Paradigms of Lower Extremity Electrical Stimulation Training After Spinal Cord Injury

Summary

Spinal cord injury is a traumatic medical condition that may result in elevated risks of chronic secondary metabolic disorders. Here, we presented a protocol using surface neuromuscular electrical stimulation-resistance training in conjunction with functional electrical stimulation-lower extremities cycling as a strategy to ameliorate several of these medical problems.

Abstract

Skeletal muscle atrophy, increased adiposity and reduced physical activity are key changes observed after spinal cord injury (SCI) and are associated with numerous cardiometabolic health consequences. These changes are likely to increase the risk of developing chronic secondary conditions and impact the quality of life in persons with SCI. Surface neuromuscular electrical stimulation evoked resistance training (NMES-RT) was developed as a strategy to attenuate the process of skeletal muscle atrophy, decrease ectopic adiposity, improve insulin sensitivity and enhance mitochondrial capacity. However, NMES-RT is limited to only a single muscle group. Involving multiple muscle groups of the lower extremities may maximize the health benefits of training. Functional electrical stimulation-lower extremity cycling (FES-LEC) allows for the activation of 6 muscle groups, which is likely to evoke greater metabolic and cardiovascular adaptation. Appropriate knowledge of the stimulation parameters is key to maximizing the outcomes of electrical stimulation training in persons with SCI. Adopting strategies for long-term use of NMES-RT and FES-LEC during rehabilitation may maintain the integrity of the musculoskeletal system, a pre-requisite for clinical trials aiming to restore walking after injury. The current manuscript presents a combined protocol using NMES-RT prior to FES-LEC. We hypothesize that muscles conditioned for 12 weeks prior to cycling will be capable of generating greater power, cycle against higher resistance and result in greater adaptation in persons with SCI.

Introduction

It is estimated that approximately 282,000 persons in the U.S. are currently living with spinal cord injury (SCI)¹. On average, there are roughly 17,000 new cases annually, primarily caused by motor vehicle crashes, acts of violence, and sporting activities¹. SCI results in partial or total interruption of neural transmission across and below the level of injury², leading to sub-lesional sensory and/or motor loss. After injury, activity of skeletal muscle below the level of injury is greatly reduced, leading to a rapid decline in lean mass and concomitant infiltration of ectopic adipose tissue, or intramuscular fat (IMF). Studies have shown that lower extremity skeletal muscle experiences significant atrophy within the first few weeks of injury, continuing throughout the end of the first year^3,4. As soon as 6 weeks post-injury, individuals with complete SCI experienced an 18-46% decrease in sub-lesional muscle size compared to age and weight-matched abled-bodied controls. By 24 weeks post-injury, skeletal muscle cross-sectional area (CSA) could be as low as 30 to 50%³. Gorgey and Dudley showed that skeletal muscle continues to atrophy by 43% of the original size 4.5 months post-injury and noted a three times greater amount of IMF in persons with incomplete SCI compared to abled-bodied controls⁴. Loss of metabolically active lean mass results in a reduction in basal metabolic rate (BMR)^2,6, which accounts for ∼65-70% of the total daily energy expenditure; such reductions in BMR can lead to a detrimental energy imbalance and increasing adiposity after injury^{2,7,8,9,10,18}. Heightened adiposity has been linked to the development of chronic secondary conditions including hypertension, type II diabetes mellitus (T2DM) and cardiovascular disease^{2,10,11,12,13,14,15,16,17,18}. Moreover, persons with SCI may suffer from malnutrition and reliance on a high fat diet. Dietary fat intake may account for 29 to 34% of the fat mass in persons with SCI, which is likely a factor explaining increasing adiposity and the escalating prevalence of obesity within the SCI population^12,13.

Neuromuscular electrical stimulation evoked resistance training (NMES-RT) was designed to induce hypertrophy of paralyzed skeletal muscle^{19,20,21,22,23,24}. Following twelve weeks of twice-weekly NMES-RT, skeletal muscle CSA of the whole thigh, knee extensor and knee flexor muscle groups increased by 28%, 35% and 16%, respectively²². Dudley et al. showed that 8 weeks twice-weekly of NMES-RT restored knee extensor muscle size to 75% of the original size at six weeks post-injury¹⁹. Moreover, Mahoney et al. utilized the same protocol and noted a 35% and 39% increase in the right and left rectus femoris muscles after 12 weeks of NMES-RT²⁰.

Functional electrical stimulation-lower extremities cycling (FES-LEC) is a common rehabilitation technique used to exercise lower extremity muscle groups after SCI^25,26. Unlike NMES-RT, FES-LEC relies on stimulation of 6 muscle groups, which may result in increased hypertrophy and improvements in the cardiometabolic profile^{10,25,26,27,28}. Dolbow et al. found that total body lean mass increased by 18.5% following 56 months of FES-LEC in an individual with SCI²⁷. Following twelve months of thrice-weekly FES-LEC, a 60-year old female with paraplegia experienced a 7.7% increase in total body lean mass and a 4.1% increase in leg lean mass²⁸. Routine use of functional electrical stimulation (FES) is associated with improvement in risk factors of cardiometabolic conditions after SCI^10,25,26.

Ideal candidates for electrical stimulation training will have either motor complete or incomplete injuries, with intact peripheral motor neurons and limited lower extremity sensation. The current manuscript, describes a combined approach using NMES-RT and FES-LEC designed to improve outcomes of electrical stimulation training in persons with chronic SCI. The process of NMES-RT using ankle weights will be outlined, while highlighting key steps within the protocol and the overall benefit the intervention provides to persons with chronic SCI. The second aim is to describe the process of FES-LEC designed to maximize the overall cardiometabolic effect of intervention. Previous work has affirmed our rational that a combined training protocol may evoke greater outcomes following 24 weeks of electrical stimulation training^{20,21,22,23,24,25,26,31,32,33,34,35,36}.

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Protocol

The training protocol described in this manuscript is registered with clinicaltrials.gov identifier (NCT01652040). The training program involves NMES-RT with ankle weights and FES-LEC. All necessary equipment is listed in Table 2. The study protocol and informed consent were reviewed and approved by the Richmond VAMC Institutional Review Board (IRB) and Virginia Commonwealth University (VCU) IRB. All study procedures were explained in-detail to each participant before beginning the trial.

1. Participant Recruitment

1. Perform a pre-screening evaluation with potential participants.
   1. Thoroughly explain the details of the training protocol including the length of study (24 weeks), times per week (bi-weekly) and length of sessions (NMES-RT: 30 min and FES-LEC: 45-60 min).
      NOTE: NMES-RT is conducted for the first 12 weeks, followed by 12 weeks of FES-LEC.
   2. Describe the medical requirements to the potential participant including: male or female with SCI, American Spinal Injury Classification (AIS) A, B or C (those with an AIS "C" classification who are unable to stand up and walk), 18 to 65-year old, greater than 1-year post-injury, body mass index (BMI) ≤ 30 kg/m², motor complete or incomplete C5-L2 level of injury.
   3. Describe the medical restrictions to the potential participant including: a diagnosis of cardiovascular disease, uncontrolled type II diabetes mellitus or those on insulin, uncontrolled hypertension, pressure sores stage 3 or greater, urinary tract infection or symptoms, osteoporosis with T-Score -2.5, and pregnancy for women with SCI.

2. NMES-RT

1. Ensure the participant voids his/her bladder and measure the resting blood pressure and heart rate. While participant is seated in wheelchair, instruct the participant to take off his/her shoes. Then, place a pillow behind the calf to cushion the leg during knee flexion. Apply ankle weights (0-26 lbs.) to the participant's ankles (Figure 1).
   NOTE: The initial 2 sessions are conducted without ankle weights to ensure the participant can lift his/her leg against gravity.
2. Apply two 7.5 cm x 12.7 cm adhesive carbon electrodes bilaterally on the skin over the knee extensor muscle group.
   1. Place the distal electrode ~1/3 the distance between the patella and inguinal fold and medial to the midline of the quadriceps. Place the electrode longitudinally and parallel to the midline axis running from the hip to the knee joints (Figure 2).
   2. Place the proximal electrode laterally and adjacent to the inguinal fold over the vastus lateralis muscle. Place the electrode longitudinally and parallel to the midline axis (Figure 2).
3. Set a portable stimulator to a frequency of 30 Hz and a biphasic rectangular pulse width of 450 µs and 50 µs interpulse interval^{19,20,21,22,23,24,37,38,39}. Connect the cables from the stimulator to each electrode.
   NOTE: The polarity of the electrodes does not influence the stimulation pattern as long as the electrodes are positioned correctly.
4. Beginning with the right leg, gradually increase the current until a noticeable visible tension is recognized in the knee extensor muscle group. Continue to slowly ramp the current to evoke full knee extension (max. 200 mA). Allow the leg to remain extended for 3-5 s to evoke maximum tension in the activated motor units.
5. Gradually decrease the current until it's below 50% of the target current required to extend the leg and move leg eccentrically back to the starting position. Record the current amplitude necessary to evoke full leg extension.
6. Complete unilateral training including 4 sets of 10 repetitions per leg and alternate between right and left legs. Allow the leg to rest 3-5 s between each repetition and 3 min between sets. If participant does not reach full knee extension, record the %range of motion and increase the time between repetitions.
   NOTE: Muscle fatigue is defined as two consecutive repetitions with a range of motion ≤ 25%.
7. Attempt each of the four sets, but if participant experiences muscle fatigue, end the current set and continue training on the opposite leg. If full knee extension is achieved without muscle fatigue for 2 consecutive training sessions, add 2 lbs. of ankle weights the following week of training.

3. FES-LEC

1. Measure the participant's resting blood pressure and heart rate. Position the participant in front of the FES ergometer bike (Table of Materials) seated in his/her personal power or manual wheelchair (Figure 3a, Figure 3b).
2. Apply adhesive carbon electrodes to the knee extensor, knee flexor and gluteus maximus muscle groups bilaterally.
   1. For knee extensors, place the distal electrode (7.5 x 12.7 cm) on the skin 1/3 the distance between the patella and inguinal fold, over the vastus medialis muscle. Place the proximal electrode laterally and adjacent to the inguinal fold over the vastus lateralis muscle (Figure 4a).
   2. For knee flexors, place the distal electrode (7.5 x 10 cm) on the skin 2-3 cm above the popliteal fossa. Place the proximal electrode 20 cm above the popliteal fossa (Figure 4b). To prevent movement of the distal electrode, apply an elastic wrap to secure positioning of the electrode (Figure 3a).
   3. For gluteus maximus, instruct the participant to lean forward towards the ergometer. Place two electrodes (5 x 9 cm) parallel and on the bulk of the muscle belly; allow ~two fingers width of separation between the electrodes.
3. With the participant seated in his/her wheelchair and centered in front of the ergometer, connect the cables from the stimulator to each of the 12 electrodes. Check the front and back of the ergometer to make sure the participant is correctly centered.
4. Ensure that the participant's wheelchair is locked and gently place the participant's feet (wearing tennis shoes) inside the pedals (Figure 6). Secure the lower leg to the ergometer using the elastic straps wrapped in a fabric covering. Secure the participant's feet in place with the two crossing elastic straps and Velcro located on each petal (Figure 5).
5. After strapping the legs to the ergometer, passively move the legs so observe the cycling pattern. If the legs are too compressed or hyperextended, adjust the height of the bike and recheck the position by passively moving the leg.
6. Secure the participant's wheelchair to the ergometer using the two extendable hooks located at the base of the ergometer. Connect the hooks to a stable structure underneath the wheelchair (Figure 5). Place two wooden breaks underneath the wheels of the wheelchair, to prevent any movement of chair during cycling.
7. Set the stimulation frequency to 33.3 Hz, pulse duration to 350 µs and the current amplitude to 140, 100, 100 mA for the knee extensor, knee flexor and gluteus maximus muscle groups, respectively.
8. Set the cycle parameters as follows: target speed of 40-45 revolutions per minute (RPM); adjustable motor torque starting at 10 Nm; resistance of 1.0, 1.5 and 2.0 Nm for exercise stages I, II and III.
9. Set the interval training parameters as follows: 3 min "warm up" phase; three 10-min exercise stages (stimulation on); a 2-min resting phase following each exercise stage; and 3 min "cool down" phase.
10. Based on the level of injury (above or below T4), measure the blood pressure and heart rate every 2 to 5 min to prevent the occurrence of any symptoms of autonomic dysreflexia.
11. If blood pressure remains elevated, stop the ergometer and instruct the participant to void his/her bladder or rest if they have already voided. In addition, check to ensure the participant is seated properly to reduce any pressure points and check that the shoes or any straps are not overly-tightened. Monitor blood pressure closely every 2 min. If blood pressure recovers, resume training; if blood pressure remains unrecovered, end the session and instruct the participant to see his/her primary care physician.
    NOTE: It is vital to ensure that participants consistently take their blood pressure medication, if any, and void their bladder before FES-cycling.
12. Record the participant's heart rate, speed, power, distance, resistance and % stimulation every 30 s.
13. If participant completes an entire exercise session without fatigue (speed < 18 RPM during active cycling), decrease the servo motor torque assistance by 1 Nm the following session, otherwise keep all parameters the same.
14. If participant completes two exercise training sessions without fatigue or the use of servo motor assistance during exercise stages, increase the resistance by 0.5 Nm in each exercise stage.

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Results

Ankle weights increased progressively for 22 participants, over 16 weeks of NMES-RT (Figure 6a). The average weights lifted by the participants was 19.6 ± 6.5 lb. (right leg) and 20 ± 6 lbs. (left leg) [8-24 lb.]. Current amplitude fluctuated throughout the trial for right and left legs (Figure 6b).

Progression of an individual with motor complete SCI followin...

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Discussion

The current study demonstrated two different paradigms of electrical stimulation. One paradigm is focused on implementing progressive loading to the trained muscle to evoke skeletal muscle hypertrophy and the other paradigm is primarily intended to enhance cardio-metabolic performance via enhancing aerobic capacity. The study ensured to compare both paradigms and to highlight the pros and cons of each.

NMES-RT is proven to be effective in restoring muscle size and evoking hypertrophy in person...

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Materials

Name	Company	Catalog Number	Comments
adhesive carbon electrodes (2 of each)	Physio Tech (Richmond, VA, USA 23233)	PT3X5 PALS3X4 E7300	7.5' x 12.7' 7.5' x 10' 5' x 9'
TheraTouch 4.7 stimulator	Richmar (Chattanooga, TN, USA 37406)	400-082	41.28' x 39.37' x 17.78' (8.91 kg) power: 110 VAC at 60 Hz / 220VAC at 50 Hz power consumption: 110 Watts
Red & White Lead Cords (2)	Richmar (Chattanooga, TN, USA 37406)	A1717	2.0 m
RT300-SL FES Ergometer	Restorative Therapies, Inc. (Baltimore, MD, USA 21231)	RT300-SL	80' x 49' x 92-103' (39 kg) 16 channel speed: 15 – 55 rev/min
elastic NuStim wraps (2)	Fabrifoam (Exton, PA, USA 19341)	PP108666	36"
wooden wheelchair break (2)	n/a	n/a	n/a
pillow/cushion	n/a	n/a	standard
ankle weights	n/a	n/a	2-26 lb.