Bone and energy metabolism parameters in professional cyclists during the Giro d'Italia 3-weeks stage race
Giovanni Lombardi, Patrizia Lanteri, Rosa Graziani, Alessandra Colombini, Giuseppe Banfi, Roberto Corsetti, Giovanni Lombardi, Patrizia Lanteri, Rosa Graziani, Alessandra Colombini, Giuseppe Banfi, Roberto Corsetti
Abstract
Cycling is a not weight-bearing activity and is known to induce bone resorption. Stage races are really strenuous endurance performances affecting the energy homeostasis. The recently highlighted link, in the co-regulation of bone and energy metabolism, demonstrates a central role for the equilibrium between carboxylated and undercarboxylated forms of osteocalcin. Aim of this study was to understand the acute physiological responses to a cycling stage race in terms of bone turnover and energy metabolism and the possible co-regulative mechanisms underlying their relationship. We studied nine professional cyclists engaged in 2011 Giro d'Italia stage race. Pre-analytical and analytical phases tightly followed academic and anti-doping authority's recommendations. Bone and energy metabolism markers (bone alkaline phosphatase, tartrate-resistant acid phosphatase 5b, total and undercarboxylated osteocalcin, leptin and adiponectin) and related hormones (cortisol and testosterone) were measured, by Sandwich Enzyme Immunoassays, at days -1 (pre-race), 12 and 22 during the race. The power output and the energy expenditure (mean and accumulated) were derived and correlated with the biochemical indexes. During the race, bone metabolism showed that an unbalance in behalf of resorption, which is enhanced, occurred along with a relative increase in the concentration of the undercarboxylated form of osteocalcin that was indirectly related to the enhanced energy expenditure, through adipokines modifications, with leptin decrease (high energy consumption) and adiponectin increase (optimization of energy expenditure). The exertion due to heavy effort induced a decrease of cortisol, while testosterone levels resulted unchanged. In conclusion, during a 3-weeks stage race, bone metabolism is pushed towards resorption. A possible relationship between the bone and the energy metabolisms is suggested by the relative correlations among absolute and relative concentrations trends of undercarboxylated OC, adipokines concentrations, BMI, fat mass (%), power output and the derived energy expenditure.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
![Figure 1. Modification of serum bone markers…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/3407078/bin/pone.0042077.g001.jpg)
Figure 2. Modification of plasma osteocalcin levels…
Figure 2. Modification of plasma osteocalcin levels and relative concentration of Glu-OC over the race.
Figure 3. Modification of adipokines levels over…
Figure 3. Modification of adipokines levels over the race.
The Figure shows the trends of…
Figure 4. Modification of cortisol and testosterone…
Figure 4. Modification of cortisol and testosterone concentrations over the race.
The Figure shows the…
- Reciprocal regulation of calcium-/phosphate-regulating hormones in cyclists during the Giro d'Italia 3-week stage race.Lombardi G, Corsetti R, Lanteri P, Grasso D, Vianello E, Marazzi MG, Graziani R, Colombini A, Galliera E, Corsi Romanelli MM, Banfi G. Lombardi G, et al. Scand J Med Sci Sports. 2014 Oct;24(5):779-87. doi: 10.1111/sms.12080. Epub 2013 May 7. Scand J Med Sci Sports. 2014. PMID: 23647316
- Serum creatine kinase activity and its relationship with renal function indices in professional cyclists during the Giro d'Italia 3-week stage race.Colombini A, Corsetti R, Machado M, Graziani R, Lombardi G, Lanteri P, Banfi G. Colombini A, et al. Clin J Sport Med. 2012 Sep;22(5):408-13. doi: 10.1097/JSM.0b013e31825e66cc. Clin J Sport Med. 2012. PMID: 22744001
- Cardiac indexes, cardiac damage biomarkers and energy expenditure in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Barassi A, Lanteri P, Colombini A, D'Eril GM, Banfi G. Corsetti R, et al. Biochem Med (Zagreb). 2012;22(2):237-46. doi: 10.11613/bm.2012.026. Biochem Med (Zagreb). 2012. PMID: 22838189 Free PMC article.
- Haematological and iron metabolism parameters in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Lanteri P, Colombini A, Graziani R, Banfi G. Corsetti R, et al. Clin Chem Lab Med. 2012 Jan 13;50(5):949-56. doi: 10.1515/cclm-2011-0857. Clin Chem Lab Med. 2012. PMID: 22628339
- Science and cycling: current knowledge and future directions for research.Atkinson G, Davison R, Jeukendrup A, Passfield L. Atkinson G, et al. J Sports Sci. 2003 Sep;21(9):767-87. doi: 10.1080/0264041031000102097. J Sports Sci. 2003. PMID: 14579871 Review.
- Effect of increased protein intake and exogenous ketosis on body composition, energy expenditure and exercise capacity during a hypocaloric diet in recreational female athletes.Hiroux C, Schouten M, de Glisezinski I, Simon C, Crampes F, Hespel P, Koppo K. Hiroux C, et al. Front Physiol. 2023 Jan 13;13:1063956. doi: 10.3389/fphys.2022.1063956. eCollection 2022. Front Physiol. 2023. PMID: 36714318 Free PMC article.
- Bone-to-Brain: A Round Trip in the Adaptation to Mechanical Stimuli.Gerosa L, Lombardi G. Gerosa L, et al. Front Physiol. 2021 Apr 28;12:623893. doi: 10.3389/fphys.2021.623893. eCollection 2021. Front Physiol. 2021. PMID: 33995117 Free PMC article. Review.
- Physical Activity-Dependent Regulation of Parathyroid Hormone and Calcium-Phosphorous Metabolism.Lombardi G, Ziemann E, Banfi G, Corbetta S. Lombardi G, et al. Int J Mol Sci. 2020 Jul 29;21(15):5388. doi: 10.3390/ijms21155388. Int J Mol Sci. 2020. PMID: 32751307 Free PMC article. Review.
- Ketone ester supplementation blunts overreaching symptoms during endurance training overload.Poffé C, Ramaekers M, Van Thienen R, Hespel P. Poffé C, et al. J Physiol. 2019 Jun;597(12):3009-3027. doi: 10.1113/JP277831. Epub 2019 May 22. J Physiol. 2019. PMID: 31039280 Free PMC article. Clinical Trial.
- Physical Activity and Bone Health: What Is the Role of Immune System? A Narrative Review of the Third Way.Lombardi G, Ziemann E, Banfi G. Lombardi G, et al. Front Endocrinol (Lausanne). 2019 Feb 7;10:60. doi: 10.3389/fendo.2019.00060. eCollection 2019. Front Endocrinol (Lausanne). 2019. PMID: 30792697 Free PMC article. Review.
-
- Foster C, Hoyos J, Earnest C, Lucia A (2005) Regulation of energy expenditure during prolonged athletic competition. Med Sci Sports Exerc 37: 670–675. - PubMed
-
- Saris WH, van Erp-Baart MA, Brouns F, Westerterp KR, ten Hoor F (1989) Study on food intake and energy expenditure during extreme sustained exercise: the Tour de France. Int J Sports Med 10 Suppl 1S26–31. - PubMed
-
- Padilla S, Mujika I, Santisteban J, Impellizzeri FM, Goiriena JJ (2008) Exercise intensity and load during uphill cycling in professional 3-week races. Eur J Appl Physiol 102: 431–438. - PubMed
-
- Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19: 1231–1240. - PubMed
- Research Support, Non-U.S. Gov't
- Adipokines / blood
- Anthropometry
- Athletes*
- Bicycling / physiology*
- Biomarkers / blood
- Body Composition
- Bone and Bones / metabolism*
- Energy Metabolism*
- Hormones / blood
- Humans
- Kidney / physiology
- Osteocalcin / blood
- Time Factors
- Adipokines
- Biomarkers
- Hormones
- Osteocalcin
- Full Text Sources
- Medical
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Figure 2. Modification of plasma osteocalcin levels…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/3407078/bin/pone.0042077.g002.jpg)
Figure 3. Modification of adipokines levels over…
Figure 3. Modification of adipokines levels over the race.
The Figure shows the trends of…
Figure 4. Modification of cortisol and testosterone…
Figure 4. Modification of cortisol and testosterone concentrations over the race.
The Figure shows the…
- Reciprocal regulation of calcium-/phosphate-regulating hormones in cyclists during the Giro d'Italia 3-week stage race.Lombardi G, Corsetti R, Lanteri P, Grasso D, Vianello E, Marazzi MG, Graziani R, Colombini A, Galliera E, Corsi Romanelli MM, Banfi G. Lombardi G, et al. Scand J Med Sci Sports. 2014 Oct;24(5):779-87. doi: 10.1111/sms.12080. Epub 2013 May 7. Scand J Med Sci Sports. 2014. PMID: 23647316
- Serum creatine kinase activity and its relationship with renal function indices in professional cyclists during the Giro d'Italia 3-week stage race.Colombini A, Corsetti R, Machado M, Graziani R, Lombardi G, Lanteri P, Banfi G. Colombini A, et al. Clin J Sport Med. 2012 Sep;22(5):408-13. doi: 10.1097/JSM.0b013e31825e66cc. Clin J Sport Med. 2012. PMID: 22744001
- Cardiac indexes, cardiac damage biomarkers and energy expenditure in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Barassi A, Lanteri P, Colombini A, D'Eril GM, Banfi G. Corsetti R, et al. Biochem Med (Zagreb). 2012;22(2):237-46. doi: 10.11613/bm.2012.026. Biochem Med (Zagreb). 2012. PMID: 22838189 Free PMC article.
- Haematological and iron metabolism parameters in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Lanteri P, Colombini A, Graziani R, Banfi G. Corsetti R, et al. Clin Chem Lab Med. 2012 Jan 13;50(5):949-56. doi: 10.1515/cclm-2011-0857. Clin Chem Lab Med. 2012. PMID: 22628339
- Science and cycling: current knowledge and future directions for research.Atkinson G, Davison R, Jeukendrup A, Passfield L. Atkinson G, et al. J Sports Sci. 2003 Sep;21(9):767-87. doi: 10.1080/0264041031000102097. J Sports Sci. 2003. PMID: 14579871 Review.
- Effect of increased protein intake and exogenous ketosis on body composition, energy expenditure and exercise capacity during a hypocaloric diet in recreational female athletes.Hiroux C, Schouten M, de Glisezinski I, Simon C, Crampes F, Hespel P, Koppo K. Hiroux C, et al. Front Physiol. 2023 Jan 13;13:1063956. doi: 10.3389/fphys.2022.1063956. eCollection 2022. Front Physiol. 2023. PMID: 36714318 Free PMC article.
- Bone-to-Brain: A Round Trip in the Adaptation to Mechanical Stimuli.Gerosa L, Lombardi G. Gerosa L, et al. Front Physiol. 2021 Apr 28;12:623893. doi: 10.3389/fphys.2021.623893. eCollection 2021. Front Physiol. 2021. PMID: 33995117 Free PMC article. Review.
- Physical Activity-Dependent Regulation of Parathyroid Hormone and Calcium-Phosphorous Metabolism.Lombardi G, Ziemann E, Banfi G, Corbetta S. Lombardi G, et al. Int J Mol Sci. 2020 Jul 29;21(15):5388. doi: 10.3390/ijms21155388. Int J Mol Sci. 2020. PMID: 32751307 Free PMC article. Review.
- Ketone ester supplementation blunts overreaching symptoms during endurance training overload.Poffé C, Ramaekers M, Van Thienen R, Hespel P. Poffé C, et al. J Physiol. 2019 Jun;597(12):3009-3027. doi: 10.1113/JP277831. Epub 2019 May 22. J Physiol. 2019. PMID: 31039280 Free PMC article. Clinical Trial.
- Physical Activity and Bone Health: What Is the Role of Immune System? A Narrative Review of the Third Way.Lombardi G, Ziemann E, Banfi G. Lombardi G, et al. Front Endocrinol (Lausanne). 2019 Feb 7;10:60. doi: 10.3389/fendo.2019.00060. eCollection 2019. Front Endocrinol (Lausanne). 2019. PMID: 30792697 Free PMC article. Review.
-
- Foster C, Hoyos J, Earnest C, Lucia A (2005) Regulation of energy expenditure during prolonged athletic competition. Med Sci Sports Exerc 37: 670–675. - PubMed
-
- Saris WH, van Erp-Baart MA, Brouns F, Westerterp KR, ten Hoor F (1989) Study on food intake and energy expenditure during extreme sustained exercise: the Tour de France. Int J Sports Med 10 Suppl 1S26–31. - PubMed
-
- Padilla S, Mujika I, Santisteban J, Impellizzeri FM, Goiriena JJ (2008) Exercise intensity and load during uphill cycling in professional 3-week races. Eur J Appl Physiol 102: 431–438. - PubMed
-
- Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19: 1231–1240. - PubMed
- Research Support, Non-U.S. Gov't
- Adipokines / blood
- Anthropometry
- Athletes*
- Bicycling / physiology*
- Biomarkers / blood
- Body Composition
- Bone and Bones / metabolism*
- Energy Metabolism*
- Hormones / blood
- Humans
- Kidney / physiology
- Osteocalcin / blood
- Time Factors
- Adipokines
- Biomarkers
- Hormones
- Osteocalcin
- Full Text Sources
- Medical
NCBI Literature Resources
The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
8600 Rockville Pike
Bethesda, MD 20894
![Figure 3. Modification of adipokines levels over…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/3407078/bin/pone.0042077.g003.jpg)
Figure 4. Modification of cortisol and testosterone…
Figure 4. Modification of cortisol and testosterone concentrations over the race.
The Figure shows the…
- Reciprocal regulation of calcium-/phosphate-regulating hormones in cyclists during the Giro d'Italia 3-week stage race.Lombardi G, Corsetti R, Lanteri P, Grasso D, Vianello E, Marazzi MG, Graziani R, Colombini A, Galliera E, Corsi Romanelli MM, Banfi G. Lombardi G, et al. Scand J Med Sci Sports. 2014 Oct;24(5):779-87. doi: 10.1111/sms.12080. Epub 2013 May 7. Scand J Med Sci Sports. 2014. PMID: 23647316
- Serum creatine kinase activity and its relationship with renal function indices in professional cyclists during the Giro d'Italia 3-week stage race.Colombini A, Corsetti R, Machado M, Graziani R, Lombardi G, Lanteri P, Banfi G. Colombini A, et al. Clin J Sport Med. 2012 Sep;22(5):408-13. doi: 10.1097/JSM.0b013e31825e66cc. Clin J Sport Med. 2012. PMID: 22744001
- Cardiac indexes, cardiac damage biomarkers and energy expenditure in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Barassi A, Lanteri P, Colombini A, D'Eril GM, Banfi G. Corsetti R, et al. Biochem Med (Zagreb). 2012;22(2):237-46. doi: 10.11613/bm.2012.026. Biochem Med (Zagreb). 2012. PMID: 22838189 Free PMC article.
- Haematological and iron metabolism parameters in professional cyclists during the Giro d'Italia 3-weeks stage race.Corsetti R, Lombardi G, Lanteri P, Colombini A, Graziani R, Banfi G. Corsetti R, et al. Clin Chem Lab Med. 2012 Jan 13;50(5):949-56. doi: 10.1515/cclm-2011-0857. Clin Chem Lab Med. 2012. PMID: 22628339
- Science and cycling: current knowledge and future directions for research.Atkinson G, Davison R, Jeukendrup A, Passfield L. Atkinson G, et al. J Sports Sci. 2003 Sep;21(9):767-87. doi: 10.1080/0264041031000102097. J Sports Sci. 2003. PMID: 14579871 Review.
- Effect of increased protein intake and exogenous ketosis on body composition, energy expenditure and exercise capacity during a hypocaloric diet in recreational female athletes.Hiroux C, Schouten M, de Glisezinski I, Simon C, Crampes F, Hespel P, Koppo K. Hiroux C, et al. Front Physiol. 2023 Jan 13;13:1063956. doi: 10.3389/fphys.2022.1063956. eCollection 2022. Front Physiol. 2023. PMID: 36714318 Free PMC article.
- Bone-to-Brain: A Round Trip in the Adaptation to Mechanical Stimuli.Gerosa L, Lombardi G. Gerosa L, et al. Front Physiol. 2021 Apr 28;12:623893. doi: 10.3389/fphys.2021.623893. eCollection 2021. Front Physiol. 2021. PMID: 33995117 Free PMC article. Review.
- Physical Activity-Dependent Regulation of Parathyroid Hormone and Calcium-Phosphorous Metabolism.Lombardi G, Ziemann E, Banfi G, Corbetta S. Lombardi G, et al. Int J Mol Sci. 2020 Jul 29;21(15):5388. doi: 10.3390/ijms21155388. Int J Mol Sci. 2020. PMID: 32751307 Free PMC article. Review.
- Ketone ester supplementation blunts overreaching symptoms during endurance training overload.Poffé C, Ramaekers M, Van Thienen R, Hespel P. Poffé C, et al. J Physiol. 2019 Jun;597(12):3009-3027. doi: 10.1113/JP277831. Epub 2019 May 22. J Physiol. 2019. PMID: 31039280 Free PMC article. Clinical Trial.
- Physical Activity and Bone Health: What Is the Role of Immune System? A Narrative Review of the Third Way.Lombardi G, Ziemann E, Banfi G. Lombardi G, et al. Front Endocrinol (Lausanne). 2019 Feb 7;10:60. doi: 10.3389/fendo.2019.00060. eCollection 2019. Front Endocrinol (Lausanne). 2019. PMID: 30792697 Free PMC article. Review.
-
- Foster C, Hoyos J, Earnest C, Lucia A (2005) Regulation of energy expenditure during prolonged athletic competition. Med Sci Sports Exerc 37: 670–675. - PubMed
-
- Saris WH, van Erp-Baart MA, Brouns F, Westerterp KR, ten Hoor F (1989) Study on food intake and energy expenditure during extreme sustained exercise: the Tour de France. Int J Sports Med 10 Suppl 1S26–31. - PubMed
-
- Padilla S, Mujika I, Santisteban J, Impellizzeri FM, Goiriena JJ (2008) Exercise intensity and load during uphill cycling in professional 3-week races. Eur J Appl Physiol 102: 431–438. - PubMed
-
- Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19: 1231–1240. - PubMed
- Research Support, Non-U.S. Gov't
- Adipokines / blood
- Anthropometry
- Athletes*
- Bicycling / physiology*
- Biomarkers / blood
- Body Composition
- Bone and Bones / metabolism*
- Energy Metabolism*
- Hormones / blood
- Humans
- Kidney / physiology
- Osteocalcin / blood
- Time Factors
- Adipokines
- Biomarkers
- Hormones
- Osteocalcin
- Full Text Sources
- Medical
![Figure 4. Modification of cortisol and testosterone…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/3407078/bin/pone.0042077.g004.jpg)
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Source: PubMed