Length–tension properties of ankle muscles in chronic human spinal cord injury

Abstract

Contracture, or loss of range of motion (ROM) of a joint, is a common clinical problem in individuals with spinal cord injury (SCI). In order to measure the possible contribution of changes in muscle length to the loss of ankle ROM, the active force vs. angle curves for the tibialis anterior (TA) and gastrocnemius⧹soleus (GS) were measured in 20 participants, 10 with SCI, and 10 gender and age matched, neurologically intact (NI) individuals. Electrical stimuli were applied to the TA and GS motor nerves at incremented angles of the entire ROM of the ankle and the resulting ankle and knee torques were measured using a multi-axis load cell. The muscle forces of the TA and GS were calculated from the torque measurements using estimates of their respective moment arms and the resulting forces were plotted against joint angle. The force–angle relation for the GS at the ankle (GSA) was significantly shifted into plantar flexion in SCI subjects, compared to NI controls (t-test, p<0.001). Similar results were obtained based upon the GS knee (GSK) force–angle measurements (p<0.05). Conversely, no significant shift in the force–angle relation was found for the TA (p=0.138). Differences in the passive ROM were consistent with the force–angle changes. The ROM in the dorsiflexion direction was significantly smaller in SCI subjects compared to NI controls (p<0.05) while the plantar flexion ROM was not significantly different (p=0.114). Based upon these results, we concluded that muscle shortening is an important component of contracture in SCI.

Introduction

Contracture, a common complication of spinal cord injury (SCI), consists of a loss of joint range of motion (ROM) and is associated with a change in the mechanical properties of the joint tissues. It has been suggested that contracture occurs through two mechanisms. The first is an increase in the stiffness of the connective tissue within the joint capsule or in the associated muscles (Akeson et al., 1977; Botte et al., 1988). A second is that muscles shorten by removing sarcomeres and/or muscle fibers, which then leads to a decrease in joint ROM (Tabary et al., 1972; Williams and Goldspink, 1978; Friden and Lieber, 2003).

Due to disuse, SCI is likely to result in changes in the structural components of the muscle and joint capsule. For example, molecular changes in muscle connective filament proteins, like titin, occur after prolonged disuse in animals (Toursel et al., 2002). In addition, biochemical changes in the collagenous tissues of the rabbit knee occur with disuse, resulting in changes in mechanical properties of the joint (Akeson et al., 1973; Woo et al., 1975). As a result, changes in connective tissue have been implicated as a contributing cause of contracture (Botte et al., 1988; Akeson et al., 1987).

Contracture may also result from changes in muscle length due to a loss of sarcomeres or a change in muscle architecture. Immobilization in a shortened position results in a decrease in the number of sarcomeres in mouse (Williams and Goldspink, 1978) and rat (Witzmann et al., 1982) hindlimb muscles. The decrease in number of sarcomeres results in a decrease in the optimal fiber length, altering the length–tension properties of the muscle (Williams and Goldspink, 1978; Witzmann et al., 1982). While these changes in muscle length have been documented in immobilization studies in animals, it is unknown whether they contribute to contracture in humans following a neural injury.

For the current study, we postulated that ankle contracture in SCI is, at least in part, the result of muscle length changes. The active torque–angle properties of the ankle muscles were measured in chronic human SCI and in age-matched, neurologically intact (NI) controls. It was inferred that differences in the active torque–angle relations reflected a physiological change in the muscle length, manifested as a change in length–tension characteristics.

Contracture was quantified using measurements of the passive resistance to imposed movements at the ankle and was represented using curves of torque vs. angle. A correlation analysis of active torque–angle measurements and contracture was used to determine whether changes in muscle length, presumably through muscle shortening, contribute to contracture in human SCI.