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Electrical Stimulation to Enhance Lower Limb Muscle Function

After SCI, it is well established that muscles experience deconditioning, especially those denervated following complete SCI. The most visible effect of deconditioning is muscle atrophy, characterized by a reduction in size of individual muscle fibers (Castro et al., 1999a; Castro et al., 1999b). Deconditioning is also associated with a complex cascade of biochemical events and alterations over time in muscle composition such as changes to muscle fiber type (Stewart et al., 2004; Round et al., 1993). Functionally, these changes manifest as loss of strength and endurance of muscular contractions and have been targets for various interventions. It should be noted that there might be additional benefits to enhancing muscle structure and function in addition to the immediate functional consequences of enhancing strength and endurance. For example, muscular contractions have the added potential of ameliorating loss of bone density following SCI. In addition, Anderson (2004) noted that future treatments developed for chronic SCI may require the reversal of muscle atrophy in order for benefits of the treatment to be detectable. Others have noted the potential health benefits (e.g., reduction in secondary conditions) that may be associated with reducing muscle atrophy and enhancing muscular strength and endurance (Shields and Dudley-Javoroski, 2006). Various rehabilitation techniques have focused on reducing or reversing these detrimental changes to the muscles of the lower limb following SCI.

A variety of electrical stimulation techniques have been employed to enhance lower limb muscle structure and function in people with SCI. These typically involve delivering a series of electrical pulse trains to the muscle (or nerve supplying the muscle) over time such that it simulates the “normal” exercise experience. Specific stimulation parameters (i.e., pulse width, training duration, between training intervals, method of application) and other exercise-related variables (i.e., frequency, duration, intensity, and program length) may each be varied to attain an optimal training stimulus. Given the number and variety of these factors, it is not surprising that there is considerable heterogeneity among the specific electrical stimulation interventions that have been investigated to date. In the present review we focus on two strategies: NMES and FES. Whereas both methods typically employ cyclical patterns of electrical stimulation that simulate natural muscular activity, FES is directed towards the attainment of purposeful movement such as cycling or walking, although it has also been used to address other issues such as pressure sores and spasticity (Bersch et al., 2015, Kawasaki et al., 2014). NMES, on the other hand, is focused on producing muscle contractions to generate muscle force such as in an isometric condition. In some applications, NMES techniques have been used as a training stimulus to prepare muscles for a subsequent FES training condition (e.g., Kern et al., 2005; Hjeltnes and Lannem, 1990). In situations where increased muscle torque and endurance are primary goals to improve function, for example in the quadriceps in an incomplete SCI, the outcomes of these experimental studies have direct clinical relevance.

Table 5: NMES Studies Examining Muscle Function and Morphology

Author Year; Country
Score
Research Design
Total Sample Size
MethodsOutcomes
Harvey et al. 2010; Australia

PEDro=10

RCT

Level 1

N=20

Population: Complete or incomplete SCI patients

Experimental group – 7 males, 3 females; mean age 40; mean YPI 3

Control group – 7 males, 3 females; mean age 39; mean YPI 4.

 

Treatment: ES superimposed on PRT 3 days/week for 8 weeks (12 sets of 10 knee extension repetitions against increasing resistance, the first 6 using ES and voluntary contraction and the second 6 using only ES).

 

Outcome Measures: Quadriceps strength and endurance, the performance and satisfaction scales of the Canadian Occupational Performance Measure (COPM), the ES-evoked quadriceps strength (Nm), ES-evoked quadriceps endurance (fatigue ratio), participant perception of treatment effectiveness.

 

1.   There was a statistically significant group differences for voluntary quadriceps strength change (14 Nm), but the magnitude may not be clinically important.

2.   ES group had greater perception of treatment effectiveness over control.

3.   There was no group difference in any other variables.

Effect Sizes: Forest plot of standardized mean differences (SMD ± 95%C.I.) as calculated from pre- and post-intervention data
Baldi et al. 1998;

USA

PEDro=5

RCT

Level 1

N=26

Population: 26 males and females; age 25-28 yrs; traumatic motor complete; cervical or thoracic lesion level; 15 wks post-injury.

 

Treatment: Random assignment to 3-6 months of 1. FES-assisted cycle ergometry (n=8), 30 min, 3X/week; 2. PES-assisted isometric exercise group (n=8) (same muscle groups as FES group) for 1 hr, 5X/week and 3 control group (n=9) with no stimulation.

 

Outcome Measures: lean body mass lower limb.

1.   Lean body mass increased with FES-cycling at all regions and declined for control and PES group.

2.   With respect to total body lean mass, lower limb lean mass and gluteal lean mass, controls lost an average of 6.1%, 10.1%, 12.4% after 3 months and 9.5%, 21.4%, 26.8% after 6 months.

Effect Sizes: Forest plot of standardized mean differences (SMD ± 95%C.I.) as calculated from pre- and post-intervention data

Shields & Dudley-Javoroski 2006;

USA

Prospective Controlled Trial

Level 2

N=7

Population: 7 males; age 21-43 yrs; AIS A; C5-T10 lesion level; ³ 6 weeks post-injury

 

Treatment: PES exercise to unilateral ankle plantarflexion (untrained leg served as a control). Four 4 min exercise bouts, 5 days/week for 1.87-3.05 years.

 

Outcome Measures: Stimulated ankle torque and soleus twitch profiles at baseline and every 6 months up to 3 years.

1.   Compared to the untrained side, stimulated limb had:

2.   Increased strength (increased peak stimulated ankle torque and higher torque-time integrals).

3.   More resistant to fatigue (increased muscle fatigue indexes).

4.   Increased twitch difference (indicative of force generating capacity), especially with successive stimulation trains.

 

 

 

Ryan et al. 2013;

USA

Pre-post

Level 4

N=14

Population: 14 participants with chronic motor complete SCI (11M 3F); 2 diabetic. Inclusion criteria included: 18-65 yrs of age; AIS A or B classification; normative range of motion in the knee and hip joints.

 

Treatment: Participants performed RET of the knee extensor muscles 2 times/week for 16 weeks. 4 sets of 10 knee extensions were performed using NMES.

 

Outcome Measures: Plasma glucose and insulin throughout a standard clinical oral glucose tolerance test; thigh muscle and fat mass via dual-energy x-ray absorptiometry; quadriceps and hamstrings muscle size and composition via MRI; muscle oxidative metabolism using phosphorus magnetic resonance spectroscopy.

1.     After RET, thigh fat tissue (g), thigh percentage fat and bone mineral density of the femur bone was not different. Lean tissue of the thigh area increased by approximately a mean(SD) of 10(15)%g.

2.     Quadriceps muscle volume (average of both legs) was increased by 39(27)% after RET (pre vs post: 618(343) vs 815(399) cm3). No change was observed in absolute fat volume for either the quadriceps or hamstring muscles. No relation was found between the magnitude of muscle hypertrophy and improvements in glucose or insulin status.

3.     8 participants had measurements of PCr recovery kinetics. Time constants for the recovery of PCr after electrical stimulation were 102(24) and 77(18) seconds before and after RET; this represents an approximate 25% improvement in skeletal muscle oxidative capacity, which was statistically significant.

Sabatier et al. 2006; USA

Pre-post

Level 4

N=5

Population: 5 males; mean (SD) age 35.6(4.9) yrs; complete; C5-T10 lesion level; 13.4(6.5) yrs post-injury

 

Treatment: 18 weeks of neuromuscular electrical stimulation resistance training for the quadriceps combined with additional weight around the shin, 2x/week with 4 sets of knee extensions.

 

Outcome Measures: Weight lifted, muscle mass, muscle fatigue

 

1.     All participants increased weight lifted during training by an average (SD) of 6.9(1.4) kg

2.     Significant increases in cross-sectional area of quadriceps femoris in both thighs (right mean CSA increased from 32.6 to 44.0 cm2, left mean increased from 34.6 to 47.9 cm2)

3.     Progressive decrease in fatigue throughout training and after 18 weeks of training. Decreases significantly at 12 weeks and 18 weeks.

 

Belanger et al. 2000; Canada

Pre-post

Level 4

N=14

Population: 14 males and females; age 23-42 yrs; 2 incomplete, 12 complete lesions; C5-T5 lesion level; 1.2-23 yrs post-injury

 

Treatment: Bilateral functional electrical stimulation to quadriceps combined with isokinetic resistance training on left side and unresisted on right; 5 days/week, 24 weeks; each session was 1 hr or until fatigue

 

Outcome Measures: knee torque, endurance

1.   Average increase in knee extensor muscle torque on resisted side was 150% (average 8.1% increase/week)

2.   Average increase in knee muscle torque on unresisted side was 75% (average 4.5% increase/week)

3.   No change in endurance (fatigability)

Kagaya et al. 1996; Japan
Pre-postLevel 4
N = 5
Population: 5 males; age 19-68 yrs; with complete paraplegia (T5-L2 lesion level); 3-60 months post-injury.

 

Treatment: Subcutaneous PES to various lower limb nerves and muscles for 6 months. Applied at 10 min, 3X/day and gradually increased to 60 min, 3X/day at 10 weeks.

Outcome Measures: Muscle cross-sectional area (CT scan), manual muscle test, stimulated muscle torque.

1.   No group statistical analysis performed, limited by heterogeneity across participants.

2.   All cross-sectional muscle areas except gluteus maximus increased significantly.

3.   Muscle torques generally increased after PES.

4.   Manual muscle tests generally increased significantly for muscles that initially graded as poor-minus (no voluntary movement against gravity).

Hjeltnes and Lannem 1990;

Norway

Pre-post

Level 4

N=4

Population: 4 males and females; age 20-36 yrs; Frankel A; T5-T12 lesion level; 3 mos-5 yrs post-injury

 

Treatment: PES, 4 weeks, 2x/day, 5-10mins, isokinetic resistance to quadriceps muscles followed by 4 weeks, 30 min, 2X/day, 4-5X/day of integrated training of rising and standing.

 

Outcome Measures: Knee extension torque, thigh circumference, CK, collected monthly.

1.     No group statistics done. At least 2 participants had increased knee extension torque, increased muscular endurance, increased thigh circumference, increased CK (indicator of muscle injury). The more acute participant stopped training due to muscle spasms.

2.     One participant progressed to the planned stage of FNS-assisted ambulation training.

 

 

 

 

 

 

 

 

Gerasimenko et al. 2015

Russia

Post-test

Level 4

N=10

Population: 10 individuals- 5 able bodied and 5 with SCI.

 

Treatment: Painless transcutaneous electrical enabling motor control (pcEmc) neuromodulates the physiological state of the spinal cord. This method includes electrically activating the spinal circuitry via electrodes placed on the skin overlying the vertebrae of the lower thoracic and/or lumbosacral vertebrae. This waveform consists of 0.3- to 1.0-ms bursts with a carrier frequency of 10 kHz administered at 5 to 40 Hz. PcEmc stimulation was delivered by a 2.5-cm round electrode placed midline at the C5, T11, and/or L1 spinous processes as cathodes and two 5.0 10.2 cm2 rectangular plates made of conductive plastic placed symmetrically on the skin over the iliac crests as anodes. Biphasic rectangular 0.5- to 1.0-ms pulses with a carrier frequency of 10 kHz and at an intensity ranging from 30 to 200 mA were used.

 

Outcome Measures: EMG amplitude

1.   Use of the multielectrode surface array can fine-tune the control of the locomotor behavior.

2.   The pcEmc strategy combined with exoskeleton technology is effective for improving motor function in paralyzed patients with SCI.

Discussion

Most studies involving NMES and strength evaluated this in individuals with complete or motor complete SCI (Hjeltnes and Lannem, 1990; Kagaya et al. 1996; Shields and Dudley-Javoroski, 2006). In general, all studies produced beneficial results on muscle size (i.e., reduced muscle atrophy). In addition to enhancing muscle bulk, most interventions also focused on improving muscle function, most notably strength and endurance, as well as contractile speed and muscle fatigue.

 

Studies with the strongest research design and supporting the efficacy of NMES were conducted by Harvey et al. (2010) and Shields and Dudley-Javorski (2006). Harvey et al. (2010) used an RCT design in persons with both complete and incomplete SCI and found that NMES-assisted exercise increased voluntary quadriceps strength over those that received no intervention. The increase in strength was statistically higher in the experimental group, but it was uncertain if the increase had a clinically important effect. Shields and Dudley-Javorski (2006) employed an experimental non-RCT design to examine the effect of long-term (up to 3 years) NMES exercise to unilateral ankle plantarflexor muscles with the untrained leg serving as a control. This study examined 7 males with complete and relatively recent injuries (~6 weeks post-injury). Peak stimulated ankle torque (i.e, non-voluntary) was found to be significantly greater in the stimulated leg as compared to the untrained leg. The trained side also generated significantly higher torque-time integrals than the untrained side. Other pre-post study designs of NMES-assisted exercise also found increased stimulated muscle forces or torques following training although the participants involved in these studies were generally more chronic (Sabatier et al., 2006; Kagaya et al., 1996; Hjeltnes and Lannem, 1990).

Conclusion

  • There is level 1b evidence (Harvey et al., 2010) that PES-assisted exercise may increase voluntary muscle strength, but the increase may not have a clinically important treatment effect.
  • There is level 2 evidence (Baldi et al., 1998) that PES-assisted isometric exercise reduces the degree of lower limb muscle atrophy in individuals with recent (~10 weeks post-injury) motor complete SCI, but not to the same extent as a comparable program of FES-assisted cycling exercise.

There is level 4 evidence (Sabatier et al., 2006) that PES-assisted exercise may partially reverse the lower limb muscle atrophy found in individuals with long-standing (>1 year post-injury) motor complete SCI.