parasitol 2013; 197(3-4): 696-701. http://dx.doi.org/10.1016/j.vetpar.2013.07.025. PMid:23932454.
http://dx.doi.org/10.1016/j.vetpar.2013...
); Europe: Germany ( DENGJEL et al., 2001 Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke A, et al. Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol 2001; 39(12): 4495-4499. http://dx.doi.org/10.1128/JCM.39.12.4495-4499.2001. PMid:11724868.
http://dx.doi.org/10.1128/JCM.39.12.449...
), Switzerland ( MATHIS et al., 1999 Mathis A, Breitenmoser AC, Deplazes P. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite 1999; 6(2): 189-193. http://dx.doi.org/10.1051/parasite/1999062189. PMid:10416194.
http://dx.doi.org/10.1051/parasite/1999...
), Portugal ( LOBO et al., 2006 Lobo ML, Xiao L, Cama V, Stevens T, Antunes F, Matos O. Genotypes of Enterocytozoon bieneusi in mammals in Portugal. J Eukaryot Microbiol 2006;53(s1 Suppl 1): S61-S64. http://dx.doi.org/10.1111/j.1550-7408.2006.00174.x. PMid:17169069.
http://dx.doi.org/10.1111/j.1550-7408.2...
) and Poland ( PIEKARSKA et al., 2017 Piekarska J, Kicia M, Wesołowska M, Kopacz Ż, Gorczykowski M, Szczepankiewicz B, et al. Zoonotic microsporidia in dogs and cats in Poland. Vet Parasitol 2017; 246: 108-111. http://dx.doi.org/10.1016/j.vetpar.2017.09.011. PMid:28969771.
http://dx.doi.org/10.1016/j.vetpar.2017...
); and in South America: Colombia ( SANTÍN et al., 2006 Santín M, Trout JM, Vecino JAC, Dubey JP, Fayer R. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol 2006; 141(3-4): 334-339. http://dx.doi.org/10.1016/j.vetpar.2006.06.004. PMid:16860480.
http://dx.doi.org/10.1016/j.vetpar.2006...
), with prevalence rates varying from 5 to 31.3% in studies involving 40 or more samples. The prevalence rate found in this study was 3.3%. In a study conducted in South America ( SANTÍN et al., 2006 Santín M, Trout JM, Vecino JAC, Dubey JP, Fayer R. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol 2006; 141(3-4): 334-339. http://dx.doi.org/10.1016/j.vetpar.2006.06.004. PMid:16860480.
http://dx.doi.org/10.1016/j.vetpar.2006...
), 46 cats from 15 days to 10 years of age were euthanized in Colombia and fecal samples were collected directly from the rectum and ileum; eight (17%) animals were considered E. bieneusi positive after molecular analysis.

E. bieneusi DNA has already been identified in fecal samples in Brazil collected from humans ( FENG et al., 2011 Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, et al. Development of a multilocus sequence typing tool for High-Resolution Genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 2011; 77(14): 4822-4828. http://dx.doi.org/10.1128/AEM.02803-10. PMid:21622791.
http://dx.doi.org/10.1128/AEM.02803-10 ...
), cattle (FIUZA et al., 2016b Fiuza VRS, Lopes CW, Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 2016b; 216: 46-51. http://dx.doi.org/10.1016/j.vetpar.2015.12.008. PMid:26801594.
http://dx.doi.org/10.1016/j.vetpar.2015...
), birds (CUNHA et al., 2016 Cunha MJ, Cury MC, Santín M. Widespread presence of human-pathogenic Enterocytozoon bieneusi genotypes in chickens. Vet Parasitol 2016; 217: 108-112. http://dx.doi.org/10.1016/j.vetpar.2015.12.019. PMid:26827870.
http://dx.doi.org/10.1016/j.vetpar.2015...
, 2017 Cunha MJR, Cury MC, Santín M. Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res 2017; 116(2): 487-493. http://dx.doi.org/10.1007/s00436-016-5309-6. PMid:27815734.
http://dx.doi.org/10.1007/s00436-016-53...
; LALLO et al., 2012 Lallo MA, Calabria P, Milanelo L. Encephalitozoon and Enterocytozoon (microsporidia) spores in stool from pigeons and exotic birds: microsporidia spores in birds. Vet Parasitol 2012; 190(3-4): 418-422. http://dx.doi.org/10.1016/j.vetpar.2012.06.030. PMid:22853863.
http://dx.doi.org/10.1016/j.vetpar.2012...
), pigs ( FIUZA et al., 2015 Fiuza VRS, Oliveira FCR, Fayer R, Santín M. First report of Enterocytozoon bieneusi in pigs in Brazil. Parasitol Int 2015; 64(4): 18-23. http://dx.doi.org/10.1016/j.parint.2015.01.002. PMid:25582928.
http://dx.doi.org/10.1016/j.parint.2015...
) and sheep (FIUZA et al., 2016a Fiuza VRS, Lopes CWG, Cosendey RIJ, Oliveira FCR, Fayer R, Santín M. Zoonotic Enterocytozoon bieneusi genotypes found in brazilian sheep. Res Vet Sci 2016a; 107: 196-201. http://dx.doi.org/10.1016/j.rvsc.2016.06.006. PMid:27473995.
http://dx.doi.org/10.1016/j.rvsc.2016.0...
). In addition, microsporidium was also detected in a sample of treated effluent water collected in the region of Campinas, São Paulo, demonstrating the significant possibility of dispersion of this agent even after sewage treatment ( YAMASHIRO et al., 2017 Yamashiro S, Fiuza VRS, Teixeira ÂTLS, Branco N, Levy CE, Castro ICVS, et al. Enterocytozoon bieneusi detected by molecular methods in raw sewage and treated effluent from a combined system in Brazil. Mem Inst Oswaldo Cruz 2017; 112(6): 403-410. http://dx.doi.org/10.1590/0074-02760160435. PMid:28591400.
http://dx.doi.org/10.1590/0074-02760160...
). However, epidemiologic factors and the occurrence of clinical disease in the country are still uncertain and need further clarification.

No clinical symptomatology has been associated with domestic animals in Brazil. In the state of Rio de Janeiro, Fiuza et al. (2016b) Fiuza VRS, Lopes CW, Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 2016b; 216: 46-51. http://dx.doi.org/10.1016/j.vetpar.2015.12.008. PMid:26801594.
http://dx.doi.org/10.1016/j.vetpar.2015...
compared the feces consistency and body condition score of cattle of different age groups, but were unable to correlate the parameters with the occurrence of E. bieneusi.

In this study, all the fecal samples collected from cats were diarrheic. However, due to the low prevalence rate and the non-comprehensive diagnosis of other parasitic, bacterial and viral etiological agents wich are expected to cause diarrhea, we could not correlate the presence of E. bieneusi with this clinical manifestation. Similarly, Dengjel et al. (2001) Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke A, et al. Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol 2001; 39(12): 4495-4499. http://dx.doi.org/10.1128/JCM.39.12.4495-4499.2001. PMid:11724868.
http://dx.doi.org/10.1128/JCM.39.12.449...
, who analyzed fecal samples from 60 diarrheic cats in Germany, found only three samples positive for E. bieneusi. Piekarska et al. (2017) Piekarska J, Kicia M, Wesołowska M, Kopacz Ż, Gorczykowski M, Szczepankiewicz B, et al. Zoonotic microsporidia in dogs and cats in Poland. Vet Parasitol 2017; 246: 108-111. http://dx.doi.org/10.1016/j.vetpar.2017.09.011. PMid:28969771.
http://dx.doi.org/10.1016/j.vetpar.2017...
analyzed fecal samples from 44 domestic cats (nine diarrheic) in Poland and found four E. bieneusi positive samples, only one of which was diarrheic. None of these studies was able to correlate the presence of E. bieneusi DNA with diarrhea in the cats.

E. bieneusi genotyping contributes as an essential information to a better knowledge on this microorganism, indicating both possible species-specific genotypes as well as those already found in more than one animal species. Genotypes found in humans and animals are considered zoonotic, even when clinical disease is not evident. The presence of DNA of this organism in feces suggests the presence of infection and the possibility of spore dissemination through feces.

Among more than 200 known E. bieneusi genotypes, 12 are considered specific to cats ( Table 1 ), whereas two others have been reported in cats and other animals ( Table 2 ). Hence, these genotypes are considered non-zoonotic. On the other hand, six genotypes that have been found in cats are considered zoonotic, since they have also been observed in humans ( Table 3 ). Genotypes D and Type IV are of major importance and have been described in several countries in humans and in a wide variety of animal species ( Table 3 ). In this study, both positive cats had the genotype D. This genotype was described in cats for the first time by Mori et al. (2013) Mori H, Mahittikorn A, Thammasonthijarern N, Chaisiri K, Rojekittikhun W, Sukthana Y. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Vet Parasitol 2013; 197(3-4): 696-701. http://dx.doi.org/10.1016/j.vetpar.2013.07.025. PMid:23932454.
http://dx.doi.org/10.1016/j.vetpar.2013...
in Thailand, where it was detected in 22 out of 25 E. bieneusi positive animals, demonstrating that domestic cats may play an important role in the propagation of zoonotic microsporidiosis caused by this genotype. Since that first description, genotype D has also been identified in cats by Karim et al. (2014a) Karim MR, Dong H, Yu F, Jian F, Zhang L, Wang R, et al. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J Clin Microbiol 2014a; 52(9): 3297-3302. http://dx.doi.org/10.1128/JCM.01352-14. PMid:24989604.
http://dx.doi.org/10.1128/JCM.01352-14 ...
, Li et al. (2015) Li W, Li Y, Song M, Lu Y, Yang J, Tao W, et al. Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Vet Parasitol 2015; 208(3-4): 125-134. http://dx.doi.org/10.1016/j.vetpar.2015.01.014. PMid:25665462.
http://dx.doi.org/10.1016/j.vetpar.2015...
and Xu et al. (2016b) Xu H, Jin Y, Wu W, Li P, Wang L, Li N, et al. Genotypes of Cryptosporidium spp., Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai, China. Parasit Vectors 2016b; 9(1): 121. http://dx.doi.org/10.1186/s13071-016-1409-5. PMid:26932267.
http://dx.doi.org/10.1186/s13071-016-14...
, in researches carried out in China. Therefore, this is the first report of genotype D in cats outside the Asian continent. In Brazil, genotype D has already been found in fecal samples from humans ( FENG et al., 2011 Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, et al. Development of a multilocus sequence typing tool for High-Resolution Genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 2011; 77(14): 4822-4828. http://dx.doi.org/10.1128/AEM.02803-10. PMid:21622791.
http://dx.doi.org/10.1128/AEM.02803-10 ...
), cattle (FIUZA et al., 2016b Fiuza VRS, Lopes CW, Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 2016b; 216: 46-51. http://dx.doi.org/10.1016/j.vetpar.2015.12.008. PMid:26801594.
http://dx.doi.org/10.1016/j.vetpar.2015...
) and birds ( CUNHA et al., 2016 Cunha MJ, Cury MC, Santín M. Widespread presence of human-pathogenic Enterocytozoon bieneusi genotypes in chickens. Vet Parasitol 2016; 217: 108-112. http://dx.doi.org/10.1016/j.vetpar.2015.12.019. PMid:26827870.
http://dx.doi.org/10.1016/j.vetpar.2015...
, 2017 Cunha MJR, Cury MC, Santín M. Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res 2017; 116(2): 487-493. http://dx.doi.org/10.1007/s00436-016-5309-6. PMid:27815734.
http://dx.doi.org/10.1007/s00436-016-53...
), suggesting the possible risk of zoonotic transmission in this country. In a study conducted in birds by Cunha et al. (2016) Cunha MJ, Cury MC, Santín M. Widespread presence of human-pathogenic Enterocytozoon bieneusi genotypes in chickens. Vet Parasitol 2016; 217: 108-112. http://dx.doi.org/10.1016/j.vetpar.2015.12.019. PMid:26827870.
http://dx.doi.org/10.1016/j.vetpar.2015...
in the state of Minas Gerais, genotype D was the most prevalent, and was found in 58.3% of analyzed fecal samples from chickens purchased in public markets. In the other single research in cats in the Americas, Santín et al. (2006) Santín M, Trout JM, Vecino JAC, Dubey JP, Fayer R. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol 2006; 141(3-4): 334-339. http://dx.doi.org/10.1016/j.vetpar.2006.06.004. PMid:16860480.
http://dx.doi.org/10.1016/j.vetpar.2006...
, using molecular methods, found 17% of 46 cats tested positive for E. bieneusi in Colombia, and also found four other genotypes (Type IV, WL11, Peru10 and D-like).

Table 1
Enterocytozoon bieneusi genotypes found only in cats.
Table 2
Enterocytozoon bieneusi genotypes found in cats and other hosts.
Table 3
Enterocytozoon bieneusi genotypes found in cats and humans (and some genotypes also in other hosts).

Our findings reveal the presence of E. bieneusi infection by a zoonotic genotype in domestic cats in Brazil. Cats, along with dogs, are the most common companion pets that live inside homes around the world, in very close contact with humans of all ages and health conditions. The detection of a zoonotic genotype emphasizes the risk of human infection, since cats can contribute to the direct and indirect transmission of this parasite through the contamination of water and food with feces containing E. bieneusi spores. This study imputes cats as potential dispersing agents of zoonotic genotype D in Brazil. However, further studies should be carried out to confirm this hypothesis.

Knowledge about and identification of possible pathogenic agents transmitted by these animals is of major public health importance, especially to immunocompromised patients. Thus, to gain a better understanding of the zoonotic transmission of E. bieneusi in Brazil, new epidemiological investigations on cats and other animals are needed, as well as simultaneous studies on animals and humans living together in the same house.

References

  • Abe N, Kimata I, Iseki M. Molecular evidence of Enterocytozoon bieneusi in Japan. J Vet Med Sci 2009; 71(2): 217-219. http://dx.doi.org/10.1292/jvms.71.217. PMid:19262036.
    » http://dx.doi.org/10.1292/jvms.71.217
  • Abe N, Kimata I. Molecular survey of Enterocytozoon bieneusi in a Japanese porcine population. Vector Borne Zoonotic Dis 2010; 10(4): 425-427.
  • Agholi M, Hatam GR, Motazedian MH. HIV/AIDS-associated opportunistic protozoal diarrhea. AIDS Res Hum Retroviruses 2013a; 29(1): 35-41. http://dx.doi.org/10.1089/aid.2012.0119. PMid:22873400.
    » http://dx.doi.org/10.1089/aid.2012.0119
  • Agholi M, Hatam GR, Motazedian MH. Microsporidia and coccidia as causes of persistence diarrhea among liver transplant children: incidence rate and species/genotypes. Pediatr Infect Dis J 2013b; 32(2): 185-187. http://dx.doi.org/10.1097/INF.0b013e318273d95f. PMid:22982981.
    » http://dx.doi.org/10.1097/INF.0b013e318273d95f
  • Akinbo FO, Omoregie R, Xiao L, Dearen T, Leon ET, Okaka CE. Molecular epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in Benin City, Nigeria. Am J Trop Med Hyg 2012; 86(3): 441-445. http://dx.doi.org/10.4269/ajtmh.2012.11-0548. PMid:22403314.
    » http://dx.doi.org/10.4269/ajtmh.2012.11-0548
  • Ayinmode AB, Ojuromi OT, Xiao L. Molecular Identification of Enterocytozoon bieneusi Isolates from Nigerian Children. J Parasitol Res 2011; 2011: 1-2. http://dx.doi.org/10.1155/2011/129542. PMid:22132304.
    » http://dx.doi.org/10.1155/2011/129542
  • Baroudi D, Khelef D, Hakem A, Abdelaziz A, Chen X, Lysen C, et al. Molecular characterization of zoonotic pathogens Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in calves in Algeria. Vet Parasitol Reg Stud Rep 2017; 8: 66-69.
  • Bern C, Kawai V, Vargas D, Rabke-Verani J, Williamson J, Chavez-Valdez R, et al. The epidemiology of intestinal microsporidiosis in patients with HIV/AIDS in Lima, Peru. J Infect Dis 2005; 191(10): 1658-1664. http://dx.doi.org/10.1086/429674. PMid:15838792.
    » http://dx.doi.org/10.1086/429674
  • Brasil P, Lima DB, Paiva DD, Lobo MS, Sodré FC, Silva SP, et al. Clinical and diagnostic aspects of intestinal microsporidiosis in HIV-infected patients with chronic diarrhea in Rio de Janeiro, Brazil. Rev Inst Med Trop São Paulo 2000; 42(6): 299-304. http://dx.doi.org/10.1590/S0036-46652000000600001. PMid:11136515.
    » http://dx.doi.org/10.1590/S0036-46652000000600001
  • Breton J, Bart-Delabesse E, Biligui S, Carbone A, Seiller X, Okome-Nkoumou M, et al. New highly divergent rRNA sequence among biodiverse genotypes of Enterocytozoon bieneusi strains isolated from humans in Gabon and Cameroon. J Clin Microbiol 2007; 45(8): 2580-2589. http://dx.doi.org/10.1128/JCM.02554-06. PMid:17537939.
    » http://dx.doi.org/10.1128/JCM.02554-06
  • Buckholt MA, Lee JH, Tzipori S. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 2002; 68(5): 2595-2599. http://dx.doi.org/10.1128/AEM.68.5.2595-2599.2002. PMid:11976142.
    » http://dx.doi.org/10.1128/AEM.68.5.2595-2599.2002
  • Cama VA, Pearson J, Cabrera L, Pacheco L, Gilman R, Meyer S, et al. Transmission of Enterocytozoon bieneusi between a Child and Guinea Pigs. J Clin Microbiol 2007; 45(8): 2708-2710. http://dx.doi.org/10.1128/JCM.00725-07. PMid:17537930.
    » http://dx.doi.org/10.1128/JCM.00725-07
  • Chabchoub N, Abdelmalek R, Breton J, Kanoun F, Thellier M, Bouratbine A, et al. Genotype identification of Enterocytozoon bieneusi isolates from stool samples of HIV-infected Tunisian patients. Parasite 2012; 19(2): 147-151. http://dx.doi.org/10.1051/parasite/2012192147. PMid:22550625.
    » http://dx.doi.org/10.1051/parasite/2012192147
  • Chalifoux LV, Carville A, Pauley D, Thompson B, Lackner AA, Mansfield KG. Enterocytozoon bieneusi as a cause of proliferative serositis in simian immunodeficiency virus-infected immunodeficient macaques (Macaca mulatta). Arch Pathol Lab Med 2000; 124(10): 1480-1484. PMid:11035580.
  • Cunha MJ, Cury MC, Santín M. Widespread presence of human-pathogenic Enterocytozoon bieneusi genotypes in chickens. Vet Parasitol 2016; 217: 108-112. http://dx.doi.org/10.1016/j.vetpar.2015.12.019. PMid:26827870.
    » http://dx.doi.org/10.1016/j.vetpar.2015.12.019
  • Cunha MJR, Cury MC, Santín M. Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res 2017; 116(2): 487-493. http://dx.doi.org/10.1007/s00436-016-5309-6. PMid:27815734.
    » http://dx.doi.org/10.1007/s00436-016-5309-6
  • Del Coco VF, Córdoba MA, Bilbao G, Almeida Castro P, Basualdo JA, Santín M. First report of Enterocytozoon bieneusi from dairy cattle in Argentina. Vet Parasitol 2014; 199(1-2): 112-115. http://dx.doi.org/10.1016/j.vetpar.2013.09.024. PMid:24126086.
    » http://dx.doi.org/10.1016/j.vetpar.2013.09.024
  • Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke A, et al. Zoonotic potential of Enterocytozoon bieneusi. J Clin Microbiol 2001; 39(12): 4495-4499. http://dx.doi.org/10.1128/JCM.39.12.4495-4499.2001. PMid:11724868.
    » http://dx.doi.org/10.1128/JCM.39.12.4495-4499.2001
  • Deplazes P, Mathis A, Muller C, Weber R. Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J Eukaryot Microbiol 1996; 43(5): 93S. http://dx.doi.org/10.1111/j.1550-7408.1996.tb05018.x. PMid:8822883.
    » http://dx.doi.org/10.1111/j.1550-7408.1996.tb05018.x
  • Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, 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(2): 250-254. http://dx.doi.org/10.1111/j.1550-7408.1985.tb03046.x. PMid:4009510.
    » http://dx.doi.org/10.1111/j.1550-7408.1985.tb03046.x
  • Espern A, Morio F, Miegeville M, Illa H, Abdoulaye M, Meyssonnier V, 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. J Clin Microbiol 2007; 45(9): 2999-3002. http://dx.doi.org/10.1128/JCM.00684-07. PMid:17634305.
    » http://dx.doi.org/10.1128/JCM.00684-07
  • Fayer R, Santín M, Macarisin D. Detection of concurrent infection of dairy cattle with Blastocystis, Cryptosporidium, Giardia, and Enterocytozoon by molecular and microscopic methods. Parasitol Res 2012; 111(3): 1349-1355. http://dx.doi.org/10.1007/s00436-012-2971-1. PMid:22710524.
    » http://dx.doi.org/10.1007/s00436-012-2971-1
  • Fayer R, Santín M, Trout JM. Enterocytozoon bieneusi in mature dairy cattle on farms in the eastern United States. Parasitol Res 2007; 102(1): 15-20. http://dx.doi.org/10.1007/s00436-007-0746-x. PMid:17899197.
    » http://dx.doi.org/10.1007/s00436-007-0746-x
  • Fayer R, Santín M. Epidemiology of Microsporidia in human infections. In: Weiss LM, Becnel JJ. Microsporidia: pathogens of opportunity 1st ed. Hoboken: John Wiley & Sons, Inc. 2014. p. 135-164. http://dx.doi.org/10.1002/9781118395264.ch3.
    » http://dx.doi.org/10.1002/9781118395264.ch3
  • Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, et al. Development of a multilocus sequence typing tool for High-Resolution Genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 2011; 77(14): 4822-4828. http://dx.doi.org/10.1128/AEM.02803-10. PMid:21622791.
    » http://dx.doi.org/10.1128/AEM.02803-10
  • Fiuza VRS, Lopes CWG, Cosendey RIJ, Oliveira FCR, Fayer R, Santín M. Zoonotic Enterocytozoon bieneusi genotypes found in brazilian sheep. Res Vet Sci 2016a; 107: 196-201. http://dx.doi.org/10.1016/j.rvsc.2016.06.006. PMid:27473995.
    » http://dx.doi.org/10.1016/j.rvsc.2016.06.006
  • Fiuza VRS, Lopes CW, Oliveira FC, Fayer R, Santin M. New findings of Enterocytozoon bieneusi in beef and dairy cattle in Brazil. Vet Parasitol 2016b; 216: 46-51. http://dx.doi.org/10.1016/j.vetpar.2015.12.008. PMid:26801594.
    » http://dx.doi.org/10.1016/j.vetpar.2015.12.008
  • Fiuza VRS, Oliveira FCR, Fayer R, Santín M. First report of Enterocytozoon bieneusi in pigs in Brazil. Parasitol Int 2015; 64(4): 18-23. http://dx.doi.org/10.1016/j.parint.2015.01.002. PMid:25582928.
    » http://dx.doi.org/10.1016/j.parint.2015.01.002
  • Galván AL, Sánchez AM, Valentín MA, Henriques-Gil N, Izquierdo F, Fenoy S, et al. First cases of microsporidiosis in transplant recipients in spain and review of the literature. J Clin Microbiol 2011; 49(4): 1301-1306. http://dx.doi.org/10.1128/JCM.01833-10. PMid:21325545.
    » http://dx.doi.org/10.1128/JCM.01833-10
  • Galván-Díaz AL, Magnet A, Fenoy S, Henriques-Gil N, Haro M, Gordo FP, et al. Microsporidia detection and genotyping study of human pathogenic E. bieneusi in animals from Spain. PLoS One 2014; 9(3): e92289. http://dx.doi.org/10.1371/journal.pone.0092289. PMid:24651457.
    » http://dx.doi.org/10.1371/journal.pone.0092289
  • Guo Y, Alderisio KA, 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(1): 218-225. http://dx.doi.org/10.1128/AEM.02997-13. PMid:24141128.
    » http://dx.doi.org/10.1128/AEM.02997-13
  • Jamshidi S, Tabrizi AS, Bahrami M, Momtaz H. Microsporidia in household dogs and cats in Iran; a zoonotic concern. Vet Parasitol 2012; 185(2-4): 121-123. http://dx.doi.org/10.1016/j.vetpar.2011.10.002. PMid:22035849.
    » http://dx.doi.org/10.1016/j.vetpar.2011.10.002
  • Jiang Y, Tao W, Wan Q, Li Q, Yang Y, Lin Y, et al. Zoonotic and potentially host-adapted Enterocytozoon bieneusi genotypes in sheep and cattle in northeast china and an increasing concern about the Zoonotic importance of previously considered Ruminant-Adapted Genotypes. Appl Environ Microbiol 2015; 81(10): 3326-3335. http://dx.doi.org/10.1128/AEM.00328-15. PMid:25746997.
    » http://dx.doi.org/10.1128/AEM.00328-15
  • Juránková J, Kamler M, Kovarcik K, Koudela B. Enterocytozoon bieneusi in Bovine Viral Diarrhea Virus (BVDV) infected and noninfected cattle herds. Res Vet Sci 2013; 94(1): 100-104. http://dx.doi.org/10.1016/j.rvsc.2012.07.016. PMid:22858000.
    » http://dx.doi.org/10.1016/j.rvsc.2012.07.016
  • Karim MR, Dong H, Li T, Yu F, Li D, Zhang L, et al. Predomination and new genotypes of Enterocytozoon bieneusi in captive nonhuman primates in zoos in China: high genetic diversity and zoonotic significance. PLoS One 2015; 10(2): e0117991. http://dx.doi.org/10.1371/journal.pone.0117991. PMid:25705879.
    » http://dx.doi.org/10.1371/journal.pone.0117991
  • Karim MR, Dong H, Yu F, Jian F, Zhang L, Wang R, et al. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J Clin Microbiol 2014a; 52(9): 3297-3302. http://dx.doi.org/10.1128/JCM.01352-14. PMid:24989604.
    » http://dx.doi.org/10.1128/JCM.01352-14
  • Karim MR, Wang R, Dong H, Zhang L, Li J, Zhang S, et al. Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China. Appl Environ Microbiol 2014b; 80(6): 1893-1898. http://dx.doi.org/10.1128/AEM.03845-13. PMid:24413605.
    » http://dx.doi.org/10.1128/AEM.03845-13
  • Karim MR, Wang R, He X, Zhang L, Li J, Rume FI, et al. Multilocus sequence typing of Enterocytozoon bieneusi in nonhuman primates in China. Vet Parasitol 2014c; 200(1-2): 13-23. http://dx.doi.org/10.1016/j.vetpar.2013.12.004. PMid:24388499.
    » http://dx.doi.org/10.1016/j.vetpar.2013.12.004
  • Karim MR, Yu F, Li J, Li J, Zhang L, Wang R, et al. First molecular characterization of enteric protozoa and the human pathogenic microsporidian, Enterocytozoon bieneusi , in captive snakes in China. Parasitol Res 2014d; 113(8): 3041-3048. http://dx.doi.org/10.1007/s00436-014-3967-9. PMid:24906991.
    » http://dx.doi.org/10.1007/s00436-014-3967-9
  • Kicia M, Wesolowska M, Jakuszko K, Kopacz Z, Sak B, Kvetonova D, et al. Concurrent infection of the urinary tract with Encephalitozoon cuniculi and Enterocytozoon bieneusi in a renal transplant recipient. J Clin Microbiol 2014; 52(5): 1780-1782. http://dx.doi.org/10.1128/JCM.03328-13. PMid:24523472.
    » http://dx.doi.org/10.1128/JCM.03328-13
  • Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33(7): 1870-1874. http://dx.doi.org/10.1093/molbev/msw054. PMid:27004904.
    » http://dx.doi.org/10.1093/molbev/msw054
  • Laatamna AE, Wagnerova P, Sak B, Kvetonova D, Xiao L, Rost M, et al. Microsporidia and Cryptosporidium in horses and donkeys in Algeria: detection of a novel Cryptosporidium hominis subtype family (Ik) in a horse. Vet Parasitol 2015; 208(3-4): 135-142. http://dx.doi.org/10.1016/j.vetpar.2015.01.007. PMid:25638716.
    » http://dx.doi.org/10.1016/j.vetpar.2015.01.007
  • Lallo MA, Calabria P, Milanelo L. Encephalitozoon and Enterocytozoon (microsporidia) spores in stool from pigeons and exotic birds: microsporidia spores in birds. Vet Parasitol 2012; 190(3-4): 418-422. http://dx.doi.org/10.1016/j.vetpar.2012.06.030. PMid:22853863.
    » http://dx.doi.org/10.1016/j.vetpar.2012.06.030
  • Lee JH. Molecular detection of Enterocytozoon bieneusi and identification of a potentially human-pathogenic genotype in milk. Appl Environ Microbiol 2008; 74(5): 1664-1666. http://dx.doi.org/10.1128/AEM.02110-07. PMid:18192409.
    » http://dx.doi.org/10.1128/AEM.02110-07
  • Lee JH. Prevalence and molecular characteristics of Enterocytozoon bieneusi in cattle in Korea. Parasitol Res 2007; 101(2): 391-396.
  • Leelayoova S, Subrungruang I, Suputtamongkol Y, Worapong J, Petmitr PC, Mungthin M. Identification of genotypes of Enterocytozoon bieneusi from stool samples from human immunodeficiency virus-infected patients in Thailand. J Clin Microbiol 2006; 44(8): 3001-3004. http://dx.doi.org/10.1128/JCM.00945-06. PMid:16891527.
    » http://dx.doi.org/10.1128/JCM.00945-06
  • Li J, Luo N, Wang C, Qi M, Cao J, Cui Z, et al. Occurrence, molecular characterization and predominant genotypes of Enterocytozoon bieneusi in dairy cattle in Henan and Ningxia, China. Parasit Vectors 2016a; 9(1): 142. http://dx.doi.org/10.1186/s13071-016-1425-5. PMid:26968376.
    » http://dx.doi.org/10.1186/s13071-016-1425-5
  • Li W, Cama V, Akinbo FO, Ganguly S, Kiulia NM, Zhang X, et al. Multilocus sequence typing of Enterocytozoon bieneusi: Lack of geographic segregation and existence of genetically isolated sub-populations. Infect Genet Evol 2013; 14: 111-119. http://dx.doi.org/10.1016/j.meegid.2012.11.021. PMid:23262155.
    » http://dx.doi.org/10.1016/j.meegid.2012.11.021
  • Li W, Deng L, Yu X, Zhong Z, Wang Q, Liu X, et al. Multilocus genotypes and broad host-range of Enterocytozoon bieneusi in captive wildlife at zoological gardens in China. Parasit Vectors 2016b; 9(1): 395. http://dx.doi.org/10.1186/s13071-016-1668-1. PMid:27391225.
    » http://dx.doi.org/10.1186/s13071-016-1668-1
  • Li W, Diao R, Yang J, Xiao L, Lu Y, Li Y, et al. High diversity of human-pathogenic Enterocytozoon bieneusi genotypes in swine in northeast China. Parasitol Res 2014a; 113(3): 1147-1153. http://dx.doi.org/10.1007/s00436-014-3752-9. PMid:24442159.
    » http://dx.doi.org/10.1007/s00436-014-3752-9
  • Li W, Kiulia NM, Mwenda JM, Nyachieo A, Taylor MB, Zhang X, et al. Cyclospora papionis, Cryptosporidium hominis, and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya. J Clin Microbiol 2011; 49(12): 4326-4329. http://dx.doi.org/10.1128/JCM.05051-11. PMid:21956988.
    » http://dx.doi.org/10.1128/JCM.05051-11
  • Li W, Li Y, Li W, Yang J, Song M, Diao R, et al. Genotypes of Enterocytozoon bieneusi in livestock in China: high prevalence and zoonotic potential. PLoS One 2014b; 9(5): e97623. http://dx.doi.org/10.1371/journal.pone.0097623. PMid:24845247.
    » http://dx.doi.org/10.1371/journal.pone.0097623
  • Li W, Li Y, Song M, Lu Y, Yang J, Tao W, et al. Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Vet Parasitol 2015; 208(3-4): 125-134. http://dx.doi.org/10.1016/j.vetpar.2015.01.014. PMid:25665462.
    » http://dx.doi.org/10.1016/j.vetpar.2015.01.014
  • Liguory O, David F, Sarfati C, Derouin F, Molina JM. Determination of Types of Enterocytozoon bieneusi Strains Isolated from Patients with Intestinal Microsporidiosis. J Clin Microbiol 1998; 36(7): 1882-1885. PMid:9650929.
  • Liguory O, Sarfati C, Derouin F, Molina JM. Evidence of different Enterocytozoon bieneusi genotypes in patients with and without human immunodeficiency virus infection. J Clin Microbiol 2001; 39(7): 2672-2674. http://dx.doi.org/10.1128/JCM.39.7.2672-2674.2001. PMid:11427592.
    » http://dx.doi.org/10.1128/JCM.39.7.2672-2674.2001
  • Lobo ML, Augusto J, Antunes F, Ceita J, Xiao L, Codices V, et al. Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi and Other Intestinal Parasites in Young Children in Lobata Province, Democratic Republic of São Tomé and Principe. PLoS One 2014; 9(5): e97708. http://dx.doi.org/10.1371/journal.pone.0097708. PMid:24846205.
    » http://dx.doi.org/10.1371/journal.pone.0097708
  • Lobo ML, Xiao L, Antunes F, Matos O. Microsporidia as emerging pathogens and the implication for public health: a 10-year study on HIV-positive and -negative patients. Int J Parasitol 2012; 42(2): 197-205. http://dx.doi.org/10.1016/j.ijpara.2011.12.002. PMid:22265899.
    » http://dx.doi.org/10.1016/j.ijpara.2011.12.002
  • Lobo ML, Xiao L, Cama V, Stevens T, Antunes F, Matos O. Genotypes of Enterocytozoon bieneusi in mammals in Portugal. J Eukaryot Microbiol 2006;53(s1 Suppl 1): S61-S64. http://dx.doi.org/10.1111/j.1550-7408.2006.00174.x. PMid:17169069.
    » http://dx.doi.org/10.1111/j.1550-7408.2006.00174.x
  • Ma J, Cai J, Ma J, Feng Y, Xiao L. Enterocytozoon bieneusi genotypes in yaks (Bos grunniens) and their public health potential. J Eukaryot Microbiol 2015a; 62(1): 21-25. http://dx.doi.org/10.1111/jeu.12141. PMid:25040451.
    » http://dx.doi.org/10.1111/jeu.12141
  • Ma J, Li P, Zhao X, Xu H, Wu W, Wang Y, et al. Occurrence and molecular characterization of Cryptosporidium spp. and Enterocytozoon bieneusi in dairy cattle, beef cattle and water buffaloes in China. Vet Parasitol 2015b; 207(3-4): 220-227. http://dx.doi.org/10.1016/j.vetpar.2014.10.011. PMid:25541482.
    » http://dx.doi.org/10.1016/j.vetpar.2014.10.011
  • Maikai BV, Umoh JU, Lawal IA, Kudi AC, Ejembi CL, Xiao L. Molecular characterizations of Cryptosporidium, Giardia, and Enterocytozoon in humans in Kaduna State, Nigeria. Exp Parasitol 2012; 131(4): 452-456. http://dx.doi.org/10.1016/j.exppara.2012.05.011. PMid:22664352.
    » http://dx.doi.org/10.1016/j.exppara.2012.05.011
  • Mathis A, Breitenmoser AC, Deplazes P. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite 1999; 6(2): 189-193. http://dx.doi.org/10.1051/parasite/1999062189. PMid:10416194.
    » http://dx.doi.org/10.1051/parasite/1999062189
  • Mathis A, Weber R, Deplazes P. Zoonotic potential of the microsporidia. Clin Microbiol Rev 2005; 18(3): 423-445. http://dx.doi.org/10.1128/CMR.18.3.423-445.2005. PMid:16020683.
    » http://dx.doi.org/10.1128/CMR.18.3.423-445.2005
  • Mori H, Mahittikorn A, Thammasonthijarern N, Chaisiri K, Rojekittikhun W, Sukthana Y. Presence of zoonotic Enterocytozoon bieneusi in cats in a temple in central Thailand. Vet Parasitol 2013; 197(3-4): 696-701. http://dx.doi.org/10.1016/j.vetpar.2013.07.025. PMid:23932454.
    » http://dx.doi.org/10.1016/j.vetpar.2013.07.025
  • Müller MG, Kinne J, Schuster RK, Walochnik J. Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons. Vet Parasitol 2008; 152(1-2): 67-78. http://dx.doi.org/10.1016/j.vetpar.2007.11.019. PMid:18166273.
    » http://dx.doi.org/10.1016/j.vetpar.2007.11.019
  • Němejc K, Sak B, Kvetonova D, Hanzal V, Janiszewski P, Forejtek P, et al. Prevalence and diversity of Encephalitozoon spp. and Enterocytozoon bieneusi in wild boars (Sus scrofa) in Central Europe. Parasitol Res 2014; 113(2): 761-767. http://dx.doi.org/10.1007/s00436-013-3707-6. PMid:24292543.
    » http://dx.doi.org/10.1007/s00436-013-3707-6
  • Piekarska J, Kicia M, Wesołowska M, Kopacz Ż, Gorczykowski M, Szczepankiewicz B, et al. Zoonotic microsporidia in dogs and cats in Poland. Vet Parasitol 2017; 246: 108-111. http://dx.doi.org/10.1016/j.vetpar.2017.09.011. PMid:28969771.
    » http://dx.doi.org/10.1016/j.vetpar.2017.09.011
  • 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. http://dx.doi.org/10.1016/j.meegid.2013.10.007. PMid:24427811.
    » http://dx.doi.org/10.1016/j.meegid.2013.10.007
  • Prasertbun R, Mori H, Pintong AR, Sanyanusin S, Popruk S, Komalamisra C, et al. Zoonotic potential of Enterocytozoon genotypes in humans and pigs in Thailand. Vet Parasitol 2017; 233: 73-79. http://dx.doi.org/10.1016/j.vetpar.2016.12.002. PMid:28043391.
    » http://dx.doi.org/10.1016/j.vetpar.2016.12.002
  • Qi M, Jing B, Jian F, Wang R, Zhang S, Wang H, et al. Dominance of Enterocytozoon bieneusi genotype J in dairy calves in Xinjiang, Northwest China. Parasitol Int 2017; 66(1): 960-963. http://dx.doi.org/10.1016/j.parint.2016.10.019. PMid:27794506.
    » http://dx.doi.org/10.1016/j.parint.2016.10.019
  • Qi M, Wang R, Wang H, Jian F, Li J, Zhao J, et al. Enterocytozoon bieneusi Genotypes in grazing horses in China and their zoonotic transmission potential. J Eukaryot Microbiol 2016; 63(5): 591-597. http://dx.doi.org/10.1111/jeu.12308. PMid:26909747.
    » http://dx.doi.org/10.1111/jeu.12308
  • Queen EV, Marks SL, Farver TB. Prevalence of Selected bacterial and parasitic agents in feces from diarrheic and healthy control cats from Northern California. J Vet Intern Med 2012; 26(1): 54-60. http://dx.doi.org/10.1111/j.1939-1676.2011.00843.x. PMid:22182203.
    » http://dx.doi.org/10.1111/j.1939-1676.2011.00843.x
  • Rinder H, Thomschke A, Dengjel B, Gothe R, Loscher T, Zahler M. Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J Parasitol 2000; 86(1): 185-188. http://dx.doi.org/10.1645/0022-3395(2000)086[0185:CGRBEB]2.0.CO;2. PMid:10701590.
    » http://dx.doi.org/10.1645/0022-3395(2000)086[0185:CGRBEB]2.0.CO;2
  • Sadler F, Peake N, Borrow R, Rowl PL, Wilkins EG, Curry A. Genotyping of Enterocytozoon bieneusi in AIDS patients from the north west of England. J Infect 2002; 44(1): 39-42. http://dx.doi.org/10.1053/jinf.2001.0934. PMid:11972417.
    » http://dx.doi.org/10.1053/jinf.2001.0934
  • Sak B, Kvac M, Hanzlikova D, Cama V. First report of Enterocytozoon bieneusi infection on a pig farm in the Czech Republic. Vet Parasitol 2008; 153(3-4): 220-224. http://dx.doi.org/10.1016/j.vetpar.2008.01.043. PMid:18342450.
    » http://dx.doi.org/10.1016/j.vetpar.2008.01.043
  • Sak B, Kvac M, Kvetonova D, Albrecht T, Pialek 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(3-4): 246-250. http://dx.doi.org/10.1016/j.vetpar.2010.12.044. PMid:21269775.
    » http://dx.doi.org/10.1016/j.vetpar.2010.12.044
  • Saksirisampant W, Prownebon J, Saksirisampant P, Mungthin M, Siripatanapipong S, Leelayoova S. Intestinal parasitic infections: prevalences in HIV/AIDS patients in a Thai AIDS-care centre. Ann Trop Med Parasitol 2009; 103(7): 573-581. http://dx.doi.org/10.1179/000349809X12502035776072. PMid:19825279.
    » http://dx.doi.org/10.1179/000349809X12502035776072
  • Samra NA, Thompson PN, Jori F, Zhang H, Xiao L. Enterocytozoon bieneusi at the wildlife/livestock interface of the Kruger National Park, South Africa. Vet Parasitol 2012; 190(3-4): 587-590. http://dx.doi.org/10.1016/j.vetpar.2012.06.031. PMid:22824060.
    » http://dx.doi.org/10.1016/j.vetpar.2012.06.031
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977; 74(12): 5463-5467. http://dx.doi.org/10.1073/pnas.74.12.5463. PMid:271968.
    » http://dx.doi.org/10.1073/pnas.74.12.5463
  • Santín M, Dargatz D, Fayer R. Prevalence and genotypes of Enterocytozoon bieneusi in weaned beef calves on cow-calf operations in the USA. Parasitol Res 2012; 110(5): 2033-2041. http://dx.doi.org/10.1007/s00436-011-2732-6. PMid:22146995.
    » http://dx.doi.org/10.1007/s00436-011-2732-6
  • Santín M, Fayer R. A longitudinal study of Enterocytozoon bieneusi in dairy cattle. Parasitol Res 2009; 105(1): 141-144. http://dx.doi.org/10.1007/s00436-009-1374-4. PMid:19259701.
    » http://dx.doi.org/10.1007/s00436-009-1374-4
  • Santín M, Fayer R. Enterocytozoon bieneusi, Giardia, and Cryptosporidium infecting white-tailed deer. J Eukaryot Microbiol 2015; 62(1): 34-43. http://dx.doi.org/10.1111/jeu.12155. PMid:25066778.
    » http://dx.doi.org/10.1111/jeu.12155
  • Santín M, Fayer R. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Res Vet Sci 2011; 90(3): 363-371. http://dx.doi.org/10.1016/j.rvsc.2010.07.014. PMid:20699192.
    » http://dx.doi.org/10.1016/j.rvsc.2010.07.014
  • Santín M, Cortes Vecino JA, Fayer R. Enterocytozoon bieneusi genotypes in dogs in Bogota, Colombia. Am J Trop Med Hyg 2008; 79(2): 215-217. http://dx.doi.org/10.4269/ajtmh.2008.79.215. PMid:18689627.
    » http://dx.doi.org/10.4269/ajtmh.2008.79.215
  • Santín M, Trout JM, Fayer R. Enterocytozoon bieneusi genotypes in dairy cattle in the eastern United States. Parasitol Res 2005; 97(6): 535-538. http://dx.doi.org/10.1007/s00436-005-1482-8. PMid:16167161.
    » http://dx.doi.org/10.1007/s00436-005-1482-8
  • Santín M, Trout JM, Vecino JAC, Dubey JP, Fayer R. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet Parasitol 2006; 141(3-4): 334-339. http://dx.doi.org/10.1016/j.vetpar.2006.06.004. PMid:16860480.
    » http://dx.doi.org/10.1016/j.vetpar.2006.06.004
  • Santín M, Vecino JA, Fayer R. A zoonotic genotype of Enterocytozoon bieneusi in horses. J Parasitol 2010; 96(1): 157-161. http://dx.doi.org/10.1645/GE-2184.1. PMid:19799490.
    » http://dx.doi.org/10.1645/GE-2184.1
  • Santín M. Enterocytozoon bieneusi. In: Xiao L, Ryan U, Feng Y. Biology of foodborne parasites United States of America: CRC Press; 2015. p. 149-174.
  • Sarfati C, Ngole EM, Delaporte E, Moyou-Somo R, Molina J-M, Derouin F, et al. Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg 2006; 74(1): 162-164. http://dx.doi.org/10.4269/ajtmh.2006.74.162. PMid:16407362.
    » http://dx.doi.org/10.4269/ajtmh.2006.74.162
  • Shi K, Li M, Wang X, Li J, Karim MR, Wang R, et al. Molecular survey of Enterocytozoon bieneusi in sheep and goats in China. Parasit Vectors 2016; 9(1): 23. http://dx.doi.org/10.1186/s13071-016-1304-0. PMid:26782742.
    » http://dx.doi.org/10.1186/s13071-016-1304-0
  • Sokolova OI, Demyanov AV, Bowers LC, Didier ES, Yakovlev AV, Skarlato SO, et al. Emerging microsporidian infections in Russian HIV-infected patients. J Clin Microbiol 2011; 49(6): 2102-2108. http://dx.doi.org/10.1128/JCM.02624-10. PMid:21450962.
    » http://dx.doi.org/10.1128/JCM.02624-10
  • Stensvold CR, Beser J, Ljungström B, Troell K, Lebbad M. Low host-specific Enterocytozoon bieneusi genotype BEB6 is common in Swedish lambs. Vet Parasitol 2014; 205(1-2): 371-374. http://dx.doi.org/10.1016/j.vetpar.2014.06.010. PMid:24986434.
    » http://dx.doi.org/10.1016/j.vetpar.2014.06.010
  • Sulaiman IM, Bern C, Gilman R, Cama V, Kawai V, Vargas D, et al. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. J Eukaryot Microbiol 2003a;50(s1 Suppl): 591-596. http://dx.doi.org/10.1111/j.1550-7408.2003.tb00642.x. PMid:14736175.
    » http://dx.doi.org/10.1111/j.1550-7408.2003.tb00642.x
  • Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW 3rd, Xiao L. Molecular characterization of microsporidia indicates that wild mammals Harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol 2003b; 69(8): 4495-4501. http://dx.doi.org/10.1128/AEM.69.8.4495-4501.2003. PMid:12902234.
    » http://dx.doi.org/10.1128/AEM.69.8.4495-4501.2003
  • Sulaiman IM, Fayer R, Yang C, Santín M, Matos O, Xiao L. Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Parasitol Res 2004; 92(4): 328-334. http://dx.doi.org/10.1007/s00436-003-1049-5. PMid:14727187.
    » http://dx.doi.org/10.1007/s00436-003-1049-5
  • ten Hove RJ, Van Lieshout L, Beadsworth MB, Perez MA, Spee K, Claas EC, et al. Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups. J Eukaryot Microbiol 2009; 56(4): 388-393. http://dx.doi.org/10.1111/j.1550-7408.2009.00393.x. PMid:19602086.
    » http://dx.doi.org/10.1111/j.1550-7408.2009.00393.x
  • Tumwine JK, Kekitiinwa A, Tzipori S, Buckholt MA, Akiyoshi DE, Nabukeera N. Enterocytozoon bieneusi among children with diarrhea attending Mulago Hospital in Uganda. Am J Trop Med Hyg 2002; 67(3): 299-303. http://dx.doi.org/10.4269/ajtmh.2002.67.299. PMid:12408671.
    » http://dx.doi.org/10.4269/ajtmh.2002.67.299
  • Vávra J, Lukeš J. Microsporidia and ‘The Art of Living Together’. In: Rollinson D. Advances in parasitology United States of America: Academic Press; 2013. p. 253-319.
  • Wagnerová P, Sak B, Kvetonova D, Bunatova Z, Civisova H, Marsalek M, et al. Enterocytozoon bieneusi and Encephalitozoon cuniculi in horses kept under different management systems in the Czech Republic. Vet Parasitol 2012; 190(3-4): 573-577. http://dx.doi.org/10.1016/j.vetpar.2012.07.013. PMid:22877825.
    » http://dx.doi.org/10.1016/j.vetpar.2012.07.013
  • Wang L, Xiao L, Duan L, Ye J, Guo Y, Guo M, et al. Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China. PLoS Negl Trop Dis 2013a; 7(9): e2437. http://dx.doi.org/10.1371/journal.pntd.0002437. PMid:24069491.
    » http://dx.doi.org/10.1371/journal.pntd.0002437
  • Wang L, Zhang H, Zhao X, Zhang L, Zhang G, Guo M, et al. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. J Clin Microbiol 2013b; 51(2): 557-563. http://dx.doi.org/10.1128/JCM.02758-12. PMid:23224097.
    » http://dx.doi.org/10.1128/JCM.02758-12
  • Wang SS, Wang RJ, Fan XC, Liu TL, Zhang LX, Zhao GH. Prevalence and genotypes of Enterocytozoon bieneusi in China. Acta Trop 2018; 183: 142-152. http://dx.doi.org/10.1016/j.actatropica.2018.04.017. PMid:29660311.
    » http://dx.doi.org/10.1016/j.actatropica.2018.04.017
  • Wumba R, Jean M, Benjamin LM, Madone M, Fabien K, Josué Z, et al. Enterocytozoon bieneusi Identification Using Real-Time Polymerase Chain Reaction and Restriction Fragment Length Polymorphism in HIV-Infected Humans from Kinshasa Province of the Democratic Republic of Congo. J Parasitol Res 2012; 2012: 278028. http://dx.doi.org/10.1155/2012/278028. PMid:22811884.
    » http://dx.doi.org/10.1155/2012/278028
  • Xu C, Ma X, Zhang H, Zhang XX, Zhao JP, Ba HX, et al. Prevalence, risk factors and molecular characterization of Enterocytozoon bieneusi in raccoon dogs (Nyctereutes procyonoides ) in five provinces of Northern China. Acta Trop 2016a; 161: 68-72. http://dx.doi.org/10.1016/j.actatropica.2016.05.015. PMid:27260667.
    » http://dx.doi.org/10.1016/j.actatropica.2016.05.015
  • Xu H, Jin Y, Wu W, Li P, Wang L, Li N, et al. Genotypes of Cryptosporidium spp., Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai, China. Parasit Vectors 2016b; 9(1): 121. http://dx.doi.org/10.1186/s13071-016-1409-5. PMid:26932267.
    » http://dx.doi.org/10.1186/s13071-016-1409-5
  • Yamashiro S, Fiuza VRS, Teixeira ÂTLS, Branco N, Levy CE, Castro ICVS, et al. Enterocytozoon bieneusi detected by molecular methods in raw sewage and treated effluent from a combined system in Brazil. Mem Inst Oswaldo Cruz 2017; 112(6): 403-410. http://dx.doi.org/10.1590/0074-02760160435. PMid:28591400.
    » http://dx.doi.org/10.1590/0074-02760160435
  • Yang Y, Lin Y, Li Q, Zhang S, Tao W, Wan Q, et al. Widespread presence of human-pathogenic Enterocytozoon bieneusi genotype D in farmed foxes (Vulpes vulpes ) and raccoon dogs (Nyctereutes procyonoides) in China: first identification and zoonotic concern. Parasitol Res 2015; 114(11): 4341-4348. http://dx.doi.org/10.1007/s00436-015-4714-6. PMid:26341801.
    » http://dx.doi.org/10.1007/s00436-015-4714-6
  • Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, et al. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitol Int 2014; 63(1): 132-137. http://dx.doi.org/10.1016/j.parint.2013.10.007. PMid:24157444.
    » http://dx.doi.org/10.1016/j.parint.2013.10.007
  • Ye J, Xiao L, Ma J, Guo M, Liu L, Feng Y. Anthroponotic enteric parasites in monkeys in public park, China. Emerg Infect Dis 2012; 18(10): 1640-1643. http://dx.doi.org/10.3201/eid1810.120653. PMid:23017776.
    » http://dx.doi.org/10.3201/eid1810.120653
  • Ye J, Xiao L, Wang Y, Guo Y, Roellig DM, Feng Y. Dominance of Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotype BEB6 in sheep in Inner Mongolia, China. Vet Parasitol 2015; 210(3-4): 235-239. http://dx.doi.org/10.1016/j.vetpar.2015.04.011. PMid:25944405.
    » http://dx.doi.org/10.1016/j.vetpar.2015.04.011
  • Zhang X, Wang Z, Su Y, Liang X, Sun X, Peng S, et al. Identification and Genotyping of Enterocytozoon bieneusi in China. J Clin Microbiol 2011; 49(5): 2006-2008. http://dx.doi.org/10.1128/JCM.00372-11. PMid:21389159.
    » http://dx.doi.org/10.1128/JCM.00372-11
  • Zhao GH, Du SZ, Wang HB, Hu XF, Deng MJ, Yu SK, et al. First report of zoonotic Cryptosporidium spp., Giardia intestinalis and Enterocytozoon bieneusi in golden takins (Budorcas taxicolor bedfordi). Infect Genet Evol 2015a; 34: 394-401. http://dx.doi.org/10.1016/j.meegid.2015.07.016. PMid:26190449.
    » http://dx.doi.org/10.1016/j.meegid.2015.07.016
  • Zhao W, Zhang W, Wang R, Liu W, Liu A, Yang D, et al. Enterocytozoon bieneusi in sika deer (Cervus nippon) and red deer (Cervus elaphus ): deer specificity and zoonotic potential of ITS genotypes. Parasitol Res 2014a; 113(11): 4243-4250. http://dx.doi.org/10.1007/s00436-014-4100-9. PMid:25185666.
    » http://dx.doi.org/10.1007/s00436-014-4100-9
  • Zhao W, Zhang W, Yang D, Zhang L, Wang R, Liu A. Prevalence of Enterocytozoon bieneusi and genetic diversity of ITS genotypes in sheep and goats in China. Infect Genet Evol 2015b; 32: 265-270. http://dx.doi.org/10.1016/j.meegid.2015.03.026. PMid:25818401.
    » http://dx.doi.org/10.1016/j.meegid.2015.03.026
  • Zhao W, Zhang W, Yang F, Cao J, Liu H, Yang D, et al. High prevalence of Enterocytozoon bieneusi in asymptomatic pigs and assessment of zoonotic risk at the genotype level. Appl Environ Microbiol 2014b; 80(12): 3699-3707. http://dx.doi.org/10.1128/AEM.00807-14. PMid:24727270.
    » http://dx.doi.org/10.1128/AEM.00807-14
  • Zhao W, Zhang W, Yang F, Zhang L, Wang R, Cao J, et al. Enterocytozoon bieneusi in dairy cattle in the Northeast of China: Genetic diversity of ITS Gene and Evaluation of Zoonotic Transmission Potential. J Eukaryot Microbiol 2015c; 62(4): 553-560. http://dx.doi.org/10.1111/jeu.12210. PMid:25712195.
    » http://dx.doi.org/10.1111/jeu.12210
  • Zhao W, Zhang W, Yang Z, Liu A, Zhang L, Yang F, et al. Genotyping of Enterocytozoon bieneusi in Farmed Blue Foxes (Alopex lagopus) and Raccoon Dogs (Nyctereutes procyonoides) in China. PLoS One 2015d; 10(11): e0142611. http://dx.doi.org/10.1371/journal.pone.0142611. PMid:26544711.
    » http://dx.doi.org/10.1371/journal.pone.0142611

Publication Dates

  • Publication in this collection
    14 Feb 2019
  • Date of issue
    Jan-Mar 2019

History

  • Received
    06 Sept 2018
  • Accepted
    10 Dec 2018
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br