Maternal pregnancy diet quality, night eating, and offspring metabolic health: the GUSTO study.
Journal
Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714
Informations de publication
Date de publication:
19 Sep 2024
19 Sep 2024
Historique:
received:
01
03
2024
accepted:
05
09
2024
revised:
25
06
2024
medline:
20
9
2024
pubmed:
20
9
2024
entrez:
19
9
2024
Statut:
aheadofprint
Résumé
We investigated the understudied influence of maternal diet quality, food timing, and their interactions during pregnancy on offspring metabolic health. Maternal diet at 26-28 weeks' gestation was assessed using a 24-h recall and adherence to the modified-healthy-eating-index (HEI-SGP) reflects diet quality. Predominant night-eating (PNE) was defined as consuming >50% of total daily energy intake from 19:00 to 06:59. Outcomes were offspring composite metabolic syndrome score and its components measured at age 6 years. Multivariable linear regressions adjusted for relevant maternal and child covariates assessed associations of diet quality and PNE with these outcomes. Up to 758 mother-child pairs were included. The mean(SD) maternal HEI-SGP score was 52.3(13.7) points (theoretical range: 0-100) and 15% of the mothers demonstrated PNE. Maternal diet quality showed inverse relationship with offspring Homeostatic Model Assessment for Insulin Resistance (HOMA-IR) [β(95% CI): -0.08(-0.15, -0.02) per-10-point HEI-SGP increment; P = 0.012]. Maternal PNE was associated with a higher offspring HOMA-IR [0.28(0.06, 0.50); P = 0.012], with similar estimates after adjustment for children's BMI and diet quality; the association was stronger for boys (P-interaction<0.001) and among mothers with lower diet quality (<median HEI-SGP) (P-interaction = 0.062). Maternal PNE and low dietary quality were associated with a higher level of insulin resistance in early childhood, especially among boys. We demonstrated that maternal predominant night-eating behavior and low-quality diet are associated with higher offspring insulin resistance. Maternal low-quality diet and predominant night-eating behavior synergistically interact to influence offspring insulin resistance, particularly among boys. While maternal diet quality and food timing impact the mother's health, their influence on offspring long-term health outcomes through developmental programming is not well understood. Our findings highlight the significance of maternal food timing and calls for further studies on its influence on child health through developmental programming. Targeting both dietary quality and food timing during pregnancy could be a promising intervention strategy.
Sections du résumé
BACKGROUND
BACKGROUND
We investigated the understudied influence of maternal diet quality, food timing, and their interactions during pregnancy on offspring metabolic health.
METHODS
METHODS
Maternal diet at 26-28 weeks' gestation was assessed using a 24-h recall and adherence to the modified-healthy-eating-index (HEI-SGP) reflects diet quality. Predominant night-eating (PNE) was defined as consuming >50% of total daily energy intake from 19:00 to 06:59. Outcomes were offspring composite metabolic syndrome score and its components measured at age 6 years. Multivariable linear regressions adjusted for relevant maternal and child covariates assessed associations of diet quality and PNE with these outcomes.
RESULTS
RESULTS
Up to 758 mother-child pairs were included. The mean(SD) maternal HEI-SGP score was 52.3(13.7) points (theoretical range: 0-100) and 15% of the mothers demonstrated PNE. Maternal diet quality showed inverse relationship with offspring Homeostatic Model Assessment for Insulin Resistance (HOMA-IR) [β(95% CI): -0.08(-0.15, -0.02) per-10-point HEI-SGP increment; P = 0.012]. Maternal PNE was associated with a higher offspring HOMA-IR [0.28(0.06, 0.50); P = 0.012], with similar estimates after adjustment for children's BMI and diet quality; the association was stronger for boys (P-interaction<0.001) and among mothers with lower diet quality (<median HEI-SGP) (P-interaction = 0.062).
CONCLUSIONS
CONCLUSIONS
Maternal PNE and low dietary quality were associated with a higher level of insulin resistance in early childhood, especially among boys.
IMPACT
CONCLUSIONS
We demonstrated that maternal predominant night-eating behavior and low-quality diet are associated with higher offspring insulin resistance. Maternal low-quality diet and predominant night-eating behavior synergistically interact to influence offspring insulin resistance, particularly among boys. While maternal diet quality and food timing impact the mother's health, their influence on offspring long-term health outcomes through developmental programming is not well understood. Our findings highlight the significance of maternal food timing and calls for further studies on its influence on child health through developmental programming. Targeting both dietary quality and food timing during pregnancy could be a promising intervention strategy.
Identifiants
pubmed: 39300274
doi: 10.1038/s41390-024-03574-w
pii: 10.1038/s41390-024-03574-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to the International Pediatric Research Foundation, Inc.
Références
Obesity and overweight. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight .
Noubiap, J. J. et al. Global, regional, and country estimates of metabolic syndrome burden in children and adolescents in 2020: a systematic review and modelling analysis. Lancet Child Adolesc. Health 6, 158–170 (2022).
pubmed: 35051409
doi: 10.1016/S2352-4642(21)00374-6
Georgesen, S. E. The Complex Problem of Childhood Obesity. West. J. Nurs. Res. 36, 579–580 (2014).
pubmed: 24733350
doi: 10.1177/0193945914525353
Gluckman, P. D., Buklijas, T. & Hanson, M. A. Chapter 1 - The Developmental Origins of Health and Disease (DOHaD) Concept: Past, Present, and Future. in The Epigenome and Developmental Origins of Health and Disease (ed. Rosenfeld, C. S.) 1–15 (Academic Press, Boston, 2016). https://doi.org/10.1016/B978-0-12-801383-0.00001-3 .
Schoenaker, D. A., Soedamah-Muthu, S. S. & Mishra, G. D. The association between dietary factors and gestational hypertension and pre-eclampsia: a systematic review and meta-analysis of observational studies. BMC Med 12, 157 (2014).
pubmed: 25241701
pmcid: 4192458
doi: 10.1186/s12916-014-0157-7
Pang, W. W. et al. Higher Maternal Dietary Protein Intake Is Associated with a Higher Risk of Gestational Diabetes Mellitus in a Multiethnic Asian Cohort. J. Nutr. 147, 653–660 (2017).
pubmed: 28275101
doi: 10.3945/jn.116.243881
Maslova, E. et al. Maternal protein intake during pregnancy and offspring overweight 20 y later. Am. J. Clin. Nutr. 100, 1139–1148 (2014).
pubmed: 25099541
doi: 10.3945/ajcn.113.082222
Chen, L.-W. et al. Associations of maternal macronutrient intake during pregnancy with infant BMI peak characteristics and childhood BMI. Am. J. Clin. Nutr. 105, 705–713 (2017).
pubmed: 28179222
doi: 10.3945/ajcn.116.148270
Cespedes, E. M. & Hu, F. B. Dietary patterns: from nutritional epidemiologic analysis to national guidelines. Am. J. Clin. Nutr. 101, 899–900 (2015).
pubmed: 25832336
pmcid: 4409695
doi: 10.3945/ajcn.115.110213
Johnston, J. D., Ordovás, J. M., Scheer, F. A. & Turek, F. W. Circadian rhythms, metabolism, and chrononutrition in rodents and humans123. Adv. Nutr. 7, 399–406 (2016).
pubmed: 26980824
pmcid: 4785478
doi: 10.3945/an.115.010777
Berry, S. E. et al. Human postprandial responses to food and potential for precision nutrition. Nat. Med. 26, 964–973 (2020).
pubmed: 32528151
pmcid: 8265154
doi: 10.1038/s41591-020-0934-0
Acosta-Rodríguez, V. A., Rijo-Ferreira, F., Green, C. B. & Takahashi, J. S. Importance of circadian timing for aging and longevity. Nat. Commun. 12, 2862 (2021).
pubmed: 34001884
pmcid: 8129076
doi: 10.1038/s41467-021-22922-6
Soh, S.-E. et al. Cohort profile: Growing Up in Singapore towards healthy outcomes (GUSTO) birth cohort study. Int. J. Epidemiol. 43, 1401–1409 (2014).
pubmed: 23912809
doi: 10.1093/ije/dyt125
Wright, K. P. et al. Entrainment of the human circadian clock to the natural light-dark cycle. Curr. Biol. CB 23, 1554–1558 (2013).
pubmed: 23910656
doi: 10.1016/j.cub.2013.06.039
Washington, DC: U.S. Naval Observatory, 2016. Table of Sunrise/Sunset, Moonrise/Moonset, or Twilight Times for an Entire Year. https://aa.usno.navy.mil/calculated/rstt/year?ID=AA&year=2024&task=0&lat=1.3&lon=103.8&label=&tz=8&tz_sign=1&submit=Get+Data .
Han, C. Y. et al. A healthy eating index to measure diet quality in pregnant women in Singapore: a cross-sectional study. BMC Nutr. 1, 39 (2015).
doi: 10.1186/s40795-015-0029-3
Ong, Y. Y. et al. Cardiometabolic Profile of Different Body Composition Phenotypes in Children. J. Clin. Endocrinol. Metab. 106, e2015–e2024 (2021).
pubmed: 33524127
doi: 10.1210/clinem/dgab003
Ahrens, W. et al. Metabolic syndrome in young children: Definitions and results of the IDEFICS study. Int. J. Obes. 38, S4–S14 (2014).
doi: 10.1038/ijo.2014.130
Matthews, D. R. et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985).
pubmed: 3899825
doi: 10.1007/BF00280883
Yin, J. et al. Insulin resistance determined by Homeostasis Model Assessment (HOMA) and associations with metabolic syndrome among Chinese children and teenagers. Diabetol. Metab. Syndr. 5, 71 (2013).
pubmed: 24228769
pmcid: 3833654
doi: 10.1186/1758-5996-5-71
Ong, Y. Y. et al. Timing of introduction of complementary foods, breastfeeding, and child cardiometabolic risk: a prospective multiethnic Asian cohort study. Am. J. Clin. Nutr. 117, 83–92 (2023).
pubmed: 36789947
doi: 10.1016/j.ajcnut.2022.10.021
Chen, L.-W. et al. Maternal dietary quality, inflammatory potential and childhood adiposity: an individual participant data pooled analysis of seven European cohorts in the ALPHABET consortium. BMC Med. 19, 1–14 (2021).
doi: 10.1186/s12916-021-01908-7
Loy, S. L. et al. Associations of circadian eating pattern and diet quality with substantial postpartum weight retention. Nutrients 11, 2686 (2019).
pubmed: 31698715
pmcid: 6893719
doi: 10.3390/nu11112686
Loy, S. L. et al. Maternal night-fasting interval during pregnancy is directly associated with neonatal head circumference and adiposity in girls but not boys. J. Nutr. 147, 1384–1391 (2017).
pubmed: 28592516
pmcid: 5483968
doi: 10.3945/jn.117.250639
Padmapriya, N. et al. Associations of physical activity and sedentary behavior during pregnancy with gestational diabetes mellitus among Asian women in Singapore. BMC Pregnancy Childbirth 17, 364 (2017).
pubmed: 29047402
pmcid: 5648496
doi: 10.1186/s12884-017-1537-8
Rolands, M. R. et al. Development and evaluation of a diet quality index for preschool-aged children in an Asian population: The growing Up in Singapore towards healthy outcomes cohort. J. Acad. Nutr. Diet. 123, 299–308.e3 (2023).
pubmed: 35728798
doi: 10.1016/j.jand.2022.06.013
Francis, E. C., Dabelea, D., Shankar, K. & Perng, W. Maternal diet quality during pregnancy is associated with biomarkers of metabolic risk among male offspring. Diabetologia 64, 2478–2490 (2021).
pubmed: 34370046
pmcid: 8499858
doi: 10.1007/s00125-021-05533-0
Loy, S. L. et al. Maternal circadian eating time and frequency are associated with blood glucose concentrations during pregnancy. J. Nutr. 147, 70–77 (2017).
pubmed: 27798346
doi: 10.3945/jn.116.239392
Lakka, T. A. et al. A 2 year physical activity and dietary intervention attenuates the increase in insulin resistance in a general population of children: the PANIC study. Diabetologia 63, 2270–2281 (2020).
pubmed: 32816094
pmcid: 7527318
doi: 10.1007/s00125-020-05250-0
Chen, Y.-E., Loy, S. L. & Chen, L.-W. Chrononutrition during pregnancy and its association with maternal and offspring outcomes: A systematic review and meta-analysis of ramadan and non-ramadan studies. Nutrients 15, 756 (2023).
pubmed: 36771469
pmcid: 9921927
doi: 10.3390/nu15030756
Loy, S. L. et al. Predominantly night-time feeding and maternal glycaemic levels during pregnancy. Br. J. Nutr. 115, 1563–1570 (2016).
pubmed: 26949026
pmcid: 4924604
doi: 10.1017/S0007114516000441
Deniz, Ç. D., Özler, S., Sayın, F. K. & Eryılmaz, M. A. Associations between night eating syndrome and metabolic parameters in pregnant women. Turk. J. Obstet. Gynecol. 16, 107–111 (2019).
pubmed: 31360584
pmcid: 6637782
doi: 10.4274/tjod.galenos.2019.77864
Gontijo, C. A. et al. Higher energy intake at night effects daily energy distribution and contributes to excessive weight gain during pregnancy. Nutrition 74, 110756 (2020).
pubmed: 32278857
doi: 10.1016/j.nut.2020.110756
Koop, S. & Oster, H. Eat, sleep, repeat – endocrine regulation of behavioural circadian rhythms. FEBS J. 289, 6543–6558 (2022).
pubmed: 34228879
doi: 10.1111/febs.16109
Wehrens, S. M. T. et al. Meal timing regulates the human circadian system. Curr. Biol. 27, 1768–1775.e3 (2017).
pubmed: 28578930
pmcid: 5483233
doi: 10.1016/j.cub.2017.04.059
Ruddick-Collins, L. C., Morgan, P. J. & Johnstone, A. M. Mealtime: A circadian disruptor and determinant of energy balance? J. Neuroendocrinol. 32, e12886 (2020).
pubmed: 32662577
doi: 10.1111/jne.12886
Hood, M. M., Reutrakul, S. & Crowley, S. J. Night eating in patients with type 2 diabetes. Associations with glycemic control, eating patterns, sleep, and mood. Appetite 79, 91–96 (2014).
pubmed: 24751916
doi: 10.1016/j.appet.2014.04.009
Bermúdez-Millán, A. et al. Night eating among latinos with diabetes: Exploring associations with heart rate variability, eating patterns, and sleep. J. Nutr. Educ. Behav. 54, 449–454 (2022).
pubmed: 35534102
pmcid: 9097230
doi: 10.1016/j.jneb.2022.02.006
Paul, H. A., Bomhof, M. R., Vogel, H. J. & Reimer, R. A. Diet-induced changes in maternal gut microbiota and metabolomic profiles influence programming of offspring obesity risk in rats. Sci. Rep. 6, 20683 (2016).
pubmed: 26868870
pmcid: 4751613
doi: 10.1038/srep20683
Godfrey, K. M. et al. Epigenetic gene promoter methylation at birth is associated with child’s later adiposity. Diabetes 60, 1528–1534 (2011).
pubmed: 21471513
pmcid: 3115550
doi: 10.2337/db10-0979
Heijmans, B. T. et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. 105, 17046–17049 (2008).
pubmed: 18955703
pmcid: 2579375
doi: 10.1073/pnas.0806560105
Giugliano, D., Ceriello, A. & Esposito, K. The effects of diet on inflammation: emphasis on the metabolic syndrome. J. Am. Coll. Cardiol. 48, 677–685 (2006).
pubmed: 16904534
doi: 10.1016/j.jacc.2006.03.052
Tajaddini, A., Kendig, M. D., Prates, K. V., Westbrook, R. F. & Morris, M. J. Male rat offspring are more impacted by maternal obesity induced by cafeteria diet than females—additive effect of postweaning diet. Int. J. Mol. Sci. 23, 1442 (2022).
pubmed: 35163366
pmcid: 8835941
doi: 10.3390/ijms23031442
Ricart, W. et al. Maternal glucose tolerance status influences the risk of macrosomia in male but not in female fetuses. J. Epidemiol. Community Health 63, 64–68 (2009).
pubmed: 18718980
doi: 10.1136/jech.2008.074542
Chen, L.-W. et al. Maternal macronutrient intake during pregnancy is associated with neonatal abdominal adiposity: The growing up in Singapore towards healthy outcomes (GUSTO) study. J. Nutr. 146, 1571–1579 (2016).
pubmed: 27385763
doi: 10.3945/jn.116.230730
Chen, L.-W. et al. Associations of maternal dietary inflammatory potential and quality with offspring birth outcomes: An individual participant data pooled analysis of 7 European cohorts in the ALPHABET consortium. PLoS Med. 18, e1003491 (2021).
Rojas-Gómez, A. et al. Pregnancy homocysteine and cobalamin status predict childhood metabolic health in the offspring. Pediatr. Res. 93, 633–642 (2023).
pubmed: 35641553
doi: 10.1038/s41390-022-02117-5
Pedersen, J. F. Ultrasound evidence of sexual difference in fetal size in first trimester. Br. Med. J. 281, 1253 (1980).
pubmed: 7427655
pmcid: 1714654
doi: 10.1136/bmj.281.6250.1253
Bukowski, R. et al. Human sexual size dimorphism in early pregnancy. Am. J. Epidemiol. 165, 1216–1218 (2007).
pubmed: 17344203
doi: 10.1093/aje/kwm024
Eriksson, J. G., Kajantie, E., Osmond, C., Thornburg, K. & Barker, D. J. P. Boys live dangerously in the womb. Am. J. Hum. Biol. 22, 330–335 (2010).
pubmed: 19844898
pmcid: 3923652
doi: 10.1002/ajhb.20995
Finan, B. et al. Targeted estrogen delivery reverses the metabolic syndrome. Nat. Med. 18, 1847–1856 (2012).
pubmed: 23142820
pmcid: 3757949
doi: 10.1038/nm.3009
Igarashi, M. et al. Female-dominant estrogen production in healthy children before adrenarche. Endocr. Connect. 10, 1221–1226 (2021).
pubmed: 34468399
pmcid: 8494404
doi: 10.1530/EC-21-0134
Tian, S. et al. Prevalence of prediabetes risk in offspring born to mothers with hyperandrogenism. eBioMedicine 16, 275–283 (2017).
pubmed: 28111236
pmcid: 5474435
doi: 10.1016/j.ebiom.2017.01.011
Aiken, C. E. & Ozanne, S. E. Sex differences in developmental programming models. Reproduction 145, R1–R13 (2013).
pubmed: 23081892
doi: 10.1530/REP-11-0489
Savard, C. et al. Trimester-specific assessment of diet quality in a sample of Canadian pregnant women. Int. J. Environ. Res. Public. Health 16, 311 (2019).
pubmed: 30678329
pmcid: 6388152
doi: 10.3390/ijerph16030311
Tao, M.-H., Liu, J.-L. & Nguyen, U.-S. D. T. Trends in diet quality by race/ethnicity among adults in the United States for 2011–2018. Nutrients 14, 4178 (2022).
pubmed: 36235830
pmcid: 9570938
doi: 10.3390/nu14194178
Loy, S. L. et al. Chrononutrition during pregnancy: A review on maternal night-time eating. Nutrients 12, 2783 (2020).
pubmed: 32932985
pmcid: 7551833
doi: 10.3390/nu12092783