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.

Stretching adversely modulates locomotor capacity following spinal cord injury via activation of nociceptive afferents.

“…Clonic-like responses and spasms were also present in the ipsilateral limb when it was stretched at week 8, but air stepping could not be observed because the limb was held in a stretched position. These three responses were observed in all animals and are consistent with our previous observations [171,254]. The responses can be observed while the limbs are being positioned ("pre-stretch") and stretched and then typically decline while the limb is maintained in the stretch position for 1 minutes.…”

“…However, some observations regarding the effects of stretch on locomotor function were made. Stretching of one limb for the first 6 weeks did not result in overall disruption to the locomotor function as in previous studies [165,171,218,254].…”

“…This observation, as suggested by Grau et al, demonstrates that NMDA-dependent adaptive plasticity remains functional since the spinal learning impairment was reversed with an opioid antagonist treatment and furthermore implies that this phenomenon is an example of metaplasticity as described by W. Abraham [250,303]. In our experiments 4-5 weeks of stretching resulted only in transient locomotor deficits as the animals' recovered locomotor function within 2 weeks of cessation of daily stretching [218,254]. However, when the rats are stretched for 8 weeks locomotor recovery is limited and some deficits in the finer aspects of locomotion persist [165,171].…”

“…Previously [171,218,254] we observed that stretching hindlimb muscles after an incomplete thoracic spinal cord injury induces motor responses in both the stretched (ipsilateral) and unstretched (contralateral) hindlimb. These responses have been noted and referred to as air stepping, spasms and kicking.…”

“…However, this type of intervention may lead to the DOMS as a result of eccentric muscle contractions. We have speculated that the activation and sensitization of nociceptive afferents as occurs in DOMS could be responsible for the disruption of locomotor function at least in our dynamic stretching study [254]. Therefore, if stretching in combination with muscle contraction is to be used for the treatment of muscle contractures, the assessment of the effects of such intervention on motor function should be done.…”