Is there a critical period for bone response to weight-bearing exercise in children and adolescents? a systematic review
Open accessAbstract
This systematic review examines and compares the bone mineral changes in children and adolescents, as measured by dual energy x ray absorptiometry, reported in exercise intervention studies. The effects of hormonal factors and growth on bone mineral change during puberty are examined, and the possibility of a critical period during which bone is especially adaptable to exercise is discussed.
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During childhood and adolescence, it is necessary to engage in weight-bearing physical activities, such as running and jumping, in order to attain peak bone mass and maintain healthy bone mineral accrual.
“During childhood and adolescence, it is necessary to engage in weight-bearing physical activities, such as running and jumping, in order to attain peak bone mass and maintain healthy bone mineral accrual.64–67”
From Physical activity and health in Chinese children and adolescents: expert consensus statement (2020) (2020) · cites this paper as [66]
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Cites
Growth, Maturation, and Physical Activity
Malina, R. M., Bouchard, C., & Bar‐Or, O. (2004) · Human Kinetics eBooks · doi:10.5040/9781492596837 · Cited by 3,301 · see citing works
Bailey, D. A., McKay, H. A., Mirwald, R. L., Crocker, P. R. E., & Faulkner, R. A. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.10.1672 · Cited by 1,032 · see citing works
Self-citationAdolescent Self-assessment of Sexual Maturation
Neinstein, L. S. (1982) · Clinical Pediatrics · doi:10.1177/000992288202100806 · Cited by 783 · see citing works
Adolescents' Self-Assessment of Sexual Maturation
Duke, P. M., Litt, I. F., & Gross, R. T. (1980) · PEDIATRICS · doi:10.1542/peds.66.6.918 · Cited by 685 · see citing works
Bass, S., Pearce, G., Bradney, M., Hendrich, E., Delmas, P. D., Harding, A. T., & Seeman, E. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.3.500 · Cited by 615 · see citing works
Fuchs, R. K., Bauer, J. J., & Snow, C. M. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.1.148 · Cited by 583 · see citing works
Predicting Femoral Neck Strength From Bone Mineral Data
Beck, T., Ruff, C. B., WARDEN, K. E., Scott, W. W., & Rao, G. U. V. (1990) · Investigative Radiology · doi:10.1097/00004424-199001000-00004 · Cited by 551 · see citing works
Heinonen, A. O., Kannus, P., Sievänen, H. T., Oja, P., Pasanen, M. E., Rinne, M. B., Uusi‐Rasi, K., & VUORI, I. M. (1996) · The Lancet · doi:10.1016/s0140-6736(96)04214-6 · Cited by 472 · see citing works
Bradney, M., Pearce, G., Naughton, G. A., Sullivan, C., Bass, S., Beck, T., Carlson, J., & Seeman, E. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.12.1814 · Cited by 471 · see citing works
Juul, A., Dalgaard, P., Blum, W. F., Bang, P., Hall, K. E., Michaelsen, K. F., Müller, J., & Skakkebæk, N. E. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.8.7543116 · Cited by 463 · see citing works
Morris, F. L., Naughton, G. A., Gibbs, J. L., Carlson, J. S., & Wark, J. D. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.9.1453 · Cited by 453 · see citing works
The two faces of growth: Benefits and risks to bone integrity
PARFITT, A. M. (1994) · Osteoporosis International · doi:10.1007/bf01622201 · Cited by 404 · see citing works
Alexander, J. R., & Tanner, J. M. (1979) · Biometrics · doi:10.2307/2530274 · Cited by 395 · see citing works
Snow-Harter, C., Bouxsein, M., Lewis, B., Carter, D. R. P., & Marcus, R. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650070706 · Cited by 383 · see citing works
Slemenda, C. W., Reister, T., Hui, S. L., Miller, J. Z., Christian, J. C., & Johnston, C. C. (1994) · The Journal of Pediatrics · doi:10.1016/s0022-3476(94)70193-8 · Cited by 382 · see citing works
High-Impact Exercise and Bones of Growing Girls: A 9-Month Controlled Trial
Heinonen, A. O., Sievänen, H. T., Kannus, P., Oja, P., Pasanen, M. E., & VUORI, I. M. (2001) · Osteoporosis International · doi:10.1007/s001980070021 · Cited by 339 · see citing works
Hip fractures in Finland between 1970 and 1997 and predictions for the future
Kannus, P., Niemi, S. T., Parkkari, J. P., et al. (1999) · The Lancet · doi:10.1016/s0140-6736(98)04235-4 · Cited by 334 · see citing works
Petit, M. A., McKay, H. A., MacKelvie, K. J., Heinonen, A. O., Khan, K. M., & Beck, T. (2002) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2002.17.3.363 · Cited by 333 · see citing works
Self-citationMcKay, H. A., Petit, M. A., Schutz, R. W., Prior, J. C., Barr, S. I., & Khan, K. M. (2000) · The Journal of Pediatrics · doi:10.1016/s0022-3476(00)70095-3 · Cited by 324 · see citing works
Self-citationDrop jumping. I. The influence of jumping technique on the biomechanics of jumping
Bobbert, M. F., HUIJING, P. A., & SCHENAU, G. J. V. I. (1987) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198708000-00003 · Cited by 319 · see citing works
Effect of Long-Term Unilateral Activity on Bone Mineral Density of Female Junior Tennis Players
Haapasalo, H. H., Kannus, P., Sievänen, H., Pasanen, M. E., Uusi‐Rasi, K., Heinonen, A. O., Oja, P., & VUORI, I. M. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.2.310 · Cited by 317 · see citing works
A school-based exercise intervention augments bone mineral accrual in early pubertal girls
MacKelvie, K. J., McKay, H. A., Khan, K. M., & Crocker, P. R. E. (2001) · The Journal of Pediatrics · doi:10.1067/mpd.2001.118190 · Cited by 317 · see citing works
Self-citationFrom Density to Structure: Growing Up and Growing Old on the Surfaces of Bone
Seeman, E. (1997) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1997.12.4.509 · Cited by 302 · see citing works
Bailey, D. B. (1997) · International Journal of Sports Medicine · doi:10.1055/s-2007-972713 · Cited by 285 · see citing works
Aging changes mechanical loading thresholds for bone formation in rats
Turner, C. H., Takano, Y., & Owan, I. (1995) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650101016 · Cited by 275 · see citing works
Effects of plyometric jump training on bone mass in adolescent girls
Witzke, K. A., & Snow, C. M. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200006000-00003 · Cited by 260 · see citing works
Courteix, D., Lespessailles, É., Peres, S. L., Obert, P., Germain, P., & Benhamou, C. L. (1998) · Osteoporosis International · doi:10.1007/bf02672512 · Cited by 259 · see citing works
The role of estrogen in bone growth and maturation during childhood and adolescence
Cutler, G. B. (1997) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(97)80005-2 · Cited by 241 · see citing works
Mauras, N., Rogol, A. D., Haymond, M. W., & Veldhuis, J. D. (2008) · Hormone Research · doi:10.1159/000184763 · Cited by 219 · see citing works
Mechanical loading regime and its relationship to bone mineral density in children
Grimston, S. K., Willows, N. D., & Hanley, D. A. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199311000-00002 · Cited by 213 · see citing works
Exercise during growth and bone mineral density and fractures in old age
Karlsson, M., Lindén, C., Karlsson, C., Johnell, O., Obrant, K. J., & Seeman, E. (2000) · The Lancet · doi:10.1016/s0140-6736(00)82020-6 · Cited by 201 · see citing works
Impact of a 12‐Month Exercise Program on the Physical and Psychological Health of Osteopenic Women
Bravo, G., Gauthier, P., Roy, P., Payette, H., Gaulin, P., Harvey, M., Péloquin, L., & Dubois, M. (1996) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1996.tb03730.x · Cited by 200 · see citing works
Kontulainen, S. A., Kannus, P., Haapasalo, H. H., Sievänen, H. T., Pasanen, M. E., Heinonen, A. O., Oja, P., & VUORI, I. M. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.2.195 · Cited by 189 · see citing works
Grumbach, M. M. (2000) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem-2000-s619 · Cited by 173 · see citing works
Winters, K. M., & Snow, C. M. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.12.2495 · Cited by 165 · see citing works
Peak bone mineral accrual and age at menarche in adolescent girls: A 6-year longitudinal study
McKay, H. A., Bailey, D. A., Mirwald, R. L., Davison, K. S., & Faulkner, R. A. (1998) · The Journal of Pediatrics · doi:10.1016/s0022-3476(98)70112-x · Cited by 153 · see citing works
Self-citationNordström, P., Pettersson, U., & Lorentzon, R. (1998) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1998.13.7.1141 · Cited by 150 · see citing works
Effects of resistance training on bone mineral content and density in adolescent females
Blimkie, C. J. R., Rice, S., Webber, C. E., Martin, J., Levy, D., & Gordon, C. L. (1996) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y96-099 · Cited by 149 · see citing works
The Course of Bone Gain and the Phases of Bone Loss
Garn, S. M. (1972) · Orthopedic Clinics of North America · doi:10.1016/s0030-5898(20)30477-6 · Cited by 149 · see citing works
Does childhood and adolescence provide a unique opportunity for exercise to strengthen the skeleton?
Karim, K., McKay, H. A., Haapasalo, H. H., Bennell, K. L., Forwood, M. R., Kannus, P., & Wark, J. D. (2000) · Journal of science and medicine in sport · doi:10.1016/s1440-2440(00)80077-8 · Cited by 146 · see citing works
Self-citationDaly, R. M., Rich, P., Klein, R., & Bass, S. L. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.7.1222 · Cited by 141 · see citing works
Khan, K. M., Bennell, K. L., Hopper, J. L., Flicker, L. A., Nowson, C. A., Sherwin, A. J., Crichton, K. J., Harcourt, P. R., & Wark, J. D. (1998) · Osteoporosis International · doi:10.1007/bf02672514 · Cited by 140 · see citing works
Self-citationLee, P. A., XENAKIS, T., WINER, J., & MATSENBAUGH, S. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-43-4-775 · Cited by 130 · see citing works
Bass, S. L. (2000) · Sports Medicine · doi:10.2165/00007256-200030020-00001 · Cited by 124 · see citing works
Klein, K. O., MARTHA, P. M., Blizzard, R. M., et al. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.9.8784070 · Cited by 108 · see citing works
Davies, D. P. (1990) · Archives of Disease in Childhood · doi:10.1136/adc.65.5.562 · Cited by 104 · see citing works
Fitness, Training, and the Growth Hormone→Insulin-Like Growth Factor I Axis in Prepubertal Girls1
Eliakim, A., Scheett, T. P., Newcomb, R. L., et al. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7560 · Cited by 100 · see citing works
Effects of Activity on Bone Growth and Development in the Rat
Steinberg, M. E., & Trueta, J. (1981) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-198105000-00007 · Cited by 98 · see citing works
Lee, P. A., & Migeon, C. J. (1975) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-41-3-556 · Cited by 97 · see citing works
Studies on the Potential Mediators of Skeletal Changes Occurring during Puberty in Girls1
Libanati, C. R., Baylink, D. J., Lois-Wenzel, E., Srinivasan, N., & Mohan, S. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5905 · Cited by 82 · see citing works
Mechanical loading and bone: What sort of exercise is beneficial to the skeleton?
Skerry, T. M. (1997) · Bone · doi:10.1016/s8756-3282(96)00387-0 · Cited by 76 · see citing works
Bone Mineral Content of Junior Competitive Weightlifters
Virvidakis, K., Georgiou, E., Korkotsidis, A., et al. (1990) · International Journal of Sports Medicine · doi:10.1055/s-2007-1024800 · Cited by 74 · see citing works
Skeletal growth estimation using radiographic image processing and analysis
Mahmoodi, S., Sharif, B. S., Chester, E. G., et al. (2000) · IEEE Transactions on Information Technology in Biomedicine · doi:10.1109/4233.897061 · Cited by 72 · see citing works
Nutrition, Exercise, and Bone Status in Youth
Barr, S. I., & McKay, H. A. (1998) · International Journal of Sport Nutrition · doi:10.1123/ijsn.8.2.124 · Cited by 69 · see citing works
Self-citationEffects of Exercise Training on Bone Density in Older Men and Women
Blumenthal, J. A., Emery, C. F., Madden, D. J., Schniebolk, S., Riddle, M. W., Cobb, F. R., Higginbotham, M. B., & Coleman, R. E. (1991) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1991.tb02870.x · Cited by 67 · see citing works
Mora, S., Pitukcheewanont, P., Nelson, J. C., & Gilsanz, V. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5874 · Cited by 62 · see citing works
Studies on the Potential Mediators of Skeletal Changes Occurring during Puberty in Girls
Libanati, C. R. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.8.2807 · Cited by 61 · see citing works
Heterogeneity of growth of bone in children at the spine, radius and total skeleton.
Geusens, P., Cantatore, F., Nijs, J., et al. (1991) · PubMed · Cited by 54 · see citing works
The Somatotropic Axis in Puberty
Brook, C. G. D., & Hindmarsh, P. C. (1992) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(18)30188-9 · Cited by 51 · see citing works
Klein, K. O. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.9.3203 · Cited by 51 · see citing works
Fitness, Training, and the Growth Hormone Insulin-Like Growth Factor I Axis in Prepubertal Girls
Eliakim, A. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.6.2797 · Cited by 47 · see citing works
External loading comparisons between able-bodied and below-knee-amputee children during walking.
Engsberg, J. R., Lee, A. G., Patterson, J. L., et al. (1991) · PubMed · Cited by 45 · see citing works
Physical Activity and Stages of Change in Fifth and Sixth Graders
Walton, J. A., Hoerr, S. L., Heine, L., Frost, S., Roisen, D., & Berkimer, M. (1999) · Journal of School Health · doi:10.1111/j.1746-1561.1999.tb06410.x · Cited by 45 · see citing works
Daly, R. M., Rich, P., & Klein, R. (1997) · Calcified Tissue International · doi:10.1007/s002239900252 · Cited by 44 · see citing works
Lifestyle risk factors for osteoporosis in Asian and Caucasian girls
MacKelvie, K. J., McKay, H. A., Khan, K. M., et al. (2001) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200111000-00004 · Cited by 42 · see citing works
Self-citationStructured Opportunities for Student Physical Activity in Ontario Elementary and Secondary Schools
Allison, K. R., & Adlaf, E. M. (2000) · Canadian Journal of Public Health · doi:10.1007/bf03404810 · Cited by 36 · see citing works
Making an impact on pediatric bone health
Bachrach, L. K. (2000) · The Journal of Pediatrics · doi:10.1016/s0022-3476(00)70088-6 · Cited by 25 · see citing works
The Role of Estrogen in Bone Growth and Maturation During Childhood and Adolescence
Cutler, G. B. (1997) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(96)00219-1 · Cited by 23 · see citing works
The Hip Joint: Structure, Stability, and Stress: A Review
Singleton, M. C., & LeVeau, B. F. (1975) · Physical Therapy · doi:10.1093/ptj/55.9.957 · Cited by 19 · see citing works
Hormonal responses to exercise in girls during sexual maturation.
Laaneots, L., Karelson, K., Smirnova, T., et al. (1998) · PubMed · Cited by 10 · see citing works
The Achilles' Heel of Exercise-Induced Bone Mass Increments: Cessation of Exercise
Seeman, E. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.7.1370 · Cited by 7 · see citing works
Sievänen, H. T., McKay, H. A., Heinonen, A. O., et al. (2000) · The Lancet · doi:10.1016/s0140-6736(05)73354-7 · Cited by 7 · see citing works
Self-citationThe Achilles heel of exercise [letter; comment]
Lorentzon, R., Nordström, P., & Pettersson, U. (2000) · The Lancet · Cited by 1 · see citing works
Cessation of Treatment: A Universal Achilles' Heel
Kontulainen, S. A., Kannus, P., & Sievänen, H. T. (2001) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2001.16.7.1372 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Khan KM, Bennell KL, Hopper JL, et al. Self-reported ballet classes undertaken between 10 and 12 years of age and hip bone mineral density. Osteoporosis Int 1998;8:165-73.
- Grumbach M. Estrogen, bone, growth and sex: a sea change in conventional wisdom. J Pediatr Endocrinol Metab 2000;13:1439-55.
- Singleton MC, LeVeau BF. The hip joint: structure, stability and stress. Phys Ther 1975;55:957-73.
Cited by
Sorted by citations
The educational benefits claimed for physical education and school sport: an academic review
Bailey, R., Armour, K., Kirk, D., Jess, M., Pickup, I., Sandford, R., & P, B. P. E. A. S. (2009) · Research Papers in Education · doi:10.1080/02671520701809817 · Cited by 869 · see citing works
The aging of Wolff’s “law”: Ontogeny and responses to mechanical loading in cortical bone
Pearson, O. M., & Lieberman, D. E. (2004) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20155 · Cited by 745 · see citing works
Rizzoli, R., Bianchi, M. L., Garabédian, M., McKay, H. A., & Moreno, L. A. (2010) · Bone · doi:10.1016/j.bone.2009.10.005 · Cited by 643 · see citing works
Self-citationPhysical activity and health in Chinese children and adolescents: expert consensus statement (2020)
Chen, P., Wang, D., Shen, H., Yu, L., Gao, Q., Mao, L., Jiang, F., Luo, Y., Xie, M., Zhang, Y., et al. (2020) · British Journal of Sports Medicine · doi:10.1136/bjsports-2020-102261 · Cited by 225 · see citing works
Ducher, G., Daly, R. M., & Bass, S. L. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090415 · Cited by 86 · see citing works
Ng, C.-A., Gandham, A., Mesinovic, J., Owen, P. J., Ebeling, P. R., & Scott, D. (2023) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.4899 · Cited by 36 · see citing works
- Authors
- MacKelvie, K. J., Khan, K. M., & McKay, H. A.
- Affiliations
- University of British Columbia (CA)
- Corresponding author
- Khan, K M
- ORCID
- McKay, H A
- Venue
- British Journal of Sports Medicine
- Publisher
- BMJ
- Published
- 2002-08
- Volume
- 36
- Issue
- 4
- Pages
- 250-257
- ISSN
- 0306-3674 (ISSN-L)
- 1473-0480
- PMC
- PMC1724536
- OpenAlex
- W2096885396
- Cited by
- 364
- References
- 74
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 11 · 2023: 13 · 2022: 4 · 2021: 16 · 2020: 20 · 2019: 11 · 2018: 20 · 2017: 25 · 2016: 16 · 2015: 24 · 2014: 21 · 2013: 16 · 2012: 14
- FWCI
- 1.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal of Sports Medicine (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Physiology › Physical Activity and Health
- Social Sciences › Arts and Humanities › Archeology › Forensic Anthropology and Bioarchaeology Studies
- Keywords
- bone mineral density, weight-bearing exercise, children, adolescents, puberty, critical period, bone adaptation, hormonal factors, growth, exercise intervention
- MeSH terms
- Adolescent, Anthropometry, Bone Development, Calcification, Physiologic, Child, Humans, Puberty, Exercise, Absorptiometry, Photon, Bone Density, Weight-Bearing
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