Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation

H Pontzer,B HallgríMsson,E Momin,J D Polk,D M L Cooper,D E Lieberman,M J Devlin

doi:10.1242/jeb.01971

Abstract

Wolff's law of trajectorial orientation proposes that trabecular struts align with the orientation of dominant compressive loads within a joint. Although widely considered in skeletal biology, Wolff's law has never been experimentally tested while controlling for ontogenetic stage, activity level, and species differences, all factors that may affect trabecular bone growth. Here we report an experimental test of Wolff's law using a within-species design in age-matched subjects experiencing physiologically normal levels of bone strain. Two age-matched groups of juvenile guinea fowl Numida meleagris ran on a treadmill set at either 0 degrees (Level group) or 20 degrees (Incline group), for 10 min per day over a 45-day treatment period. Birds running on the 20 degrees inclined treadmill used more-flexed knees than those in the Level group at midstance (the point of peak ground reaction force). This difference in joint posture enabled us to test the sensitivity of trabecular alignment to altered load orientation in the knee. Using a new radon transform-based method for measuring trabecular orientation, our analysis shows that the fine trabecular bone in the distal femur has a high degree of correspondence between changes in joint angle and trabecular orientation. The sensitivity of this response supports the prediction that trabecular bone adapts dynamically to the orientation of peak compressive forces.

Highlights

Since the late 19th century, it has been suggested that the thin struts and plates in trabecular bone adapt dynamically to meet the demands of mechanical loading (von Meyer, 1867; Wolff, 1982)
Several modeling studies have shown that the arcuate trajectories of trabeculae in the human femur and calcaneus tend to be aligned with the orientation of peak compressive stresses predicted from finite-element models (e.g. Carter and Beaupre, 2002; Gefen and Seliktar, 2004)
Assuming the trajectory of the joint reaction force (JRF) relative to the proximal tibiotarsus was the same in both groups, we predicted this 13.7° difference in knee flexion would result in a corresponding difference in the orientation of the thickest trabecular struts in the lateral femoral condyle

Summary

Introduction

Since the late 19th century, it has been suggested that the thin struts and plates in trabecular bone adapt dynamically to meet the demands of mechanical loading (von Meyer, 1867; Wolff, 1982). Wolff (1892) proposed that trabecular struts grow to align with the trajectory of the predominant loads experienced within a joint. This hypothesis, often termed ‘Wolff’s law’, has been widely employed, few controlled experiments have tested if the orientation of trabeculae changes as a consequence of altered loading patterns. A number of more clinically focused studies have examined the effect of pathologies and surgically based, tissue engineering approaches on trabecular architecture. These studies find that the mechanical environment of a joint has considerable effects on mechanisms of tissue repair relevant to trabecular bone (Hollister et al, 2001; Smith-Adeline et al, 2002; Goldstein, 2004; Papaloucas et al, 2004)

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