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DOI: 10.1055/s-0040-1709483
Sports and Metabolic Bone Disease
Abstract
Physical activity (PA) increases bone mass and bone strength through different mechanisms and also reduces the risk of falls in the elderly, through proprioception and balance training. The benefits seen in adolescence continue into adulthood. Exercise delays and attenuates the effects of osteoporosis, and particular sports activities may be recommended to improve bone mineral density (BMD) of the spine or regional BMD, improve balance, and prevent falls. Stress injuries related to exercise are more common in osteopenic and osteoporotic individuals.
Sports activity may in some cases be detrimental for bone health, with nutrition restriction a frequent cause for negative effects of the practice of PA on bone. The examples are the so-called female athlete triad of menstrual dysfunction resulting in reduced estrogen levels, low energy due to malnutrition, and decreased BMD. A similar triad is described in male athletes. This review analyzes the effects of sport on bone metabolism and in particular its relationship with metabolic bone disease.
Publikationsverlauf
Artikel online veröffentlicht:
28. September 2020
© 2020. Thieme. All rights reserved.
Thieme Medical Publishers
333 Seventh Avenue, New York, NY 10001, USA.
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References
- 1 Eriksen EF. Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev 1986; 7 (04) 379-408
- 2 Riggs BL, Melton III LJ. Involutional osteoporosis. N Engl J Med 1986; 314 (26) 1676-1686
- 3 Hannan MT, Felson DT, Anderson JJ. Bone mineral density in elderly men and women: results from the Framingham osteoporosis study. J Bone Miner Res 1992; 7 (05) 547-553
- 4 Hannan MT, Felson DT, Dawson-Hughes B. , et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 2000; 15 (04) 710-720
- 5 Bouxsein ML, Karasik D. Bone geometry and skeletal fragility. Curr Osteoporos Rep 2006; 4 (02) 49-56
- 6 Greenspan SL, Myers ER, Maitland LA, Resnick NM, Hayes WC. Fall severity and bone mineral density as risk factors for hip fracture in ambulatory elderly. JAMA 1994; 271 (02) 128-133
- 7 Browner WS, Seeley DG, Vogt TM, Cummings SR. Study of Osteoporotic Fractures Research Group. Non-trauma mortality in elderly women with low bone mineral density. Lancet 1991; 338 (8763): 355-358
- 8 Hernandez CJ, Beaupré 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 2003; 14 (10) 843-847
- 9 Adami G, Saag KG. Glucocorticoid-induced osteoporosis update. Curr Opin Rheumatol 2019; 31 (04) 388-393
- 10 Wilson DJ. Osteoporosis and sport. Eur J Radiol 2019; 110: 169-174
- 11 Nguyen TV, Sambrook PN, Eisman JA. Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J Bone Miner Res 1998; 13 (09) 1458-1467
- 12 Fletcher JA. Canadian Academy of Sport and Exercise Medicine position statement: osteoporosis and exercise. Clin J Sport Med 2013; 23 (05) 333-338
- 13 Cashman KD. Diet, nutrition, and bone health. J Nutr 2007; 137 (11) 2507S-2512S
- 14 Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res 2011; 6: 30
- 15 Tomlinson DJ, Erskine RM, Morse CI, Onambélé GL. Body fat percentage, body mass index, fat mass index and the ageing bone: their singular and combined roles linked to physical activity and diet. Nutrients 2019; 11 (01) 195
- 16 Morse A, McDonald MM, Kelly NH. , et al. Mechanical load increases in bone formation via a sclerostin-independent pathway. J Bone Miner Res 2014; 29 (11) 2456-2467
- 17 Russo CR. The effects of exercise on bone. Basic concepts and implications for the prevention of fractures. Clin Cases Miner Bone Metab 2009; 6 (03) 223-228
- 18 Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone 2002; 30 (05) 781-786
- 19 Baxter-Jones ADG, Kontulainen SA, Faulkner RA, Bailey DA. A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone 2008; 43 (06) 1101-1107
- 20 Howe TE, Shea B, Dawson LJ. , et al. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev 2011; (07) CD000333
- 21 MacKnight JM. Osteopenia and osteoporosis in female athletes. Clin Sports Med 2017; 36 (04) 687-702
- 22 Whiting SJ, Vatanparast H, Baxter-Jones A, Faulkner RA, Mirwald R, Bailey DA. Factors that affect bone mineral accrual in the adolescent growth spurt. J Nutr 2004; 134 (03) 696S-700S
- 23 Kelley GA, Kelley KS, Kohrt WM. Exercise and bone mineral density in premenopausal women: a meta-analysis of randomized controlled trials. Int J Endocrinol 2013; 2013: 741639
- 24 Nordström A, Karlsson C, Nyquist F, Olsson T, Nordström P, Karlsson M. Bone loss and fracture risk after reduced physical activity. J Bone Miner Res 2005; 20 (02) 202-207
- 25 Kemmler W, Bebenek M, Kohl M, von Stengel S. Exercise and fractures in postmenopausal women. Final results of the controlled Erlangen Fitness and Osteoporosis Prevention Study (EFOPS). Osteoporos Int 2015; 26 (10) 2491-2499
- 26 Bischoff-Ferrari HA, Dawson-Hughes B, Willett WC. , et al. Effect of vitamin D on falls: a meta-analysis. JAMA 2004; 291 (16) 1999-2006
- 27 Järvinen TLN, Sievänen H, Khan KM, Heinonen A, Kannus P. Shifting the focus in fracture prevention from osteoporosis to falls. BMJ 2008; 336 (7636): 124-126
- 28 Curtis E, Litwic A, Cooper C, Dennison E. Determinants of muscle and bone aging. J Cell Physiol 2015; 230 (11) 2618-2625
- 29 Diano D, Ponti F, Guerri S. , et al. Upper and lower limbs composition: a comparison between anthropometry and dual-energy X-ray absorptiometry in healthy people. Arch Osteoporos 2017; 12 (01) 78
- 30 Guerri S, Mercatelli D, Aparisi Gómez MP. , et al. Quantitative imaging techniques for the assessment of osteoporosis and sarcopenia. Quant Imaging Med Surg 2018; 8 (01) 60-85
- 31 Tagliaferri C, Wittrant Y, Davicco M-J, Walrand S, Coxam V. Muscle and bone, two interconnected tissues. Ageing Res Rev 2015; 21: 55-70
- 32 Bonewald L. Use it or lose it to age: a review of bone and muscle communication. Bone 2019; 120: 212-218
- 33 Beck BR, Daly RM, Singh MAF, Taaffe DR. Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 2017; 20 (05) 438-445
- 34 Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 1984; 66 (03) 397-402
- 35 Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 1985; 37 (04) 411-417
- 36 Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodelling. J Biomech 1984; 17 (12) 897-905
- 37 Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 2005; 35 (09) 779-830
- 38 Rubin C, Recker R, Cullen D, Ryaby J, McCabe J, McLeod K. Prevention of postmenopausal bone loss by a low-magnitude, high-frequency mechanical stimuli: a clinical trial assessing compliance, efficacy, and safety. J Bone Miner Res 2004; 19 (03) 343-351
- 39 Bosco C, Colli R, Introini E. , et al. Adaptive responses of human skeletal muscle to vibration exposure. Clin Physiol 1999; 19 (02) 183-187
- 40 Russo CR, Lauretani F, Bandinelli S. , et al. High-frequency vibration training increases muscle power in postmenopausal women. Arch Phys Med Rehabil 2003; 84 (12) 1854-1857
- 41 Verschueren SM, Roelants M, Delecluse C, Swinnen S, Vanderschueren D, Boonen S. Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study. J Bone Miner Res 2004; 19 (03) 352-359
- 42 Lau RW, Liao L-R, Yu F, Teo T, Chung RC, Pang MY. The effects of whole body vibration therapy on bone mineral density and leg muscle strength in older adults: a systematic review and meta-analysis. Clin Rehabil 2011; 25 (11) 975-988
- 43 Gusi N, Raimundo A, Leal A. Low-frequency vibratory exercise reduces the risk of bone fracture more than walking: a randomized controlled trial. BMC Musculoskelet Disord 2006; 7 (01) 92
- 44 Bruyere O, Wuidart M-A, Di Palma E. , et al. Controlled whole body vibration to decrease fall risk and improve health-related quality of life of nursing home residents. Arch Phys Med Rehabil 2005; 86 (02) 303-307
- 45 Koopman R, van Loon LJC. Aging, exercise, and muscle protein metabolism. J Appl Physiol (1985) 2009; 106 (06) 2040-2048
- 46 Pruitt LA, Taaffe DR, Marcus R. Effects of a one-year high-intensity versus low-intensity resistance training program on bone mineral density in older women. J Bone Miner Res 1995; 10 (11) 1788-1795
- 47 Notelovitz M, Martin D, Tesar R. , et al. Estrogen therapy and variable-resistance weight training increase bone mineral in surgically menopausal women. J Bone Miner Res 1991; 6 (06) 583-590
- 48 Martin D, Notelovitz M. Effects of aerobic training on bone mineral density of postmenopausal women. J Bone Miner Res 1993; 8 (08) 931-936
- 49 Nikander R, Kannus P, Dastidar P. , et al. Targeted exercises against hip fragility. Osteoporos Int 2009; 20 (08) 1321-1328
- 50 Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JAL. Exercise and bone mass in adults. Sports Med 2009; 39 (06) 439-468
- 51 Gómez-Bruton A, Gónzalez-Agüero A, Gómez-Cabello A, Casajús JA, Vicente-Rodríguez G. Is bone tissue really affected by swimming? A systematic review. PLOS One 2013; 8 (08) e70119
- 52 Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res 2011; 25 (03) 727-734
- 53 Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med 2007; 41 (10) 664-668 ; discussion 668
- 54 Nattiv A, Kennedy G, Barrack MT. , et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med 2013; 41 (08) 1930-1941
- 55 Martyn-St James M, Carroll S. Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 2008; 43 (03) 521-531
- 56 Ma D, Wu L, He Z. Effects of walking on the preservation of bone mineral density in perimenopausal and postmenopausal women: a systematic review and meta-analysis. Menopause 2013; 20 (11) 1216-1226
- 57 Velez NF, Zhang A, Stone B, Perera S, Miller M, Greenspan SL. The effect of moderate impact exercise on skeletal integrity in master athletes. Osteoporos Int 2008; 19 (10) 1457-1464
- 58 Alfredson H, Nordström P, Lorentzon R. Bone mass in female volleyball players: a comparison of total and regional bone mass in female volleyball players and nonactive females. Calcif Tissue Int 1997; 60 (04) 338-342
- 59 Bagur-Calafat C, Farrerons-Minguella J, Girabent-Farrés M, Serra-Grima JR. The impact of high level basketball competition, calcium intake, menses, and hormone levels in adolescent bone density: a three-year follow-up. J Sports Med Phys Fitness 2015; 55 (1-2): 58-67
- 60 Snow CM, Williams DP, LaRiviere J, Fuchs RK, Robinson TL. Bone gains and losses follow seasonal training and detraining in gymnasts. Calcif Tissue Int 2001; 69 (01) 7-12
- 61 Tsuzuku S, Ikegami Y, Yabe K. Effects of high-intensity resistance training on bone mineral density in young male powerlifters. Calcif Tissue Int 1998; 63 (04) 283-286
- 62 Matthews BL, Bennell KL, McKay HA. , et al. Dancing for bone health: a 3-year longitudinal study of bone mineral accrual across puberty in female non-elite dancers and controls. Osteoporos Int 2006; 17 (07) 1043-1054
- 63 Kontulainen S, Sievänen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 2003; 18 (02) 352-359
- 64 Kohrt WM, Barry DW, Schwartz RS. Muscle forces or gravity: what predominates mechanical loading on bone?. Med Sci Sports Exerc 2009; 41 (11) 2050-2055
- 65 Zehnacker CH, Bemis-Dougherty A. Effect of weighted exercises on bone mineral density in postmenopausal women. A systematic review. J Geriatr Phys Ther 2007; 30 (02) 79-88
- 66 Zhao R, Zhao M, Xu Z. The effects of differing resistance training modes on the preservation of bone mineral density in postmenopausal women: a meta-analysis. Osteoporos Int 2015; 26 (05) 1605-1618
- 67 Wilhelm M, Roskovensky G, Emery K, Manno C, Valek K, Cook C. Effect of resistance exercises on function in older adults with osteoporosis or osteopenia: a systematic review. Physiother Can 2012; 64 (04) 386-394
- 68 Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American College of Sports Medicine. American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc 2004; 36 (11) 1985-1996
- 69 Teixeira LEPP, Silva KNG, Imoto AM. , et al. Progressive load training for the quadriceps muscle associated with proprioception exercises for the prevention of falls in postmenopausal women with osteoporosis: a randomized controlled trial. Osteoporos Int 2010; 21 (04) 589-596
- 70 Chow TH, Lee BY, Ang ABF, Cheung VYK, Ho MMC, Takemura S. The effect of Chinese martial arts Tai Chi Chuan on prevention of osteoporosis: A systematic review. J Orthop Translat 2017; 12: 74-84
- 71 Huntoon EA, Schmidt CK, Sinaki M. Significantly fewer refractures after vertebroplasty in patients who engage in back-extensor-strengthening exercises. Mayo Clin Proc 2008; 83 (01) 54-57
- 72 Moreira L, Fronza FCAO, dos Santos RN, Teixeira LR, Kruel LFM, Lazaretti-Castro M. High-intensity aquatic exercises (HydrOS) improve physical function and reduce falls among postmenopausal women. Menopause 2013; 20 (10) 1012-1019
- 73 Aparisi Gómez MP. Nonspinal fragility fractures. Semin Musculoskelet Radiol 2016; 20 (04) 330-344
- 74 Barrack MT, Gibbs JC, De Souza MJ. , et al. Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med 2014; 42 (04) 949-958
- 75 Gourlay M, Franceschini N, Sheyn Y. Prevention and treatment strategies for glucocorticoid-induced osteoporotic fractures. Clin Rheumatol 2007; 26 (02) 144-153
- 76 Bultink IEM, Baden M, Lems WF. Glucocorticoid-induced osteoporosis: an update on current pharmacotherapy and future directions. Expert Opin Pharmacother 2013; 14 (02) 185-197
- 77 Nazem TG, Ackerman KE. The female athlete triad. Sports Health 2012; 4 (04) 302-311
- 78 Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med 1994; 13 (02) 405-418
- 79 Dusek T. Influence of high intensity training on menstrual cycle disorders in athletes. Croat Med J 2001; 42 (01) 79-82
- 80 Bachmann GA, Kemmann E. Prevalence of oligomenorrhea and amenorrhea in a college population. Am J Obstet Gynecol 1982; 144 (01) 98-102
- 81 Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med 2004; 14 (01) 25-32
- 82 Khan KM, Liu-Ambrose T, Sran MM, Ashe MC, Donaldson MG, Wark JD. New criteria for female athlete triad syndrome? As osteoporosis is rare, should osteopenia be among the criteria for defining the female athlete triad syndrome?. Br J Sports Med 2002; 36 (01) 10-13
-
83
International Society for Clinical Densitometry.
Updated 2015 official positions for the International Society for Clinical Densitometry. http://www.iscd.org/Visitors/positions/OfficialPositionsText.cfm . Accessed November 20, 2019
- 84 Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 2007; 39 (10) 1867-1882
- 85 Torstveit MK, Sundgot-Borgen J. The female athlete triad exists in both elite athletes and controls. Med Sci Sports Exerc 2005; 37 (09) 1449-1459
- 86 Perregaux D, Chaudhuri A, Mohanty P. , et al. Effect of gender differences and estrogen replacement therapy on vascular reactivity. Metabolism 1999; 48 (02) 227-232
- 87 Harber VJ, Petersen SR, Chilibeck PD. Thyroid hormone concentrations and muscle metabolism in amenorrheic and eumenorrheic athletes. Can J Appl Physiol 1998; 23 (03) 293-306
- 88 Shaffer RA, Rauh MJ, Brodine SK, Trone DW, Macera CA. Predictors of stress fracture susceptibility in young female recruits. Am J Sports Med 2006; 34 (01) 108-115
- 89 Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med 1999; 28 (02) 91-122
- 90 Drinkwater BL, Bruemner B, Chesnut III CH. Menstrual history as a determinant of current bone density in young athletes. JAMA 1990; 263 (04) 545-548
- 91 Kreipe RE, Forbes GB. Osteoporosis: a “new morbidity” for dieting female adolescents?. Pediatrics 1990; 86 (03) 478-480
- 92 Manore MM, Kam LC, Loucks AB. International Association of Athletics Federations. The female athlete triad: components, nutrition issues, and health consequences. J Sports Sci 2007; 25 (Suppl. 01) S61-S71
- 93 Arcelus J, Mitchell AJ, Wales J, Nielsen S. Mortality rates in patients with anorexia nervosa and other eating disorders. A meta-analysis of 36 studies. Arch Gen Psychiatry 2011; 68 (07) 724-731
- 94 Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sports Med 2016; 46 (02) 171-182
- 95 Hackney AC, Fahrner CL, Gulledge TP. Basal reproductive hormonal profiles are altered in endurance trained men. J Sports Med Phys Fitness 1998; 38 (02) 138-141
- 96 Hackney AC. Endurance exercise training and reproductive endocrine dysfunction in men: alterations in the hypothalamic-pituitary-testicular axis. Curr Pharm Des 2001; 7 (04) 261-273
- 97 Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec CY. Decrease in serum leptin after prolonged physical activity in men. Med Sci Sports Exerc 2002; 34 (10) 1594-1599
- 98 Dolan E, Crabtree N, McGoldrick A, Ashley DT, McCaffrey N, Warrington GD. Weight regulation and bone mass: a comparison between professional jockeys, elite amateur boxers, and age, gender and BMI matched controls. J Bone Miner Metab 2012; 30 (02) 164-170
- 99 Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone 2006; 39 (04) 880-885
- 100 Tenforde AS, Fredericson M, Sayres LC, Cutti P, Sainani KL. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med 2015; 43 (06) 1494-1504