Bone Turnover Markers and Lean Mass in Pubescent Boys: Comparison Between Elite Soccer Players and Controls

in Pediatric Exercise Science

Click name to view affiliation

Ammar Nebigh Sousse University

Search for other papers by Ammar Nebigh in
Current site
Google Scholar
PubMed Close
*
,
Mohamed Elfethi Abed Sfax University

Search for other papers by Mohamed Elfethi Abed in
Current site
Google Scholar
PubMed Close
*
,
Rihab Borji Sfax University

Search for other papers by Rihab Borji in
Current site
Google Scholar
PubMed Close
*
,
Sonia Sahli Sfax University

Search for other papers by Sonia Sahli in
Current site
Google Scholar
PubMed Close
*
,
Slaheddine Sellami La Rabta Hospital Tunis

Search for other papers by Slaheddine Sellami in
Current site
Google Scholar
PubMed Close
*
,
Zouhair Tabka Sousse University

Search for other papers by Zouhair Tabka in
Current site
Google Scholar
PubMed Close
*
, and
Haithem Rebai Sfax University

Search for other papers by Haithem Rebai in
Current site
Google Scholar
PubMed Close
*
DOI:
https://doi.org/10.1123/pes.2017-0090
Keywords:
BMD; BMC; bone metabolic markers
In Print:
Volume 29: Issue 4
Page Range:
513–519
Restricted access

The aim of this study was to examine the relationship between bone mass and bone turnover markers with lean mass (LM) in pubescent soccer players. Two groups participated in this study, which included 65 elite young soccer players who trained for 6–8 hours per week and 60 controls. Bone mineral density; bone mineral content in the whole body, lower limbs, lumbar spine, and femoral neck; biochemical markers of osteocalcin; bone-specific alkaline phosphatase; C-telopeptide type I collagen; and total LM were assessed. Young soccer players showed higher bone mineral density and bone mineral content in the whole body and weight-bearing sites (P < .001). Indeed, the total LM correlated with whole-body bone mineral density and bone mineral content (P < .001). There were significant differences within the bone formation markers and osteocalcin (formation)/C-telopeptide type I collagen (resorption) ratio between young soccer players compared with the control group, but no significant difference in C-telopeptide type I collagen was observed between the 2 groups. This study showed a significant positive correlation among bone-specific alkaline phosphatase, osteocalcin, and total LM (r = .29; r = .31; P < .05) only for the young soccer players. Findings of this study highlight the importance of soccer practice for bone mineral parameters and bone turnover markers during the puberty stage.

Nebigh and Tabka are with the Research Unit: Physiology of Exercise and Pathophysiology of Molecular Integration “Biology Medicine and Health,” 12ES06, Faculty of Medicine Ibn El Jazzar, Sousse University, Sousse, Tunisia. Abed, Borji, Sahli, and Rebai are with the Research Unit: Education, Motricity, Sports and Health, UR15JS01, High Institute of Sport and Physical Education, Sfax University, Sfax, Tunisia. Sellami is with the Dept. of Rheumatology, La Rabta Hospital Tunis, Tunis, Tunisia.

Address author correspondence to Ammar Nebigh at ammarnebigh@yahoo.fr.
  • Collapse
  • Expand

Pediatric Exercise Science

Cover Pediatric Exercise Science
  • 1.

    Arabi A, Tamim H, Nabulsi M, et al. Sex differences in the effect of body-composition variables on bone mass in healthy children and adolescents. Am J Clin Nutr. 2004;80(5):1428–35. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Banfi G, Lombardi G, Colombini A, Lippi G. Bone metabolism markers in sports medicine. Sports Med. 2010;40(8):697–714. PubMed doi:10.2165/11533090-000000000-00000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. 2002;30:781–6. PubMed doi:10.1016/S8756-3282(02)00707-X

  • 4.

    Chaari H, Zouch M, Denguezli M, Bouajina E, Zaouali M, Tabka Z. A high level of volleyball practice enhances bone formation markers and hormones in prepubescent boys. Biol Sport. 2012;29(4):57–63. doi:10.5604/20831862.1019894

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Chaari H, Zouch M, Zribi A, Bouajina E, Zaouali M, Tabka Z. Specific sites of bone expansion depend on the level of volleyball practice in prepubescent boys. Biol Sport. 2013;30(3):229–34. PubMed doi:10.5604/20831862.1059297

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Chahla SE, Frohnert BI, Thomas W, et al. Higher daily physical activity is associated with higher osteocalcin levels in adolescents. Prev Med Rep. 2015;2:568–71. PubMed doi:10.5604/20831862.1059297

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Eriksen EF. Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord. 2010;11(4):219–27. PubMed doi:10.1007/s11154-010-9153-1

  • 8.

    Frost HM. Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol. 2003;275(2):1081–101. PubMed doi:10.1002/ar.a.10119

  • 9.

    Gil S, Ruiz F, Irazusta A, Gil J, Irazusta J. Selection of young soccer players in terms of anthropometric and physiological factors. J Sports Med Phys Fitness. 2007;47:25–32. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Gracia-Marco L, Ortega FB, Jiménez-Pavón D, et al. Contribution of bone turnover markers to bone mass in pubertal boys and girls. J Pediatr Endocrinol Metab. 2011;24(11–12):971–4. PubMed doi:10.1515/JPEM.2011.326

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact. 2010;10:64–70. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Helge EW, Aagaard P, Jakobsen MD, et al. Recreational football training decreases risk factors for bone fractures in untrained premenopausal women. Scand J Med Sci Sports. 2010;20:31–9. PubMed doi:10.1111/j.1600-0838.2010.01107.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Helge EW, Andersen TR, Schmidt JF, et al. Recreational football improves bone mineral density and bone turnover marker profile in elderly men. Scand J Med Sci Sports. 2014;24:98–104. PubMed doi:10.1111/sms.12239

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Hu M, Finni T, Xu L, Zou L, Cheng S. Effects of resistance training on biomarkers of bone formation and association with red blood cell variables. J Physiol Biochem. 2011;67:351–58. PubMed doi:10.1007/s13105-011-0082-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Kalai E, Bahlous A, Nbigh A, Sahli H, Sellami S, Abdelmoula J. Effect of physical activity on bone turnover in young boys. Ann Biol Clin. 2007;65:519–24. PubMed

    • Search Google Scholar
    • Export Citation
  • 16.

    Khadilkar AV, Sanwalka N, Mughal MZ, Chiplonkar S, Khadilkar V. Indian girls have higher bone mineral content per unit of lean body than boys through puberty. J Bone Miner Metab. 2017. PubMed doi:10.1007/s00774-017-0843-6

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Krustrup P, Nielsen JJ, Krustrup BR, et al. Recreational soccer is an effective health-promoting activity for untrained men. Br J Sports Med. 2009;43:825–31. PubMed doi:10.1136/bjsm.2008.053124

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Lehtonen-Veromaa M, Mottonen T, Irjala K, Nuotio I, Leino A, Viikari J. A 1-year prospective study on the relationship between physical activity, markers of bone metabolism, and bone acquisition in peripubertal girls. J Clin Endocrinol Metab. 2000;85(10):3726–32. PubMed doi:10.1210/jcem.85.10.6889

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Mackelvie KJ, Khan KM, Mckay HA. Is there a critical period for bone response to weight-bearing exercise in children and adolescents? A systematic review. Br J Sports Med. 2002;36:250–7. PubMed doi:10.1136/bjsm.36.4.250

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Maïmoun L, Lumbroso S, Manetta J, Paris F, Leroux JL, Sultan C. Testosterone is significantly reduced in endurance athletes without impact on bone mineral density. Horm Res. 2003;59(6):285–92. PubMed

    • Search Google Scholar
    • Export Citation
  • 21.

    Maïmoun L, Sultan CH. Effects of physical activity on bone remodelling. Metabolism. 2011;60:373–88. PubMed doi:10.1016/j.metabol.2010.03.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Malina RM, Eisenmann JC, Cumming SP, Horta L, Rodrigues J, Miller R. Height, mass and skeletal maturity of elite Portuguese soccer players aged 11-16 years. J Sports Sci. 2000;18:685–93. PubMed doi:10.1080/02640410050120069

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Markou KB, Theodoropoulou A, Tsekouras A, Vagenakis AG, Georgopoulos NA. Bone acquisition during adolescence in athletes. Ann N Y Acad Sci. 2010;1205:12–6. PubMed doi:10.1111/j.1749-6632.2010.05675.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Mohr M, Helge EW, Petersen LF, et al. Effects of soccer vs swim training on bone formation in sedentary middle-aged women. Eur J Appl Physiol. 2015;115(12):2671–9. PubMed doi:10.1007/s00421-015-3231-8

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Nebigh A, Rebai H, Elloumi M, et al. Bone mineral density of young boy soccer players at different pubertal stages: relationships with hormonal concentration. Joint Bone Spine. 2009;76:63–9. PubMed doi:10.1016/j.jbspin.2008.03.002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Nemet D, Eliakim A. Growth hormone-insulin-like growth factor-1 and inflammatory response to a single exercise bout in children and adolescents. Med Sport Sci. 2010;55:141–55. PubMed doi:10.1159/000321978

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Rizzoli R, Bianchi ML, Garabedian M, et al. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46(2):294–305. PubMed doi:10.1016/j.bone.2009.10.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Silva CC, Goldberg TB, Nga HS, et al. Impact of skeletal maturation on bone metabolism biomarkers and bone mineral density in healthy Brazilian male adolescents. J Pediatr (Rio J). 2011;87(5):450–6. PubMed doi:10.2223/JPED.2125

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Soden SE, Garrison CB, Egan AM, Beckwith AM. Nutrition, physical activity, and bone mineral density in youth with autistic spectrum disorders. J Dev Behav Pediatr. 2012;33(8):618–24. PubMed doi:10.1097/DBP.0b013e318260943c

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Soderman K, Bergstrom E, Lorentzon R, Alfredson H. Bone mass and muscle strength in young female soccer players. Calcif Tissue Int. 2000;67:297–303. PubMed doi:10.1007/s002230001149

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Tanner JM. Physical growth and development. In: Forfar JO, Arnell CC, editors. Textbook of Pediatrics. 2nd ed. Scotland, UK: Churchill Livingstone; 1988: pp. 249–303.

    • Search Google Scholar
    • Export Citation
  • 32.

    Tobias JH, Gould V, Brunton L, et al. Physical activity and bone: may the force be with you. Front Endocrinol. 2014;5:20. PubMed doi:10.3389/fendo.2014.00020

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Tosun A, Bölükbasi N, Cingi E, Beyazova M, Unlü M. Acute effects of a single session of aerobic exercise with or without weight-lifting on bone turnover in healthy young women. Mod Rheumatol. 2006;16(5):300–4. PubMed doi:10.3109/s10165-006-0503-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Vicente-Rodriguez G. How does exercise affect bone development during growth? Sport Med. 2006;36:561–9. PubMed doi:10.2165/00007256-200636070-00002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Vicente-Rodriguez G, Ara I, Perez-Gomez J, Dorado C, Calbet JA. Muscular development and physical activity as major determinants of femoral bone mass acquisition during growth. Br J Sports Med. 2005;39(9):611–6. PubMed doi:10.1136/bjsm.2004.014431

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Vicente-Rodriguez G, Jimenez-Ramirez J, Ara I, Serrano-Sanchez JA, Dorado C, Calbet JA. Enhanced bone mass and physical fitness in prepubescent footballers. Bone. 2003;33(5):853–9. PubMed doi:10.1016/j.bone.2003.08.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Yïlmaz D, Erosy B, Bilgin E, Gümüşer G, Onur E, Pinar ED. Bone mineral density in girls and boys at different pubertal stages: relation with gonadal steroids, bone formation markers, and growth parameters. J Bone Miner Metab. 2005;23:476–82. PubMed doi:10.1007/s00774-005-0631-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Zouch M, Jaffré C, Thomas T, et al. Long-term soccer practice increases bone mineral content gain in prepubescent boys. Joint Bone Spine. 2008;75:41–9. PubMed doi:10.1016/j.jbspin.2006.12.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Zouch M, Zribi A, Alexandre C, et al. Soccer increases bone mass in prepubescent boys during growth: a 3-yr longitudinal study. J Clin Densitom. 2015;18(2):179–86. PubMed doi:10.1016/j.jocd.2014.10.004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Zribi A, Zouch M, Chaari H, et al. Enhanced bone mass and physical fitness in prepubescent basketball players. J Clin Densitom. 2014;17(1):156–62. PubMed doi:10.1016/j.jocd.2013.04.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Zribi A, Zouch M, Chaari H, et al. Short-term lower-body plyometric training improves whole body BMC, bone metabolic markers, and physical fitness in early pubertal male basketball players. Pediatr Exerc Sci. 2014;26(1):22–32. PubMed doi:10.1123/pes.2013-0053

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 1686 365 6
Full Text Views 14 11 1
PDF Downloads 8 5 0