Abstract

BackgroundThe role of breastfeeding in modulating epigenetic factors has been suggested as a possible mechanism conferring its benefits on child development but it lacks evidence. Using extensive DNA methylation data from the ALSPAC child cohort, we characterized the genome-wide landscape of DNA methylation variations associated with the duration of exclusive breastfeeding and assessed whether these variations mediate the association between exclusive breastfeeding and BMI over different epochs of child growth.ResultsExclusive breastfeeding elicits more substantial DNA methylation variations during infancy than at other periods of child growth. At the genome-wide level, 13 CpG sites in girls (miR-21, SNAPC3, ATP6V0A1, DHX15/PPARGC1A, LINC00398/ALOX5AP, FAM238C, NATP/NAT2, CUX1, TRAPPC9, OSBPL1A, ZNF185, FAM84A, PDPK1) and 2 CpG sites in boys (IL16 and NREP), mediate the association between exclusive breastfeeding and longitudinal BMI. We found enrichment of CpG sites located within miRNAs and key pathways (AMPK signaling pathway, insulin signaling pathway, endocytosis). Overall DNA methylation variation corresponding to 3 to 5 months of exclusive breastfeeding was associated with slower BMI growth the first 6 years of life compared to no breastfeeding and in a dose–response manner with exclusive breastfeeding duration.ConclusionsOur study confirmed the early postnatal period as a critical developmental period associated with substantial DNA methylation variations, which in turn could mitigate the development of overweight and obesity from infancy to early childhood. Since an accelerated growth during these developmental periods has been linked to the development of sustained obesity later in life, exclusive breastfeeding could have a major role in preventing the risks of overweight/obesity and children and adults through DNA methylation mechanisms occurring early in life.

Highlights

  • The role of breastfeeding in modulating epigenetic factors has been suggested as a possible mecha‐ nism conferring its benefits on child development but it lacks evidence

  • exclusive breastfeeding (EBF) is associated with much larger DNA methylation (DNAm) variations the first 3 years of life compared to other ages and in a dose-dependent manner with EBF duration

  • In Avon Longitudinal Study of Parents and Children (ALSPAC) girls, the average effect of 3 to 5 months EBF vs. no EBF is associated with DNAm variations ranging from − 0.34 to 0.19 (M-value) the first year of life compared to − 0.23 to 0.07, − 0.09 to 0.06 and − 0.12 to 0.09 at age 2, 7 and 15 years, respectively (Additional file 1: Table S1)

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Summary

Introduction

The role of breastfeeding in modulating epigenetic factors has been suggested as a possible mecha‐ nism conferring its benefits on child development but it lacks evidence. It is well established that early life exposure can impact our long-term health, in particular the risk of developing adult diseases such as obesity [1,2,3,4,5,6]. Briollais et al Clinical Epigenetics (2021) 13:231 non-communicable chronic diseases, as well as later in life, termed metabolic programming [9, 10]. Postnatal intervention such as breastfeeding has the potential to mitigate risk factors and prevent metabolic and immune-related diseases. There is growing evidence that breastfeeding may reduce the risk of being overweight [12, 13]

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