Osteoporosis International

, Volume 30, Issue 2, pp 375–381 | Cite as

Effect of acute downhill running on bone markers in responders and non-responders

  • S. A. Alkahtani
  • S. M. Yakout
  • J.-Y. Reginster
  • N. M. Al-DaghriEmail author
Original Article



This study showed that procollagen type 1 amino-terminal pro-peptide and N-MID osteocalcin significantly increased after exercise independent of the form of muscle contraction. Thus, these preliminary results will be useful for future studies that will consider bone turnover characteristics of responders and non-responders to acute and chronic aerobic exercise.


The aim of the current study was to compare the effects of acute flat running (FR) and downhill running (DHR) on bone turnover markers in men.


Fourteen healthy young active men performed three exercise tests in a counterbalanced order, including rest condition, FR, and DHR, at 60% maximal aerobic capacity on a treadmill with 0 and − 12% inclines. Blood samples were taken in the pre-exercise, immediately post-exercise, and 24-h post-exercise periods, and bone markers included total procollagen type 1 amino-terminal pro-peptide (total PINP) and N-MID osteocalcin.


Total P1NP significantly increased after exercise independent of the form of muscle contraction (p > 0.05). N-MID osteocalcin increased after DHR by 17% compared to after pre-exercise, but the difference did not reach significance (p = 0.07; partial eta square, 0.21). Biomarker responses to exercise were dependent on the exercise form and independent of hormone type in half of the participants who were classified as responders. Physiological parameters and changes in muscle voluntary contraction did not explain the differences between responders and non-responders.


The effect of acute DHR on bone turnover is determined by biomarker type and participant characteristics. Future studies should discriminate between the characteristics of responders and those of non-responders.


Bone markers Downhill running Eccentric exercise Responders 



The authors thank all participants, the Cardiovascular Laboratory, and all research assistants, particularly Mr. Abdullah Al-Qawati and Mr. Thabit Al-Aizari. Blood samples were collected by Mr. Abdul Aziz Alsahali from the Department of Clinical Laboratory Sciences at College of Applied Medical Sciences at KSU. The statistical analysis was performed by Mr. Malak Nawaz Khan Khattak from the Prince Mutaib bin Abdullah Chair for Biomarkers Research on Osteoporosis. The authors also thank Prof. Mark Willems from the University of Chichester for providing a DHR consultation.


SA, SY, and NA designed the study; SA supervised the data collection process; and SY supervised the blood analysis. SA wrote the first draft of manuscript, SY and NA carefully revised some sections. JR intellectually contributed to the final version of the paper. All authors approved the final draft for publication submission.

Funding information

This research project was supported by a grant from the Research Centre for the Sports Science and Physical Activity, Deanship of Scientific Research at KSU.

Compliance with ethical standards

Conflicts of interest


Ethical approval

The study was approved by the KSU Institutional Review Board (IRB No. E-16-1831).


  1. 1.
    Bolam KA, Van Uffelen JG, Taaffe DR (2013) The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int 24(11):2749–2762CrossRefGoogle Scholar
  2. 2.
    Chubak J, Ulrich C, Tworoger S, Sorensen B, Yasui Y, Irwin M, Stanczyk F, Potter J, McTietnan A (2006) Effect of exercise on bone mineral density and lean mass in postmenopausal women. Med Sci Sports Exerc 38(7):1236–1244CrossRefGoogle Scholar
  3. 3.
    Fernandez-Real JM, Ricart W (2011) Osteocalcin: a new link between bone and energy metabolism. Some evolutionary clues. Curr Opin Clin Nutr Metab Care 14(4):360–366CrossRefGoogle Scholar
  4. 4.
    Rantalainen T, Heinonen A, Linnamo V, Komi P, Takala T, Kainulainen H (2009) Short-term bone biochemical response to a single bout of high-impact exercise. J Sports Sci Med 8(4):553–559Google Scholar
  5. 5.
    Morgan A, Weiss J, Kelley E (2015) Bone turnover response to acute exercise with varying impact levels: a preliminary investigation. Int J Exerc Sci 8(2):6Google Scholar
  6. 6.
    English KL, Loehr JA, Lee SM, Smith SM (2014) Early-phase musculoskeletal adaptations to different levels of eccentric resistance after 8 weeks of lower body training. Eur J Appl Physiol 114(11):2263–2280CrossRefGoogle Scholar
  7. 7.
    Cadore EL, Brentano MA, Kruel LFM (2005) Effects of the physical activity on the mineral bone density and remodelling the bone tissue. Rev Bras Med Esporte 11(6):1e–7eCrossRefGoogle Scholar
  8. 8.
    Boudenot A, Achiou Z, Portier H (2015) Does running strengthen bone? Appl Physiol Nutr Metab 40(12):1309–1312. CrossRefGoogle Scholar
  9. 9.
    Penailillo L, Blazevich A, Nosaka K (2014) Energy expenditure and substrate oxidation during and after eccentric cycling. Eur J Appl Physiol 114(4):805–814CrossRefGoogle Scholar
  10. 10.
    Isner-Horobeti M, Dufour S, Vautravers P, Geny B, Coudeyre E, Richard R (2013) Eccentric exercise training: modalities, applications and perspectives. Sports Med 43(6):483–512CrossRefGoogle Scholar
  11. 11.
    Ellis R, Shields N, Lim K, Dodd K (2015) Eccentric exercise in adults with cardiorespiratory disease: a systematic review. Clin Rehabil 29:1178–1197CrossRefGoogle Scholar
  12. 12.
    Alkahtani S (2017) Acute downhill running does not induce fat oxidation. Sport Sciences for Health In pressGoogle Scholar
  13. 13.
    Cook MD, Myers SD, Kelly JS, Willems ME (2015) Effect of level and downhill running on breathing efficiency. Sports 3(1):12–20CrossRefGoogle Scholar
  14. 14.
    Scott JPR, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD (2010) The effect of training status on the metabolic response of bone to an acute bout of exhaustive treadmill running. J Clin Endocrinol Metab 95(8):3918–3925. CrossRefGoogle Scholar
  15. 15.
    Salvesen H, Piehl-Aulin K, Ljunghall S (1994) Change in levels of the carboxyterminal propeptide of type I procollagen, the carboxyterminal cross-linked telopeptide of type I collagen and osteocalcin in response to exercise in well-trained men and women. Scand J Med Sci Sports 4(3):186–190. CrossRefGoogle Scholar
  16. 16.
    Thorsen K, Kristoffersson A, Lorentzon R (1996) The effects of brisk walking on markers of bone and calcium metabolism in postmenopausal women. Calcif Tissue Int 58(4):221–225. CrossRefGoogle Scholar
  17. 17.
    Kristoffersson A, Hultdin J, Holmlund I, Thorsen K, Lorentzon R (1995) Effects of short-term maximal work on plasma calcium, parathyroid hormone, osteocalcin and biochemical markers of collagen metabolism. Int J Sports Med 16(03):145–149CrossRefGoogle Scholar
  18. 18.
    Wallace J, Cuneo R, Lundberg P, Rosén T, Jørgensen J, Longobardi S, Keay N, Sacca L, Christiansen J, Bengtsson B, Sönksen P (2000) Responses of markers of bone and collagen turnover to exercise, growth hormone (GH) administration, and GH withdrawal in trained adult males. J Clin Endocrinol Metab 85(1):124–133. Google Scholar
  19. 19.
    Micallef J, Peruchon E, Rossi M (2006) The intensity level of physical exercise and the bone metabolism response. Int J Sports Med 27:105–121CrossRefGoogle Scholar
  20. 20.
    Maimoun L, Sultan C (2010) Effects of Physical Activity on Bone Remodeling. 60.
  21. 21.
    Kishimoto K, Lynch R, Reiger J, Yingling V (2012) Short-term jump activity on bone metabolism in female college-aged nonathletes. J Sports Sci Med 11(1):31–38Google Scholar
  22. 22.
    Eliakim A, Raisz L, Brasel J, Cooper D (1997) Evidence for increased bone formation following a brief endurance-type training intervention in adolescent males. J Bone Miner Res 12(10):1708–1713. CrossRefGoogle Scholar
  23. 23.
    Ihle R, Loucks A (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19(8):1231–1240. CrossRefGoogle Scholar
  24. 24.
    Garanty-Bogacka B, Syrenicz M, Monika R, Krupa B, Czaja-Bulsa G, Walczak M, Sowińska-Przepiera E, Syrenicz A (2013) Association between serum osteocalcin, adiposity and metabolic risk in obese children and adolescents. Endokrynologia Polska 64(5):346–352CrossRefGoogle Scholar
  25. 25.
    Seiberl W, Power GA, Hahn D (2015) Residual force enhancement in humans: current evidence and unresolved issues. J Electromyogr Kinesiol 25(4):571–580CrossRefGoogle Scholar
  26. 26.
    Ebeling P, Akesson K (2001) Role of biochemical markers in the management of osteoporosis. Best Pract Res Clin Rheumatol 15(3):385–400CrossRefGoogle Scholar
  27. 27.
    Banfi G, Lombardi G, Colombini A, Lippi G (2010) Bone metabolism markers in sports medicine. Sports Med 40(8):697–714CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  1. 1.Department of Exercise Physiology, College of Sport Sciences and Physical ActivityKing Saud UniversityRiyadhSaudi Arabia
  2. 2.Prince Mutaib bin Abdullah Chair for Biomarkers Research on Osteoporosis, Department of Biochemistry, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Department of Public Health, Epidemiology and Health EconomicsUniversity of LiègeLiègeBelgium

Personalised recommendations