Archives of Osteoporosis

, 13:11 | Cite as

Bone metabolism markers and vitamin D in adolescent cyclists

  • Hugo Olmedillas
  • Alejandro Gonzalez-Agüero
  • Marta Rapún-López
  • Luis Gracia-Marco
  • Alba Gomez-Cabello
  • Francisco Pradas de la Fuente
  • Luís A. Moreno
  • José A. Casajús
  • Germán Vicente-Rodríguez
Original Article

Abstract

Summary

This study aimed to describe bone metabolic activity in adolescent competitive cyclists compared to age-matched controls. The main result is that younger subjects present a higher bone turnover than the older ones. Moreover, cyclists under the age of 17 have higher scores on all markers than age-matched controls.

Purpose

The purpose of this study was to describe bone metabolic activity in adolescent competitive cyclists compared to age-matched controls.

Methods

Twenty-two male adolescent cyclists between 14 and 20 years (y) and 20 age-matched controls participated in this study. Serum osteocalcin (OC), aminoterminal propeptide of type I procollagen (PINP), and β-isomerized C-telopeptides (β-CTX) were analyzed by electrochemiluminescence immunoassay (ECLIA); plasma 25 hydroxyvitamin D [25(OH)D] was analyzed by enzyme-linked immunosorbent assay (ELISA).

Results

Analysis of variance revealed no significant differences in bone metabolism markers and vitamin D between cyclists and controls. Cyclists over 17 y had a significantly lower concentration in bone formation and resorption biochemical markers compared to cyclists under 17 y (all P < 0.05). Moreover, controls over 17 y presented lower concentration for PINP (P < 0.05) compared to their peers under 17 y. Comparisons between cyclists and controls under 17 y revealed higher concentrations of OC and PINP (P < 0.05) in cyclists. Group interaction by age was found for OC, PINP, and β-CTX (P < 0.01). Cyclists over 17 y had higher concentrations of [25(OH)D] (P < 0.05) than age-matched controls.

Conclusions

The present results support the idea that cycling during adolescence may be associated to a decrease in bone turnover that may affect bone health later in life.

Keywords

Cyclists Adolescence Bone turnover Osteocalcin Vitamin D 

Notes

Acknowledgments

We wish to thank the controls, cyclists, and their coaches for their diligence and cooperation throughout this study.

Compliance with ethical standards

Written informed consent was obtained from parents and adolescents. The study was performed following the ethical guidelines of the Declaration of Helsinki 1961 (2000 Edinburgh revision). The Ethics Committee of Clinical Research for the Government of Aragón (CEICA; Spain) approved the study protocol.

References

  1. 1.
    Ferrari S (2005) Osteoporosis: a complex disorder of aging with multiple genetic and environmental determinants. Nutrition and fitness: mental health, aging, and the implementation of a healthy diet and physical activity lifestyle Karger Publishers. p. 35–51.Google Scholar
  2. 2.
    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 Min Res: Off J Am Soc Bone Min Res 14(10):1672–1679.  https://doi.org/10.1359/jbmr.1999.14.10.1672. CrossRefGoogle Scholar
  3. 3.
    Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009) Exercise and bone mass in adults. Sports Med 39(6):439–468.  https://doi.org/10.2165/00007256-200939060-00002 CrossRefPubMedGoogle Scholar
  4. 4.
    Rico H, Revilla M, Villa LF, Hernandez ER, Alvarez de Buergo M, Villa M (1993) Body composition in children and Tanner’s stages: a study with dual-energy x-ray absorptiometry. Metabolism 42(8):967–970.  https://doi.org/10.1016/0026-0495(93)90008-C CrossRefPubMedGoogle Scholar
  5. 5.
    Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC, Bonjour JP (1992) Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 75(4):1060–1065.  https://doi.org/10.1210/jcem.75.4.1400871 PubMedGoogle Scholar
  6. 6.
    Maïmoun L, Mariano-Goulart D, Couret I, Manetta J, Peruchon E, Micallef JP, Verdier R, Rossi M, Leroux JL (2004) Effects of physical activities that induce moderate external loading on bone metabolism in male athletes. J Sports Sci 22(9):875–883.  https://doi.org/10.1080/02640410410001716698 CrossRefPubMedGoogle Scholar
  7. 7.
    Pettersson U, Nordstrom P, Lorentzon R (1999) A comparison of bone mineral density and muscle strength in young male adults with different exercise level. Calcif Tissue Int 64(6):490–498.  https://doi.org/10.1007/s002239900639 CrossRefPubMedGoogle Scholar
  8. 8.
    Dyson K, Blimkie CJ, Davison KS, Webber CE, Adachi JD (1997) Gymnastic training and bone density in pre-adolescent females. Med Sci Sports Exerc 29(4):443–450.  https://doi.org/10.1097/00005768-199704000-00004 CrossRefPubMedGoogle Scholar
  9. 9.
    Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ (1995) A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 17(3):205–210.  https://doi.org/10.1016/8756-3282(95)00171-9 CrossRefPubMedGoogle Scholar
  10. 10.
    Grimston SK, Willows ND, Hanley DA (1993) Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc 25(11):1203–1210PubMedGoogle Scholar
  11. 11.
    Nevill A, Holder R, Stewart A (2004) Do sporting activities convey benefits to bone mass throughout the skeleton? J Sports Sci 22(7):645–650.  https://doi.org/10.1080/02640410310001655769 CrossRefPubMedGoogle Scholar
  12. 12.
    Olmedillas H, Gonzalez-Aguero A, Moreno LA, Casajus JA, Vicente-Rodriguez G (2012) Cycling and bone health: a systematic review. BMC Med 10(1):168.  https://doi.org/10.1186/1741-7015-10-168 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Barry DW, Kohrt WM (2008) BMD decreases over the course of a year in competitive male cyclists. J Bone Min Res: Off J Am Soc Bone Min Res 23(4):484–491.  https://doi.org/10.1359/jbmr.071203. CrossRefGoogle Scholar
  14. 14.
    Smathers AM, Bemben MG, Bemben DA (2009) Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc 41(2):290–296.  https://doi.org/10.1249/MSS.0b013e318185493e CrossRefPubMedGoogle Scholar
  15. 15.
    Warner SE, Shaw JM, Dalsky GP (2002) Bone mineral density of competitive male mountain and road cyclists. Bone 30(1):281–286.  https://doi.org/10.1016/S8756-3282(01)00704-9 CrossRefPubMedGoogle Scholar
  16. 16.
    Nagle KB, Brooks MA (2011) A systematic review of bone health in cyclists. Sports Health 3(3):235–243.  https://doi.org/10.1177/1941738111398857 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Beatty T, Webner D, Collina SJ (2010) Bone density in competitive cyclists. Curr Sports Med Reports 9(6):352–355.  https://doi.org/10.1249/JSR.0b013e3181ffe794 CrossRefGoogle Scholar
  18. 18.
    Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R (2002) Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 34(2):286–294.  https://doi.org/10.1097/00005768-200202000-00017 CrossRefPubMedGoogle Scholar
  19. 19.
    Medelli J, Lounana J, Menuet JJ, Shabani M, Cordero-MacIntyre Z (2009) Is osteopenia a health risk in professional cyclists? J Clin Densitom : Off J Int Soc Clin Densitom 12(1):28–34.  https://doi.org/10.1016/j.jocd.2008.07.057. CrossRefGoogle Scholar
  20. 20.
    Olmedillas H, Gonzalez-Aguero A, Moreno LA, Casajus JA, Vicente-Rodriguez G (2011) Bone related health status in adolescent cyclists. PLoS One 6(9):e24841.  https://doi.org/10.1371/journal.pone.0024841 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wilks DC, Gilliver SF, Rittweger J (2009) Forearm and tibial bone measures of distance- and sprint-trained master cyclists. Med Sci Sports Exerc 41(3):566–573.  https://doi.org/10.1249/MSS.0b013e31818a0ec8 CrossRefPubMedGoogle Scholar
  22. 22.
    Seibel MJ (2005) Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 26(4):97–122PubMedPubMedCentralGoogle Scholar
  23. 23.
    Banfi G, Lombardi G, Colombini A, Lippi G (2010) Bone metabolism markers in sports medicine. Sports Med 40(8):697–714.  https://doi.org/10.2165/11533090-000000000-00000. CrossRefPubMedGoogle Scholar
  24. 24.
    Vasikaran SD, Morris HA, Cooper C, Kanis JA (2011) Standardising biochemical assessment of bone turnover in osteoporosis. Clin Biochem 44(13):1033–1034.  https://doi.org/10.1016/j.clinbiochem.2011.07.001 CrossRefPubMedGoogle Scholar
  25. 25.
    Lehtonen-Veromaa M, Möttönen T, Svedström E, Hakola P, Heinonen O, Viikari J (2000) Physical activity and bone mineral acquisition in peripubertal girls. Scand J Med Sci Sports 10(4):236–243.  https://doi.org/10.1034/j.1600-0838.2000.010004236.x CrossRefPubMedGoogle Scholar
  26. 26.
    Hinton PS, Rolleston A, Rehrer NJ, Hellemans IJ, Miller BF (2010) Bone formation is increased to a greater extent than bone resorption during a cycling stage race. Appl Physiol, Nutr Metab = Physiologie appliquee, nutrition et metabolisme 35(3):344–349.  https://doi.org/10.1139/H10-025. CrossRefPubMedGoogle Scholar
  27. 27.
    Lombardi G, Lanteri P, Graziani R, Colombini A, Banfi G, Corsetti R (2012) Bone and energy metabolism parameters in professional cyclists during the Giro d’Italia 3-weeks stage race. PLoS One 7(7):e42077.  https://doi.org/10.1371/journal.pone.0042077 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cashman K (2002) Calcium intake, calcium bioavailability and bone health. Br J Nutr 87(S2):S169–SS77.  https://doi.org/10.1079/BJN/2002534 CrossRefPubMedGoogle Scholar
  29. 29.
    Zerwekh JE (2008) Blood biomarkers of vitamin D status. Am J Clin Nutr 87(4):1087S–1091SPubMedGoogle Scholar
  30. 30.
    Holick MF (2004) Vitamin D: importance in the prevention of cancers, type 1 diabetes, heart disease, and osteoporosis. Am J Clin Nutr 79(3):362–371CrossRefPubMedGoogle Scholar
  31. 31.
    Cranney A, Weiler HA, O'Donnell S, Puil L (2008) Summary of evidence-based review on vitamin D efficacy and safety in relation to bone health. Am J Clin Nutr 88(2):513S–519SPubMedGoogle Scholar
  32. 32.
    Valtuena J, Gracia-Marco L, Vicente-Rodriguez G, Gonzalez-Gross M, Huybrechts I, Rey-Lopez J et al (2012) Vitamin D status and physical activity interact to improve bone mass in adolescents. The HELENA study. Osteoporos Int 23(8):2227–2237.  https://doi.org/10.1007/s00198-011-1884-7 CrossRefPubMedGoogle Scholar
  33. 33.
    Gomez-Bruton A, Gonzalez-Aguero A, Olmedillas H, Gomez-Cabello A, Matute-Llorente A, Julian-Almarcegui C et al (2013) Do calcium and vitamin D intake influence the effect of cycling on bone mass through adolescence? Nutricion Hospitalaria 28(4):1136–1139.  https://doi.org/10.3305/nh.2013.28.4.6490. PubMedGoogle Scholar
  34. 34.
    Zhu K, Oddy WH, Holt P, Ping-Delfos WCS, Mountain J, Lye S, Pennell C, Hart PH, Walsh JP (2017) Tracking of vitamin D status from childhood to early adulthood and its association with peak bone mass. Am J Clin Nutr 106(1):276–283.  https://doi.org/10.3945/ajcn.116.150524 CrossRefPubMedGoogle Scholar
  35. 35.
    Mora S, Pitukcheewanont P, Kaufman FR, Nelson JC, Gilsanz V (1999) Biochemical markers of bone turnover and the volume and the density of bone in children at different stages of sexual development. J Bone Miner Res 14(10):1664–1671.  https://doi.org/10.1359/jbmr.1999.14.10.1664 CrossRefPubMedGoogle Scholar
  36. 36.
    Gracia-Marco L, Vicente-Rodriguez G, Valtuena J, Rey-Lopez J, Diaz Martinez A, Mesana M et al (2010) Bone mass and bone metabolism markers during adolescence: the HELENA study. Horm Res Paediatr 74(5):339–350.  https://doi.org/10.1159/000314965 CrossRefPubMedGoogle Scholar
  37. 37.
    Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R (2004) The ‘muscle-bone unit’ during the pubertal growth spurt. Bone 34(5):771–775.  https://doi.org/10.1016/j.bone.2004.01.022 CrossRefPubMedGoogle Scholar
  38. 38.
    Maimoun L, Coste O, Mura T, Philibert P, Galtier F, Mariano-Goulart D et al (2013) Specific bone mass acquisition in elite female athletes. J Clin Endocrinol Metab 98(7):2844–2853.  https://doi.org/10.1210/jc.2013-1070 CrossRefPubMedGoogle Scholar
  39. 39.
    Barrack MT, Van Loan MD, Rauh MJ, Nichols JF (2010) Physiologic and behavioral indicators of energy deficiency in female adolescent runners with elevated bone turnover. Am J Clin Nutr 92(3):652–659.  https://doi.org/10.3945/ajcn.2009.28926. CrossRefPubMedGoogle Scholar
  40. 40.
    Garnero P (1999) Biochemical markers of bone turnover: recent data and avenues for the future. Revue du rhumatisme (English ed) 66(11):538–542Google Scholar
  41. 41.
    Lombardi G, Lanteri P, Graziani R, Colombini A, Banfi G, Corsetti R (2012) Bone and energy metabolism parameters in professional cyclists during the Giro d’Italia 3-weeks stage race. PLoS One 7(7):e42077.  https://doi.org/10.1371/journal.pone.0042077 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Guillemant J, Accarie C, Peres G, Guillemant S (2004) Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int 74(5):407–414.  https://doi.org/10.1007/s00223-003-0070-0 CrossRefPubMedGoogle Scholar
  43. 43.
    Seeman E (2002) Pathogenesis of bone fragility in women and men. Lancet 359(9320):1841–1850.  https://doi.org/10.1016/S0140-6736(02)08706-8 CrossRefPubMedGoogle Scholar
  44. 44.
    González-Agüero A, Olmedillas H, Gómez-Cabello A, Casajús JA, Vicente-Rodríguez G (2016) Bone structure and geometric properties at the radius and tibia in adolescent endurance-trained cyclists. Clin J Sport Med: Off J Can Acad Sport MedGoogle Scholar
  45. 45.
    Slemenda CW, Peacock M, Hui S, Zhou L, Johnston CC (1997) Reduced rates of skeletal remodeling are associated with increased bone mineral density during the development of peak skeletal mass. J Bone Min Res: Off J Am Soc Bone Min Res 12(4):676–682.  https://doi.org/10.1359/jbmr.1997.12.4.676. CrossRefGoogle Scholar
  46. 46.
    Guillaume G, Chappard D, Audran M (2012) Evaluation of the bone status in high-level cyclists. J Clin Densitom : Off J Int Soc Clin Densitom 15(1):103–107.  https://doi.org/10.1016/j.jocd.2011.08.001. CrossRefGoogle Scholar
  47. 47.
    Pediatrics AAo (2012) Dietary reference intakes for calcium and vitamin D. Pediatrics 130(5):e1424-eCrossRefGoogle Scholar
  48. 48.
    Gomez-Bruton A, Gonzalez-Aguero A, Olmedillas H, Gomez-Cabello A, Matute-Llorente A, Julian-Almarcegui C et al (2013) Do calcium and vitamin D intake influence the effect of cycling on bone mass through adolescence? Nutr Hosp 28(4):1136–1139.  https://doi.org/10.3305/nh.2013.28.4.6490 PubMedGoogle Scholar
  49. 49.
    Nichols JF, Rauh MJ (2011) Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res 25(3):727–734.  https://doi.org/10.1519/JSC.0b013e3181c6a116 CrossRefPubMedGoogle Scholar
  50. 50.
    Chen TC, Chimeh F, Lu Z, Mathieu J, Person KS, Zhang A, Kohn N, Martinello S, Berkowitz R, Holick MF (2007) Factors that influence the cutaneous synthesis and dietary sources of vitamin D. Arch Biochem Biophys 460(2):213–217.  https://doi.org/10.1016/j.abb.2006.12.017 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Dressendorfer RH, Petersen SR, Lovshin SM, Keen CL (2002) Mineral metabolism in male cyclists during high-intensity endurance training. Int J Sport Nutr Exerc Metab 12(1):63–72.  https://doi.org/10.1123/ijsnem.12.1.63 CrossRefPubMedGoogle Scholar
  52. 52.
    Maimoun L, Manetta J, Couret I, Dupuy A, Mariano-Goulart D, Micallef J et al (2006) The intensity level of physical exercise and the bone metabolism response. Int J Sports Med 27(02):105–111.  https://doi.org/10.1055/s-2005-837621 CrossRefPubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • Hugo Olmedillas
    • 1
  • Alejandro Gonzalez-Agüero
    • 2
    • 3
    • 4
    • 5
    • 6
  • Marta Rapún-López
    • 7
  • Luis Gracia-Marco
    • 2
    • 8
  • Alba Gomez-Cabello
    • 2
    • 4
    • 5
    • 6
    • 9
  • Francisco Pradas de la Fuente
    • 7
  • Luís A. Moreno
    • 2
    • 4
    • 5
    • 6
    • 10
  • José A. Casajús
    • 2
    • 3
    • 4
    • 5
    • 6
  • Germán Vicente-Rodríguez
    • 2
    • 3
    • 4
    • 5
    • 6
  1. 1.Department of Functional BiologyUniversidad de Oviedo, Campus del Cristo B. Julián Clavería s/nAsturiasSpain
  2. 2.GENUD (Growth, Exercise, NUtrition and Development) Research GroupUniversidad de ZaragozaZaragozaSpain
  3. 3.Faculty of Health and Sport Sciences (FCSD), Department of Physiatry and NursingUniversity of ZaragozaHuescaSpain
  4. 4.Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y Nutrición (CIBERObn)Santiago de CompostelaSpain
  5. 5.Instituto Agroalimentario de Aragón (IA2)ZaragozaSpain
  6. 6.Instituto de Investigación Sanitaria de Aragón (IIS Aragón)ZaragozaSpain
  7. 7.Departamento de Expresión Musical, Plástica y Corporal, Facultad de Ciencias de la Salud y del DeporteUniversidad de ZaragozaHuescaSpain
  8. 8.PROFITH “PROmoting FITness and Health through physical activity” Research Group, Department of Physical Education and Sports, Faculty of Sport SciencesUniversity of GranadaGranadaSpain
  9. 9.Centro Universitario de la DefensaZaragozaSpain
  10. 10.Facultad de Ciencias de la SaludUniversidad de ZaragozaZaragozaSpain

Personalised recommendations