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      Microscopic and submicroscopic infection by Plasmodium falciparum: Immunoglobulin M and A profiles as markers of intensity and exposure

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          Abstract

          Assessment of serological Plasmodium falciparum–specific antibodies in highly endemic areas provides valuable information about malaria status and parasite exposure in the population. Although serological evidence of Plasmodium exposure is commonly determined by Plasmodium-specific immunoglobulin G (IgG) levels; IgM and IgA are likely markers of malaria status that remain relatively unexplored. Previous studies on IgM and IgA responses have been based on their affinity for single antigens with shortage of immune responses analysis against the whole Plasmodium proteome. Here, we provide evidence of how P. falciparum infection triggers the production of specific IgM and IgA in plasma and its relationship with parasite density and changes in hematological parameters. A total of 201 individuals attending a hospital in Breman Asikuma, Ghana, were recruited into this study. Total and P. falciparum–specific IgM, IgA, and IgG were assessed by ELISA and examined in relation to age (0–5, 14–49, and ≥50 age ranges); infection (submicroscopic vs. microscopic malaria); pregnancy and hematological parameters. Well-known IgG response was used as baseline control. P. falciparum–specific IgM and IgA levels increased in the population with the age, similarly to IgG. These data confirm that acquired humoral immunity develops by repeated infections through the years endorsing IgM and IgA as exposure markers in endemic malaria regions. High levels of specific IgA and IgM in children were associated with microscopic malaria and worse prognosis, because most of them showed severe anemia. This new finding shows that IgM and IgA may be used as diagnostic markers in this age group. We also found an extremely high prevalence of submicroscopic malaria (46.27% on average) accompanied by IgM and IgA levels indistinguishable from those of uninfected individuals. These data, together with the observed lack of sensitivity of rapid diagnostic tests (RDTs) compared to PCR, invoke the urgent need to implement diagnostic markers for submicroscopic malaria. Overall, this study opens the potential use of P. falciparum–specific IgM and IgA as new serological markers to predict malaria status in children and parasite exposure in endemic populations. The difficulties in finding markers of submicroscopic malaria are highlighted, emphasizing the need to explore this field in depth.

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          Most cited references78

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          Gamma-globulin and acquired immunity to human malaria.

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            Rapid diagnostic tests for malaria parasites.

            Malaria presents a diagnostic challenge to laboratories in most countries. Endemic malaria, population movements, and travelers all contribute to presenting the laboratory with diagnostic problems for which it may have little expertise available. Drug resistance and genetic variation has altered many accepted morphological appearances of malaria species, and new technology has given an opportunity to review available procedures. Concurrently the World Health Organization has opened a dialogue with scientists, clinicians, and manufacturers on the realistic possibilities for developing accurate, sensitive, and cost-effective rapid diagnostic tests for malaria, capable of detecting 100 parasites/microl from all species and with a semiquantitative measurement for monitoring successful drug treatment. New technology has to be compared with an accepted "gold standard" that makes comparisons of sensitivity and specificity between different methods. The majority of malaria is found in countries where cost-effectiveness is an important factor and ease of performance and training is a major consideration. Most new technology for malaria diagnosis incorporates immunochromatographic capture procedures, with conjugated monoclonal antibodies providing the indicator of infection. Preferred targeted antigens are those which are abundant in all asexual and sexual stages of the parasite and are currently centered on detection of HRP-2 from Plasmodium falciparum and parasite-specific lactate dehydrogenase or Plasmodium aldolase from the parasite glycolytic pathway found in all species. Clinical studies allow effective comparisons between different formats, and the reality of nonmicroscopic diagnoses of malaria is considered.
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              The silent threat: asymptomatic parasitemia and malaria transmission.

              Scale-up of malaria control interventions has resulted in a substantial decline in global malaria morbidity and mortality. Despite this achievement, there is evidence that current interventions alone will not lead to malaria elimination in most malaria-endemic areas and additional strategies need to be considered. Use of antimalarial drugs to target the reservoir of malaria infection is an option to reduce the transmission of malaria between humans and mosquito vectors. However, a large proportion of human malaria infections are asymptomatic, requiring treatment that is not triggered by care-seeking for clinical illness. This article reviews the evidence that asymptomatic malaria infection plays an important role in malaria transmission and that interventions to target this parasite reservoir may be needed to achieve malaria elimination in both low- and high-transmission areas.
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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                02 September 2022
                2022
                : 12
                : 934321
                Affiliations
                [1] 1 Department of Biochemistry and Molecular Biology and Research Institute Hospital 12 de Octubre (Imas12), Universidad Complutense de Madrid , Madrid, Spain
                [2] 2 Faculty of Health Sciences, Rey Juan Carlos University , Alcorcón, Spain
                [3] 3 Department of Biological, Environmental and Occupational Health Sciences, School of Public Health, College of Health Sciences, University of Ghana, Legon , Accra, Ghana
                [4] 4 Laboratory of Hematology and Infectious Diseases, Our Lady of Grace Hospital , Breman-Asikuma, Ghana
                Author notes

                Edited by: Gabriele Pradel, RWTH Aachen University, Germany

                Reviewed by: Thomas Jacobs, Bernhard Nocht Institute for Tropical Medicine (BNITM), Germany; Nigel Aminake Makoah, University of the Free State, South Africa

                *Correspondence: Isabel G. Azcárate, isabel.azcarate@ 123456urjc.es ; José M. Bautista, jmbau@ 123456ucm.es

                This article was submitted to Parasite and Host, a section of the journal Frontiers in Cellular and Infection Microbiology

                Article
                10.3389/fcimb.2022.934321
                9478039
                36118030
                26e511da-0ee4-482b-a587-c727dae27a04
                Copyright © 2022 Abad, Marín-García, Heras, Fobil, Hutchful, Diez, Puyet, Reyes-Palomares, Azcárate and Bautista

                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
                : 02 May 2022
                : 04 August 2022
                Page count
                Figures: 5, Tables: 4, Equations: 0, References: 78, Pages: 17, Words: 9195
                Funding
                Funded by: Ministerio de Economía y Competitividad , doi 10.13039/501100003329;
                Funded by: Comunidad de Madrid , doi 10.13039/100012818;
                Funded by: Universidad Complutense de Madrid , doi 10.13039/501100002911;
                Categories
                Cellular and Infection Microbiology
                Original Research

                Infectious disease & Microbiology
                plasmodium,igm,iga,igg,antibody,immunity,serological marker,submicroscopic malaria

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