Abstract: Limited data are available on infection rates and genetic identity of Enterocytozoon bieneusi and Giardia duodenalis in horses and donkeys. In this study, 865 fecal specimens were collected from donkeys (n = 540) and horses (n = 325) in three provinces and autonomous regions in northern China during 2015-2019. Enterocytozoon bieneusi was detected and genotyped by PCR and sequence analyses of the ribosomal internal transcribed spacer (ITS) and G. duodenalis was detected and genotyped by PCR and sequence analyses of the β-giardin, glutamate dehydrogenase, and triosephosphate isomerase genes. The overall infection rates of E. bieneusi and G. duodenalis were 21.9% (118/540) and 11.5% (62/540) in donkeys, and 7.4% (24/325) and 2.8% (9/325) in horses, respectively. These differences in infection rates of E. bieneusi and G. duodenalis between donkeys and horses were significant (χ = 30.9, df = 1, P < 0.0001; χ = 20.4, df = 1, P < 0.0001, respectively). By age, the 28.9% infection rate of E. bieneusi in donkeys under 6 months was significantly higher than that in animals over 6 months (6.0%; χ = 35.2, df = 1, P < 0.0001). In contrast, donkeys of 6-12 months had higher infection rate (35.9%) of G. duodenalis than donkeys under 6 months (9.9%; χ = 22.1, df = 1, P < 0.0001) and over 12 months (8.7%; χ = 17.3, df = 1, P 12 months had significantly higher infection rate (31.1%) of E. bieneusi than horses under 6 months (3.4%; χ = 29.4, df = 1, P < 0.0001) and 6-12 months (3.8%; χ = 26.1, df = 1, P < 0.0001). Twenty genotypes of E. bieneusi were detected, including six known ones and 14 new genotypes. Among them, nine genotypes in 45% E. bieneusi-positive specimens belonged to the zoonotic group 1. Similarly, three G. duodenalis assemblages were detected, including A (in 2 horses and 30 donkeys), B (in 6 horses and 29 donkeys), and E (in 1 horse); three donkeys had coinfections of assemblages A and B. The assemblage A isolates identified all belong to the sub-assemblage AI. These results indicate that unlike in other farm animals, there is a common occurrence of zoonotic E. bieneusi and G. duodenalis genotypes in horses and donkeys.
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The research article examines the infection rates and genetic types of two zoonotic parasites, Enterocytozoon bieneusi and Giardia duodenalis, in horses and donkeys in Northern China. It found that these parasites could potentially be transmitted to humans.
Methodology
The team of researchers collected 865 fecal samples from horses (325 samples) and donkeys (540 samples) across three provinces and autonomous regions in Northern China over a four-year period.
The parasites were detected and their genetic identity determined through Polymerase Chain Reaction (PCR) and sequence analysis of various genes specific to each parasite.
Results
The infection rates for E. bieneusi were 21.9% in donkeys and 7.4% in horses, while for G. duodenalis it was 11.5% in donkeys and 2.8% in horses.
There was a statistically significant difference in the infection rates of both parasites between donkeys and horses.
Across age groups, young donkeys (under 6 months) showed significantly higher infection rates for E. bieneusi compared to older animals. For G. duodenalis, donkeys aged between 6-12 months showed the highest infection rates.
In horses, older animals (over 12 months) had a higher infection rate of E. bieneusi than younger horses.
The study identified 20 genotypes of the E. bieneusi parasite, which included six known ones and 14 new genotypes, and three assemblages of G. duodenalis.
About 45% of the E. bieneusi-positive samples belonged to the zoonotic group 1, implying they can potentially infect humans. For G. duodenalis, assemblages A and B were found in both horses and donkeys. The assemblage A isolates were all from the sub-assemblage AI, which is also zoonotic.
Conclusion
The study concluded that horses and donkeys in Northern China show common occurrence of Zoonotic E. bieneusi and G. duodenalis genotypes.
These results indicate the potential risk of transmission of these parasites to humans, making it an area of concern in public health.
The discoveries of the new genotypes of E. bieneusi also expand our existing knowledge about the genetic diversity of this parasite.
Cite This Article
APA
Li F, Wang R, Guo Y, Li N, Feng Y, Xiao L.
(2020).
Zoonotic potential of Enterocytozoon bieneusi and Giardia duodenalis in horses and donkeys in northern China.
Parasitol Res, 119(3), 1101-1108.
https://doi.org/10.1007/s00436-020-06612-8
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, China.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, 510642, China.
Wang, Rui
State Key Laboratory of Bioreactor Engineering, School of Resource and Environmental, East China University of Science and Technology, Shanghai, 200237, China.
Guo, Yaqiong
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, China.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, 510642, China.
Li, Na
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, China.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, 510642, China.
Feng, Yaoyu
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, China. yyfeng@scau.edu.cn.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, 510642, China. yyfeng@scau.edu.cn.
Xiao, Lihua
Key Laboratory of Zoonosis of Ministry of Agriculture, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Road, Guangzhou, 510642, China. lxiao1961@gmail.com.
Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, 510642, China. lxiao1961@gmail.com.
MeSH Terms
Animals
Animals, Domestic / parasitology
China / epidemiology
Enterocytozoon / classification
Enterocytozoon / genetics
Enterocytozoon / physiology
Equidae / parasitology
Feces / parasitology
Genes, Protozoan / genetics
Genotype
Giardia lamblia / classification
Giardia lamblia / genetics
Giardia lamblia / physiology
Giardiasis / epidemiology
Giardiasis / parasitology
Giardiasis / veterinary
Horses / parasitology
Host Specificity
Microsporidiosis / epidemiology
Microsporidiosis / parasitology
Microsporidiosis / veterinary
Phylogeny
Prevalence
Zoonoses / transmission
Grant Funding
31630078 / National Natural Science Foundation of China
31820103014 / National Natural Science Foundation of China
References
This article includes 36 references
Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.. Clin Microbiol Rev 2011 Jan;24(1):110-40.
Decraene V, Lebbad M, Botero-Kleiven S, Gustavsson AM, Löfdahl M. First reported foodborne outbreak associated with microsporidia, Sweden, October 2009.. Epidemiol Infect 2012 Mar;140(3):519-27.
Zahedi A, Field D, Ryan U. Molecular typing of Giardia duodenalis in humans in Queensland - first report of Assemblage E.. Parasitology 2017 Aug;144(9):1154-1161.
Wumba R, Longo-Mbenza B, Mandina M, Odio WT, Biligui S, Sala J, Breton J, Thellier M. Intestinal parasites infections in hospitalized AIDS patients in Kinshasa, Democratic Republic of Congo.. Parasite 2010 Dec;17(4):321-8.
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 Feb;42(2):197-205.
Kyaw T, Curry A, Edwards-Jones V, Craske J, Mandal BK. The prevalence of Enterocytozoon bieneusi in acquired immunodeficiency syndrome (AIDS) patients from the north west of England: 1992-1995.. Br J Biomed Sci 1997 Sep;54(3):186-91.
Sarfati C, Bourgeois A, Menotti J, Liegeois F, Moyou-Somo R, Delaporte E, Derouin F, Ngole EM, Molina JM. Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study.. Am J Trop Med Hyg 2006 Jan;74(1):162-4.
Zhang XX, Zhang FK, Li FC, Hou JL, Zheng WB, Du SZ, Zhao Q, Zhu XQ. The presence of Giardia intestinalis in donkeys, Equus asinus, in China.. Parasit Vectors 2017 Jan 3;10(1):3.
Yue DM, Ma JG, Li FC, Hou JL, Zheng WB, Zhao Q, Zhang XX, Zhu XQ. Occurrence of Enterocytozoon bieneusi in Donkeys (Equus asinus) in China: A Public Health Concern.. Front Microbiol 2017;8:565.
Bern C, Kawai V, Vargas D, Rabke-Verani J, Williamson J, Chavez-Valdez R, Xiao L, Sulaiman I, Vivar A, Ticona E, Navincopa M, Cama V, Moura H, Secor WE, Visvesvara G, Gilman RH. The epidemiology of intestinal microsporidiosis in patients with HIV/AIDS in Lima, Peru.. J Infect Dis 2005 May 15;191(10):1658-64.
Jiang J, Alderisio KA, Singh A, Xiao L. Development of procedures for direct extraction of Cryptosporidium DNA from water concentrates and for relief of PCR inhibitors.. Appl Environ Microbiol 2005 Mar;71(3):1135-41.
Lores B, del Aguila C, Arias C. Enterocytozoon bieneusi (microsporidia) in faecal samples from domestic animals from Galicia, Spain.. Mem Inst Oswaldo Cruz 2002 Oct;97(7):941-5.
Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, Roellig D, Feng Y. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China.. Parasitol Int 2014 Feb;63(1):132-7.
Liu H, Jiang Z, Yuan Z, Yin J, Wang Z, Yu B, Zhou D, Shen Y, Cao J. Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region, China.. BMC Infect Dis 2017 Oct 13;17(1):684.
Yason JA, Rivera WL. Genotyping of Giardia duodenalis isolates among residents of slum area in Manila, Philippines.. Parasitol Res 2007 Aug;101(3):681-7.
Zhong Z, Li W, Deng L, Song Y, Wu K, Tian Y, Huang X, Hu Y, Fu H, Geng Y, Ren Z, Peng G. Multilocus genotyping of Enterocytozoon bieneusi derived from nonhuman primates in southwest China.. PLoS One 2017;12(5):e0176926.
Lichtmannsperger K, Harl J, Roehl SR, Schoiswohl J, Eibl C, Wittek T, Hinney B, Wiedermann S, Joachim A. Enterocytozoon bieneusi in fecal samples from calves and cows in Austria. Parasitol Res 2023 Jan;122(1):333-340.
Koehler AV, Zhang Y, Gasser RB. A Perspective on the Molecular Identification, Classification, and Epidemiology of Enterocytozoon bieneusi of Animals. Exp Suppl 2022;114:389-415.
Mohammad Rahimi H, Mirjalali H, Zali MR. Molecular epidemiology and genotype/subtype distribution of Blastocystis sp., Enterocytozoon bieneusi, and Encephalitozoon spp. in livestock: concern for emerging zoonotic infections. Sci Rep 2021 Sep 1;11(1):17467.
Cervero-Aragó S, Desvars-Larrive A, Lindner G, Sommer R, Häfeli I, Walochnik J. Surface Waters and Urban Brown Rats as Potential Sources of Human-Infective Cryptosporidium and Giardia in Vienna, Austria. Microorganisms 2021 Jul 27;9(8).
Zhang Z, Ma J, Huang X, Wen X, Jiang W, Chen L, Li N, Guo Y, Zhang L, Xiao L, Feng Y. Population genetic analysis suggests genetic recombination is responsible for increased zoonotic potential of Enterocytozoon bieneusi from ruminants in China. One Health 2020 Dec 20;11:100184.
Yu Z, Wen X, Huang X, Yang R, Guo Y, Feng Y, Xiao L, Li N. Molecular characterization and zoonotic potential of Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium sp. in farmed masked palm civets (Paguma larvata) in southern China. Parasit Vectors 2020 Aug 8;13(1):403.
Khan MZ, Li Y, Zhu M, Li M, Wang T, Zhang Z, Liu W, Ma Q, Wang C. Advances in Donkey Disease Surveillance and Microbiome Characterization in China. Microorganisms 2025 Mar 26;13(4).
Hatam-Nahavandi K, Ahmadpour E, Badri M, Eslahi AV, Anvari D, Carmena D, Xiao L. Global prevalence of Giardia infection in nonhuman mammalian hosts: A systematic review and meta-analysis of five million animals. PLoS Negl Trop Dis 2025 Apr;19(4):e0013021.
Peng X, Wang X, Jian J, Zuo Q, Liu H, Wang Y, Su Y, Cao J, Jiang B, Shen Y. Investigation of Cryptosporidium spp. and Enterocytozoon bieneusi in free-ranged livestock on the southeastern Qinghai-Xizang Plateau, China. BMC Infect Dis 2025 Mar 13;25(1):356.
Zhang Y, Ren G, Lu Q, Li J, Qiang Y, Li Y, Lai X, Wang Y, Yu X, Lei S, Li Y, Chang Y, Liu X, Qi X, Xie Z, Li T, Du J, Duan R, Chang X, Wang H, Lu G. Prevalence and molecular characterization of Enterocytozoon bieneusi in endangered Eld's deer (Rucervus eldii) in Hainan, China. Front Vet Sci 2025;12:1521055.
Meng X, Ou Y, Jiang W, Guo Y, Xiao L, Feng Y, Li N. Identification of two new genetic loci for high-resolution genotyping of Enterocytozoon bieneusi. Parasite 2025;32:6.
Zhao L, Fan W, Yi C, Liu HX, Ding Y, Wang M, Wang Y, Zhang S, Su X, Liu Y. Prevalence and Molecular Characterization of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in Donkeys of Inner Mongolia, Northern China. Acta Parasitol 2025 Jan 22;70(1):20.
Gao ZQ, Wang HT, Hou QY, Qin Y, Qin SY, Zhao Q, Ma H. Wild rodents in three provinces of China exhibit a wide range of Enterocytozoon bieneusi diversity. Front Vet Sci 2024;11:1427690.
Jiang Y, Zhou S, Yuan Z, Hu X, Li Z, Wang Y, Shen Y, Cao J. Brown rats (Rattus norvegicus) as potential reservoirs of Enterocytozoon bieneusi in Heilongjiang Province, China: high prevalence, genetic heterogeneity, and potential risk for zoonotic transmission. Front Vet Sci 2024;11:1426384.
Zhao W, Sun L, Liu L, Jiang A, Xiao Q, Tan F. Host specificity and zoonotic Enterocytozoon bieneusi genotypes in wild rodents from the Inner Mongolian Autonomous Region and Liaoning Province of China. Front Cell Infect Microbiol 2024;14:1409685.
Zhang T, Yu K, Xu J, Cao W, Wang Y, Wang J, Zhou L, Chen J, Huang H, Zhao W. Enterocytozoon bieneusi in Wild Rats and Shrews from Zhejiang Province, China: Occurrence, Genetic Characterization, and Potential for Zoonotic Transmission. Microorganisms 2024 Apr 17;12(4).
Gao WW, Zhang S, Zhang TH, Xiao HD, Su N, Tao MF, Wu ZX, Zhang ZD, Zhu XQ, Xie SC. Prevalence and Multilocus Genotyping of Giardia duodenalis in Donkeys in Shanxi Province, North China. Animals (Basel) 2023 Dec 6;13(24).
Xu C, Tuo H, Wang W, Zhang Z, Yu F, Chuai L, Qi M, Jing B. Occurrence and genetic characteristics of Giardia duodenalis in donkeys in Xinjiang, China. Parasite 2023;30:50.
Lv C, Li C, Wang J, Qian W. Prevalence and molecular characterization of Enterocytozoon bieneusi and a new Enterocytozoon sp. in pet hairless guinea pigs (Cavia porcellus) from China. Parasite 2023;30:37.