Disruption of Locomotion in Response to Hindlimb Muscle Stretch at Acute and Chronic Time Points after a Spinal Cord Injury in Rats

Abstract

After spinal cord injury (SCI) muscle contractures develop in the plegic limbs of many patients. Physical therapists commonly use stretching as an approach to avoid contractures and to maintain the extensibility of soft tissues. We found previously that a daily stretching protocol has a negative effect on locomotor recovery in rats with mild thoracic SCI. The purpose of the current study was to determine the effects of stretching on locomotor function at acute and chronic time points after moderately severe contusive SCI. Female Sprague-Dawley rats with 25 g-cm T10 contusion injuries received our standard 24-min stretching protocol starting 4 days (acutely) or 10 weeks (chronically) post-injury (5 days/week for 5 or 4 weeks, respectively). Locomotor function was assessed using the BBB (Basso, Beattie, and Bresnahan) Open Field Locomotor Scale, video-based kinematics, and gait analysis. Locomotor deficits were evident in the acute animals after only 5 days of stretching and increasing the perceived intensity of stretching at week 4 resulted in greater impairment. Stretching initiated chronically resulted in dramatic decrements in locomotor function because most animals had BBB scores of 0-3 for weeks 2, 3, and 4 of stretching. Locomotor function recovered to control levels for both groups within 2 weeks once daily stretching ceased. Histological analysis revealed no apparent signs of overt and persistent damage to muscles undergoing stretching. The current study extends our observations of the stretching phenomenon to a more clinically relevant moderately severe SCI animal model. The results are in agreement with our previous findings and further demonstrate that spinal cord locomotor circuitry is especially vulnerable to the negative effects of stretching at chronic time points. While the clinical relevance of this phenomenon remains unknown, we speculate that stretching may contribute to the lack of locomotor recovery in some patients.

Keywords: locomotor function; rehabilitation; spinal cord injury.

FIG. 1.

Timeline for the primary experimental procedures including functional assessments. SCI, spinal cord injury.

FIG. 2.

Acute and chronic Basso, Beattie, and Bresnahan (BBB) Open Field Locomotor Scores. (A) BBB scores are shown for the acute and chronic (ChS) stretch groups over the first 10 weeks post-injury. Drops in BBB scores were modest and not significant during the first 4 weeks but became significant at 5 weeks after higher perceived forces were applied starting at week 4. #Indicates significant differences between Monday morning and Friday afternoon BBB scores. *Indicates significant differences in BBB scores for stretched and unstretched groups. (B) BBB scores of the ChS group dropped dramatically after only 1 week of stretching. *Indicates significant differences between pre-stretch (week 10 Monday morning) and stretch BBB scores. SCI, spinal cord injury.

FIG. 3.

Kinematic and gait analysis of shallow water walking (SWW). Distal (hip-ankle-toe, HAT) and proximal (iliac crest-hip-ankle, IHA) joint excursions are indicated by the bars: top and bottom of the bar represents the mean peak extension and flexion, respectively, of the joint angles ± standard deviation, and thus bar length represents the mean angular excursion or range of motion (ROM). (A) Acute Stretch (AcS): Significant differences are indicated by (*) for HAT and IHA joint excursions of AcS animals compared with the Chronic Stretch (ChS) group. Significant differences are indicated by (#) for IHA and HAT excursions of AcS animals at week 4 (during stretching therapy) compared with week 8 (3 weeks after the last stretching session). (B) ChS: Significant differences indicated by (*, #) for ChS animals when comparing weeks 10 or 18 with weeks 12 and 14. In addition, IHA excursions remained significantly lower at week 10 compared with baseline (^). (C) AcS: Significant differences (*) were seen when comparing central pattern index (CPI), plantar stepping index (PSI), and regularity index (RI) for week 4 and week 8. (D) Significant differences indicated by (*, #) for ChS animals when comparing weeks 10 or 18 with weeks 12 and 14.

FIG. 4.

Nocturnal in-cage activity. (A) Acute Stretch: There were no statistically significant differences in distance traveled in the acute animals at any time points. (B) Chronic Stretch (ChS): Significant differences in overnight activity of ChS animals are indicated by (#, *) for ChS animals when comparing weeks 8 or 20 with weeks 11–14.

FIG. 5.

Amplitude of magnetically evoked muscle responses (MEMRs). Significant differences are indicated by (*, #) for Acute Stretch (AcS) and Chronic Stretch (ChS) animals when comparing normalized MEMRs at weeks 13, 16, or 20 to weeks 4 or 8. There was no difference in MEMRs when comparing AcS and ChS animals at week 4. EMG, gastrocnemius muscle responses; BL, baseline.

FIG. 6.

Passive end range of motion (ROM). Significant differences are indicated by (*) for knee (A,B) and hip (C,D) angles at end ROM when comparing the Chronic Stretch (ChS) animals with the unstretched control animals at weeks 15 and 18. By week 18, the ChS animals had recovered significantly (^) when compared with week 15. IC, iliac crest. Color image is available online at www.liebertpub.com/neu