Bone health in endurance athletes: Runners, cyclists, and swimmers

Current Sports Medicine Reports

Volumn 11, Issue 6, 2012, Pages 328-334

  Scofield, Kirk L ^a,b   Hecht, Suzanne ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Summit Orthopedics Ltd Minnesota   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; ORAL CONTRACEPTIVE AGENT; VITAMIN D; VITAMIN K GROUP;

ATHLETE; BONE; BONE DENSITY; BONE STRESS; CYCLING; DUAL ENERGY X RAY ABSORPTIOMETRY; ENDURANCE SPORT; ENERGY; EXERCISE; FAT FREE MASS; FRAGILITY FRACTURE; HUMAN; OSTEOLYSIS; OSTEOPOROSIS; REVIEW; RUNNING; STRESS FRACTURE; SWIMMING; TRIATHLON;

EID: 84872232777     PISSN: 1537890X     EISSN: 15378918     Source Type: Journal    
DOI: 10.1249/JSR.0b013e3182779193     Document Type: Review

References (77)

1. Arendt E, Agel J, Heikes C, Griffiths H. Stress injuries to bone in college athletes: a retrospective review of experience at a single institution. Am. J. Sports Med. 2003; 31: 959-68.
2. Barrack MT, Rauh MJ, Barkai HS, Nichols JF. Dietary restraint and low bone mass in female adolescent endurance runners. Am. J. Clin. Nutr. 2008; 87: 36-43.
3. Barrack MT, Rauh MJ, Nichols JF. Cross-sectional evidence of suppressed bone mineral accrual among female adolescent runners. J. Bone Miner. Res. 2010; 25: 1850-7.
4. Barrack MT, Rauh MJ, Nichols JF. Prevalence of and traits associated with low BMD among female adolescent runners. Med. Sci. Sports Exerc. 2008; 40: 2015-21.
5. BarryDW, Hansen KC, van Pelt RE, et al. Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Med. Sci. Sports Exerc. 2011; 43: 617-23.
6. Baxter-Jones AD, Faulkner RA, Forwood MR, et al. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J. Bone Miner. Res. 2011; 26: 1729-39.
7. Bennell KL, Brukner PD. Epidemiology and site specificity of stress fractures. Clin. Sports Med. 1997; 16: 179-96.
8. Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long distance runners. Med. Sci. Sports Exerc. 1989; 21: 66-70.
9. Boreham CA, McKay HA. Physical activity in childhood and bone health. Br. J. Sports Med. 2011; 45: 877-9.
10. Brubaker CE, James SL. Injuries to runners. J. Sports Med. 1974; 2: 189-98.
11. Burgi AA, Gorham ED, Garland CF, et al. High serum 25-hydroxyvitamin D is associated with a low incidence of stress fractures. J. Bone Miner. Res. 2011; 26: 2371-7.
12. Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. 2002; 30: 781-6.
13. Carbuhn AF, Fernandez TE, Bragg AF, et al. Sport and training influence bone and body composition in women collegiate athletes. J. Strength Cond. Res. 2010; 24: 1710-7.
14. Caronia LM, Martin C, Welt CK, et al. A genetic basis for functional hypothalamic amenorrhea. N. Engl. J. Med. 2011; 364: 215-25.
15. Chou SH, Chamberland JP, Liu X, et al. Leptin is an effective treatment for hypothalamic amenorrhea. Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 6585-90.
16. Christo K, Cord J, Mendes N, et al. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study. Clin. Endocrinol. (Oxf). 2008; 69: 628-33.
17. Christo K, Prabhakaran R, Lamparello B, et al. Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics. 2008; 121: 1127-36.
18. Cobb KL, Bachrach LK, Sowers M, et al. The effect of oral contraceptives on bone mass and stress fractures in female runners. Med. Sci. Sports Exerc. 2007; 39: 1464-73.
19. De Souza MJ, Arce JC, Pescatello LS, et al. Gonadal hormones and semen quality in male runners. Avolume threshold effect of endurance training. Int. J. Sports Med. 1994; 15: 383-91.
20. Dias Quiterio AL, Carnero EA, Baptista FM, Sardinha LB. Skeletal mass in adolescent male athletes and nonathletes: relationships with high-impact sports. J. Strength Cond. Res. 2011; 25: 3439-47.
21. Drysdale IP, Collins AL, Walters NJ, et al. Potential benefits of marathon training on bone health as assessed by calcaneal broadband ultrasound attenuation. J. Clin. Densitom. 2007; 10: 179-83.
22. Ducher G, Turner AI, Kukuljan S, et al. Obstacles in the optimization of bone health outcomes in the female athlete triad. Sports Med. 2011; 41: 587-607.
23. Duncan CS, Blimkie CJ, Cowell CT, et al. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med. Sci. Sports Exerc. 2002; 34: 286-94.
24. Edwards WB, Taylor D, Rudolphi TJ, et al. Effects of stride length and running mileage on a probabilistic stress fracture model. Med. Sci. Sports Exerc. 2009; 41: 2177-84.
25. Emslander HC, Sinaki M, Muhs JM, et al. Bone mass and muscle strength in female college athletes (runners and swimmers). Mayo Clin. Proc. 1998; 73: 1151-60.
26. Fanning J, Larrick L, Weinstein L, et al. Findings from a 10-year follow-up of bone mineral density in competitive perimenopausal runners. J. Reprod. Med. 2007; 52: 874-8.
27. Feldman S, Capozza RF, Mortarino PA, et al. Site and sex effects on tibia structure in distance runners and untrained people. Med. Sci. Sports Exerc. 2012.
28. Ferrari S, Bianchi ML, Eisman JA, et al For the IOF Committee of Scientific Advisors Working Group on Osteoporosis Pathophysiology. Osteoporosis in young adults: pathophysiology, diagnosis, and management. Osteoporos. Int. 2012.
29. Franks PW, Farooqi IS, Luan J, et al. Does physical activity energy expenditure explain the between-individual variation in plasma leptin concentrations after adjusting for differences in body composition? J. Clin. Endocrinol. Metab. 2003; 88: 3258-63.
30. Fredericson M, Chew K, Ngo J, et al. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br. J. Sports Med. 2007; 41: 664,8; discussion 668.
31. Fredericson M, Jennings F, Beaulieu C, Matheson GO. Stress fractures in athletes. Top Magn. Reson. Imaging. 2006; 17: 309-25.
32. Fredericson M, Ngo J, Cobb K. Effects of ball sports on future risk of stress fracture in runners. Clin. J. Sport Med. 2005; 15: 136-41.
33. Guillemant J, Accarie C, Peres G, Guillemant S. Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif. Tissue Int. 2004; 74: 407-14.
34. Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise: development of the "exercise-hypogonadal male condition". Acta Physiol. Hung. 2005; 92: 121-37.
35. Hackney AC. Effects of endurance exercise on the reproductive system of men: the "exercise-hypogonadal male condition". J. Endocrinol. Invest. 2008; 31: 932-8.
36. Harrast MA, Colonno D. Stress fractures in runners. Clin. Sports Med. 2010; 29: 399-416.
37. Hartard M, Kleinmond C, Kirchbichler A, et al. Age at first oral contraceptive use as a major determinant of vertebral bone mass in female endurance athletes. Bone. 2004; 35: 836-41.
38. Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J. Clin. Endocrinol. Metab. 1993; 77: 770-5.
39. Hind K, Gannon L, Whatley E, et al. Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: a hip-structural analysis study. Eur. J. Appl. Physiol. 2012; 112: 535-41.
40. Hoch AZ, Stavrakos JE, Schimke JE. Prevalence of female athlete triad characteristics in a club triathlon team. Arch. Phys. Med. Rehabil. 2007; 88: 681-2.
41. Horvath PJ, Eagen CK, Fisher NM, et al. The effects of varying dietary fat on performance and metabolism in trained male and female runners. J. Am. Coll. Nutr. 2000; 19: 52-60.
42. Horvath PJ, Eagen CK, Ryer-Calvin SD, Pendergast DR. The effects of varying dietary fat on the nutrient intake in male and female runners. J. Am. Coll. Nutr. 2000; 19: 42-51.
43. Karlsson MK, Rosengren BE. Training and bone V from health to injury. Scand. J. Med. Sci. Sports. 2012.
44. Kelsey JL, Bachrach LK, Procter-Gray E, et al. Risk factors for stress fracture among young female cross-country runners. Med. Sci. Sports Exerc. 2007; 39: 1457-63.
45. Lappe J, Cullen D, Haynatzki G, et al. Calcium and vitamin d supplementation decreases incidence of stress fractures in female navy recruits. J. Bone Miner. Res. 2008; 23: 741-9.
46. Lappe JM, Stegman MR, Recker RR. The impact of lifestyle factors on stress fractures in female Army recruits. Osteoporos. Int. 2001; 12: 35-42.
47. Lebrun CM. The female athlete triad: what's a doctor to do? Curr. Sports Med. Rep. 2007; 6: 397-404.
48. Lips P, Bouillon R, van Schoor NM, et al. Reducing fracture risk with calcium and vitamin D. Clin. Endocrinol. (Oxf). 2010; 73: 277-85.
49. Lloyd T, Triantafyllou SJ, Baker ER, et al. Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med. Sci. Sports Exerc. 1986; 18: 374-9.
50. Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007; 37: 348-52.
51. Maimoun L, Galy O, Manetta J, et al. Competitive season of triathlon does not alter bone metabolism and bone mineral status in male triathletes. Int. J. Sports Med. 2004; 25: 230-4.
52. McClanahan BS, Ward KD, Vukadinovich C, et al. Bone mineral density in triathletes over a competitive season. J. Sports Sci. 2002; 20: 463-9.
53. Milner CE, Hamill J, Davis IS. Distinct hip and rearfoot kinematics in female runners with a history of tibial stress fracture. J. Orthop. Sports Phys. Ther. 2010; 40: 59-66.
54. Mirsa M, Le Clair M, Mendes N. Use of SSRIs may impact bone density in adolescent and young women with anorexia nervosa. CNS Spectr. 2010; 15: 579-86.
55. Moayyeri A. The association between physical activity and osteoporotic fractures: a review of the evidence and implications for future research. Ann. Epidemiol. 2008; 18: 827-35.
56. Mudd LM, Fornetti W, Pivarnik JM. Bone mineral density in collegiate female athletes: comparisons among sports. J. Athl. Train. 2007; 42: 403-8.
57. Nagle KB, Brooks MA. A systematic review of bone health in cyclists. Sports Health. 2011; 3: 235-43.
58. Nattiv A, Loucks AB, Manore MM, et al American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med. Sci. Sports Exerc. 2007; 39: 1867-82.
59. Nichols JF, Rauh MJ, Barrack MT, Barkai HS. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone. 2007; 41: 371-7.
60. Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J. Strength Cond. Res. 2011; 25: 727-34.
61. Pollock N, Grogan C, Perry M, et al. Bone-mineral density and other features of the female athlete triad in elite endurance runners: a longitudinal and cross-sectional observational study. Int. J. Sport Nutr. Exerc. Metab. 2010; 20: 418-26.
62. Popp KL, Hughes JM, Smock AJ, et al. Bone geometry, strength, and muscle size in runners with a history of stress fracture. Med. Sci. Sports Exerc. 2009; 41: 2145-50.
63. Robling AG, Turner CH. Mechanical signaling for bone modeling and remodeling. Crit. Rev. Eukaryot. Gene. Expr. 2009; 19: 319-38.
64. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J. Bone Joint Surg. Am. 1984; 66: 397-402.
65. Smock AJ, Hughes JM, Popp KL, et al. Bone volumetric density, geometry, and strength in female and male collegiate runners. Med. Sci. Sports Exerc. 2009; 41: 2026-32.
66. Snyder RA, Koester MC, Dunn WR. Epidemiology of stress fractures. Clin Sports Med. 2006; 25: 37,52, viii.
67. Taaffe DR, Robinson TL, Snow CM, Marcus R. High-impact exercise promotes bone gain in well-trained female athletes. J. Bone Miner. Res. 1997; 12: 255-60.
68. Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature. PM R. 2011; 3: 861-7.
69. Umemura Y, Ishiko T, Yamauchi T, et al. Five jumps per day increase bone mass and breaking force in rats. J. Bone Miner. Res. 1997; 12: 1480-5.
70. Vescovi JD, Jamal SA, De Souza MJ. Strategies to reverse bone loss in women with functional hypothalamic amenorrhea: a systematic review of the literature. Osteoporos. Int. 2008; 19: 465-78.
71. Warren MP, Miller KK, Olson WH, et al. Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in women with hypothalamic amenorrhea and osteopenia: an open-label extension of a double-blind, placebo-controlled study. Contraception. 2005; 72: 206-11.
72. Wilks DC, Winwood K, Gilliver SF, et al. Bone mass and geometry of the tibia and the radius ofmaster sprinters,middle and long distance runners, race-walkers and sedentary control participants: a pQCT study. Bone. 2009; 45: 91-7.
73. Wilks DC, Winwood K, Gilliver SF, et al. Age-dependency in bone mass and geometry: a pQCT study on male and female master sprinters, middle and long distance runners, race-walkers and sedentary people. J. Musculoskelet. Neuronal Interact. 2009; 9: 236-46.
74. Wiswell RA, Hawkins SA, Dreyer HC, Jaque SV. Maintenance of BMD in older male runners is independent of changes in training volume or VO(2)peak. J Gerontol. A Biol. Sci. Med. Sci. 2002; 57: M203-8.
75. Wolff J. The Law of Bone Transformation. Berlin: A. Hirschwald; 1892.
76. Writing Group for the ISCD Position Development Conference. Diagnosis of osteoporosis in men, premenopausal women, and children. J. Clin. Densitom. 2004; 7: 17-26.
77. Zadpoor AA, Nikooyan AA. The relationship between lower-extremity stress fractures and the ground reaction force: a systematic review. Clin. Biomech. (Bristol, Avon). 2011; 26: 23-8.