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First published online August 8, 2003

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The Journal of Experimental Biology 206, 3125-3138 (2003)
doi: 10.1242/jeb.00514

Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs

Daniel E. Lieberman^1,*, Osbjorn M. Pearson², John D. Polk¹, Brigitte Demes³ and A. W. Crompton⁴

¹ Peabody Museum, Harvard University, 11 Divinity Avenue, Cambridge Massachusetts 02138, USA
² Department of Anthropology, University of New Mexico, Albuquerque, New Mexico, 87131, USA
³ Department of Anatomical Sciences, Health Sciences Center, State University of New York, Stony Brook, New York, 11794, USA
⁴ Museum of Comparative Zoology, Harvard University, 26 Oxford St., Cambridge, Massachusetts, 02138, USA

^* Author for correspondence (e-mail: danlieb{at}fas.harvard.edu)

Accepted 27 May 2003

How bones respond dynamically to mechanical loading through changes in shape and structure is poorly understood, particularly with respect to variations between bones. Structurally, cortical bones adapt in vivo to their mechanical environments primarily by modulating two processes, modeling and Haversian remodeling. Modeling, defined here as the addition of new bone, may occur in response to mechanical stimuli by altering bone shape or size through growth. Haversian remodeling is thought to be an adaptation to repair microcracks or prevent microcrack propagation. Here, we examine whether cortical bone in sheep limbs modulates periosteal modeling and Haversian remodeling to optimize strength relative to mass in hind-limb midshafts in response to moderate levels of exercise at different growth stages. Histomorphometry was used to compare rates of periosteal growth and Haversian remodeling in exercised and sedentary treatment groups of juvenile, subadult and young adult sheep. In vivo strain data were also collected for the tibia and metatarsal midshafts of juvenile sheep. The results suggest that limb bones initially optimize responses to loading according to the varying power requirements associated with adding mass at different locations. In juveniles, exercise induces higher rates of periosteal modeling in proximal midshafts and higher rates of Haversian remodeling in distal midshafts. Consequently, distal element midshafts experience higher strains and, presumably, have lower safety factors. As animals age, periosteal modeling rates decline and Haversian remodeling rates increase, but moderate levels of mechanical loading stimulate neither process significantly.

Key words: bone, periosteal modeling, Haversian re-modeling, growth, sheep, strain

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