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      Prevalence and Risk Factors for Intestinal Protozoan Infections with Cryptosporidium, Giardia, Blastocystis and Dientamoeba among Schoolchildren in Tripoli, Lebanon

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          Abstract

          Background

          Intestinal protozoan infections are confirmed as major causes of diarrhea, particularly in children, and represent a significant, but often neglected, threat to public health. No recent data were available in Lebanon concerning the molecular epidemiology of protozoan infections in children, a vulnerable population at high risk of infection.

          Methodology and Principal Findings

          In order to improve our understanding of the epidemiology of intestinal pathogenic protozoa, a cross-sectional study was conducted in a general pediatric population including both symptomatic and asymptomatic subjects. After obtaining informed consent from the parents or legal guardians, stool samples were collected in January 2013 from 249 children in 2 schools in Tripoli, Lebanon. Information obtained from a standard questionnaire included demographic characteristics, current symptoms, socioeconomic status, source of drinking water, and personal hygiene habits. After fecal examination by both microscopy and molecular tools, the overall prevalence of parasitic infections was recorded as 85%. Blastocystis spp. presented the highest infection rate (63%), followed by Dientamoeba fragilis (60.6%), Giardia duodenalis (28.5%) and Cryptosporidium spp. (10.4%). PCR was also performed to identify species and genotypes of Cryptosporidium, subtypes of Blastocystis, and assemblages of Giardia. Statistical analysis using a logistic regression model showed that contact with family members presenting gastrointestinal disorders was the primary risk factor for transmission of these protozoa.

          Conclusions

          This is the first study performed in Lebanon reporting the prevalence and the clinical and molecular epidemiological data associated with intestinal protozoan infections among schoolchildren in Tripoli. A high prevalence of protozoan parasites was found, with Blastocystis spp. being the most predominant protozoans. Although only 50% of children reported digestive symptoms, asymptomatic infection was observed, and these children may act as unidentified carriers. This survey provides necessary information for designing prevention and control strategies to reduce the burden of these protozoan infections, especially in children.

          Author Summary

          Intestinal parasites can infect the gastrointestinal tract of humans. Means of exposure include ingestion of contaminated fruits and vegetables, consumption of infected water and personal contact. Protozoa are considered one of the major groups of parasites. Children are particularly susceptible to infection by these microorganisms, and when they are infected, diarrhea can be the main clinical manifestation. In developing countries, people are at particular risk of infection. However, intestinal parasites, and in particular protozoans, have been taken into account only in a few epidemiological studies. Thus, we conducted an investigation to determine the prevalence, risk factors, and epidemiological information associated with 4 intestinal protozoan infections: Cryptosporidium, Giardia, Blastocystis and Dientamoeba, among children attending two schools of Tripoli, Lebanon. A high prevalence of protozoan parasites was found. Although only 50% of children reported digestive symptoms, asymptomatic infection was observed very often, suggesting that these children may act as unknown carriers. In addition, we found that personal contact plays an important role as a risk factor associated with protozoan infection. This epidemiological survey shows the burden of parasitic infections in Lebanese children and provides necessary information to public health authorities for creating prevention and control strategies.

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          Most cited references 77

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          Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study.

          Diarrhoeal diseases cause illness and death among children younger than 5 years in low-income countries. We designed the Global Enteric Multicenter Study (GEMS) to identify the aetiology and population-based burden of paediatric diarrhoeal disease in sub-Saharan Africa and south Asia. The GEMS is a 3-year, prospective, age-stratified, matched case-control study of moderate-to-severe diarrhoea in children aged 0-59 months residing in censused populations at four sites in Africa and three in Asia. We recruited children with moderate-to-severe diarrhoea seeking care at health centres along with one to three randomly selected matched community control children without diarrhoea. From patients with moderate-to-severe diarrhoea and controls, we obtained clinical and epidemiological data, anthropometric measurements, and a faecal sample to identify enteropathogens at enrolment; one follow-up home visit was made about 60 days later to ascertain vital status, clinical outcome, and interval growth. We enrolled 9439 children with moderate-to-severe diarrhoea and 13,129 control children without diarrhoea. By analysing adjusted population attributable fractions, most attributable cases of moderate-to-severe diarrhoea were due to four pathogens: rotavirus, Cryptosporidium, enterotoxigenic Escherichia coli producing heat-stable toxin (ST-ETEC; with or without co-expression of heat-labile enterotoxin), and Shigella. Other pathogens were important in selected sites (eg, Aeromonas, Vibrio cholerae O1, Campylobacter jejuni). Odds of dying during follow-up were 8·5-fold higher in patients with moderate-to-severe diarrhoea than in controls (odd ratio 8·5, 95% CI 5·8-12·5, p<0·0001); most deaths (167 [87·9%]) occurred during the first 2 years of life. Pathogens associated with increased risk of case death were ST-ETEC (hazard ratio [HR] 1·9; 0·99-3·5) and typical enteropathogenic E coli (HR 2·6; 1·6-4·1) in infants aged 0-11 months, and Cryptosporidium (HR 2·3; 1·3-4·3) in toddlers aged 12-23 months. Interventions targeting five pathogens (rotavirus, Shigella, ST-ETEC, Cryptosporidium, typical enteropathogenic E coli) can substantially reduce the burden of moderate-to-severe diarrhoea. New methods and accelerated implementation of existing interventions (rotavirus vaccine and zinc) are needed to prevent disease and improve outcomes. The Bill & Melinda Gates Foundation. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'.

            Giardia and Cryptosporidium are ubiquitous enteric protozoan pathogens that infect humans, domestic animals and wildlife worldwide. Both pathogens are significant causes of diarrhea and nutritional disorders in institutional and community settings. They are also significant waterborne pathogens. In developing regions of the world, Giardia and Cryptosporidium constitute part of the complex group of parasitic, bacterial and viral diseases that impair the ability to achieve full potential and impair development and socio-economic improvements. All diseases included in the WHO Neglected Diseases Initiative have a common link with poverty and, as the current view is to take a comprehensive approach to all these diseases, both Giardia and Cryptosporidium were included in 2004. Our current state of knowledge of Giardia and Cryptosporidium is summarized here, and some important questions are raised that need to be addressed if control strategies are to be effective.
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              New insights on classification, identification, and clinical relevance of Blastocystis spp.

               Kevin S W Tan (2008)
              Blastocystis is an unusual enteric protozoan parasite of humans and many animals. It has a worldwide distribution and is often the most commonly isolated organism in parasitological surveys. The parasite has been described since the early 1900s, but only in the last decade or so have there been significant advances in our understanding of Blastocystis biology. However, the pleomorphic nature of the parasite and the lack of standardization in techniques have led to confusion and, in some cases, misinterpretation of data. This has hindered laboratory diagnosis and efforts to understand its mode of reproduction, life cycle, prevalence, and pathogenesis. Accumulating epidemiological, in vivo, and in vitro data strongly suggest that Blastocystis is a pathogen. Many genotypes exist in nature, and recent observations indicate that humans are, in reality, hosts to numerous zoonotic genotypes. Such genetic diversity has led to a suggestion that previously conflicting observations on the pathogenesis of Blastocystis are due to pathogenic and nonpathogenic genotypes. Recent epidemiological, animal infection, and in vitro host-Blastocystis interaction studies suggest that this may indeed be the case. This review focuses on such recent advances and also provides updates on laboratory and clinical aspects of Blastocystis 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, CA USA )
                1935-2727
                1935-2735
                14 March 2016
                March 2016
                : 10
                : 3
                Affiliations
                [1 ]Institute Pasteur de Lille, Centre d’Infection et d’Immunitè de Lille (CIIL), UMR CNRS 8204, Inserm U1019, Université de Lille, Biologie et Diversitè des Pathogènes Eucaryotes Emergents (BDPEE), Lille, France
                [2 ]Centre AZM pour la recherche en biotechnologies et ses applications, Universitè Libanaise, Laboratoire de Microbiologie Santè et Environnement (LMSE), Tripoli, Lebanon
                [3 ]Faculté de Santé Publique, Université Libanaise, Beirut, Lebanon
                [4 ]Facultè Libre des Sciences et Technologies de Lille, Universitè Catholique de Lille, Universitè de Lille, Laboratoire Ecologie et Biodiversitè, Lille, France
                [5 ]Clermont Université, Université Blaise Pascal-Université d'Auvergne-CNRS, UMR 6023 Laboratoire Microorganismes: Génome et Environnement, Clermont-Ferrand, France
                [6 ]Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire Gabriel-Montpied, Clermont-Ferrand, France
                [7 ]CHU Clermont-Ferrand, Unité de Biostatistiques, Direction de la Recherche Clinique, Clermont-Ferrand, France
                [8 ]EA 3800, Université de Rouen & Centre Hospitalier Universitaire Charles Nicolle, Rouen, France
                [9 ]Institute Pasteur de Lille, Unité de Sécurité Microbiologique, Lille, France
                [10 ]Département de la Recherche Médicale, Groupement des Hôpitaux de l’Institut Catholique de Lille, Faculté de Médecine et Maïeutique, Université Catholique de Lille, France
                Barcelona Institute for Global Health, SPAIN
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SB FDa LF MH EV GC. Performed the experiments: MO DES AC RR. Analyzed the data: MO DES AC SB CN PP BP RR AP CL IW FDe LF EV GC. Contributed reagents/materials/analysis tools: FDa FDe LF EV. Wrote the paper: MO DES AC PP BP EV GC.

                Article
                PNTD-D-15-01009
                10.1371/journal.pntd.0004496
                4790957
                26974335
                © 2016 Osman et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 2, Tables: 2, Pages: 17
                Product
                Funding
                This work was supported by the Programme Orientations Stratégiques of the University of Lille. It was also supported by the Institut Pasteur de Lille and the Centre National de la Recherche Scientifique. MO and DES were supported by Ph.D. fellowships from the Conseil National de la Recherche Scientifique and the Azm & Saade Association of Lebanon. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                People and Places
                Population Groupings
                Age Groups
                Children
                People and Places
                Population Groupings
                Families
                Children
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Blastocystis
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Cryptosporidium
                Biology and Life Sciences
                Organisms
                Protozoans
                Cryptosporidium
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Dientamoeba Fragilis
                Medicine and Health Sciences
                Gastroenterology and Hepatology
                Gastrointestinal Infections
                Medicine and Health Sciences
                Gastroenterology and Hepatology
                Diarrhea
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Diarrhea
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Custom metadata
                All sequences were uploaded to NCBI GenBank (accession numbers KU311720-KU311975).

                Infectious disease & Microbiology

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