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      Maternal malaria but not schistosomiasis is associated with a higher risk of febrile infection in infant during the first 3 months of life: A mother-child cohort in Benin

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          Abstract

          Background

          Malaria and schistosomiasis represent two of the most prevalent and disabling parasitic infections in developing countries. Few studies have evaluated the effect of maternal schistosomiasis and malaria in the peri-conceptional period on infant’s risk of infection.

          Methods

          In Benin, women were followed from the preconception period until delivery. Subsequently, their children were followed from birth to 3 months of age. Pre-pregnancy malaria, malaria in pregnancy (MiP)—determined monthly using a thick blood smear—and urinary schistosomiasis—determined once before pregnancy and once at delivery using urine filtration—were the main maternal exposures. Infant’s febrile infection (fever with respiratory, gastrointestinal and/or cutaneous clinical signs anytime during follow-up) was the main outcome. In a secondary analysis, we checked the relation of malaria and schistosomiasis with infant’s hemoglobin (Hb) concentration. Both effects were separately assessed using logistic/mixed linear regression models.

          Results

          The prevalence of MiP was 35.7% with 10.8% occurring during the 1 st trimester, and the prevalence of schistosomiasis was 21.8%. From birth to 3 months, 25.3% of infants had at least one episode of febrile infection. In multivariate analysis, MiP, particularly malaria in the 1 st trimester, was significantly associated with a higher risk of infant’s febrile infection (aOR = 4.99 [1.1; 22.6], p = 0.03). In secondary results, pre-pregnancy malaria and schistosomiasis were significantly associated with a lower infant’s Hb concentration during the first 3 months.

          Conclusion

          We evidenced the deleterious effect of maternal parasitic infections on infant’s health. Our results argue in favor of the implementation of preventive strategies as early as in the peri-conception.

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          Most cited references 29

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          The origins of the developmental origins theory.

           Fred G Barker (2007)
          Current orthodoxy states that coronary heart disease results from the unhealthy lifestyles of westernized adults together with a contribution from genetic inheritance. This does not provide a secure basis for prevention of the disease. Geographical studies gave the first clue that the disease originates during intra-uterine development. Variations in mortality from the disease across England and Wales were shown to correlate closely with past differences in death rates among newborn babies. In the past most deaths among newborns were attributed to low birthweight. This led to the hypothesis that undernutrition in utero permanently changes the body's structure, function and metabolism in ways that lead to coronary heart disease in later life. The association between low birthweight and coronary heart disease has been confirmed in longitudinal studies of men and women around the world. The developmental model of the origins of the disease offers a new way forward.
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            Pre-Pregnancy Body Mass Index in Relation to Infant Birth Weight and Offspring Overweight/Obesity: A Systematic Review and Meta-Analysis

            Background Overweight/obesity in women of childbearing age is a serious public-health problem. In China, the incidence of maternal overweight/obesity has been increasing. However, there is not a meta-analysis to determine if pre-pregnancy body mass index (BMI) is related to infant birth weight (BW) and offspring overweight/obesity. Methods Three electronic bibliographic databases (MEDLINE, EMBASE and CINAHL) were searched systematically from January 1970 to November 2012. The dichotomous data on pre-pregnancy overweight/obesity and BW or offspring overweight/obesity were extracted. Summary statistics (odds ratios, ORs) were used by Review Manager, version 5.1.7. Results After screening 665 citations from three electronic databases, we included 45 studies (most of high or medium quality). Compared with normal-weight mothers, pre-pregnancy underweight increased the risk of small for gestational age (SGA) (odds ratios [OR], 1.81; 95% confidence interval [CI], 1.76–1.87); low BW (OR, 1.47; 95% CI, 1.27–1.71). Pre-pregnancy overweight/obesity increased the risk of being large for gestational age (LGA) (OR, 1.53; 95% CI, 1.44–1.63; and OR, 2.08; 95% CI; 1.95–2.23), high BW (OR, 1.53; 95% CI, 1.44–1.63; and OR, 2.00; 95% CI; 1.84–2.18), macrosomia (OR, 1.67; 95% CI, 1.42–1.97; and OR, 3.23; 95% CI, 2.39–4.37), and subsequent offspring overweight/obesity (OR, 1.95; 95% CI, 1.77–2.13; and OR, 3.06; 95% CI, 2.68–3.49), respectively. Sensitivity analyses revealed that sample size, study method, quality grade of study, source of pre-pregnancy BMI or BW had a strong impact on the association between pre-pregnancy obesity and LGA. No significant evidence of publication bias was observed. Conclusions Pre-pregnancy underweight increases the risk of SGA and LBW; pre-pregnancy overweight/obesity increases the risk of LGA, HBW, macrosomia, and subsequent offspring overweight/obesity. A potential effect modification by maternal age, ethnicity, gestational weight gain, as well as the role of gestational diseases should be addressed in future studies.
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              Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique.

              The measurement of vitamin A (VA) and iron status is very important in the assessment of nutritional deficiencies. The objective of this research was to develop a sandwich ELISA technique for the simultaneous measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein (CRP) as indicators for VA and iron status. The inclusion of CRP as marker of infection allows for more accurate interpretation of VA and iron status. This is accomplished in a 30-microL serum or plasma sample using an ELISA with different capture and detection antibodies and different dilutions of the sample. Commercially available clinical serum controls were used for calibration purposes. The developed assays were compared to commercially available traditional tests. Regression coefficients comparing both assays were better than 0.84 (P < 0.001). Using a limited sample set, the sandwich ELISA assay produced very similar specificity and sensitivity compared to traditional methods when common cutoff values were applied. Intra- and interassay variability was between 5 and 14% for all tests. The cost of the materials for all 5 measurements decreases to less than $1/sample if a large number of samples is analyzed. Due to the low cost, high throughput, and comparability to traditional tests, this procedure has several advantages for assessing VA and iron status in population surveys.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: Writing – original draft
                Role: ConceptualizationRole: MethodologyRole: ResourcesRole: SupervisionRole: Validation
                Role: ConceptualizationRole: MethodologyRole: ResourcesRole: SupervisionRole: Validation
                Role: ConceptualizationRole: MethodologyRole: ResourcesRole: SupervisionRole: Validation
                Role: Data curationRole: MethodologyRole: Resources
                Role: Resources
                Role: MethodologyRole: ResourcesRole: Supervision
                Role: Resources
                Role: Resources
                Role: Resources
                Role: Resources
                Role: Project administrationRole: Resources
                Role: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Supervision
                Role: ConceptualizationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Visualization
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Visualization
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 September 2019
                2019
                : 14
                : 9
                Affiliations
                [1 ] MERIT, IRD, Université Paris 5, Sorbonne Paris Cité, Paris, France
                [2 ] Centre d’Etude et de Recherche sur le Paludisme Associé à la Grossesse et à l’Enfance (CERPAGE), Cotonou, Bénin
                [3 ] Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
                [4 ] Section Infectious Diseases, Department of Health Sciences, VU Amsterdam, Amsterdam, The Netherlands
                [5 ] Nutripass, UMR204, Institut de Recherche pour le Développement, IRD/UM/SupAgro, Montpellier, France
                [6 ] Medical Diagnostic Discovery Department (MD3), bioMérieux, Marcy l’Etoile, France
                [7 ] UMR 9198, Institut de biologie Intégrative de la Cellule, Université Paris Saclay, Paris, France
                Federal University of Agriculture, Abeokuta, NIGERIA
                Author notes

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

                Article
                PONE-D-19-14649
                10.1371/journal.pone.0222864
                6752763
                31536589
                © 2019 Agbota 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: 13
                Product
                Funding
                Funded by: bioMérieux
                Award Recipient :
                Funded by: Fondation de France
                Award ID: 00074147, grant 2017
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-13-JSV1-0004, grant 2013
                Award Recipient :
                Funded by: Fondation pour la Recherche Médicale (FRM)
                Award ID: ECO20160736054
                Award Recipient : Gino Cédric AGBOTA
                Fondation pour la Recherche Médicale (FRM, grant number ECO20160736054) for PhD scholarship. The French Agence Nationale de la Recherche [ANR-13-JSV1-0004, grant 2013] and the Fondation Simone Beer under the auspices of the Fondation de France [00074147, grant 2017] funded RECIPAL project. bioMérieux funded SEPSIS project. NO - The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. SE, JYM and LV contributed to data collection in the framework of SEPSIS project and to the final revision of the manuscript in their own names and not on behalf of their employer.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Malaria
                Medicine and Health Sciences
                Tropical Diseases
                Malaria
                People and Places
                Population Groupings
                Age Groups
                Children
                Infants
                People and Places
                Population Groupings
                Families
                Children
                Infants
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Schistosomiasis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Schistosomiasis
                Medicine and Health Sciences
                Pulmonology
                Respiratory Infections
                Medicine and Health Sciences
                Women's Health
                Maternal Health
                Pregnancy
                Medicine and Health Sciences
                Women's Health
                Obstetrics and Gynecology
                Pregnancy
                Medicine and Health Sciences
                Women's Health
                Maternal Health
                Birth
                Labor and Delivery
                Medicine and Health Sciences
                Women's Health
                Obstetrics and Gynecology
                Birth
                Labor and Delivery
                Medicine and Health Sciences
                Women's Health
                Maternal Health
                Breast Feeding
                Medicine and Health Sciences
                Pediatrics
                Neonatology
                Breast Feeding
                Medicine and Health Sciences
                Infectious Diseases
                Co-Infections
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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