Concurrent Infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in Children during a Cryptosporidiosis Outbreak in a Pediatric Hospital in China

Wang, Lin; Xiao, Lihua; Duan, Liping; Ye, Jianbin; Guo, Yaqiong; Guo, Meijin; Liu, Huan; Feng, Yaoyu

doi:10.1371/journal.pntd.0002437

Cited by 175 publications

(167 citation statements)

References 29 publications

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“…The extent of genetic relationships among E. bieneusi genotypes identified in this study was evaluated by molecular phylogenetic analysis using the neighbor-joining method, which showed clustering of the known genotypes CS-4 (subgroup 1e), EbpC (1d), Henan-IV (1d), and the new genotypes NEC1 (1d), NEC2 (1d), NEC3 (1e), NEC4 (1d), and NEC5 (1e) in genetic group 1 with the zoonotic potential described by Thellier and Breton (4) (8), genotypes D, EbpA, EbpC, Henan-I (reported as SH7), IV (reported as SH12), Peru11, SH1 to SH4, SH6, and SH8 to SH11 in children in the city of Shanghai in central China (9), and some other genotypes previously reported in humans and pigs in other geographic areas of the world (3). Zoonotic potential and public health significance.…”

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confidence: 97%

“…Genotypic typing and phylogenetic analysis facilitated classification of the almost 200 genotypes identified thus far into genetic group 1 with zoonotic potential and several other host-adapted genetic clusters (4)(5)(6)(7). Infections with E. bieneusi in humans have been repeatedly reported worldwide, although epidemiologic data to indicate the prevalence and risk of human microsporidiosis in China are limited (8)(9)(10). The frequent and close contact of humans with livestock in China is of potential zoonotic concern (6,7).…”

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Enterocytozoon bieneusi Genotypes in Children in Northeast China and Assessment of Risk of Zoonotic Transmission

et al. 2014

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The prevalence (7.5%, 19/255) and genotypes of Enterocytozoon bieneusi in children of various age categories and clinical presentations were determined herein. The co-occurrence of the known genotypes (CS-4, EbpC, and Henan-IV) in children and pigs in the same study area, the phylogenetic characterization of novel genotypes (NEC1 to NEC5), and the assessment of potential risk factors associated with zoonotic transmission robustly suggested that pigs could be a significant source of human E. bieneusi infections in northeast China. Enterocytozoon bieneusi, a ubiquitous unicellular microsporidian fungal pathogen with a broad host range, infects many species of humans, livestock, wildlife, and birds and causes significant infectious diarrhea in immunocompromised hosts, notably AIDS patients and children (1-3). Approximately 90% of reported cases of human microsporidiosis are caused by E. bieneusi; the risk factors for infections include an immunosuppressive condition (AIDS patients), young age (children), and contact with contaminated food and water and other infected humans and animals (1).Investigations of both human and animal samples for E. bieneusi genotypes that rely on hypermutation of the ribosomal internal transcribed spacer (ITS) have been helpful in elucidating the transmission routes of microsporidiosis (3). Genotypic typing and phylogenetic analysis facilitated classification of the almost 200 genotypes identified thus far into genetic group 1 with zoonotic potential and several other host-adapted genetic clusters (4-7). Infections with E. bieneusi in humans have been repeatedly reported worldwide, although epidemiologic data to indicate the prevalence and risk of human microsporidiosis in China are limited (8-10). The frequent and close contact of humans with livestock in China is of potential zoonotic concern (6, 7). This study investigated 255 fecal specimens from children in the cities of Harbin and Daqing in northeast China for E. bieneusi genotypes and analyzed the risk for potentially zoonotic transmission of microsporidiosis.Study population. Fecal specimens (n ϭ 255) from children (one specimen per child) were collected in a community hospital (IH) (n ϭ 40), two nursery schools (NS) (NS1, n ϭ 20; NS2, n ϭ 17), and a primary school (PS) (PS1, n ϭ 57) in suburban Harbin in June 2013 and in four primary schools (PS2, n ϭ 41; PS3, n ϭ 11; PS4, n ϭ 29; PS5, n ϭ 40) in suburban Daqing in July 2014 (Table 1). Only four children in the community hospital had diarrhea, while the others had nongastrointestinal illnesses. The nursery and primary school children were all healthy at the time of sampling. The specimens were divided into four age groups: group I included 31 preweaned in-hospital children Ͻ1 year of age; group II included nine weaned in-hospital children aged 1 to 3 years; group III included 37 nursery school children aged 3 to 6 years; and group IV included 178 primary school children aged 6 to 12 years (Table 1). Background information on age, gender, and clinical presentations (diarrhea or ...

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Enterocytozoon bieneusi Genotypes in Children in Northeast China and Assessment of Risk of Zoonotic Transmission

et al. 2014

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“…Foodborne disease outbreaks linked to multiple pathogens could be common yet are rarely reported (Berkelman et al, 1983;Naimi et al, 2003;Wang et al, 2013). In this case, multiple pathogens were detected in the specimens from the outbreak.…”

Section: Discussionmentioning

confidence: 79%

A Large Outbreak of Salmonellosis Associated with Sandwiches Contaminated with Multiple Bacterial Pathogens Purchased via an Online Shopping Service

Wei

Huang

Liao

et al. 2014

Foodborne Pathogens and Disease

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Food sold over the internet is an emerging business that also presents a concern with regard to food safety. A nationwide foodborne disease outbreak associated with sandwiches purchased from an online shop in July 2010 is reported. Consumers were telephone interviewed with a structured questionnaire and specimens were collected for etiological examination. A total of 886 consumers were successfully contacted and completed the questionnaires; 36.6% had become ill, with a median incubation period of 18 h (range, 6-66 h). The major symptoms included diarrhea (89.2%), abdominal pain (69.8%), fever (47.5%), headache (32.7%), and vomiting (17.3%). Microbiological laboratories isolated Salmonella enterica serovar Enteritidis, Salmonella Virchow, Staphylococcus aureus, Bacillus cereus, and enterotoxigenic Escherichia coli from the contaminated sandwiches, Salmonella Enteritidis and Salmonella Virchow from the patients, and Salmonella Enteritidis and Staphylococcus aureus from food handlers. Pulsed-field gel electrophoresis genotyping suggested a common origin of Salmonella bacteria recovered from the patients, food, and a food handler. Among the pathogens detected, the symptoms and incubation period indicated that Salmonella, likely of egg origin, was the probable causative agent of the outbreak. This outbreak illustrates the importance of meticulous hygiene practices during food preparation and temperature control during food shipment and the food safety challenges posed by online food-shopping services.

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“…BEB6 was the most frequently found genotype, accounting for 28% (13/46) of all positive samples. To date, BEB6 has been usually derived from animals (especially sheep and cattle) (Ye et al 2015, Zhao et al 2015, but also identified in human and nonhuman primates in Henan Province (Wang et al 2013, Karim et al 2014b. Genotypes I and J reported in captive wildlife in Zhengzhou had also been detected in humans in Jilin, China (Zhang et al 2011).…”

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confidence: 99%

Zoonotic Enterocytozoon bieneusi in raw wastewater in Zhengzhou, China

Xiao-ming

et al. 2017

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Contamination of Enterocytozoon bieneusi Desportes, Charpentier, Galian, Bernard, Cochand-Priollet, Laverne, Ravisse, et Modigliani, 1985 in water sources may cause outbreaks of microsporidiosis. To examine the occurrence of E. bieneusi, 108 raw wastewater samples were collected from three wastewater treated plants in Zhengzhou, China. In total, 46 samples were PCR positive for E. bieneusi. A total of 15 ITS genotypes was identified, including ten known genotypes (D, BEB6, I, J, PigEbIX, PigEBITS5, EbpA, Peru6, Peru8, Type IV) and five novel genotypes (HNWW1, HNWW2, HNWW3, HNWW4, HNWW5). Nine genotypes belonged to a known zoonotic group (group 1) and the other genotypes belonged to potential zoonotic group (group 2). Most of the genotypes had been identified in wildlife or domestic animals in former reports in Zhengzhou. The occurrence of E. bieneusi in wastewater was probably related to the rainfall day before sampling. Of 36 sampling days, 20 days had rainfall on the previous day and 16 days had none. As many as 43 of 60 samples were found to be E. bieneusi-positive in the 20 days which had rainfall on the previous day. Only three of 48 samples were found to be E. bieneusi-positive in the 16 days without rainfall the day before. The significant difference of the occurrence of E. bieneusi was observed between wet days and dry days by t-test (43/60 vs 3/48, p < 0.01). This indicates that the occurrence of E. bieneusi in wastewater in Zhengzhou mainly originated from animals and was probably related to rainfall the day before sample collection. Given the zoonotic genotypes detected in wastewater, animal faeces should be treated appropriately before being drained into the water source.

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Concurrent Infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in Children during a Cryptosporidiosis Outbreak in a Pediatric Hospital in China

Cited by 175 publications

References 29 publications

Enterocytozoon bieneusi Genotypes in Children in Northeast China and Assessment of Risk of Zoonotic Transmission

Enterocytozoon bieneusi Genotypes in Children in Northeast China and Assessment of Risk of Zoonotic Transmission

A Large Outbreak of Salmonellosis Associated with Sandwiches Contaminated with Multiple Bacterial Pathogens Purchased via an Online Shopping Service

Zoonotic Enterocytozoon bieneusi in raw wastewater in Zhengzhou, China

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