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29-08-2018 | Risk factors | Review | Article

Early-Life Exposures and Risk of Diabetes Mellitus and Obesity

Journal: Current Diabetes Reports

Authors: Véronique Gingras, Marie-France Hivert, Emily Oken

Publisher: Springer US

Abstract

Purpose of Review

Type 2 diabetes is a growing concern worldwide with increasing incidence in youth. Development of preventive strategies in earlier stages of life is crucial. We aimed to examine epidemiological evidence of early-life exposures and their associations with childhood and later risk of obesity and diabetes, and to discuss potential mechanisms.

Recent Findings

Parental obesity and diabetes in the preconception period may influence offspring’s obesity risk via epigenetic mechanisms influencing gametogenesis and early development that could have significant transgenerational effects. A more comprehensive understanding of these effects is needed to identify possible avenues for interventions in both fathers and mothers to be. In addition, current evidence suggests that growth and body weight trajectories in infancy and childhood are useful indicators of later obesity and type 2 diabetes. Moreover, the composition and variations in the microbiome in early life are associated with long-term health and could mediate associations between several early-life exposures and later risk of diseases.

Summary

Altogether, the epidemiological evidence supports the need for preconception and early-life interventions to reduce the obesity and diabetes burden in later life.
Literature
1.
World Health Organization. Global report on diabetes. Geneva, Switzerland; 2016. http://​www.​who.​int/​diabetes/​global-report/​en/​.
2.
Mayer-Davis EJ, Lawrence JM, Dabelea D, Divers J, Isom S, Dolan L, et al. Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. N Engl J Med. 2017;376(15):1419–29. https://​doi.​org/​10.​1056/​NEJMoa1610187.CrossRefPubMedPubMedCentral
3.
Williams DE, Cadwell BL, Cheng YJ, Cowie CC, Gregg EW, Geiss LS, et al. Prevalence of impaired fasting glucose and its relationship with cardiovascular disease risk factors in US adolescents, 1999–2000. Pediatrics. 2005;116(5):1122–6. https://​doi.​org/​10.​1542/​peds.​2004-2001.CrossRefPubMed
4.
Fryar CD, Carroll MD, Ogden CL. Prevalence of overweight and obesity among children and adolescents aged 2–19 years: United States, 1963–1965 through 2013–2014. http://​www.​cdc.​gov/​nchs/​data/​hestat/​obesity_​child_​13_​14/​obesity_​child_​13_​14.​htm. Published July 2016. Accessed May 2018.
5.
Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4(2B):611–24.CrossRefPubMed
6.
Gillman MW, Barker D, Bier D, Cagampang F, Challis J, Fall C, et al. Meeting report on the 3rd International Congress on Developmental Origins of Health and Disease (DOHaD). Pediatr Res. 2007;61(5 Pt 1):625–9. https://​doi.​org/​10.​1203/​pdr.​0b013e3180459fcd​.CrossRefPubMed
7.
Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73. https://​doi.​org/​10.​1056/​NEJMra0708473.CrossRefPubMedPubMedCentral
8.
Ozanne SE, Fernandez-Twinn D, Hales CN. Fetal growth and adult diseases. Semin Perinatol. 2004;28(1):81–7.CrossRefPubMed
9.
Oken E, Gillman MW. Fetal origins of obesity. Obes Res. 2003;11(4):496–506. https://​doi.​org/​10.​1038/​oby.​2003.​69.CrossRefPubMed
10.
Freeman DJ. Effects of maternal obesity on fetal growth and body composition: implications for programming and future health. Semin Fetal Neonatal Med. 2010;15(2):113–8. https://​doi.​org/​10.​1016/​j.​siny.​2009.​09.​001.CrossRefPubMed
11.
Stumvoll M, Goldstein BJ, van Haeften TW. Type 2 diabetes: principles of pathogenesis and therapy. Lancet. 2005;365(9467):1333–46. https://​doi.​org/​10.​1016/​S0140-6736(05)61032-X.CrossRefPubMed
12.
Meigs JB, Cupples LA, Wilson PW. Parental transmission of type 2 diabetes: the Framingham Offspring Study. Diabetes. 2000;49(12):2201–7.CrossRefPubMed
13.
Dabelea D, Pettitt DJ. Intrauterine diabetic environment confers risks for type 2 diabetes mellitus and obesity in the offspring, in addition to genetic susceptibility. J Pediatr Endocrinol Metab. 2001;14(8):1085–91.CrossRefPubMed
14.
Philipps LH, Santhakumaran S, Gale C, Prior E, Logan KM, Hyde MJ, et al. The diabetic pregnancy and offspring BMI in childhood: a systematic review and meta-analysis. Diabetologia. 2011;54(8):1957–66. https://​doi.​org/​10.​1007/​s00125-011-2180-y.CrossRefPubMed
15.
Lindsay RS, Dabelea D, Roumain J, Hanson RL, Bennett PH, Knowler WC. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes. 2000;49(3):445–9.CrossRefPubMed
16.
Lindsay RS, Nelson SM, Walker JD, Greene SA, Milne G, Sattar N, et al. Programming of adiposity in offspring of mothers with type 1 diabetes at age 7 years. Diabetes Care. 2010;33(5):1080–5. https://​doi.​org/​10.​2337/​dc09-1766.CrossRefPubMedPubMedCentral
17.
Weiss PA, Scholz HS, Haas J, Tamussino KF, Seissler J, Borkenstein MH. Long-term follow-up of infants of mothers with type 1 diabetes: evidence for hereditary and nonhereditary transmission of diabetes and precursors. Diabetes Care. 2000;23(7):905–11.CrossRefPubMed
18.
Clausen TD, Mathiesen ER, Hansen T, Pedersen O, Jensen DM, Lauenborg J, et al. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia. Diabetes Care. 2008;31(2):340–6. https://​doi.​org/​10.​2337/​dc07-1596.CrossRefPubMed
19.
Center for Disease Control and Prevention. National Diabetes Statistics Report, 2017. https://​www.​cdc.​gov/​diabetes/​pdfs/​data/​statistics/​national-diabetes-statistics-report.​pdf. Page consulted 06–06-2018.
20.
Peng TY, Ehrlich SF, Crites Y, Kitzmiller JL, Kuzniewicz MW, Hedderson MM, et al. Trends and racial and ethnic disparities in the prevalence of pregestational type 1 and type 2 diabetes in Northern California: 1996–2014. Am J Obstet Gynecol. 2017;216(2):177 e1–8. https://​doi.​org/​10.​1016/​j.​ajog.​2016.​10.​007.CrossRef
21.
Feig DS, Palda VA. Type 2 diabetes in pregnancy: a growing concern. Lancet. 2002;359(9318):1690–2. https://​doi.​org/​10.​1016/​S0140-6736(02)08599-9.CrossRefPubMed
22.
Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes. 2000;49(12):2208–11.CrossRefPubMed
23.
American Diabetes A. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S13–27. https://​doi.​org/​10.​2337/​dc18-S002.CrossRef
24.
Hillman S, Peebles DM, Williams DJ. Paternal metabolic and cardiovascular risk factors for fetal growth restriction: a case-control study. Diabetes Care. 2013;36(6):1675–80. https://​doi.​org/​10.​2337/​dc12-1280.CrossRefPubMedPubMedCentral
25.
Moss JL, Harris KM. Impact of maternal and paternal preconception health on birth outcomes using prospective couples’ data in Add Health. Arch Gynecol Obstet. 2015;291(2):287–98. https://​doi.​org/​10.​1007/​s00404-014-3521-0.CrossRefPubMed
26.
Wei Y, Yang CR, Wei YP, Zhao ZA, Hou Y, Schatten H, et al. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A. 2014;111(5):1873–8. https://​doi.​org/​10.​1073/​pnas.​1321195111.CrossRefPubMedPubMedCentral
27.
Danielzik S, Langnase K, Mast M, Spethmann C, Muller MJ. Impact of parental BMI on the manifestation of overweight 5–7 year old children. Eur J Nutr. 2002;41(3):132–8. https://​doi.​org/​10.​1007/​s00394-002-0367-1.CrossRefPubMed
28.
Whitaker KL, Jarvis MJ, Beeken RJ, Boniface D, Wardle J. Comparing maternal and paternal intergenerational transmission of obesity risk in a large population-based sample. Am J Clin Nutr. 2010;91(6):1560–7. https://​doi.​org/​10.​3945/​ajcn.​2009.​28838.CrossRefPubMed
29.
Morandi A, Meyre D, Lobbens S, Kleinman K, Kaakinen M, Rifas-Shiman SL, et al. Estimation of newborn risk for child or adolescent obesity: lessons from longitudinal birth cohorts. PLoS One. 2012;7(11):e49919. https://​doi.​org/​10.​1371/​journal.​pone.​0049919.CrossRefPubMedPubMedCentral
30.
Aris IM, Rifas-Shiman S, Li LJ, Kleinman K, Coull B.A., Gold DR et al. Pre-, perinatal and parental predictors of body mass index trajectory milestones. J Pediatr. 2018;in press.
31.
Soubry A, Schildkraut JM, Murtha A, Wang F, Huang Z, Bernal A, et al. Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med. 2013;11:29. https://​doi.​org/​10.​1186/​1741-7015-11-29.CrossRefPubMedPubMedCentral
32.
Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF, et al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond). 2015;39(4):650–7. https://​doi.​org/​10.​1038/​ijo.​2013.​193.CrossRef
33.
Hur SS, Cropley JE, Suter CM. Paternal epigenetic programming: evolving metabolic disease risk. J Mol Endocrinol. 2017;58(3):R159–R68. https://​doi.​org/​10.​1530/​JME-16-0236.CrossRefPubMed
34.
McPherson NO, Fullston T, Aitken RJ, Lane M. Paternal obesity, interventions, and mechanistic pathways to impaired health in offspring. Ann Nutr Metab. 2014;64(3–4):231–8. https://​doi.​org/​10.​1159/​000365026.CrossRefPubMed
35.
Mighty HE, Fahey AJ. Obesity and pregnancy complications. Curr Diab Rep. 2007;7(4):289–94.CrossRefPubMed
36.
Kral JG, Biron S, Simard S, Hould FS, Lebel S, Marceau S, et al. Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics. 2006;118(6):e1644–9. https://​doi.​org/​10.​1542/​peds.​2006-1379.CrossRefPubMed
37.
Johansson K, Cnattingius S, Naslund I, Roos N, Trolle Lagerros Y, Granath F, et al. Outcomes of pregnancy after bariatric surgery. N Engl J Med. 2015;372(9):814–24. https://​doi.​org/​10.​1056/​NEJMoa1405789.CrossRefPubMed
38.
Soubry A. Epigenetic inheritance and evolution: a paternal perspective on dietary influences. Prog Biophys Mol Biol. 2015;118(1–2):79–85. https://​doi.​org/​10.​1016/​j.​pbiomolbio.​2015.​02.​008.CrossRefPubMed
39.
•• Sales VM, Ferguson-Smith AC, Patti ME. Epigenetic mechanisms of transmission of metabolic disease across generations. Cell Metab. 2017, 25(3):559–71. https://​doi.​org/​10.​1016/​j.​cmet.​2017.​02.​016. This review describes how epigenetic mechanisms could contribute to the intergenerational cycle of metabolic disease, with a focus on paternal lineage effects.CrossRefPubMedPubMedCentral
40.
McPherson NO, Owens JA, Fullston T, Lane M. Preconception diet or exercise intervention in obese fathers normalizes sperm microRNA profile and metabolic syndrome in female offspring. Am J Physiol Endocrinol Metab. 2015;308(9):E805–21. https://​doi.​org/​10.​1152/​ajpendo.​00013.​2015.CrossRefPubMed
41.
de Castro Barbosa T, Ingerslev LR, Alm PS, Versteyhe S, Massart J, Rasmussen M, et al. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol Metab. 2016;5(3):184–97. https://​doi.​org/​10.​1016/​j.​molmet.​2015.​12.​002.CrossRefPubMed
42.
Mejos KK, Kim HW, Lim EM, Chang N. Effects of parental folate deficiency on the folate content, global DNA methylation, and expressions of FRalpha, IGF-2 and IGF-1R in the postnatal rat liver. Nutr Res Pract. 2013;7(4):281–6. https://​doi.​org/​10.​4162/​nrp.​2013.​7.​4.​281.CrossRefPubMedPubMedCentral
43.
Dominguez-Salas P, Moore SE, Baker MS, Bergen AW, Cox SE, Dyer RA, et al. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Commun. 2014;5:3746. https://​doi.​org/​10.​1038/​ncomms4746.CrossRefPubMed
44.
Dominguez-Salas P, Cox SE, Prentice AM, Hennig BJ, Moore SE. Maternal nutritional status, C(1) metabolism and offspring DNA methylation: a review of current evidence in human subjects. Proc Nutr Soc. 2012;71(1):154–65. https://​doi.​org/​10.​1017/​S002966511100333​8.CrossRefPubMed
45.
Soubry A. POHaD: why we should study future fathers. Environ Epigenet. 2018;4(2):dvy007. https://​doi.​org/​10.​1093/​eep/​dvy007.CrossRefPubMedPubMedCentral
46.
Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of endocrine disruptors. Reprod Toxicol. 2011;31(3):337–43. https://​doi.​org/​10.​1016/​j.​reprotox.​2010.​10.​012.CrossRefPubMed
47.
Mattison DR. Environmental exposures and development. Curr Opin Pediatr. 2010;22(2):208–18. https://​doi.​org/​10.​1097/​MOP.​0b013e32833779bf​.CrossRefPubMedPubMedCentral
48.
Stillerman KP, Mattison DR, Giudice LC, Woodruff TJ. Environmental exposures and adverse pregnancy outcomes: a review of the science. Reprod Sci. 2008;15(7):631–50. https://​doi.​org/​10.​1177/​1933719108322436​.CrossRefPubMed
49.
Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J Nutr. 2004;134(9):2169–72. https://​doi.​org/​10.​1093/​jn/​134.​9.​2169.CrossRefPubMed
50.
Hoffman DJ, Reynolds RM, Hardy DB. Developmental origins of health and disease: current knowledge and potential mechanisms. Nutr Rev. 2017;75(12):951–70. https://​doi.​org/​10.​1093/​nutrit/​nux053.CrossRefPubMed
51.
Mamun AA, Mannan M, Doi SA. Gestational weight gain in relation to offspring obesity over the life course: a systematic review and bias-adjusted meta-analysis. Obes Rev. 2014;15(4):338–47. https://​doi.​org/​10.​1111/​obr.​12132.CrossRefPubMed
52.
Taylor PD, Poston L. Developmental programming of obesity in mammals. Exp Physiol. 2007;92(2):287–98. https://​doi.​org/​10.​1113/​expphysiol.​2005.​032854.CrossRefPubMed
53.
Goldstein RF, Abell SK, Ranasinha S, Misso M, Boyle JA, Black MH, et al. Association of gestational weight gain with maternal and infant outcomes: a systematic review and meta-analysis. JAMA. 2017;317(21):2207–25. https://​doi.​org/​10.​1001/​jama.​2017.​3635.CrossRefPubMedPubMedCentral
54.
Hivert MF, Rifas-Shiman SL, Gillman MW, Oken E. Greater early and mid-pregnancy gestational weight gains are associated with excess adiposity in mid-childhood. Obesity (Silver Spring). 2016;24(7):1546–53. https://​doi.​org/​10.​1002/​oby.​21511.CrossRef
55.
American Diabetes A. 13. Management of diabetes in pregnancy: standards of medical care in diabetes—2018. Diabetes Care. 2018;41(Suppl 1):S137–S43. https://​doi.​org/​10.​2337/​dc18-S013.CrossRef
56.
Regnault N, Gillman MW, Rifas-Shiman SL, Eggleston E, Oken E. Sex-specific associations of gestational glucose tolerance with childhood body composition. Diabetes Care. 2013;36(10):3045–53. https://​doi.​org/​10.​2337/​dc13-0333.CrossRefPubMedPubMedCentral
57.
Wright CS, Rifas-Shiman SL, Rich-Edwards JW, Taveras EM, Gillman MW, Oken E. Intrauterine exposure to gestational diabetes, child adiposity, and blood pressure. Am J Hypertens. 2009;22(2):215–20. https://​doi.​org/​10.​1038/​ajh.​2008.​326.CrossRefPubMed
58.
Silverman BL, Rizzo TA, Cho NH, Metzger BE. Long-term effects of the intrauterine environment. The Northwestern University Diabetes in Pregnancy Center. Diabetes Care. 1998;21(Suppl 2):B142–9.PubMed
59.
Silverman BL, Metzger BE, Cho NH, Loeb CA. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care. 1995;18(5):611–7.CrossRefPubMed
60.
Kawasaki M, Arata N, Miyazaki C, Mori R, Kikuchi T, Ogawa Y, et al. Obesity and abnormal glucose tolerance in offspring of diabetic mothers: a systematic review and meta-analysis. PLoS One. 2018;13(1):e0190676. https://​doi.​org/​10.​1371/​journal.​pone.​0190676.CrossRefPubMedPubMedCentral
61.
Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond). 2008;32(2):201–10. https://​doi.​org/​10.​1038/​sj.​ijo.​0803760.CrossRef
62.
Albers L, Sobotzki C, Kuss O, Ajslev T, Batista RF, Bettiol H, et al. Maternal smoking during pregnancy and offspring overweight: is there a dose-response relationship? An individual patient data meta-analysis. Int J Obes (Lond). 2018; https://​doi.​org/​10.​1038/​s41366-018-0050-0.CrossRefPubMed
63.
De Long NE, Holloway AC. Early-life chemical exposures and risk of metabolic syndrome. Diabetes Metab Syndr Obes. 2017;10:101–9. https://​doi.​org/​10.​2147/​DMSO.​S95296.CrossRefPubMedPubMedCentral
64.
Thayer KA, Heindel JJ, Bucher JR, Gallo MA. Role of environmental chemicals in diabetes and obesity: a National Toxicology Program workshop review. Environ Health Perspect. 2012;120(6):779–89. https://​doi.​org/​10.​1289/​ehp.​1104597.CrossRefPubMedPubMedCentral
65.
Braun JM. Early-life exposure to EDCs: role in childhood obesity and neurodevelopment. Nat Rev Endocrinol. 2017;13(3):161–73. https://​doi.​org/​10.​1038/​nrendo.​2016.​186.CrossRefPubMed
66.
Barker DJ. The developmental origins of insulin resistance. Horm Res. 2005;64(Suppl 3):2–7. https://​doi.​org/​10.​1159/​000089311.CrossRefPubMed
67.
Eriksson JG, Kajantie E, Lampl M, Osmond C. Trajectories of body mass index amongst children who develop type 2 diabetes as adults. J Intern Med. 2015;278(2):219–26. https://​doi.​org/​10.​1111/​joim.​12354.CrossRefPubMed
68.
Gillman MW. Early infancy as a critical period for development of obesity and related conditions. Nestle Nutr Workshop Ser Pediatr Program. 2010;65:13–20; discussion −4. https://​doi.​org/​10.​1159/​000281141.CrossRefPubMedPubMedCentral
69.
Zheng M, Lamb KE, Grimes C, Laws R, Bolton K, Ong KK, et al. Rapid weight gain during infancy and subsequent adiposity: a systematic review and meta-analysis of evidence. Obes Rev. 2018;19(3):321–32. https://​doi.​org/​10.​1111/​obr.​12632.CrossRefPubMed
70.
Leunissen RW, Kerkhof GF, Stijnen T, Hokken-Koelega A. Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthood. JAMA. 2009;301(21):2234–42. https://​doi.​org/​10.​1001/​jama.​2009.​761.CrossRefPubMed
71.
Fabricius-Bjerre S, Jensen RB, Faerch K, Larsen T, Molgaard C, Michaelsen KF, et al. Impact of birth weight and early infant weight gain on insulin resistance and associated cardiovascular risk factors in adolescence. PLoS One. 2011;6(6):e20595. https://​doi.​org/​10.​1371/​journal.​pone.​0020595.CrossRefPubMedPubMedCentral
72.
Eriksson JG, Forsen TJ, Osmond C, Barker DJ. Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care. 2003;26(11):3006–10.CrossRefPubMed
73.
Eriksson JG, Osmond C, Kajantie E, Forsen TJ, Barker DJ. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 2006;49(12):2853–8. https://​doi.​org/​10.​1007/​s00125-006-0459-1.CrossRefPubMed
74.
Larnkjaer A, Schack-Nielsen L, Molgaard C, Ingstrup HK, Holst JJ, Michaelsen KF. Effect of growth in infancy on body composition, insulin resistance, and concentration of appetite hormones in adolescence. Am J Clin Nutr. 2010;91(6):1675–83. https://​doi.​org/​10.​3945/​ajcn.​2009.​27956.CrossRefPubMed
75.
Wen X, Kleinman K, Gillman MW, Rifas-Shiman SL, Taveras EM. Childhood body mass index trajectories: modeling, characterizing, pairwise correlations and socio-demographic predictors of trajectory characteristics. BMC Med Res Methodol. 2012;12:38. https://​doi.​org/​10.​1186/​471-2288-12-38.CrossRefPubMedPubMedCentral
76.
Aris IM, Bernard JY, Chen LW, Tint MT, Pang WW, Lim WY, et al. Infant body mass index peak and early childhood cardio-metabolic risk markers in a multi-ethnic Asian birth cohort. Int J Epidemiol. 2017;46(2):513–25. https://​doi.​org/​10.​1093/​ije/​dyw232.CrossRefPubMed
77.
• Marinkovic T, Toemen L, Kruithof CJ, Reiss I, van Osch-Gevers L, Hofman A, et al. Early infant growth velocity patterns and cardiovascular and metabolic outcomes in childhood. J Pediatr. 2017;186:57–63.e4. https://​doi.​org/​10.​1016/​j.​jpeds.​2017.​02.​004. This study examined the associations of detailed longitudinal infant weight velocity patterns with childhood cardiovascular and metabolic outcomes.CrossRefPubMedPubMedCentral
78.
Hughes AR, Sherriff A, Ness AR, Reilly JJ. Timing of adiposity rebound and adiposity in adolescence. Pediatrics. 2014;134(5):e1354–61. https://​doi.​org/​10.​1542/​peds.​2014-1908.CrossRefPubMed
79.
Rolland-Cachera MF, Deheeger M, Maillot M, Bellisle F. Early adiposity rebound: causes and consequences for obesity in children and adults. Int J Obes (Lond). 2006;30(Suppl 4):S11–7.CrossRef
80.
Mo-Suwan L, McNeil E, Sangsupawanich P, Chittchang U, Choprapawon C. Adiposity rebound from three to six years of age was associated with a higher insulin resistance risk at eight-and-a-half years in a birth cohort study. Acta Paediatr. 2017;106(1):128–34. https://​doi.​org/​10.​1111/​apa.​13639.CrossRefPubMed
81.
Eriksson JG, Forsen T, Tuomilehto J, Osmond C, Barker DJ. Early adiposity rebound in childhood and risk of type 2 diabetes in adult life. Diabetologia. 2003;46(2):190–4. https://​doi.​org/​10.​1007/​s00125-002-1012-5.CrossRefPubMed
82.
Koyama S, Ichikawa G, Kojima M, Shimura N, Sairenchi T, Arisaka O. Adiposity rebound and the development of metabolic syndrome. Pediatrics. 2014;133(1):e114–9. https://​doi.​org/​10.​1542/​peds.​2013-0966.CrossRefPubMed
83.
Woo JG, Martin LJ. Does breastfeeding protect against childhood obesity? Moving beyond observational evidence. Curr Obes Rep. 2015;4(2):207–16. https://​doi.​org/​10.​1007/​s13679-015-0148-9.CrossRefPubMed
84.
Oken E, Fields DA, Lovelady CA, Redman LM. TOS scientific position statement: breastfeeding and obesity. Obesity (Silver Spring). 2017;25(11):1864–6. https://​doi.​org/​10.​1002/​oby.​22024.CrossRef
85.
Martin RM, Patel R, Kramer MS, Guthrie L, Vilchuck K, Bogdanovich N, et al. Effects of promoting longer-term and exclusive breastfeeding on adiposity and insulin-like growth factor-I at age 11.5 years: a randomized trial. JAMA. 2013;309(10):1005–13. https://​doi.​org/​10.​1001/​jama.​2013.​167.CrossRefPubMedPubMedCentral
86.
Martin RM, Patel R, Kramer MS, Vilchuck K, Bogdanovich N, Sergeichick N, et al. Effects of promoting longer-term and exclusive breastfeeding on cardiometabolic risk factors at age 11.5 years: a cluster-randomized, controlled trial. Circulation. 2014;129(3):321–9. https://​doi.​org/​10.​1161/​CIRCULATIONAHA.​113.​005160.CrossRefPubMed
87.
Pearce J, Taylor MA, Langley-Evans SC. Timing of the introduction of complementary feeding and risk of childhood obesity: a systematic review. Int J Obes (Lond). 2013;37(10):1295–306. https://​doi.​org/​10.​1038/​ijo.​2013.​99.CrossRef
88.
Vail B, Prentice P, Dunger DB, Hughes IA, Acerini CL, Ong KK. Age at weaning and infant growth: primary analysis and systematic review. J Pediatr. 2015;167(2):317–24 e1. https://​doi.​org/​10.​1016/​j.​jpeds.​2015.​05.​003.CrossRefPubMedPubMedCentral
89.
Seach KA, Dharmage SC, Lowe AJ, Dixon JB. Delayed introduction of solid feeding reduces child overweight and obesity at 10 years. Int J Obes (Lond). 2010;34(10):1475–9. https://​doi.​org/​10.​1038/​ijo.​2010.​101.CrossRef
90.
Hartstra AV, Bouter KE, Backhed F, Nieuwdorp M. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care. 2015;38(1):159–65. https://​doi.​org/​10.​2337/​dc14-0769.CrossRefPubMed
91.
Kozyrskyj AL, Kalu R, Koleva PT, Bridgman SL. Fetal programming of overweight through the microbiome: boys are disproportionately affected. J Dev Orig Health Dis. 2016;7(1):25–34. https://​doi.​org/​10.​1017/​S204017441500126​9.CrossRefPubMed
92.
Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med. 2016;22(7):713–22. https://​doi.​org/​10.​1038/​nm.​4142.CrossRefPubMed
93.
•• Stiemsma LT, Michels KB. The role of the microbiome in the developmental origins of health and disease. Pediatrics. 2018;141(4). https://​doi.​org/​10.​1542/​peds.​2017-2437. This review presents the latest evidence suggesting that the microbiome would be a mechanistic mediator in the developmental origins of health and disease.CrossRefPubMed
94.
Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–17. https://​doi.​org/​10.​1016/​j.​molmed.​2014.​12.​002.CrossRefPubMed
95.
Dogra S, Sakwinska O, Soh SE, Ngom-Bru C, Bruck WM, Berger B et al. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. MBio. 2015;6(1). https://​doi.​org/​10.​1128/​mBio.​02419-14.
96.
Singh S, Karagas MR, Mueller NT. Charting the maternal and infant microbiome: what is the role of diabetes and obesity in pregnancy? Curr Diab Rep. 2017;17(2):11. https://​doi.​org/​10.​1007/​s11892-017-0836-9.CrossRefPubMedPubMedCentral
97.
Indrio F, Martini S, Francavilla R, Corvaglia L, Cristofori F, Mastrolia SA, et al. Epigenetic matters: the link between early nutrition, microbiome, and long-term health development. Front Pediatr. 2017;5:178. https://​doi.​org/​10.​3389/​fped.​2017.​00178.CrossRefPubMedPubMedCentral
98.
Stephenson J, Heslehurst N, Hall J, Schoenaker D, Hutchinson J, Cade JE, et al. Before the beginning: nutrition and lifestyle in the preconception period and its importance for future health. Lancet. 2018;391(10132):1830–41. https://​doi.​org/​10.​1016/​S0140-6736(18)30311-8.CrossRefPubMedPubMedCentral

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