Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China

Background The maternal intrauterine immune environment may affect offspring long‐term health. We aimed to investigate the association between the intrauterine placental immunological milieu and glycolipid metabolic health in children. Methods and Results This study enrolled 1803 mother–child pairs...

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Main Authors: Jixing Zhou, Yuzhu Teng, Jiajun Ouyang, Penggui Wu, Juan Tong, Guopeng Gao, Shuangqin Yan, Fangbiao Tao, Kun Huang
Format: Article
Language:English
Published: Wiley 2024-09-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
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Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.124.035754
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author Jixing Zhou
Yuzhu Teng
Jiajun Ouyang
Penggui Wu
Juan Tong
Guopeng Gao
Shuangqin Yan
Fangbiao Tao
Kun Huang
author_facet Jixing Zhou
Yuzhu Teng
Jiajun Ouyang
Penggui Wu
Juan Tong
Guopeng Gao
Shuangqin Yan
Fangbiao Tao
Kun Huang
author_sort Jixing Zhou
collection DOAJ
description Background The maternal intrauterine immune environment may affect offspring long‐term health. We aimed to investigate the association between the intrauterine placental immunological milieu and glycolipid metabolic health in children. Methods and Results This study enrolled 1803 mother–child pairs from the Ma'anshan birth cohort (2013–2014). Placental mRNA expression of inflammatory cytokines (interleukin‐1β [IL‐1β], IL‐10, monocyte chemoattractant protein‐1, tumor necrosis factor‐α, IL‐4, IL‐6, IL‐8, C‐reactive protein, and interferon‐γ) and oxidative stress biomarkers (heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, and glucose‐related protein 78) was quantified using real‐time quantitative polymerase chain reaction. Fasting blood glucose, insulin, triglycerides, high‐density lipoprotein cholesterol, low‐density lipoprotein cholesterol, and total cholesterol were assessed at 5 to 6 years old. Statistical analyses included multiple linear regression, binary logistic regression, restricted cubic spline model, and the Bayesian kernel machine regression model. Placental inflammatory cytokines (IL‐1β, monocyte chemoattractant protein‐1, C‐reactive protein, IL‐6, IL‐8, IL‐10) and oxidative stress biomarkers (heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, glucose‐related protein 78) showed positive associations with children's fasting blood glucose levels. Heme oxygenase‐1 and glucose‐related protein 78 exhibited negative correlations with children's fasting insulin levels. Elevated IL‐6, heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, and glucose‐related protein 78 were associated with increased risk of prediabetes in children. Overall upregulation of placental proinflammatory cytokines and oxidative stress factors mRNA expression correlated with higher prediabetes risk in children. Bayesian kernel machine regression analysis indicated a joint positive effect of the 12 placental inflammation and oxidative stress mixtures on children's risk of high fasting blood glucose. Conclusions This exploratory study underscores significant correlations between maternal intrauterine placental inflammation, oxidative stress markers, and offspring fasting blood glucose and insulin levels. These findings highlight the potential role of intrauterine holistic immunity in shaping offspring glucose metabolism health.
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spelling doaj-art-7a5926281e8a4b068696cc92ea97a8832025-08-20T02:07:06ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802024-09-01131710.1161/JAHA.124.035754Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in ChinaJixing Zhou0Yuzhu Teng1Jiajun Ouyang2Penggui Wu3Juan Tong4Guopeng Gao5Shuangqin Yan6Fangbiao Tao7Kun Huang8Department of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaMaternal and Child Health Care Center of Ma’anshan Anhui ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaDepartment of Maternal, Child and Adolescent Health, School of Public Health Anhui Medical University Hefei ChinaBackground The maternal intrauterine immune environment may affect offspring long‐term health. We aimed to investigate the association between the intrauterine placental immunological milieu and glycolipid metabolic health in children. Methods and Results This study enrolled 1803 mother–child pairs from the Ma'anshan birth cohort (2013–2014). Placental mRNA expression of inflammatory cytokines (interleukin‐1β [IL‐1β], IL‐10, monocyte chemoattractant protein‐1, tumor necrosis factor‐α, IL‐4, IL‐6, IL‐8, C‐reactive protein, and interferon‐γ) and oxidative stress biomarkers (heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, and glucose‐related protein 78) was quantified using real‐time quantitative polymerase chain reaction. Fasting blood glucose, insulin, triglycerides, high‐density lipoprotein cholesterol, low‐density lipoprotein cholesterol, and total cholesterol were assessed at 5 to 6 years old. Statistical analyses included multiple linear regression, binary logistic regression, restricted cubic spline model, and the Bayesian kernel machine regression model. Placental inflammatory cytokines (IL‐1β, monocyte chemoattractant protein‐1, C‐reactive protein, IL‐6, IL‐8, IL‐10) and oxidative stress biomarkers (heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, glucose‐related protein 78) showed positive associations with children's fasting blood glucose levels. Heme oxygenase‐1 and glucose‐related protein 78 exhibited negative correlations with children's fasting insulin levels. Elevated IL‐6, heme oxygenase‐1, hypoxia‐inducible factor‐1alpha, and glucose‐related protein 78 were associated with increased risk of prediabetes in children. Overall upregulation of placental proinflammatory cytokines and oxidative stress factors mRNA expression correlated with higher prediabetes risk in children. Bayesian kernel machine regression analysis indicated a joint positive effect of the 12 placental inflammation and oxidative stress mixtures on children's risk of high fasting blood glucose. Conclusions This exploratory study underscores significant correlations between maternal intrauterine placental inflammation, oxidative stress markers, and offspring fasting blood glucose and insulin levels. These findings highlight the potential role of intrauterine holistic immunity in shaping offspring glucose metabolism health.https://www.ahajournals.org/doi/10.1161/JAHA.124.035754childrencohortglucoseinflammationplacenta
spellingShingle Jixing Zhou
Yuzhu Teng
Jiajun Ouyang
Penggui Wu
Juan Tong
Guopeng Gao
Shuangqin Yan
Fangbiao Tao
Kun Huang
Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
children
cohort
glucose
inflammation
placenta
title Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
title_full Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
title_fullStr Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
title_full_unstemmed Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
title_short Associations of Placental Inflammation and Oxidative Stress Biomarkers with Glucolipid Metabolism in Children: A Birth Cohort Study in China
title_sort associations of placental inflammation and oxidative stress biomarkers with glucolipid metabolism in children a birth cohort study in china
topic children
cohort
glucose
inflammation
placenta
url https://www.ahajournals.org/doi/10.1161/JAHA.124.035754
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