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Published in: Reviews in Endocrine and Metabolic Disorders 3/2013

01-09-2013

Metabolic syndrome: Role of maternal undernutrition and fetal programming

Author: Ramakrishnan Lakshmy

Published in: Reviews in Endocrine and Metabolic Disorders | Issue 3/2013

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Abstract

Development of metabolic syndrome is attributed to genes, dietary intake, physical activity and environmental factors. Fetal programming due to maternal nutrition is also an important factor especially in developing countries where intrauterine growth retardation followed by excess nutrition postnatally is causing mismatch predisposing individuals to development of metabolic syndrome and its components. Several epidemiological and animal studies have provided evidence for the link between intrauterine growth retardation and adult metabolic diseases. Deficiency of macronutrients, protein and carbohydrates, during pregnancy and gestation results in lower infant birth weight, a surrogate marker of fetal growth and subsequently insulin resistance, glucose intolerance, hypertension and adiposity in adulthood. The role of micronutrients is less extensively studied but however gaining attention with several recent studies focusing on this aspect. Several mechanisms have been proposed to explain the developmental origin of adult diseases important among them being alteration of hypothalamic pituitary axis, epigenetic regulation of gene expression and oxidative stress. All of these mechanisms may be acting at different time during gestation and contributing to development of metabolic syndrome in adulthood.
Literature
1.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
2.
go back to reference 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.CrossRef 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.CrossRef
3.
go back to reference 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.CrossRef 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.CrossRef
4.
go back to reference World Health Organization. Obesity and overweight. Fact Sheet N0311. Geneva: World Health Organization; 2006. World Health Organization. Obesity and overweight. Fact Sheet N0311. Geneva: World Health Organization; 2006.
6.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference 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.PubMed 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.PubMed
8.
go back to reference Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71:1344S–52.PubMed Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71:1344S–52.PubMed
9.
go back to reference Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185:73–9.PubMedCrossRef Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185:73–9.PubMedCrossRef
10.
go back to reference UNICEF and WHO. Low birthweight: country, regional and global estimates. UNICEF; 2004. pgs 27. UNICEF and WHO. Low birthweight: country, regional and global estimates. UNICEF; 2004. pgs 27.
11.
go back to reference Jain V, Singhal A. Catchup growth in low birth weight infants: striking a healthy balance. Rev Endocr Metab Disord. 2012;13:141–7.PubMedCrossRef Jain V, Singhal A. Catchup growth in low birth weight infants: striking a healthy balance. Rev Endocr Metab Disord. 2012;13:141–7.PubMedCrossRef
12.
go back to reference Gluckman PD, Hanson MA. Developmental origins of diseases paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004;56:311–7.PubMedCrossRef Gluckman PD, Hanson MA. Developmental origins of diseases paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004;56:311–7.PubMedCrossRef
13.
go back to reference Gluckman PD, Hanson MA, Beedle AS, Spencer HG. Predictive adaptive responses in perspective. Trends Endocrinol Metab. 2008;19:109–10.PubMedCrossRef Gluckman PD, Hanson MA, Beedle AS, Spencer HG. Predictive adaptive responses in perspective. Trends Endocrinol Metab. 2008;19:109–10.PubMedCrossRef
14.
go back to reference Barker DJ, Osmond C. Low birth weight and hypertension. Br Med J. 1988;297:134–5.CrossRef Barker DJ, Osmond C. Low birth weight and hypertension. Br Med J. 1988;297:134–5.CrossRef
15.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
16.
go back to reference 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.PubMed 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.PubMed
17.
go back to reference 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.CrossRef 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.CrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
20.
go back to reference 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.CrossRef 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.CrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference Patti ME. Intergenerational programming of metabolic diseases: evidence from human populations and experimental animal models. Cell Mol Life Sci. 2013;70:1597–608.PubMedCrossRef Patti ME. Intergenerational programming of metabolic diseases: evidence from human populations and experimental animal models. Cell Mol Life Sci. 2013;70:1597–608.PubMedCrossRef
23.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
24.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
26.
go back to reference 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.CrossRef 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.CrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference Phillips DJ, Barker DJ, Hales CN, Hirst S, Osmund C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994;37:150–4.PubMedCrossRef Phillips DJ, Barker DJ, Hales CN, Hirst S, Osmund C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994;37:150–4.PubMedCrossRef
31.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
32.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
33.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
34.
go back to reference 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. 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.
go back to reference 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.PubMed 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.PubMed
36.
go back to reference 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.CrossRef 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.CrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.CrossRef 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.CrossRef
39.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
40.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
41.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
43.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
44.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
46.
go back to reference 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.PubMed 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.PubMed
47.
go back to reference Brown LD, Green AS, Limesand SW, Rozance PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci. 2011;1:428–44.CrossRef Brown LD, Green AS, Limesand SW, Rozance PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci. 2011;1:428–44.CrossRef
48.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
49.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
51.
go back to reference 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.PubMed 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.PubMed
52.
go back to reference Simmons RA, Templeton LJ, Gertz SI. Intrauterine growth retardation leads to development of type 2 diabetes in rat. Diabetes. 2001;50:2279–86.PubMedCrossRef Simmons RA, Templeton LJ, Gertz SI. Intrauterine growth retardation leads to development of type 2 diabetes in rat. Diabetes. 2001;50:2279–86.PubMedCrossRef
53.
go back to reference 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.PubMed 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.PubMed
54.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
55.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
56.
go back to reference 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.PubMed 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.PubMed
57.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
58.
go back to reference Roseboom T, de Rooji S, Painter RC. The Dutch famine and its long consequences for adult health. Early Hum Dev. 2006;82:485–91.PubMedCrossRef Roseboom T, de Rooji S, Painter RC. The Dutch famine and its long consequences for adult health. Early Hum Dev. 2006;82:485–91.PubMedCrossRef
59.
go back to reference 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.CrossRef 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.CrossRef
60.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
61.
go back to reference 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.CrossRef 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.CrossRef
62.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
63.
go back to reference 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.PubMed 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.PubMed
64.
go back to reference 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 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
66.
go back to reference 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.CrossRef 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.CrossRef
67.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
68.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
69.
go back to reference 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.PubMed 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.PubMed
70.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
71.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
72.
go back to reference 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.PubMed 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.PubMed
73.
go back to reference 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.PubMed 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.PubMed
74.
go back to reference 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.CrossRef 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.CrossRef
75.
go back to reference 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.PubMed 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.PubMed
76.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
78.
go back to reference Christian P, Stewart CP. Maternal micronutrient deficiency, fetal development and risk of chronic disease. J Nutr. 2010;140:437–45.PubMedCrossRef Christian P, Stewart CP. Maternal micronutrient deficiency, fetal development and risk of chronic disease. J Nutr. 2010;140:437–45.PubMedCrossRef
79.
go back to reference Bourque SL, Komolova M, Nakatsu K, Adams MA. Perinatal iron deficiency and blood pressure. Hypertension. 2008;51:154–9.PubMedCrossRef Bourque SL, Komolova M, Nakatsu K, Adams MA. Perinatal iron deficiency and blood pressure. Hypertension. 2008;51:154–9.PubMedCrossRef
80.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
81.
go back to reference 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.CrossRef 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.CrossRef
82.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
83.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
84.
go back to reference Cefalu WT, Hu FB. Role of chromium in human health and in diabetes. Diabetes Care. 2004;27:2741–51.PubMedCrossRef Cefalu WT, Hu FB. Role of chromium in human health and in diabetes. Diabetes Care. 2004;27:2741–51.PubMedCrossRef
85.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
86.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
87.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
88.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
89.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
90.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
91.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
92.
go back to reference Lapillonne A. Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Med Hypotheses. 2010;74:71–5.PubMedCrossRef Lapillonne A. Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Med Hypotheses. 2010;74:71–5.PubMedCrossRef
93.
go back to reference Merlet-Benichou C. Influence of fetal environment on kidney development. Int J Dev Biol. 1999;43:453–6.PubMed Merlet-Benichou C. Influence of fetal environment on kidney development. Int J Dev Biol. 1999;43:453–6.PubMed
94.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
95.
go back to reference 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.PubMed 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.PubMed
96.
go back to reference 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 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.
go back to reference 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.PubMed 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.PubMed
98.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
99.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
100.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
101.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
103.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
104.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
105.
go back to reference Hales CN, Barker DJP. Type 2 diabetes: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601.PubMedCrossRef Hales CN, Barker DJP. Type 2 diabetes: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595–601.PubMedCrossRef
106.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
107.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
108.
go back to reference Giabfarani S, Germani D, Branca F. Low birthweight and adult insulin resistance: the catchup growth hypothesis. Arch Dis Childhood. 1999;81:171–3. Giabfarani S, Germani D, Branca F. Low birthweight and adult insulin resistance: the catchup growth hypothesis. Arch Dis Childhood. 1999;81:171–3.
109.
go back to reference 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.CrossRef 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.CrossRef
110.
go back to reference Willcox JK, Ash SL, Gatignani L. Antioxidants and prevention of chronic diseases. Crit Rev Food Sci Nutr. 2004;44:275–95.PubMedCrossRef Willcox JK, Ash SL, Gatignani L. Antioxidants and prevention of chronic diseases. Crit Rev Food Sci Nutr. 2004;44:275–95.PubMedCrossRef
111.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
112.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
113.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
114.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
115.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
116.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
117.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
118.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
119.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
120.
go back to reference Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005;146:4211–6.PubMedCrossRef Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005;146:4211–6.PubMedCrossRef
121.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
122.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
123.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
124.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
125.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
126.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
127.
go back to reference 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.PubMed 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.PubMed
128.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
130.
go back to reference 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.CrossRef 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.CrossRef
131.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
132.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
133.
go back to reference 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.PubMed 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.PubMed
134.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
135.
go back to reference 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.PubMed 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.PubMed
136.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
137.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
138.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
139.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
140.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Metabolic syndrome: Role of maternal undernutrition and fetal programming
Author
Ramakrishnan Lakshmy
Publication date
01-09-2013
Publisher
Springer US
Published in
Reviews in Endocrine and Metabolic Disorders / Issue 3/2013
Print ISSN: 1389-9155
Electronic ISSN: 1573-2606
DOI
https://doi.org/10.1007/s11154-013-9266-4

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