Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study

Abstract Background Asthma and allergic diseases (such as allergic rhinitis) are multifactorial chronic respiratory diseases, and have many common pathogenic mechanisms. This study aimed to assess the joint effects of breastfeeding and genetic susceptibility on asthma, allergic disease in children a...

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Main Authors: Wenyan Hou, Fengjun Guan, Wenying Chen, Jike Qi, Shuiping Huang, Ping Zeng
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Public Health
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Online Access:https://doi.org/10.1186/s12889-024-20501-0
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author Wenyan Hou
Fengjun Guan
Wenying Chen
Jike Qi
Shuiping Huang
Ping Zeng
author_facet Wenyan Hou
Fengjun Guan
Wenying Chen
Jike Qi
Shuiping Huang
Ping Zeng
author_sort Wenyan Hou
collection DOAJ
description Abstract Background Asthma and allergic diseases (such as allergic rhinitis) are multifactorial chronic respiratory diseases, and have many common pathogenic mechanisms. This study aimed to assess the joint effects of breastfeeding and genetic susceptibility on asthma, allergic disease in children and adolescents and sought to examine whether the effect of breastfeeding was consistent under distinct levels of genetic risk. Methods A total of 351,931 UK Biobank participants were analyzed. Firstly, Cox proportional hazards model was used to evaluate the relation between breastfeeding and asthma, allergic disease and their comorbidity. Next, we incorporated the polygenic risk score as an additional covariate into the model. Then, we explored the role of breastfeeding at each stage of asthma and allergic disease through a multi-state model. Meanwhile, several sensitivity analyses were conducted to evaluate the robustness of our results. Finally, we calculated the attributable protection and population attributable protection of breastfeeding. Results Breastfeeding was related to a reduced risk of occurring asthma (adjusted hazard ratio [HR] = 0.89, 95% confidence interval [CI] 0.86 ~ 0.93), allergic disease (HR = 0.89, 95%CI 0.87 ~ 0.91) and comorbidity (HR = 0.89, 95%CI 0.83 ~ 0.94). The effect of breastfeeding was almost unchanged after considering PRS and did not substantially differ across distinct genetic risk levels. Breastfeeding showed a stronger risk-decreased impact on individuals who developed from allergic rhinitis to comorbidity (HR = 0.83, 95%CI 0.73 ~ 0.93). Further, the influence of breastfeeding was robust against covariates considered and the confounding influence of adolescent smoking. Finally, due to breastfeeding, 12.0%, 13.0% or 13.0% of the exposed population would not suffer from asthma, allergic diseases and the comorbidity, while 7.1%, 7.6% or 7.6% of the general population would not suffer from these diseases. Conclusions This study provided supportive evidence for the risk-reduced effect of breastfeeding on asthma, allergic diseases, and the comorbidity in children and adolescents, and further revealed that such an influence was consistent across distinct genetic risk levels.
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spelling doaj-art-60f95db2f7a643d49a329890d01a926f2024-11-10T12:46:05ZengBMCBMC Public Health1471-24582024-11-012411910.1186/s12889-024-20501-0Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort studyWenyan Hou0Fengjun Guan1Wenying Chen2Jike Qi3Shuiping Huang4Ping Zeng5Department of Biostatistics, School of Public Health, Xuzhou Medical UniversityDepartment of Pediatrics, Affiliated Hospital of Xuzhou Medical UniversityDepartment of Biostatistics, School of Public Health, Xuzhou Medical UniversityDepartment of Biostatistics, School of Public Health, Xuzhou Medical UniversityDepartment of Biostatistics, School of Public Health, Xuzhou Medical UniversityDepartment of Biostatistics, School of Public Health, Xuzhou Medical UniversityAbstract Background Asthma and allergic diseases (such as allergic rhinitis) are multifactorial chronic respiratory diseases, and have many common pathogenic mechanisms. This study aimed to assess the joint effects of breastfeeding and genetic susceptibility on asthma, allergic disease in children and adolescents and sought to examine whether the effect of breastfeeding was consistent under distinct levels of genetic risk. Methods A total of 351,931 UK Biobank participants were analyzed. Firstly, Cox proportional hazards model was used to evaluate the relation between breastfeeding and asthma, allergic disease and their comorbidity. Next, we incorporated the polygenic risk score as an additional covariate into the model. Then, we explored the role of breastfeeding at each stage of asthma and allergic disease through a multi-state model. Meanwhile, several sensitivity analyses were conducted to evaluate the robustness of our results. Finally, we calculated the attributable protection and population attributable protection of breastfeeding. Results Breastfeeding was related to a reduced risk of occurring asthma (adjusted hazard ratio [HR] = 0.89, 95% confidence interval [CI] 0.86 ~ 0.93), allergic disease (HR = 0.89, 95%CI 0.87 ~ 0.91) and comorbidity (HR = 0.89, 95%CI 0.83 ~ 0.94). The effect of breastfeeding was almost unchanged after considering PRS and did not substantially differ across distinct genetic risk levels. Breastfeeding showed a stronger risk-decreased impact on individuals who developed from allergic rhinitis to comorbidity (HR = 0.83, 95%CI 0.73 ~ 0.93). Further, the influence of breastfeeding was robust against covariates considered and the confounding influence of adolescent smoking. Finally, due to breastfeeding, 12.0%, 13.0% or 13.0% of the exposed population would not suffer from asthma, allergic diseases and the comorbidity, while 7.1%, 7.6% or 7.6% of the general population would not suffer from these diseases. Conclusions This study provided supportive evidence for the risk-reduced effect of breastfeeding on asthma, allergic diseases, and the comorbidity in children and adolescents, and further revealed that such an influence was consistent across distinct genetic risk levels.https://doi.org/10.1186/s12889-024-20501-0BreastfeedingAsthmaAllergic diseasesComorbidityPolygenic risk scoreMulti-state model
spellingShingle Wenyan Hou
Fengjun Guan
Wenying Chen
Jike Qi
Shuiping Huang
Ping Zeng
Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
BMC Public Health
Breastfeeding
Asthma
Allergic diseases
Comorbidity
Polygenic risk score
Multi-state model
title Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
title_full Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
title_fullStr Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
title_full_unstemmed Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
title_short Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study
title_sort breastfeeding genetic susceptibility and the risk of asthma and allergic diseases in children and adolescents a retrospective national population based cohort study
topic Breastfeeding
Asthma
Allergic diseases
Comorbidity
Polygenic risk score
Multi-state model
url https://doi.org/10.1186/s12889-024-20501-0
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