Skip to main content
SpringerLink
Log in

Relationship Between Markers of Body Fat and Calcaneal Bone Stiffness Differs Between Preschool and Primary School Children: Results from the IDEFICS Baseline Survey

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the relationship between markers of body fat and bone status assessed as calcaneal bone stiffness in a large sample of European healthy pre- and primary school children. Participants were 7,447 children from the IDEFICS study (spread over eight different European countries), age 6.1 ± 1.8 years (range 2.1–9.9), 50.5 % boys. Anthropometric measurements (weight, height, bioelectrical impedance, waist and hip circumference, and tricipital and subscapular skinfold thickness) as well as quantitative ultrasonographic measurements to determine calcaneal stiffness index (SI) were performed. Partial correlation analysis, linear regression analysis, and ANCOVA were stratified by sex and age group: preschool boys (n = 1,699) and girls (n = 1,599) and primary school boys (n = 2,062) and girls (n = 2,087). In the overall study population, the average calcaneal SI was equal to 80.2 ± 14.0, ranging 42.4–153. The results showed that preschool children with higher body fat had lower calcaneal SI (significant correlation coefficients between −0.05 and −0.20), while primary school children with higher body fat had higher calcaneal SI (significant correlation coefficients between 0.05 and 0.13). After adjusting for fat-free mass, both preschool and primary school children showed an inverse relationship between body fat and calcaneal stiffness. To conclude, body fat is negatively associated with calcaneal bone stiffness in children after adjustment for fat-free mass. Fat-free mass may confound the association in primary school children but not in preschool children. Muscle mass may therefore be an important determinant of bone stiffness.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Schoenau E, Saggese G, Peter F, Baroncelli GI, Shaw NJ, Crabtree NJ, Zadik Z, Neu CM, Noordam C, Radetti G, Hochberg Z (2004) From bone biology to bone analysis. Horm Res 61:257–269

    Article  PubMed  CAS  Google Scholar 

  2. Binkley TL, Berry R, Specker BL (2008) Methods for measurement of pediatric bone. Rev Endocr Metab Dis 9:95–106

    Article  Google Scholar 

  3. Wunsche K, Wunsche B, Fahnrich H, Mentzel HJ, Vogt S, Abendroth K, Kaiser WA (2000) Ultrasound bone densitometry of the os calcis in children and adolescents. Calcif Tissue Int 67:349–355

    Article  PubMed  CAS  Google Scholar 

  4. Rizzoli R, Bianchi ML, Garabedian M, Mckay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46:294–305

    Article  PubMed  Google Scholar 

  5. Leonard MB, Shults J, Wilson BA, Tershakovec AM, Zemel BS (2004) Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 80:514–523

    PubMed  CAS  Google Scholar 

  6. Gracia-Marco L, Ortega FB, Jimenez-Pavon D, Rodriguez G, Castillo MJ, Vicente-Rodriguez G, Moreno LA (2011) Adiposity and bone health in Spanish adolescents. The HELENA study. Osteoporos Int 23:937–947

    Article  PubMed  Google Scholar 

  7. Ellis KJ, Shypailo RJ, Wong WW, Abrams SA (2003) Bone mineral mass in overweight and obese children: diminished or enhanced? Acta Diabetol 40(Suppl 1):S274–S277

    Article  PubMed  Google Scholar 

  8. Falk B, Braid S, Moore M, O’Leary D, Sullivan P, Klentrou P (2008) Bone properties in overweight pre- and early-pubertal boys. Pediatr Exerc Sci 20:50–61

    PubMed  Google Scholar 

  9. Goulding A, Taylor RW, Jones IE, McAuley KA, Manning PJ, Williams SM (2000) Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord 24:627–632

    Article  PubMed  CAS  Google Scholar 

  10. Rocher E, Chappard C, Jaffre C, Benhamou CL, Courteix D (2008) Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26:73–78

    Article  PubMed  Google Scholar 

  11. Duquette J, Lin J, Hoffman A, Houde J, Ahmadi S, Baran D (1997) Correlations among bone mineral density, broadband ultrasound attenuation, mechanical indentation testing, and bone orientation in bovine femoral neck samples. Calcif Tissue Int 60:181–186

    Article  PubMed  CAS  Google Scholar 

  12. Baroncelli GI (2008) Quantitative ultrasound methods to assess bone mineral status in children: technical characteristics, performance, and clinical application. Pediatr Res 63:220–228

    Article  PubMed  Google Scholar 

  13. Goh SY, Aragon JM, Lee YS, Loke KY (2011) Normative data for quantitative calcaneal ultrasound in Asian children. Ann Acad Med Singap 40:74–76

    PubMed  Google Scholar 

  14. Falcini F, Bindi G, Ermini M, Galluzzi F, Poggi G, Rossi S, Masi L, Cimaz R, Brandi ML (2000) Comparison of quantitative calcaneal ultrasound and dual energy X-ray absorptiometry in the evaluation of osteoporotic risk in children with chronic rheumatic diseases. Calcif Tissue Int 67:19–23

    Article  PubMed  CAS  Google Scholar 

  15. Fielding KT, Nix DA, Bachrach LK (2003) Comparison of calcaneus ultrasound and dual X-ray absorptiometry in children at risk of osteopenia. J Clin Densitom 6:7–15

    Article  PubMed  Google Scholar 

  16. Gluer CC, Wu CY, Jergas M, Goldstein SA, Genant HK (1994) Three quantitative ultrasound parameters reflect bone structure. Calcif Tissue Int 55:46–52

    Article  PubMed  CAS  Google Scholar 

  17. Njeh CF, Hans D, Wu C, Kantorovich E, Sister M, Fuerst T, Genant HK (1999) An in vitro investigation of the dependence on sample thickness of the speed of sound along the specimen. Med Eng Phys 21:651–659

    Article  PubMed  CAS  Google Scholar 

  18. Jaworski M, Lebiedowski M, Lorenc RS, Trempe J (1995) Ultrasound bone-measurement in pediatric subjects. Calcif Tissue Int 56:368–371

    Article  PubMed  CAS  Google Scholar 

  19. Mughal MZ, Langton CM, Utretch G, Morrison J, Specker BL (1996) Comparison between broad-band ultrasound attenuation of the calcaneum and total body bone mineral density in children. Acta Paediatr 85:663–665

    Article  PubMed  CAS  Google Scholar 

  20. Brukx LJCE, Waelkens JJJ (2003) Evaluation of the usefulness of a quantitative ultrasound device in screening of bone mineral density in children. Ann Hum Biol 30:304–315

    Article  PubMed  CAS  Google Scholar 

  21. Sundberg M, Gardsell P, Johnell O, Ornstein E, Sernbo I (1998) Comparison of quantitative ultrasound measurements in calcaneus with DXA and SXA at other skeletal sites: a population-based study on 280 children aged 11–16 years. Osteoporos Int 8:410–417

    Article  PubMed  CAS  Google Scholar 

  22. Lum CK, Wang MC, Moore E, Wilson DM, Marcus R, Bachrach LK (1999) A comparison of calcaneus ultrasound and dual X-ray absorptiometry in healthy North American youths and young adults. J Clin Densitom 2:403–411

    Article  PubMed  CAS  Google Scholar 

  23. Mughal MZ, Ward K, Qayyum N, Langton CM (1997) Assessment of bone status using the contact ultrasound bone analyser. Arch Dis Child 76:535–536

    Article  PubMed  CAS  Google Scholar 

  24. Wetter AC, Economos CD (2004) Relationship between quantitative ultrasound, anthropometry and sports participation in college aged adults. Osteoporos Int 15:799–806

    Article  PubMed  Google Scholar 

  25. Lee M, Nahhas RW, Choh AC, Demerath EW, Duren DL, Chumlea WC, Sherwood RJ, Towne B, Siervogel RM, Czerwinski SA (2011) Longitudinal changes in calcaneal quantitative ultrasound measures during childhood. Osteoporos Int 22:2295–2305

    Article  PubMed  CAS  Google Scholar 

  26. van den Bergh JP, Noordam C, Thijssen JM, Otten BJ, Smals AG, Hermus AR (2001) Measuring skeletal changes with calcaneal ultrasound imaging in healthy children and adults: the influence of size and location of the region of interest. Osteoporos Int 12:970–979

    Article  PubMed  Google Scholar 

  27. Alwis G, Rosengren B, Nilsson JA, Stenevi-Lundgren S, Sundberg M, Sernbo I, Karlsson MK (2010) Normative calcaneal quantitative ultrasound data as an estimation of skeletal development in Swedish children and adolescents. Calcif Tissue Int 87:493–506

    Article  PubMed  CAS  Google Scholar 

  28. Nohara T, Ueda M, Ohta A, Sugimoto T (2009) Correlation of body growth and bone mineral density measured by ultrasound densitometry of the calcaneus in children and adolescents. Tohoku J Exp Med 219:63–69

    Article  PubMed  Google Scholar 

  29. Sawyer A, Moore S, Fielding KT, Nix DA, Kiratli J, Bachrach LK (2001) Calcaneus ultrasound measurements in a convenience sample of healthy youth. J Clin Densitom 4:111–120

    Article  PubMed  CAS  Google Scholar 

  30. Dib L, Arabi A, Maalouf J, Nabulsi M, El-Hajj FG (2005) Impact of anthropometric, lifestyle, and body composition variables on ultrasound measurements in school children. Bone 36:736–742

    Article  PubMed  Google Scholar 

  31. Baroncelli GI, Federico G, Vignolo M, Valerio G, del Puente A, Maghnie M, Baserga M, Farello G, Saggese G (2006) Cross-sectional reference data for phalangeal quantitative ultrasound from early childhood to young-adulthood according to gender, age, skeletal growth, and pubertal development. Bone 39:159–173

    Article  PubMed  Google Scholar 

  32. Wang QJ, Nicholson PHF, Timonen J, Alen M, Moilanen P, Suominen H, Cheng SL (2008) Monitoring bone growth using quantitative ultrasound in comparison with DXA and pQCT. J Clin Densitom 11:295–301

    Article  PubMed  Google Scholar 

  33. Prais D, Diamond G, Kattan A, Salzberg J, Inbar D (2008) The effect of calcium intake and physical activity on bone quantitative ultrasound measurements in children: a pilot study. J Bone Miner Metab 26:248–253

    Article  PubMed  CAS  Google Scholar 

  34. Zadik Z, Price D, Diamond G (2003) Pediatric reference curves for multi-site quantitative ultrasound and its modulators. Osteoporos Int 14:857–862

    Article  PubMed  Google Scholar 

  35. Christoforidis A, Papadopoulou E, Dimitriadou M, Stilpnopoulou D, Gkogka C, Katzos G, Thanassiou-Metaxa M (2009) Reference values for quantitative ultrasonography (QUS) of radius and tibia in healthy Greek pediatric population: clinical correlations. J Clin Densitom 12:360–368

    Article  PubMed  Google Scholar 

  36. Ahrens W, Bammann K, Siani A, Buchecker K, De Henauw S, Iacoviello L, Hebestreit A, Krogh V, Lissner L, Marild S, Molnar D, Moreno LA, Pitsiladis Y, Reisch L, Tornaritis M, Veidebaum T, Pigeot I, on behalf of the IDEFICS Consortium (2011) The IDEFICS cohort: design, characteristics and participation in the baseline survey. Int J Obes 35:S3–S15

    Article  Google Scholar 

  37. Stomfai S, Ahrens W, Bammann K, Kovacs E, Marild S, Michels N, Moreno LA, Pohlabeln H, Siani A, Tornaritis M, Veidebaum T, Molnar D (2011) Intra- and inter-observer reliability in anthropometric measurements in children. Int J Obes 35:S45–S51

    Article  Google Scholar 

  38. Cole TJ, Freeman JV, Preece MA (1998) British 1990 growth reference centiles for weight, height, body mass index and head circumference fitted by maximum penalized likelihood. Stat Med 17:407–429

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  40. Tyrrell VJ, Richards G, Hofman P, Gillies GF, Robinson E, Cutfield WS (2001) Foot-to-foot bioelectrical impedance analysis: a valuable tool for the measurement of body composition in children. Int J Obes 25:273–278

    Article  CAS  Google Scholar 

  41. Marfell-Jones M, Olds T, Stewart A, Carter L (2006) International standards for anthropometric assessment. ISAK, Potchefstroom

    Google Scholar 

  42. Zebaze RMD, Brooks E, High M, Duty E, Bronson W (2003) Reproducibility of heel ultrasound measurement in prepubescent children—lack of influence of ethnicity, sex, or body size. J Ultrasound Med 22:1337–1340

    PubMed  Google Scholar 

  43. Economos CD, Sacheck JM, Wacker W, Shea K, Naumova EN (2007) Precision of Lunar Achilles plus bone quality measurements: time dependency and multiple machine use in field studies. Br J Radiol 80:919–925

    Article  PubMed  CAS  Google Scholar 

  44. Hans D, Schott AM, Chapuy MC, Benamar M, Kotzki PD, Cormier C, Pouilles JM, Meunier PJ (1994) Ultrasound measurements on the os calcis in a prospective multicenter study. Calcif Tissue Int 55:94–99

    Article  PubMed  CAS  Google Scholar 

  45. Hasanoglu A, Bideci A, Cinaz P, Tumer L, Unal S (2000) Bone mineral density in childhood obesity. J Pediatr Endocrinol Metab 13:307–311

    Article  PubMed  CAS  Google Scholar 

  46. Babaroutsi E, Magkos F, Manios Y, Sidossis LS (2005) Body mass index, calcium intake, and physical activity affect calcaneal ultrasound in healthy Greek males in an age-dependent and parameter-specific manner. J Bone Miner Metab 23:157–166

    Article  PubMed  Google Scholar 

  47. van den Bergh JP, Noordam C, Ozyilmaz A, Hermus AR, Smals AG, Otten BJ (2000) Calcaneal ultrasound imaging in healthy children and adolescents: relation of the ultrasound parameters BUA and SOS to age, body weight, height, foot dimensions and pubertal stage. Osteoporos Int 11:967–976

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was done as part of the IDEFICS Study (http://www.idefics.eu). We gratefully acknowledge the financial support of the European Community within the Sixth RTD Framework Programme (contract 016181, FOOD). We also thank the IDEFICS children and their parents who generously volunteered and participated in this project. I. S. is financially supported by the Research Foundation—Flanders (Grant 1.2.683.11.N.00). The information in this document reflects the authors’ view and is provided as is.

Author information

Authors and Affiliations

  1. Department of Public Health, Ghent University, UZ 2 Blok A, De Pintelaan 185, 9000, Ghent, Belgium

    Isabelle Sioen & Stefaan De Henauw

  2. FWO, Research Foundation Flanders, Egmontstraat 5, 1000, Brussels, Belgium

    Isabelle Sioen

  3. GENUD (Growth, Exercise, Nutrition and Development) Research Group, University of Zaragoza, C/Corona de Aragon 42, 50009, Zaragoza, Spain

    Theodora Mouratidou & Luis A. Moreno

  4. BIPS—Institute for Epidemiology and Prevention Research, Achterstrasse 30, 28359, Bremen, Germany

    Diana Herrmann & Wolfgang Ahrens

  5. Department of Health Sciences, Vesalius, University College Ghent, Keramiekstraat 80, 9000, Ghent, Belgium

    Stefaan De Henauw

  6. Department of Endocrinology, Ghent University, UZ-K12, De Pintelaan 185, 9000, Ghent, Belgium

    Jean-Marc Kaufman

  7. Unit for Osteoporosis and Metabolic Bone Diseases, Ghent University Hospital, UZ-K12, De Pintelaan 185, 9000, Ghent, Belgium

    Jean-Marc Kaufman

  8. Department of Pediatrics, University of Pécs, 7 József Attila St., Pecs, 7623, Hungary

    Dénes Molnár

  9. Department of Pediatrics, Institute of Clinical Sciences, The Queen Silvia Children’s Hospital, Sahlgrenska Academy at University of Gothenburg, 416 85, Göteborg, Sweden

    Staffan Marild

  10. Epidemiology & Population Genetics, Institute of Food Sciences, CNR, Via Roma 64, 83100, Avellino, AV, Italy

    Gianvincenzo Barba & Alfonso Siani

  11. Research Laboratories, Fondazione di Ricerca e Cura “Giovanni Paolo II”, Università Cattolica del Sacro Cuore, Largo A. Gemelli 1, 86100, Campobasso, CB, Italy

    Francesco Gianfagna

  12. Research and Education Institute of Child Health, 8 Attikis St., 2027, Strovolos, Cyprus

    Michael Tornaritis

  13. National Institute for Health Development, Tervise Arengu Instituut, Hiiu 42, 11619, Tallinn, Estonia

    Toomas Veidebaum

  14. Institute for Statistics, University of Bremen, Bibliothekstraße 1, 28359, Bremen, Germany

    Wolfgang Ahrens

Authors
  1. Isabelle Sioen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Theodora Mouratidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diana Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefaan De Henauw
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Marc Kaufman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dénes Molnár
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luis A. Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Staffan Marild
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gianvincenzo Barba
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alfonso Siani
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Francesco Gianfagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Michael Tornaritis
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Toomas Veidebaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Wolfgang Ahrens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Sioen.

Additional information

This study was conducted on behalf of the IDEFICS Consortium.

The authors have stated that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sioen, I., Mouratidou, T., Herrmann, D. et al. Relationship Between Markers of Body Fat and Calcaneal Bone Stiffness Differs Between Preschool and Primary School Children: Results from the IDEFICS Baseline Survey. Calcif Tissue Int 91, 276–285 (2012). https://doi.org/10.1007/s00223-012-9640-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-012-9640-3

Keywords

Search

Navigation