Carta Acesso aberto Revisado por pares

Fragile bones of elite cyclists: to treat or not to treat?

2021; American Physiological Society; Volume: 131; Issue: 1 Linguagem: Inglês

10.1152/japplphysiol.01034.2020

ISSN

8750-7587

Autores

Luuk Hilkens, Pim Knuiman, Mathieu Heijboer, Robert Kempers, Asker E. Jeukendrup, Luc J. C. van Loon, Jan‐Willem van Dijk,

Tópico(s)

Genetics and Physical Performance

Resumo

ViewpointFragile bones of elite cyclists: to treat or not to treat?Luuk Hilkens, Pim Knuiman, Mathieu Heijboer, Robert Kempers, Asker E. Jeukendrup, Luc J.C van Loon, and Jan-Willem van DijkLuuk HilkensSchool of Sport and Exercise, HAN University of Applied Sciences, Nijmegen, The NetherlandsDepartment of Human Biology, School of Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Centre, Maastricht, The Netherlands, Pim KnuimanSchool of Biomedical Sciences, University of Leeds, Leeds, United Kingdom, Mathieu HeijboerTeam Jumbo-Visma (Professional Cycling Team), Den Bosch, The Netherlands, Robert KempersRoyal Dutch Cycling Union (KNWU), Arnhem, The Netherlands, Asker E. JeukendrupTeam Jumbo-Visma (Professional Cycling Team), Den Bosch, The NetherlandsSchool of Sport, Exercise, and Health Sciences, Loughborough University, Loughborough, United Kingdom, Luc J.C van LoonSchool of Sport and Exercise, HAN University of Applied Sciences, Nijmegen, The NetherlandsDepartment of Human Biology, School of Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Centre, Maastricht, The Netherlands, and Jan-Willem van DijkSchool of Sport and Exercise, HAN University of Applied Sciences, Nijmegen, The NetherlandsPublished Online:28 Jun 2021https://doi.org/10.1152/japplphysiol.01034.2020This is the final version - click for previous versionMoreSectionsPDF (233 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Accumulating evidence suggests that most elite cyclists have lower bone mineral density (BMD) values when compared with their nonelite counterparts (1) or sedentary young males (2, 3). This raises the question whether these ostensibly healthy athletes have a higher acute bone fracture risk and a higher risk of osteoporosis and associated comorbidities later in life. Although treatment of low BMD seems warranted in elite cyclists, the benefits of treatment for health and performance in this population remain to be established. In this viewpoint, we describe the etiology and consequences of impaired bone health in elite cyclists and discuss the need for interventions to optimize bone health in this unique population.IMPAIRED BONE HEALTH IN ELITE CYCLISTS: WHAT ARE THE CAUSES?The cause of impaired bone health in elite cyclists is likely multifactorial. Lack of mechanical loading of the skeleton is an important factor contributing to impaired bone health in elite cyclists (4). Elite cyclists perform extremely high volumes of exercise training and competition (20–30 h/wk; 500–1,000 km/wk), spending a large part of their days on a bike. As the recovery periods are largely spent in a seated or supine position, these cyclists generally obtain insufficient robust osteogenic stimuli throughout daily life.Low energy availability (LEA) and low body mass are also implicated in the compromised bone health of elite cyclists. Indeed, male and female elite cyclists have been identified as a population at risk for LEA (5, 6), which may eventually lead to the relative energy deficiency in sport (RED-S) syndrome. LEA can be partly attributed to extremely high energy demands for long periods, which may even exceed 30 MJ/day during multistage races (7). Energy intake may also be purposely low when aiming to reduce body mass to enhance the power-to-mass ratio (8). Furthermore, LEA has a major impact on the endocrine system, affecting key hormones that regulate bone metabolism (9).Another factor that may be involved in low BMD in elite cyclists is dermal calcium loss through sweating, which can be as high as ∼150 mg/h (10). In response to dermal calcium losses, the parathyroid gland will release the parathyroid hormone (PTH), which activates demineralization of bone tissue to prevent or attenuate a decline in serum calcium levels. Chronic activation of this mechanism may contribute to low BMD in elite cyclists (11), although the impact of dermal calcium loss in calcium homeostasis has also been challenged recently (12).It can also be speculated that chronic exercise stress is implicated in impaired bone health in elite cyclists. Although research on this topic is lacking, there is some evidence to suggest that chronic inflammation (13) and elevated cortisol levels (14) are related to bone loss, albeit in nonathletes.It can be argued that the use of glucocorticoids, as a treatment for musculoskeletal injuries, asthma, and exercise-induced bronchoconstriction, may also contribute to low BMD. However, it should be noted that the use of systemic glucocorticoids seems rare in modern elite cycling, which is also evidenced by a steady decline in "adverse analytical findings" due to glucocorticoid use over the past 2 decades (15). Although inhaled glucocorticoids may be used by some elite cyclists for the treatment of asthma or exercise-induced bronchoconstriction (16), their systemic bioavailability (17) and impact on BMD (18, 19) seem rather limited. Taken together, we believe that the potential contribution of glucocorticoids to the decreased BMD in the current generation of elite cyclists is likely to be negligible.IMPAIRED BONE HEALTH IN ELITE CYCLISTS: WHAT ARE THE CONSEQUENCES?Short-term consequences of low BMD in athletes include an increased risk of stress fractures and traumatic bone fractures (5). Stress fractures, however, seem very uncommon among elite cyclists due to the minimal bone stress during cycling. Traumatic bone fractures, on the other hand, are highly prevalent among elite cyclists due to the considerable risk of crashes during training and competition. In this regard, Haeberle and coworkers (20) showed that fractures as a result of crashes were the most common reason for withdrawal during the Tour de France between 2010 and 2017. Moreover, half of the cyclists with fractures underwent surgery (20), emphasizing the importance of this problem. Crashes, however, are inherent to cycling races, and it remains to be established whether stronger bones reduce the risk of bone fractures due to crashes.An important long-term consequence of low peak bone mass in elite cyclists could be an increased risk of bone fractures later in life. It has been proposed that a high peak bone mass during early adulthood is the single most important factor for the prevention of osteoporosis with aging (21). An increase in peak bone mass of 10% has been estimated to delay the onset of osteoporosis by 13 years (22), thereby emphasizing the necessity for healthy bones in young adulthood. However, the progression and/or regression of impaired bone status during and after the cyclists' active career remain(s) to be established, and no (anecdotal) evidence is available that indicates a higher prevalence of bone fractures in retired elite cyclists.The implications of poor bone health for performance should be considered as well. RED-S syndrome, which is often associated with low BMD, has been linked to impaired exercise performance (5). However, when low BMD occurs without other features of RED-S syndrome, there is no direct evidence to assume that cycling performance will be affected. Nevertheless, given the function of bone in hematopoiesis, and the emerging evidence regarding bone-muscle cross talk (23), it should be realized that the importance of healthy bones may extend well beyond bone fracture risk alone.IMPAIRED BONE HEALTH IN ELITE CYCLISTS: CONSIDERATIONS FOR TREATMENTAlthough oral bisphosphonates are effective in increasing BMD and reducing the risk of bone fractures in men with osteoporosis (24), we feel that pharmacological treatment should be the last line of defense, especially in young athletes. The impact of exercise and nutritional interventions to increase BMD has been reported extensively, particularly for older adults and postmenopausal women (25, 26). To our knowledge, no exercise and/or nutritional interventions aimed at increasing BMD have been documented in elite cyclists. Possible interventions should result in clinically relevant increments in BMD, without interfering with training targets and cycling performance.Resistance exercise training and impact training (e.g., jumping or bounding) are generally prescribed as the more effective exercise strategies to increase BMD (27). Although resistance exercise training may support cycling performance, many elite cyclists are afraid of potential negative effects of resistance-type exercise training on body mass and cycling performance (8). Impact training is likely more effective than resistance exercise training (28) and may interfere less with the adaptation to endurance training (29). In support, daily short bouts of high-impact jumping exercise have been shown to increase BMD (30), making this a possible intervention to integrate into an elite cyclist's training program. It is unknown, however, if such a low-dose osteogenic stimulus outweighs the deleterious effects of elite cycling on bone health.Energy availability, calcium, vitamin D, and protein are among the major nutritional factors that should be considered (31). Careful assessment of nutritional intake and regular blood testing (for vitamin D) are needed to assess whether cyclists have an inadequate energy and calcium intake and/or vitamin D status. An adequate calcium intake is needed for bone mineralization, with adequate serum 25-hydroxyvitamin D levels promoting the absorption of calcium from the gut. Deficiencies should be addressed, whereas supplementation above intake recommendations seems to provide little (32) or no (33) benefit for bone health. Being the most abundant protein in the bone matrix, collagen could be an interesting target for novel nutritional strategies as well. Indeed, 12 mo of daily supplementation with collagen has been shown to positively affect BMD and markers of bone metabolism in postmenopausal women (34), whereas a combination of gelatin supplementation with jumping exercise has been shown to increase the (bone) collagen synthesis marker N-terminal propeptide of type I collagen (P1NP) in young males (35).It is clear that both exercise and nutrition have the potential to increase BMD in elite cyclists, but more work is needed to establish their efficacy and effectiveness in this specific population.IMPAIRED BONE HEALTH IN ELITE CYCLISTS: TO TREAT OR NOT TO TREAT?The answer to the question whether low BMD in elite cyclists should be treated may not be as clear-cut as initially thought. It is concerning that elite cyclists have a low bone mass at an age where peak bone mass is normally achieved. However, the potential short- and long-term consequences of impaired bone health in terms of health and performance are unclear in this specific population. Although BMD can generally be increased by exercise and/or nutritional interventions, the feasibility, effectiveness, and potential side effects of such interventions remain to be established in this population. The ultimate piece of evidence would reveal the relationship between bone health and the incidence of traumatic bone fractures during and after the active career of elite cyclists. Until more evidence becomes available, all elite cyclists and their supporting staff should at least be aware of this issue and carefully consider the available treatment options for low BMD.GRANTSThe work of L. Hilkens and J. W. van Dijk on this topic is part of the Eat2Move project and sponsored by a grant from the Province of Gelderland, the Netherlands.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the authors.AUTHOR CONTRIBUTIONSL.H. and J.W.v.D conceived and designed research; L.H. and J.W.v.D. drafted manuscript; L.H., P.K., M.H., R.K., A.E.J., L.J.v. and J.W.v.D. edited and revised manuscript; L.H., P.K., M.H., R.K., A.E.J., L.J.v. and J.W.v.D. approved final version of manuscript.REFERENCES1. Mojock CD, Ormsbee MJ, Kim JS, Arjmandi BH, Louw GA, Contreras RJ, Panton LB. Comparisons of bone mineral density between recreational and trained male road cyclists. Clin J Sport Med 26: 152–156, 2016. doi:10.1097/JSM.0000000000000186.Crossref | ISI | Google Scholar2. Campion F, Nevill AM, Karlsson M, Lounana J, Shabani M, Fardellone P, Medelli J. Bone status in professional cyclists. Int J Sports Med 31: 511–515, 2010. doi:10.1055/s-0029-1243616.Crossref | ISI | Google Scholar3. Medelli J, Lounana J, Menuet J-J, Shabani M, Cordero-MacIntyre Z. Is osteopenia a health risk in professional cyclists? J Clini Densitom 12: 28–34, 2009. doi:10.1016/j.jocd.2008.07.057.Crossref | ISI | Google Scholar4. Santos L, Elliott-Sale KJ, Sale C. Exercise and bone health across the lifespan. Biogerontology 18: 931–946, 2017. doi:10.1007/s10522-017-9732-6. Crossref | PubMed | ISI | Google Scholar5. Mountjoy M, Sundgot-Borgen JK, Burke LM, Ackerman KE, Blauwet C, Constantini N, Lebrun C, Lundy B, Melin AK, Meyer NL, Sherman RT, Tenforde AS, Klungland Torstveit M, Budgett R. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med 52: 687–697, 2018. doi:10.1136/bjsports-2018-099193. Crossref | PubMed | ISI | Google Scholar6. Viner RT, Harris M, Berning JR, Meyer NL. Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. Int J Sport Nutr Exerc Metab 25: 594–602, 2015. doi:10.1123/ijsnem.2015-0073.Crossref | ISI | Google Scholar7. Plasqui G, Rietjens G, Lambriks L, Wouters L, Saris WH. Energy expenditure during extreme endurance exercise: the Giro d'Italia. Medi Sci Sports Exerc 51: 568–574, 2018. doi:10.1249/MSS.0000000000001814.Crossref | ISI | Google Scholar8. Hoon MW, Haakonssen EC, Menaspà P, Burke LM. Racing weight and resistance training: perceptions and practices in trained male cyclists. Phys Sportsmed 47: 421–426, 2019. doi:10.1080/00913847.2019.1607602.Crossref | ISI | Google Scholar9. Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman KE. Endocrine effects of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab 28: 335–349, 2018. doi:10.1123/ijsnem.2018-0127.Crossref | PubMed | ISI | Google Scholar10. Barry DW, Hansen KC, van Pelt RE, Witten M, Wolfe P, Kohrt WM. Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Med Sci Sports Exerc 43: 617–623, 2011. doi:10.1249/MSS.0b013e3181f79fa8. Crossref | PubMed | ISI | Google Scholar11. Barry DW, Kohrt WM. BMD decreases over the course of a year in competitive male cyclists. J Bone Miner Res 23: 484–491, 2007. doi:10.1359/jbmr.071203.Crossref | ISI | Google Scholar12. Kohrt WM, Wolfe P, Sherk VD, Wherry SJ, Wellington T, Melanson EL, Swanson CM, Weaver CM, Boxer RS. Dermal calcium loss is not the primary determinant of parathyroid hormone secretion during exercise. Med Sci Sports Exerc 51: 2117–2124, 2019. doi:10.1249/MSS.0000000000002017.Crossref | ISI | Google Scholar13. Redlich K, Smolen JS. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat Rev Drug Discov 11: 234–250, 2012. Crossref | PubMed | ISI | Google Scholar14. Reynolds R, Dennison E, Walker B, Syddall H, Wood P, Andrew R, Phillips DI, Cooper C. Cortisol secretion and rate of bone loss in a population-based cohort of elderly men and women. Calcif Tissue Int 77: 134–138, 2005. doi:10.1007/s00223-004-0270-2. Crossref | PubMed | ISI | Google Scholar15. Vernec A, Slack A, Harcourt PR, Budgett R, Duclos M, Kinahan A, Mjøsund K, Strasburger CJ. Glucocorticoids in elite sport: current status, controversies and innovative management strategies—a narrative review. Br J Sports Med 54: 8–12, 2020. doi:10.1136/bjsports-2018-100196. Crossref | PubMed | ISI | Google Scholar16. Boulet L-P, O'Byrne PM. Asthma and exercise-induced bronchoconstriction in athletes. N Engl J Med 372: 641–648, 2015. doi:10.1056/NEJMra1407552. Crossref | PubMed | ISI | Google Scholar17. Daley-Yates PT. Inhaled corticosteroids: potency, dose equivalence and therapeutic index. Br J Clin Pharmacol 80: 372–380, 2015. doi:10.1111/bcp.12637. Crossref | PubMed | ISI | Google Scholar18. Kumarathas I, Harsløf T, Andersen CU, Langdahl B, Hilberg O, Bjermer L, Løkke A. The risk of osteoporosis in patients with asthma. Eur Clin Respir J 7: 1763612, 2020. doi:10.1080/20018525.2020.1763612. Crossref | PubMed | ISI | Google Scholar19. Loke YK, Gilbert D, Thavarajah M, Blanco P, Wilson AM. Bone mineral density and fracture risk with long-term use of inhaled corticosteroids in patients with asthma: systematic review and meta-analysis. BMJ Open 5: e008554, 2015. doi:10.1136/bmjopen-2015-008554.Crossref | ISI | Google Scholar20. Haeberle HS, Navarro SM, Power EJ, Schickendantz MS, Farrow LD, Ramkumar PN. Prevalence and epidemiology of injuries among elite cyclists in the Tour de France. Orthop J Sports Med 6: 2325967118793392, 2018. doi:10.1177/2325967118793392. Crossref | PubMed | ISI | Google Scholar21. Bonjour JP, Chevalley T, Ferrari S, Rizzoli R. The importance and relevance of peak bone mass in the prevalence of osteoporosis. Salud Publica Mex 51 : S5–17, 2009. doi:10.1590/s0036-36342009000700004. Crossref | PubMed | ISI | Google Scholar22. Hernandez CJ, Beaupr -GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int 14: 843–847, 2003. doi:10.1007/s00198-003-1454-8.Crossref | PubMed | ISI | Google Scholar23. Brotto M, Bonewald L. Bone and muscle: interactions beyond mechanical. Bone 80: 109–114, 2015. doi:10.1016/j.bone.2015.02.010. Crossref | PubMed | ISI | Google Scholar24. Nayak S, Greenspan SL. Osteoporosis treatment efficacy for men: a systematic review and meta-analysis. J Am Geriatr Soc 65: 490–495, 2017. doi:10.1111/jgs.14668. Crossref | PubMed | ISI | Google Scholar25. Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, Harbour RT, Caldwell LM, Creed G. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev 6: CD000336, 2011. doi:10.1002/14651858.CD000333.pub2.Crossref | Google Scholar26. McMillan LB, Zengin A, Ebeling PR, Scott D. Prescribing physical activity for the prevention and treatment of osteoporosis in older adults. Healthcare 5: 85, 2017. doi:10.3390/healthcare5040085.Crossref | ISI | Google Scholar27. Beck BR, Daly RM, Singh MA, Taaffe DR. Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 20: 438–445, 2017. doi:10.1016/j.jsams.2016.10.001. Crossref | PubMed | ISI | Google Scholar28. Weeks BK, Beck BR. The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int 19: 1567–1577, 2008. doi:10.1007/s00198-008-0606-2.Crossref | ISI | Google Scholar29. Baar K. Using molecular biology to maximize concurrent training. Sports Med 44 : S117–125, 2014. doi:10.1007/s40279-014-0252-0. Crossref | PubMed | ISI | Google Scholar30. Zhao R, Zhao M, Zhang L. Efficiency of jumping exercise in improving bone mineral density among premenopausal women: a meta-analysis. Sports Med 44: 1393–1402, 2014. doi:10.1007/s40279-014-0220-8.Crossref | ISI | Google Scholar31. Sale C, Elliott-Sale KJ. Nutrition and athlete bone health. Sports Med 49: 139–151, 2019. doi:10.1007/s40279-019-01161-2. Crossref | PubMed | ISI | Google Scholar32. Yao P, Bennett D, Mafham M, Lin X, Chen Z, Armitage J, Clarke R. Vitamin D and calcium for the prevention of fracture: a systematic review and meta-analysis. JAMA Netw Open 2: e1917789, 2019. doi:10.1001/jamanetworkopen.2019.17789. Crossref | PubMed | ISI | Google Scholar33. Jin J. Vitamin D and calcium supplements for preventing Ffractures. JAMA 319: 1630–1630, 2018. doi:10.1001/jama.2018.3892. Crossref | PubMed | ISI | Google Scholar34. König D, Oesser S, Scharla S, Zdzieblik D, Gollhofer A. Specific collagen peptides improve bone mineral density and bone markers in postmenopausal women-A randomized controlled study. Nutrients 10: 97, 2018. doi:10.3390/nu10010097.Crossref | ISI | Google Scholar35. Shaw G, Lee-Barthel A, Ross ML, Wang B, Baar K. Vitamin C-enriched gelatin supplementation before intermittent activity augments collagen synthesis. Am J Clin Nutr 105: 136–143, 2017. doi:10.3945/ajcn.116.138594. Crossref | PubMed | ISI | Google ScholarAUTHOR NOTESCorrespondence: Dr. J.-W. van Dijk (JanWillem.[email protected]nl). Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Related ArticlesCommentaries on Viewpoint: Fragile bones of elite cyclists: to treat or not to treat? 28 Jun 2021Journal of Applied PhysiologyLast Word on Viewpoint: Fragile bones of elite cyclists: to treat or not to treat? 28 Jun 2021Journal of Applied PhysiologyCited ByCommentaries on Viewpoint: Do we need to change the guideline values for determining low bone mineral density in athletes?19 May 2022 | Journal of Applied Physiology, Vol. 132, No. 5Do we need to change the guideline values for determining low bone mineral density in athletes?Kristin L. Jonvik, Monica K. 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Jeukendrup, Luc J.C. van Loon, and Jan-Willem van Dijk28 June 2021 | Journal of Applied Physiology, Vol. 131, No. 1 More from this issue > Volume 131Issue 1July 2021Pages 26-28 Crossmark Copyright & PermissionsCopyright © 2021 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.01034.2020PubMed33703944History Received 3 December 2020 Accepted 8 March 2021 Published online 28 June 2021 Published in print 1 July 2021 Keywordsboneelite cyclistsexercisenutritionosteoporosis Metrics

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