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Developmental Origins of Disease: Emerging Prenatal Risk Factors and Future Disease Risk

  • Reproductive and Perinatal Epidemiology (R Platt, Section Editor)
  • Published:
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Abstract

Purpose of Review

Many of the diseases and dysfunctions described in the paradigm of the developmental origins of health and disease have been studied in relation to prenatal nutrition or environmental toxicant exposures. Here, we selectively review the current research on four exposures—two nutritional and two environmental—that have recently emerged as prenatal risk factors for long-term health outcomes.

Recent Findings

Recent studies have provided strong evidence that prenatal exposure to (1) excessive intake of sugar-sweetened beverages, (2) unhealthy dietary patterns, (3) perfluoroalkyl substances, and (4) fine particulate matter may increase risk of adverse health outcomes, such as obesity, cardiometabolic dysfunction, and allergy/asthma.

Summary

Emerging prenatal nutritional factors and environmental toxicants influence offspring long-term health. More work is needed to identify the role of paternal exposures and maternal exposures during the preconception period and to further elucidate causality through intervention studies. The ubiquity of these emerging nutritional and environmental exposures makes this area of inquiry of considerable public health importance.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004;93(446):26–33.

    PubMed  CAS  Google Scholar 

  2. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489):1077–81.

    Article  PubMed  CAS  Google Scholar 

  4. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80.

    Article  PubMed  CAS  Google Scholar 

  5. Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health. 2012;11:42. https://doi.org/10.1186/476-069X-11-42.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004;56(3):311–7. https://doi.org/10.1203/01.PDR.0000135998.08025.FB.

    Article  PubMed  Google Scholar 

  7. Hanson MA, Gluckman PD. Developmental origins of health and disease—global public health implications. Best Pract Res Clin Obstet Gynaecol. 2015;29(1):24–31. https://doi.org/10.1016/j.bpobgyn.2014.06.007.

    Article  PubMed  CAS  Google Scholar 

  8. Roseboom TJ, Watson ED. The next generation of disease risk: are the effects of prenatal nutrition transmitted across generations? Evidence from animal and human studies. Placenta. 2012;33(Suppl 2):e40–4. https://doi.org/10.1016/j.placenta.2012.07.018.

    Article  PubMed  Google Scholar 

  9. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001;185(1–2):93–8.

    Article  PubMed  CAS  Google Scholar 

  10. Godfrey KM, Reynolds RM, Prescott SL, Nyirenda M, Jaddoe VW, 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.

    Article  PubMed  Google Scholar 

  11. Poston L. Gestational weight gain: influences on the long-term health of the child. Curr Opin Clin Nutr Metab Care. 2012;15(3):252–7. https://doi.org/10.1097/MCO.0b013e3283527cf2.

    Article  PubMed  Google Scholar 

  12. Hiersch L, Yogev Y. Impact of gestational hyperglycemia on maternal and child health. Curr Opin Clin Nutr Metab Care. 2014;17(3):255–60. https://doi.org/10.1097/MCO.0000000000000030.

    Article  PubMed  CAS  Google Scholar 

  13. Padmanabhan V, Cardoso RC, Puttabyatappa M. Developmental programming, a pathway to disease. Endocrinology. 2016;157(4):1328–40.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Ambrosini GL. Sugar: what are the current facts and where to now? Curr Nutr Rep. 2014;3(4):299–301. https://doi.org/10.1007/s13668-014-0097-z.

    Article  CAS  Google Scholar 

  15. Choo VL, Ha V, Sievenpiper JL. Sugars and obesity: is it the sugars or the calories? Nutr Bull. 2015;40(2):88–96. https://doi.org/10.1111/nbu.12137.

    Article  Google Scholar 

  16. Zheng J, Feng Q, Zhang Q, Wang T, Xiao X. Early life fructose exposure and its implications for long-term cardiometabolic health in offspring. Nutrients. 2016;8(11).

  17. Malik VS, Pan A, Willett WC, Hu FB. Sugar-sweetened beverages and weight gain in children and adults: a systematic review and meta-analysis. Am J Clin Nutr. 2013;98(4):1084–102. https://doi.org/10.3945/ajcn.113.058362.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Malik VS, Popkin BM, Bray GA, Despres JP, Willett WC, Hu FB. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care. 2010;33(11):2477–83.

    Article  PubMed  PubMed Central  Google Scholar 

  19. •• Gillman MW, Rifas-Shiman SL, Fernandez-Barres S, Kleinman K, Taveras EM, Oken E. Beverage intake during pregnancy and childhood adiposity. Pediatrics 2017;140(2).(pii):peds.2017–0031. doi: https://doi.org/10.1542/peds.2017-0031. The most recent study from a US pre-birth cohort linking prenatal intake of sugar-sweetened beverages with increased child adiposity. Findings suggested that the associations were due primarily to maternal, not child, sugar-sweetened beverage intake and to sugary soda rather than fruit drinks or juice.

  20. Jen V, Erler NS, Tielemans MJ, Braun KV, Jaddoe VW, Franco OH, et al. Mothers’ intake of sugar-containing beverages during pregnancy and body composition of their children during childhood: the generation R study. Am J Clin Nutr. 2017;105(4):834–41. https://doi.org/10.3945/ajcn.116.147934.

    Article  PubMed  CAS  Google Scholar 

  21. Perng W, Gillman MW, Mantzoros CS, Oken E. A prospective study of maternal prenatal weight and offspring cardiometabolic health in midchildhood. Ann Epidemiol 2014;24(11):793–800.e1. doi: https://doi.org/10.1016/j.annepidem.2014.08.002.

  22. •• Azad MB, Sharma AK, de Souza RJ, Dolinsky VW, Becker AB, Mandhane PJ, et al. Association between artificially sweetened beverage consumption during pregnancy and infant body mass index. JAMA Pediatr. 2016;170(7):662–70. https://doi.org/10.1001/jamapediatrics.2016.0301. This paper describes the first human evidence that prenatal consumption of artificial sweeteners during pregnancy may influence infant body mass index and risk of overweight.

  23. Zhu Y, Olsen SF, Mendola P, Halldorsson TI, Rawal S, Hinkle SN, et al. Maternal consumption of artificially sweetened beverages during pregnancy, and offspring growth through 7 years of age: a prospective cohort study. Int J Epidemiol. 2017;46(5):1499–508.

  24. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514(7521):181–6. https://doi.org/10.1038/nature13793.

  25. Maslova E, Strom M, Olsen SF, Halldorsson TI. Consumption of artificially-sweetened soft drinks in pregnancy and risk of child asthma and allergic rhinitis. PLoS One. 2013;8(2):e57261. https://doi.org/10.1371/journal.pone.0057261.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. •• Wright LS, Rifas-Shiman SL, Oken E, Litonjua AA, Gold DR. Prenatal and early life fructose, fructose-containing beverages, and midchildhood asthma. Ann Am Thorac Soc. 2018;15(2):217–24. https://doi.org/10.1513/AnnalsATS.201707-530OC. The most recent study conducted in a US pre-birth cohort that details the relationship between higher prenatal sugar-sweetened beverage intake and risk of asthma during mid-childhood. The observed associations were independent of child adiposity.

    Article  PubMed  Google Scholar 

  27. Singh VP, Aggarwal R, Singh S, Banik A, Ahmad T, Patnaik BR, et al. Metabolic syndrome is associated with increased oxo-nitrative stress and asthma-like changes in lungs. PLoS One. 2015;10(6):e0129850. https://doi.org/10.1371/journal.pone. eCollection 2015.

  28. Perng W, Oken E. Chapter 15—programming long-term health: maternal and fetal nutrition and diet needs A2 - Saavedra, Jose M. In: Dattilo AM, editor. Early nutrition and long-term health. Woodhead Publishing; 2017. p. 375–411.

  29. Starling P, Charlton K, McMahon AT, Lucas C. Fish intake during pregnancy and foetal neurodevelopment—a systematic review of the evidence. Nutrients. 2015;7(3):2001–14. https://doi.org/10.3390/nu7032001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Brantsaeter AL, Olafsdottir AS, Forsum E, Olsen SF, Thorsdottir I. Does milk and dairy consumption during pregnancy influence fetal growth and infant birthweight? A systematic literature review. Food Nutr Res. 2012;56(pii):–20050. https://doi.org/10.3402/fnr.v56i0.

  31. Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol. 2002;13(1):3–9.

    Article  PubMed  CAS  Google Scholar 

  32. Kant AK. Indexes of overall diet quality: a review. J Am Diet Assoc. 1996;96(8):785–91. https://doi.org/10.1016/S0002-8223(96)00217-9.

    Article  PubMed  CAS  Google Scholar 

  33. Shapiro AL, Kaar JL, Crume TL, Starling AP, Siega-Riz AM, Ringham BM, et al. Maternal diet quality in pregnancy and neonatal adiposity: the Healthy Start Study. Int J Obes. 2016;40(7):1056–62.

    Article  CAS  Google Scholar 

  34. •• Chia AR, Tint MT, Han CY, Chen LW, Colega M, Aris IM, et al. Adherence to a healthy eating index for pregnant women is associated with lower neonatal adiposity in a multiethnic Asian cohort: the Growing Up in Singapore Towards healthy Outcomes (GUSTO) Study. Am J Clin Nutr. 2018;107(1):71–9. https://doi.org/10.1093/ajcn/nqx003. A recent paper that observed significant associations between higher maternal diet quality lower neonatal adiposity. One of the few studies in the world to detail this relationship in a multi-ethnic Asian birth cohort.

    Article  PubMed  Google Scholar 

  35. Dhana K, Zong G, Yuan C, Schernhammer E, Zhang C, Wang X, et al. Lifestyle of women before pregnancy and the risk of offspring obesity during childhood through early adulthood. Int J Obes. 2018;3(10):018–0052.

    Google Scholar 

  36. • Chen LW, Aris IM, Bernard JY, Tint MT, Chia A, Colega M, et al. Associations of maternal dietary patterns during pregnancy with offspring adiposity from birth until 54 months of age. Nutrients. 2016;9(1) Another paper from a multi-ethnic Asian birth cohort that describes the associations of a “healthy dietary pattern” with lower offspring adiposity. These associations were observed only at ages 18 months and older, until 54 months of age.

  37. Martin CL, Siega-Riz AM, Sotres-Alvarez D, Robinson WR, Daniels JL, Perrin EM, et al. Maternal dietary patterns during pregnancy are associated with child growth in the first 3 years of life. J Nutr. 2016;146(11):2281–8. https://doi.org/10.3945/jn.116.234336.

  38. van den Broek M, Leermakers ET, Jaddoe VW, Steegers EA, Rivadeneira F, Raat H, et al. Maternal dietary patterns during pregnancy and body composition of the child at age 6 y: the generation R study. Am J Clin Nutr. 2015;102(4):873–80. https://doi.org/10.3945/ajcn.114.102905.

    Article  PubMed  CAS  Google Scholar 

  39. Leermakers ETM, Tielemans MJ, van den Broek M, Jaddoe VWV, Franco OH, Kiefte-de Jong JC. Maternal dietary patterns during pregnancy and offspring cardiometabolic health at age 6 years: the generation R study. Clin Nutr. 2017;36(2):477–84. https://doi.org/10.1016/j.clnu.2015.12.017.

    Article  PubMed  Google Scholar 

  40. Huo R, Du T, Xu Y, Xu W, Chen X, Sun K, et al. Effects of Mediterranean-style diet on glycemic control, weight loss and cardiovascular risk factors among type 2 diabetes individuals: a meta-analysis. Eur J Clin Nutr. 2015;69(11):1200–8.

    Article  PubMed  CAS  Google Scholar 

  41. Kastorini CM, Milionis HJ, Esposito K, Giugliano D, Goudevenos JA, Panagiotakos DB. The effect of Mediterranean diet on metabolic syndrome and its components: a meta-analysis of 50 studies and 534,906 individuals. J Am Coll Cardiol. 2011;57(11):1299–313.

    Article  PubMed  CAS  Google Scholar 

  42. Fernandez-Barres S, Romaguera D, Valvi D, Martinez D, Vioque J, Navarrete-Munoz EM, et al. Mediterranean dietary pattern in pregnant women and offspring risk of overweight and abdominal obesity in early childhood: the INMA birth cohort study. Pediatr Obes. 2016;11(6):491–9. https://doi.org/10.1111/ijpo.12092.

    Article  PubMed  CAS  Google Scholar 

  43. •• Chatzi L, Rifas-Shiman SL, Georgiou V, Joung KE, Koinaki S, Chalkiadaki G, et al. Adherence to the Mediterranean diet during pregnancy and offspring adiposity and cardiometabolic traits in childhood. Pediatr Obes. 2017;12(Suppl 1):47–56. https://doi.org/10.1111/ijpo.12191. This study pooled data from two longitudinal birth cohorts in the USA and Greece to illustrate that greater adherence to Mediterranean diet during pregnancy protected against excess offspring cardiometabolic risk.

  44. Sedaghat F, Naja F, Darand M, Beyzai B, Rashidkhani B. Adherence to a Mediterranean dietary pattern and overweight and obesity among female adolescents in Iran. Int J Adolesc Med Health. 2017;23(10):2016–0160.

    Google Scholar 

  45. • Sen S, Rifas-Shiman SL, Shivappa N, Wirth MD, Hebert JR, Gold DR, et al. Dietary inflammatory potential during pregnancy is associated with lower fetal growth and breastfeeding failure: results from Project Viva. J Nutr. 2016;146(4):728–36. https://doi.org/10.3945/jn.115.225581. Most recent study from a US pre-birth cohort that describes associations of a pro-inflammatory diet during pregnancy with impaired fetal growth.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. • Sen S, Rifas-Shiman SL, Shivappa N, Wirth MD, Hebert JR, Gold DR, et al. Associations of prenatal and early life dietary inflammatory potential with childhood adiposity and cardiometabolic risk in Project Viva. Pediatr Obes. 2017;10(10):12221. Most recent study from a US pre-birth cohort that describes associations of a pro-inflammatory diet during pregnancy may promote development of adiposity in the offspring.

    Google Scholar 

  47. Julia V, Macia L, Dombrowicz D. The impact of diet on asthma and allergic diseases. Nat Rev Immunol. 2015;15(5):308–22. https://doi.org/10.1038/nri3830.

    Article  PubMed  CAS  Google Scholar 

  48. von Ehrenstein OS, Aralis H, Flores ME, Ritz B. Fast food consumption in pregnancy and subsequent asthma symptoms in young children. Pediatr Allergy Immunol. 2015;26(6):571–7. https://doi.org/10.1111/pai.12433.

    Article  Google Scholar 

  49. Lau C, Anitole K, Hodes C, Lai D, Pfahles-Hutchens A, Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci. 2007;99(2):366–94. https://doi.org/10.1093/toxsci/kfm128.

    Article  PubMed  CAS  Google Scholar 

  50. Olsen GW, Burris JM, Ehresman DJ, Froehlich JW, Seacat AM, Butenhoff JL, et al. Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect. 2007;115(9):1298–305.

  51. Kato K, Wong LY, Jia LT, Kuklenyik Z, Calafat AM. Trends in exposure to polyfluoroalkyl chemicals in the U.S. population: 1999–2008. Environ Sci Technol. 2011;45(19):8037–45. https://doi.org/10.1021/es1043613.

    Article  PubMed  CAS  Google Scholar 

  52. Kjeldsen LS, Bonefeld-Jorgensen EC. Perfluorinated compounds affect the function of sex hormone receptors. Environ Sci Pollut Res Int. 2013;20(11):8031–44. https://doi.org/10.1007/s11356-013-1753-3.

    Article  PubMed  CAS  Google Scholar 

  53. Zhang L, Ren XM, Wan B, Guo LH. Structure-dependent binding and activation of perfluorinated compounds on human peroxisome proliferator-activated receptor gamma. Toxicol Appl Pharmacol. 2014;279(3):275–83. https://doi.org/10.1016/j.taap.2014.06.020.

    Article  PubMed  CAS  Google Scholar 

  54. Long M, Ghisari M, Bonefeld-Jorgensen EC. Effects of perfluoroalkyl acids on the function of the thyroid hormone and the aryl hydrocarbon receptor. Environ Sci Pollut Res Int. 2013;20(11):8045–56. https://doi.org/10.1007/s11356-013-1628-7.

    Article  PubMed  CAS  Google Scholar 

  55. Taxvig C, Dreisig K, Boberg J, Nellemann C, Schelde AB, Pedersen D, et al. Differential effects of environmental chemicals and food contaminants on adipogenesis, biomarker release and PPARgamma activation. Mol Cell Endocrinol. 2012;361(1–2):106–15. https://doi.org/10.1016/j.mce.2012.03.021.

  56. Hines EP, White SS, Stanko JP, Gibbs-Flournoy EA, Lau C, Fenton SE. Phenotypic dichotomy following developmental exposure to perfluorooctanoic acid (PFOA) in female CD-1 mice: low doses induce elevated serum leptin and insulin, and overweight in mid-life. Mol Cell Endocrinol. 2009;304(1–2):97–105. https://doi.org/10.1016/j.mce.2009.02.021.

    Article  PubMed  CAS  Google Scholar 

  57. •• Braun JM, Chen A, Romano ME, Calafat AM, Webster GM, Yolton K, et al. Prenatal perfluoroalkyl substance exposure and child adiposity at 8 years of age: the HOME study. Obesity (Silver Spring). 2016;24(1):231–7. https://doi.org/10.1002/oby.21258. One of the more recent studies in humans that have detailed associations between exposure to higher prenatal PFAS and greater adiposity in mid-childhood.

  58. Hoyer BB, Ramlau-Hansen CH, Vrijheid M, Valvi D, Pedersen HS, Zviezdai V, et al. Anthropometry in 5- to 9-year-old Greenlandic and Ukrainian children in relation to prenatal exposure to perfluorinated alkyl substances. Environ Health Perspect. 2015;123(8):841–6. https://doi.org/10.1289/ehp.1408881.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Mora AM, Fleisch AF, Rifas-Shiman SL, Woo Baidal JA, Pardo L, Webster TF, et al. Early life exposure to per- and polyfluoroalkyl substances and mid-childhood lipid and alanine aminotransferase levels. Environ Int. 2018;111:1–13. https://doi.org/10.1016/j.envint.2017.11.008.

    Article  PubMed  CAS  Google Scholar 

  60. Lauritzen HB, Larose TL, Oien T, Sandanger TM, Odland JO, van de Bor M, et al. Prenatal exposure to persistent organic pollutants and child overweight/obesity at 5-year follow-up: a prospective cohort study. Environ Health. 2018;17(1):9. https://doi.org/10.1186/s12940-017-0338-x.

    Article  PubMed  PubMed Central  Google Scholar 

  61. •• Fleisch AF, Rifas-Shiman SL, Mora AM, Calafat AM, Ye X, Luttmann-Gibson H, et al. Early-life exposure to perfluoroalkyl substances and childhood metabolic function. Environ Health Perspect. 2017;125(3):481–7. https://doi.org/10.1289/EHP303. A recent study form a US pre-birth cohort that showed prenatal PFAS plasma concentrations were not associated with markers of cardiometabolic risk (leptin, adiponectin, and insulin resistance) in children.

  62. •• Mora AM, Oken E, Rifas-Shiman SL, Webster TF, Gillman MW, Calafat AM, et al. Prenatal exposure to perfluoroalkyl substances and adiposity in early and mid-childhood. Environ Health Perspect. 2017;125(3):467–73. https://doi.org/10.1289/EHP246. In this recent study, although prenatal PFAS exposure was associated with small increases in adiposity measurements in mid-childhood, the confidence intervals were wide and crossed the null.

  63. Manzano-Salgado CB, Casas M, Lopez-Espinosa MJ, Ballester F, Iniguez C, Martinez D, et al. Prenatal exposure to perfluoroalkyl substances and cardiometabolic risk in children from the Spanish INMA birth cohort study. Environ Health Perspect. 2017;125(9):097018. https://doi.org/10.1289/EHP1330.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Qazi MR, Abedi MR, Nelson BD, DePierre JW, Abedi-Valugerdi M. Dietary exposure to perfluorooctanoate or perfluorooctane sulfonate induces hypertrophy in centrilobular hepatocytes and alters the hepatic immune status in mice. Int Immunopharmacol. 2010;10(11):1420–7.

    Article  PubMed  CAS  Google Scholar 

  65. Goudarzi H, Miyashita C, Okada E, Kashino I, Kobayashi S, Chen CJ, et al. Effects of prenatal exposure to perfluoroalkyl acids on prevalence of allergic diseases among 4-year-old children. Environ Int. 2016;94:124–32. https://doi.org/10.1016/j.envint.2016.05.020.

    Article  PubMed  CAS  Google Scholar 

  66. Okada E, Sasaki S, Kashino I, Matsuura H, Miyashita C, Kobayashi S, et al. Prenatal exposure to perfluoroalkyl acids and allergic diseases in early childhood. Environ Int. 2014;65:127–34. https://doi.org/10.1016/j.envint.2014.01.007.

  67. Impinen A, Nygaard UC, Lodrup Carlsen KC, Mowinckel P, Carlsen KH, Haug LS, et al. Prenatal exposure to perfluoralkyl substances (PFASs) associated with respiratory tract infections but not allergy- and asthma-related health outcomes in childhood. Environ Res. 2018;160:518–23. https://doi.org/10.1016/j.envres.2017.10.012.

    Article  PubMed  CAS  Google Scholar 

  68. Timmermann CA, Budtz-Jorgensen E, Jensen TK, Osuna CE, Petersen MS, Steuerwald U, et al. Association between perfluoroalkyl substance exposure and asthma and allergic disease in children as modified by MMR vaccination. J Immunotoxicol. 2017;14(1):39–49. https://doi.org/10.1080/1547691X.2016.254306.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  69. Kannan S, Misra DP, Dvonch JT, Krishnakumar A. Exposures to airborne particulate matter and adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect modification by nutrition. Environ Health Perspect. 2006;114(11):1636–42.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Xu X, Yavar Z, Verdin M, Ying Z, Mihai G, Kampfrath T, et al. Effect of early particulate air pollution exposure on obesity in mice: role of p47phox. Arterioscler Thromb Vasc Biol. 2010;30(12):2518–27. https://doi.org/10.1161/ATVBAHA.110.215350.

  71. Bolton JL, Auten RL, Bilbo SD. Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflammatory outcomes in adult offspring. Brain Behav Immun. 2014;37:30–44. https://doi.org/10.1016/j.bbi.2013.10.029.

    Article  PubMed  CAS  Google Scholar 

  72. •• Fleisch AF, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, Melly S, et al. Prenatal exposure to traffic pollution: associations with reduced fetal growth and rapid infant weight gain. Epidemiology. 2015;26(1):43–50. https://doi.org/10.1097/EDE.0000000000000203. One of the few studies that have shown associations between increased prenatal exposure to traffic-related pollution and rapid weight gain in infancy.

  73. •• Schembari A, de Hoogh K, Pedersen M, Dadvand P, Martinez D, Hoek G, et al. Ambient air pollution and newborn size and adiposity at birth: differences by maternal ethnicity (the born in Bradford study cohort). Environ Health Perspect. 2015;123(11):1208–15. One of the few recent studies that have described associations of fine particulate matter exposure during pregnancy with newborn size and adiposity.

  74. • Lavigne E, Ashley-Martin J, Dodds L, Arbuckle TE, Hystad P, Johnson M, et al. Air pollution exposure during pregnancy and fetal markers of metabolic function: the MIREC study. Am J Epidemiol. 2016;183(9):842–51. https://doi.org/10.1093/aje/kwv256. One of the few epidemiological studies that have assessed the association between prenatal exposure to air pollution and indicators of fetal metabolic function, in a relative large cohort ( n= 1,257).

  75. Madhloum N, Janssen BG, Martens DS, Saenen ND, Bijnens E, Gyselaers W, et al. Cord plasma insulin and in utero exposure to ambient air pollution. Environ Int. 2017;105:126–32. https://doi.org/10.1016/j.envint.2017.05.012.

    Article  PubMed  CAS  Google Scholar 

  76. Chiu YH, Hsu HH, Wilson A, Coull BA, Pendo MP, Baccarelli A, et al. Prenatal particulate air pollution exposure and body composition in urban preschool children: examining sensitive windows and sex-specific associations. Environ Res. 2017;158:798–805. https://doi.org/10.1016/j.envres.2017.07.026.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  77. Mao G, Nachman RM, Sun Q, Zhang X, Koehler K, Chen Z, et al. Individual and joint effects of early-life ambient exposure and maternal prepregnancy obesity on childhood overweight or obesity. Environ Health Perspect. 2017;125(6):067005. https://doi.org/10.1289/EHP261.

  78. Lee A, Leon Hsu HH, Mathilda Chiu YH, Bose S, Rosa MJ, Kloog I, et al. Prenatal fine particulate exposure and early childhood asthma: effect of maternal stress and fetal sex. J Allergy Clin Immunol. 2017;8(17):31273–3.

  79. Rosa MJ, Just AC, Kloog I, Pantic I, Schnaas L, Lee A, et al. Prenatal particulate matter exposure and wheeze in Mexican children: effect modification by prenatal psychosocial stress. Ann Allergy Asthma Immunol. 2017;119(3):232–7.e1. https://doi.org/10.1016/j.anai.2017.06.016.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  80. Pennington AF, Strickland MJ, Klein M, Zhai X, Bates JT, Drews-Botsch C, et al. Exposure to mobile source air pollution in early-life and childhood asthma incidence: the Kaiser air pollution and pediatric asthma study. Epidemiology. 2018;29(1):22–30. https://doi.org/10.1097/EDE.0000000000000754.

  81. Oken E, Choi AL, Karagas MR, Marien K, Rheinberger CM, Schoeny R, et al. Which fish should I eat? Perspectives influencing fish consumption choices. Environ Health Perspect. 2012;120(6):790–8. https://doi.org/10.1289/ehp.1104500.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Oken E, Bellinger DC. Fish consumption, methylmercury and child neurodevelopment. Curr Opin Pediatr. 2008;20(2):178–83. https://doi.org/10.1097/MOP.0b013e3282f5614c.

    Article  PubMed  PubMed Central  Google Scholar 

  83. •• Leung YK, Govindarajah V, Cheong A, Veevers J, Song D, Gear R, et al. Gestational high-fat diet and bisphenol A exposure heightens mammary cancer risk. Endocr Relat Cancer. 2017;24(7):365–78. https://doi.org/10.1530/ERC-17-0006. An animal study that describes the concurrent effects of exposure to a high-fat diet and bisphenol A during pregnancy with incidence in mammary tumor formation, alterations in mammary gland development, and gene expression. This study illustrates the potential synergistic effects of exposure to nutritional imbalances and environmental chemicals.

  84. •• Schaider LA, Balan SA, Blum A, Andrews DQ, Strynar MJ, Dickinson ME, Lunderberg DM, Lang JR, Peaslee GF Fluorinated compounds in US fast food packaging. Environ Sci Technol Lett 2017;4(3):105–11. A recent study that details the prevalence of fluorinated chemicals in fast food packaging and demonstrates their potentially significant contribution to dietary PFAS exposure and environmental contamination during production and disposal.

  85. Averina M, Brox J, Huber S, Furberg AS. Perfluoroalkyl substances in adolescents in northern Norway: lifestyle and dietary predictors. The Tromso study, Fit Futures 1. Environ Int. 2018;114:123–30. https://doi.org/10.1016/j.envint.2018.02.031.

    Article  PubMed  CAS  Google Scholar 

  86. Garcia G, Sunil TS, Hinojosa P. The fast food and obesity link: consumption patterns and severity of obesity. Obes Surg. 2012;22(5):810–8. https://doi.org/10.1007/s11695-012-0601-8.

    Article  PubMed  Google Scholar 

  87. Robledo CA, Mendola P, Yeung E, Mannisto T, Sundaram R, Liu D, et al. Preconception and early pregnancy air pollution exposures and risk of gestational diabetes mellitus. Environ Res. 2015;137:316–22. https://doi.org/10.1016/j.envres.2014.12.020.

    Article  PubMed  CAS  Google Scholar 

  88. Genuis SJ, Genuis RA. Preconception care: a new standard of care within maternal health services. Biomed Res Int. 2016;2016:6150976. https://doi.org/10.1155/2016/6150976.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Hatch EE, Wesselink AK, Hahn KA, Michiel JJ, Mikkelsen EM, Sorensen HT, et al. Intake of sugar-sweetened beverages and fecundability in a North American Preconception Cohort. Epidemiology. 2018;29(3):369–78. https://doi.org/10.1097/EDE.0000000000000812.

  90. • Zhang C, Sundaram R, Maisog J, Calafat AM, Barr DB, Buck Louis GM. A prospective study of prepregnancy serum concentrations of perfluorochemicals and the risk of gestational diabetes. Fertil Steril. 2015;103(1):184–9. https://doi.org/10.1016/j.fertnstert.2014.10.001. One of the few studies that have examined exposure to perfluoroalkyl substances during preconception and its associated risks with gestational diabetes during pregnancy, which is suggestive of a possible environmental etiology for gestational diabetes.

    Article  PubMed  CAS  Google Scholar 

  91. Stuppia L, Franzago M, Ballerini P, Gatta V, Antonucci I. Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics. 2015;7:120. https://doi.org/10.1186/s13148-015-0155-4. eCollection 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. •• Schagdarsurengin U, Steger K. Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat Rev Urol. 2016;13(10):584–95. https://doi.org/10.1038/nrurol.2016.157. An important review that summarizes various studies in animal models and human epidemiological data describing the transgenerational effect of the paternally contributed sperm epigenome on long-term health outcomes of the offspring.

    Article  PubMed  CAS  Google Scholar 

  93. Harris MH, Rifas-Shiman SL, Calafat AM, Ye X, Mora AM, Webster TF, et al. Predictors of per- and polyfluoroalkyl substance (PFAS) plasma concentrations in 6–10 year old American children. Environ Sci Technol. 2017;51(9):5193–204. https://doi.org/10.1021/acs.est.6b05811.

  94. Doyle IM, Borrmann B, Grosser A, Razum O, Spallek J. Determinants of dietary patterns and diet quality during pregnancy: a systematic review with narrative synthesis. Public Health Nutr. 2017;20(6):1009–28.

    Article  PubMed  Google Scholar 

  95. Kramer MS. Randomized trials and public health interventions: time to end the scientific double standard. Clin Perinatol 2003. 2003;30(2):351–61.

    Article  Google Scholar 

  96. Abdel Rahman A, Jomaa L, Kahale LA, Adair P, Pine C. Effectiveness of behavioral interventions to reduce the intake of sugar-sweetened beverages in children and adolescents: a systematic review and meta-analysis. Nutr Rev. 2018;76(2):88–107. https://doi.org/10.1093/nutrit/nux061.

    Article  PubMed  Google Scholar 

  97. Vargas-Garcia EJ, Evans CEL, Prestwich A, Sykes-Muskett BJ, Hooson J, Cade JE. Interventions to reduce consumption of sugar-sweetened beverages or increase water intake: evidence from a systematic review and meta-analysis. Obes Rev. 2017;18(11):1350–63.

    Article  PubMed  CAS  Google Scholar 

  98. Asci O, Rathfisch G. Effect of lifestyle interventions of pregnant women on their dietary habits, lifestyle behaviors, and weight gain: a randomized controlled trial. J Health Popul Nutr. 2016;35:7. https://doi.org/10.1186/s41043-016-0044-2.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Allen RW, Barn PK, Lanphear BP. Randomized controlled trials in environmental health research: unethical or underutilized? PLoS Med. 2015;12(1):e1001775. https://doi.org/10.1371/journal.pmed. eCollection 2015 Jan.

  100. •• Fleming TP, Watkins AJ, Velazquez MA, Mathers JC, Prentice AM, Stephenson J, et al. Origins of lifetime health around the time of conception: causes and consequences. Lancet. 2018;16(18):30312-X. The most recent review from Lancet describing the evidence for the effects of preconception health on the growth, development, and long-term health of the offspring. This paper also discusses potential strategies for preconception interventions that are scalable, which could have positive effects on a range of health outcomes.

    Google Scholar 

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Funding

Izzuddin M Aris is supported by the National University of Singapore Overseas Postdoctoral Fellowship (NUS OPF/2017). Abby Fleisch is supported by the National Institutes of Health (K23 ES024803). Emily Oken is supported by the National Institutes of Health (UG3OD023286, P30 DK092924, R01AI102960, R01 HD034568).

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Correspondence to Emily Oken.

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Izzuddin M Aris and Abby F. Fleisch declare no conflicts of interest; Emily Oken reports grants from US National Institutes of Health, during the conduct of the study.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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This article is part of the Topical Collection on Reproductive and Perinatal Epidemiology

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Aris, I.M., Fleisch, A.F. & Oken, E. Developmental Origins of Disease: Emerging Prenatal Risk Factors and Future Disease Risk. Curr Epidemiol Rep 5, 293–302 (2018). https://doi.org/10.1007/s40471-018-0161-0

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