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The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe

BACKGROUND: Cognitive function is negatively impacted by schistosomiasis and might be caused by systemic inflammation which has been hypothesized to be one of the mechanisms driving cognitive decline, This study explored the association of systemic inflammatory biomarkers; interleukin (IL)-10, IL-6,...

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Autores principales: Kasambala, Maritha, Mukaratirwa, Samson, Vengesai, Arthur, Mduluza-Jokonya, Tariro, Jokonya, Luxwell, Midzi, Herald, Makota, Rutendo Birri, Mutemeri, Arnold, Maziti, Emmanuel, Dube-Marimbe, Bazondlile, Chibanda, Dixon, Mutapi, Francisca, Mduluza, Takafira
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10151793/
https://www.ncbi.nlm.nih.gov/pubmed/37143686
http://dx.doi.org/10.3389/fimmu.2023.1139912
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author Kasambala, Maritha
Mukaratirwa, Samson
Vengesai, Arthur
Mduluza-Jokonya, Tariro
Jokonya, Luxwell
Midzi, Herald
Makota, Rutendo Birri
Mutemeri, Arnold
Maziti, Emmanuel
Dube-Marimbe, Bazondlile
Chibanda, Dixon
Mutapi, Francisca
Mduluza, Takafira
author_facet Kasambala, Maritha
Mukaratirwa, Samson
Vengesai, Arthur
Mduluza-Jokonya, Tariro
Jokonya, Luxwell
Midzi, Herald
Makota, Rutendo Birri
Mutemeri, Arnold
Maziti, Emmanuel
Dube-Marimbe, Bazondlile
Chibanda, Dixon
Mutapi, Francisca
Mduluza, Takafira
author_sort Kasambala, Maritha
collection PubMed
description BACKGROUND: Cognitive function is negatively impacted by schistosomiasis and might be caused by systemic inflammation which has been hypothesized to be one of the mechanisms driving cognitive decline, This study explored the association of systemic inflammatory biomarkers; interleukin (IL)-10, IL-6, IL-17, transforming growth factor (TGF-β), tumor necrosis factor (TNF-α), C-reactive protein (CRP) and hematological parameters with cognitive performance of preschool-aged children (PSAC) from an Schistosoma haematobium endemic area METHODS: The Griffith III tool was used to measure the cognitive performance of 136 PSAC. Whole blood and sera were collected and used to quantify levels of IL-10, TNF-α, IL-6, TGF-β, IL-17 A and CRP using the enzyme-linked immunosorbent assay and hematological parameters using the hematology analyzer. Spearman correlation analysis was used to determine the relationship between each inflammatory biomarker and cognitive performance. Multivariate logistic regression analysis was used to determine whether systemic inflammation due to S. haematobium infection affected cognitive performance in PSAC. RESULTS: Higher levels of TNF-α and IL-6, were correlated with lower performance in the Foundations of Learning domain (r = -0.30; p < 0.001 and r = -0.26; p < 0.001), respectively. Low cognitive performance in the Eye-Hand-Coordination Domain was observed in PSAC with high levels of the following inflammatory biomarkers that showed negative correlations to performance; TNF-α (r = -0.26; p < 0.001), IL-6 (r = -0.29; p < 0.001), IL-10 (r = -0.18; p < 0.04), WBC (r = -0.29; p < 0.001), neutrophils (r = -0.21; p = 0.01) and lymphocytes (r = -0.25; p = 0.003) The General Development Domain correlated with TNF-α (r = -0.28; p < 0.001) and IL-6 (r = -0.30; p < 0.001). TGF-β, L-17A and MXD had no significant correlations to performance in any of the cognitive domains. The overall general development of PSAC was negatively impacted by S. haematobium infections (OR = 7.6; p = 0.008) and (OR = 5.6; p = 0.03) where the PSAC had higher levels of TNF-α and IL-6 respectively. CONCLUSION: Systemic inflammation and S. haematobium infections are negatively associated with cognitive function. We recommend the inclusion of PSAC into mass drug treatment programs.
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spelling pubmed-101517932023-05-03 The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe Kasambala, Maritha Mukaratirwa, Samson Vengesai, Arthur Mduluza-Jokonya, Tariro Jokonya, Luxwell Midzi, Herald Makota, Rutendo Birri Mutemeri, Arnold Maziti, Emmanuel Dube-Marimbe, Bazondlile Chibanda, Dixon Mutapi, Francisca Mduluza, Takafira Front Immunol Immunology BACKGROUND: Cognitive function is negatively impacted by schistosomiasis and might be caused by systemic inflammation which has been hypothesized to be one of the mechanisms driving cognitive decline, This study explored the association of systemic inflammatory biomarkers; interleukin (IL)-10, IL-6, IL-17, transforming growth factor (TGF-β), tumor necrosis factor (TNF-α), C-reactive protein (CRP) and hematological parameters with cognitive performance of preschool-aged children (PSAC) from an Schistosoma haematobium endemic area METHODS: The Griffith III tool was used to measure the cognitive performance of 136 PSAC. Whole blood and sera were collected and used to quantify levels of IL-10, TNF-α, IL-6, TGF-β, IL-17 A and CRP using the enzyme-linked immunosorbent assay and hematological parameters using the hematology analyzer. Spearman correlation analysis was used to determine the relationship between each inflammatory biomarker and cognitive performance. Multivariate logistic regression analysis was used to determine whether systemic inflammation due to S. haematobium infection affected cognitive performance in PSAC. RESULTS: Higher levels of TNF-α and IL-6, were correlated with lower performance in the Foundations of Learning domain (r = -0.30; p < 0.001 and r = -0.26; p < 0.001), respectively. Low cognitive performance in the Eye-Hand-Coordination Domain was observed in PSAC with high levels of the following inflammatory biomarkers that showed negative correlations to performance; TNF-α (r = -0.26; p < 0.001), IL-6 (r = -0.29; p < 0.001), IL-10 (r = -0.18; p < 0.04), WBC (r = -0.29; p < 0.001), neutrophils (r = -0.21; p = 0.01) and lymphocytes (r = -0.25; p = 0.003) The General Development Domain correlated with TNF-α (r = -0.28; p < 0.001) and IL-6 (r = -0.30; p < 0.001). TGF-β, L-17A and MXD had no significant correlations to performance in any of the cognitive domains. The overall general development of PSAC was negatively impacted by S. haematobium infections (OR = 7.6; p = 0.008) and (OR = 5.6; p = 0.03) where the PSAC had higher levels of TNF-α and IL-6 respectively. CONCLUSION: Systemic inflammation and S. haematobium infections are negatively associated with cognitive function. We recommend the inclusion of PSAC into mass drug treatment programs. Frontiers Media S.A. 2023-04-18 /pmc/articles/PMC10151793/ /pubmed/37143686 http://dx.doi.org/10.3389/fimmu.2023.1139912 Text en Copyright © 2023 Kasambala, Mukaratirwa, Vengesai, Mduluza-Jokonya, Jokonya, Midzi, Makota, Mutemeri, Maziti, Dube-Marimbe, Chibanda, Mutapi and Mduluza https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Immunology
Kasambala, Maritha
Mukaratirwa, Samson
Vengesai, Arthur
Mduluza-Jokonya, Tariro
Jokonya, Luxwell
Midzi, Herald
Makota, Rutendo Birri
Mutemeri, Arnold
Maziti, Emmanuel
Dube-Marimbe, Bazondlile
Chibanda, Dixon
Mutapi, Francisca
Mduluza, Takafira
The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title_full The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title_fullStr The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title_full_unstemmed The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title_short The association of systemic inflammation and cognitive functions of pre-school aged children residing in a Schistosoma haematobium endemic area in Zimbabwe
title_sort association of systemic inflammation and cognitive functions of pre-school aged children residing in a schistosoma haematobium endemic area in zimbabwe
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10151793/
https://www.ncbi.nlm.nih.gov/pubmed/37143686
http://dx.doi.org/10.3389/fimmu.2023.1139912
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