Influence of physical activity on bone strength in children and adolescents: A systematic review and narrative synthesis

Journal of Bone and Mineral Research

Volumn 29, Issue 10, 2014, Pages 2161-2181

  Tan, Vina P S ^a,b,c   Macdonald, Heather M ^a,b,d   Kim, SoJung ^a,b   Nettlefold, Lindsay ^b   Gabel, Leigh ^a,b,d   Ashe, Maureen C ^a,b   McKay, Heather A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

^c SCHOOL OF HEALTH SCIENCES   (Malaysia)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adolescent; Bone strength; Child; Physical activity; Systematic review

Indexed keywords

ADOLESCENT HEALTH; BONE DENSITY; BONE MASS; BONE STRENGTH; BONE STRUCTURE; CHILD HEALTH; HUMAN; MUSCLE; PHYSICAL ACTIVITY; PREPUBERTY; REVIEW; SEX DIFFERENCE; SPORT; SYSTEMATIC REVIEW; ADOLESCENT; BIOMECHANICS; BONE; CHILD; FEMALE; MALE; META ANALYSIS; MOTOR ACTIVITY; OBSERVATIONAL STUDY; ORGAN SIZE; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

ADOLESCENT; BIOMECHANICAL PHENOMENA; BONE AND BONES; CHILD; FEMALE; HUMANS; MALE; MOTOR ACTIVITY; OBSERVATIONAL STUDY AS TOPIC; ORGAN SIZE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SPORTS;

EID: 84903621449     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2254     Document Type: Review

References (100)

1. Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26(8):1729-39.
2. Forwood MR. Growing a healthy skeleton: the importance of mechanical loading. In: Rosen CJ, Bouillon R, Compston JE, Rosen V Primer on the metabolic diseases and disorders of mineral metabolism. Hoboken, NJ: John Wiley & Sons, Inc; p. 149-55. 2013.
3. Tarride J-E, Hopkins RB, Leslie WD, et al. The burden of illness of osteoporosis in Canada. Osteoporos Int. 2012;23(11):2591-600.
4. Behringer M, Gruetzner S, McCourt M, Mester J. Effects of weight-bearing activities on bone mineral content and density in children and adolescents: a meta-analysis. J Bone Miner Res. 2014;29(2):467-78.
5. Hind K, Burrows M. Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials. Bone. 2007;40(1):14-27.
6. MacKelvie KJ, Khan KM, McKay HA. Is there a critical period for bone response to weight-bearing exercise in children and adolescents? A systematic review. Br J Sports Med. 2002;36(4):250-7.
7. Ishikawa S, Kim Y, Kang M, Morgan DW. Effects of weight-bearing exercise on bone health in girls: a meta-analysis. Sports Med. 2013;43(9):875-92.
8. Bailey DA, McKay HA, Mirwald RL, Crocker PRE, Faulkner RA. A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the University of Saskatchewan Bone Mineral Accrual Study. J Bone Miner Res. 1999;14(10):1672-9.
9. 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(6):1101-7.
10. McKay H, Smith E. Winning the battle against childhood physical inactivity: the key to bone strength? J Bone Miner Res. 2008;23(7):980-5.
11. Hamrick M. JMNI special issue: Basic science and mechanisms of muscle-bone interactions. J Musculoskelet Neuronal Interact. 2010;10(1):1-2.
12. Frost HM. Muscle, bone, and the Utah paradigm: a 1999 overview. Med Sci Sports Exerc. 2000;32(5):911-7.
13. Bonnet N, Ferrari SL. Exercise and the skeleton: how it works and what it really does. IBMS Bonekey. 2010;7(7):235-48.
14. Beck T. Measuring the structural strength of bones with dual-energy X-ray absorptiometry: principles, technical limitations, and future possibilities. Osteoporos Int. 2003;14(0):81-8.
15. Einhorn TA. Bone strength: the bottom line. Calcif Tissue Int. 1992;51(5):333-9.
16. Carter DR, Bouxsein ML, Marcus R. New approaches for interpreting projected bone densitometry data. J Bone Miner Res. 1992;7(2):137-45.
17. Sievänen H, Kannus P, Nieminen V, Heinonen A, Oja P, Vuori I. Estimation of various mechanical characteristics of human bones during dual energy x-ray absorptiometry: methodology and precision. Bone. 1996;18(1):S17-27.
18. Beck TJ. Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep. 2007;5(2):49-55.
19. Karlamangla AS, Barrett-Connor E, Young J, Greendale GA. Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int. 2004;15(1):62-70.
20. Griffith JF, Genant HK. New imaging modalities in bone. Curr Rheumatol Rep. 2011;13(3):241-50.
21. Burrows M, Liu D, Moore S, McKay H. Bone microstructure at the distal tibia provides a strength advantage to males in late puberty: a HR-pQCT study. J Bone Miner Res. 2010;25(6):1423-32.
22. Högler W, Blimkie CJR, Cowell CT, et al. Sex-specific developmental changes in muscle size and bone geometry at the femoral shaft. Bone. 2008;42(5):982-9.
23. Sarin VK, Loboa Polefka EG, Beaupré GS, Kiratli BJ, Carter DR, van der Meulen MC. DXA-derived section modulus and bone mineral content predict long-bone torsional strength. Acta Orthop Scand. 1999;70(1):71-6.
24. Liu D, Manske S, Kontulainen S, et al. Tibial geometry is associated with failure load ex vivo: a MRI, pQCT and DXA study. Osteoporos Int. 2007;18(7):991-7.
25. Nikander R, Sievänen H, Heinonen A, Daly R, Uusi-Rasi K, Kannus P. Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med. 2010;8(1):47.
26. Fleurence RL, Naci H, Jansen JP. The critical role of observational evidence in comparative effectiveness research. Health Aff (Millwood). 2010;29(10):1826-33.
27. Centre for Reviews and Dissemination. Systematic reviews: CRD's guidance for undertaking reviews in health care. York, UK: York Publishing Services Ltd; 2009.
28. Popay J, Roberts H, Sowden A, et al., Guidance on the conduct of narrative synthesis in systematic reviews. Swindon, UK: Economic and Social Research Council (ESRC) Research Methods Programme. 2006.
29. Moher D, Liberati A, Tetzlaff J. Altman DG; The PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA statement. Ann Intern Med. 2009;151(4): 264-9.
30. Kastner M, Wilczynski NL, Walker-Dilks C, McKibbon KA, Haynes B. Age-specific search strategies for Medline. J Med Internet Res. 2006;8(4):e25.
31. Bouxsein ML, Karasik D. Bone geometry and skeletal fragility. Curr Osteoporos Rep. 2006;4(2):49-56.
32. Manske SL, Macdonald HM, Nishiyama KK, Boyd SK, McKay HA. Clinical tools to evaluate bone strength. Clin Rev Bone Miner Metab. 2010;8(3):122-34.
33. Kontulainen SA, Johnston JD, Liu D, et al. Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact. 2008;8(4):401-9.
34. Thomas BH, Ciliska D, Dobbins M, Micucci S. A process for systematically reviewing the literature: providing the research evidence for public health nursing interventions. Worldviews Evid Based Nurs. 2004;1(3):176-84.
35. Preedy VR, Watson RR. editors. Handbook of disease burdens and quality of life measures. New York: Springer; 2010.
36. Rodgers M, Sowden A, Petticrew M, et al. Testing methodological guidance on the conduct of narrative synthesis in systematic reviews effectiveness of interventions to promote smoke alarm ownership and function. Evaluation. 2009;15(1):49-73.
37. Macdonald H, Kontulainen S, Mackelvie-O'Brien K, et al. Maturity- and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. Bone. 2005;36(6):1003-11.
38. Dempster DW, Compston JE, Drezner MK, et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 2013;28(1):2-17.
39. Weeks BK, Young CM, Beck BR. Eight months of regular in-school jumping improves indices of bone strength in adolescent boys and girls: the POWER PE Study. J Bone Miner Res. 2008;23(7):1002-11.
40. Heinonen A, Sievänen H, Kannus P, Oja P, Pasanen M, Vuori I. High-impact exercise and bones of growing girls: a 9-month controlled trial. Osteoporos Int. 2000;11(12):1010-7.
41. Greene DA, Wiebe PN, Naughton GA. Influence of drop-landing exercises on bone geometry and biomechanical properties in prepubertal girls: a randomized controlled study. Calcif Tissue Int. 2009;85(2):94-103.
42. MacKelvie K, Petit M, Khan K, Beck T, Choi H. Bone mass and structure are enhanced following a 2-year randomized controlled trial of exercise in prepubertal boys. Bone. 2004;34(4):755-64.
43. Petit MA, McKay HA, MacKelvie KJ, Heinonen A, Khan KM, Beck TJ. A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res. 2002;17(3):363-72.
44. Alwis G, Linden C, Ahlborg HG, Dencker M, Gardsell P, Karlsson MK. A 2-year school-based exercise programme in pre-pubertal boys induces skeletal benefits in lumbar spine. Acta Paediatr. 2008;97(11):1564-71.
45. Alwis G, Linden C, Stenevi-Lundgren S, et al. A one-year exercise intervention program in pre-pubertal girls does not influence hip structure. BMC Musculoskelet Disord. 2008;9(1):9.
46. Alwis G, Linden C, Stenevi-Lundgren S, et al. A school-curriculum-based exercise intervention program for two years in pre-pubertal girls does not influence hip structure. Dyn Med. 2008;7(1):8.
47. McKay HA, McLean L, Petit M, MacKelvie-O'Brian K, Jansen P, Beck T, Khan KM. "Bounce at the Bell": a novel program of short bouts of exercise improves proximal femur bone mass in early pubertal children. Br J Sports Med. 2005;39(8):521-6.
48. Anliker E, Dick C, Rawer R, Toigo M. Effects of jumping exercise on maximum ground reaction force and bone in 8-to 12-year-old boys and girls: a 9-month randomized controlled trial. J Musculoskelet Neuronal Interact. 2012;12(2):56-67.
49. Macdonald HM, Kontulainen SA, Khan KM, McKay HA. Is a school-based physical activity intervention effective for increasing tibial bone strength in boys and girls? J Bone Miner Res. 2007;22(3):434-46.
50. Macdonald HM, Kontulainen SA, Petit MA, Beck TJ, Khan KM, McKay HA. Does a novel school-based physical activity model benefit femoral neck bone strength in pre- and early pubertal children? Osteoporos Int. 2008;19(10):1445-56.
51. Macdonald HM, Cooper DML, McKay HA. Anterior-posterior bending strength at the tibial shaft increases with physical activity in boys: evidence for non-uniform geometric adaptation. Osteoporos Int. 2009;20(1):61-70.
52. Bradney M, Pearce G, Naughton G, et al. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res. 1998;13(12):1814-21.
53. Janz KF, Burns TL, Levy SM, et al. Everyday activity predicts bone geometry in children: the Iowa bone development study. Med Sci Sports Exerc. 2004;36(7):1124-31.
54. Sardinha LB, Baptista F, Ekelund U. Objectively measured physical activity and bone strength in 9-year-old boys and girls. Pediatrics. 2008;122(3):e728-36.
55. Janz KF, Gilmore JME, Levy SM, Letuchy EM, Burns TL, Beck TJ. Physical activity and femoral neck bone strength during childhood: The Iowa Bone Development Study. Bone. 2007;41(2):216-22.
56. McKay H, Liu D, Egeli D, Boyd S, Burrows M. Physical activity positively predicts bone architecture and bone strength in adolescent males and females. Acta Paediatr. 2011;100(1):97-101.
57. Moyer-Mileur L, Xie B, Ball S, Bainbridge C, Stadler D, Jee WSS. Predictors of bone mass by peripheral quantitative computed tomography in early adolescent girls. J Clin Densitom. 2001;4(4):313-23.
58. Farr JN, Blew RM, Lee VR, Lohman TG, Going SB. Associations of physical activity duration, frequency, and load with volumetric BMD, geometry, and bone strength in young girls. Osteoporos Int. 2011;22(5):1419-30.
59. Wang QJ, Suominen H, Nicholson PHF, et al. Infl uence of physical activity and maturation status on bone mass and geometry in early pubertal girls. Scand J Med Sci Sports. 2005;15(2):100-6.
60. Kowalski KC, Crocker PRE, Faulkner RA. Validation of the physical activity questionnaire for older children. Pediatr Exerc Sci. 1997;9:174-86.
61. Forwood MR, Baxter-Jones AD, Beck TJ, Mirwald RL, Howard A, Bailey DA. Physical activity and strength of the femoral neck during the adolescent growth spurt: a longitudinal analysis. Bone. 2006;38(4):576-83.
62. Bhattacharya A, Watts NB, Gordon J, et al. Bone quantity and quality of youths working on a farm - a pilot study. J Agromedicine. 2008;12(4):27-38.
63. Kardinaal AFM, Hoorneman G, Väänänen K, et al. Determinants of bone mass and bone geometry in adolescent and young adult women. Calcif Tissue Int. 2000;66(2):81-9.
64. Bass SL, Saxon L, Daly RM, et al. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res. 2002;17(12):2274-80.
65. Greene DA, Naughton GA, Briody JN, Kemp A, Woodhead H, Corrigan L. Bone strength index in adolescent girls: does physical activity make a difference? Br J Sports Med. 2005;39(9):622-7.
66. Ferry B, Duclos M, Burt L, et al. Bone geometry and strength adaptations to physical constraints inherent in different sports: comparison between elite female soccer players and swimmers. J Bone Miner Metab. 2011;29(3):342-51.
67. Duncan CS, Blimkie CJR, Kemp A, et al. Mid-femur geometry and biomechanical properties in 15-to 18-yr-old female athletes. Med Sci Sports Exerc. 2002;34(4):673.
68. Dowthwaite JN, Rosenbaum PF, Scerpella TA. Mechanical loading during growth is associated with plane-specific differences in vertebral geometry: a cross-sectional analysis comparing artistic gymnasts vs. non-gymnasts. Bone. 2011;49(5):1046-54.
69. Faulkner RA, Forwood MR, Beck TJ, Mafukidze JC, Russell K, Wallace W. Strength indices of the proximal femur and shaft in prepubertal female gymnasts. Med Sci Sports Exerc. 2003;35(3):513-8.
70. Dowthwaite JN, Flowers PPE, Spadaro JA, Scerpella TA. Bone geometry, density, and strength indices of the distal radius reflect loading via childhood gymnastic activity. J Clin Densitom. 2007; 10(1):65-75.
71. Tournis S, Michopoulou E, Fatouros IG, et al. Effect of rhythmic gymnastics on volumetric bone mineral density and bone geometry in premenarcheal female athletes and controls. J Clin Endocrinol Metab. 2010;95(6):2755-62.
72. Erlandson MC, Kontulainen SA, Baxter-Jones ADG. Precompetitive and recreational gymnasts have greater bone density, mass, and estimated strength at the distal radius in young childhood. Osteoporos Int. 2011;22(1):75-84.
73. Burt LA, Naughton GA, Greene DA, Courteix D, Ducher G. Non-elite gymnastics participation is associated with greater bone strength, muscle size, and function in pre- and early pubertal girls. Osteoporos Int. 2012;23(4):1277-86.
74. Ward K, Roberts S, Adams J, Mughal M. Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children. Bone. 2005;36(6):1012-8.
75. Beck TJ, Ruff CB, Warden KE, Scott WW, Rao GU. Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol. 1990;25:6-18.
76. Dowthwaite JN, Scerpella TA. Distal radius geometry and skeletal strength indices after peripubertal artistic gymnastics. Osteoporos Int. 2011;22(1):207-16.
77. Dowthwaite JN, Rosenbaum PF, Scerpella TA. Site-specific advantages in skeletal geometry and strength at the proximal femur and forearm in young female gymnasts. Bone. 2012;50(5):1173-83.
78. Forwood M. Physical activity and bone development during childhood: insights from animal models. J Appl Physiol. 2008;105:334-41.
79. Rubin CT, Lanyon LE. Osteoregulatory nature of mechanical stimuli: Function as a determinant for adaptive remodeling in bone. J Orthop Res. 1987;5(2):300-10.
80. Robling AG, Hinant FM, Burr DB, Turner CH. Shorter, more frequent mechanical loading sessions enhance bone mass. Med Sci Sports Exerc. 2002;34(2):196-202.
81. Frost HM. Bone's mechanostat: a 2003 update. Anat Rec. 2003;275A(2):1081-101.
82. Robling AG, Hinant FM, Burr DB, Turner CH. Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res. 2002;17(8):1545-54.
83. Warden SJ, Fuchs RK, Castillo AB, Nelson IR, Turner CH. Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res. 2007;22(2):251-9.
84. Daly RM, Bass SL. Lifetime sport and leisure activity participation is associated with greater bone size, quality and strength in older men. Osteoporos Int. 2006;17(8):1258-67.
85. Easterbrook PJ, Berlin JA, Gopalan R, Matthews DR. Publication bias in clinical research. Lancet. 1991;337(8746):867.
86. 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. 2002;17(12):2281-9.
87. Dorn LD, Biro FM. Puberty and its measurement: a decade in review. J Res Adolesc. 2011;21(1):180-95.
88. Xu L, Wang Q, Wang Q, et al. Concerted actions of insulin-like growth factor 1, testosterone, and estradiol on peripubertal bone growth: a 7-year longitudinal study. J Bone Miner Res. 2011;26(9):2204-11.
89. Xu L, Nicholson P, Wang Q, Alén M, Cheng S. Bone and muscle development during puberty in girls: a seven-year longitudinal study. J Bone Miner Res. 2009;24(10):1693-8.
90. Kontulainen SA, Macdonald HM, McKay HA. Change in cortical bone density and its distribution differs between boys and girls during puberty. J Clin Endocrinol Metab. 2006;91(7):2555-61.
91. Iuliano-Burns S, Hopper J, Seeman E. The age of puberty determines sexual dimorphism in bone structure: a male/female co-twin control study. J Clin Endocrinol Metab. 2009;94(5):1638-43.
92. Faulkner RA, Bailey DA. Osteoporosis: a pediatric concern? Med Sport Sci. 2007;51:1-12.
93. Khosla S. Update in male osteoporosis. J Clin Endocrinol Metab. 2010;95(1):3-10.
94. Baxter-Jones ADG, Eisenmann JC, Mirwald RL, Faulkner RA, Bailey DA. The influence of physical activity on lean mass accrual during adolescence: a longitudinal analysis. J Appl Physiol. 2008;105(2):734-41.
95. DiGirolamo DJ, Kiel DP, Esser KA. Bone and skeletal muscle: neighbors with close ties. J Bone Miner Res. 2013;28:1509-18.
96. Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. 2003;31(1):45-50.
97. Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S. Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res. 1997;12(9):1480-5.
98. Srinivasan S, Ausk BJ, Poliachik SL, Warner SE, Richardson TS, Gross TS. Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. J Appl Physiol. 2007;102(5):1945-52.
99. OCEBM Levels of Evidence Working GroupHowick J, Chalmers I, Glasziou P, et al. The Oxford 2011 Levels of Evidence [Internet]. Oxford, UK: Centre for Evidence-Based Medicine; 2011 [cited 2014 Jun 3]. Available from: http://www.cebm.net/index.aspx?o=5653.
100. Zemel B, Bass S, Binkley T, et al. Peripheral quantitative computed tomography in children and adolescents: The 2007 ISCD Pediatric Official Positions. J Clin Densitom. 2008;11(1):59-74.