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Research Article

Physical activity when young provides lifelong benefits to cortical bone size and strength in men

Stuart J. Warden, Sara M. Mantila Roosa, Mariana E. Kersh, Andrea L. Hurd, Glenn S. Fleisig, Marcus G. Pandy, and Robyn K. Fuchs
  1. aCenter for Translational Musculoskeletal Research and
  2. bDepartment of Physical Therapy, School of Health and Rehabilitation Sciences, Indiana University, Indianapolis, IN 46202;
  3. cDepartment of Mechanical Engineering, University of Melbourne, Parkville, VIC 3010, Australia; and
  4. dAmerican Sports Medicine Institute, Birmingham, AL 35205

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PNAS first published March 24, 2014; https://doi.org/10.1073/pnas.1321605111
Stuart J. Warden
aCenter for Translational Musculoskeletal Research and
bDepartment of Physical Therapy, School of Health and Rehabilitation Sciences, Indiana University, Indianapolis, IN 46202;
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  • For correspondence: stwarden@iu.edu
Sara M. Mantila Roosa
aCenter for Translational Musculoskeletal Research and
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Mariana E. Kersh
cDepartment of Mechanical Engineering, University of Melbourne, Parkville, VIC 3010, Australia; and
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Andrea L. Hurd
aCenter for Translational Musculoskeletal Research and
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Glenn S. Fleisig
dAmerican Sports Medicine Institute, Birmingham, AL 35205
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Marcus G. Pandy
cDepartment of Mechanical Engineering, University of Melbourne, Parkville, VIC 3010, Australia; and
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Robyn K. Fuchs
aCenter for Translational Musculoskeletal Research and
bDepartment of Physical Therapy, School of Health and Rehabilitation Sciences, Indiana University, Indianapolis, IN 46202;
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  1. Edited by Christopher B. Ruff, The Johns Hopkins University School of Medicine, Baltimore, MD, and accepted by the Editorial Board February 21, 2014 (received for review November 22, 2013)

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Significance

Bones adapt to mechanical forces in youth to increase their size and strength but are more at risk for breaking later in life. Do the skeletal benefits of physical activity in youth persist with aging? Here we show at an upper extremity site that half of the benefit in bone size and one-third of the benefit in bone strength obtained from physical activity during youth are maintained throughout life, even though the bone mass benefits are lost. When physical activity was continued during aging, some mass and more strength benefits were preserved. These data suggest that physical activity during youth should be encouraged for lifelong bone health, with the focus being optimization of bone size rather than increasing mass.

Abstract

The skeleton shows greatest plasticity to physical activity-related mechanical loads during youth but is more at risk for failure during aging. Do the skeletal benefits of physical activity during youth persist with aging? To address this question, we used a uniquely controlled cross-sectional study design in which we compared the throwing-to-nonthrowing arm differences in humeral diaphysis bone properties in professional baseball players at different stages of their careers (n = 103) with dominant-to-nondominant arm differences in controls (n = 94). Throwing-related physical activity introduced extreme loading to the humeral diaphysis and nearly doubled its strength. Once throwing activities ceased, the cortical bone mass, area, and thickness benefits of physical activity during youth were gradually lost because of greater medullary expansion and cortical trabecularization. However, half of the bone size (total cross-sectional area) and one-third of the bone strength (polar moment of inertia) benefits of throwing-related physical activity during youth were maintained lifelong. In players who continued throwing during aging, some cortical bone mass and more strength benefits of the physical activity during youth were maintained as a result of less medullary expansion and cortical trabecularization. These data indicate that the old adage of “use it or lose it” is not entirely applicable to the skeleton and that physical activity during youth should be encouraged for lifelong bone health, with the focus being optimization of bone size and strength rather than the current paradigm of increasing mass. The data also indicate that physical activity should be encouraged during aging to reduce skeletal structural decay.

  • exercise
  • intracortical remodeling
  • osteoporosis
  • peak bone mass

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: stwarden{at}iu.edu.
  • Author contributions: S.J.W., M.E.K., M.G.P., and R.K.F. designed research; S.J.W., S.M.M.R., M.E.K., A.L.H., G.S.F., M.G.P., and R.K.F. performed research; S.J.W., S.M.M.R., M.E.K., M.G.P., and R.K.F. analyzed data; and S.J.W., M.E.K., M.G.P., and R.K.F. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. C.B.R. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1321605111/-/DCSupplemental.

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Lifelong skeletal benefits of physical activity
Stuart J. Warden, Sara M. Mantila Roosa, Mariana E. Kersh, Andrea L. Hurd, Glenn S. Fleisig, Marcus G. Pandy, Robyn K. Fuchs
Proceedings of the National Academy of Sciences Mar 2014, 201321605; DOI: 10.1073/pnas.1321605111

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Lifelong skeletal benefits of physical activity
Stuart J. Warden, Sara M. Mantila Roosa, Mariana E. Kersh, Andrea L. Hurd, Glenn S. Fleisig, Marcus G. Pandy, Robyn K. Fuchs
Proceedings of the National Academy of Sciences Mar 2014, 201321605; DOI: 10.1073/pnas.1321605111
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