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      Identification of Subsets of Enteroaggregative Escherichia coli Associated with Diarrheal Disease among Under 5 Years of Age Children from Rural Gambia

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          Abstract.

          Enteroaggregative Escherichia coli (EAEC) cause acute and persistent diarrhea, mostly in children worldwide. Outbreaks of diarrhea caused by EAEC have been described, including a large outbreak caused by a Shiga toxin expressing strain. This study investigated the association of EAEC virulence factors with diarrhea in children less than 5 years. We characterized 428 EAEC strains isolated from stool samples obtained from moderate-to-severe diarrhea cases (157) and healthy controls (217) children aged 0–59 months recruited over 3 years as part of the Global Enteric Multicenter Study (GEMS) in The Gambia. Four sets of multiplex polymerase chain reaction were applied to detect 21 EAEC-virulence genes from confirmed EAEC strains that target pCVD432 (aatA) and AAIC (aaiC). In addition, Kirby-Bauer disc diffusion antimicrobial susceptibility testing was performed on 88 EAEC strains following Clinical Laboratory Standard Institute guidelines. We observed that the plasmid-encoded enterotoxin [odds ratio (OR): 6.9, 95% confidence interval (CI): 2.06–29.20, P < 0.001], aggregative adherence fimbriae/I fimbriae (aggA) [OR: 2.2, 95% CI: 1.16–4.29, P = 0.008], and hexosyltransferase (capU) [OR: 1.9, 95% CI 1.02–3.51, P = 0.028] were associated with moderate-to-severe diarrhea among children < 12 months old but not in the older age strata (> 12 months). Our data suggest that some EAEC-virulent factors have age-specific associations with moderate-to-severe diarrhea in infants. Furthermore, our study showed that 85% and 72% of EAEC strains tested were resistant to sulphamethoxazole-trimethoprim and ampicillin, respectively. Sulphamethoxazole-trimethoprim and ampicillin are among the first-line antibiotics used for the treatment of diarrhea in The Gambia.

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          Most cited references44

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          Diarrheagenic Escherichia coli.

          Escherichia coli is the predominant nonpathogenic facultative flora of the human intestine. Some E. coli strains, however, have developed the ability to cause disease of the gastrointestinal, urinary, or central nervous system in even the most robust human hosts. Diarrheagenic strains of E. coli can be divided into at least six different categories with corresponding distinct pathogenic schemes. Taken together, these organisms probably represent the most common cause of pediatric diarrhea worldwide. Several distinct clinical syndromes accompany infection with diarrheagenic E. coli categories, including traveler's diarrhea (enterotoxigenic E. coli), hemorrhagic colitis and hemolytic-uremic syndrome (enterohemorrhagic E. coli), persistent diarrhea (enteroaggregative E. coli), and watery diarrhea of infants (entero-pathogenic E. coli). This review discusses the current level of understanding of the pathogenesis of the diarrheagenic E. coli strains and describes how their pathogenic schemes underlie the clinical manifestations, diagnostic approach, and epidemiologic investigation of these important pathogens.
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            Diagnostic Microbiologic Methods in the GEMS-1 Case/Control Study

            To understand the etiology of moderate-to-severe diarrhea among children in high mortality areas of sub-Saharan Africa and South Asia, we performed a comprehensive case/control study of children aged <5 years at 7 sites. Each site employed an identical case/control study design and each utilized a uniform comprehensive set of microbiological assays to identify the likely bacterial, viral and protozoal etiologies. The selected assays effected a balanced consideration of cost, robustness and performance, and all assays were performed at the study sites. Identification of bacterial pathogens employed streamlined conventional bacteriologic biochemical and serological algorithms. Diarrheagenic Escherichia coli were identified by application of a multiplex polymerase chain reaction assay for enterotoxigenic, enteroaggregative, and enteropathogenic E. coli. Rotavirus, adenovirus, Entamoeba histolytica, Giardia enterica, and Cryptosporidium species were detected by commercially available enzyme immunoassays on stool samples. Samples positive for adenovirus were further evaluated for adenovirus serotypes 40 and 41. We developed a novel multiplex assay to detect norovirus (types 1 and 2), astrovirus, and sapovirus. The portfolio of diagnostic assays used in the GEMS study can be broadly applied in developing countries seeking robust cost-effective methods for enteric pathogen detection.
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              Pathogenesis of enteroaggregative Escherichia coli infection.

              Enteroaggregative Escherichia coli (EAEC) is emerging as a significant diarrheal pathogen in multiple population groups. Although most commonly associated with pediatric diarrhea in developing countries, EAEC is also linked to diarrhea in adults including HIV-positive patients and travelers and has been a cause of food-borne outbreaks in the industrialized world. Current data suggest that one set of virulence elements is not associated with all EAEC strains, but that combinations of multiple factors prevail. Pathogenesis is believed to be initiated with adherence to the terminal ileum and colon in an aggregative, stacked-brick-type pattern by means of one of several different hydrophobic aggregative adherence fimbriae. Some strains of EAEC may then elaborate cytotoxins including the plasmid-encoded toxin and the enterotoxins, EAST1 and ShET1. An AraC homolog termed AggR regulates several genes contributing to fimbrial biogenesis in 'typical EAEC strains'. AggR has now also been shown to regulate genes on a chromosomal island. Sequencing of the EAEC type strain 042 completed at the Sanger Center has revealed two other chromosomal islands that are being explored for their pathogenetic potential. This article reviews these virulence elements and presents on-going areas of research in EAEC pathogenesis.
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                Author and article information

                Journal
                Am J Trop Med Hyg
                Am. J. Trop. Med. Hyg
                tpmd
                tropmed
                The American Journal of Tropical Medicine and Hygiene
                The American Society of Tropical Medicine and Hygiene
                0002-9637
                1476-1645
                11 October 2017
                07 August 2017
                07 August 2017
                : 97
                : 4
                : 997-1004
                Affiliations
                [1 ]Vaccines and Immunity Theme, Medical Research Council Unit The Gambia, Banjul, The Gambia;
                [2 ]Disease Control and Elimination Theme, Medical Research Council Unit The Gambia, Banjul, The Gambia;
                [3 ]Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark;
                [4 ]Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, United Kingdom;
                [5 ]Centre for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland;
                [6 ]Department of Pediatrics, University of Virginia School of Medicine, Charlottesville, Virginia;
                [7 ]Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom;
                [8 ]Microbiology and Infection Unit, Warwick Medical School, University of Warwick, Coventry, United Kingdom
                Author notes
                [* ]Address correspondence to Martin Antonio, Vaccines and Immunity Theme, Medical Research Council Unit, Atlantic Road, Fajara, Banjul, The Gambia. E-mail: mantonio@ 123456mrc.gm

                Financial support: The financial support for this study was from The Medical Research Council, (United Kingdom), and the Bill & Melinda Gates Foundation via Professor James P. Nataro who was previously at CVD-University of Maryland, Baltimore, now at the University of Virginia, Virginia.

                Authors’ addresses: Usman N. Ikumapayi, Mohammad J. Hossain, Modupeh Betts, Modou Lamin, Brenda Kwambana-Adams, Michel Dione, Anna Roca, and Martin Antonio, Medical Research Council Unit, Banjul, The Gambia, E-mails: uikumapayi@ 123456mrc.gm , jhossain@ 123456mrc.gm , mbetts@ 123456mrc.gm , mlamin@ 123456mc.gm , bkwambana@ 123456mrc.gm , m.dione@ 123456cgiar.org , aroca@ 123456mrc.gm , and mantonio@ 123456mrc.gm . Nadia Boisen, Department of Microbiological Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark, E-mail: nboboisen@ 123456gmail.com . Debasish Saha and Richard A. Adegbola, GlaxoSmithKline Vaccines, Wavre, Belgium, E-mails: debasish.x.saha@ 123456gsk.com and richard.a.adegbola@ 123456gsk.com . James P. Nataro, Department of Pediatrics, University of Virginia School of Medicine, Charlottesville, VA, E-mail: jpn2r@ 123456hscmail.mcc.virginia.edu .

                Article
                tpmd160705
                10.4269/ajtmh.16-0705
                5637583
                28820687
                a8ce45cd-af1f-4fd4-8d81-d318c8065640
                © The American Society of Tropical Medicine and Hygiene

                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.

                History
                : 29 August 2016
                : 22 May 2017
                Page count
                Pages: 8
                Categories
                Articles

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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