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Evidence for fetal programming of obesity with a focus on putative mechanisms

Published online by Cambridge University Press:  14 December 2007

Sarah H. Wild  and
Christopher D. Byrne
Sarah H. Wild
Affiliation:
Public Health Sciences, University of Edinburgh, Teviot Place, Edinburgh, EH8 9AG, UK
Christopher D. Byrne*
Affiliation:
University of Southampton School of Medicine, Developmental Origins of Health and Disease Division, Level F, Centre Block, MP113, Southampton General Hospital, Southampton SO16 6YD, UK
*
*Corresponding author: Professor Christopher D. Byrne, fax +44 2380 794945, email C.D.Byrne@soton.ac.uk
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Abstract

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Obesity is associated with insulin resistance, the metabolic syndrome (a clustering of three or more of increased waist circumference, blood pressure, fasting glucose and fasting plasma triacylglycerol levels and reduced HDL levels), and a marked increase in the risk of type 2 diabetes and CHD. The impact of obesity differs between individuals, particularly between men and women and between ethnic groups. For example, in South Asians, although overall obesity is less prevalent, central obesity and the metabolic syndrome are more prevalent than in Europeans and this pattern is associated with the development of type 2 diabetes and CHD at an earlier age. It is important to examine individual risk factors contributing to obesity because they may have a different impact in population subgroups. Many factors contribute to the aetiology of obesity and there is increasing evidence to suggest that altered early development is one such factor and is associated with abnormal fat accumulation, the metabolic syndrome and type 2 diabetes in later life. The present review presents this evidence and discusses some of the mechanisms that may be involved in the pathogenesis of the programming of obesity.

Keywords

Fetal programmingDiabetes mellitusObesityMetabolic syndromeCoronary heart disease
Type
research-article
Information
Nutrition Research Reviews , Volume 17 , Issue 2 , December 2004 , pp. 153 - 162
Copyright
Copyright © The Authors 2004

References

Anand, SSOunpuu, S & Yusuf, S (2003) Ethnicity and cardiovascular disease. In Evidence-Based Cardiology, vol. II, 2nd ed., pp. 171–190 [S Yusuf, JA Cairns, AJ Camm EL Fallen and BJ Gersh editors]. London: BMJ Publishing Group.Google Scholar
Barker, DJ (2002) Foetal programming of coronary heart disease. Trends in Endocrinology and Metabolism 13, 364–368.CrossRefGoogle ScholarPubMed
Breier, BH, Vickers, MH, Ikenasio, BA, Chan, KY, & Wong, WPS (2001) Foetal programming of appetite and obesity. Molecular and Cellular Endocrinology 185, 73–79.CrossRefGoogle ScholarPubMed
Brochu, M, Tchernof, A, Dionne, IJ, Sites, CK, Eltabbakh, GH, Sims, EAH, & Poehlman, ET (2001) What are the physical characteristics associated with a normal metabolic profile despite a high level of obesity in postmenopausal women? Journal of Clinical Endocrinology and Metabolism 86, 1020–1025.Google ScholarPubMed
Byrne, CD & Phillips, DI (2000) Fetal origins of adult disease: epidemiology and mechanisms. Journal of Clinical Pathology 53, 822–828.CrossRefGoogle ScholarPubMed
Chan, JM, Rimm, EB, Colditz, GA, Stampfer, MJ & Willett, WC (1994) Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 17, 961–969.CrossRefGoogle ScholarPubMed
Després, JP, Lemieux, I & Prud’homme, D (2001) Treatment of obesity: need to focus on high risk abdominally obese patients. British Medical Journal 322, 716–720.CrossRefGoogle ScholarPubMed
Deurenberg, P, Deurenberg-Yap, M & Guricci, S (2002) Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obesity Reviews 3, 141–146.CrossRefGoogle ScholarPubMed
Deurenberg, P, van der Kooy, K, Hulshof, T & Evers, P (1989) Body mass index as a measure of body fatness in the elderly. European Journal of Clinical Nutrition 43, 231–236.Google ScholarPubMed
Dudeja, V, Misra, A, Pandey, RM, Devina, G, Kumar, G & Vikram, NK (2001) BMI does not accurately predict overweight in Asian Indians in northern India. British Journal of Nutrition 86, 105–112.CrossRefGoogle Scholar
Ekert, JE, Gatford, KL, Luxford, BG, Campbell, RG & Owens, PC (2000) Leptin expression in offspring is programmed by nutrition in pregnancy. Journal of Endocrinology 165, R1–R6.CrossRefGoogle Scholar
Elia, M (2001) Obesity in the elderly. Obesity Research 9, Suppl. 4, 244S–248S.CrossRefGoogle ScholarPubMed
Enns, MP, Wilson, MW, Grinker, JA, Faust, IM, Jones, AP & Friedman, MI (1983) Prenatal food restriction and subsequent weight gain in male rats. Science 219, 1093–1094.CrossRefGoogle ScholarPubMed
Eriksson, JG, Forsén, T, Tuomilehto, J, Jaddoe, VW, Osmond, C & Barker, DJ (2002) Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 45, 342–348.CrossRefGoogle ScholarPubMed
Eriksson, JG, Forsén, T, Tuomilehto, J, Osmond, C & Barker, D (2001) Size at birth, childhood growth and obesity in later life. International Journal of Obesity and Related Metabolic Disorders 25, 735–740.CrossRefGoogle Scholar
Fernandez, JR, Heo, M, Heymsfield, SB, Pierson, RN, Pi-Sunyer, FX, Wang, ZM, Wang, J, Hayes, M, Allison, DB & Gallagher, D (2003) Is percentage body fat differentially related to body mass index in Hispanic Americans, African Americans, and European Americans? American Journal of Clinical Nutrition 77, 71–75.CrossRefGoogle ScholarPubMed
Forsen, T, Eriksson, J, Tuomilehto, J, Reunanen, A, Osmond, C & Barker, D (2000) The foetal and childhood growth of persons who develop type 2 diabetes. Annals of Internal Medicine 133, 176–182.CrossRefGoogle ScholarPubMed
Frayling, TM & Hattersley, AT (2001) The role of genetic susceptibility in the association of low birth weight with type 2 diabetes. British Medical Bulletin 60, 89–101.CrossRefGoogle ScholarPubMed
Gallagher, D, Visser, M, Sepulveda, D, Pierson, RN, Harris, T & Heymsfield, SB (1996) How useful is body mass index for comparison of body fatness across age, sex, and ethnic groups? American Journal of Epidemiology 143, 228–239.CrossRefGoogle ScholarPubMed
Gluckman, PD (1997) Endocrine and nutritional regulation of prenatal growth. Acta Paediatrica 423, Suppl., 153–157.CrossRefGoogle ScholarPubMed
Gluckman, PD & Harding, JE (1997) Foetal growth retardation: underlying endocrine mechanisms and postnatal consequences. Acta Paediatrica 422, Suppl., 69–72.CrossRefGoogle ScholarPubMed
Hales, CN & Barker, DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.CrossRefGoogle ScholarPubMed
Hales, CN, Barker, DJ, Clark, PM, Cox, LJ, Fall, C, Osmond, C & Winter, PD (1991) Foetal and infant growth and impaired glucose tolerance at age 64. British Medical Journal 303, 1019–1022.CrossRefGoogle ScholarPubMed
Han, TS, van Leer, EM, Seidell, JC & Lean, MEJ (1995) Waist circumference action levels in the identification of cardiovascular risk factors: prevalence study in a random sample. British Medical Journal 311, 1401–1405.CrossRefGoogle ScholarPubMed
Hattersley, AT, Beards, F, Ballantyne, E, Appleton, M, Harvey, R & Ellard, S (1998) Mutations in the glucokinase gene of the fetus result in reduced birth weight. Nature Genetics 19, 268–270.CrossRefGoogle ScholarPubMed
Hattersley, AT & Tooke, JE (1999) The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 353, 1789–1792.CrossRefGoogle ScholarPubMed
Holt, RIG & Byrne, CD (2002) Intrauterine growth, the vascular system and the metabolic syndrome. Seminars in Vascular Medicine 2, 33–44.CrossRefGoogle ScholarPubMed
Hu, FB, Manson, JE, Stampfer, MJ, Colditz, G, Liu, S, Solomon, CG & Willett, WC (2001) Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. New England Journal of Medicine 345, 790–797.CrossRefGoogle ScholarPubMed
Huxley, R (2002) Commentary: modifying body weight not birthweight is the key to lowering blood pressure. International Journal of Epidemiology 31, 1051–1053.CrossRefGoogle Scholar
Janssen, I, Katzmarzyk, PT & Ross, R (2002) Body mass index, waist circumference, and health risk: evidence in support of current national institutes of health guidelines. Archives of Internal Medicine 162, 2074–2079.CrossRefGoogle ScholarPubMed
Jones, AP, Assimon, SA & Friedman, MI (1986) The effect of diet on food intake and adiposity in rats made obese by gestational undernutrition. Physiology and Behavior 37, 381–386.CrossRefGoogle ScholarPubMed
Jones, AP & Dayries, M (1990) Maternal hormone manipulations and the development of obesity in rats. Physiology and Behavior 47, 1107–1110.CrossRefGoogle ScholarPubMed
Jones, AP & Friedman, MI (1982) Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science 215, 1518–1519.CrossRefGoogle ScholarPubMed
Jones, AP, Simson, EL & Friedman, MI (1984) Gestational undernutrition and the development of obesity in rats. Journal of Nutrition 114, 1484–1492.Google ScholarPubMed
Kwong, WY, Wild, AE, Roberts, P, Willis, AC & Fleming, TP (2000) Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127, 4195–4202.CrossRefGoogle ScholarPubMed
Lamon-Fava, S, Wilson, PW & Schaefer, EJ (1996) Impact of body mass index on coronary heart disease risk factors in men and women. The Framingham Offspring Study. Arteriosclerosis, Thrombosis, and Vascular Biology 16, 1509–1515.CrossRefGoogle ScholarPubMed
Law, MR & Wald, NJ (2002) Risk factor thresholds: their existence under scrutiny. British Medical Journal 324, 1570–1576.CrossRefGoogle ScholarPubMed
Lean, MEJ, Han, TS & Morrison, CE (1995) Waist circumference as a measure for indicating need for weight management. British Medical Journal 311, 158–161.CrossRefGoogle ScholarPubMed
Li, H, Stein, AD, Barnhart, HX, Ramakrishnan, U & Martorell, R (2003) Associations between prenatal and postnatal growth and adult body size and composition. American Journal of Clinical Nutrition 77, 1498–1505.CrossRefGoogle ScholarPubMed
Lissner, L, Karlsson, C, Lindroos, AK, Carlsson, B, Carlsson, L & Bengtsson, C (1999) Birth weight, adulthood BMI, and subsequent weight gain in relation to leptin levels in Swedish women. Obesity Research 7, 150–154.CrossRefGoogle ScholarPubMed
Lithell, HO, McKeigue, PM, Berglund, L, Mohsen, R, Lithell, UB & Leon, DA (1996) Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50–60 years. British Medical Journal 312, 406–410.CrossRefGoogle ScholarPubMed
Lumey, LH & Stein, AD (1997) Offspring birth weights after maternal intrauterine undernutrition: a comparison within sibships. American Journal of Epidemiology 146, 810–819.CrossRefGoogle ScholarPubMed
Martin, ML & Jensen, MD (1991) Effects of body fat distribution on regional lipolysis in obesity. Journal of Clinical Investigation 88, 609–613.CrossRefGoogle ScholarPubMed
Molarius, A, Seidell, JC, Sans, S, Tuomilehto, J & Kuulasmaa, K (1999) Waist and hip circumferences, and waist-hip ratio in 19 populations of the WHO MONICA Project. International Journal of Obesity and Related Metabolic Disorders 23, 116–125.CrossRefGoogle Scholar
Ong, KKL, Ahmed, ML, Sherriff, A, Woods, KA, Watts, A, Golding, J & Dunger, DB (1999) Cord blood leptin is associated with size at birth and predicts infancy weight gain in humans. Journal of Clinical Endocrinology and Metabolism 84, 1145–1148.CrossRefGoogle ScholarPubMed
Ozanne, SE, Lewis, R, Jennings, BJ & Hales, CN (2003) Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clinical Science (London) 106, 141–145.CrossRefGoogle Scholar
Peeters, A, Barendregt, JJ, Willekens, F, Mackenbach, JP, Al Mamun, A & Bonneux, L (2003) Obesity in adulthood and its consequences for life expectancy: a life-table analysis. Annals of Internal Medicine 7, 24–32.CrossRefGoogle Scholar
Phillips, DIW, Fall, CHD, Cooper, C, Norman, RJ, Robinson, JS & Owens, PC (1999) Size at birth and plasma leptin concentrations in adult life. International Journal of Obesity 23, 1025–1029.CrossRefGoogle ScholarPubMed
Plagemann, A, Harder, T, Rake, A, Voits, M, Fink, H, Rohde, W & Dorner, G (1999) Perinatal elevation of hypothalamic insulin, acquired malformation of hypothalamic galaninergic neurons, and syndrome X-like alterations in adulthood of neonatally overfed rats. Brain Research 836, 146–155.CrossRefGoogle ScholarPubMed
Power, C & Parsons, T (2000) Nutritional and other influences in childhood as predictors of adult obesity. Proceedings of the Nutrition Society 59, 267–272.CrossRefGoogle ScholarPubMed
Pyorala, M, Miettinen, H, Halonen, P, Laakso, M & Pyorala, K (2000) Insulin resistance syndrome predicts the risk of coronary heart disease and stroke in healthy middle-aged men: the 22-year follow-up results of the Helsinki Policemen Study. Arteriosclerosis, Thrombosis, and Vascular Biology 20, 538–544.CrossRefGoogle ScholarPubMed
Rankinen, T, Kim, SY, Perusse, L, Despres, JP & Bouchard, C (1999) The prediction of abdominal visceral fat level from body composition and anthropometry: ROC analysis. International Journal of Obesity and Related Metabolic Disorders 23, 801–809.CrossRefGoogle ScholarPubMed
Ravussin, E & Bogardus, C (2000) Energy balance and weight regulation. British Journal of Nutrition 83, Suppl. 1, S17–S20CrossRefGoogle ScholarPubMed
Rich-Edwards, JW, Colditz, GA, Stampfer, MJ, Willett, WC, Gillman, MW, Hennekens, CH, Speizer, FE & Manson, JE (1999) Birthweight and the risk for type 2 diabetes mellitus in adult women. Annals of Internal Medicine 130, 278–284.CrossRefGoogle ScholarPubMed
Rimm, EB, Stampfer, MJ, Giovannucci, E, Ascherio, A, Spiegelman, D, Colditz, GA & Willett, WC (1995) Body size and fat distribution as predictors of coronary heart disease among middle-aged and older US men. American Journal of Epidemiology 141, 1117–1127.CrossRefGoogle ScholarPubMed
Rogers, I (2003) The influence of birthweight and intrauterine environment on adiposity and fat distribution in later life. International Journal of Obesity and Related Metabolic Disorders 27, 755–777.CrossRefGoogle ScholarPubMed
Rolland-Cachera, M-F, Deheeger, M, Bellisle, F, Sempe, M, Guilloud-Bataille, M & Patois, E (1984) Adiposity rebound in children: a simple indicator for predicting obesity. American Journal of Clinical Nutrition 39, 129–135.CrossRefGoogle ScholarPubMed
Singhal, A, Wells, J, Cole, TJ, Fewtrell, M & Lucas, A (2003) Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease? American Journal of Clinical Nutrition 77, 726–730.CrossRefGoogle Scholar
Stein, AD, Ravelli, AC & Lumey, LH (1995) Famine, third-trimester pregnancy weight gain, and intrauterine growth: the Dutch Famine Birth Cohort Study. Human Biology 67, 135–150.Google ScholarPubMed
Toth, MJ, Sites, CK, Eltabbakh, GH & Poehlman, ET (2000) Effect of menopausal status on insulin-stimulated glucose disposal: comparison of middle-aged premenopausal and early postmenopausal women. Diabetes Care 23, 801–806.CrossRefGoogle ScholarPubMed
Valdez, R, Athens, MA, Thompson, GH, Bradshaw, BS & Stern, MP (1994) Birthweight and adult health outcomes in a biethnic population in the USA. Diabetologia 37, 624–631.CrossRefGoogle Scholar
Vickers, MH, Breier, BH, Cutfield, WS, Hofman, PL & Gluckman, PD (2000) Foetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. American Journal of Physiology 279, E83–E87.Google ScholarPubMed
Vickers, MH, Breier, BH, McCarthy, D & Gluckman, PD (2003) Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. American Journal of Physiology 285, R271–R273.Google ScholarPubMed
von Eckardstein, A, Schulte, H & Assmann, G (2000) Risk for diabetes mellitus in middle-aged Caucasian male participants of the PROCAM Study: implications for the definition of impaired fasting glucose by the American Diabetes Association. Journal of Clinical Endocrinology and Metabolism 85, 3101–3108.CrossRefGoogle ScholarPubMed
West-Eberhard, MJ (1989) Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20, 249–278.CrossRefGoogle Scholar
West-Eberhard, MJ (1998) Evolution in the light of developmental and cell biology, and vice versa. Proceedings of the National Academy of Science USA 95, 8417–8419.CrossRefGoogle ScholarPubMed
World Health Organization (1997) Obesity: Preventing and Managing the Global Epidemic–Report of a WHO Consultation on Obesity. Geneva: WHO.Google Scholar
World Health Organization (2002) Quantifying selected major risks to health. In World Health Report: Reducing Risks, Promoting Healthy Life. chapter 4. Geneva: WHO.Google Scholar
Yajnik, CS, Lubree, HG, Rege, SS, Naik, SS, Deshpande, JA, Deshpande, JA, Joglekar, CV & Yudkin, JS (2002) Adiposity and hyperinsulinemia in Indians are present at birth. Journal of Clinical Endocrinology and Metabolism 87, 5575–5580.CrossRefGoogle ScholarPubMed
Zhao, M, Shu, XO, Jin, F, Yang, G, Li, H, Liu, D, Wen, W, Gao, Y & Zheng, W (2002) Birthweight, childhood growth and hypertension in adulthood. International Journal of Epidemiology 31, 1043–1051.CrossRefGoogle ScholarPubMed