Ontogeny of circulating lipid metabolism in pregnancy and early childhood - a longitudinal population study.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
02 03 2022
Historique:
received: 04 08 2021
accepted: 24 02 2022
pubmed: 3 3 2022
medline: 30 4 2022
entrez: 2 3 2022
Statut: epublish

Résumé

There is mounting evidence that in utero and early life exposures may predispose an individual to metabolic disorders in later life; and dysregulation of lipid metabolism is critical in such outcomes. However, there is limited knowledge about lipid metabolism and factors causing lipid dysregulation in early life that could result in adverse health outcomes in later life. We studied the effect of antenatal factors such as gestational age, birth weight, and mode of birth on lipid metabolism at birth; changes in the circulating lipidome in the first 4 years of life and the effect of breastfeeding in the first year of life. From this study, we aim to generate a framework for deeper understanding into factors effecting lipid metabolism in early life, to provide early interventions for those at risk of developing metabolic disorders including cardiovascular diseases. We performed comprehensive lipid profiling of 1074 mother-child dyads in the Barwon Infant Study (BIS), a population-based pre-birth cohort and measured 776 distinct lipid features across 39 lipid classes using ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS). We measured lipids in 1032 maternal serum samples at 28 weeks' gestation, 893 cord serum samples at birth, 793, 735, and 511 plasma samples at 6, 12 months, and 4 years, respectively. Cord serum was enriched with long chain poly-unsaturated fatty acids (LC-PUFAs), and corresponding cholesteryl esters relative to the maternal serum. We performed regression analyses to investigate the associations of cord serum lipid species with antenatal factors: gestational age, birth weight, mode of birth and duration of labour. The lipidome differed between mother and newborn and changed markedly with increasing child's age. Alkenylphosphatidylethanolamine species containing LC-PUFAs increased with child's age, whereas the corresponding lysophospholipids and triglycerides decreased. Majority of the cord serum lipids were strongly associated with gestational age and birth weight, with most lipids showing opposing associations. Each mode of birth showed an independent association with cord serum lipids. Breastfeeding had a significant impact on the plasma lipidome in the first year of life, with up to 17-fold increases in a few species of alkyldiaclylglycerols at 6 months of age. This study sheds light on lipid metabolism in infancy and early childhood and provide a framework to define the relationship between lipid metabolism and health outcomes in early childhood. This work was supported by the A*STAR-NHMRC joint call funding (1711624031).

Sections du résumé

Background
There is mounting evidence that in utero and early life exposures may predispose an individual to metabolic disorders in later life; and dysregulation of lipid metabolism is critical in such outcomes. However, there is limited knowledge about lipid metabolism and factors causing lipid dysregulation in early life that could result in adverse health outcomes in later life. We studied the effect of antenatal factors such as gestational age, birth weight, and mode of birth on lipid metabolism at birth; changes in the circulating lipidome in the first 4 years of life and the effect of breastfeeding in the first year of life. From this study, we aim to generate a framework for deeper understanding into factors effecting lipid metabolism in early life, to provide early interventions for those at risk of developing metabolic disorders including cardiovascular diseases.
Methods
We performed comprehensive lipid profiling of 1074 mother-child dyads in the Barwon Infant Study (BIS), a population-based pre-birth cohort and measured 776 distinct lipid features across 39 lipid classes using ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS). We measured lipids in 1032 maternal serum samples at 28 weeks' gestation, 893 cord serum samples at birth, 793, 735, and 511 plasma samples at 6, 12 months, and 4 years, respectively. Cord serum was enriched with long chain poly-unsaturated fatty acids (LC-PUFAs), and corresponding cholesteryl esters relative to the maternal serum. We performed regression analyses to investigate the associations of cord serum lipid species with antenatal factors: gestational age, birth weight, mode of birth and duration of labour.
Results
The lipidome differed between mother and newborn and changed markedly with increasing child's age. Alkenylphosphatidylethanolamine species containing LC-PUFAs increased with child's age, whereas the corresponding lysophospholipids and triglycerides decreased. Majority of the cord serum lipids were strongly associated with gestational age and birth weight, with most lipids showing opposing associations. Each mode of birth showed an independent association with cord serum lipids. Breastfeeding had a significant impact on the plasma lipidome in the first year of life, with up to 17-fold increases in a few species of alkyldiaclylglycerols at 6 months of age.
Conclusions
This study sheds light on lipid metabolism in infancy and early childhood and provide a framework to define the relationship between lipid metabolism and health outcomes in early childhood.
Funding
This work was supported by the A*STAR-NHMRC joint call funding (1711624031).

Identifiants

pubmed: 35234611
doi: 10.7554/eLife.72779
pii: 72779
pmc: PMC8942471
doi:
pii:

Substances chimiques

Triglycerides 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Investigateurs

Peter Vuillermin (P)
Fiona Collier (F)
Anne-Louise Ponsonby (AL)
John Carlin (J)
Katie Allen (K)
Mimi Tang (M)
Richard Saffery (R)
Sarath Ranganathan (S)
David Burgner (D)
Terry Dwyer (T)
Peter Sly (P)

Informations de copyright

© 2022, Burugupalli et al.

Déclaration de conflit d'intérêts

SB, AS, GO, KH, CG, TW, AG, SP, AN, TD, NM, MC, SM, LC, MW, NK, FC, RS, PV, AP, DB, PM No competing interests declared

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Auteurs

Satvika Burugupalli (S)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Adam Alexander T Smith (AAT)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Gavriel Oshlensky (G)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Kevin Huynh (K)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Corey Giles (C)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Tingting Wang (T)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Alexandra George (A)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Sudip Paul (S)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Anh Nguyen (A)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Thy Duong (T)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Natalie Mellett (N)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Michelle Cinel (M)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

Sartaj Ahmad Mir (SA)

Singapore Lipidomics Incubator, Life Sciences Institute, National University of Singapore, Singapore, Singapore.
Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.

Li Chen (L)

Singapore Lipidomics Incubator, Life Sciences Institute, National University of Singapore, Singapore, Singapore.
Singapore Institute for Clinical Sciences, A*STAR, Singapore, Singapore.

Markus R Wenk (MR)

Singapore Lipidomics Incubator, Life Sciences Institute, National University of Singapore, Singapore, Singapore.
Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.

Neerja Karnani (N)

Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.
Singapore Institute for Clinical Sciences, A*STAR, Singapore, Singapore.

Fiona Collier (F)

School of Medicine, Deakin University, Melbourne, Australia.
Child Health Research Unit, Barwon Health, Geelong, Australia.

Richard Saffery (R)

Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Australia.
Dept of Paediatrics, University of Melbourne, Parkville, Australia.

Peter Vuillermin (P)

School of Medicine, Deakin University, Melbourne, Australia.
Child Health Research Unit, Barwon Health, Geelong, Australia.
Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Australia.

Anne-Louise Ponsonby (AL)

Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Australia.
The Florey Institute of Neuroscience and Mental Health, Melbourne, Australia.

David Burgner (D)

Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Australia.
Dept of Paediatrics, University of Melbourne, Parkville, Australia.

Peter Meikle (P)

Metabolomics Laboratory, Baker Heart and Diabetes Institute, Melbourne, Australia.

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Classifications MeSH