Journal of Bone and Mineral Metabolism

, Volume 26, Issue 3, pp 288–294 | Cite as

Physical fitness effect on bone mass is mediated by the independent association between lean mass and bone mass through adolescence: a cross-sectional study

  • Germán Vicente-Rodríguez
  • Alejandro Urzanqui
  • Maria Isabel Mesana
  • Francisco B. Ortega
  • Jonatan R. Ruiz
  • Juan Ezquerra
  • José A. Casajús
  • Gloria Blay
  • Vicente A. Blay
  • Marcela Gonzalez-Gross
  • Luis A. Moreno
  • AVENA-Zaragoza Study Group
Original Article

Abstract

We studied 278 adolescents (169 females) aged 13.0–18.5 years to elucidate whether an independent effect of physical fitness and lean mass in the differences between male and female bones can be detected. Lean and fat masses and bone mineral content (BMC) were measured with DXA. Physical fitness was evaluated with six different tests included in the EUROFIT test battery (flexibility, isometric, dynamic and endurance strength, speed, and cardiovascular fitness). To test the independent relationship between physical fitness and bone mass, multiple regression analysis was applied, including lean mass, age, and Tanner development as covariates. The males had a 43% lower fat mass and 40% and 16% higher lean mass and total BMC compared with the females (all P < 0.05). After adjustment for differences in body size and lean mass, the females exhibited a 7.4% higher BMC than the males (P < 0.05). The multiple regression analysis showed that lean mass had an independent relationship with bone mass (P < 0.001), explaining 67% of the total variance in whole-body BMC. In males, change in R2 was 0.658 for hand grip and 0.035–0.151 for the rest of physical fitness-related variables; but 0.019–0.042 in females (all P–0.001); however, the independent relationships between physical fitness and bone disappeared after controlling for lean mass. In conclusion, it is likely the differences between male and female in bone mass could be explained by differences in lean mass and physical fitness.

Key words

bone mineral content exercise soft tissues muscle growth 

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References

  1. 1.
    Cooper C (1999) Epidemiology of osteoporosis. Osteoporos Int 9: S2–S8.PubMedCrossRefGoogle Scholar
  2. 2.
    World Health Organization. Available at http://www.who.int/archives/world-health-day/dg_statement.pdf
  3. 3.
    Kelly PJ, Eisman JA, Sambrook PN (1990) Interaction of genetic and environmental influences on peak bone density. Osteoporos Int 1:56–60PubMedCrossRefGoogle Scholar
  4. 4.
    Heinonen A (2001) Biomechanics. In: Khan K, McKay H, Kannus P, Bailey D, Wark J, Bennell K (eds) Physical Activity and Bone Health. Human Kinetics, Champaign, IL, pp 23–34Google Scholar
  5. 5.
    Slemenda CW, Miller JZ, Hui SL, Reister TK, Johnston CC (1991) Role of physical activity in the development of skeletal mass in children. J Bone Miner Res 6:1227–1233PubMedGoogle Scholar
  6. 6.
    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 23:157–166PubMedCrossRefGoogle Scholar
  7. 7.
    Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the University of Saskatchewan bone mineral accrual study. J Bone Miner Res 14:1672–1679PubMedCrossRefGoogle Scholar
  8. 8.
    Gustavsson A, Thorsen K, Nordstrom P (2003) A 3-year longitudinal study of the effect of physical activity on the accrual of bone mineral density in healthy adolescent males. Calcif Tissue Int 73:108–114PubMedCrossRefGoogle Scholar
  9. 9.
    Vicente-Rodriguez G, Ara I, Perez-Gomez J, Dorado C, Serrano-Sanchez JA, Calbet JAL (2004) High femoral bone mineral density accretion in prepuberal football players. Med Sci Sports Exerc 33:1789–1795CrossRefGoogle Scholar
  10. 10.
    Uzunca K, Birtane M, Durmus-Altun G, Ustun F (2005) High bone mineral density in loaded skeletal regions of former professional football (soccer) players: what is the effect of time after active career? Br J Sports Med 39:154–157PubMedCrossRefGoogle Scholar
  11. 11.
    Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E (1998) Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res 13:500–507PubMedCrossRefGoogle Scholar
  12. 12.
    Bradney M, Pearce G, Naughton G, Sullivan C, Bass S, Beck T, Carlson J, Seeman E (1998) Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res 13:1814–1821PubMedCrossRefGoogle Scholar
  13. 13.
    Przeweda R, Dobosz J (2003) Growth and physical fitness of Polish youths in two successive decades. J Sports Med Phys Fitness 43:465–474PubMedGoogle Scholar
  14. 14.
    EUROFIT CoEoSR (1993) Handbook for the EUROFIT Test of Physical Fitness. StrasbourgGoogle Scholar
  15. 15.
    Ortega FB, Ruiz JR, Castillo MJ, Moreno LA, Gonzalez-Gross M, Warnberg J, Gutierrez A (2005) Low level of physical fitness in Spanish adolescents. Relevance for future cardiovascular health (AVENA study). Rev Esp Cardiol 58:898–909PubMedCrossRefGoogle Scholar
  16. 16.
    Vicente-Rodriguez G, Jimenez-Ramirez J, Ara I, Serrano-Sanchez JA, Dorado C, Calbet JA (2003) Enhanced bone mass and physical fitness in prepubescent footballers. Bone (NY) 33:853–859Google Scholar
  17. 17.
    Vicente-Rodriguez G, Dorado C, Perez-Gomez J, Gonzalez-Henriquez JJ, Calbet JA (2004) Enhanced bone mass and physical fitness in young female handball players. Bone (NY) 35:1208–1215Google Scholar
  18. 18.
    Vicente-Rodriguez G, Ara I, Perez-Gomez J, Dorado C, Calbet JAL (2005) Muscular development and physical activity are major determinants of femoral bone mass acquisition during growth. Br J Sports Med 39:611–616PubMedCrossRefGoogle Scholar
  19. 19.
    Courteix D, Lespessailles E, Loiseau-Peres S, Obert P, Ferry B, Benhamou CL (1998) Lean tissue mass is a better predictor of bone mineral content and density than body weight in prepubertal girls. Rev Rhum Engl Ed 65:328–336PubMedGoogle Scholar
  20. 20.
    Kim J, Shen W, Gallagher D, Jones A Jr, Wang Z, Wang J, Heshka S, Heymsfield SB (2006) Total-body skeletal muscle mass: estimation by dual-energy X-ray absorptiometry in children and adolescents. Am J Clin Nutr 84:1014–1020PubMedGoogle Scholar
  21. 21.
    Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The ‘muscle-bone unit’ during the pubertal growth spurt. Bone (NY) 34:771–775Google Scholar
  22. 22.
    Schoenau E, Frost HM (2002) The “muscle-bone unit” in children and adolescents. Calcif Tissue Int 70:405–407PubMedCrossRefGoogle Scholar
  23. 23.
    Seeman E (2001) Clinical review 137: sexual dimorphism in skeletal size, density, and strength. J Clin Endocrinol Metab 86:4576–4584PubMedCrossRefGoogle Scholar
  24. 24.
    Moreno LA, Mesana MI, Fleta J, Ruiz JR, Gonzalez-Gross M, Sarria A, Marcos A, Bueno M (2005) Overweight, obesity and body fat composition in Spanish adolescents. The AVENA Study. Ann Nutr Metab 49:71–76PubMedCrossRefGoogle Scholar
  25. 25.
    Gonzalez-Gross M, Castillo MJ, Moreno L, Nova E, Gonzalez-Lamuno D, Perez-Llamas F, Gutierrez A, Garaulet M, Joyanes M, Leiva A, Marcos A (2003) Feeding and assessment of nutritional status of panish adolescents (AVENA study). Evaluation of risks and interventional proposal. I. Methodology. Nutr Hosp 18:15–28PubMedGoogle Scholar
  26. 26.
    Moreno LA, Fleta J, Mur L, Feja C, Sarria A, Bueno M (1997) Indices of body fat distribution in Spanish children aged 4.0 to 14.9 years. J Pediatr Gastroenterol Nutr 25:175–181PubMedCrossRefGoogle Scholar
  27. 27.
    Lunar (1993) LUNAR Operation Manual, Version 1.5e. Lunar Radiation Corp., Madison, WIGoogle Scholar
  28. 28.
    Instituto de Ciencias de la Educación Física y el Deporte (1992) EUROFIT. Test europeo de aptitud física. Ministerio de Educación y Ciencia, MadridGoogle Scholar
  29. 29.
    Leger LA, Mercier D, Gadoury C, Lambert J (1988) The multistage 20 metre shuttle run test for aerobic fitness. J Sports Sci 6:93–101.PubMedGoogle Scholar
  30. 30.
    Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone (NY) 35:973–981Google Scholar
  31. 31.
    Pietrobelli A, Faith MS, Wang J, Brambilla P, Chiumello G, Heymsfield SB (2002) Association of lean tissue and fat mass with bone mineral content in children and adolescents. Obes Res 10: 56–60PubMedCrossRefGoogle Scholar
  32. 32.
    Rodriguez Martinez G, Blay G, Blay VA, Moreno LA, Bueno M (2002) Association of fat mass with bone mineral content in female adolescents. Obes Res 10:715PubMedGoogle Scholar
  33. 33.
    Young D, Hopper JL, Macinnis RJ, Nowson CA, Hoang NH, Wark JD (2001) Changes in body composition as determinants of longitudinal changes in bone mineral measures in 8-to 26-year-old female twins. Osteoporos Int 12:506–515PubMedCrossRefGoogle Scholar
  34. 34.
    Jarvinen TL, Kannus P, Pajamaki I, Vuohelainen T, Tuukkanen J, Jarvinen M, Sievanen H (2003) Estrogen deposits extra mineral into bones of female rats in puberty, but simultaneously seems to suppress the responsiveness of female skeleton to mechanical loading. Bone (NY) 32:642–651Google Scholar
  35. 35.
    Weiss EP, Racette SB, Villareal DT, Fontana L, Steger-May K, Schechtman KB, Klein S, Ehsani AA, Holloszy JO (2007) Lower extremity muscle size and strength and aerobic capacity decrease with caloric restriction but not with exercise-induced weight loss. J Appl Physiol 102:634–640PubMedCrossRefGoogle Scholar
  36. 36.
    Ackerman A, Thornton JC, Wang J, Pierson RN Jr, Horlick M (2006) Sex difference in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity (Silver Spring) 14:819–825CrossRefGoogle Scholar
  37. 37.
    Wang Q, Alen M, Nicholson P, Suominen H, Koistinen A, Kroger H, Cheng S (2007) Weight-bearing, muscle loading and bone mineral accrual in pubertal girls: a 2-year longitudinal study. Bone (NY) 40:1196–1202Google Scholar
  38. 38.
    Komi PV (1992) Strength and Power in Sport. Blackwell, BostonGoogle Scholar
  39. 39.
    Faulkner RA, Bailey DA, Drinkwater DT, McKay HA, Arnold C, Wilkinson AA (1996) Bone densitometry in Canadian children 8–17 years of age. Calcif Tissue Int 59:344–351PubMedCrossRefGoogle Scholar
  40. 40.
    Lohman T, Going S, Pamenter R, Hall M, Boyden T, Houtkooper L, Ritenbaugh C, Bare L, Hill A, Aickin M (1995) Effects of resistance training on regional and total bone mineral density in premenopausal women: a randomized prospective study. J Bone Miner Res 10:1015–1024PubMedCrossRefGoogle Scholar
  41. 41.
    Van Praagh E, Dore E (2002) Short-term muscle power during growth and maturation. Sports Med 32:701–728PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2008

Authors and Affiliations

  • Germán Vicente-Rodríguez
    • 1
    • 2
  • Alejandro Urzanqui
    • 3
  • Maria Isabel Mesana
    • 1
  • Francisco B. Ortega
    • 4
  • Jonatan R. Ruiz
    • 4
  • Juan Ezquerra
    • 1
  • José A. Casajús
    • 1
    • 2
  • Gloria Blay
    • 3
  • Vicente A. Blay
    • 3
  • Marcela Gonzalez-Gross
    • 3
  • Luis A. Moreno
    • 1
  • AVENA-Zaragoza Study Group
  1. 1.University School of Health Science and Pediatrics DepartmentUniversity of ZaragozaZaragozaSpain
  2. 2.Faculty of Health and Sport Science, Department of Physiotherapy and NursingUniversity of ZaragozaHuescaSpain
  3. 3.Facultad de Ciencias de la Actividad Física y del DeporteUniversidad Politécnica de MadridMadridSpain
  4. 4.Departamento de Fisiología, Facultad de MedicinaUniversidad de GranadaGranadaSpain

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