Article | Published:

Epidemiology and Population Health

Subcutaneous fat mass in infancy and abdominal, pericardial and liver fat assessed by Magnetic Resonance Imaging at the age of 10 years

International Journal of Obesityvolume 43pages392401 (2019) | Download Citation



Fat mass development in infancy contributes to later adiposity, but its relation to ectopic fat depots is unknown. We examined the associations of infant subcutaneous fat with childhood general and organ-specific fat.


Among 593 children from a population-based prospective cohort study, we obtained total subcutaneous fat mass (as sum of biceps, triceps, suprailiacal, and subscapular skinfolds thickness), central-to-total subcutaneous fat ratio (sum of suprailiacal and subscapular skinfold thickness/total subcutaneous fat) at 1.5, 6 and 24 months of age. At 10 years, we assessed BMI, fat mass index (FMI) based on total body fat by dual-energy X-ray absorptiometry, and abdominal subcutaneous, visceral and pericardial fat mass indices, and liver fat fraction by Magnetic Resonance Imaging.


A higher central-to-total subcutaneous fat ratio at 1.5 months only and higher total subcutaneous fat at 6 and 24 months were associated with higher BMI, FMI and subcutaneous fat mass index at 10 years. The observed associations were the strongest between total subcutaneous fat at 24 months and these childhood outcomes (difference per 1-SDS increase in total subcutaneous fat: 0.15 SDS (95% Confidence Interval (CI) 0.08, 0.23), 0.17 SDS (95% CI 0.10, 0.24), 0.16 SDS (95% CI 0.08, 0.23) for BMI, FMI and childhood subcutaneous fat mass index, respectively). Infant subcutaneous fat measures at any time point were not associated with visceral and pericardial fat mass indices, and liver fat fraction at 10 years.


Our results suggest that infant subcutaneous fat is associated with later childhood abdominal subcutaneous fat and general adiposity, but not with other organ-specific fat depots.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Guo SS, Chumlea WC. Tracking of body mass index in children in relation to overweight in adulthood. Am J Clin Nutr. 1999;70:145S–8.

  2. 2.

    Rolland-Cachera MF, Deheeger M, Guilloud-Bataille M, Avons P, Patois E, Sempe M. Tracking the development of adiposity from one month of age to adulthood. Ann Hum Biol. 1987;14:219–29.

  3. 3.

    Kuzawa CW. Adipose tissue in human infancy and childhood: an evolutionary perspective. Am J Phys Anthropol. 1998;Suppl 27:177–209.

  4. 4.

    Budge H, Sebert S, Sharkey D, Symonds ME. Session on ‘obesity’. adipose tissue development, nutrition in early life and its impact on later obesity. Proc Nutr Soc. 2009;68:321–6.

  5. 5.

    Berry DC, Stenesen D, Zeve D, Graff JM. The developmental origins of adipose tissue. Development. 2013;140:3939–49.

  6. 6.

    Baird J, Fisher D, Lucas P, Kleijnen J, Roberts H, Law C. Being big or growing fast: systematic review of size and growth in infancy and later obesity. BMJ. 2005;331:929.

  7. 7.

    Gishti O, Gaillard R, Manniesing R, Abrahamse-Berkeveld M, van der Beek EM, Heppe DH, et al. Fetal and infant growth patterns associated with total and abdominal fat distribution in school-age children. J Clin Endocrinol Metab. 2014;99:2557–66.

  8. 8.

    Perng W, Rifas-Shiman SL, Kramer MS, Haugaard LK, Oken E, Gillman MW, et al. Early weight gain, linear growth, and mid-childhood blood pressure: a prospective study in project viva. Hypertension. 2016;67:301–8.

  9. 9.

    Demerath EW, Schubert CM, Maynard LM, Sun SS, Chumlea WC, Pickoff A, et al. Do changes in body mass index percentile reflect changes in body composition in children? Data from the Fels Longitudinal Study. Pediatrics. 2006;117:e487–95.

  10. 10.

    Despres JP. Body fat distribution and risk of cardiovascular disease: an update. Circulation. 2012;126:1301–13.

  11. 11.

    Britton KA, Fox CS. Ectopic fat depots and cardiovascular disease. Circulation. 2011;124:e837–41.

  12. 12.

    Wells JC, Chomtho S, Fewtrell MS. Programming of body composition by early growth and nutrition. Proc Nutr Soc. 2007;66:423–34.

  13. 13.

    Santos S, Gaillard R, Oliveira A, Barros H, Abrahamse-Berkeveld M, van der Beek EM, et al. Associations of infant subcutaneous fat mass with total and abdominal fat mass at school-age: The Generation R Study. Paediatr Perinat Epidemiol. 2016;30:511–20.

  14. 14.

    Santos S, Gaillard R, Oliveira A, Barros H, Hofman A, Franco OH, et al. Subcutaneous fat mass in infancy and cardiovascular risk factors at school-age: The generation R study. Obes (Silver Spring). 2016;24:424–9.

  15. 15.

    Lim S, Meigs JB. Ectopic fat and cardiometabolic and vascular risk. Int J Cardiol. 2013;169:166–76.

  16. 16.

    Kooijman MN, Kruithof CJ, van Duijn CM, Duijts L, Franco OH, van IMH, et al. The Generation R Study: design and cohort update 2017. Eur J Epidemiol. 2016;31:1243–64.

  17. 17.

    Ay L, Hokken-Koelega AC, Mook-Kanamori DO, Hofman A, Moll HA, Mackenbach JP, et al. Tracking and determinants of subcutaneous fat mass in early childhood: the Generation R Study. Int J Obes (Lond). 2008;32:1050–9.

  18. 18.

    Ketel IJ, Volman MN, Seidell JC, Stehouwer CD, Twisk JW, Lambalk CB. Superiority of skinfold measurements and waist over waist-to-hip ratio for determination of body fat distribution in a population-based cohort of Caucasian Dutch adults. Eur J Endocrinol. 2007;156:655–61.

  19. 19.

    Freedman DS, Wang J, Ogden CL, Thornton JC, Mei Z, Pierson RN, et al. The prediction of body fatness by BMI and skinfold thicknesses among children and adolescents. Ann Hum Biol. 2007;34:183–94.

  20. 20.

    Wells JC, Cole TJ. steam As. Adjustment of fat-free mass and fat mass for height in children aged 8 y. Int J Obes Relat Metab Disord. 2002;26:947–52.

  21. 21.

    Fredriks AM, van Buuren S, Wit JM, Verloove-Vanhorick SP. Body index measurements in 1996-7 compared with 1980. Arch Dis Child. 2000;82:107–12.

  22. 22.

    Hu H, Nayak K, Goran M. Assessment of abdominal adipose tissue and organ fat content by magnetic resonance imaging. Obes Rev. 2011;12:e504–15.

  23. 23.

    Shuster A, Patlas M, Pinthus J, Mourtzakis M. The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol. 2012;85:1–10.

  24. 24.

    Thomas E, Fitzpatrick J, Malik S, Taylor-Robinson S, Bell J. Whole body fat: content and distribution. Progress Nucl Magn Reson Spectrosc. 2013;73:56–80.

  25. 25.

    Mitra S, Fernandez-Del-Valle M, Hill J. The role of MRI in understanding the underlying mechanisms in obesity associated diseases. Biochim Biophys Acta. 2016;1863:1115–31.

  26. 26.

    Langeslag S, Schmidt M, Ghassabian A, Jaddoe V, Hofman A, van der Lugt A, et al. Functional connectivity between parietal and frontal brain regions and intelligence in young children: The Generation R Study. Hum Brain Mapp. 2013;34:3299–307.

  27. 27.

    Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging. 2011;34:729–49.

  28. 28.

    Keijzer-Veen MG, Euser AM, van Montfoort N, Dekker FW, Vandenbroucke JP, Van Houwelingen HC. A regression model with unexplained residuals was preferred in the analysis of the fetal origins of adult diseases hypothesis. J Clin Epidemiol. 2005;58:1320–4.

  29. 29.

    Jones A, Charakida M, Falaschetti E, Hingorani AD, Finer N, Masi S, et al. Adipose and height growth through childhood and blood pressure status in a large prospective cohort study. Hypertension. 2012;59:919–25.

  30. 30.

    Vogelezang S, Gishti O, Felix JF, van der Beek EM, Abrahamse-Berkeveld M, Hofman A, et al. Tracking of abdominal subcutaneous and preperitoneal fat mass during childhood. The Generation R Study. Int J Obes (Lond). 2016;40:595–600.

  31. 31.

    Gishti O, Gaillard R, Durmus B, Abrahamse M, van der Beek EM, Hofman A, et al. BMI, total and abdominal fat distribution, and cardiovascular risk factors in school-age children. Pediatr Res. 2015;77:710–8.

  32. 32.

    Abraham TM, Pedley A, Massaro JM, Hoffmann U, Fox CS. Association between visceral and subcutaneous adipose depots and incident cardiovascular disease risk factors. Circulation. 2015;132:1639–47.

  33. 33.

    Sandboge S, Perala MM, Salonen MK, Blomstedt PA, Osmond C, Kajantie E, et al. Early growth and non-alcoholic fatty liver disease in adulthood-the NAFLD liver fat score and equation applied on the Helsinki Birth Cohort Study. Ann Med. 2013;45:430–7.

  34. 34.

    Breij LM, Kerkhof GF, Hokken-Koelega AC. Accelerated infant weight gain and risk for nonalcoholic fatty liver disease in early adulthood. J Clin Endocrinol Metab. 2014;99:1189–95.

  35. 35.

    Anderson EL, Howe LD, Fraser A, Callaway MP, Sattar N, Day C, et al. Weight trajectories through infancy and childhood and risk of non-alcoholic fatty liver disease in adolescence: the ALSPAC study. J Hepatol. 2014;61:626–32.

  36. 36.

    Ayonrinde OT, Olynyk JK, Marsh JA, Beilin LJ, Mori TA, Oddy WH, et al. Childhood adiposity trajectories and risk of nonalcoholic fatty liver disease in adolescents. J Gastroenterol Hepatol. 2015;30:163–71.

  37. 37.

    Kindblom JM, Lorentzon M, Hellqvist A, Lonn L, Brandberg J, Nilsson S, et al. BMI changes during childhood and adolescence as predictors of amount of adult subcutaneous and visceral adipose tissue in men: the GOOD Study. Diabetes. 2009;58:867–74.

  38. 38.

    Demerath EW, Reed D, Choh AC, Soloway L, Lee M, Czerwinski SA, et al. Rapid postnatal weight gain and visceral adiposity in adulthood: the Fels Longitudinal Study. Obes (Silver Spring). 2009;17:2060–6.

  39. 39.

    Gonzalez DA, Nazmi A, Victora CG. Growth from birth to adulthood and abdominal obesity in a Brazilian birth cohort. Int J Obes (Lond). 2010;34:195–202.

  40. 40.

    Kuh D, Hardy R, Chaturvedi N, Wadsworth ME. Birth weight, childhood growth and abdominal obesity in adult life. Int J Obes Relat Metab Disord. 2002;26:40–7.

  41. 41.

    McCarthy A, Hughes R, Tilling K, Davies D, Smith GD, Ben-Shlomo Y. Birth weight; postnatal, infant, and childhood growth; and obesity in young adulthood: evidence from the Barry Caerphilly Growth Study. Am J Clin Nutr. 2007;86:907–13.

  42. 42.

    Samara A, Ventura EE, Alfadda AA, Goran MI. Use of MRI and CT for fat imaging in children and youth: what have we learned about obesity, fat distribution and metabolic disease risk? Obes Rev. 2012;13:723–32.

Download references


We gratefully acknowledge the contribution of general practitioners, hospitals, midwives, and pharmacies in Rotterdam.


The general design of the Generation R Study is made possible by financial support from the Erasmus MC, University Medical Center, Rotterdam, Erasmus University Rotterdam, Netherlands Organization for Health Research and Development (ZonMw), Netherlands Organisation for Scientific Research (NWO), Ministry of Health, Welfare and Sport and Ministry of Youth and Families. Research that has leaded to these findings received support by a grant from the Netherlands Organization for Health Research and Development (VIDI 016.136.361), a European Research Council Consolidator Grant (ERC-2014-CoG-648916), an unrestricted grant from Nutricia Research and from the European Union’s Horizon 2020 research and innovation programme under grant agreements no 733206 (LifeCycle). Bernadeta Patro Golab received a research training fellowship grant from the Nestle Nutrition Institute.

Author information


  1. The Generation R Study Group, Erasmus Medical Center, Rotterdam, The Netherlands

    • Bernadeta Patro Golab
    • , Ellis Voerman
    • , Susana Santos
    •  & Vincent W. V. Jaddoe
  2. Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands

    • Bernadeta Patro Golab
    • , Ellis Voerman
    • , Susana Santos
    •  & Vincent W. V. Jaddoe
  3. Department of Pediatrics, Sophia Children’s Hospital, Erasmus Medical Center, Rotterdam, The Netherlands

    • Bernadeta Patro Golab
    • , Ellis Voerman
    • , Susana Santos
    •  & Vincent W. V. Jaddoe
  4. Department of Pediatrics, Medical University of Warsaw, Warsaw, Poland

    • Bernadeta Patro Golab
  5. Department of Radiology, Erasmus Medical Center, Rotterdam, The Netherlands

    • Aad van der Lugt


  1. Search for Bernadeta Patro Golab in:

  2. Search for Ellis Voerman in:

  3. Search for Aad van der Lugt in:

  4. Search for Susana Santos in:

  5. Search for Vincent W. V. Jaddoe in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Vincent W. V. Jaddoe.

Supplementary information

About this article

Publication history