The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.
Maternal nutrition and its intergenerational links to non-communicable disease metabolic risk factors: a systematic review and narrative synthesis
Open accessAbstract
Background: Non-communicable diseases (NCDs) are the leading cause of death and disability globally, while malnutrition presents a major global burden. An increasing body of evidence suggests that poor maternal nutrition is related to the development of NCDs and their risk factors in adult offspring. However, there has been no systematic evaluation of this evidence. Methods: We searched eight electronic databases and reference lists for primary research published between 1 January 1996 and 31 May 2016 for studies presenting data on various dimensions of maternal nutritional status (including maternal exposure to famine, maternal gestational weight gain (GWG), maternal weight and/or body mass index (BMI), and maternal dietary intake) during pregnancy or lactation, and measures of at least one of three NCD metabolic risk factors (blood pressure, blood lipids and blood glucose) in the study population of offspring aged 18 years or over. Owing to high heterogeneity across exposures and outcomes, we employed a narrative approach for data synthesis (PROSPERO= CRD42016039244, CRD42016039247). Results: Twenty-seven studies from 10 countries with 62,607 participants in total met our inclusion criteria. The review revealed considerable heterogeneity in findings across studies. There was evidence of a link between maternal exposure to famine during pregnancy with adverse blood pressure, blood lipid, and glucose metabolism outcomes in adult offspring in some contexts, with some tentative support for an influence of adult offspring adiposity in this relationship. However, the evidence base for maternal BMI, GWG, and dietary intake of specific nutrients during pregnancy was more limited and revealed no consistent support for a link between these exposures and adult offspring NCD metabolic risk factors. Conclusion: The links identified between maternal exposure to famine and offspring NCD risk factors in some contexts, and the tentative support for the role of adult offspring adiposity in influencing this relationship, suggest the need for increased collaboration between maternal nutrition and NCD sectors. However, in view of the current scant evidence base for other aspects of maternal nutrition, and the overall heterogeneity of findings, ongoing monitoring and evaluation using large prospective studies and linked data sets is a major priority.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
There is a close relationship between maternal dietary trends and metabolic health, as well as the risk of non-communicable disease development in children, such as obesity, insulin resistance, and metabolic syndrome.
“There is a close relationship between maternal dietary trends and metabolic health, as well as the risk of non-communicable disease development in children, such as obesity, insulin resistance, and metabolic syndrome (15).”
From Maternal nutritional status and the risk of metabolic syndrome in pregnancy: implications for public health nutrition (2026) · cites this paper as [15]
The Background describes a possible link between sub-optimal maternal nutrition and later offspring metabolic risk factors, including overweight or obesity and impaired glucose tolerance. But the Discussion reports a link chiefly for famine exposure in some contexts and no consistent support for maternal dietary intake; the review focuses on adult offspring, not children, and does not establish the claimed close relationship across obesity, insulin resistance, and metabolic syndrome. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The biology of developmental plasticity and the predictive adaptive response hypothesis
Bateson, P., Gluckman, P., & Hanson, M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271460 · Cited by 533
Flagged first, then by citations
Research works printed but not linked: 45
- Bruce K, HM. The developmental origins, mechanisms, and implications of metabolic syndrome. J Nutr. 2010;140(3):648–52. https://doi.org/10.3945/jn.109.111179. · DOI
- Rinaudo P, Wang E. Fetal programming and metabolic syndrome. Ann Rev Physiol. 2012;74(1):107–30. https://doi.org/10.1146/annurev-physiol-020911-153245. · DOI
- Symonds ME, Sebert SP, Hyatt MA, Budge H. Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol. 2009;5(11):604–10. https://doi.org/10.1038/nrendo.2009.195. · DOI
- Wells J. The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc. 2007;82(1):143–72. https://doi.org/10.1111/j.1469-185X.2006.00007.x. · DOI
- Pasternak Y, Aviram A, Proaz I, Hod M. Maternal nutrition and offspring's adulthood NCDs: a review. J Maternal Fetal Neonatal Med. 2013;26(5):439–44. https://doi.org/10.3109/14767058.2012.745505. · DOI
- Carolan-Olah M, Duarte-Gardea M, Lechuga J. A critical review: early life nutrition and prenatal programming for adult disease. J Clin Nurs. 2015;24(23-24):3716–29. https://doi.org/10.1111/jocn.12951. · DOI
- Godfrey KM, Reynolds RM, Prescott SL, Nyirenda M, Jaddoe VWV, Eriksson JG, et al. Influence of maternal obesity on the long-term health of offspring. Lancet Diabetes Endocrinol. 2017;5(1):53–64. https://doi.org/10.1016/S2213-8587(16)30107-3. · DOI · Paper page
- World Health Organization. The double burden of malnutrition. Policy brief. Geneva: World Health Organization; 2017.
- Godfrey K. The 'developmental origins' hypothesis: epidemiology. In: Gluckman P, Hanson M, editors. Developmental Origins of Health and Disease. Cambridge: Cambridge University Press; 2006. p. 6–32. · DOI
- Moher D, Liberati A, Tetzlaff J, Altman DG, for the PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339(jul21 1):b2535. https://doi.org/10.1136/bmj.b2535. · DOI · Paper page
- De Rooij SR, et al. Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia. 2006;49(4):637–43. https://doi.org/10.1007/s00125-005-0136-9. · DOI
- de Rooij SR, Painter RC, Holleman F, Bossuyt PMM, Roseboom TJ. The metabolic syndrome in adults prenatally exposed to the Dutch famine. Am J Clin Nutr. 2007;86(4):1219–24. https://doi.org/10.1093/ajcn/86.4.1219. · DOI
- Huang C, Li Z, Wang M, Martorell R. Early life exposure to the 1959-1961 Chinese famine has long-term health consequences. J Nutr. 2010;140(10):1874–8. https://doi.org/10.3945/jn.110.121293. · DOI
- Li Y, He Y, Qi L, Jaddoe VW, Feskens EJM, Yang X, et al. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes. 2010;59(10):2400–6. https://doi.org/10.2337/db10-0385. · DOI · Paper page
- Ravelli ACJ, van der Meulen J, Michels RPJ, Osmond C, Barker DJP, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. The Lancet. 1998;351(9097):173–7. https://doi.org/10.1016/S0140-6736(97)07244-9. · DOI · Paper page
- Roseboom T, van der Meulen J, Ravelli A, van Montfrans G, Osmond C, Barker DBO. Blood pressure in adults after prenatal exposure to famine. J Hypertension. 1999;17(3):325–30. https://doi.org/10.1097/00004872-199917030-00004. · DOI
- Roseboom T, van der Meulen J, Osmond C, Barker D, Ravelli A, Bleker O. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2000;72(5):1101–6. https://doi.org/10.1093/ajcn/72.5.1101. · DOI · Paper page
- Stanner SA, Bulmer K, Andres C, Lantseva OE, Borodina V, Poteen VV, et al. Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study. Bmj. 1997;315(7119):1342–8. https://doi.org/10.1136/bmj.315.7119.1342. · DOI · Paper page
- Stein AD, Zybert PA, van der Pal-de Bruin K, Lumey LH. Exposure to famine during gestation, size at birth, and blood pressure at age 59 Y: evidence from the Dutch famine. Eur J Epidemiol. 2006;21(10):759–65. https://doi.org/10.1007/s10654-006-9065-2. · DOI
- Wang N, et al. “The famine exposure in early life and metabolic syndrome in adulthood”. Clin Nutr. 2017;36(1):253–9. · DOI
- Zheng X, Wang Y, Ren W, Luo R, Zhang S, Zhang JH, et al. Risk of metabolic syndrome in adults exposed to the great Chinese famine during the fetal life and early childhood. Eur J Clin Nutr. 2012;66(2):231–6. https://doi.org/10.1038/ejcn.2011.161. · DOI
- Loos RJF, Phillips DIW, Fagard R, Beunen G, Derom C, Mathieu C, et al. The influence of maternal BMI and age in twin pregnancies on insulin resistance in the offspring. Diabetes Care. 2002;25(12):2191–6. https://doi.org/10.2337/diacare.25.12.2191. · DOI
- Mamun AA, O'Callaghan M, Callaway L, Williams G, Najman J, Lawlor DA. Associations of gestational weight gain with offspring body mass index and blood pressure at 21 years of age. Circulation. 2009;119(13):1720–7. https://doi.org/10.1161/CIRCULATIONAHA.108.813436. · DOI
- Hochner H, et al. Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors. Jerusalem Perinatal Family Follow-Up Study. 2012;125(11):1381–9.
- Hrolfsdottir L, Rytter D, Olsen SF, Bech BH, Maslova E, Henriksen TB, et al. Gestational weight gain in normal weight women and offspring cardio-metabolic risk factors at 20 years of age. Int J Obes. 2015;39(4):671–6. https://doi.org/10.1038/ijo.2014.179. · DOI
- Mi J, Law C, Zhang KL, Osmond C, Stein C, Barker D. EFfects of infant birthweight and maternal body mass index in pregnancy on components of the insulin resistance syndrome in china. Ann Internal Med. 2000;132(4):253–60. https://doi.org/10.7326/0003-4819-132-4-200002150-00002. · DOI
- Scheers Andersson E, Tynelius P, Nohr EA, Sørensen TIA, Rasmussen F. No association of maternal gestational weight gain with offspring blood pressure and hypertension at age 18 years in male sibling-pairs: a prospective register-based cohort study. PLOS ONE. 2015;10(3):e0121202. https://doi.org/10.1371/journal.pone.0121202. · DOI
- Webb AL, Conlisk AJ, Barnhart HX, Martorell R, Grajeda R, Stein AD. Maternal and childhood nutrition and later blood pressure levels in young Guatemalan adults. Int J Epidemiol. 2005;34(4):898–904. https://doi.org/10.1093/ije/dyi097. · DOI
- Campbell DM, Hall MH, Barker DJP, Cross J, Shiell AW, Godfrey KM. Diet in pregnancy and the offspring's blood pressure 40 years later. BJOG. 1996;103(3):273–80. https://doi.org/10.1111/j.1471-0528.1996.tb09718.x. · DOI
- Conlisk AJ, Barnhart HX, Martorell R, Grajeda R, Stein AD. Maternal and child nutritional supplementation are inversely associated with fasting plasma glucose concentration in young Guatemalan adults. J Nutr. 2004;134(4):890–7. https://doi.org/10.1093/jn/134.4.890. · DOI
- Danielsen I, Granström C, Haldorsson T, Rytter D, Hammer Bech B, Henriksen TB, et al. Dietary glycemic index during pregnancy is associated with biomarkers of the metabolic syndrome in offspring at age 20 years. PloS one. 2013;8(5):e64887. https://doi.org/10.1371/journal.pone.0064887. · DOI
- Macleod J, Tang L, Hobbs FDR, Wharton B, Holder R, Hussain S, et al. Effects of nutritional supplementation during pregnancy on early adult disease risk: follow up of offspring of participants in a randomised controlled trial investigating effects of supplementation on infant birth weight. PloS one. 2013;8(12):e83371. https://doi.org/10.1371/journal.pone.0083371. · DOI
- Roseboom T, van der Meulen JHP, van Montfrans G, Ravelli ACJ, Osmond C, Barker D, et al. Maternal nutrition during gestation and blood pressure in later life. J Hypertension. 2001;19(1):29–34. https://doi.org/10.1097/00004872-200101000-00004. · DOI
- Rytter D, Schmidt EB, Bech BH, Christensen JH, Henriksen TB, Olsen SF. Fish oil supplementation during late pregnancy does not influence plasma lipids or lipoprotein levels in young adult offspring. Lipids. 2011;46(12):1091–9. https://doi.org/10.1007/s11745-011-3606-5. · DOI
- Rytter D, Christensen JH, Bech BH, Schmidt EB, Henriksen TB, Olsen SF. The effect of maternal fish oil supplementation during the last trimester of pregnancy on blood pressure, heart rate and heart rate variability in the 19-year-old offspring. Br J Nutr. 2012;108(8):1475–83. https://doi.org/10.1017/S0007114511006799. · DOI
- Rytter D, Bech BH, Halldorsson T, Christensen JH, Schmidt EB, Danielsen I, et al. No association between the intake of marine n-3 PUFA during the second trimester of pregnancy and factors associated with cardiometabolic risk in the 20-year-old offspring. Br J Nutr. 2013;110(11):2037–46. https://doi.org/10.1017/S0007114513001335. · DOI
- Shiell AW, Campbell-Brown M, Haselden S, Robinson S, Godfrey KM, Barker DJP. High-meat, low-carbohydrate diet in pregnancy. Hypertension. 2001;38(6):1282–8. https://doi.org/10.1161/hy1101.095332. · DOI
- Fleiss JL, Levin B, Paik MC. The measurement of interrater agreement. In: Statistical Methods for Rates and Proportions: John Wiley & Sons, Inc; 2004. p. 598–626.
- Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Neonatology. 1990;57(2):107–18. https://doi.org/10.1159/000243170. · DOI
- Gopalakrishnan GS, et al. Influence of maternal pre-pregnancy body composition and diet during early–mid pregnancy on cardiovascular function and nephron number in juvenile sheep. Br J Nutr. 2007;94(6):938–47. · DOI
- Meaney MJ, Szyf M, Seckl JR. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med. 2007;13(7):269–77. https://doi.org/10.1016/j.molmed.2007.05.003. · DOI
- Dunford AR, Sangster JM. Maternal and paternal periconceptional nutrition as an indicator of offspring metabolic syndrome risk in later life through epigenetic imprinting: A systematic review. Diabetes Metab Syndr. 2017;17:39198–1.
- Zeisel S. Epigenetic mechanisms for nutrition determinants of later health outcomes. Am J Clin Nutr. 2009;89(5):1488S–93S. https://doi.org/10.3945/ajcn.2009.27113B. · DOI
- Desai M, Byrne C, Zhang J, Petry C, Lucas A, Hales C. Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. Am J Physiol. 1997;272(5 Pt1):G1083–90.
- Plagemann A, Harder T, Franke K, Kohlhoff R. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care. 2002;25(1):16–22. https://doi.org/10.2337/diacare.25.1.16. · DOI · Paper page
Cited by
Sorted by citations
Wu, Y., Gao, Z., Gou, Y., Yan, L., & Duan, Y. (2026) · Frontiers in Public Health · doi:10.3389/fpubh.2026.1862412
Metadata
- Authors
- Wilkins, E., Wickramasinghe, K., Pullar, J., Demaio, A. R., Roberts, N., Perez-Blanco, K.-M., Noonan, K., & Townsend, N.
- Affiliations
- University of Oxford (GB)
- Government of Western Australia Department of Health (AU)
- University of Bath (GB)
- Corresponding author
- Townsend, Nick
- ORCID
- Venue
- Journal of Health, Population and Nutrition
- Published
- 2021-04-26
- Volume
- 40
- Issue
- 1
- Pages
- 20-20
- ISSN
- 1606-0997 (ISSN-L)
- 2072-1315
- PMC
- PMC8077952
- OpenAlex
- W3159346440
- Cited by
- 24
- References
- 1
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 10 · 2023: 4 · 2022: 2
- FWCI
- 0.97
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Health Population and Nutrition (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Explore Bristol Research (submittedVersion, cc-by)
- Bristol Research (University of Bristol) (submittedVersion, cc-by)
- Funders
- World Health Organization (2016/630545-0)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Obesity, Physical Activity, Diet
- Keywords
- maternal nutrition, non-communicable diseases, metabolic risk factors, gestational weight gain, maternal body mass index, maternal diet, offspring adiposity, blood pressure, serum lipids, blood glucose, intergenerational health, malnutrition
- MeSH terms
- Global Burden of Disease, Noncommunicable Diseases, Diet, Female, Humans, Male, Nutritional Status, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Risk Factors, Adult Children, Maternal Nutritional Physiological Phenomena, Malnutrition
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review