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Tracking of abdominal subcutaneous and preperitoneal fat mass during childhood. The Generation R Study

International Journal of Obesity volume 40, pages 595–600 (2016)Cite this article

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Abstract

Background:

Overweight and obesity in early life tends to track into later life. Not much is known about tracking of abdominal fat. Our objective was to examine the extent of tracking of abdominal fat measures during the first six years of life.

Design:

We performed a prospective cohort study among 393 Dutch children followed from the age of 2 years (90% range 1.9; 2.3) until the age of 6 years (90% range 5.7; 6.2). At both ages, we performed abdominal ultrasound to measure abdominal subcutaneous and preperitoneal fat distances and areas, and we calculated the preperitoneal/subcutaneous fat distance ratio. High abdominal fat measures were defined as values in the upper 15%.

Results:

Abdominal subcutaneous fat distance and area, and preperitoneal fat area at 2 years were correlated with their corresponding measures at 6 years (all P-values <0.01), with the strongest coefficients for abdominal subcutaneous fat measures. Preperitoneal fat distance at the age of 2 years was not correlated with the corresponding measure at 6 years. The tracking coefficient for preperitoneal/subcutaneous fat distance ratio from 2 to 6 years was r=0.36 (P<0.01). Children with high abdominal subcutaneous fat measures at 2 years had increased risk of having high abdominal subcutaneous fat measures at 6 years (odds ratios 9.2 (95% confidence interval (CI) 4.1–20.8) and 12.4 (95% CI 5.4–28.6) for subcutaneous fat distance and area, respectively). These associations were not observed for preperitoneal fat measures.

Conclusions:

Our findings suggest that both abdominal subcutaneous and preperitoneal fat mass measures track during childhood, but with stronger tracking for abdominal subcutaneous fat measures. An adverse abdominal fat distribution in early life may have long-term consequences.

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References

  1. Dietz WH . Critical periods in childhood for the development of obesity. Am J Clin Nutr 1994; 59: 955–959.

    Article  CAS  Google Scholar 

  2. l'Allemand-Jander D . Clinical diagnosis of metabolic and cardiovascular risks in overweight children: early development of chronic diseases in the obese child. Int J Obes (Lond) 2010; 34 (Suppl 2): S32–S36.

    Article  Google Scholar 

  3. 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.

    Article  CAS  Google Scholar 

  4. Kopelman PG . Obesity as a medical problem. Nature 2000; 404: 635–643.

    Article  CAS  Google Scholar 

  5. Stettler N . Nature and strength of epidemiological evidence for origins of childhood and adulthood obesity in the first year of life. Int J Obes (Lond) 2007; 31: 1035–1043.

    Article  CAS  Google Scholar 

  6. Druet C, Ong KK . Early childhood predictors of adult body composition. Best Pract Res Clin Endocrinol Metab 2008; 22: 489–502.

    Article  Google Scholar 

  7. Di Pietro L, Mossberg HO, Stunkard AJ . A 40-year history of overweight children in Stockholm: life-time overweight, morbidity, and mortality. Int J Obes Relat Metab Disord 1994; 18: 585–590.

    CAS  Google Scholar 

  8. Whitaker RC, Wright JA, Pepe MS, Seidel KD, Dietz WH . Predicting obesity in young adulthood from childhood and parental obesity. N Engl J Med 1997; 337: 869–873.

    Article  CAS  Google Scholar 

  9. Gunnell DJ, Frankel SJ, Nanchahal K, Peters TJ, Davey Smith G . Childhood obesity and adult cardiovascular mortality: a 57-y follow-up study based on the Boyd Orr cohort. Am J Clin Nutr 1998; 67: 1111–1118.

    Article  CAS  Google Scholar 

  10. Morrison JA, Friedman LA, Gray-McGuire C . Metabolic syndrome in childhood predicts adult cardiovascular disease 25 years later: the Princeton Lipid Research Clinics Follow-up Study. Pediatrics 2007; 120: 340–345.

    Article  Google Scholar 

  11. Wang Y, Ge K, Popkin BM . Tracking of body mass index from childhood to adolescence: a 6-y follow-up study in China. Am J Clin Nutr 2000; 72: 1018–1024.

    Article  CAS  Google Scholar 

  12. Guo SS, Chumlea WC . Tracking of body mass index in children in relation to overweight in adulthood. Am J Clin Nutr 1999; 70: 145S–148SS.

    Article  CAS  Google Scholar 

  13. Mossberg HO . 40-year follow-up of overweight children. Lancet 1989; 2: 491–493.

    Article  CAS  Google Scholar 

  14. 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: 219–229.

    Article  CAS  Google Scholar 

  15. Lake JK, Power C, Cole TJ . Child to adult body mass index in the 1958 British birth cohort: associations with parental obesity. Arch Dis Child 1997; 77: 376–381.

    Article  CAS  Google Scholar 

  16. Guo SS, Roche AF, Chumlea WC, Gardner JD, Siervogel RM . The predictive value of childhood body mass index values for overweight at age 35 y. Am J Clin Nutr 1994; 59: 810–819.

    Article  CAS  Google Scholar 

  17. Gishti O, Gaillard R, Durmus B, Abrahamse M, van der Beek EM, Hofman A et al. Body mass index, total and abdominal fat distribution and cardiovascular risk factors in school-age children. Pediatr Res 2015; 77: 710–718.

    Article  Google Scholar 

  18. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 2007; 116: 39–48.

    Article  Google Scholar 

  19. Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K et al. General and abdominal adiposity and risk of death in Europe. N Engl J Med 2008; 359: 2105–2120.

    Article  CAS  Google Scholar 

  20. Lee CM, Huxley RR, Wildman RP, Woodward M . Indices of abdominal obesity are better discriminators of cardiovascular risk factors than BMI: a meta-analysis. J Clin Epidemiol 2008; 61: 646–653.

    Article  Google Scholar 

  21. Mook-Kanamori DO, Holzhauer S, Hollestein LM, Durmus B, Manniesing R, Koek M et al. Abdominal fat in children measured by ultrasound and computed tomography. Ultrasound Med Biol 2009; 35: 1938–1946.

    Article  CAS  Google Scholar 

  22. Jaddoe VW, van Duijn CM, Franco OH, van der Heijden AJ, van Iizendoorn MH, de Jongste JC et al. The Generation R Study: design and cohort update 2012. Eur J Epidemiol 2012; 27: 739–756.

    Article  Google Scholar 

  23. Kruithof CJ, Kooijman MN, van Duijn CM, Franco OH, de Jongste JC, Klaver CC et al. The Generation R Study: Biobank update 2015. Eur J Epidemiol 2014; 29: 911–927.

    Article  CAS  Google Scholar 

  24. Suzuki R, Watanabe S, Hirai Y, Akiyama K, Nishide T, Matsushima Y et al. Abdominal wall fat index, estimated by ultrasonography, for assessment of the ratio of visceral fat to subcutaneous fat in the abdomen. Am J Med 1993; 95: 309–314.

    Article  CAS  Google Scholar 

  25. Holzhauer S, Zwijsen RM, Jaddoe VW, Boehm G, Moll HA, Mulder PG et al. Sonographic assessment of abdominal fat distribution in infancy. Eur J Epidemiol 2009; 24: 521–529.

    Article  Google Scholar 

  26. Statistics Netherlands. Standard classification of education 2003 (Standaard Onderwijsindeling 2003). Voorburg/Heerlen, 2004. http://www.cbs.nl.

  27. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH . Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000; 320: 1240–1243.

    Article  CAS  Google Scholar 

  28. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 2009; 338: b2393.

    Article  Google Scholar 

  29. Guo SS, Wu W, Chumlea WC, Roche AF . Predicting overweight and obesity in adulthood from body mass index values in childhood and adolescence. Am J Clin Nutr 2002; 76: 653–658.

    Article  CAS  Google Scholar 

  30. Clarke WR, Lauer RM . Does childhood obesity track into adulthood? Crit Rev Food Sci Nutr 1993; 33: 423–430.

    Article  CAS  Google Scholar 

  31. Campbell PT, Katzmarzyk PT, Malina RM, Rao DC, Perusse L, Bouchard C . Stability of adiposity phenotypes from childhood and adolescence into young adulthood with contribution of parental measures. Obes Res 2001; 9: 394–400.

    Article  CAS  Google Scholar 

  32. Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS . The relation of childhood BMI to adult adiposity: the Bogalusa Heart Study. Pediatrics 2005; 115: 22–27.

    Article  Google Scholar 

  33. Katzmarzyk PT, Perusse L, Malina RM, Bouchard C . Seven-year stability of indicators of obesity and adipose tissue distribution in the Canadian population. Am J Clin Nutr 1999; 69: 1123–1129.

    Article  CAS  Google Scholar 

  34. Serdula MK, Ivery D, Coates RJ, Freedman DS, Williamson DF, Byers T . Do obese children become obese adults? A review of the literature. Prev Med 1993; 22: 167–177.

    Article  CAS  Google Scholar 

  35. Power C, Lake JK, Cole TJ . Measurement and long-term health risks of child and adolescent fatness. Int J Obes Relat Metab Disord 1997; 21: 507–526.

    Article  CAS  Google Scholar 

  36. Singh AS, Mulder C, Twisk JW, van Mechelen W, Chinapaw MJ . Tracking of childhood overweight into adulthood: a systematic review of the literature. Obes Rev 2008; 9: 474–488.

    Article  CAS  Google Scholar 

  37. Guo SS, Chumlea WC, Roche AF, Siervogel RM . Age- and maturity-related changes in body composition during adolescence into adulthood: the Fels longitudinal study. Appl Radiat Isot 1998; 49: 581–585.

    Article  CAS  Google Scholar 

  38. Rolland-Cachera MF, Bellisle F, Sempe M . The prediction in boys and girls of the weight/height index and various skinfold measurements in adults: a two-decade follow-up study. Int J Obes 1989; 13: 305–311.

    CAS  PubMed  Google Scholar 

  39. Hawk LJ, Brook CG . Influence of body fatness in childhood on fatness in adult life. Br Med J 1979; 1: 151–152.

    Article  CAS  Google Scholar 

  40. Freedman DS, Shear CL, Burke GL, Srinivasan SR, Webber LS, Harsha DW et al. Persistence of juvenile-onset obesity over eight years: the Bogalusa Heart Study. Am J Public Health 1987; 77: 588–592.

    Article  CAS  Google Scholar 

  41. 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: 1050–1059.

    Article  CAS  Google Scholar 

  42. Garn SM, LaVelle M . Two-decade follow-up of fatness in early childhood. Am J Dis Child 1985; 139: 181–185.

    CAS  PubMed  Google Scholar 

  43. van Lenthe FJ, Kemper HC, van Mechelen W, Twisk JW . Development and tracking of central patterns of subcutaneous fat in adolescence and adulthood: the Amsterdam Growth and Health Study. Int J Epidemiol 1996; 25: 1162–1171.

    Article  CAS  Google Scholar 

  44. Taylor AE, Ebrahim S, Ben-Shlomo Y, Martin RM, Whincup PH, Yarnell JW et al. Comparison of the associations of body mass index and measures of central adiposity and fat mass with coronary heart disease, diabetes, and all-cause mortality: a study using data from 4 UK cohorts. Am J Clin Nutr 2010; 91: 547–556.

    Article  CAS  Google Scholar 

  45. Tamura A, Mori T, Hara Y, Komiyama A . Preperitoneal fat thickness in childhood obesity: association with serum insulin concentration. Pediatr Int 2000; 42: 155–159.

    Article  CAS  Google Scholar 

  46. Falaschetti E, Hingorani AD, Jones A, Charakida M, Finer N, Whincup P et al. Adiposity and cardiovascular risk factors in a large contemporary population of pre-pubertal children. Eur Heart J 2010; 31: 3063–3072.

    Article  CAS  Google Scholar 

  47. Lawlor DA, Benfield L, Logue J, Tilling K, Howe LD, Fraser A et al. Association between general and central adiposity in childhood, and change in these, with cardiovascular risk factors in adolescence: prospective cohort study. Bmj 2010; 341: c6224.

    Article  Google Scholar 

  48. Iwata F, Taniguchi K, Yamazaki H, Hara M, Okada T, Harada K . Intra-abdominal fat in obese children. Acta Paediatr Jpn 1995; 37: 617–620.

    Article  CAS  Google Scholar 

  49. Nohr EA, Frydenberg M, Henriksen TB, Olsen J . Does low participation in cohort studies induce bias? Epidemiology 2006; 17: 413–418.

    Article  Google Scholar 

  50. Liu KH, Chan YL, Chan WB, Chan JC, Chu CW . Mesenteric fat thickness is an independent determinant of metabolic syndrome and identifies subjects with increased carotid intima-media thickness. Diabetes Care 2006; 29: 379–384.

    Article  Google Scholar 

  51. Liska D, Dufour S, Zern TL, Taksali S, Cali AM, Dziura J et al. Interethnic differences in muscle, liver and abdominal fat partitioning in obese adolescents. PLoS One 2007; 2: e569.

    Article  Google Scholar 

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Acknowledgements

The Generation R Study is conducted by the Erasmus MC in close collaboration with the School of Law and Faculty of Social Sciences of the Erasmus University Rotterdam, the Municipal Health Service Rotterdam area, Rotterdam, the Rotterdam Homecare Foundation, Rotterdam and the Stichting Trombosedienst and Artsenlaboratorium Rijnmond (STAR), Rotterdam. We gratefully acknowledge the contribution of participating mothers, general practitioners, hospitals, midwives and pharmacies in Rotterdam. This work was supported by the Erasmus MC, Rotterdam, the Erasmus University Rotterdam and by the Netherlands Organization for Health Research and Development and the Netherlands Organization for Health Research and Development. This research also received funding from the European Union’s Seventh Framework Programme (FP7/2007–2013), project EarlyNutrition under grant agreement no. 289346 and an unrestricted grant from Nutricia Research. VWVJ received an additional grant from the Netherlands Organization for Health Research and Development (VIDI 016.136.361) and an European Research Council Consolidator Grant (ERC-2014-CoG-648916).

Author contributions

SV, OG and VWVJ designed and conducted the research and wrote the paper. SV analysed the data. OG, JFF, EMB, MAB, AH and RG provided comments and consultation regarding the analyses, interpretation of the results and manuscript. SV and VWVJ had primary responsibility for final content. All authors gave final approval of the version to be published.

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Authors and Affiliations

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

    S Vogelezang, O Gishti, J F Felix, R Gaillard & V W V Jaddoe

  2. Department of Epidemiology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands

    S Vogelezang, O Gishti, J F Felix, A Hofman, R Gaillard & V W V Jaddoe

  3. Department of Paediatrics, Erasmus MC, University Medical Center, Rotterdam, the Netherlands

    S Vogelezang, O Gishti, J F Felix, R Gaillard & V W V Jaddoe

  4. Nutricia Research, Utrecht, The Netherlands

    E M van der Beek & M Abrahamse-Berkeveld

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  1. S Vogelezang
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Correspondence to V W V Jaddoe.

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Vogelezang, S., Gishti, O., Felix, J. et al. Tracking of abdominal subcutaneous and preperitoneal fat mass during childhood. The Generation R Study. Int J Obes 40, 595–600 (2016). https://doi.org/10.1038/ijo.2015.252

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