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Maternal Diet, Developmental Origins, and the Intergenerational Transmission of Cardiometabolic Traits: A Window of Opportunity for the Prevention of Metabolic Syndrome?

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Abstract

Hales and Barker’s alternative hypothesis moved beyond simplistic genetic or lifestyle explanations and eventually led to a new paradigm for understanding chronic disease risk. Their main contribution to the advancement of science was the recognition of the powerful role of developmental plasticity, the ability of a gene to generate a range of possible phenotypes depending on environmental experience. This pathway is typified by nutritional excess in early life (e.g., maternal high fat/sugar/energy diets), followed by a “Western” high-energy/low-fiber diet in adulthood. The forefront of the primary mechanisms that drive developmental programming and its transmission from one generation to the next is epigenetics. Both human and animal studies surmise that the effects of developmentally programmed traits may be transmitted to subsequent generations even if not exposed to the same environmental unbalances. Major example of this trans-generational programming is represented by the high prevalence of cardiovascular risks in the US native Indians and Afro-Americans. Beyond this, a new concept of multigenerational programming is emerging from epigenetic studies. For instance, when a pregnant mother is consuming an inadequate, low-protein diet, three generations are effectively being exposed simultaneously to this dietary insult: the pregnant mother (F0), her fetal offspring (F1), and the primordial germ cells (PGCs)—the precursors of sperm and eggs—within the F1 fetus. Multigenerational (i.e., F1, F2) effects have been documented through extensive experimental animal studies as well as epidemiological studies.

The existing worldwide obesity epidemic, in tandem with persistent undernutrition and poor food availability, emphasize the importance of research involving the developmental origins and the multigenerational transmission of cardiometabolic dysregulation. If it is true that maternal (and paternal) epigenomes do transmit multigenerational information that affects developmental programming, then this aspect of the evolution of phenotypic plasticity in humans must be accounted for in the structure and content of interventions to improve adult health.

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References

  1. Hales CN, Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601.

    Article  CAS  PubMed  Google Scholar 

  2. Stearns SC. The evolution of life histories. Oxford: Oxford University Press; 1992.

    Google Scholar 

  3. West-Eberhard MJ. Developmental plasticity and evolution. New York: Oxford University Press; 2003.

    Google Scholar 

  4. Benyshek DC. The developmental origins of obesity and related health disorders–prenatal and perinatal factors. Coll Antropol. 2007;31:11–7.

    PubMed  Google Scholar 

  5. Popkin BM. Global nutrition dynamics: The world is shifting rapidly toward a diet linked with noncommunicable diseases. Am J Clin Nutr. 2006;84:289–98.

    CAS  PubMed  Google Scholar 

  6. Eriksson JG. Patterns of growth: relevance to developmental origins of health and disease. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 223–32.

    Chapter  Google Scholar 

  7. Alfaradhi M, Ozanne S. Developmental programming in response to maternal overnutrition. Front Genet. 2011;2:1–27.

    Article  Google Scholar 

  8. Rkhzay-Jaf J, O’dowd JF, Stocker CJ. Maternal obesity and the fetal origins of the metabolic syndrome. Curr Cardiovasc Risk Rep. 2012;6:487–95.

    Article  PubMed Central  PubMed  Google Scholar 

  9. Stettler N, Stallings VA, Troxel AB, Zhao J, Schinnar R, Nelson SE, Ziegler EE, Strom BL. Weight gain in the first week of life and overweight in adulthood a cohort study of European American subjects fed infant formula. Circulation. 2005;111:1897–903.

    Article  PubMed  Google Scholar 

  10. Singhal A, Cole TJ, Fewtrell M, Lucas A. Breastmilk feeding and lipoprotein profile in adolescents born preterm: follow-up of a prospective randomised study. Lancet. 2004;363:1571–8.

    Article  CAS  PubMed  Google Scholar 

  11. Dewey KG, Heinig M, Nommsen L, Peerson J, Lönnerdal B. Breast-fed infants are leaner than formula-fed infants at 1 y of age: the darling study. Am J Clin Nutr. 1993;57:140–5.

    CAS  PubMed  Google Scholar 

  12. Pirkola J, Pouta A, Bloigu A, Hartikainen A-L, Laitinen J, Järvelin M-R, Vääräsmäki M. Risks of overweight and abdominal obesity at age 16 years associated with prenatal exposures to maternal prepregnancy overweight and gestational diabetes mellitus. Diabetes Care. 2010;33:1115–21.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Guénard F, Deshaies Y, Cianflone K, Kral J, Marceau P, Vohl M. Differential methylation in glucoregulatory genes of offspring born before vs after maternal gastrointestinal bypass surgery. Proc Natl Acad Sci U S A. 2013;110(28):11439–44.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Reynolds R, Osmond C, Phillips D, Godfrey K. Maternal BMI, parity, and pregnancy weight gain: Influences on offspring adiposity in young adulthood. J Clin Endocrinol Metab. 2010;95:5365–9.

    Article  CAS  PubMed  Google Scholar 

  15. Dabelea D. The predisposition to obesity and diabetes in offspring of diabetic mothers. Diabetes Care. 2007;30:S169–74.

    Article  PubMed  Google Scholar 

  16. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005;115:e290–6.

    Article  PubMed  Google Scholar 

  17. Yu Z, Han S, Zhu J, Sun X, Ji C, Guo X. Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: a systematic review and meta-analysis. PLoS One. 2013;8:e61627.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Cnattingius S, Villamor E, Lagerros YT, Wikström AK, Granath F. High birth weight and obesity: a vicious circle across generations. Int J Obes (Lond). 2012;36:1320–4.

    Article  CAS  Google Scholar 

  19. Gluckman PD, Hanson M, Zimmet P, Forrester T. Losing the war against obesity: the need for a developmental perspective. Sci Transl Med. 2011;3(93):93cm19.

    Google Scholar 

  20. Breton C. The hypothalamus-adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol. 2013;216:R19–31.

    Article  CAS  PubMed  Google Scholar 

  21. Sloboda DM, Newnham JP, Moss TJM, Challis JRG. The fetal hypothalamic-pituitary-adrenal axis: relevance to developmental origins of health and disease. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 191–205.

    Chapter  Google Scholar 

  22. Feng B, Zhang T, Xu H. Human adipose dynamics and metabolic health. Ann N Y Acad Sci. 2013;1281:160–77.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. McConnell JML. A mitochondrial component of developmental programming. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 75–81.

    Chapter  Google Scholar 

  24. Portha B, Chavey A, Movassat J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res. 2011;2011:1–16.

    Google Scholar 

  25. Reusens B, Kalbe L, Remacle C. The developmental environment and the endocrine pancreas. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 233–43.

    Chapter  Google Scholar 

  26. Thompson JA, Regnault TRH. In utero origins of adult insulin resistance and vascular dysfunction. Semin Reprod Med. 2011;29:211–24.

    Article  CAS  PubMed  Google Scholar 

  27. Napoli C, Pignalosa O, Rossi L, Botti C, Guarino C, Sica V, de Nigris F. The developmental environment and atherogenesis. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 300–9.

    Chapter  Google Scholar 

  28. Myatt L, Roberts V. Placental mechanisms and developmental origins of health and disease. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 130–42.

    Chapter  Google Scholar 

  29. Waddington CH. The epigenotype. Endeavour. 1942;1:18–20.

    Google Scholar 

  30. Lim JP, Brunet A. Bridging the transgenerational gap with epigenetic memory. Trends Genet. 2013;29:176–86.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet. 2008;9:465–76.

    Article  CAS  PubMed  Google Scholar 

  32. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–95.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Thayer ZM, Kuzawa CW. Biological memories of past environments: epigenetic pathways to health disparities. Epigenetics. 2011;6:798–803.

    Article  PubMed  Google Scholar 

  34. Burdge GC, Lillycrop KA. Nutrition, epigenetics, and developmental plasticity: Implications for understanding human disease. Annu Rev Nutr. 2010;30:315–39.

    Article  CAS  PubMed  Google Scholar 

  35. Drake AJ, Walker BR. The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol. 2004;180:1–16.

    Article  CAS  PubMed  Google Scholar 

  36. Drake AJ, Liu L. Intergenerational transmission of programmed effects: public health consequences. Trends Endocrinol Metab. 2010;21:206–13.

    Article  CAS  PubMed  Google Scholar 

  37. Benyshek D, Johnston C, Martin J. Glucose metabolism is altered in the adequately-nourished grand-offspring (f 3 generation) of rats malnourished during gestation and perinatal life. Diabetologia. 2006;49:1117–9.

    Article  CAS  PubMed  Google Scholar 

  38. Benyshek DC, Johnston CS, Martin JF, Ross WD. Insulin sensitivity is normalized in the third generation (F3) offspring of developmentally programmed insulin resistant (F2) rats fed an energy-restricted diet. Nutr Metab (Lond). 2008;5:26.

    Article  CAS  Google Scholar 

  39. Wells JCK. Maternal capital and the metabolic ghetto: An evolutionary perspective on the transgenerational basis of health inequalities. Am J Hum Biol. 2010;22(1):1–17.

    Article  PubMed  Google Scholar 

  40. Benyshek DC, Martin JF, Johnston CS. A reconsideration of the origins of the type 2 diabetes epidemic among Native Americans and the implications for intervention policy. Med Anthropol. 2001;20(1):25–64.

    Article  CAS  PubMed  Google Scholar 

  41. Kuzawa CW, Sweet E. Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health. Am J Hum Biol. 2009;21:2–15.

    Article  PubMed  Google Scholar 

  42. Li J, Huang J, Li J-S, Chen H, Huang K, Zheng L. Accumulation of endoplasmic reticulum stress and lipogenesis in the liver through generational effects of high fat diets. J Hepatol. 2012;56:900–7.

    Article  CAS  PubMed  Google Scholar 

  43. Plagemann A, Harder T, Brunn M, Harder A, Roepke K, Wittrock-Staar M, Ziska T, Schellong K, Rodekamp E, Melchior K. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol. 2009;587:4963–76.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Skinner MK. What is an epigenetic transgenerational phenotype?: F3 or F2. Reprod Toxicol. 2008;25:2–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Gluckman PD, Hanson MA. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006.

    Book  Google Scholar 

  46. Gluckman PD, Hanson MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004;9:419–25.

    Article  PubMed  Google Scholar 

  47. Hendrix N, Berghella V. Non-placental causes of intrauterine growth restriction. Semin Perinatol. 2008;32:161–5.

    Article  PubMed  Google Scholar 

  48. Walton A, Hammond J. The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proc R Soc Lond B. 1938;125:311–35. Available from: http://rspb.royalsocietypublishing.org/content/125/840/311.

    Article  Google Scholar 

  49. Lunde A, Melve KK, Gjessing HK, Skjærven R, Irgens LM. Genetic and environmental influences on birth weight, birth length, head circumference, and gestational age by use of population-based parent-offspring data. Am J Epidemiol. 2007;165:734–41.

    Article  PubMed  Google Scholar 

  50. Kuzawa CW, Eisenberg DT. Intergenerational predictors of birth weight in the Philippines: correlations with mother’s and father’s birth weight and test of maternal constraint. PLoS One. 2012;7(7):e40905.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Magnus P, Gjessing H, Skrondal A, Skjaerven R. Paternal contribution to birth weight. J Epidemiol Community Health. 2001;55:873–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Coutinho R, David RJ, Collins JW. Relation of parental birth weights to infant birth weight among African Americans and whites in Illinois: a transgenerational study. Am J Epidemiol. 1997;146:804–9.

    Article  CAS  PubMed  Google Scholar 

  53. Agnihotri B, Antonisamy B, Priya G, Fall CHD, Raghupathy P. Trends in human birth weight across two successive generations. Indian J Pediatr. 2008;75:111–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Lumey L, Stein AD, Kahn HS, Romijn J. Lipid profiles in middle-aged men and women after famine exposure during gestation: the Dutch hunger winter families study. Am J Clin Nutr. 2009;89:1737–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Painter R, Osmond C, Gluckman P, Hanson M, Phillips D, Roseboom T. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG. 2008;115:1243–9.

    Article  CAS  PubMed  Google Scholar 

  56. Martin JF, Johnston CS, Han CT, Benyshek DC. Nutritional origins of insulin resistance: a rat model for diabetes-prone human populations. J Nutr. 2000;130:741–4.

    CAS  PubMed  Google Scholar 

  57. Zambrano E, Martínez-Samayoa P, Bautista C, Deas M, Guillen L, Rodríguez-González G, Guzman C, Larrea F, Nathanielsz P. Sex differences in transgenerational alterations of growth and metabolism in progeny (f2) of female offspring (f1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005;566:225–36.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette RR, Otis JP, Chow A, Diaz R, Ferguson-Smith A. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes. 2009;58:460–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Harrison M, Langley-Evans SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr. 2009;101:1020–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol. 2005;288:R34–8.

    Article  CAS  PubMed  Google Scholar 

  61. Anderson CM, Lopez F, Zimmer A, Benoit JN. Placental insufficiency leads to developmental hypertension and mesenteric artery dysfunction in two generations of Sprague-Dawley rat offspring. Biol Reprod. 2006;74:538–44.

    Article  CAS  PubMed  Google Scholar 

  62. Dunn GA, Bale TL. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology. 2009;150:4999–5009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Gniuli D, Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, Vettor R. Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res. 2008;49:1936–45.

    Article  CAS  PubMed  Google Scholar 

  64. Srinivasan M, Mitrani P, Sadhanandan G, Dodds C, Shbeir-Eldika S, Thamotharan S, Ghanim H, Dandona P, Devaskar SU, Patel MS. A high-carbohydrate diet in the immediate postnatal life of rats induces adaptations predisposing to adult-onset obesity. J Endocrinol. 2008;197:565–74.

    Article  CAS  PubMed  Google Scholar 

  65. Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hote JJ. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes. 1991;40:115–20.

    Article  CAS  PubMed  Google Scholar 

  66. Reik W, Collick A, Norris ML, Barton SC, Surani MA. Genomic imprinting determines methylation of parental alleles in transgenic mice. Nature. 1987;328(6127):248–51.

    Article  CAS  PubMed  Google Scholar 

  67. Brunner AM, Nanni P, Mansuy M. Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin. 2014;7:2.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  68. O’Doherty AM, McGettigan PA. Epigenetic processes in the male germline. Reprod Fertil Dev. 2014. doi:10.1071/RD14167.

    PubMed  Google Scholar 

  69. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA, Surani MA. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science. 2013;339:448–52.

    Article  CAS  PubMed  Google Scholar 

  70. Erkek S, Hisano M, Liang CY, Gill M, Murr R, Dieker J, Schübeler D, van der Vlag J, Stadler MB, Peters AH. Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat Struct Mol Biol. 2013;20(7):868–75.

    Article  CAS  PubMed  Google Scholar 

  71. Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur J Hum Genet. 2002;10:682–8.

    Article  CAS  PubMed  Google Scholar 

  72. Kaati G, Bygren LO, Pembrey M, Sjöström M. Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet. 2007;15:784–90.

    Article  CAS  PubMed  Google Scholar 

  73. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M, Golding J. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006;14:159–66.

    Article  PubMed  Google Scholar 

  74. Soubry A, Schildkraut JM, Murtha A, Wang F, Huang Z, Bernal A, Kurtzberg J, Jirtle RL, Murphy SK, Hoyo C. Paternal obesity is associated with igf2 hypomethylation in newborns: results from a newborn epigenetics study (NEST) cohort. BMC Med. 2013;11:29.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Lin WY, Chiu TY, Lee LT, Lin CC, Huang CY, Huang KC. Betel nut chewing is associated with increased risk of cardiovascular disease and all-cause mortality in Taiwanese men. Am J Clin Nutr. 2008;87:1204–11.

    CAS  PubMed  Google Scholar 

  76. Boucher B, Ewen S, Stowers J. Betel nut (areca catechu) consumption and the induction of glucose intolerance in adult cd1 mice and in their f1 and f2 offspring. Diabetologia. 1994;37:49–55.

    Article  CAS  PubMed  Google Scholar 

  77. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology. 2011;152:2228–36.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Jablonka E, Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol. 2009;84:131–76.

    Article  PubMed  Google Scholar 

  79. WHO [Internet]. Controlling the global obesity epidemic; 2013 [cited 2013 Mar 12]. Available from: http://www.who.int/nutrition/topics/obesity/en/.

  80. FAO. The state of food insecurity in the world 2012: economic growth is necessary but not sufficient to accelerate reduction of hunger and malnutrition. Rome: Food and Agricultural Organization of the United Nations; 2012.

    Google Scholar 

  81. Gluckman PD, Hanson MA. The fetal matrix: evolution, development and disease. Cambridge: Cambridge University Press; 2004.

    Book  Google Scholar 

  82. Forrester T. Developmental origins of health and disease: implications for primary intervention for cardiovascular and metabolic disease. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 436–45.

    Chapter  Google Scholar 

  83. Ma N, Hardy DB. The fetal origins of the metabolic syndrome: can we intervene? J Pregnancy. 2012;2012:1–11.

    Article  Google Scholar 

  84. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect. 2006;114(4):567–72.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Li S, Tse IM, Li ET. Maternal green tea extract supplementation to rats fed a high-fat diet ameliorates insulin resistance in adult male offspring. J Nutr Biochem. 2012;23(12):1655–60.

    Article  CAS  PubMed  Google Scholar 

  86. Azemi M, Berisha M, Ismaili-Jaha V, Kolgeci S, Hoxha R, Grajçevci-Uka V, Hoxha- Kamberi T. Vitamin D - dependent rickets, type II case report. Mater Sociomed. 2014;26(1):68–70.

    Article  PubMed Central  PubMed  Google Scholar 

  87. Sardinha FL, Fernandes FS, Tavares do Carmo MG, Herrera E. Sex-dependent nutritional programming: fish oil intake during early pregnancy in rats reduces age-dependent insulin resistance in male, but not female, offspring. Am J Physiol Regul Integr Comp Physiol. 2013;304(4):R313–20.

    Article  CAS  PubMed  Google Scholar 

  88. Benyshek DC, Kachinski JJ, Jin HB. F0 prenatal/lactation diets varying in saturated fat and long-chain polyunsaturated fatty acids alters the insulin sensitivity of F1 rats fed a high fat western diet postweaning. Open J Endocr Metab Dis. 2014;4:245–52.

    Article  Google Scholar 

  89. Imhoff-Kunsch B, Briggs V, Goldenberg T, Ramakrishnan U. Effect of n-3 long-chain polyunsaturated fatty acid intake during pregnancy on maternal, infant, and child health outcomes: a systematic review. Paediatr Perinat Epidemiol. 2012;26(s1):91–107.

    Article  PubMed  Google Scholar 

  90. Courville AB, Harel O, Lammi-Keefe CJ. Consumption of a DHA-containing functional food during pregnancy is associated with lower infant ponderal index and cord plasma insulin concentration. Br J Nutr. 2011;106(2):208–12.

    Article  CAS  PubMed  Google Scholar 

  91. Korotkova TM, Eriksson KS, Haas HL, Brown RE. Selective excitation of GABAergic neurons in the substantia nigra of the rat by orexin/hypocretin in vitro. Regul Pept. 2002;104:83–9.

    Article  CAS  PubMed  Google Scholar 

  92. Carlson SE, Colombo J, Gajewski BJ, Gustafson KM, Mundy D, Yeast J, Georgieff MK, Markley LA, Kerling EH, Shaddy DJ. DHA supplementation and pregnancy outcomes. Am J Clin Nutr. 2013;97(4):808–15.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  93. Carvajal JA. Docosahexaenoic acid supplementation early in pregnancy may prevent deep placentation disorders. BioMed Res Int. 2014;2014:1–10.

    Article  Google Scholar 

  94. Zhao JP, Levy E, Fraser WD, Julien P, Delvin E, Montoudis A, Spahis S, Garofalo C, Nuyy AM, Luo ZC. Circulating docosahexaenoic acid levels are associated with fetal insulin sensitivity. PLoS One. 2014;9(1):e85054.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  95. Rytter D, Bech BH, Christensen JH, Schmidt EB, Henriksen TB, Olsen SF. Intake of fish oil during pregnancy and adiposity in 19-y-old offspring: follow-up on a randomized controlled trial. Am J Clin Nutr. 2011;94(3):701–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  96. 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.

    Article  CAS  PubMed  Google Scholar 

  97. Merialdi M, Carroli G, Villar J, Abalos E, Gülmezoglu AM, Kulier R, Onis M. Nutritional interventions during pregnancy for the prevention or treatment of impaired fetal growth: an overview of randomized controlled trials. J Nutr. 2003;133:1626S–31.

    CAS  PubMed  Google Scholar 

  98. Morton SMB. Maternal nutrition and fetal growth and development. In: Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006. p. 98–129.

    Chapter  Google Scholar 

  99. Kramer MS, Kakuma R. Energy and protein intake in pregnancy. Cochrane Database Syst Rev. 2010;3:1–74.

    Google Scholar 

  100. Behrman J, Calderon M, Preston S, Hoddinott J, Martorell R, Stein A. Nutritional supplementation in girls influences the growth of their children: prospective study in Guatemala. Am J Clin Nutr. 2009;90:1372–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  101. Kuzawa CW, Thayer ZM. Timescales of human adaptation: the role of epigenetic processes. Epigenomics. 2011;3:221–34.

    Article  CAS  PubMed  Google Scholar 

  102. Ozaki T, Nishina H, Hanson MA, Poston L. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol. 2001;530(1):141–52.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  103. Kind KL, Simonetta G, Clifton PM, Robinson JS, Owens JA. Effect of maternal feed restriction on blood pressure in the adult guinea pig. Exp Physiol. 2002;87(4):469–77.

    Article  PubMed  Google Scholar 

  104. Gopalakrishnan GS, Gardner DS, Rhind SM. Programming of adult cardiovascular function after early maternal undernutrition in sheep. Am J Physiol. 2004;287(1):R12–20.

    Article  CAS  Google Scholar 

  105. Roseboom TJ, Van Der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJP, 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  CAS  PubMed  Google Scholar 

  106. Franco MC, Arruda RM, Dantas AP. Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc Res. 2002;56(1):145–53.

    Article  CAS  Google Scholar 

  107. Gardner DS, Tingey K, Van Bon BWM. Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. Am J Physiol. 2005;289(4):R947–54.

    CAS  Google Scholar 

  108. Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305:1733–6.

    Article  CAS  PubMed  Google Scholar 

  109. Wells JCK. The thrifty phenotype as an adaptive maternal effect. Biol Rev. 2007;82:143–72.

    Article  PubMed  Google Scholar 

  110. Kuzawa CW. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol. 2005;17(1):5–21.

    Article  PubMed  Google Scholar 

  111. Huber K, Miles J, Norman A, Thompson N, Davison M, Breier B. Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrinology. 2009;150:4135–44.

    Article  CAS  PubMed  Google Scholar 

  112. Miles J, Huber K, Thompson N, Davison M, Breier B. Moderate daily exercise activates metabolic flexibility to prevent prenatally induced obesity. Endocrinology. 2009;150:179–86.

    Article  CAS  PubMed  Google Scholar 

  113. Vickers MH, Sloboda DM. Strategies for reversing the effects of metabolic disorders induced as a consequence of developmental programming. Front Physiol. 2012;3:242.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Correspondence to Daniel C. Benyshek PhD .

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Benyshek, D.C. (2015). Maternal Diet, Developmental Origins, and the Intergenerational Transmission of Cardiometabolic Traits: A Window of Opportunity for the Prevention of Metabolic Syndrome?. In: Ferrazzi, E., Sears, B. (eds) Metabolic Syndrome and Complications of Pregnancy. Springer, Cham. https://doi.org/10.1007/978-3-319-16853-1_13

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  • DOI: https://doi.org/10.1007/978-3-319-16853-1_13

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