Influence of Physical Activity on Bone Strength in Children and Adolescents: A Systematic Review and Narrative Synthesis

A preponderance of evidence from systematic reviews supports the effectiveness of weight‐bearing exercises on bone mass accrual, especially during the growing years. However, only one systematic review (limited to randomized controlled trials) examined the role of physical activity (PA) on bone strength. Thus, our systematic review extended the scope of the previous review by including all PA intervention and observational studies, including organized sports participation studies, with child or adolescent bone strength as the main outcome. We also sought to discern the skeletal elements (eg, mass, structure, density) that accompanied significant bone strength changes. Our electronic‐database, forward, and reference searches yielded 14 intervention and 23 observational studies that met our inclusion criteria. We used the Effective Public Health Practice Project (EPHPP) tool to assess the quality of studies. Due to heterogeneity across studies, we adopted a narrative synthesis for our analysis and found that bone strength adaptations to PA were related to maturity level, sex, and study quality. Three (of five) weight‐bearing PA intervention studies with a strong rating reported significantly greater gains in bone strength for the intervention group (3% to 4%) compared with only three significant (of nine) moderate intervention studies. Changes in bone structure (eg, bone cross‐sectional area, cortical thickness, alone or in combination) rather than bone mass most often accompanied significant bone strength outcomes. Prepuberty and peripuberty may be the most opportune time for boys and girls to enhance bone strength through PA, although this finding is tempered by the few available studies in more mature groups. Despite the central role that muscle plays in bones' response to loading, few studies discerned the specific contribution of muscle function (or surrogates) to bone strength. Although not the focus of the current review, this seems an important consideration for future studies. © 2014 American Society for Bone and Mineral Research.

[1]  D. Bailey,et al.  A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. , 2008, Bone.

[2]  M. Forwood Growing a Healthy Skeleton: The Importance of Mechanical Loading , 2013 .

[3]  A. Heinonen,et al.  A Randomized School‐Based Jumping Intervention Confers Site and Maturity‐Specific Benefits on Bone Structural Properties in Girls: A Hip Structural Analysis Study , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[4]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

[5]  M. Michalopoulou,et al.  Effect of rhythmic gymnastics on volumetric bone mineral density and bone geometry in premenarcheal female athletes and controls. , 2010, The Journal of clinical endocrinology and metabolism.

[6]  P. Easterbrook,et al.  Publication bias in clinical research , 1991, The Lancet.

[7]  M. Alen,et al.  Concerted actions of insulin‐like growth factor 1, testosterone, and estradiol on peripubertal bone growth: A 7‐year longitudinal study , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[8]  H. Suominen,et al.  Influence of physical activity and maturation status on bone mass and geometry in early pubertal girls. , 2005, Scandinavian journal of medicine & science in sports.

[9]  H. Ahlborg,et al.  A school-curriculum-based exercise intervention program for two years in pre-pubertal girls does not influence hip structure , 2008, Dynamic medicine : DM.

[10]  P. Rosenbaum,et al.  Mechanical loading during growth is associated with plane-specific differences in vertebral geometry: A cross-sectional analysis comparing artistic gymnasts vs. non-gymnasts. , 2011, Bone.

[11]  T. Einhorn Bone strength: The bottom line , 1992, Calcified Tissue International.

[12]  H. McKay,et al.  Change in cortical bone density and its distribution differs between boys and girls during puberty. , 2006, The Journal of clinical endocrinology and metabolism.

[13]  G U Rao,et al.  Predicting femoral neck strength from bone mineral data. A structural approach. , 1990, Investigative radiology.

[14]  M. Alen,et al.  Bone and Muscle Development During Puberty in Girls: A Seven‐Year Longitudinal Study , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[15]  D. Cooper,et al.  Anterior–posterior bending strength at the tibial shaft increases with physical activity in boys: evidence for non-uniform geometric adaptation , 2008, Osteoporosis International.

[16]  Minsoo Kang,et al.  Effects of Weight-Bearing Exercise on Bone Health in Girls: A Meta-Analysis , 2013, Sports Medicine.

[17]  K. Khan,et al.  Is there a critical period for bone response to weight-bearing exercise in children and adolescents? a systematic review , 2002, British journal of sports medicine.

[18]  T. Oxland,et al.  Tibial geometry is associated with failure load ex vivo: a MRI, pQCT and DXA study , 2007, Osteoporosis International.

[19]  P. Rosenbaum,et al.  Site-specific advantages in skeletal geometry and strength at the proximal femur and forearm in young female gymnasts. , 2012, Bone.

[20]  N. Bonnet,et al.  Exercise and the skeleton: How it works and what it really does , 2010 .

[21]  D R Carter,et al.  New approaches for interpreting projected bone densitometry data , 1992, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  D. Bailey,et al.  Osteoporosis: a pediatric concern? , 2007, Medicine and sport science.

[23]  T R Oxland,et al.  Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. , 2008, Journal of musculoskeletal & neuronal interactions.

[24]  K. Khan,et al.  Does a novel school-based physical activity model benefit femoral neck bone strength in pre- and early pubertal children? , 2008, Osteoporosis International.

[25]  D. Bailey,et al.  Bone mineral accrual from 8 to 30 years of age: An estimation of peak bone mass , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[26]  M. Hamrick JMNI special issue: basic science and mechanisms of muscle-bone interactions. , 2010, Journal of musculoskeletal & neuronal interactions.

[27]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2009, Journal of clinical epidemiology.

[28]  Victor R. Preedy,et al.  Handbook of disease burdens and quality of life measures , 2010 .

[29]  T. Rowland Effect of Rhythmic Gymnastics on Volumetric Bone Mineral Density and Bone Geometry in Premenarcheal Female Athletes and Controls , 2011 .

[30]  Pekka Kannus,et al.  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 , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[31]  J. Hopper,et al.  The age of puberty determines sexual dimorphism in bone structure: a male/female co-twin control study. , 2009, The Journal of clinical endocrinology and metabolism.

[32]  C. Cowell,et al.  Sex-specific developmental changes in muscle size and bone geometry at the femoral shaft. , 2008, Bone.

[33]  Thomas J Beck,et al.  Physical activity and strength of the femoral neck during the adolescent growth spurt: a longitudinal analysis. , 2006, Bone.

[34]  A. Baxter-Jones,et al.  Precompetitive and recreational gymnasts have greater bone density, mass, and estimated strength at the distal radius in young childhood , 2010, Osteoporosis International.

[35]  G. Naughton,et al.  Influence of Drop-Landing Exercises on Bone Geometry and Biomechanical Properties in Prepubertal Girls: A Randomized Controlled Study , 2009, Calcified Tissue International.

[36]  U. Ekelund,et al.  Objectively Measured Physical Activity and Bone Strength in 9-Year-Old Boys and Girls , 2008, Pediatrics.

[37]  H. McKay,et al.  Physical activity positively predicts bone architecture and bone strength in adolescent males and females , 2011, Acta paediatrica.

[38]  E. Anliker,et al.  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. , 2012, Journal of musculoskeletal & neuronal interactions.

[39]  E. Barrett-Connor,et al.  Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study , 2004, Osteoporosis International.

[40]  Huseyin Naci,et al.  The critical role of observational evidence in comparative effectiveness research. , 2010, Health affairs.

[41]  Douglas P Kiel,et al.  Bone and Skeletal Muscle: Neighbors With Close Ties , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[42]  S. Khosla Update in male osteoporosis. , 2010, The Journal of clinical endocrinology and metabolism.

[43]  Thomas J Beck,et al.  Extending DXA beyond bone mineral density: Understanding hip structure analysis , 2007, Current osteoporosis reports.

[44]  Heather A McKay,et al.  Bone mass and structure are enhanced following a 2-year randomized controlled trial of exercise in prepubertal boys. , 2004, Bone.

[45]  Y. Umemura,et al.  Five Jumps per Day Increase Bone Mass and Breaking Force in Rats , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[46]  G Pearce,et al.  Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[47]  M. Forwood Physical activity and bone development during childhood: insights from animal models. , 2008, Journal of applied physiology.

[48]  P. Kannus,et al.  Targeted exercise against osteoporosis: A systematic review and meta-analysis for optimising bone strength throughout life , 2010, BMC medicine.

[49]  M. Behringer,et al.  Effects of Weight‐Bearing Activities on Bone Mineral Content and Density in Children and Adolescents: A Meta‐Analysis , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[50]  Stuart J Warden,et al.  Exercise When Young Provides Lifelong Benefits to Bone Structure and Strength , 2006, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[51]  G. Beaupré,et al.  DXA-derived section modulus and bone mineral content predict long-bone torsional strength. , 1999, Acta orthopaedica Scandinavica.

[52]  F. Biro,et al.  Puberty and Its Measurement: A Decade in Review , 2011 .

[53]  C. Cowell,et al.  Mid-femur geometry and biomechanical properties in 15- to 18-yr-old female athletes. , 2002, Medicine and science in sports and exercise.

[54]  H. Suominen,et al.  Influence of physical activity and maturation status on bone mass and geometry in early pubertal girls 1 , 2005 .

[55]  J. Eisenmann,et al.  The influence of physical activity on lean mass accrual during adolescence: a longitudinal analysis. , 2008, Journal of applied physiology.

[56]  David Karasik,et al.  Bone geometry and skeletal fragility , 2006, Current osteoporosis reports.

[57]  K. Khan,et al.  Maturity- and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. , 2005, Bone.

[58]  Alexander G Robling,et al.  Improved Bone Structure and Strength After Long‐Term Mechanical Loading Is Greatest if Loading Is Separated Into Short Bouts , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  Jennie Popay,et al.  Guidance on the conduct of narrative synthesis in systematic Reviews. A Product from the ESRC Methods Programme. Version 1 , 2006 .

[60]  M. Duclos,et al.  Bone geometry and strength adaptations to physical constraints inherent in different sports: comparison between elite female soccer players and swimmers , 2011, Journal of Bone and Mineral Metabolism.

[61]  B. Weeks,et al.  Eight Months of Regular In‐School Jumping Improves Indices of Bone Strength in Adolescent Boys and Girls: The POWER PE Study , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[62]  B. H. Thomas,et al.  A process for systematically reviewing the literature: providing the research evidence for public health nursing interventions. , 2004, Worldviews on evidence-based nursing.

[63]  E. Letuchy,et al.  Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study. , 2007, Bone.

[64]  Thomas S Richardson,et al.  Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. , 2007, Journal of applied physiology.

[65]  J. N. Dowthwaite,et al.  Distal radius geometry and skeletal strength indices after peripubertal artistic gymnastics , 2010, Osteoporosis International.

[66]  P. Kannus,et al.  Estimation of various mechanical characteristics of human bones using dual energy X-ray absorptiometry: methodology and precision. , 1996, Bone.

[67]  B. Gutin,et al.  Validation of the Physical Activity Questionnaire for Older Children in children of different races. , 2007, Pediatric exercise science.

[68]  Monika Kastner,et al.  Age-Specific Search Strategies for Medline , 2006, Journal of medical Internet research.

[69]  J. Kanis,et al.  Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[70]  J. Spadaro,et al.  Bone geometry, density, and strength indices of the distal radius reflect loading via childhood gymnastic activity. , 2007, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[71]  H. Ahlborg,et al.  A one-year exercise intervention program in pre-pubertal girls does not influence hip structure , 2008, BMC musculoskeletal disorders.

[72]  R. Goeree,et al.  The burden of illness of osteoporosis in Canada , 2012, Osteoporosis International.

[73]  J. Heikkinen,et al.  Determinants of Bone Mass and Bone Geometry in Adolescent and Young Adult Women , 2000, Calcified Tissue International.

[74]  T. Waters,et al.  Bone Quantity and Quality of Youths Working on a Farm—A Pilot Study , 2008, Journal of agromedicine.

[75]  Keith Russell,et al.  Strength indices of the proximal femur and shaft in prepubertal female gymnasts. , 2003, Medicine and science in sports and exercise.

[76]  G. Naughton,et al.  Bone strength index in adolescent girls: does physical activity make a difference? , 2005, British Journal of Sports Medicine.

[77]  H. Frost Muscle, bone, and the Utah paradigm: a 1999 overview. , 2000, Medicine and science in sports and exercise.

[78]  E. Tacconelli Systematic reviews: CRD's guidance for undertaking reviews in health care , 2010 .

[79]  Alexander G Robling,et al.  Designing Exercise Regimens to Increase Bone Strength , 2003, Exercise and sport sciences reviews.

[80]  H. Ahlborg,et al.  A 2‐year school‐based exercise programme in pre‐pubertal boys induces skeletal benefits in lumbar spine , 2008, Acta paediatrica.

[81]  J. Adams,et al.  Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children. , 2005, Bone.

[82]  J. Torner,et al.  Everyday activity predicts bone geometry in children: the iowa bone development study. , 2004, Medicine and science in sports and exercise.

[83]  H. Genant,et al.  New Imaging Modalities in Bone , 2011, Current rheumatology reports.

[84]  S. Going,et al.  Associations of physical activity duration, frequency, and load with volumetric BMD, geometry, and bone strength in young girls , 2011, Osteoporosis International.

[85]  H. Frost Bone's mechanostat: a 2003 update. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[86]  T. Beck,et al.  Measuring the structural strength of bones with dual-energy X-ray absorptiometry: principles, technical limitations, and future possibilities , 2003, Osteoporosis International.

[87]  D. Courteix,et al.  Non-elite gymnastics participation is associated with greater bone strength, muscle size, and function in pre- and early pubertal girls , 2012, Osteoporosis International.

[88]  Alexander G Robling,et al.  Shorter, more frequent mechanical loading sessions enhance bone mass. , 2002, Medicine and science in sports and exercise.

[89]  K. Hind,et al.  Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials. , 2007, Bone.

[90]  A. Robling,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 , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[91]  H. McKay,et al.  Winning the Battle Against Childhood Physical Inactivity: The Key to Bone Strength? , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[92]  S. Bass,et al.  Lifetime sport and leisure activity participation is associated with greater bone size, quality and strength in older men , 2006, Osteoporosis International.

[93]  Primer on the metabolic bone diseases and disorders of mineral metabolism. , 2013 .

[94]  Heather A McKay,et al.  Is a School‐Based Physical Activity Intervention Effective for Increasing Tibial Bone Strength in Boys and Girls? , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[95]  B. Zemel,et al.  Peripheral quantitative computed tomography in children and adolescents: the 2007 ISCD Pediatric Official Positions. , 2008, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[96]  K M Khan,et al.  “Bounce at the Bell”: a novel program of short bouts of exercise improves proximal femur bone mass in early pubertal children , 2005, British Journal of Sports Medicine.

[97]  J. Popay,et al.  Guidance on the conduct of narrative synthesis in sytematic reviews , 2006 .

[98]  H. McKay,et al.  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 , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[99]  A. Heinonen,et al.  High-Impact Exercise and Bones of Growing Girls: A 9-Month Controlled Trial , 2000, Osteoporosis International.

[100]  H. McKay,et al.  Bone microstructure at the distal tibia provides a strength advantage to males in late puberty: An HR‐pQCT study , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[101]  L. Lanyon,et al.  Osteoregulatory nature of mechanical stimuli: Function as a determinant for adaptive remodeling in bone , 1987, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[102]  P. Crocker,et al.  Validation of the Physical Activity Questionnaire for Older Children , 1997 .

[103]  R. K. Ro D G E R S A N D A N G E L A S Ow D E N,et al.  Testing Methodological Guidance on the Conduct of Narrative Synthesis in Systematic Reviews Effectiveness of Interventions to Promote Smoke Alarm Ownership and Function , 2008 .

[104]  Kyle K. Nishiyama,et al.  Clinical Tools to Evaluate Bone Strength , 2010 .

[105]  D. Stadler,et al.  Predictors of bone mass by peripheral quantitative computed tomography in early adolescent girls. , 2001, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.