Nutrition
Volume 23, Issue 9 , Pages 640-646 , September 2007

Body fat distribution in stunted compared with normal-height children from the shantytowns of São Paulo, Brazil

  • Daniel J. Hoffman, Ph.D.

      Affiliations

    • Department of Nutritional Sciences, Rutgers, the State University of New Jersey, New Brunswick, New Jersey, USA
    • Corresponding Author InformationCorresponding author. Tel.: +732-932-6568; fax: +732-932-6522.
  • ,
  • Paula A. Martins, Ph.D.

      Affiliations

    • Department of Endocrine Physiology, Federal University of São Paulo School of Medicine, São Paulo, São Paulo, Brazil
  • ,
  • Susan B. Roberts, Ph.D.

      Affiliations

    • Energy Metabolism Laboratory, Tufts University Friedman School of Nutrition Science and Policy, USDA-HNRCA, Boston, Massachusetts, USA
  • ,
  • Ana Lydia Sawaya, Ph.D.

      Affiliations

    • Department of Endocrine Physiology, Federal University of São Paulo School of Medicine, São Paulo, São Paulo, Brazil

Received 18 January 2007 ,Accepted 5 June 2007.

References 

  1. de Onis M, Monteiro C, Akre J, Glugston G. The worldwide magnitude of protein-energy malnutrition: an overview from the WHO Global Database on Child Growth. Bull World Health Organ. 1993;71:703–712
  2. Stephenson LS, Latham MC, Ottesen EA. Global malnutrition. Parasitology. 2000;121(suppl):S5–S22
  3. Schroeder DG, Martorell R, Flores R. Infant and child growth and fatness and fat distribution in Guatemalan adults. Am J Epidemiol. 1999;149:177–185
  4. Jinabhai CC, Taylor M, Sullivan KR. Changing patterns of under- and over-nutrition in South African children-future risks of non-communicable diseases. Ann Trop Paediatr. 2005;25:3–15
  5. Roseboom TJ, van der Meulen JH, Ravelli AC, Bleker OP. [Link between prenatal exposure to the “Winter of Famine” and long-term medical consequences]. Ned Tijdschr Geneeskd. 2000;144:2488–2491
  6. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Adult survival after prenatal exposure to the Dutch famine 1944–45. Paediatr Perinat Epidemiol. 2001;15:220–225
  7. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart. 2000;84:595–598
  8. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Plasma fibrinogen and factor VII concentrations in adults after prenatal exposure to famine. Br J Haematol. 2000;111:112–117
  9. Roseboom TJ, van der Meulen JH, Ravelli AC, van Montfrans GA, Osmond C, Barker DJ, et al. Blood pressure in adults after prenatal exposure to famine. J Hypertens. 1999;17:325–330
  10. Popkin BM, Richards MK, Montiero CA. Stunting is associated with overweight in children of four nations that are undergoing the nutrition transition. J Nutr. 1996;126:3009–3016
  11. Phillips DI, Young JB. Birth weight, climate at birth and the risk of obesity in adult life. Int J Obes Relat Metab Disord. 2000;24:281–287
  12. Vanhala MJ, Vanhala PT, Keinanen-Kiukaanniemi SM, Kumpusalo EA, Takala JK. Relative weight gain and obesity as a child predict metabolic syndrome as an adult. Int J Obes Relat Metab Disord. 1999;23:656–659
  13. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non–insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36:62–67
  14. Bo S, Cavallo-Perin P, Scaglione L, Ciccone G, Pagano G. Low birthweight and metabolic abnormalities in twins with increased susceptibility to type 2 diabetes mellitus. Diabet Med. 2000;17:365–370
  15. Barker DJ. The fetal origins of hypertension. J Hypertens. 1996;14(suppl):S117–S120
  16. Walker SP, Gaskin PS, Powell CA, Bennett FI. The effects of birth weight and postnatal linear growth retardation on body mass index, fatness and fat distribution in mid and late childhood. Public Health Nutr. 2002;5:391–396
  17. Carr DB, Utzschneider KM, Hull RL, Kodama K, Retzlaff BM, Brunzell JD, et al. Intra-abdominal fat is a major determinant of the National Cholesterol Education Program Adult Treatment Panel III criteria for the metabolic syndrome. Diabetes. 2002;53:2087–2094
  18. Turkoglu C, Duman BS, Gunay D, Cagatay P, Ozcan R, Buyukdevrim AS. Effect of abdominal obesity on insulin resistance and the components of the metabolic syndrome: evidence supporting obesity as the central feature. Obes Surg. 2003;13:699–705
  19. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes. 1997;46:1579–1585
  20. Lamarche B, Lemieux S, Dagenais GR, Despres JP. Visceral obesity and the risk of ischaemic heart disease: insights from the Quebec Cardiovascular Study. Growth Horm IGF Res. 1998;8(suppl B):1–8
  21. Nicklas BJ, Cesari M, Penninx BW, Kritchevsky SB, Ding J, Newman A, et al. Abdominal obesity is an independent risk factor for chronic heart failure in older people. J Am Geriatr Soc. 2006;54:413–420
  22. Hoffman DJ, Sawaya AL, Verreschi I, Tucker KL, Roberts SB. Why are nutritionally stunted children at increased risk of obesity? (Studies of metabolic rate and fat oxidation in shantytown children from Sao Paulo, Brazil). Am J Clin Nutr. 2000;72:702–707
  23. Sawaya AL, Grillo LP, Verreschi I, da Silva AC, Roberts SB. Mild stunting is associated with higher susceptibility to the effects of high fat diets: studies in a shantytown population in Sao Paulo, Brazil. J Nutr. 1998;128:415S–420S
  24. Garnett SP, Cowell CT, Baur LA, Fay RA, Lee J, Coakley J, et al. Abdominal fat and birth size in healthy prepubertal children. Int J Obes Relat Metab Disord. 2001;25:1667–1673
  25. Law CM, Barker DJ, Osmond C, Fall CH, Simmonds SJ. Early growth and abdominal fatness in adult life. J Epidemiol Community Health. 1992;46:184–186
  26. 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;82:980–987
  27. Kensara OA, Wootton SW, Phillips DI, Patel M, Elia M. Does body mass index reflect percentage body fat and body fat distribution in low and high birth weight subjects?. Asia Pac J Clin Nutr. 2004;13:S99
  28. Martins PA, Hoffman DJ, Fernandes MT, Nascimento CR, Roberts SB, Sesso R, et al. Stunted children gain less lean body mass and more fat mass than their non-stunted counterparts: a prospective study. Br J Nutr. 2004;92:819–825
  29. Hoffman DJ, Sawaya AL, Coward WA, Wright A, Martins PA, de Nascimento C, et al. Energy expenditure of stunted and nonstunted boys and girls living in the shantytowns of Sao Paulo, Brazil. Am J Clin Nutr. 2000;72:1025–1031
  30. Bosaeus I, Johannsson G, Rosen T, Hallgren P, Tolli J, Sjostrom L, et al. Comparison of methods to estimate body fat in growth hormone deficient adults. Clin Endocrinol (Oxf). 1996;44:395–402
  31. Wang J, Thornton JC, Horlick M, Formica C, Wang W, Pierson RN. Dual X-Ray absorptiometry in pediatric studies: changing scan modes alters bone and body composition measurements. J Clin Densitom. 1999;2:135–141
  32. Ellis KJ, Shypailo RJ, Pratt JA, Pond WG. Accuracy of DXA-based body composition measurements for pediatric studies. Basic Life Sci. 1993;60:153–156
  33. Ellis KJ, Shypailo RJ, Pratt JA, Pond WG. Accuracy of dual-energy x-ray absorptiometry for body-composition measurements in children. Am J Clin Nutr. 1994;60:660–665
  34. Treuth MS, Butte NF, Wong WW, Ellis KJ. Body composition in prepubertal girls: comparison of six methods. Int J Obes Relat Metab Disord. 2001;25:1352–1359
  35. Sopher AB, Thornton JC, Wang J, Pierson RN, Heymsfield SB, Horlick M. Measurement of percentage of body fat in 411 children and adolescents: a comparison of dual-energy X-ray absorptiometry with a four-compartment model. Pediatrics. 2004;113:1285–1290
  36. Barker DJ. The fetal and infant origins of adult disease. BMJ. 1990;301:1111
  37. Barker DJ. Fetal growth and adult disease. Br J Obstet Gynaecol. 1992;99:275–276
  38. Schroeder DG, Martorell R. Fatness and body mass index from birth to young adulthood in a rural Guatemalan population. Am J Clin Nutr. 1999;70:137S–144S
  39. Okosun IS, Liao Y, Rotimi CN, Dever GE, Cooper RS. Impact of birth weight on ethnic variations in subcutaneous and central adiposity in American children aged 5–11 years (A study from the Third National Health and Nutrition Examination Survey). Int J Obes Relat Metab Disord. 2000;24:479–484
  40. Smith SA. Central role of the adipocyte in the insulin-sensitising and cardiovascular risk modifying actions of the thiazolidinediones. Biochimie. 2003;85:1219–1230
  41. Daniels SR, Morrison JA, Sprecher DL, Khoury P, Kimball TR. Association of body fat distribution and cardiovascular risk factors in children and adolescents. Circulation. 1999;99:541–545
  42. Nielsen S, Guo Z, Johnson CM, Hensrud DD, Jensen MD. Splanchnic lipolysis in human obesity. J Clin Invest. 2004;113:1582–1588
  43. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol. 1999;277:E1130–E1141
  44. Colberg SR, Simoneau JA, Thaete FL, Kelley DE. Skeletal muscle utilization of free fatty acids in women with visceral obesity. J Clin Invest. 1995;95:1846–1853
  45. Simoneau JA, Colberg SR, Thaete FL, Kelley DE. Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J. 1995;9:273–278
  46. Kensara OA, Wooton SA, Phillips DI, Patel M, Hoffman DJ, Jackson AA, et al. Substrate-energy metabolism and metabolic risk factors for cardiovascular disease in relation to fetal growth and adult body composition. Am J Physiol Endocrinol Metab. 2006;291:E365–E371
  47. Boule NG, Tremblay A, Gonzalez-Barranco J, Aguilar-Salinas CA, Lopez-Alvarenga JC, Despres JP, et al. Insulin resistance and abdominal adiposity in young men with documented malnutrition during the first year of life. Int J Obes Relat Metab Disord. 2003;27:598–604
  48. Phillips DI, Walker BR, Reynolds RM, Flanagan DE, Wood PJ, Osmond C, et al. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension. 2000;35:1301–1306
  49. Kajantie E, Eriksson J, Barker DJ, Forsen T, Osmond C, Wood PJ, et al. Birthsize, gestational age and adrenal function in adult life: studies of dexamethasone suppression and ACTH1-24 stimulation. Eur J Endocrinol. 2003;149:569–575
  50. Kajantie E, Phillips DI, Andersson S, Barker DJ, Dunkel L, Forsen T, et al. Size at birth, gestational age and cortisol secretion in adult life: foetal programming of both hyper- and hypocortisolism?. Clin Endocrinol (Oxf). 2002;57:635–641
  51. Drapeau V, Therrien F, Richard D, Tremblay A. Is visceral obesity a physiological adaptation to stress?. Panminerva Med. 2003;45:189–195
  52. Wallerius S, Rosmond R, Ljung T, Holm G, Bjorntorp P. Rise in morning saliva cortisol is associated with abdominal obesity in men: a preliminary report. J Endocrinol Invest. 2003;26:616–619
  53. Bjorntorp P. Do stress reactions cause abdominal obesity and comorbidities?. Obes Rev. 2001;2:73–86
  54. Pedersen SB, Jonler M, Richelsen B. Characterization of regional and gender differences in glucocorticoid receptors and lipoprotein lipase activity in human adipose tissue. J Clin Endocrinol Metab. 1994;78:1354–1359
  55. Richard D, Chapdelaine S, Deshaies Y, Pepin MC, Barden N. Energy balance and lipid metabolism in transgenic mice bearing an antisense GCR gene construct. Am J Physiol. 1993;265:R146–R150
  56. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, et al. A transgenic model of visceral obesity and the metabolic syndrome. Science. 2001;294:2166–2170
  57. Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, Phillips DI. Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab. 2006;91:1868–1871
  58. Reynolds RM, Walker BR, Syddall HE, Andrew R, Wood PJ, Phillips DI. Is there a gender difference in the associations of birthweight and adult hypothalamic-pituitary-adrenal axis activity?. Eur J Endocrinol. 2005;152:249–253
  59. Reynolds RM, Walker BR, Syddall HE, Andrew R, Wood PJ, Whorwood CB, et al. Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors. J Clin Endocrinol Metab. 2001;86:245–250

 Financial support for various aspects of the work was received from the Nestle International Foundation and the International Atomic Energy Agency.

PII: S0899-9007(07)00183-9

doi: 10.1016/j.nut.2007.06.006

Nutrition
Volume 23, Issue 9 , Pages 640-646 , September 2007