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Clinical Studies and Practice

Association of nutrition in early life with body fat and serum leptin at adult age

International Journal of Obesity volume 37, pages 1116–1122 (2013)Cite this article

Subjects

Abstract

Background:

There is overwhelming evidence that experiences during early life could have long-term health consequences. However, the role of early nutrition in programming obesity and leptin resistance is still poorly understood.

Objective:

We aimed at determining whether nutritional intakes in early life are associated with body composition and hormonal status at 20 years.

Subjects:

Healthy infants participating in the two-decade-long prospective ELANCE (Etude Longitudinale Alimentation Nutrition Croissance des Enfants) study were examined at 10 months and 2 years. At 20 years, weight, height, subscapular and triceps skinfold thicknesses, fat mass (FM) and fat-free mass (FFM) assessed via bioelectrical impedance analysis, and serum leptin concentration were recorded in 73 subjects still participating in the follow-up.

Results:

In adjusted linear regression models, an increase by 100 kcal in energy intake at 2 years was associated with higher subscapular skinfold thickness (β=6.4% SF, 95% confidence interval 2.53–10.30, P=0.002) and higher FFM (0.50 kg, 0.06–0.95, P=0.03) at 20 years. An increase by 1% energy from fat at 2 years was associated with lower subscapular skinfold thickness (−2.3% SF, −4.41 to −0.18, P=0.03), lower FM (−0.31 kg, −0.60 to −0.01, P=0.04) and lower serum leptin concentration (−0.21 μg l−1, −0.39 to −0.03, P=0.02) at 20 years.

Conclusions:

Low-fat intake in early life was negatively associated with body fat (particularly at the trunk site) and serum leptin concentration at 20 years, suggesting that early low-fat intake could increase the susceptibility to develop overweight and leptin resistance at later ages. These findings substantiate current recommendations against restricting fat intake in early life and open new directions for investigating the origin of obesity.

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References

  1. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ . Weight in infancy and death from ischaemic heart disease. Lancet 1989; 2: 577–580.

    Article  CAS  Google Scholar 

  2. Singhal A, Cole TJ, Fewtrell M, Deanfield J, Lucas A . Is slower early growth beneficial for long-term cardiovascular health? Circulation 2004; 109: 1108–1113.

    Article  Google Scholar 

  3. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L et al Maternal and Child Undernutrition Study Group. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371: 357.

    Article  Google Scholar 

  4. Cianfarani S, Agostoni C, Bedogni G, Berni Canani R, Brambilla P, Nobili V et al. Effect of intrauterine growth retardation on liver and long-term metabolic risk. Int J Obes (Lond) 2012; 36: 1270–1277.

    Article  CAS  Google Scholar 

  5. Rolland-Cachera MF, Deheeger M, Bellisle F, Sempé M, Guilloud-Bataille M, Patois E . Adiposity rebound in children: a simple indicator for predicting obesity. Am J Clin Nutr 1984; 39: 129–135.

    Article  CAS  Google Scholar 

  6. Lucas A . Programming by early nutrition in man. In: Bock GR, Whelan J, (eds) The Childhood Environment and Adult Diseases. CIBA Foundation Symposium 156. Whiley: Chichester, UK, 1991. pp 38–55.

    Google Scholar 

  7. Gillman MW, Rifas-Shiman SL, Camargo CA, Berkey CS, Frazier AL, Rockett HR et al. Risk of overweight among adolescents who were breastfed as infants. JAMA 2001; 285: 2461–2467.

    Article  CAS  Google Scholar 

  8. Parsons TJ, Power C, Logan S, Summerbell CD . Childhood predictors of adult obesity: a systematic review. Int J Obes Relat Metab Disord 1999; 23 (Suppl 8): S1–S107.

    Google Scholar 

  9. Macé K, Shahkhalili Y, Aprikian O, Stan S . Dietary fat and fat types as early determinants of childhood obesity: a reappraisal. Int J Obes (Lond) 2006; 30 (Suppl 4): S50–S57.

    Article  Google Scholar 

  10. Butte NF . Impact of infant feeding practices on childhood obesity. J Nutr 2009; 139: 412S–416S.

    Article  CAS  Google Scholar 

  11. Troiano RP, Briefel RR, Carroll MD, Bialostosky K . Energy and fat intakes of children and adolescents in the United States: data from the national health and nutrition examination surveys. Am J Clin Nutr 2000; 72 (Suppl 5): S1343–S1353.

    Article  Google Scholar 

  12. Gibson S . Trends in energy and sugar intakes and body mass index between 1983 and 1997 among children in Great Britain. J Hum Nutr Diet 2010; 23: 371–381.

    Article  CAS  Google Scholar 

  13. Rolland-Cachera MF, Deheeger M, Bellisle F . Increasing prevalence of obesity among 18-year-old males in Sweden: evidence for early determinants. Acta Paediatr 1999; 88: 365–367.

    Article  CAS  Google Scholar 

  14. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996; 334: 292–295.

    Article  CAS  Google Scholar 

  15. Hanley B, Dijane J, Fewtrell M, Grynberg A, Hummel S, Junien C et al. Metabolic imprinting, programming and epigenetics—a review of present priorities and future opportunities. Br J Nutr 2010; 104 (Suppl 1): S1–25.

    Article  CAS  Google Scholar 

  16. Rolland-Cachera MF, Deheeger M, Akrout M, Bellisle F . Influence of macronutrients on adiposity development: a follow up study of nutrition and growth from 10 months to 8 years of age. Int J Obes Relat Metab Disord 1995; 19: 573–578.

    CAS  Google Scholar 

  17. Lohman TG, Roche AF, Martorell R . Anthropometric Standardization. Reference Manual. Human Kinetics Books: Champaign, Illinois, 1988.

    Google Scholar 

  18. Cole TJ . Sympercents: symmetric percentage differences on the 100 log(e) scale simplify the presentation of log transformed data. Stat Med 2000; 19: 3109–3125.

    Article  CAS  Google Scholar 

  19. Willett W, Stampfer M . Implications of total energy intake for epidemiologic analyses. In: Willett W, (ed) Nutritional Epidemiology. 2nd edn Oxford University Press: New York, NY, 1998. pp 273–301.

    Chapter  Google Scholar 

  20. Report of the 33rd Session of the Standing Committee of nutrition participant’s statement. The window of opportunity: pre-pregnancy to 24 months of age. WHO: Geneva, USA; 13–17 March 2006.

  21. Rolland-Cachera MF, Deheeger M, Maillot M, Bellisle F . Early adiposity rebound: causes and consequences for obesity in children and adults. Int J Obes Relat Metab Disord 2006; 30 (Suppl 4): S11–S17.

    Article  Google Scholar 

  22. Uauy R, Dangour AD . Fat and fatty acids requirements and recommendations for infants of 0–2 years and children of 12–18 years. Ann Nutr Metab 2009; 55: 76–96.

    Article  CAS  Google Scholar 

  23. Food and Agriculture Organization of the United Nations. Fats and fatty acids in human nutrition. Report of an expert consultation N° 91, Rome, 2010, pp 1–166.

  24. Michaelsen KF, Jorgensen MH . Dietary fat content and energy density during infancy and childhood; the effect on energy intake and growth. Eur J Clin Nutr 1995; 49: 467–483.

    CAS  PubMed  Google Scholar 

  25. Noble S, Emmett P, ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Food and nutrient intake in a cohort of 8-month-old infants in the south-west of England in 1993. Eur J Clin Nutr 2001; 55: 698–707.

    Article  CAS  Google Scholar 

  26. Hoppe C, Mølgaard C, Thomsen BL, Juul A, Michaelsen KF . Protein intake at 9 mo of age is associated with body size but not with body fat in 10-y-old Danish children. Am J Clin Nutr 2004; 79: 494–501.

    Article  CAS  Google Scholar 

  27. Karaolis-Danckert N, Günther AL, Kroke A, Hornberg C, Buyken AE . How early dietary factors modify the effect of rapid weight gain in infancy on subsequent body-composition development in term children whose birth weight was appropriate for gestational age. Am J Clin Nutr 2007; 86: 1700–1708.

    Article  CAS  Google Scholar 

  28. Butte NF, Fox MK, Briefel RR, Siega-Riz AM, Dwyer JT, Deming DM et al. Nutrient intakes of US infants, toddlers, and preschoolers meet or exceed dietary reference intakes. J Am Diet Assoc 2010; 110 (Suppl 12): S27–S37.

    Article  CAS  Google Scholar 

  29. Rolland-Cachera MF, Péneau S . Stabilization in the prevalence of childhood obesity: a role for early nutrition? Int J Obes Relat Metab Disord (Lond) 2010; 34: 1524–1525.

    Article  Google Scholar 

  30. Dwyer JT, Butte NF, Deming DM, Siega-Riz AM, Reidy KC . Feeding Infants and Toddlers Study 2008: progress, continuing concerns, and implications. J Am Diet Assoc 2010; 110 (12 Suppl): S60–S67.

    Article  Google Scholar 

  31. Butte NF . Fat intake of children in relation to energy requirements. Am J Clin Nutr 2000; 72 (Suppl 5): S1246–S1252.

    Article  Google Scholar 

  32. Hoppe C, Udam TR, Lauritzen L, Mølgaard C, Juul A, Michaelsen KF . Animal protein intake, serum insulin-like growth factor I, and growth in healthy 2.5-y-old Danish children. Am J Clin Nutr 2004; 80: 447–452.

    Article  CAS  Google Scholar 

  33. Ong KK, Loos RJ . Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr 2006; 95: 904–908.

    Google Scholar 

  34. Singhal A, Fewtrell M, Cole TJ, Lucas A . Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet 2003; 361: 1089–1097.

    Article  CAS  Google Scholar 

  35. Hales CN, Barker DJ . The thrifty phenotype hypothesis. Br Med Bull 2001; 60: 5–20.

    Article  CAS  Google Scholar 

  36. Gluckman PD, Hanson MA, Bateson P, Beedle AS, Law CM, Bhutta ZA et al. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet 2009; 373: 1654–1657.

    Article  Google Scholar 

  37. 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.

    Article  CAS  Google Scholar 

  38. Leonard WR, Sorensen MV, Mosher MJ, Spitsyn V, Comuzzie AG . Reduced fat oxidation and obesity risks among the Buryat of Southern Siberia. Am J Hum Biol 2009; 21: 664–670.

    Article  Google Scholar 

  39. 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 1997; 128 (Suppl 2): S415–S420.

    Google Scholar 

  40. Forouhi NG, Sharp SJ, Du H, van der A DL, Halkjaer J, Schulze MB et al. Dietary fat intake and subsequent weight change in adults: results from the European Prospective Investigation into Cancer and Nutrition cohorts. Am J Clin Nutr 2009; 90: 1632–1641.

    Article  CAS  Google Scholar 

  41. Ailhaud G, Massiera F, Weill P, Legrand P, Alessandri JM, Guesnet P . Temporal changes in dietary fats: role of n-6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity. Prog Lipid Res 2006; 45: 203–236.

    Article  CAS  Google Scholar 

  42. Kennedy K, Ross S, Isaacs EB, Weaver LT, Singhal A, Lucas A et al. The 10-year follow-up of a randomised trial of long-chain polyunsaturated fatty acid supplementation in preterm infants: effects on growth and blood pressure. Arch Dis Child 2010; 95: 588–595.

    Article  Google Scholar 

  43. Conn JA, Davies MJ, Walker RB, Moore VM . Food and nutrient intakes of 9-month-old infants in Adelaide, Australia. Public Health Nutr 2009; 12: 2448–2456.

    Article  Google Scholar 

  44. Malina RM, Katzmarzyk PT, Beunen G . Birth weight and its relationship to size attained and relative fat distribution at 7 to 12 years of age. Obes Res 1996; 4: 385–390.

    Article  CAS  Google Scholar 

  45. Rolfe Ede L, Loos RJ, Druet C, Stolk RP, Ekelund U, Griffin SJ et al. Association between birth weight and visceral fat in adults. Am J Clin Nutr 2010; 92: 347–352.

    Article  Google Scholar 

  46. Ong KK, Ahmed ML, Sherriff A, Woods KA, Watts A, Golding J et al. Cord blood leptin is associated with size at birth and predicts infancy weight gain in humans. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. J Clin Endocrinol Metab 1999; 84: 1145–1148.

    Article  CAS  Google Scholar 

  47. Phillips DI, Fall CH, Cooper C, Norman RJ, Robinson JS, Owens PC . Size at birth and plasma leptin concentrations in adult life. Int J Obes Relat Metab Disord 1999; 23: 1025–1029.

    Article  CAS  Google Scholar 

  48. Sternson SM . Metabolism: let them eat fat. Nature 2011; 477: 166–167.

    Article  CAS  Google Scholar 

  49. Bouret SG, Draper SJ, Simerly RB . Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004; 304: 108–110.

    Article  CAS  Google Scholar 

  50. Miralles O, Sánchez J, Palou A, Picó C . A physiological role of breast milk leptin in body weight control in developing infants. Obesity (Silver Spring) 2006; 14: 1371–1377.

    Article  CAS  Google Scholar 

  51. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A et al. Neonatal leptin treatment reverses developmental programming. Endocrinology 2005; 146: 4211–4216.

    Article  CAS  Google Scholar 

  52. Koletzko B, von Kries R, Closa R, Escribano J, Scaglioni S, Giovannini M et al European Childhood Obesity Trial Study Group. Lower protein in infant formula is associated with lower weight up to age two y: a randomized clinical trial. Am J Clin Nutr 2009; 89: 1836–1845.

    Article  CAS  Google Scholar 

  53. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJ . Early adiposity rebound in childhood and risk of Type 2 diabetes in adult life. Diabetologia 2003; 46: 190–194.

    Article  CAS  Google Scholar 

  54. Okasha M, Gunnell D, Holly J, Davey Smith G . Breast feeding. Childhood growth and adult cancer. Best Pract Res Clin Endocrinol Metab 2002; 16: 225–241.

    Article  Google Scholar 

  55. Must A, Jacques PF, Dallal GE, Bajema CJ, Dietz WH . Long term morbidity and mortality of overweight adolescents. A follow-up of the Harvard group study of 1922 to 1935. N Engl J Med 1992; 327: 1350–1355.

    Article  CAS  Google Scholar 

  56. Singhal A, Wells J, Cole TJ, Fewtrell M, Lucas A . Programming of lean body mass: a link between birth weight, obesity, and cardiovascular disease? Am J Clin Nutr 2003; 77: 726–730.

    Article  CAS  Google Scholar 

  57. Völgyi E, Tylavsky FA, Lyytikäinen A, Suominen H, Alén M, Cheng S . Assessing body composition with DXA and bioimpedance: effects of obesity, physical activity, and age. Obesity (Silver Spring) 2008; 16: 700–705.

    Article  Google Scholar 

  58. Livingstone MB, Prentice AM, Coward WA, Strain JJ, Black AE, Davies PS et al. Validation of estimates of energy intake by weighed dietary record and diet history in children and adolescents. Am J Clin Nutr 1992; 56: 29–35.

    Article  CAS  Google Scholar 

  59. Schack-Nielsen L, TIa Sørensen, Mortensen EL, Michaelsen KF . Late introduction of complementary feeding, rather than duration of breastfeeding, may protect against adult overweight. Am J Clin Nutr 2010; 91: 619–627.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the ‘Caisse Primaire d’Assurance Maladie de Paris’ for its support in conducting the study at the health centers for children and adults. We are indebted to the participants and their parents and to the field and laboratory staff for their involvement and contribution. A grant from the Institut Benjamin Delessert was obtained to perform the data collection at the age of 20 years.

Disclaimer

Institut Benjamin Delessert had no role in the design and conduct of the study; collection, analysis, and interpretation of the data; and preparation or review of the manuscript.

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Authors and Affiliations

  1. Nutritional Epidemiology Research Unit (UREN), INSERM U557, INRA U1125, CNAM, University of Paris 13, Sorbonne Paris Cité; CRNH Idf,

    M F Rolland-Cachera, M Deheeger, S Péneau & S Hercberg

  2. CRNH Idf, Bobigny, France

    M F Rolland-Cachera, M Deheeger, S Péneau & S Hercberg

  3. Aix-Marseille Université, NORT, 13005, Marseille, France

    M Maillot

  4. Inserm, UMR_S 1062, 13005, Marseille, France; Inra, UMR_INRA 1260, 13005,

    M Maillot

  5. Inra, UMR_INRA 1260, 13005, Marseille, France

    M Maillot

  6. INSERM U845, Université René Descartes, Paris, France

    J C Souberbielle

  7. Laboratoire d'Explorations Fonctionnelles, Hôpital Necker-Enfants Malades, Paris, France

    J C Souberbielle

  8. Institut de Veille Sanitaire—Université Paris13; Unité de Surveillance et d’Epidémiologie Nutritionnelle (USEN),

    S Hercberg

  9. Unité de Surveillance et d’Epidémiologie Nutritionnelle (USEN), Bobigny, France

    S Hercberg

  10. Département de Santé publique, Hôpital Avicenne, Bobigny, France

    S Hercberg

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  1. M F Rolland-Cachera
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  2. M Maillot
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  3. M Deheeger
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  4. J C Souberbielle
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Correspondence to M F Rolland-Cachera.

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Rolland-Cachera, M., Maillot, M., Deheeger, M. et al. Association of nutrition in early life with body fat and serum leptin at adult age. Int J Obes 37, 1116–1122 (2013). https://doi.org/10.1038/ijo.2012.185

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