First report and multilocus genotyping of Enterocytozoon bieneusi from Tibetan pigs in southwestern China

Enterocytozoon bieneusi is a common intestinal pathogen and a major cause of diarrhea and enteric diseases in a variety of animals. While the E. bieneusi genotype has become better-known, there are few reports on its prevalence in the Tibetan pig. This study investigated the prevalence, genetic diversity, and zoonotic potential of E. bieneusi in the Tibetan pig in southwestern China. Tibetan pig feces (266 samples) were collected from three sites in the southwest of China. Feces were subjected to PCR amplification of the internal transcribed spacer (ITS) region. E. bieneusi was detected in 83 (31.2%) of Tibetan pigs from the three different sites, with 25.4% in Kangding, 56% in Yaan and 26.7% in Qionglai. Age group demonstrated the prevalence of E. bieneusi range from 24.4%(aged 0 to 1 years) to 44.4%(aged 1 to 2 years). Four genotypes of E. bieneusi were identified: two known genotypes EbpC (n=58), Henan-IV (n=24) and two novel genotypes, SCT01 and SCT02 (one of each). Phylogenetic analysis showed these four genotypes clustered to group 1 with zoonotic potential. Multilocus sequence typing (MLST) analysis three microsatellites (MS1, MS3, MS7) and one minisatellite (MS4) revealed 47, 48, 23 and 47 positive specimens were successfully sequenced, and identified ten, ten, five and five genotypes at four loci, respectively. This study indicates the potential danger of E. bieneusi to Tibetan pigs in southwestern China, and offers basic data for preventing and controlling infections.

[1]  Longxian Zhang,et al.  The Potential Role of Synanthropic Rodents and Flies in the Transmission of Enterocytozoon bieneusi on a Dairy Cattle farm in China , 2018, The Journal of eukaryotic microbiology.

[2]  F. Zou,et al.  Prevalence and genotypes of Enterocytozoon bieneusi in pigs in southern China. , 2018, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[3]  F. Zou,et al.  Prevalence and multi-locus genotypes of Enterocytozoon bieneusi in black-boned sheep and goats in Yunnan Province, southwestern China. , 2018, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[4]  Longxian Zhang,et al.  Novel genotypes and multilocus genotypes of Enterocytozoon bieneusi in pigs in northwestern China: A public health concern. , 2018, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[5]  S. Qin,et al.  Molecular characterization and new genotypes of Enterocytozoon bieneusi in minks (Neovison vison) in China , 2018, Parasite.

[6]  Xian-Cheng Fan,et al.  Prevalence and genotypes of Enterocytozoon bieneusi in China. , 2018, Acta tropica.

[7]  Guo-Hua Liu,et al.  Enterocytozoon bieneusi in Minks (Neovison vison) in Northern China: A Public Health Concern , 2018, Front. Microbiol..

[8]  Longxian Zhang,et al.  Occurrence, Molecular Characterization, and Assessment of Zoonotic Risk of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in Pigs in Henan, Central China , 2018, The Journal of eukaryotic microbiology.

[9]  Wei Huang,et al.  Genotype Identification and Phylogenetic Analysis of Enterocytozoon bieneusi Isolates from Stool Samples of Diarrheic Children , 2018, The Journal of Parasitology.

[10]  Longxian Zhang,et al.  Host specificity of Enterocytozoon bieneusi genotypes in Bactrian camels (Camelus bactrianus) in China , 2018, Parasites & Vectors.

[11]  Lihua Xiao,et al.  Genetic diversity within dominant Enterocytozoon bieneusi genotypes in pre-weaned calves , 2018, Parasites & Vectors.

[12]  F. Zou,et al.  Prevalence, genotypes, and risk factors of Enterocytozoon bieneusi in Asiatic black bear (Ursus thibetanus) in Yunnan Province, Southwestern China , 2018, Parasitology Research.

[13]  R. Gasser,et al.  First detection and genetic characterisation of Enterocytozoon bieneusi in wild deer in Melbourne’s water catchments in Australia , 2018, Parasites & Vectors.

[14]  J. Saki,et al.  Molecular diagnosis of potentially human pathogenic Enterocytozoon bieneusi and Encephalitozoon species in exotic birds in Southwestern Iran. , 2017, Journal of infection and public health.

[15]  Lihua Xiao,et al.  Enterocytozoon bieneusi genotypes in Tibetan sheep and yaks , 2018, Parasitology Research.

[16]  Jianguang Wang,et al.  Dominance of the Enterocytozoon bieneusi genotype BEB6 in red deer (Cervus elaphus) and Siberian roe deer (Capreolus pygargus) in China and a brief literature review , 2017, Parasite.

[17]  Longxian Zhang,et al.  Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. , 2017, Veterinary parasitology.

[18]  B. Sak,et al.  Zoonotic microsporidia in dogs and cats in Poland. , 2017, Veterinary parasitology.

[19]  Jianhai Yin,et al.  Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region, China , 2017, BMC Infectious Diseases.

[20]  Z. Zhong,et al.  Molecular characterization and multi-locus genotypes of Enterocytozoon bieneusi from captive red kangaroos (Macropus Rfus) in Jiangsu province, China , 2017, PloS one.

[21]  Longxian Zhang,et al.  New Genotypes of Enterocytozoon bieneusi Isolated from Sika Deer and Red Deer in China , 2017, Front. Microbiol..

[22]  Z. Zhong,et al.  Multilocus genotyping of Enterocytozoon bieneusi derived from nonhuman primates in southwest China , 2017, PloS one.

[23]  Longxian Zhang,et al.  Dominance of Enterocytozoon bieneusi genotype J in dairy calves in Xinjiang, Northwest China. , 2017, Parasitology international.

[24]  T. Changbunjong,et al.  Zoonotic potential of Enterocytozoon genotypes in humans and pigs in Thailand. , 2017, Veterinary parasitology.

[25]  Z. Zhong,et al.  Presence of zoonotic Cryptosporidium scrofarum, Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotypes in captive Eurasian wild boars (Sus scrofa) in China: potential for zoonotic transmission , 2017, Parasites & Vectors.

[26]  Z. Zhong,et al.  Molecular characterization and multilocus genotypes of Enterocytozoon bieneusi among horses in southwestern China , 2016, Parasites & Vectors.

[27]  Wei Li,et al.  First Report of the Human-Pathogenic Enterocytozoon bieneusi from Red-Bellied Tree Squirrels (Callosciurus erythraeus) in Sichuan, China , 2016, PloS one.

[28]  Longxian Zhang,et al.  Enterocytozoon bieneusi Genotypes in Grazing Horses in China and their Zoonotic Transmission Potential , 2016, The Journal of eukaryotic microbiology.

[29]  Lihua Xiao,et al.  Human infective potential of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in urban wastewater treatment plant effluents. , 2016, Journal of water and health.

[30]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[31]  Chenrong Wang,et al.  Occurrence, molecular characterization and predominant genotypes of Enterocytozoon bieneusi in dairy cattle in Henan and Ningxia, China , 2016, Parasites & Vectors.

[32]  Wei Tao,et al.  High Prevalence and Widespread Distribution of Zoonotic Enterocytozoon bieneusi Genotypes in Swine in Northeast China: Implications for Public Health , 2016, The Journal of eukaryotic microbiology.

[33]  Xing-Quan Zhu,et al.  Prevalence, risk factors and multilocus genotyping of Enterocytozoon bieneusi in farmed foxes (Vulpes lagopus), Northern China , 2016, Parasites & Vectors.

[34]  Longxian Zhang,et al.  Molecular survey of Enterocytozoon bieneusi in sheep and goats in China , 2016, Parasites & Vectors.

[35]  Jingze Liu,et al.  Abundance and seasonal activity of Haemaphysalis concinna (Acari: Ixodidae) at the border between China and Russia in Northern Inner Mongolia, China , 2016, Parasites & Vectors.

[36]  Longxian Zhang,et al.  Correction: Genotyping of Enterocytozoon bieneusi in Farmed Blue Foxes (Alopex lagopus) and Raccoon Dogs (Nyctereutes procyonoides) in China , 2015, PloS one.

[37]  Longxian Zhang,et al.  Genotyping of Enterocytozoon bieneusi in Farmed Blue Foxes (Alopex lagopus) and Raccoon Dogs (Nyctereutes procyonoides) in China , 2015, PloS one.

[38]  Longxian Zhang,et al.  Zoonotic Enterocytozoon bieneusi genotypes in Pere David's deer (Elaphurus davidianus) in Henan, China. , 2015, Experimental parasitology.

[39]  Longxian Zhang,et al.  First report of zoonotic Cryptosporidium spp., Giardia intestinalis and Enterocytozoon bieneusi in golden takins (Budorcas taxicolor bedfordi). , 2015, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[40]  Longxian Zhang,et al.  First report of Enterocytozoon bieneusi from giant pandas (Ailuropoda melanoleuca) and red pandas (Ailurus fulgens) in China. , 2015, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[41]  R. Fayer,et al.  First report of Enterocytozoon bieneusi in pigs in Brazil. , 2015, Parasitology international.

[42]  Wei Tao,et al.  Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. , 2015, Veterinary parasitology.

[43]  Longxian Zhang,et al.  Predomination and New Genotypes of Enterocytozoon bieneusi in Captive Nonhuman Primates in Zoos in China: High Genetic Diversity and Zoonotic Significance , 2015, PloS one.

[44]  Lihua Xiao,et al.  Occurrence, source, and human infection potential of Cryptosporidium and Enterocytozoon bieneusi in drinking source water in Shanghai, China, during a pig carcass disposal incident. , 2014, Environmental science & technology.

[45]  Wei Tao,et al.  Enterocytozoon bieneusi Genotypes in Children in Northeast China and Assessment of Risk of Zoonotic Transmission , 2014, Journal of Clinical Microbiology.

[46]  Wei Tao,et al.  Genotypic Distribution and Phylogenetic Characterization of Enterocytozoon bieneusi in Diarrheic Chickens and Pigs in Multiple Cities, China: Potential Zoonotic Transmission , 2014, PloS one.

[47]  Longxian Zhang,et al.  Genetic Diversity in Enterocytozoon bieneusi Isolates from Dogs and Cats in China: Host Specificity and Public Health Implications , 2014, Journal of Clinical Microbiology.

[48]  Yi-jing Li,et al.  Genotypes of Enterocytozoon bieneusi in Livestock in China: High Prevalence and Zoonotic Potential , 2014, PloS one.

[49]  Jianping Cao,et al.  High Prevalence of Enterocytozoon bieneusi in Asymptomatic Pigs and Assessment of Zoonotic Risk at the Genotype Level , 2014, Applied and Environmental Microbiology.

[50]  Yi-jing Li,et al.  High diversity of human-pathogenic Enterocytozoon bieneusi genotypes in swine in northeast China , 2014, Parasitology Research.

[51]  Longxian Zhang,et al.  Genetic Polymorphism and Zoonotic Potential of Enterocytozoon bieneusi from Nonhuman Primates in China , 2014, Applied and Environmental Microbiology.

[52]  P. Janiszewski,et al.  Prevalence and diversity of Encephalitozoon spp. and Enterocytozoon bieneusi in wild boars (Sus scrofa) in Central Europe , 2013, Parasitology Research.

[53]  M. Guo,et al.  Concurrent Infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in Children during a Cryptosporidiosis Outbreak in a Pediatric Hospital in China , 2013, PLoS neglected tropical diseases.

[54]  M. Guo,et al.  Zoonotic Cryptosporidium Species and Enterocytozoon bieneusi Genotypes in HIV-Positive Patients on Antiretroviral Therapy , 2012, Journal of Clinical Microbiology.

[55]  M. Guo,et al.  Molecular Surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by Genotyping and Subtyping Parasites in Wastewater , 2012, PLoS neglected tropical diseases.

[56]  L. Weiss,et al.  Microsporidiosis: not just in AIDS patients , 2011, Current opinion in infectious diseases.

[57]  R. Fayer,et al.  Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. , 2011, Research in veterinary science.

[58]  V. Cama,et al.  Development of a Multilocus Sequence Typing Tool for High-Resolution Genotyping of Enterocytozoon bieneusi , 2011, Applied and Environmental Microbiology.

[59]  I. Kimata,et al.  Molecular survey of Enterocytozoon bieneusi in a Japanese porcine population. , 2010, Vector borne and zoonotic diseases.

[60]  R. Fayer,et al.  Enterocytozoon bieneusi Genotype Nomenclature Based on the Internal Transcribed Spacer Sequence: A Consensus , 2009, The Journal of eukaryotic microbiology.

[61]  L. Weiss,et al.  Microsporidiosis: current status , 2006, Current opinion in infectious diseases.

[62]  R. Fayer,et al.  Molecular Characterization of Microsporidia Indicates that Wild Mammals Harbor Host-Adapted Enterocytozoon spp. as well as Human-Pathogenic Enterocytozoon bieneusi , 2003, Applied and Environmental Microbiology.

[63]  J. N. Oldham Veterinary Parasitology , 1952, Nature.