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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

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          Abstract

          Background

          Over 200 cryptosporidiosis outbreaks have been reported, but little is known if other enteric pathogens were also involved in some of these outbreaks. Recently, an outbreak of cryptosporidiosis linked to poor hygiene by two Cryptosporidium hominis subtypes occurred in a pediatric hospital ward (Ward A) in China, lasting for more than 14 months. In this study, the concurrence during the outbreak of three other enteric pathogens with a similar transmission route, Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile, was assessed.

          Methods/Principal Findings

          The occurrence of G. duodenalis, E. bieneusi, and C. difficile in 78 inpatients from Ward A and 283 and 216 inpatients from two control wards (Wards C and D) in the same hospital was examined using molecular diagnostic tools. Significantly higher infection rates were found in children in Ward A for all study pathogens than in Wards C and D ( P<0.01): 9.5% versus 1.4% and 0% for G. duodenalis, 10.8% versus 2.8% and 3.7% for E. bieneusi, and 60.8% versus 37.8% and 27.8% for C. difficile, respectively. These differences were mostly seen in children ≤12 months. Enteric pathogen-positive children in Ward A (31/58 or 53.4%) were more likely to have mixed infections than those in Ward C (4/119 or 3.4%) or D (5/68, 7.4%; P<0.01). Having cryptosporidiosis was a risk factor for G. duodenalis (OR = 4.3; P = 0.08), E. bieneusi (OR = 3.1; P = 0.04), and C. difficile (OR = 4.7; P<0.01) infection. In addition, a lower diversity of G. duodenalis, E. bieneusi, and C. difficile genotypes/subtypes was observed in Ward A.

          Conclusions/Significance

          Data from this study suggest that multiple pathogens were concurrently present during the previous cryptosporidiosis outbreak. Examination of multiple enteric pathogens should be conducted when poor hygiene is the likely cause of outbreaks of diarrhea.

          Author Summary

          The transmission of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile is poorly understood in developing countries despite their wide occurrence. Because they are transmitted by the same fecal-oral route as Cryptosporidium, in this study, we have examined the occurrence of these enteric pathogens in children during a cryptosporidiosis outbreak in a pediatric hospital in China. Using molecular diagnostic tools, we have detected significantly higher infection rates of these enteric pathogens in the outbreak ward than in two control wards in the same hospital. We have also shown a much higher occurrence of these pathogens in children having cryptosporidiosis than those having no cryptosporidiosis. We have demonstrated that the genetic diversity of enteric pathogens is much lower in the outbreak ward than in control wards. Therefore, other enteric pathogens are concurrently present during the cryptosporidiosis outbreak, and examinations for multiple enteric pathogens should be conducted when poor hygiene is considered the likely cause of outbreaks of diarrhea.

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          Most cited references 28

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          Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.

          Molecular diagnostic tools have been used recently in assessing the taxonomy, zoonotic potential, and transmission of Giardia species and giardiasis in humans and animals. The results of these studies have firmly established giardiasis as a zoonotic disease, although host adaptation at the genotype and subtype levels has reduced the likelihood of zoonotic transmission. These studies have also identified variations in the distribution of Giardia duodenalis genotypes among geographic areas and between domestic and wild ruminants and differences in clinical manifestations and outbreak potentials of assemblages A and B. Nevertheless, our efforts in characterizing the molecular epidemiology of giardiasis and the roles of various animals in the transmission of human giardiasis are compromised by the lack of case-control and longitudinal cohort studies and the sampling and testing of humans and animals living in the same community, the frequent occurrence of infections with mixed genotypes and subtypes, and the apparent heterozygosity at some genetic loci for some G. duodenalis genotypes. With the increased usage of multilocus genotyping tools, the development of next-generation subtyping tools, the integration of molecular analysis in epidemiological studies, and an improved understanding of the population genetics of G. duodenalis in humans and animals, we should soon have a better appreciation of the molecular epidemiology of giardiasis, the disease burden of zoonotic transmission, the taxonomy status and virulences of various G. duodenalis genotypes, and the ecology of environmental contamination.
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            Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt.

            At least 325 water-associated outbreaks of parasitic protozoan disease have been reported. North American and European outbreaks accounted for 93% of all reports and nearly two-thirds of outbreaks occurred in North America. Over 30% of all outbreaks were documented from Europe, with the UK accounting for 24% of outbreaks, worldwide. Giardia duodenalis and Cryptosporidium parvum account for the majority of outbreaks (132; 40.6% and 165; 50.8%, respectively), Entamoeba histolytica and Cyclospora cayetanensis have been the aetiological agents in nine (2.8%) and six (1.8%) outbreaks, respectively, while Toxoplasma gondii and Isospora belli have been responsible for three outbreaks each (0.9%) and Blastocystis hominis for two outbreaks (0.6%). Balantidium coli, the microsporidia, Acanthamoeba and Naegleria fowleri were responsible for one outbreak, each (0.3%). Their presence in aquatic ecosystems makes it imperative to develop prevention strategies for water and food safety. Human incidence and prevalence-based studies provide baseline data against which risk factors associated with waterborne and foodborne transmission can be identified. Standardized methods are required to maximize public health surveillance, while reporting lessons learned from outbreaks will provide better insight into the public health impact of waterborne pathogenic protozoa.
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              Triosephosphate Isomerase Gene Characterization and Potential Zoonotic Transmission of Giardia duodenalis

              To address the source of infection in humans and public health importance of Giardia duodenalis parasites from animals, nucleotide sequences of the triosephosphate isomerase (TPI) gene were generated for 37 human isolates, 15 dog isolates, 8 muskrat isolates, 7 isolates each from cattle and beavers, and 1 isolate each from a rat and a rabbit. Distinct genotypes were found in humans, cattle, beavers, dogs, muskrats, and rats. TPI and small subunit ribosomal RNA (SSU rRNA) gene sequences of G. microti from muskrats were also generated and analyzed. Phylogenetic analysis on the TPI sequences confirmed the formation of distinct groups. Nevertheless, a major group (assemblage B) contained most of the human and muskrat isolates, all beaver isolates, and the rabbit isolate. These data confirm that G. duodenalis from certain animals can potentially infect humans and should be useful in the detection, differentiation, and taxonomy of Giardia spp.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                September 2013
                12 September 2013
                : 7
                : 9
                Affiliations
                [1 ]State Key Laboratory of Bioreactor Engineering, School of Resources and Environmental Engineering, East China University of Science and Technology, Shanghai, People's Republic of China
                [2 ]Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
                Christian Medical College, India
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LX YF. Performed the experiments: LW LD JY YG. Analyzed the data: LW LX MG LL YF. Wrote the paper: LW LX MG LL YF.

                Article
                PNTD-D-13-00393
                10.1371/journal.pntd.0002437
                3772047
                24069491

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Pages: 9
                Funding
                This work was supported by the National Natural Science Foundation of China (No. 31110103901, 31229005, 41001316); the National Basic Research Program of China (973 Project No. 2011CB200903); and Fundamental Research Funds for the Central Universities, China. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article

                Infectious disease & Microbiology

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