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Journal of Obesity
Volume 2014 (2014), Article ID 204295, 10 pages
http://dx.doi.org/10.1155/2014/204295
Review Article

Periconception Weight Loss: Common Sense for Mothers, but What about for Babies?

1School of Medicine, The University of Queensland, 288 Herston Road, Herston, QLD 4006, Australia
2The UQ Centre for Clinical Research, The University of Queensland, RBWH Campus, Butterfield Street, Herston, QLD 4029, Australia
3The Royal Brisbane and Women’s Hospital, Butterfield Street, Herston, QLD 4029, Australia

Received 11 October 2013; Accepted 3 March 2014; Published 2 April 2014

Academic Editor: Kieron Rooney

Copyright © 2014 Kristine Matusiak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. David McIntyre, K. S. Gibbons, V. J. Flenady, and L. K. Callaway, “Overweight and obesity in Australian mothers: epidemic or endemic?” Medical Journal of Australia, vol. 196, no. 3, pp. 184–188, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. L. K. Callaway, J. B. Prins, A. M. Chang, and H. D. McIntyre, “The prevalence and impact of overweight and obesity in an Australian obstetrics population,” Medical Journal of Australia, vol. 184, no. 2, pp. 56–59, 2006. View at Scopus
  3. S. Y. Chu, S. Y. Kim, and C. L. Bish, “Prepregnancy obesity prevalence in the United States, 2004-2005,” Maternal and Child Health Journal, vol. 13, no. 5, pp. 614–620, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Bellver, L. P. Rossal, E. Bosch et al., “Obesity and the risk of spontaneous abortion after oocyte donation,” Fertility and Sterility, vol. 79, no. 5, pp. 1136–1140, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. J. M. Dodd, R. M. Grivell, A.-M. Nguyen, A. Chan, and J. S. Robinson, “Maternal and perinatal health outcomes by body mass index category,” Australian and New Zealand Journal of Obstetrics and Gynaecology, vol. 51, no. 2, pp. 136–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Flenady, L. Koopmans, P. Middleton et al., “Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis,” The Lancet, vol. 377, no. 9774, pp. 1331–1340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. N. L. Glazer, A. F. Hendrickson, G. D. Schellenbaum, and B. A. Mueller, “Weight change and the risk of gestational diabetes in obese women,” Epidemiology, vol. 15, no. 6, pp. 733–737, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. S. D. McDonald, Z. Han, S. Mulla, and J. Beyene, “Overweight and obesity in mothers and risk of preterm birth and low birth weight infants: systematic review and meta-analyses,” British Medical Journal, vol. 341, p. c3428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Rkhzay-Jaf, J. F. O'Dowd, and C. J. Stocker, “Maternal obesity and the fetal origins of the metabolic syndrome,” Current Cardiovascular Risk Reports, vol. 6, no. 5, pp. 487–495, 2012.
  10. M. R. Torloni, A. P. Betrán, S. Daher et al., “Maternal BMI and preterm birth: a systematic review of the literature with meta-analysis,” Journal of Maternal-Fetal & Neonatal Medicine, vol. 22, no. 11, pp. 957–970, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Villamor and S. Cnattingius, “Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study,” The Lancet, vol. 368, no. 9542, pp. 1164–1170, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. X. Wang, M. J. Davies, and R. J. Norman, “Obesity increases the risk of spontaneous abortion during infertility treatment,” Obesity Research, vol. 10, no. 6, pp. 551–554, 2002. View at Scopus
  13. American College of Obstetricians and Gynecologists, “ACOG Committee opinion no. 549: obesity in pregnancy,” Obstetrics and Gynecology, vol. 121, no. 1, pp. 213–217, 2013.
  14. National Institute for Health and Care Excellence, Weight Management Before, During and after Pregnancy (PH27), National Institute for Health and Care Excellence, London, UK, 2010.
  15. The Royal Australian and New Zealand College of Obstetricians and Gynaecologists, Management of Obesity in Pregnancy (C-Obs 49), 2013.
  16. S. F. Ehrlich, M. M. Hedderson, J. Feng, E. R. Davenport, E. P. Gunderson, and A. Ferrara, “Change in body mass index between pregnancies and the risk of gestational diabetes in a second pregnancy,” Obstetrics and Gynecology, vol. 117, no. 6, pp. 1323–1330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Getahun, C. V. Ananth, Y. Oyelese, M. R. Chavez, R. S. Kirby, and J. C. Smulian, “Primary preeclampsia in the second pregnancy: effects of changes in prepregnancy body mass index between pregnancies,” Obstetrics and Gynecology, vol. 110, no. 6, pp. 1319–1325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Watson, S. Howell, T. Johnston, L. Callaway, S. L. Khor, and S. Cornes, “Pre-pregnancy BMI: costs associated with maternal underweight and obesity in Queensland,” Australian and New Zealand Journal of Obstetrics and Gynaecology, vol. 53, no. 3, pp. 243–249, 2013.
  19. S. Y. Chu, D. J. Bachman, W. M. Callaghan et al., “Association between obesity during pregnancy and increased use of health care,” The New England Journal of Medicine, vol. 358, no. 14, pp. 1444–1453, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. K. L. Connor, J. R. G. Challis, P. van Zijl et al., “Do Alterations in placental 11β-hydroxysteroid dehydrogenase (11βHSD) activities explain differences in fetal hypothalamic-pituitary- adrenal (HPA) function following periconceptional undernutrition or twinning in sheep?” Reproductive Sciences, vol. 16, no. 12, pp. 1201–1212, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. S. McMullen, J. C. Osgerby, L. M. Thurston et al., “Alterations in placental 11β-hydroxysteroid dehydrogenase (11β HSD) activities and fetal cortisol:cortisone ratios induced by nutritional restriction prior to conception and at defined stages of gestation in ewes,” Reproduction, vol. 127, no. 6, pp. 717–725, 2004. View at Scopus
  22. L. J. Edwards and I. C. McMillen, “Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation,” Biology of Reproduction, vol. 66, no. 5, pp. 1562–1569, 2002. View at Scopus
  23. F. H. Bloomfield, M. H. Oliver, P. Hawkins et al., “Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic-pituitary-adrenal axis in late gestation,” Endocrinology, vol. 145, no. 9, pp. 4278–4285, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Kumarasamy, M. D. Mitchell, F. H. Bloomfield et al., “Effects of periconceptional undernutrition on the initiation of parturition in sheep,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 288, no. 1, pp. R67–R72, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. F. H. Bloomfield, M. H. Oliver, P. Hawkins et al., “A periconceptional nutritional origin for noninfectious preterm birth,” Science, vol. 300, no. 5619, p. 606, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. S. E. Chadio, B. Kotsampasi, G. Papadomichelakis et al., “Impact of maternal undernutrition in the hypothalamic-pituitary-adrenal axis responsiveness in sheep at different ages postnatal,” Journal of Endocrinology, vol. 192, no. 3, pp. 495–503, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. M. H. Oliver, F. H. Bloomfield, A. L. Jaquiery, S. E. Todd, E. B. Thorstensen, and J. E. Harding, “Periconceptional undernutrition suppresses cortisol response to arginine vasopressin and corticotropin-releasing hormone challenge in adult sheep offspring,” Journal of Developmental Origins of Health and Disease, vol. 3, no. 1, pp. 52–58, 2012.
  28. S. Zhang, L. Rattanatray, S. M. MacLaughlin et al., “Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring,” The FASEB Journal, vol. 24, no. 8, pp. 2772–2782, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. S. M. MacLaughlin, S. K. Walker, C. T. Roberts, D. O. Kleemann, and I. C. McMillen, “Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep,” Journal of Physiology, vol. 565, no. part 1, pp. 111–124, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. C. W. H. Rumball, F. H. Bloomfield, M. H. Oliver, and J. E. Harding, “Different periods of periconceptional undernutrition have different effects on growth, metabolic and endocrine status in fetal sheep,” Pediatric Research, vol. 66, no. 6, pp. 605–613, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Stevens, G. Begum, A. Cook et al., “Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition,” Endocrinology, vol. 151, no. 8, pp. 3652–3664, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Rattanatray, S. M. MacLaughlin, D. O. Kleemann, S. K. Walker, B. S. Muhlhausler, and I. C. McMillen, “Impact of maternal periconceptional overnutrition on fat mass and expression of adipogenic and lipogenic genes in visceral and subcutaneous fat depots in the postnatal lamb,” Endocrinology, vol. 151, no. 11, pp. 5195–5205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. A. L. Jaquiery, M. H. Oliver, M. Honeyfield-Ross, J. E. Harding, and F. H. Bloomfield, “Periconceptional undernutrition in sheep affects adult phenotype only in males,” Journal of Nutrition and Metabolism, vol. 2012, Article ID 123610, 7 pages, 2012. View at Publisher · View at Google Scholar
  34. E. L. Donovan, C. E. Hernandez, L. R. Matthews, M. H. Oliver, A. L. Jaquiery, F. H. Bloomfield, et al., “Periconceptional undernutrition in sheep leads to decreased locomotor activity in a natural environment,” Journal of Developmental Origins of Health and Disease, vol. 4, no. 4, pp. 296–299, 2013.
  35. A. L. Jaquiery, M. H. Oliver, C. W. H. Rumball, F. H. Bloomfield, and J. E. Harding, “Undernutrition before mating in ewes impairs the development of insulin resistance during pregnancy,” Obstetrics and Gynecology, vol. 114, no. 4, pp. 869–876, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. M. H. Oliver, P. Hawkins, B. H. Breier, P. L. van Zijl, S. A. Sargison, and J. E. Harding, “Maternal undernutrition during the periconceptual period increases plasma taurine levels and insulin response to glucose but not arginine in the late gestation fetal sheep,” Endocrinology, vol. 142, no. 10, pp. 4576–4579, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Lie, J. L. Morrison, O. Williams-Wyss, et al., “Impact of embryo number and periconceptional undernutrition on factors regulating adipogenesis, lipogenesis and metabolism in adipose tissue in the sheep fetus,” The American Journal of Physiology: Endocrinology and Metabolism, vol. 305, no. 8, pp. E931–E941, 2013.
  38. N. A. Smith, F. M. McAuliffe, K. Quinn, P. Lonergan, and A. C. O. Evans, “The negative effects of a short period of maternal undernutrition at conception on the glucose-insulin system of offspring in sheep,” Animal Reproduction Science, vol. 121, no. 1-2, pp. 94–100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. L. M. Nicholas, L. Rattanatray, S. M. MacLaughlin, et al., “Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring,” The FASEB Journal, vol. 27, no. 9, pp. 3786–3796, 2013.
  40. S. E. Todd, M. H. Oliver, A. L. Jaquiery, F. H. Bloomfield, and J. E. Harding, “Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring,” Pediatric Research, vol. 65, no. 4, pp. 409–413, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. L. J. Edwards and I. C. McMillen, “Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 283, no. 3, pp. R669–R679, 2002. View at Scopus
  42. C. Torrens, T. H. Snelling, R. Chau et al., “Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent,” Experimental Physiology, vol. 94, no. 9, pp. 1024–1033, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. B. W. Gallaher, B. H. Breier, C. L. Keven, J. E. Harding, and P. D. Gluckman, “Fetal programming of insulin-like growth factor (IGF)-I and IGF-binding protein-3: evidence for an altered response to undernutrition in late gestation following exposure to periconceptual undernutrition in the sheep,” Journal of Endocrinology, vol. 159, no. 3, pp. 501–508, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. J. L. Weiss, F. D. Malone, D. Emig et al., “Obesity, obstetric complications and cesarean delivery rate—a population-based screening study,” The American Journal of Obstetrics and Gynecology, vol. 190, no. 4, pp. 1091–1097, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. E. S. Morgan, E. Wilson, T. Watkins, F. Gao, and B. J. Hunt, “Maternal obesity and venous thromboembolism,” International Journal of Obstetric Anesthesia, vol. 21, no. 3, pp. 253–263, 2012.
  46. H. E. Robinson, C. M. O'Connell, K. S. Joseph, and N. L. McLeod, “Maternal outcomes in pregnancies complicated by obesity,” Obstetrics and Gynecology, vol. 106, no. 6, pp. 1357–1364, 2005. View at Scopus
  47. L. Bellamy, J.-P. Casas, A. D. Hingorani, and D. Williams, “Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis,” The Lancet, vol. 373, no. 9677, pp. 1773–1779, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Bellamy, J.-P. Casas, A. D. Hingorani, and D. J. Williams, “Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis,” British Medical Journal, vol. 335, no. 7627, pp. 974–977, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. T. J. Rosenberg, S. Garbers, W. Chavkin, and M. A. Chiasson, “Prepregnancy weight and adverse perinatal outcomes in an ethnically diverse population,” Obstetrics and Gynecology, vol. 102, no. 5, part 1, pp. 1022–1027, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. I. C. McMillen, S. M. MacLaughlin, B. S. Muhlhausler, S. Gentili, J. L. Duffield, and J. L. Morrison, “Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition,” Basic and Clinical Pharmacology and Toxicology, vol. 102, no. 2, pp. 82–89, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Dabelea, E. J. Mayer-Davis, A. P. Lamichhane et al., “Association of intrauterine exposure to maternal diabetes and obesity with type 2 diabetes in youth: the SEARCH case-control study,” Diabetes Care, vol. 31, no. 7, pp. 1422–1426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. A. J. Buckley, A. L. Jaquiery, and J. E. Harding, “Nutritional programming of adult disease,” Cell and Tissue Research, vol. 322, no. 1, pp. 73–79, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Mostello, J. Jen Chang, J. Allen, L. Luehr, J. Shyken, and T. Leet, “Recurrent preeclampsia: the effect of weight change between pregnancies,” Obstetrics and Gynecology, vol. 116, no. 3, pp. 667–672, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. J. B. Dixon, M. E. Dixon, and P. E. O'Brien, “Birth outcomes in obese women after laparoscopic adjustable gastric banding,” Obstetrics and Gynecology, vol. 106, no. 5 I, pp. 965–972, 2005. View at Scopus
  55. W. L. Bennett, M. M. Gilson, R. Jamshidi et al., “Impact of bariatric surgery on hypertensive disorders in pregnancy: retrospective analysis of insurance claims data,” British Medical Journal, vol. 340, no. 7757, p. c1662, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. N. L. Hezelgrave and E. Oteng-Ntim, “Pregnancy after bariatric surgery: a review,” Journal of Obesity, vol. 2011, Article ID 501939, 5 pages, 2011. View at Publisher · View at Google Scholar
  57. J. Smith, K. Cianflone, S. Biron et al., “Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 11, pp. 4275–4283, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. J. G. Kral, S. Biron, S. Simard et al., “Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years,” Pediatrics, vol. 118, no. 6, pp. e1644–e1649, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Guenard, Y. Deshaies, K. Cianflone, J. G. Kral, P. Marceau, and M. C. Vohl, “Differential methylation in glucoregulatory genes of offspring born before vs. after maternal gastrointestinal bypass surgery,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 28, pp. 11439–11444, 2013.
  60. F. Guenard, A. Tchernof, Y. Deshaies, et al., “Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients,” Journal of Obesity, vol. 2013, Article ID 492170, 9 pages, 2013. View at Publisher · View at Google Scholar
  61. J. R. Wax, A. Cartin, R. Wolff, S. Lepich, M. G. Pinette, and J. Blackstone, “Pregnancy following gastric bypass for morbid obesity: effect of surgery-to-conception interval on maternal and neonatal outcomes,” Obesity Surgery, vol. 18, no. 12, pp. 1517–1521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. M. M. Kjaer and L. Nilas, “Timing of pregnancy after gastric bypass-a national register-based cohort study,” Obesity Surgery, vol. 23, no. 8, pp. 1281–1285, 2013.
  63. M. S. International, “Real choices, women, contraception and unplanned pregnancy,” Websurvery, commisioned by Marie Stopes International, 2008.
  64. S. M. MacLaughlin, B. S. Mühlhäusler, S. Gentili, and I. C. McMillen, “When in gestation do nutritional alterations exert their effects? A focus on the early origins of adult disease,” Current Opinion in Endocrinology, Diabetes and Obesity, vol. 13, no. 6, pp. 516–522, 2006. View at Publisher · View at Google Scholar
  65. T. Roseboom, S. de Rooij, and R. Painter, “The Dutch famine and its long-term consequences for adult health,” Early Human Development, vol. 82, no. 8, pp. 485–491, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. H. W. Hoek, A. S. Brown, and E. Susser, “The Dutch Famine and schizophrenia spectrum disorders,” Social Psychiatry and Psychiatric Epidemiology, vol. 33, no. 8, pp. 373–379, 1998. View at Publisher · View at Google Scholar · View at Scopus
  67. T. J. Roseboom, J. H. P. van der Meulen, C. Osmond, D. J. P. Barker, A. C. J. Ravelli, and O. P. Bleker, “Plasma lipid profiles in adults after prenatal exposure to the Dutch famine,” The American Journal of Clinical Nutrition, vol. 72, no. 5, pp. 1101–1106, 2000. View at Scopus
  68. T. J. Roseboom, J. H. P. van der Meulen, C. Osmond et al., “Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45,” Heart, vol. 84, no. 6, pp. 595–598, 2000. View at Scopus
  69. T. J. Roseboom, J. H. P. van der Meulen, A. C. J. Ravelli, C. Osmond, D. J. P. Barker, and O. P. Bleker, “Plasma fibrinogen and factor VII concentrations in adults after prenatal exposure to famine,” British Journal of Haematology, vol. 111, no. 1, pp. 112–117, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. R. C. Painter, S. R. de Rooij, P. M. M. Bossuyt et al., “A possible link between prenatal exposure to famine and breast cancer: a preliminary study,” The American Journal of Human Biology, vol. 18, no. 6, pp. 853–856, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. S. R. de Rooij, R. C. Painter, D. I. W. Phillips et al., “Hypothalamic-pituitary-adrenal axis activity in adults who were prenatally exposed to the Dutch famine,” European Journal of Endocrinology of the European Federation of Endocrine Societies, vol. 155, no. 1, pp. 153–160, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. R. C. Painter, S. R. de Rooij, P. M. Bossuyt et al., “Blood pressure response to psychological stressors in adults after prenatal exposure to the Dutch famine,” Journal of Hypertension, vol. 24, no. 9, pp. 1771–1778, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. E. J. Franzek, N. Sprangers, A. C. J. W. Janssens, C. M. van Duijn, and B. J. M. van de Wetering, “Prenatal exposure to the 1944-45 Dutch “hunger winter” and addiction later in life,” Addiction, vol. 103, no. 3, pp. 433–438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. S. R. de Rooij, R. C. Painter, D. I. W. Phillips et al., “Impaired insulin secretion after prenatal exposure to the Dutch famine,” Diabetes Care, vol. 29, no. 8, pp. 1897–1901, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. S. R. de Rooij, R. C. Painter, T. J. Roseboom 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, vol. 49, no. 4, pp. 637–643, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. R. C. Painter, T. J. Roseboom, and O. P. Bleker, “Prenatal exposure to the Dutch famine and disease in later life: an overview,” Reproductive Toxicology, vol. 20, no. 3, pp. 345–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. A. C. J. Ravelli, J. H. P. van der Meulen, C. Osmond, D. J. P. Barker, and O. P. Bleker, “Obesity at the age of 50 y in men and women exposed to famine prenatally,” The American Journal of Clinical Nutrition, vol. 70, no. 5, pp. 811–816, 1999. View at Scopus
  78. C. E. Lopuhaä, T. J. Roseboom, C. Osmond et al., “Atopy, lung function, and obstructive airways disease after prenatal exposure to famine,” Thorax, vol. 55, no. 7, pp. 555–561, 2000. View at Publisher · View at Google Scholar · View at Scopus
  79. R. C. Painter, T. J. Roseboom, G. A. van Montfrans et al., “Microalbuminuria in adults after prenatal exposure to the Dutch famine,” Journal of the American Society of Nephrology, vol. 16, no. 1, pp. 189–194, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. L. H. Lumey, “Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944-1945,” Paediatric and Perinatal Epidemiology, vol. 6, no. 2, pp. 240–253, 1992. View at Scopus
  81. B. T. Heijmans, E. W. Tobi, A. D. Stein et al., “Persistent epigenetic differences associated with prenatal exposure to famine in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 44, pp. 17046–17049, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Rayco-Solon, A. J. Fulford, and A. M. Prentice, “Differential effects of seasonality on preterm birth and intrauterine growth restriction in rural Africans,” The American Journal of Clinical Nutrition, vol. 81, no. 1, pp. 134–139, 2005. View at Scopus
  83. P. Rayco-Solon, A. J. Fulford, and A. M. Prentice, “Maternal preconceptional weight and gestational length,” The American Journal of Obstetrics and Gynecology, vol. 192, no. 4, pp. 1133–1136, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. S. E. Moore, T. J. Cole, E. M. E. Poskitt et al., “Season of birth predicts mortality in rural Gambia,” Nature, vol. 388, no. 6641, p. 434, 1997. View at Publisher · View at Google Scholar · View at Scopus
  85. R. A. Waterland, R. Kellermayer, E. Laritsky et al., “Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles,” PLoS Genetics, vol. 6, no. 12, Article ID e1001252, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. F. Rutters, A. G. Nieuwenhuizen, S. G. T. Lemmens, J. M. Born, and M. S. Westerterp-Plantenga, “Hypothalamic-Pituitary-Adrenal (HPA) axis functioning in relation to body fat distribution,” Clinical Endocrinology, vol. 72, no. 6, pp. 738–743, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Kumari, M. Shipley, M. Stafford, and M. Kivimaki, “Association of diurnal patterns in salivary cortisol with all-cause and cardiovascular mortality: findings from the Whitehall II study,” Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 5, pp. 1478–1485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. J. R. G. Challis, F. H. Bloomfield, A. D. Booking et al., “Fetal signals and parturition,” Journal of Obstetrics and Gynaecology Research, vol. 31, no. 6, pp. 492–499, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. L. J. Edwards, A. E. Bryce, C. L. Coulter, and I. C. McMillen, “Maternal undernutrition throughout pregnancy increases adrenocorticotrophin receptor and steroidogenic acute regulatory protein gene expression in the adrenal gland of twin fetal sheep during late gestation,” Molecular and Cellular Endocrinology, vol. 196, no. 1-2, pp. 1–10, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. J. A. Glickman and J. R. G. Challis, “The changing response pattern of sheep fetal adrenal cells throughout the course of gestation,” Endocrinology, vol. 106, no. 5, pp. 1371–1376, 1980. View at Scopus
  91. D. S. Gardner, B. W. M. van Bon, J. Dandrea et al., “Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep,” Journal of Endocrinology, vol. 190, no. 2, pp. 203–212, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. J. T. Ross, I. C. McMillen, F. Lok, A. G. Thiel, J. A. Owens, and C. L. Coulter, “Intrafetal insulin-like growth factor-I infusion stimulates adrenal growth but not steroidogenesis in the sheep fetus during late gestation,” Endocrinology, vol. 148, no. 11, pp. 5424–5432, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. W. Y. Kwong, A. E. Wild, P. Roberts, A. C. Willis, and T. P. Fleming, “Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension,” Development, vol. 127, no. 19, pp. 4195–4202, 2000. View at Scopus
  94. S. N. Hancock, M. H. Oliver, C. Mclean, A. L. Jaquiery, and F. H. Bloomfield, “Size at birth and adult fat mass in twin sheep are determined in early gestation,” Journal of Physiology, vol. 590, no. part 5, pp. 1273–1285, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Romero-Corral, V. K. Somers, J. Sierra-Johnson et al., “Normal weight obesity: a risk factor for cardiometabolic dysregulation and cardiovascular mortality,” European Heart Journal, vol. 31, no. 6, pp. 737–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. G. Begum, A. Davies, A. Stevens, et al., “Maternal under nutrition programs tissue-specific epigenetic changes in the glucocorticoid receptor in adult offspring,” Endocrinology, vol. 154, no. 12, pp. 4560–4569, 2013.
  97. D. S. Gardner, K. Tingey, B. W. M. van Bon et al., “Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 289, no. 4, pp. R947–R954, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. P. M. Catalano, E. D. Tyzbir, R. R. Wolfe et al., “Carbohydrate metabolism during pregnancy in control subjects and women with gestational diabetes,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 264, no. 1, part 1, pp. E60–E67, 1993. View at Scopus
  99. S. Joshi, V. Garole, M. Daware, S. Girigosavi, and S. Rao, “Maternal protein restriction before pregnancy affects vital organs of offspring in Wistar rats,” Metabolism: Clinical and Experimental, vol. 52, no. 1, pp. 13–18, 2003. View at Scopus
  100. R. H. Eckel, S. M. Grundy, and P. Z. Zimmet, “The metabolic syndrome,” The Lancet, vol. 365, no. 9468, pp. 1415–1428, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. J. A. Whitworth, G. J. Mangos, and J. J. Kelly, “Cushing, cortisol, and cardiovascular disease,” Hypertension, vol. 36, no. 5, pp. 912–916, 2000. View at Scopus
  102. R. M. Reynolds, B. R. Walker, H. E. Syddall et al., “Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 1, pp. 245–250, 2001. View at Publisher · View at Google Scholar · View at Scopus
  103. S. M. Gold, I. Dziobek, K. Rogers, A. Bayoumy, P. F. McHugh, and A. Convit, “Hypertension and hypothalamo-pituitary-adrenal axis hyperactivity affect frontal lobe integrity,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 6, pp. 3262–3267, 2005. View at Publisher · View at Google Scholar · View at Scopus