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      Levels of serum eosinophil cationic protein are associated with hookworm infection and intensity in endemic communities in Ghana

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          Abstract

          Background

          The eosinophil cationic protein (ECP) is a cytotoxic protein mainly secreted by eosinophils granulocytes and plays a role in host defense against parasitic infections. Infection with Necator americanus (hookworm) is traditionally diagnosed by the Kato-Katz method which is inherently tedious, subjective and known to underestimate infection intensity. This study aimed to assess levels of serum ECP in relation to hookworm infection intensity.

          Methods

          Stool samples from 984 (aged 4 to 80 years) participants in a cross-sectional study conducted in the Kintampo North Municipality of Ghana were examined using the Kato-Katz and formol-ether concentration methods. Serum ECP levels were measured by ECP assay kit and compared between 40 individuals infected with hookworm only, 63 with hookworm- Plasmodium falciparum co-infection, 59 with P. falciparum infection and 36 with no infection.

          Results

          Hookworm infection prevalence was 18.1% (178/984). ECP levels were significantly higher in individuals infected with hookworm only (β = 2.96, 95%CI = 2.69, 3.23, p<0.001) or co-infected with P. falciparum (β = 3.15, 95%CI = 2.91, 3.39, p<0.001) compared to the negative control. Levels of ECP were similar between those with only P. falciparum infection and the uninfected control (p>0.05). Increased hookworm intensity was associated with a significant increase in ECP level (β = 4.45, 95%CI = 2.25, 9.11, r s = 0.193, n = 103, p<0.01). ECP threshold of 84.98ng/ml was associated with a positive predictive value (PPV) of 98% (95% CI = 92, 100), and negative predictive value (NPV) of 76% (95% CI = 62, 87) in classifying hookworm infection status with an AUROC of 96.3%.

          Conclusion

          Serum ECP level may be a good biomarker of hookworm infection and intensity and warrant further investigations to help improve current hookworm diagnosis.

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          Most cited references20

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          Soil-transmitted helminth infections: updating the global picture.

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            Effects of iron supplementation and anthelmintic treatment on motor and language development of preschool children in Zanzibar: double blind, placebo controlled study.

            To measure the effects of iron supplementation and anthelmintic treatment on iron status, anaemia, growth, morbidity, and development of children aged 6-59 months. Double blind, placebo controlled randomised factorial trial of iron supplementation and anthelmintic treatment. Community in Pemba Island, Zanzibar. 614 preschool children aged 6-59 months. Development of language and motor skills assessed by parental interview before and after treatment in age appropriate subgroups. Before intervention, anaemia was prevalent and severe, and geohelminth infections were prevalent and light-Plasmodium falciparum infection was nearly universal. Iron supplementation significantly improved iron status, but not haemoglobin status. Iron supplementation improved language development by 0.8 (95% confidence interval 0.2 to 1.4) points on the 20 point scale. Iron supplementation also improved motor development, but this effect was modified by baseline haemoglobin concentrations (P=0.015 for interaction term) and was apparent only in children with baseline haemoglobin concentrations <90 g/l. In children with a baseline haemoglobin concentration of 68 g/l (one standard deviation below the mean value), iron treatment increased scores by 1.1 (0.1 to 2.1) points on the 18 point motor scale. Mebendazole significantly reduced the number and severity of infections caused by Ascaris lumbricoides and Trichuris trichiura, but not by hookworms. Mebendazole increased development scores by 0.4 (-0.3 to 1.1) points on the motor scale and 0.3 (-0.3 to 0.9) points on the language scale. Iron supplementation improved motor and language development of preschool children in rural Africa. The effects of iron on motor development were limited to children with more severe anaemia (baseline haemoglobin concentration <90 g/l). Mebendazole had a positive effect on motor and language development, but this was not statistically significant.
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              Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials.

              To summarise the effects of anthelmintic drug treatment on growth and cognitive performance in children. Electronic databases: Cochrane Infectious Diseases Group controlled trial register, Cochrane controlled trials register, Embase, and Medline. Citations of all identified trials. Contact with the World Health Organization and field researchers. Systematic review of randomised controlled trials in children aged 1-16 that compared anthelmintic treatment with placebo or no treatment. Assessment of validity and data abstraction conducted independently by two reviewers. Growth and cognitive performance. Thirty randomised controlled trials in more than 15 000 children were identified. Effects on mean weight were unremarkable, and heterogeneity was evident in the results. There were some positive effects on mean weight change in the trials reporting this outcome: after a single dose (any anthelmintic) the pooled estimates were 0.24 kg (95% confidence interval 0.15 kg to 0. 32 kg; fixed effects model assumed) and 0.38 kg (0.01 kg to 0.77 kg; random effects model assumed). Results from trials of multiple doses showed mean weight change in up to one year of follow up of 0.10 kg (0.04 kg to 0.17 kg; fixed effects) or 0.15 kg (0.00 to 0.30; random effects). At more than one year of follow up, mean weight change was 0.12 kg (-0.02 kg to 0.26 kg; fixed effects) and 0.43 (-0.61 to 1. 47; random effects). Results from studies of cognitive performance were inconclusive. There is some limited evidence that routine treatment of children in areas where helminths are common has effects on weight gain, but this is not consistent between trials. There is insufficient evidence as to whether this intervention improves cognitive performance.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Investigation
                Role: ConceptualizationRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 September 2019
                2019
                : 14
                : 9
                : e0222382
                Affiliations
                [1 ] Department of Biomedical Science, College of Health Sciences, University of Cape Coast, Cape Coast, Ghana
                [2 ] Department of Immunology, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana
                [3 ] Molecular Medicine Department, School of Medical Sciences, Kwame Nkrumah University of Science and Technology, Ghana
                [4 ] Department of Microbiology, College of Health Sciences, University of Cape Coast, Cape Coast, Ghana
                [5 ] Parasitology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana, Legon, Ghana
                Helen Keller International, UNITED KINGDOM
                Author notes

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

                Author information
                http://orcid.org/0000-0002-4086-3033
                Article
                PONE-D-19-10360
                10.1371/journal.pone.0222382
                6742367
                31513658
                106ea5c1-fe59-4d71-b693-a4b708130d5a
                © 2019 Amoani 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
                : 11 April 2019
                : 28 August 2019
                Page count
                Figures: 2, Tables: 2, Pages: 10
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 1R01AI099623
                Award Recipient :
                This work was supported by National Institutes of Health, grant ID #: 1R01AI099623 awarded to MDW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Medicine and Health Sciences
                Parasitic Diseases
                Helminth Infections
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Blood Cells
                White Blood Cells
                Eosinophils
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Immune Cells
                White Blood Cells
                Eosinophils
                Biology and Life Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Eosinophils
                Medicine and Health Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Eosinophils
                Medicine and Health Sciences
                Parasitic Diseases
                Biology and Life Sciences
                Parasitology
                Parasite Groups
                Apicomplexa
                Plasmodium
                Research and Analysis Methods
                Immunologic Techniques
                Immunoassays
                Enzyme-Linked Immunoassays
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Hookworms
                Necator Americanus
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Necator
                Necator Americanus
                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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                Uncategorized

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