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

Abstract

This study investigated fecal specimens from 489 sheep and 537 cattle in multiple cities in northeast China for the prevalence and genetic characteristics of Enterocytozoon bieneusi by PCR and sequencing of the ribosomal internal transcribed spacer. Sixty-eight sheep specimens (13.9%) and 32 cattle specimens (6.0%) were positive for E. bieneusi. Sequence polymorphisms enabled the identification of 9 known genotypes (BEB4, BEB6, CM7, CS-4, EbpC, G, I, J, and OEB1) and 11 new genotypes (NESH1 to NESH6 and NECA1 to NECA5). The genotypes formed two genetic clusters in a phylogenetic analysis, with CS-4, EbpC, G, NESH1 to NESH3, and NECA1 to NECA5 distributed in zoonotic group 1 and BEB4, BEB6, CM7, EbpI, J, OEB1, and NESH4 to NESH6 distributed in potentially host-adapted group 2. Nearly 70% of cases of E. bieneusi infections in sheep were contributed by human-pathogenic genotypes BEB6, CS-4, and EbpC, and over 80% of those in cattle were by genotypes BEB4, CS-4, EbpC, I, and J. The cooccurrence of genotypes BEB4, CS-4, EbpC, I, and J in domestic ruminants and children in northeast China and the identification of BEB6 and EbpC in humans and water in central China imply the possibility of zoonotic transmission. This study also summarizes E. bieneusi genotypes obtained from ruminants worldwide and displays their host ranges, geographical distributions, and phylogenetic relationships. The data suggest a host range expansion in some group 2 genotypes (notably BEB4, BEB6, I, and J) that were previously considered to be adapted to ruminants. We should be concerned about the increasing zoonotic importance of group 2 genotypes with low host specificity. Microsporidia are a large and diverse group of obligately intracellular parasites that have been implicated as both human and animal pathogens (1). These parasitic protists are genetically related to fungi and feature environmentally resistant spore forms (1). Microsporidia differentiate from meronts into spores that are then defecated by the host into the environment and start a new round of eukaryotic cell invasion by using a highly specialized organelle, the polar tube, followed by intracellular replication (2). Of approximately 1,300 microsporidian species in 160 genera reported thus far, 14 species in 8 genera have been documented in human infections (3). Enterocytozoon bieneusi has emerged as an opportunistic pathogen leading to infectious diarrhea in humans; it has been associated with immune suppression and is responsible for almost 90% of reported cases of human microsporidiosis (4). It also affects immunocompetent individuals and a variety of domestic and wild animals, and even birds (4). Contact with infected humans and animals or contaminated food and water may contribute to the acquisition of E. bieneusi infections (1, 5-7).At present, genotyping of E. bieneusi on the basis of the ribosomal internal transcribed spacer (ITS) has characterized over 200 distinct genotypes (5). The genotype nomenclature used here is according to the established naming system (8). Cou...

Molecular Characterization and Phylogenetic Analysis of Enterocytozoon bieneusi in Lambs in Oromia Special Zone, Central Ethiopia

“…In the present study, E. bieneusi was found in 10.03% of lambs in Central Ethiopia. Similar rate of infection was reported for E. bieneusi in sheep in Northeast China (13.9%, 68/489) (11), Southwest China (10.6%, 70/661) (12), and Egypt (11.2%, 10/89) (13); while lower infection rates were detected in sheep in East-central China (3.4%, 28/832) (14) and Slovakia (0/33) (15). However, a higher prevalence of E. bieneusi was found in Inner Mongolian (China) lambs (77.8%, 126/162) (16), Swedish lambs (68%, 49/72) (17), Brazilian sheep (19.2%, 24/125) (18), and in sheep from some other studies in China (19)(20)(21)(22).…”

“…Many other studies demonstrated that the genotype BEB6 was the dominant E. Bieneusi genotype in sheep in Sweden (17), Brazil (18), and China (16,21). Although this genotype was considered to be cattle-specific, it is now recognized as a dominant genotype in humans, animals and birds in a wide geographic distribution, and has zoonotic potential (11,17,19,24,25). Genotypes COS-I and COS-II, commonly reported in cattle, sheep, deer, and non-human primates in previous studies (2,14,26,27), were recognized as the known E. bieneusi genotypes.…”

Molecular detection of Enterocytozoon bieneusi in farm-raised pigs in Hainan Province, China: infection rates, genotype distributions, and zoonotic potential

“…GenBank accession no. 2 11 14 31 32 82 96 132 137 138 142 144 148 159 197 224 including non-human primates [14], sheep [13], and horses [32]. It was shown that genotype CS-4 has the ability to infect humans, particularly children [51], and has been found in river water [11].…”

Molecular characterization and multilocus genotypes of Enterocytozoon bieneusi among horses in southwestern China

“…To date, more than 240 genotypes have been identified in various animal hosts [6, 9]. By phylogenetic analysis, the ITS genotypes of E. bieneusi have been divided into nine different groups [10, 11].…”