On the relationship between tibia torsional deformation and regional muscle contractions in habitual human exercises in vivo

Abstract

The mechanical relationship between bone and muscle has been long recognized. However, it still remains unclear how muscles exactly load on bone. In this study, utilizing an optical segment tracking technique, the in vivo tibia loading regimes in terms of tibia segment deformation in humans were investigated during walking, forefoot and rear foot stair ascent and running and isometric plantar flexion. Results suggested that the proximal tibia primarily bends to the posterior aspect and twists to the external aspect with respect to the distal tibia. During walking, peak posterior bending and peak torsion occurred in the first half (22%) and second half (76%) of the stance phase, respectively. During stair ascent, two noticeable peaks of torsion were found with forefoot strike (38% and 82% of stance phase), but only one peak of torsion was found with rear foot strike (78% of stance phase). The torsional deformation angle during both stair ascent and running was larger with forefoot strike than rear foot strike. During isometric plantar flexion, the tibia deformation regimes were characterized more by torsion (maximum 1.35°) than bending (maximum 0.52°). To conclude, bending and torsion predominated the tibia loading regimes during the investigated activities. Tibia torsional deformation is closely related to calf muscle contractions, which further confirm the notion of the muscle–bone mechanical link and shift the focus from loading magnitude to loading regimes in bone mechanobiology. It thus is speculated that torsion is another, yet under-rated factor, besides the compression and tension, to drive long bone mechano-adaptation.

Introduction

Mechanical loading is a key determinant for bone adaptions. Locomotor activities evoke various types of bone deformation that differ in terms of type, amplitude, rate and frequency (Turner et al., 1995, Warden and Turner, 2004). It follows from beam theory that the hollow cylindrical geometry of the limb long bones is well designed to resist bending and torsion. Evidence also suggested that bending and torsion primarily constitute the human tibia loading regimes during walking and running (Yang et al., 2014b). However, in contrast to the amount of attention that compression, tension and thus loading has received in literature, the occurrence of torsional loading on bone has mostly been neglected—an omission that is probably owed to the technical difficulties of assessing torsion with conventional approaches.

Ample evidence demonstrates that muscles are closely related to bone adaptation (Kohrt et al., 2009, Rittweger, 2008, Rittweger et al., 2000, Sharir et al., 2011, Zanchetta et al., 1995). As muscles generally work against short levers, there is a good mechanical reason to hold that muscle contractions are responsible for the largest forces experienced by bone and would cause considerable bone bending. However, the near cylindrical structure of long bones does not only resist harness against unidirectional bending. Rather, it is speculated that torsion plays an important role in maintaining the near cylindrical structure of long bones, e.g. the distal tibia. And further suppose that muscle contractions may greatly contribute to the torsional loading. Nevertheless, to date, it remains unclear which loading regimes on bone are primarily produced by muscle contractions—another apparent omission in literature.

The aim of the present paper is to examine the hypotheses that regional muscle contractions would be temporarily related to bone deformations (hypothesis 1), and that these contractions would engender specific deformation regimens, e.g. antero-posterior (AP) and medio-lateral (ML) bending, internal–external (IE) torsion (hypothesis 2). For this purpose, an optical segment tracking (OST) approach previously described (Ganse et al., 2014, Yang et al., 2014a) was utilized to assess tibia deformation regimes in a set of characteristic habitual exercises, namely during walking, stair ascent and running with forefoot and rear foot strike, and isometric plantar flexion. The character of calf muscular contractions in tibia loading regimes was examined by analyzing the phase constitution of the tibia deformation regimes, assessing phase relationship between peak muscle activities and peak tibia deformation, comparing the tibia deformation between forefoot and rear foot exercises, respectively.