Surface electrical stimulation of skeletal muscle after spinal cord injury.

STUDY DESIGN: Survey. OBJECTIVE: Examine muscle contractile activity during electrical stimulation (ES) after spinal cord injury (SCI). SETTING: General community of Athens, Georgia, USA. METHODS: Eight clinically complete SCI adults (C6 to T12) 4+/-1 (mean+/-SE) years post injury and eight able-bodied adults were studied. Surface ES was applied to the left m. quadriceps femoris for three sets of 10, 1 s isometric actions (50 Hz trains, 400 micros biphasic pulses, 50 micros phase delay, 1 s: 1 s duty cycle) with 90 s of rest between sets. Current was set to evoke isometric torque that was (1) sufficient to elicit knee extension with 2.3 kg attached to the ankle (low level ES), and (2) intended to equal 30% (mid level ES) or 60% of maximal voluntary torque of able-bodied adults (high level ES, able-bodied only). The absolute and relative cross-sectional area (CSA) of m. quadriceps femoris that was stimulated as reflected by contrast shift in magnetic resonance images and torque were measured. RESULTS: Six+/-2, 20+/-2 and 38+/-4% of the average CSA of m. quadriceps was stimulated during low, mid and high level ES, respectively, for able-bodied. Corresponding values for SCI for low and mid level ES were greater (61+/-12 and 92+/-7%, P = 0.0002). Torque was related to the CSA (cm2) of stimulated muscle (Nm = 3.53 x stimulated CSA+13, r2 = 0.68, P = 0.0010), thus ES of a greater per cent of m. quadriceps femoris in SCI was attributed to their smaller muscle (24+/-3 vs 73+/-5 cm2, P = 0.0001). The decline in torque ranged from 9+/-l to 15+/-4% within and over sets for low, mid or high level ES in able-bodied. SCI showed greater (P = 0.0001) fatigue (19+/-3 to 47+/-6%). CONCLUSION: The territory of muscle activation by surface electrical stimulation varies among SCI patients. Given sufficient current, a large portion of the muscle of interest can be stimulated. The resulting torque is modest, however, compared to that attainable in able-bodied individuals due to the small size and limited fatigue resistance of skeletal muscle years after spinal cord injury.     

Morphometric analysis of rabbit skeletal muscle and peripheral nerve tissue after electrical stimulation

Transcutaneous medium frequency electrical stimulation is used extensively to improve muscle strength in people who encounter difficulty in improving strength voluntarily. The purpose of this study was to describe some morphometric effects of electrical stimulation applied to rabbit skeletal muscle and peripheral nerve tissue (N = 5 control and 7 experimental rabbits). Intermittent electrical current (4000 Hz pulse modulated at 50 Hz) was applied transcutaneously to adult female rabbit thigh muscle 3 times/week for 3 months. Muscle ATPase histochemical staining, followed by morphometric analysis, demonstrated that type IIB fibers in stimulated muscles (sartorius and vastus lateralis) had larger cross-sectional areas in comparison to nonstimulated muscle fibers. Type IIA fibers of the stimulated sartorius muscle also were hypertrophied in comparison to nonstimulated muscle fibers. The percentage distribution of muscle fiber types did not change significantly as a result of stimulation. The femoral nerves of these rabbits were fixed and stained. Morphometric analysis did not detect any significant change in myelin cross-sectional area or thickness. Also, nerve axoplasmic cross-sectional area in stimulated femoral nerves was not significantly different from controls. These data suggest that electrical stimulation can increase the size of skeletal muscle fibers if applied consistently for an extended period of time. Further research is needed to further characterize this effect and to determine whether the same effect can be observed in humans after prolonged stimulation. J Orthop Sports Phys Ther 1990;11(7):313-320.     

Acute and long-term effects on muscle force after intramuscular aponeurotic lengthening

Intramuscular aponeurotic lengthening of muscles or intramuscular tenotomy involves bisecting the connective tissue fibers of the aponeurosis or tendon within the muscle belly. Because of its superficial location in the muscle, the aponeurosis may be bisected without damaging muscle fibers. Despite the existence of common operative methods for gaining length in short muscles, the effects on force and muscle function have not been studied. For this purpose animal experiments were performed. The medial gastrocnemius muscle of six male Wistar rats was lengthened by cutting the proximal aponeurosis at 50% of its length perpendicularly to the collagen fibers. The length gain was maintained by 3 days of cast immobilization at maximal dorsiflexion of the ankle. The long-term effect of the treatment was studied after 6 weeks and compared with 10 untreated controls and with six sham operated animals. The muscle was isolated in situ, and the force length characteristics were determined. In the untreated controls, the aponeurotomy was performed and the length force experiment was repeated to study the acute effects. The aponeurotic lengthening led acutely to a temporary loss of force because of an incomplete connection of the distal part of the muscle to the proximal insertion, but force recovered completely within 6 weeks. Although results from animal experiments cannot be transferred directly to humans, the principles of physiology are similar. Thus, for clinical use, aponeurotic lengthening should be considered if muscle force needs to be preserved. However, the drop of muscle force after surgery must be respected when mobilizing the patient during the postoperative rehabilitation program.     

失神经骨骼肌萎缩电刺激治疗研究进展

显微外科早期修复周围神经损伤虽已取得很大进展,但神经修复后靶器官肌肉功能常不能完全恢复,因此周围神经损伤后常见并发症失神经骨骼肌萎缩的防治仍是临床面临的难题.基础研究和临床实践均证实电刺激治疗可有效防治失神经骨骼肌萎缩.该文就失神经骨骼肌萎缩病理机制及电刺激治疗机制、作用和临床应用作一综述.     

Response of the diaphragm muscle to electrical stimulation of the phrenic nerve. A histochemical and ultrastructural study

The histological, histochemical, and ultrastructural features of canine diaphragms subjected to pacing by high-frequency electrical stimulation (27 to 33 Hz) of the phrenic nerve are compared with unstimulated diaphragms and with diaphragms subjected to pacing by low-frequency stimulation (11 to 13 Hz). The high-frequency group showed a reduced tidal volume (fatigue) after long-term stimulation, and myopathic changes which included enlarged internal and sarcolemmal nuclei, ring fibers, moth-eaten fibers with irregular histochemical staining, core/targetoid fibers, and smearing and aggregation of Z-band material with electron microscopy. The low-frequency group did not develop a significant degree of fatigue or pathological changes, and showed histochemical evidence of transformation to fast-twitch (type II) fibers. Possible pathogenic mechanisms and their similarity to those in certain human neuromuscular diseases are discussed. The application of the findings resulting from high- and low-frequency stimulation to long-term diaphragm pacing in humans with chronic ventilatory insufficiency is also discussed.     

骨骼肌肌内血管瘤的诊断及手术治疗

目的：探讨彩色多普勒超声及磁共振成像（magnetic resonance imaging,MRI）对肌内血管瘤（intramuscular hemangioma,IMH）的诊断价值,及其手术疗效.方法：自2000年12月至2013年1月,手术治疗54例经术后病理证实为IMH的患者,其中男19例,女35例;年龄11～59岁,平均33.6岁;病程2.5～15年,平均5.2年.38例行彩色多普勒超声检查,14例行MRI检查.所有患者证实后均采用手术治疗,观察手术时间、术中出血量及术后并发症、术后病理分型的情况,并采用IMH疗效评定标准对其手术疗效进行评价.结果：43例获得随访,时间7～49个月,平均28.4个月.手术时间（53～187） min,平均76.3 min;术中出血量（70～350） ml,平均223.6ml;术后无伤口感染及死亡等并发症发生.经彩色多普勒超声检查确诊35例（92.12％）;MRI检查确诊13例（92.86％）.术后Brown病理分型：毛细血管型20例,海绵状血管型22例,混合型12例.根据IMH疗效评价标准,优29例,良8例,不满意4例,差2例.结论：彩色多普勒超声、MRI对肌内血管瘤的确诊率高,临床应用价值显著;手术治疗肌内血管瘤疗效好,术后症状明显缓解或彻底消失,生活质量显著提高,复发率低.     

Light and electron microscopic studies of phrenic nerves after long-term electrical stimulation

Light and electron microscopic evaluation were carried out on canine phrenic nerves subjected to long-term electrical stimulation. A total of 34 stimulated and 19 control nerves were studied by light microscopy, and 10 stimulated and five control nerves were evaluated by electron microscopy. Except in a few cases in which a higher current was used, the current used for stimulation was between 1 and 2 mA. The pulse width was 150 microseconds. The typical charge per pulse was 0.22 microC and charge density per pulse 1.125 microC/sq cm of real area. The total number of days of electrical stimulation in individual phrenic nerves ranged from 4 to 374. No morphological changes in the phrenic nerve that could be attributed to the electrical stimulation were observed by light or electron microscopic study. There were, however, two phrenic nerves cuffed with bipolar electrodes which showed focal demyelination at the electrode level, but these changes were caused by factors other than the electrical stimulation. The results of the studies have direct clinical implications to long-term stimulation of phrenic nerves.     

Functional electrical stimulation of long-term denervated, degenerated human skeletal muscle: estimating activation using T2-parameter magnetic resonance imaging methods

Abstract:  Functional electrical stimulation (FES) of long-term denervated, degenerated human skeletal muscle has proven to be a suitable method for improving a number of physiological parameters. The underlying mechanisms of activation of a denervated muscle fiber can be described with suitably modified and extended Hodgin-Huxley type models, coupled with three-dimensional (3D) finite element models of the surrounding electrical field. Regions of activation within a muscle can be determined using a 3D computer model. However, simulation results have not yet been validated experimentally. During and immediately after exercise, muscle shows increased T2-relaxation times. It is thus possible to estimate muscle activation noninvasively and spatially resolved with the magnetic resonance imaging (MRI) method of T2 mapping, which was, therefore, chosen as a suitable validation approach. Six patients were scanned prior to FES training with a multislice multiecho MSME-sequence at 3 Tesla and then asked to perform one of their regular daily training-sessions (leg extensions). Subjects were then repositioned in the MR-scanner and two to five postexercise scans were recorded. Pre- and postexercise scans were coregistered and T2-parameter maps were calculated. Regions of interest (ROIs) were drawn manually around quadriceps femoris and its antagonists. Activation was detected in all patients. In well-trained patients, activation in the quadriceps was found to be considerably higher than in its antagonists. These experimental results will help further improve existing models of FES of denervated degenerated human skeletal muscle.     

Quantitative histochemical evaluation of skeletal muscle ischemia and reperfusion injury

Acute arterial obstruction to the extremities is associated with significant morbidity and mortality. The evaluation of accompanying skeletal muscle injury has thus far been indirect and imprecise. Triphenyltetrazolium chloride (TTC) is an oxidation-reduction indicator which allows for the histochemical quantitation of skeletal muscle injury. In 21 anesthetized nonheparinized adult mongrel dogs, the isolated in vivo gracilis muscle underwent 4, 6, or 8 hr of ischemia with and without reperfusion. The muscles were excised and cut into 1-cm segments, representative muscle biopsies for electron microscopy were taken, each segment was stained in 1% TTC, and the total area of staining was measured with computerized planimetry. All control muscles stained completely with a dark red color. After 4, 6, or 8 hr of ischemia, quantitative measurements of muscle staining indicative of normal tissue were present in 98 +/- 1%, 59 +/- 5%, and 23 +/- 9% of the total muscle areas, respectively. Six hours of ischemia followed by reperfusion was associated with only 36 +/- 9% of the muscle being stained. Segmental TTC staining demonstrated that reperfusion was associated with greater injury, and less TTC staining, in the proximal portion of the gracilis muscle at the site of entry of the major arterial pedicle. The distal muscle did not demonstrate increased damage with reperfusion. It is hypothesized that protection of the distal muscle from reperfusion injury may be due to an absence of reflow farther away from the artery.     

Importance of the adaptive properties of skeletal muscle in long-term electrophrenic stimulation of the diaphragm

Clinical experience reviewed elsewhere in this issue supports the use of electrical stimulation of the diaphragm via the phrenic nerve in selected patients in whom ventilation is inadequate, intermittent or absent. This paper represents a muscle biologist's view of some of the fundamental problems posed by this technique. It reviews the long-term changes that take place in skeletal muscles in response to chronic stimulation, and it indicates how these may be exploited in order to make electrophrenic respiration more effective and more acceptable both to the patient and to the clinical support team.     

Alteration in the force and fatigability of skeletal muscle in quadriplegic humans following exercise induced by chronic electrical stimulation.

The paralyzed forearm finger flexor muscles of 10 quadriplegic subjects were exercised via electrical stimulation to determine changes in the contractile force and fatigability of the muscle that could be externally induced. The force of contraction initially produced by most muscles was less than that required for functional activity. Following exercise, the strength of all muscles was increased above the level for functional use. In general, no correlation was noted between the amount of exercise and the force change. Two subjects had high contraction forces after prolonged periods before stimulation began, and 4 subjects who were followed after the stimulation program maintained near the contractile force achieved at the end of the program in the absence of stimulation. Fatigue of the muscle during the course of the exercise program was increased to above that recorded initially, although this was more variable and sometimes dropped to less than that recorded initially. Generally, no correlation was demonstrated between usage and fatigue. It is concluded that exercise induced by electrical stimulation alters the cantractile properties of the muscle toward a state usable for functional, tonic activation.     

The cut intramuscular nerve affects the recovery in the lacerated skeletal muscle.

The recovery of lacerated skeletal muscles are said to be slow and incomplete. Often the intramuscular (IM-) nerve is concomitantly cut, but never repaired. We questioned whether the IM-nerve should also be reanastamosed before repairing the skeletal muscle. Before answering this, it was necessary to know if the cut IM nerve would have an effect on the recovery of the segment of muscle distal to the level of the laceration. This study investigates the recovery of lacerated muscles after repair, and compares a complete muscle laceration where the main IM-nerve was concomitantly cut and an incomplete muscle laceration where the IM-nerve was preserved intact. The medial gastrocnemius (MG) of the adult male New Zealand White rabbit was used, with the contralateral muscle as a sham control. The laceration was at the proximal quarter of the muscle, distal to the entry point of the nerve branch from the tibial nerve into the muscle belly. Twenty-eight weeks post-repair, the lacerated MG with the IM-nerve intact showed improved muscle wet weight, near normal morphology and contractile properties, and return of muscle fiber type mix and size. The repaired lacerated MG with their IM-nerve concomitantly cut demonstrated loss of muscle wet weight, obvious fibrosis, mononuclear proliferation with fatty infiltration, increase in type-1 fibers and muscle fiber atrophy in the distal portion. We postulate that it might be important to repair the intramuscular nerve branch by microanastomosis when repairing a vital skeletal muscle that is lacerated.     

Quantitation of postischemic skeletal muscle necrosis: histochemical and radioisotope techniques

Skeletal muscle necrosis will result from prolonged periods of ischemia. The purpose of this study was to develop a method to estimate the extent of necrosis using nitroblue tetrazolium staining and technetium scanning. The bilateral canine gracilis muscle preparation with total vascular isolation was exposed to 4 hr of complete normothermic ischemia followed by reperfusion. After 45 hr of reperfusion 99mTc pyrophosphate (PYP) was injected and 3 hr later the muscles were harvested, cut into six slices, and stained with nitroblue tetrazolium. Biopsies were taken from tetrazolium-positive and -negative areas for electron microscopy to confirm the ability of the stain to distinguish viable from necrotic muscle. Computerized planimetry of the staining pattern was used to estimate the extent of necrosis as a percentage of the total muscle. Electron microscopy confirmed the validity of nitroblue tetrazolium to discriminate between viable and necrotic skeletal muscle in this experimental model. After 4 hr of ischemia the percentage necrosis was 30.2 +/- 6.1% (mean +/- SEM, n = 12), there was no difference in the extent of necrosis in left vs right paired muscles, using tetrazolium staining or technetium PYP uptake. There was a statistically significant correlation between the percentage necrosis and the density of 99mTc PYP uptake per muscle (r = 0.83, P less than 0.001) and per slice (r = 0.94, P less than 0.001). This study demonstrates the ability of tetrazolium staining to accurately differentiate between viable and necrotic skeletal muscle and provides a reproducible method for estimating the extent of necrosis in the gracilis muscle model.     

Functional electrical stimulation after spinal cord injury.

This article reviews work mainly from my own laboratory on the effects of electrical stimulation for therapy and function following spinal cord injury. One to two hours per day of intermittent stimulation can increase muscle strength and endurance and also reverse some of the osteoporosis in bones that are stressed by the stimulation. Stimulation during walking can also be used to improve speed and other parameters of the gait. Surface stimulation systems with 1-4 channels of stimulation were used in a multicenter study. Initial increases of almost 20% in walking speed were seen and overall increases of nearly 50% in subjects who continued to receive stimulation for a year on average. Some changes were due to improved strength and coordination with stimulation and additional walking, but a specific effect of stimulation persisted throughout the trial. Improved devices will soon be available commercially that were developed on the basis of feedback from users.     

Electrophysiological studies of long-term electrical stimulation of the cerebellum in monkeys.

Six rhesus monkeys were stimulated on the paravermal cortex for 205 hours (18 days) with different charge densities in order to determine the electrode performance and neural damage that may result from long-term cerebellar stimulation comparable to that being used in man. The electrode-tissue interface was relatively stable and no neural damage was found when the charge/phase (0.5 muC/ph) or charge density (7.4 muC/sq cm/ph) was very low. At all higher charge levels tested (2.4, 4.8, 10, and 22 muC/ph), changes in the electrode-tissue interface, meningeal encapsulation, and neural damage were directly related to the charge density delivered. Unstimulated electrodes on the opposite paravermal cortex exhibited mild tissue reactivity and cell damage, probably due to mechanical compression of the molecular layer and pial vessels. Motor cortex field potentials could be evoked by charges as low as 0.1 muC/ph delivered to paravermal cortex; for a given charge/phase longer pulses were more effective than short pulses. After neural damage resulting from 205 hours of 4.8 muC pulses at 10 per second (total charge 14.76 C), the threshold for the motor cortex evoked potential increased by a factor of four or more. With the charge held constant to different-sized electrodes placed bilaterally in the same monkey, damage was greater under the smaller electtrode. This finding suggests that the charge density to cerebellar cortex must be controlled to avoid neural damage.     

Tissue reactions to long-term electrical stimulation of the cerebellum in monkeys.

Light and electron microscopic analyses were carried out on the stimulated and unstimulated paravermal cortices of six rhesus monkeys that had electrodes implanted on their cerebella for 2 months. The electrodes and the stimulation regime (10 p.p.s.: 8 min on, 8 min off) were similar to those used to stimulate the human cerebellum for treatment of certain neurological disorders. Mere presence of the electrode array in the posterior fossa for 2 months resulted in some meningeal thickening, attenuation of the molecular layer, and loss of Purkinje cells immediately beneath the electrode array. There was no evidence of scarring. After 205 hours of stimulation (7.35 X 10(6) pulses) over 18 days, a charge of 0.5 muC/ph or estimated charge density of 7.4 muC/sq cm/ph resulted in no damage to the cerebellum attributable to electrical stimulation per se. Such a charge/phase is about five times the threshold for evocation of cerebellar efferent activity, and might be considered "safe" for stimulation of human cerebellum. Charge density/phase and charge/phase were directly related to increased cerebellar injury in the six other cerebellar cortices stimulated. Leptomeningeal thickening increased with increased charge density. Injury included severe molecular layer attenuation, ongoing destruction of Purkinje cells, gliosis, ongoing degeneration of myelinated axons, collagen intrusion, and increased levels of local polysaccharides. In all cases, even with damage that destroyed all conducting elements beneath the electrodes, there was no damage further than 1 to 2 mm from the edges of the electrode arrays.     

Blink reflex recovery after electrical stimulation of the reinnervated orbicularis oculi muscle in dogs

The paralytic lagophthalmos following palpebral nerve neurotmesis and consequent peripheral denervation of the orbicularis oculi muscle is often associated with harmful effects on the exposed cornea. This study investigated how daily electrical stimulation affects the blink reflex recovery of this muscle after its reinnervation. Six dogs underwent unilateral facial nerve neurotmesis with immediate epineurial repair of the palpebral nerve. Three dogs were randomly chosen to receive electrical stimulation of the reinnervated orbicularis oculi muscles for 75 days. The remaining 3 dogs were controls (nonstimulated muscles). During the study, the reinnervated orbicularis oculi muscle electrophysiology and blink reflex recovery were investigated. The Student's t test was used for statistical analysis. The results can be summarized as follows: (1) between 30 and 50 days, the minimum mean stimulus intensities evoking complete up-per palpebral closure of the stimulated muscles were significantly lower than those of the nonstimulated muscles (p less than 0.01) and (2) the stimulated muscles recovered complete closure of the interpalpebral fissure (blink reflex) at 49.6 days, significantly earlier (p less than 0.01) than the nonstimulated muscles (72.6 days). It is concluded that daily electrical stimulation of the orbicularis oculi muscles, if started immediately after epineurial repair of the palpebral nerve neurotmesis, promotes a faster blink reflex recovery in the dog model.     

A clinically applicable method for long-term salvage of postischemic skeletal muscle.

The clinical significance and applicability of interventions aimed at reducing reperfusion injury in postischemic skeletal muscle remain unproven, since long-term muscle salvage has not been demonstrated by most treatment protocols that attenuate early reperfusion injury. We have shown that reperfusion of ischemic skeletal muscle results in an early and prolonged sequestration of white blood cells and activation of the alternative complement cascade. The purpose of this study was to determine if 40 minutes of reperfusion with blood depleted of white blood cells and complement proteins, followed by 2 days of normal perfusion, would reduce muscle necrosis after 5 hours of ischemia. The isolated paired canine gracilis muscle model was used. The treatment muscle was initially reperfused with arterial blood that had been spun, washed, passed through a leukocyte removal filter, and resuspended in hydroxyethyl starch (greater than 99.9% removal of white blood cells and the complement proteins factor B and C4). The contralateral control muscle was subjected to unaltered reperfusion. Blood flow (ml/min/100 gm) was measured by timed collection of gracilis venous blood. Myeloperoxidase activity (absorbance at 655 nm/min/mg tissue protein) in muscle biopsies was used to monitor white blood cell sequestration. After 48 hours of reperfusion in vivo, necrosis was quantified by nitroblue tetrazolium staining. Initial reperfusion with white blood cell and complement depleted blood significantly reduced muscle necrosis (53% +/- 3% vs 29% +/- 8%, p less than 0.0025, paired t test). Early blood flow was improved, (p = 0.0025, repeated measure-ANOVA), but subsequent white blood cell sequestration was not altered (p = 0.33, repeated measure-ANOVA). This suggests that a significant amount of white blood cell mediated injury occurs during the first 40 minutes of reperfusion. Preventing early complement activation and white blood cell mediated reperfusion injury is an intervention that is feasible during surgery and may result in clinically significant salvage of postischemic skeletal muscle.     

Short-term transcutaneous electrical nerve stimulation after cardiac surgery: effect on pain, pulmonary function and electrical muscle activity

This study aimed to evaluate the effectiveness of transcutaneous electrical nerve stimulation (TENS) for treatment of postoperative pain in patients who underwent cardiac surgery. In addition, we sought to determine whether TENS would be related to improved pulmonary function and muscle electrical activity in this patient population. Forty-five patients, 32 males and 13 females, aged 41-74 years were randomly allocated to receive TENS (n=23) or sham treatment (n=22) during 4 h on the third postoperative day. A 0-10 visual analogic scale was used to assess pain; lung function was evaluated by spirometry and surface electromyography (n=10 in each group) was used to quantify electrically-induced muscle activity (trapezius and pectoralis major). TENS was associated with significant reductions on spontaneous and cough-induced postoperative pain as compared to sham (P<0.05). There was also improvement in chest wall-pulmonary mechanics after TENS with proportional increases in tidal volume and vital capacity (P<0.05). In addition, electrical activity of both muscle groups was enhanced after TENS, but not post sham (P<0.05). TENS is a valuable strategy to alleviate postoperative pain following cardiac surgery with positive effects on pulmonary ventilatory function and electrical activity of thoracic and girdle muscles.