Metabolic syndrome: Role of maternal undernutrition and fetal programming

Reviews in Endocrine and Metabolic Disorders

Volumn 14, Issue 3, 2013, Pages 229-240

  Lakshmy, Ramakrishnan ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Fetal programming; Intrauterine growth retardation; Macronutrients; Metabolic syndrome; Micronutrients

Indexed keywords

CALCIUM ION; CARBOHYDRATE; CHROMIUM; IRON; MAGNESIUM ION; PROTEIN; TRACE ELEMENT; VITAMIN D; ZINC;

ADULT DISEASE; ARTICLE; BIRTH WEIGHT; CALCIUM DEFICIENCY; CALORIC RESTRICTION; CARBOHYDRATE DIET; CELL AGING; CHRONIC DISEASE; CIRCADIAN RHYTHM; DIETARY INTAKE; DISEASE ASSOCIATION; EMBRYONIC AND FETAL FUNCTIONS; EPIGENETICS; FETAL PROGRAMMING; FETUS; FETUS GROWTH; FETUS OUTCOME; FOOD INTAKE; GENE EXPRESSION; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAUTERINE GROWTH RETARDATION; IRON DEFICIENCY; LIPID DIET; MACRONUTRIENT; MAGNESIUM DEFICIENCY; MALNUTRITION; MATERNAL NUTRITION; METABOLIC SYNDROME X; NONHUMAN; NUTRITIONAL HEALTH; OXIDATIVE STRESS; PHYSICAL ACTIVITY; PREGNANCY; PROTEIN RESTRICTION; SENESCENCE; TELOMERE; VITAMIN D DEFICIENCY; VITAMIN DEFICIENCY; VITAMIN INTAKE;

FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; HUMANS; METABOLIC SYNDROME X; MICRONUTRIENTS;

EID: 84885582821     PISSN: 13899155     EISSN: 15732606     Source Type: Journal    
DOI: 10.1007/s11154-013-9266-4     Document Type: Article

References (140)

1. Alberti KG, Zimmet P, Shaw J. Metabolic syndrome-a new world definition. A consensus statement from International Diabetes Federation. Diabet Med. 2006;23:469-80.
2. Kelly T, Yang W, Chen CS, Reynolds K, He J. Global burden of obesity in 2005 and projections in 2030. Int J Obes. 2008;32:1431-7.
3. Van Dieren S, Beulens JW, van der Schouw YT, Grobbee DE, Neal B. The global burden of diabetes and its complications: an emerging pandemic. Eur J Prev Rehabil. 2010;17:S3-8.
4. 0311. Geneva: World Health Organization; 2006.
5. Han JC, Lawlor DA, Kimm SY. Childhood obesity. Lancet. 2010;375:1737-48.
6. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: finding from the Third National Health and Nutrition Examination Survey. JAMA. 2002;287:356-9.
7. Misra A, Misra R, Wijesuriya M, Banerjee D. The metabolic syndrome in South Asians: continuing escalation and possible solutions. Indian J Med Res. 2007;125:345-54.
8. Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71:1344S-52.
9. Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185:73-9.
10. UNICEF and WHO. Low birthweight: country, regional and global estimates. UNICEF; 2004. pgs 27.
11. Jain V, Singhal A. Catchup growth in low birth weight infants: striking a healthy balance. Rev Endocr Metab Disord. 2012;13:141-7.
12. Gluckman PD, Hanson MA. Developmental origins of diseases paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004;56:311-7.
13. Gluckman PD, Hanson MA, Beedle AS, Spencer HG. Predictive adaptive responses in perspective. Trends Endocrinol Metab. 2008;19:109-10.
14. Barker DJ, Osmond C. Low birth weight and hypertension. Br Med J. 1988;297:134-5.
15. Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976;295:349-53.
16. Ravelli AC, van Der Meulen JH, Osmund C, Barker DJ, Bleker OP. Obesity at the age of 50 in men and women exposed to famine prenatally. Am J Clin Nutr. 1999;70:811-6.
17. Osmund C, Barker DJ, Winter PD, Fall CH, Simmonds SJ. Early growth and death from cardiovascular disease in women. Br Med J. 1993;307:1519-24.
18. Edwards LJ, McMillen IC. Impact of maternal undernutrition during periconceptual period, fetal number, and fetal sex on the development of the hypothalamic pituitary axis in sheep during late gestation. Biol Reprod. 2002;66:1562-9.
19. Brennan KA, Gopalakrishnan GS, Kurlak L, Rhind SM, Kyle CE, Brooks AN, et al. Impact of maternal undernutrition and fetal number on glucocorticoid, growth hormone and insulin like growth factor receptor mRNA abundance in the ovine fetal kidney. Reproduction. 2005;129:151-9.
20. Bhavdekar A, Yagnik CS, Fall CHD, et al. Insulin resistance syndrome in 8-year old Indian children: small at birth, big at 8 years or both? Diabetes. 1999;48:2422-9.
21. Lear SA, Kohli A, Bondy GP, Tchernof A, Sniderman AD. Ethnic variation in fat and lean body mass and the association with insulin resistance. J Clin Endocrinol Metab. 2009;94:4696-702.
22. Patti ME. Intergenerational programming of metabolic diseases: evidence from human populations and experimental animal models. Cell Mol Life Sci. 2013;70:1597-608.
23. Barker DJP, Hales CN, Fall CHD, Osmond C, Phipps K, Clark PMS. Type 2 diabetes (non insulin dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X) relation to reduced fetal growth. Diabetologia. 1993;36:62-7.
24. De Rooji SR, Painter RC, Holleman F, Bossuyt PM, Roseboom TJ. The metabolic syndrome in adults prenatally exposed to the Dutch famine. Am J Clin Nutr. 2007;86:1219-24.
25. Yarbrough DE, Barrett-Connor E, Kritz-Silverstein D, Wingard DL. Birth weight, adult weight, and girth as predictors of metabolic syndrome in postmenopausal women: the Rancho Bernardo study. Diabetes Care. 1998;21:1652-8.
26. Ramdhani MK, Grobbee DE, Bots ML, Castro CM, Vos LE, et al. Lower birth weight predicts metabolic syndrome in young adults: the atherosclerosis risk in young adults (ARYA)-study. Atheroslerosis. 2006;184:21-7.
27. 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.
28. Xiao X, Zhang ZX, Li WH, Feng K, Sun Q, Cohen HJ, et al. Low birth weight is associated with components of the metabolic syndrome. Metab Clin Exp. 2010;59:1282-6.
29. Hult M, Tornhammar P, Ueda P, Chima C, Edstedt Bonamy A-K, et al. Hypertension, diabetes and overweight: looming legacies of the Biafram famine. PLoS One. 2010;5:e13582.
30. Phillips DJ, Barker DJ, Hales CN, Hirst S, Osmund C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994;37:150-4.
31. Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J Clin Endocrinol Metab. 2000;85:1401-6.
32. Lussana F, Painter RC, Ocke MC, Buller HR, Bossuyt PM, Roseboom TJ. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr. 2008;88:1648-52.
33. Kajantie E, Barker DJ, Osmund C, Forsen T, Erikkson JG. Growth before 2 years of age and serum lipids 60 years later: the Helsinki Birth Cohort study. Int J Epidemiol. 2008;37:280-9.
34. Lauren L, Jarvelin MR, Elliott P, Sovio U, Spellman A, et al. Relationship between birth weight and blood lipid concentrations in later life: evidence from the existing literature. Int J Epidemiol. 2003;37:280-9.
35. Kensara OA, Wootton SA, Phillips DI, Patel M, Jackson AA, Elia M. Fetal programming of body composition: relation between birth weight and body composition measured with dual energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr. 2005;82:980-7.
36. Parsons TJ, Power C, Manor O. Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: longitudinal study. Br Med J. 2001;323:1331-5.
37. Lawlor DA, Ronalds G, Clark H, Smith GD, Leon DA. Birth weight is inversely associated with incident coronary heart disease and stroke among individuals born in the 1950s: finding from the Aberdeen Children of the 1950s cohort study. Circulation. 2005;112:1414-8.
38. Rich-Edwards JW, Kleinman K, Michels KB, Stamfer MJ, Manson JE, et al. Longitudinal study of birth weight and adult body mass index in predicting risk of coronary heart disease and stroke in women. Br Med J. 2005;330:1115.
39. Fall CHD, Sachdev HPS, Osmond C, et al. Adult metabolic syndrome and impaired glucose tolerance are associated with different patterns of body mass index gain during infancy; data from the New Delhi birth cohort. Diabetes Care. 2008;31:2349-56.
40. Desai M, Growther NJ, Lucas A, Hales CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr. 1996;76:591-603.
41. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21 days old female offspring. Am J Physiol Regul Integr Comp Physiol. 2005;288:R 368-73.
42. Ozanne S, Olsen GS, Hansen LL, Tingey KJ, Nave BT, Wang CL, et al. Early growth restriction leads to down regulation of protein Kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003;177:235-41.
43. Maloney CA, Gosby AK, Phuyal JI, Denyer GS, Bryson JM, Caterson ID. Site specific changes in the expression of fat portioning genes in the weanling rats exposed to a low protein diet in utero. Obes Res. 2003;11:461-8.
44. Berends LM, Fernandez-Twinn DS, Martin-Gronert MS, Cripps RL, Ozanne SE. Catchup growth following intrauterine growth restriction programmes an insulin resistant phenotype in adipose tissue. Int J Obes. 2012. doi: 10.1038/ijo.2012.196.
45. Campbell DM, Hall MH, Barker DJP, Cross J, Sheill AW, Godfrey KM. Diet in pregnancy and the offspring's blood pressure 40 years later. Br J Obstet Gynaecol. 1996;103:273-80.
46. Rerkasem K, Wongthanee A, Rerkasem A, Chiowanich P, Sritara P, Pruenlampoo S, et al. Intrauterine nutrition and carotid intimal media thickness in young Thai adults. Asia Pac J Clin Nutr. 2012;21:247-52.
47. Brown LD, Green AS, Limesand SW, Rozance PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci. 2011;1:428-44.
48. Wu G, Bazer FW, Satterfield MC, Li X, Wang X, Johnson GA, et al. Impacts of arginine nutrition on embryonic and fetal development in mammals. Amino Acids. 2013;45:241-56.
49. Fidalgo M, Falcao-Tebas F, Bento-Santos A, de Oliveira E, Nogueira-Neto JF, de Moura EG, et al. Programmed changes in the adult rat offspring caused by maternal protein restriction during gestation and lactation are attenuated by maternal low physical training. Br J Nutr. 2012;1:1-8.
50. Garofano A, Czernichow P, Bréant B. Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat. Diabetologia. 1998;41:1114-20.
51. Holemans K, Gerber R, Meurrens K, De Clerck F, Poston I, Van Assche FA. Maternal food restriction in the second hals of pregnancy affects vascular function but not blood pressure of rat female offsprings. Br J Nutr. 1999;81:73-9.
52. Simmons RA, Templeton LJ, Gertz SI. Intrauterine growth retardation leads to development of type 2 diabetes in rat. Diabetes. 2001;50:2279-86.
53. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD. Fetal origins of hyperphagia, obesity and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000;279:E83-7.
54. Krechowec SO, Vickers M, Gertler A, Breier BH. Prenatal influences on leptin sensitivity and susceptibility to diet induced obesity. J Endocrinol. 2006;189:355-63.
55. Ikenasio-Thorpe BA, Breier BH, Vickers MH, Fraser M. Prenatal influences on susceptibility to diet induced obesity are mediated by altered neuroendocrine gene expression. J Endocrinol. 2007;193:31-7.
56. Vickers MH, Breier BH, McCarthy D, Gluckman PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrtion. Am J Physiol Regul Integr Comp Physiol. 2003;285:R271-3.
57. Desai M, Gayle D, Babu J, Rose MG. Programmed obesity in intrauterine growth restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288:R91-6.
58. Roseboom T, de Rooji S, Painter RC. The Dutch famine and its long consequences for adult health. Early Hum Dev. 2006;82:485-91.
59. De Rooji SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ. Prenatal undernutrition and cognitive function in late adulthood. PNAS USA. 2010;107:16881-6.
60. Ravelli AC, van der Meulen JH, Michels RP, Osmund C, Barker DJ, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351:173-7.
61. Pennigton KA, Harper JL, Sigafoos AN, Beffa LM, Carleton SM, Phillips CL, et al. Effect of food restriction and leptin supplementation on fetal programming in mice. Endocrinology. 2012;153:4556-67.
62. Bhargava SK, Sachdev HPS, Fall CHD, Osmund C, Lakshmy R, Barker DJP, et al. Relation of serial changes in childhood body mass index to impaired glucose tolerance in young adulthood. N Engl J Med. 2004;350:865-75.
63. Sachdev HPS, Fall CHD, Osmond C, Lakshmy R, Dey Biswas SK, Leary SD, et al. Anthropometric indicators of body composition in young adults: relation to size at birth and serial measurements of body mass index in childhood; the New Delhi birth cohort. Am J Clin Nutr. 2005;82:456-66.
64. Fall CHD, Sachdev HPS, Osmond C, Lakshmy R, Biswas SD, Prabhakaran D, et al. Adult metabolic syndrome and impaired glucose tolerance are associated with different patterns of body mass index gain during infancy; Data from the New Delhi birth cohort. Diabetes Care. 2008;31:2349-56
65. Sachdev HPS, Osmond C, Fall CHD, Lakshmy R, Ramji S, Dey Biswas SK, et al. Predicting adult metabolic syndrome from childhood body mass index; follow-up of the New Delhi Birth Cohort. Arch Dis Child. 2009;94:768-74.
66. Huffman MD, Prabhakaran D, Osmond C, Fall CHD, Tandon N, Lakshmy R, et al. Incidence of cardiovascular risk factors in an Indian urban cohort. J Am Coll Cardiol. 2011;57:1766-74.
67. Yajnik C. Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult onset disease. Proc Nutr Soc. 2000;59:257-65.
68. Hartil K, Vuguin PM, Kruse M, Schmuel E, Fiallo A, Vargas C, et al. Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero. Pediatr Res. 2009;66:368-73.
69. Chechi K, Cheema SK. Maternal diet rich in saturated fats has deleterious effects on plasma lipids of mice. Exp Clin Cardiol. 2006;11:129-35.
70. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008;51:383-92.
71. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, et al. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology. 2009;50:1796-808.
72. Kruse M, Seki Y, Vuguin PM, Du XQ, Fiallo A, Glenn AS, et al. High fat intake during pregnancy and lactation exacerbates high fat diet induced complications in male offspring in mice. Endocrinology. 2013. doi: 10.1210/en.2012-1877.
73. Brenseke B, Prater MR, Bahamonde J, Gutierrez C. Current thoughts on maternal nutrition and fetal programming of the metabolic syndrome. J Pregnancy. 2013. doi: 10.1155/2013/368461.
74. Burueno AL, Cabrerizo R, Mansilla NG, Sookoian S, Pirola CJ. Maternal high fat intake during pregnancy programs metabolic syndrome related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. J Nutr Biochem. 2013;24:6-13.
75. Rawana S, Clark K, Zhong S, Buison, Chackunkal S, Jen KL. Low dose fructose ingestion during gestation and lactation affects carbohydrate metabolism in rat dams and their offspring. J Nutr. 1993;123:2158-65.
76. Vickers MH, Clayton ZE, Yap C, Sloboda DM. Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology. 2011;152:1378-87.
77. Goran MI, Dumke K, Bouret SG, Kayser B, Walker RW, Blumberg B. The obesogenic effect of high fructose exposure during early development. Nat Rev Endocrinol. 2013. doi: 10.1038/nrendo.2013.108.
78. Christian P, Stewart CP. Maternal micronutrient deficiency, fetal development and risk of chronic disease. J Nutr. 2010;140:437-45.
79. Bourque SL, Komolova M, Nakatsu K, Adams MA. Perinatal iron deficiency and blood pressure. Hypertension. 2008;51:154-9.
80. Lisle SJ, Lewis RM, Petry CJ, Ozanne SE, Hales CN, Forhead AJ. Effect of maternal iron restriction during pregnancy on renal morphology in the adult rat offspring. Br J Nutr. 2003;90:33-9.
81. Gambling L, Dunford S, Wallace DI, Zuur G, Solanky N, Srai SK, et al. Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol (Lond). 2003;552:603-10.
82. Lewis RM, Petry CJ, Ozanne SE, Hales CN. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring. Metabolism. 2001;50:562-7.
83. Bourque SL, Komolova M, McCabe K, Adams MA, Nakatsu K. Perinatal iron deficiency combined with a high-fat diet causes obesity and cardiovascular dysregulation. Endocrinology. 2012;153:1174-82.
84. Cefalu WT, Hu FB. Role of chromium in human health and in diabetes. Diabetes Care. 2004;27:2741-51.
85. Padmavathi IJN, Rao KR, Venu L, Ganeshan M, Kumar AK, Rao CN, et al. Chronic maternal dietary chromium restriction modulates visceral adiposity: probable underlying mechanisms. Diabetes. 2010;59:98-104.
86. Venu L, Harishankar N, Krishna TP, Raghunath M. Maternal dietary vitamin restriction increases body fat content but not insulin resistance in WNIN rat offspring up to 6 months of age. Diabetologia. 2004;47:1493-501.
87. Kumar KA, Lalitha A, Pavithra D, Padmavathi IJN, Ganeshan M, Rao KR, et al. Maternal dietary folate and/or vitamin B12 restrctions alter body composition (adiposity) and lipid metabolism in Wistar rat offspring. J Nutr Biochem. 2013;24:25-31.
88. Lewis SJ, Leary S, Davey Smith G, Ness A. Body composition at age 9 years, maternal folate intake during pregnancy and methyltetrahydrofolate reductase (MTHFR) C677T genotype. Br J Nutr. 2009;102:493-6.
89. Yajnik CS, Deshpande SS, Jackson AA, Refsum H, Rao S, Fisher DJ, et al. Vitamin B(12) and folate concentrations during pregnancy and insulin resistance in the off- spring: the Pune Maternal Nutrition Study. Diabetologia. 2008;51:29-38.
90. Morris GE, Zhou Q, Hegsted M, Keenan MJ. Maternal consumption of low vitamin D diet retards metabolic and contractile development in neonatal rat heart. J Mol Cell Cardiol. 1995;27:1245-50.
91. Gale CR, Robinson SM, Harvey NC, Javaid MK, Jiang B, Martyn CN, et al. Maternal vitamin D status during pregnancy and child outcomes. Eur J Clin Nutr. 2008;62:68-77.
92. Lapillonne A. Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Med Hypotheses. 2010;74:71-5.
93. Merlet-Benichou C. Influence of fetal environment on kidney development. Int J Dev Biol. 1999;43:453-6.
94. Lelievre-Pegorier M, Vilar J, Ferrier ML, Moreau E, Freund N, Gilbert T, et al. Mild vitamin A deficiency leads to inborn nephron deficit in the rat. Kidney Int. 1998;54:1455-62.
95. Matthews KA, Rhoten WB, Driscoll HK, Chertow BS. Vitamin A deficiency impairs fetal islet development and causes subsequent glucose intolerance in adult rats. J Nutr. 2004;134:1958-63.
96. Khatry SK, West KP, Stewart CP, Katz J, LeClerq SC, Schulze KJ, et al. Maternal vitamin A supplementation during pregnancy has no impact on blood pressure in pre-adolescent children in rural Nepal. The 2nd international meeting of the Micronutrient Forum, May 12-15, Beijing, China, Abst No. W56; 2009
97. Venu L, Kishore YD, Raghunath M. Maternal and perinatal magnesium restriction predisposes rat pups to insulin resistance and glucose intolerance. J Nutr. 2005;135:1353-8.
98. Venu L, Harishankar N, Krishna TP, Raghunath M. Does maternal dietary mineral restriction per se predispose the offspring to insulin resistance? Eur J Endocrinol. 2004;151:287-94.
99. Jou MY, Phillips AF, Lonnerdal B. Maternal zinc deficiency in rats affects growth and glucose metabolism in the offspring by inducing insulin resistance postnatally. J Nutr. 2010;140:1621-7.
100. Jou MY, Lonnerdal B, Phillips AF. Maternal Zinc restriction affects postnatal growth and glucose homeostasis in rat offspring diffenetly depending upo adequancy of their nutirents. Pediatr Res. 2012;71:228-34.
101. Bergel E, Belizan JM. A deficient maternal calcium intake during pregnancy increases blood pressure of the offspring in adult rats. BJOG. 2002;109:540-5.
102. Bakker R, Rifas-Shiman SL, Kleinman KP, Lipshultz SE, Gillman MW. Maternal calcium intake during pregnancy and blood pressure in the offspring at age 3 years: a follow-up analysis of the Project Viva cohort. Am J Epidemiol. 2008;168:1374-80.
103. Hiller JE, Crowther CA, Moore VA, Willson K, Robinson JS. Calcium supplementation in pregnancy and its impact on blood pressure in children and women: follow up of a randomised controlled trial. Aust N Z J Obstet Gynaecol. 2007;47:115-21.
104. Hawkesworth S. Conference on "Multidisciplinary Approaches to Nutritional Problems". Postgraduate Symposium. Exploiting dietary supplementation trials to assess the impact of the prenatal environment on CVD risk. Proc Nutr Soc. 2009;68:78-88.
105. Hales CN, Barker DJP. Type 2 diabetes: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595-601.
106. Simmons RA, Gounis AS, Bangalore SA, Ogata ES. Intrauterine growth retardation: fetal glucose transport is diminished to lungs but spared in brain. Pediatr Res. 1992;31:59-63.
107. Simmons RA, Flozak AS, Ogata ES. The effect of insulin and insulin like growth factor-I on glucose transport in normal and small for gestational age fetal rats. Endocrinology. 1993;133:1361-8.
108. Giabfarani S, Germani D, Branca F. Low birthweight and adult insulin resistance: the catchup growth hypothesis. Arch Dis Childhood. 1999;81:171-3.
109. Luo ZC, Fraser WD, Julien P, Deal AC, Audibert F, Smith GN, et al. Tracing the origins of fetal origins of adult diseases: programming by oxidative stress. Med Hypotheses. 2006;66:18-44.
110. Willcox JK, Ash SL, Gatignani L. Antioxidants and prevention of chronic diseases. Crit Rev Food Sci Nutr. 2004;44:275-95.
111. Gupta P, Narang M, Banerjee BD, Basu S. Oxidative stress in term small for gestational age neonates born to undernourished mothers: a case control study. BMC Pediatr. 2004;4:14.
112. Baydas G, Karatas E, Gursu MF, Bozkurt HA, Ilhan N, Yassar A, et al. Antioxidant vitamin levels in term and preterm infants and their relation to maternal vitamin status. Arch Med Res. 2002;33:276-80.
113. Datta S, Patterson EH, Vincitore M, Tonkiss J, Morgane PJ, Galler JR. Prenatal protein malnourished rats show changes in sleep/wake behavior as adults. J Sleep Res. 2000;9:71-9.
114. Breton C, Lukaszewski MA, Risold PY, Enache M, Guillemot J, Delahaye F, et al. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am J Physiol Endocrinol Metab. 2009;296:E462-72.
115. Edwards GR, Benediktsson R, Lindsay RS, Secki JR. Dysfunctions of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet. 1993;341:355-7.
116. Phillips DIW, Walker BR, Reynolds RM, Flanagan DEH, Wood PJ, Osmond C, et al. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension. 2000;35:1301-6.
117. Phillips DIW, Barker DJP, Fall CHD, Secki JR, Whorwood CB, Wood PJ, et al. Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome? J Clin Endocrinol Metab. 1998;83:757-60.
118. Reynolds RM. Glucocorticoid excess and the developmental origins of disease: two decades of testing hypothesis-2012 Curt Richter Award Winner. Psychoneuroendocrinology. 2013;38:1-11.
119. Ahima RS, Prabakaran D, Flier JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest. 1998;101:1020-7.
120. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005;146:4211-6.
121. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046-9.
122. Godfrey KM, Sheppard A, Gluckman PD, Lillycrop KA, Burdge GC, McLean C, et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes. 2011;60:1528-34.
123. Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Investig. 2008;118:2316-24.
124. Jennings BJ, Ozanne SE, Dorling MW, Hales CN. Early growth determines longevity in male rats and may be related to telomere shortening in the kidneys. FEBS Lett. 1999;448:4-8.
125. Tarry Adkins JL, Martin-Gronert MS, Cehn JH, Cripps RL, Ozanne SE. Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 2008;22:2037-44.
126. Tarry-Adkins JL, Chen JH, Smith NS, Jones RH, Cherif H, Ozanne SE. Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 2009;23:1521-8.
127. Raqib R, Alam DS, Sarker P, Ahmad SM, Ara G, Yunus M, et al. Low birth weight is associated with altered immune function in rural Bangladesh children: a birth cohort study. Am J Clin Nutr. 2007;85:845-52.
128. Kajantie E, Pietillainen KH, Wehkalampi K, Kananen L, Raikkonen K, Rissanen A, et al. No association between body size at birth and leucocyte telomere length in adult life-evidence from three cohort studies. Int J Epidemiol. 2012;41:1400-8.
129. Hallows SE, Regnault TRH, Betts DH. The long and short of it: the role of telomeres in fetal origins of adult disease. J Pregnancy. 2012. doi: 10.1155/2012/638476.
130. Chang E, Harley CB. Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Med Sci U S A. 1995;92:11190-4.
131. Sattar N, McConnachie A, O'Reilly D, Upton MN, Greer IA, Davey SG, et al. Inverse association between birth weight and C-reactive protein concentrations in MIDSPAN family study. Arterioscler Thromb Vasc Biol. 2004;24:583-7.
132. Tzoulaki I, Jarvelin MR, Hartikainen AL, Leinonen M, Pouta A, Paldanius M, et al. Size at birth, weight gain over the life course, and low grade inflammation in young adulthood: northern Finland 1966 birth cohort study. Eur Heart J. 2008;29:1049-56.
133. Gillum RF. Association of serum C-reactive protein and indices of bodyfat distribution and overweight in Mexican American children. J Natl Med Assoc. 2003;95:545-52.
134. Lakshmy R, Fall CHD, Sachdev HPS, Osmund C, Prabhakaran D, Biswas SD, et al. Childhood body mass index and adult proinfammatory and prothrombotic risk factors: data from New Delhi Birth cohort. Int J Epidemiol. 2011;40:102-11.
135. Park KS, Kim SK, Kim MS, Cho EY, Lee JH, Lee KU, et al. Fetal and early postnatal protein malnutrition cause long-term changes in rat liver and muscle mitochondria. J Nutr. 2003;133:3085-90.
136. Mortensen OH, Olsen HL, Frandsen L, Nielsen PE, Nielsen FC, Grunnet N, et al. Gestational protein restriction in mice has pronounced effects on gene expression in newborn offspring's liver and skeletal muscle; protective effect of taurine. Pediatr Res. 2010;67:47-53.
137. Mortensen OH, Olsen HL, Frandsen L, Nielsen PE, Nielsen FC, Grunnet N, et al. A maternal low protein diet has pronounced effects on mitochondrial gene expression in offspring liver and skeletal muscle; protective effect of taurine. J Biomed Sci. 2010;17:S38.
138. Lee YY, Park KS, Pak YK, Lee HK. The role of mitochondrial DNA in the development of type 2 diabetes caused by fetal malnutrition. J Nutr Biochem. 2005;16:195-204.
139. Simmons RA, Suponitsky-Kroyter I, Selak MA. Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure. J Biol Chem. 2005;280:28785-91.
140. Lee HK, Cho YM, Kwak SH, Lim S, Park KS, Shim EB. Mitochondrial dysfunction and metabolic syndrome- looking for environmental factors. Biochim Biophys Acta. 2010;1800:282-9.