Musculoskeletal plasticity after acute spinal cord injury: effects of long-term neuromuscular electrical stimulation training

Abstract

Maintaining the physiologic integrity of paralyzed limbs may be critical for those with spinal cord injury (SCI) to be viable candidates for a future cure. No long-term intervention has been tested to attempt to prevent the severe musculoskeletal deterioration that occurs after SCI. The purposes of this study were to determine whether a long-term neuromuscular electrical stimulation training program can preserve the physiological properties of the plantar flexor muscles (peak torque, fatigue index, torque-time integral, and contractile speed) as well as influence distal tibia trabecular bone mineral density (BMD). Subjects began unilateral plantar flexion electrical stimulation training within 6 wk after SCI while the untrained leg served as a control. Mean compliance for the 2-yr training program was 83%. Mean estimated compressive loads delivered to the tibia were approximately 1-1.5 times body weight. The training protocol yielded significant trained versus untrained limb differences for torque (+24%), torque-time integral (+27%), fatigue index (+50%), torque rise time (+45%), and between-twitch fusion (+15%). These between-limb differences were even greater when measured at the end of a repetitive stimulation protocol (125 contractions). Peripheral quantitative computed tomography revealed 31% higher distal tibia trabecular BMD in trained limbs than in untrained limbs. The intervention used in this study was sufficient to limit many of the deleterious muscular and skeletal adaptations that normally occur after SCI. Importantly, this method of load delivery was feasible and may serve as the basis for an intervention to preserve the musculoskeletal properties of individuals with SCI.

FIG. 1

Representative examples. A: soleus torque at the end of a 125-train fatigue bout for a single subject. B: illustration of twitch difference (TD).

FIG. 2

Training and temporal effects for torque. Statistical significance is set at P < 0.05. A: mean ± SE soleus torque during the 125-train fatigue bout. Mean values for 5 consecutive trains at 7 points during the bout are depicted. B: mean ± SE soleus torque for trains 1–5 only. *, greater than untrained limb. §, greater than bin 1. C: mean ± SE soleus torque for trains 120–125 only. *, greater than untrained limb. §, greater than bin 1. §§, less than bin 1.

FIG. 3

Training and temporal effects for torque-time integral. Statistical significance is set at P < 0.05. A: mean ± SE soleus integral for trains 1–5 only. *, greater than untrained limb. §, greater than bin 1. B: mean ± SE soleus integral for trains 120–125 only. *, greater than untrained limb. §, greater than bin 1. †, less than bins 1–3.

FIG. 4

Temporal change in fatigue index. Statistical significance is set at P < 0.05. Mean ± SE fatigue index = 100 * minimum torque/maximum torque in a fatigue bout. *, greater than untrained limb. †, less than bins 1–3. §, less than bin 1.

FIG. 5

Training and temporal effects for torque rise time. Statistical significance is set at P < 0.05. A: mean ± SE soleus torque rise time during the 125-train fatigue bout. Mean values for 5 consecutive trains at 7 points during the bout are depicted. B: mean ± SE torque rise time for trains 1–5 only. *, greater than untrained limb. §, different from bin 1. †, less than bins 2 and 3. ‡, less than bins 2–5. C: mean ± SE soleus torque rise time for trains 120–125 only. *, greater than untrained limb. †, greater than bin 1. **, greater than bins 2 and 3. ‡, greater than bins 1 and 2. §, greater than bins 1–4. §§, greater than bins 1 and 2 and less than bins 4 and 5.

FIG. 6

Mean ± SE twitch difference for pulse 2. Within each train of 10 pulses, the minimum torque after pulse 1 was subtracted from the maximum torque generated by pulse 2, yielding a difference value that reflects the degree of torque fusion (see Fig. 1B). Statistical significance is set at P < 0.05. A: mean ± SE twitch difference for trains 1–5 only. *, greater than untrained limb. §, greater than bin 1. B: mean ± SE soleus twitch difference for trains 120–125 only. *, greater than untrained limb. §, greater than bin 1. §§, less than bin 1.

FIG. 7

Representative example of peripheral quantitative computed tomography (pQCT) scan image at the 4% site (distal tibial epiphysis) of the trained (right) and untrained (left) limbs at 2.5 yr post injury: subject 6 (Table 1).

FIG. 8

Mean ± SE bone mineral density at the distal tibia (4% site) for 4 subjects who underwent pQCT analysis. - - -, typical able-bodied bone density at this site (Eser et al. 2004).