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      Association between Subclinical Malaria Infection and Inflammatory Host Response in a Pre-Elimination Setting

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          Abstract

          Background

          Subclinical infections in endemic areas of Southeast Asia sustain malaria transmission. These asymptomatic infections might sustain immunity against clinical malaria and have been considered benign for the host, but if they are associated with chronic low-grade inflammation this could be harmful. We conducted a case-control study to explore the association between subclinical malaria and C-reactive protein (CRP), an established biomarker of inflammation.

          Methods

          Blood samples from asymptomatic villagers in Pailin, Western Cambodia were tested for malaria by high-volume ultra-sensitive polymerase chain reaction (uPCR) to determine the Plasmodium species. Plasma CRP concentration was measured in 328 individuals with parasitaemia (cases) and compared with: i) the same individual’s value at the first time point when they had no detectable parasites (n = 282); and ii) age- sex- and village-matched controls (n = 328) free of Plasmodium infection. Plasma CRP concentrations were compared against thresholds of 3mg/L and 10mg/L. Subgroup analysis was carried out for cases with P vivax and P falciparum mono-infections.

          Results

          Median plasma CRP level for all samples was 0.59mg/L (interquartile range: 0.24–1.64mg/L). CRP concentrations were higher in parasitaemic individuals compared with same-person-controls (p = 0.050); and matched-controls (p = 0.025). 4.9% of samples had CRP concentrations above 10mg/L and 14.6% were above 3mg/L. Cases were more likely to have plasma CRP concentrations above these thresholds than age/sex matched controls, odds ratio 3.5 (95%CI 1.5–9.8) and 1.8 (95%CI 1.1–2.9), respectively. Amongst cases, parasite density and CRP were positively correlated (p<0.001), an association that remained significant when controlling for age and fever. Individuals with P. vivax mono-infections had the highest plasma CRP concentrations with the greatest association with parasitaemia.

          Discussion

          In this setting persistent malaria infections in asymptomatic individuals were associated with moderately elevated plasma CRP concentrations; chiefly evident in cases with P. vivax mono-infections. As well as interrupting malaria transmission within the community, treatment of asymptomatic malaria infections, in particular radical cure of vivax malaria, may benefit the health of infected individuals.

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          Most cited references14

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          “Asymptomatic” Malaria: A Chronic and Debilitating Infection That Should Be Treated

          Roland Gosling and colleagues argue that "asymptomatic" malaria infections have significant health and societal consequences, and propose that they should be renamed "chronic" malaria infections.
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            Fighting fire with fire: mass antimalarial drug administrations in an era of antimalarial resistance.

            The emergence and spread of antimalarial resistance has been a major liability for malaria control. The spread of chloroquine-resistant Plasmodium falciparum strains had catastrophic consequences for people in malaria-endemic regions, particularly in sub-Saharan Africa. The recent emergence of artemisinin-resistant P. falciparum strains is of highest concern. Current efforts to contain artemisinin resistance have yet to show success. In the absence of more promising plans, it has been suggested to eliminate falciparum malaria from foci of artemisinin resistance using a multipronged approach, including mass drug administrations. The use of mass drug administrations is controversial as it increases drug pressure. Based on current knowledge it is difficult to conceptualize how targeted malaria elimination could contribute to artemisinin resistance, provided a full treatment course is ensured.
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              Inflammatory biomarkers and risks of myocardial infarction, stroke, diabetes, and total mortality: implications for longevity.

              Inflammation is recognized as a major etiologic determinant of multiple disease states including myocardial infarction, stroke, diabetes, and metabolic syndrome, and individuals with elevated levels of the inflammatory biomarker high-sensitivity C-reactive protein (hsCRP) are at increased risk of mortality and morbidity from these conditions. Novel screening algorithms, such as the Reynolds Risk Score, that incorporate inflammation can greatly improve risk detection in primary prevention. In high-risk secondary prevention settings such as acute coronary syndrome patients being treated with statin therapy, achieving low levels of plasma hsCRP concentration appears to be of similar importance as achieving low levels of LDL cholesterol. Whether inflammation in general or CRP in particular are appropriate targets for therapy remains controversial and is under investigation. Several novel methods to reduce CRP have been proposed, including direct inhibitors as well as antisense technologies.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 July 2016
                2016
                : 11
                : 7
                : e0158656
                Affiliations
                [1 ]Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                [2 ]Centre for Tropical Medicine and Global Health, University of Oxford, Oxford, United Kingdom
                [3 ]National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia
                [4 ]Worldwide Antimalarial Resistance Network, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                [5 ]Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                Institut de Recherche pour le Développement, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AD NJW ND MD YL. Performed the experiments: TP RT CP JC MI. Analyzed the data: YL TP SL SD. Wrote the paper: TP YL SD NW TA LvS. Wrote the protocol, supervised the fieldwork during which the samples were collected, contributed to the manuscript and reviewed final version: CN.

                Article
                PONE-D-16-12166
                10.1371/journal.pone.0158656
                4936742
                27386859
                6f4b5f18-4f4c-4a79-bf69-4f027693b21e
                © 2016 Peto 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.

                History
                : 5 April 2016
                : 20 June 2016
                Page count
                Figures: 2, Tables: 2, Pages: 11
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: OPP1081420
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 101148/Z/13/Z
                Funded by: Grand Challenges Canada (CA)
                Award ID: Round 5, Grant number S5 0443-01
                Award Recipient :
                This study was funded by the Bill and Melinda Gates Foundation ( gatesfoundation.org/) BMGF OPP1081420 and was part of the Wellcome Trust-Mahidol University-Oxford Tropical Medicine Research Programme funded by the Wellcome Trust of Great Britain ( wellcome.ac.uk/) reference 101148/Z/13/Z. Yoel Lubell received a Grand Challenges Canada Stars in Global Health ( grandchallenges.ca/) award to work on biomarkers of infection and their use as diagnostic tools in the rural tropics (Round 5, Grant number S5 0443-01). 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
                Malaria
                Medicine and Health Sciences
                Tropical Diseases
                Malaria
                Medicine and Health Sciences
                Parasitic Diseases
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Malarial Parasites
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                Parasitology
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                Apicomplexa
                Plasmodium
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                Anatomy
                Body Fluids
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                Custom metadata
                Data are from the Targeted Malaria Elimination study whose authors may be contacted via the study coordinator: Dr Lorenz von Seidlein, Faculty of Tropical Medicine, Mahidol University, 10400, Bangkok, Thailand lorenz@ 123456tropmedres.ac .

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