Dynamic "Range of Motion" Hindlimb Stretching Disrupts Locomotor Function in Rats with Moderate Subacute Spinal Cord Injuries

Abstract

Joint contractures and spasticity are two common secondary complications of a severe spinal cord injury (SCI), which can significantly reduce quality of life, and stretching is one of the top strategies for rehabilitation of these complications. We have previously shown that a daily static stretching protocol administered to rats at either acute or chronic time points after a moderate or moderate-severe T10 SCI significantly disrupts their hindlimb locomotor function. The objective of the current study was to examine the effects of dynamic range of motion (ROM) stretching on the locomotor function of rats with SCI as an alternative to static stretching. Starting at 6 weeks post-injury (T10 moderate contusion) eight adult Sprague-Dawley rats were subjected to hindlimb stretching for 4 weeks. Our standard stretching protocol (six maneuvers to stretch the major hindlimb muscle groups) was modified from 1 min static stretch-and-hold at the end ROM of each stretch position to a dynamic 2 sec hold, 1 sec release rhythm repeated for a duration of 1 min. Four weeks of daily (5 days/week) dynamic stretching led to significant disruption of locomotor function as assessed by the Basso, Beattie, Bresnahan (BBB) Open Field Locomotor Scale and three-dimensional (3D) kinematic and gait analyses. In addition, we identified and analyzed an apparently novel hindlimb response to dynamic stretch that resembles human clonus. The results of the current study extend the observation of the stretching phenomenon to a new modality of stretching that is also commonly used in SCI rehabilitation. Although mechanisms and clinical relevance still need to be established, our findings continue to raise concerns that stretching as a therapy can potentially hinder aspects of locomotor recovery.

Keywords: SCI; dynamic stretching; locomotor function; physical therapy; rehabilitation.

FIG. 1.

Locomotor function. (A) Dynamic stretching protocol began 6 weeks after spinal cord injury (SCI) when locomotor function had reached a stable plateau and continued on for 4 weeks. At the end of the first week of stretching, the animals had significantly lower Basso, Beattie, Bresnahan (BBB) scores as compared with their pre-stretch values. Over the weekend animals achieve significant recovery; however, the first session of the 2nd week of stretching induced deficits in the locomotor function that persisted to the end of the week. Similar pattern of recovery/disruption followed for the remaining 2 weeks of the stretching protocol. Four of the eight animals were euthanized after 2 h of stretching, for histological muscle assessment and the other four were allowed to recover for 4 weeks before being euthanized. Their locomotor function was assessed weekly (dotted line). (B,C) Analysis of biweekly kinematic and gait recordings showed that the animals had significantly reduced joint excursions (B) and gait indices (C) indicative of lack of stepping or even sweeping in some animals during the weeks of the stretching therapy (weeks 6 and 8), as compared with the pre-stretch stepping ability and hindlimb joints excursions (week 4). By week 12, the locomotor function of the remaining four animals had achieved significant recovery back to pre-stretch levels.

FIG. 2.

Characteristics of vibration response. Kinematic analysis was performed on the contralateral limb vibration response during a release of 2 sec hamstring stretch of the opposite limb. Vibrations occurred in both limbs simultaneously; however, kinematic analysis was performed on the contralateral limb, as more points were visually available and could be tracked with the software for analysis. (A) During a vibration response, the limb goes through multiple clonic-like contractions, as evidenced by the multiple peaks in velocity of the toe–ankle–knee angle in 1 sec. (B) Stick figure of the contralateral limb during a vibration response. The black line shows a steady position of the limb during the 2 sec stretch hold period of the opposite limb. Upon release of stretch, the clonic-like contractions (gray stick figures) are initiated as the limb is pulled in toward the body (knee and hip are flexed). Most of the movement occurs in the ankle joint, with an average range of motion of 14 degrees, and contractions occurring at high frequency (∼12 peaks per second).