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      Visitors to a Tropical Marine Beach Show Evidence of Immunoconversions to Multiple Waterborne Pathogens

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          Abstract

          Determining infections from environmental exposures, particularly from waterborne pathogens is a challenging proposition. The study design must be rigorous and account for numerous factors including study population selection, sample collection, storage, and processing, as well as data processing and analysis. These challenges are magnified when it is suspected that individuals may potentially be infected by multiple pathogens at the same time. Previous work demonstrated the effectiveness of a salivary antibody multiplex immunoassay in detecting the prevalence of immunoglobulin G (IgG) antibodies to multiple waterborne pathogens and helped identify asymptomatic norovirus infections in visitors to Boquerón Beach, Puerto Rico. In this study, we applied the immunoassay to three serially collected samples from study participants within the same population to assess immunoconversions (incident infections) to six waterborne pathogens: Helicobacter pylori, Campylobacter jejuni, Toxoplasma gondii, hepatitis A virus, and noroviruses GI. I and GII.4. Further, we examined the impact of sampling on the detection of immunoconversions by comparing the traditional immunoconversion definition based on two samples to criteria developed to capture trends in three sequential samples collected from study participants. The expansion to three samples makes it possible to capture the IgG antibody responses within the survey population to more accurately assess the frequency of immunoconversions to target pathogens. Based on the criteria developed, results showed that when only two samples from each participant were used in the analysis, 25.9% of the beachgoers immunoconverted to at least one pathogen; however, the addition of the third sample reduced immunoconversions to 6.5%. Of these incident infections, the highest levels were to noroviruses followed by T. gondii. Moreover, many individuals displayed evidence of immunoconversions to multiple pathogens. This study suggests that detection of simultaneous infections is possible, with far reaching consequences for the population. The results may lead to further studies to understand the complex interactions that occur within the body as the immune system attempts to ward off these infections. Such an approach is critical to our understanding of medically important synergistic or antagonistic interactions and may provide valuable and critical information to public health officials, water treatment personnel, and environmental managers.

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          Most cited references38

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          The nature and consequences of coinfection in humans

          Summary Objective Many fundamental patterns of coinfection (multi-species infections) are undescribed, including the relative frequency of coinfection by various pathogens, differences between single-species infections and coinfection, and the burden of coinfection on human health. We aimed to address the paucity of general knowledge on coinfection by systematically collating and analysing data from recent publications to understand the types of coinfection and their effects. Methods From an electronic search to find all publications from 2009 on coinfection and its synonyms in humans we recorded data on i) coinfecting pathogens and their effect on ii) host health and iii) intensity of infection. Results The most commonly reported coinfections differ from infections causing highest global mortality, with a notable lack of serious childhood infections in reported coinfections. We found that coinfection is generally reported to worsen human health (76% publications) and exacerbate infections (57% publications). Reported coinfections included all kinds of pathogens, but were most likely to contain bacteria. Conclusions These results suggest differences between coinfected patients and those with single infections, with coinfection having serious health effects. There is a pressing need to quantify the tendency towards negative effects and to evaluate any sampling biases in the coverage of coinfection research.
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            Suppression of non-specific binding in serological Luminex assays.

            Bead-based suspension array technology (xMAP, Luminex Corp.) permits the simultaneous analysis of antibodies with specificities for up to 100 different antigens in a single reaction and the high through-put screening of up to 1,000 sera per day. Therefore, this technology is becoming more and more popular for serological analyses, replacing ELISA techniques at least for epidemiological purposes. However, a major intrinsic problem of Luminex technology is that human sera may contain antibodies that directly bind to the beads, resulting in intolerably high non-specific background. The proportion of such "bead binders" in different serum panels frequently exceeds 5% and is therefore a severe problem. We screened for background inhibitors and found that serum pre-incubation with polyvinylalcohol, polyvinylpyrrolidone and a proprietary reagent (Super ChemiBlock, Chemicon) significantly reduced non-specific background, whereas use of Luminex SeroMap beads only partially solved the problem.
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              Spectrum of enteropathogens detected by the FilmArray GI Panel in a multicentre study of community-acquired gastroenteritis.

              The European, multicentre, quarterly point-prevalence study of community-acquired diarrhoea (EUCODI) analysed stool samples received at ten participating clinical microbiology laboratories (Austria, Finland, France, Germany, Greece, Ireland, Italy, Portugal, Romania, and the UK) in 2014. On four specified days, each local laboratory submitted samples from ≤20 consecutive patients to the Austrian Study Centre for further testing with the FilmArray GI Panel (BioFire Diagnostics, Salt Lake City, UT, USA). Of the 709 samples from as many patients received, 325 (45.8%) tested negative, 268 (37.8%) yielded only one organism, and 116 (16.4%) yielded multiple organisms. Positivity rates ranged from 41% (30 of 73 samples) in France to 74% (59 of 80 samples) in Romania. With the exception of Entamoeba histolytica and Vibrio cholerae, all of the 22 targeted pathogens were detected at least once. Enteropathogenic Escherichia coli, Campylobacter species, toxigenic Clostridium difficile, enteroaggregative E. coli, norovirus and enterotoxigenic E. coli were the six most commonly detected pathogens. When tested according to local protocols, seven of 128 positive samples (5.5%) yielded multiple organisms. Overall, the FilmArray GI Panel detected at least one organism in 54.2% (384/709) of the samples, as compared with 18.1% (128/709) when testing was performed with conventional techniques locally. This underlines the considerable potential of multiplex PCR to improve routine stool diagnostics in community-acquired diarrhoea. Classic culture methods directed at the isolation of specific pathogens are increasingly becoming second-line tools, being deployed when rapid molecular tests give positive results. This optimizes the yield from stool examinations and dramatically improves the timeliness of diagnosis.
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                Author and article information

                Contributors
                Journal
                Front Public Health
                Front Public Health
                Front. Public Health
                Frontiers in Public Health
                Frontiers Media S.A.
                2296-2565
                19 August 2019
                2019
                : 7
                : 231
                Affiliations
                [1] 1Department of Arts & Sciences/Learning Support, Fort Valley State University , Fort Valley, GA, United States
                [2] 2National Risk Management Research Laboratory, U.S. Environmental Protection Agency , Cincinnati, OH, United States
                [3] 3Oak Ridge Institute for Science Education , Oak Ridge, TN, United States
                [4] 4National Exposure Research Laboratory, U.S. Environmental Protection Agency , Cincinnati, OH, United States
                [5] 5National Health and Environmental Effects Research Laboratory , Research Triangle Park, NC, United States
                Author notes

                Edited by: Ethel Eljarrat, Institute of Environmental Assessment and Water Research (CSIC), Spain

                Reviewed by: Jill Stewart, University of North Carolina at Chapel Hill, United States; M. Jahangir Alam, University of Houston, United States

                *Correspondence: Swinburne A. J. Augustine augustine.swinburne@ 123456epa.gov

                This article was submitted to Environmental Health, a section of the journal Frontiers in Public Health

                †These authors have contributed equally to this work

                Article
                10.3389/fpubh.2019.00231
                6709658
                13783f23-fb06-43d2-996b-69d8db9504f8
                Copyright © 2019 Simmons, Eason, Curioso, Griffin, Ramudit, Oshima, Sams, Wade, Grimm, Dufour and Augustine.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 10 June 2019
                : 02 August 2019
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 42, Pages: 10, Words: 6810
                Categories
                Public Health
                Original Research

                immunoconversions,incident infections,exposure,multiplex immunoassay,salivary antibodies,antibody response,luminex,boquerón beach

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