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Clinical applications of electrical stimulation for individuals with spinal cord injury.


ABSTRACT

Electrical stimulation (ES) has been used to restore musculoskeletal musculoskeletal /mus·cu·lo·skel·e·tal/ (-skel´e-t'l) pertaining to or comprising the skeleton and muscles.

mus·cu·lo·skel·e·tal
adj.
Relating to or involving the muscles and the skeleton.
, sensory and anatomical functions following spinal cord injury Spinal Cord Injury Definition

Spinal cord injury is damage to the spinal cord that causes loss of sensation and motor control.
Description

Approximately 10,000 new spinal cord injuries (SCIs) occur each year in the United States.
 (SCI (Scalable Coherent Interface) An IEEE standard for a high-speed bus that uses wire or fiber-optic cable. It can transfer data up to 1GBytes/sec.

(hardware) SCI - 1. Scalable Coherent Interface.

2. UART.
). The reported benefits of ES in SCI rehabilitation include assisting respiration, improving muscle strength and endurance, improving cardiovascular fitness, increasing lower limb circulation, improving bowel and bladder function, assisting in wound management, and preventing osteoporosis. However due to divisive reports on its effectiveness, ES is often overshadowed by skepticism and clinicians usually choose alternative treatments that are simpler and less expensive. Therefore, ES treatment outcomes and applications need to be more evident for the healthcare payers, providers, and clients to make informed decision when utilizing ES in rehabilitation of SCI patients.

Overall Article Objective: To critically summarize the literature in regard to the clinical application of ES and its impact on improving functional and rehabilitation outcomes of person with SCI. This paper presents the advantages and disadvantages of many ES systems and discusses possible opportunities and challenges for the future use of ES technology for individuals with SCI.

Key Words: Spinal cord injury; Electrical stimulation; Rehabilitation.

INTRODUCTION

Following spinal cord injury (SCI), loss of voluntary muscle control as well as sensory, autonomic, reflexes and visceral organ changes limit mobility. These changes may lead to muscle atrophy (57), bone demineralization demineralization /de·min·er·al·iza·tion/ (de-min?er-al-i-za´shun) excessive elimination of mineral or organic salts from tissues of the body.

de·min·er·al·i·za·tion
n.
 (134), elevated risk of abnormal thrombus thrombus /throm·bus/ (throm´bus) pl. throm´bi   a stationary blood clot along the wall of a blood vessel, frequently causing vascular obstruction.  formation (89), decubitus ulcer formation (5), urinary tract infection urinary tract infection (UTI),
n infection in one or more of the structures that make up the urinary system. Occurs more often in women and is most commonly caused by bacteria.
 (UTI UTI urinary tract infection.

UTI
abbr.
urinary tract infection



UTI

urinary tract infection.

UTI Urinary tract infection, see there
) (16, 31), increased incidence of heart disease (110), and a general loss of cardiopulmonary fitness (49). These complications often require more hospitalizations, resulting in periods of inactivity and compromised function, decreasing the quality of life for these individuals (4).

Application of electrical stimulation during the rehabilitation of persons with SCI has been to either for treatment of weaknesses (physiological or physical) that stems from SCI (therapeutic electrical stimulation or TES TES Times Educational Supplement (publication)
TES The Elder Scrolls (series of computer games)
TES Thermal Emission Spectrometer
TES Teaching Every Student
TES Thermal Energy Storage
)(2) or it may be used to induce function such as walking or cycling (functional electrical stimulation FES, or neuromuscular electrical stimulation NMES NMES Neuromuscular Electrical Stimulation
NMES National Medical Expenditure Survey
) (116). Often times, FES, NMES and TES are used interchangeably in the clinics and may cause some confusion for healthcare provides caregivers, and insurance companies. Therefore, this paper refrains from using the terms FES, TES, on NMES as separate entities, but rather presents them under the general umbrella of ES. This review summarizes the mechanisms of ES action, types of stimulation options, state of research in ES clinical application, clarifies ES methodologies, discusses gaps and inconsistencies in the literature, and presents challenges and opportunities for future application of ES technology for rehabilitation of individuals with SCI.

MECHANISMS OF ES ACTION

The primary action of ES is to stimulate intact motor and sensory neurons of the peripheral nervous system peripheral nervous system: see nervous system. . This action leads to direct and indirect physiological changes to underlying tissue which can be thermal, chemical, and/or physical in nature (2). Thermal changes occur due to the combined effects of ES duration, impedance, and current produced (2). This refers to Joule's Law that quantifies heat generation in an electrical resistor. Physical and chemical changes also occur as a direct consequence of ES where excitation of neurons following electrical stimulation causes increased mobility of [Na.sup.+] and [K.sup.+] ions across semi-permeable cell membranes (2).

In contrast to muscles whose activation is controlled by the central nervous system, in an electrically stimulated muscle contraction is controlled by the electrically stimulated motor neurons and motor units. These motor neurons and motor units excite synchronously with preferential activation of motor units in closer proximity to the stimulation source (116). Thus limited activation occurs for motor units further away from the stimulation source. This may lead to rapid fatigue and the need for higher stimulation output in order to maintain a strong muscle contraction. ES also provides "selective" activation of larger diameter motor neurons, as these are easier to stimulate secondary to their lower threshold of excitation (68, 96, 131). This is opposite to normal muscle fiber recruitment, which targets small diameter fibers first (61). Muscles having a higher proportion of type 2 fibers tend to fatigue more quickly than smaller diameter fibers (generally composed of greater numbers of type I fibers). Reversal of normal fiber recruitment and synchronous activation of motor units result in less efficient and less selective contraction compared with normal physiology, which leads to faster muscle fatigue (67, 96). Furthermore, the effectiveness of ES action in eliciting a smooth muscle contraction depends largely on the type of electrical simulation, selection of appropriate ES parameters, electrodes, and type of control system. For instance, it is possible to reduce onset of muscle fatigue by using lower frequencies and amplitudes, adjusting duty cycle, changing electrode size and position, and stimulating different motor points of a muscle group. Since this paper focuses on the clinical application of ES, the details pertaining to ES characteristics such as waveforms, frequency, and duty cycle will not be discussed.

CLINICAL APPLICATIONS OF ES

Applications of ES technology for individuals with SCI may provide a wide array of therapeutic benefits. Table 1 provides a comprehensive summary of these applications along with methods, advantages, disadvantages, and alternative treatments. More detailed discussion of these applications is discussed below.

Assisted Breathing and Coughing

Respiratory complications are a major cause of morbidity and mortality Morbidity and Mortality can refer to:
  • Morbidity & Mortality, a term used in medicine
  • Morbidity and Mortality Weekly Report, a medical publication
See also
  • Morbidity, a medical term
  • Mortality, a medical term
 in acute and chronic cervical SCI and most prevalent in those individuals with high-level tetraplegia tetraplegia /tet·ra·ple·gia/ (-ple´jah) quadriplegia.

tet·ra·ple·gia
n.
See quadriplegia.



tetraplegia

paralysis of all four extremities; quadriplegia.
 who have problems with independent breathing and voluntary cough (113). The National SCI Statistical Center reported that approximately 10% of all persons with complete tetraplegia require re-hospitalization for pneumonia or atelectasis atelectasis
 or lung collapse

Lack of expansion of pulmonary alveoli (see pulmonary alveolus). With a large-enough collapsed area, the victim stops breathing.
 (17). Jaeger jaeger (yā`gər), common name for several members of the family Stercorariidae, member of a family of hawklike sea birds closely related to the gull and the tern. The skua is also a member of this family.  et al. (69) found a positive correlation between peak expiratory flow peak expiratory flow
n.
The maximum flow of air at the outset of forced expiration, which is reduced in proportion to the severity of airway obstruction, as in asthma.
 and motor level (r = 0.46) in 200 persons with SCI, suggesting that individuals with high cervical injuries may have complete or partial loss of voluntary respiration and coughing secondary to paralysis to the diaphragm, abdominal, and intercostal muscles. Without volitional control of muscles, these individuals require some form of assisted breathing and coughing. Many ES approaches have been use to improve the ventilation in people with SCI, especially those with tetraplegia some of which are discussed below.

1) Phrenic nerve stimulation using ES to induce contraction of the diaphragm has been shown to improve ventilation for individuals with high tetraplegia (24, 92). By stimulating the phrenic nerve, the diaphragm muscle contracts, and inspiration strength increases. In some patients this may eliminate the need for a ventilator (22). This approach is more invasive than surface stimulation since patients are thoracotomized and electrodes are placed directly on the nerve. Complications associated with this procedure include risks associated with surgery, injury to the phrenic nerve, cost, and inpatient hospital stay.

2) Intramuscular intramuscular /in·tra·mus·cu·lar/ (-mus´ku-ler) within the muscular substance.

in·tra·mus·cu·lar
adj. Abbr. IM
Within a muscle.
 diaphragm pacing has been investigated most recently (23, 25, 30). Intramuscular electrodes are placed directly on the diaphragm in close proximity to the phrenic nerve. This method is less invasive, reducing the risk of phrenic nerve damage, and can also be done outpatient making it less costly (50, 51).

3) Intercostals muscles stimulation is performed by placing a single electrode on the ventral epidural epidural /epi·du·ral/ (-dur´il) situated upon or outside the dura mater.

ep·i·du·ral
adj.
Located on or over the dura mater.

n.
 surface of the SCI at T2 level. This procedure resulted in significant increase in inspiratory in·spi·ra·to·ry
adj.
Of, relating to, or used for the drawing in of air.



inspiratory

pertaining to or used in the inspiration of air into the lungs.
 volume, however, it was sustained for only a modest amount of time (less than 20 minutes) (26). However, successful long-term ventilation support using ES has not been reported.

4) People with SCI may also need chest physical therapy Chest Physical Therapy Definition

Chest physical therapy is the term for a group of treatments designed to improve respiratory efficiency, promote expansion of the lungs, strengthen respiratory muscles, and eliminate secretions from the respiratory
 (e.g., quad cough), which is generally prescribed to assist in productive cough and prevent respiratory infections. Unfortunately many persons with SCI are unable to do this form of coughing independently. Linder (83) found that surface ES of abdominal wall muscles augments productive coughing by increasing the maximum expiratory ex·pi·ra·to·ry
adj.
Of, relating to, or involving the expiration of air from the lungs.



expiratory

relating to or employed in the expiration of air from the lungs.
 pressure (MEP MEP maximum expiratory pressure.
MEP,
n muscle energy procedure; diagnostic and therapeutic technique. Pulsed muscle energy techniques (MET) and integrated neuromuscular inhibition technique (INIT) are two examples.
) in high cervical SCI subjects. The results suggest that by increasing MEP, productive coughs may be enhanced. Taylor et al. (130) compared the effects of surface ES to manual assisted cough in a ventilator-dependent individual with tetraplegia. Measurements of peak expiratory flow were significantly different between the two methods; 275 liters per minute (manual cough) to 425 liters per minute (ES), suggesting that ES could be an effective means to assist in productive coughing.

Reaching/Hand Grasping

For many individuals with high-level SCI (i.e., tetraplegia), performing reaching and hand grasping tasks independently is limited. For instance, a person with tetraplegia has difficulty with most, if not all, activities of daily living (ADL). ADLs require motor control of the trunk and upper extremities for everyday tasks such as dressing, body washing, hair brushing, handwriting, and holding a phone. It is clear that improving upper extremity function and movement control would be extremely beneficial. Within the last 10 years, researchers have found reaching and hand grasping using ES in persons with tetraplegia increases upper extremity function, decreases time and effort required to perform ADLs, increases grasp force, decreases reliance on orthoses, and increases user's self-esteem and independence (94, 126, 141).

The Freehand See Macromedia FreeHand.  System (56) was the first FDA-approved ES neuroprosthetic system to restore hand grasp function to individuals with C5 and C6 tetraplegia. Implanted and external components of the Freehand System include an extensive electrode system connected to selected forearm and hand muscles, and a shoulder joint transducer for sensory feedback (120). Hand grasping is possible through stimulation of the extrinsic hand muscles (i.e., extensor extensor /ex·ten·sor/ (-ser) [L.]
1. causing extension.

2. a muscle that extends a joint.


ex·ten·sor
n.
A muscle that extends or straightens a limb or body part.
 and flexor flexor /flex·or/ (flek´ser)
1. causing flexion.

2. a muscle that flexes a joint.


flexor retina´culum  see entries under retinaculum.
 pollicis longi muscles, extensor digitorum comminis, flexor digitorum profundus, and abductor and adductor adductor /ad·duc·tor/ (ah-duk´tor) [L.] that which adducts, as the adductor muscle.

ad·duc·tor
n.
 pollicis brevi) (70). Generally, using an external microcontroller, stimulation is transmitted via a coupling coil to the implanted stimulator. By assisting in lateral and palmar hand grasping, the Freehand System has been shown to: 1) provides overall increase in functional independence; 2) decrease the need for caregiver assistance; 3) decrease the time and effort required to perform ADLs; 4) increase the range of motion (ROM); 5) increase the grasp force; 6) improved grasp-release test, and 7) decreased reliance on orthoses (93, 126). This technology was removed from the market in 2001 and now only available at the FES Center in Cleveland, OH.

Transfers/Standing and Ambulation am·bu·late  
intr.v. am·bu·lat·ed, am·bu·lat·ing, am·bu·lates
To walk from place to place; move about.



[Latin ambul
 

Electrical stimulation technology offers the opportunity for functional use of the lower extremities in individuals having complete or incomplete SCI. The desirable outcomes of these ES-induced applications are to achieve safe, reliable ES control during transfers, standing, and ambulation, minimizing energy demands, decreasing overall expenses, and making function cosmetically appealing (12, 19, 44, 53, 55, 64-66, 73, 75, 85, 122, 132).

In individuals with tetraplegia who are dependent on caregivers to assist them with proper trunk and limb placement, appropriate ES to leg and trunk muscles may be used to facilitate the transfer process and reduce physical demands of the caregiver. Triolo and colleagues (132) studied the use of ES and standing transfers on 24 individuals with low cervical SCI. Electrical stimulation was administered percutaneously to provide stimulation to selected lower extremity muscles using a stand-to-sit switch controller. The researchers concluded that application of ES may provide an effective alternative to assisted stand-pivot and sliding board transfers.

Electrical stimulation combined with an assistive device such as a walker, parallel bars, or orthoses is often referred to as a hybrid system. Therapeutic benefits of hybrid systems have been reported to include: 1) increased strength of lower extremities; 2) increased bulk of muscles; 3) improved muscular and cardiovascular endurance; 4) independent standing and ambulation; 5) improved self-esteem; and 6) a perception of enhanced well-being (18, 58, 67). Users that benefit most from these hybrid systems for ambulation have reported to have the following characteristics: 1) SCI at or below 7th cervical wheel rolling walker (54, 55). The controller operates within an open-loop to provide ES to the peroneal peroneal /per·o·ne·al/ (-ne´al) pertaining to the fibula or to the lateral aspect of the leg; fibular.

per·o·ne·al
adj.
Of or relating to the fibula or to the outer portion of the leg.
 nerves as well as the quadriceps, glutei, and paraspinals muscles. The 6-channel system is noninvasive and transmits ES with a rate of 24 pulses per second, intensity of 300 milliamps, and pulse duration of 120-150 microseconds. The controller is secured around the patient's waist, and typically is used with bilateral ankle-foot orthoses for ankle stability. Follow-up studies suggest ambulation with the Parastep System is beneficial for individuals with thoracolumbar thoracolumbar /tho·ra·co·lum·bar/ (-lum´bar) pertaining to thoracic and lumbar vertebrae.

tho·ra·co·lum·bar
adj.
1. Of or relating to the thoracic and lumbar parts of the spinal column.
 SCI, but less effective for individuals with injury levels above fourth thoracic vertebrae (58, 67, 74, 97). Of 31 patients who completed the vertebra vertebra /ver·te·bra/ (ver´te-brah) pl. ver´tebrae   [L.] any of the 33 bones of the vertebral (spinal) column, comprising 7 cervical, 12 thoracic, 5 lumbar, 5 sacral, and 4 coccygeal vertebrae . , 2) good physical and mental health, 3) little to no injury to peripheral nervous system, 4) high degree of lower extremity and trunk range of motion, 5) at least 14 years of age, 6) motivation, and 7) body awareness and balance control with upper extremities and an assistive device (loftstrand crutches, parallel bars, walker) (18, 58, 67). There are various combinations of hybrid systems that include surface, percutaneous, or implanted electrodes (2-48 channels) with bracing (i.e., Louisiana State University--Reciprocating Gait Orthoses (LSURGO) (27)) and customized orthoses (3). Marsolais and colleagues (84, 85) implanted intramuscular electrodes in 9 lower extremity muscles in persons with SCI to assist them in ambulation using a rolling walker. They reported that during ES walking, energy consumption was near 75% of maximal aerobic power and energy costs were similar to long-leg brace ambulation at speeds between 0.4 and 0.6 meters per second. Reciprocal gait orthoses in conjunction with ES to the quadriceps muscles has been shown to improve ambulation speed while reducing total energy expenditure by as much as 16% (63).

Another type of hybrid system used for assisted-ambulation is the ParaWalker System (Orthotic orthotic /or·thot·ic/ (or-thot´ik) serving to protect or to restore or improve function; pertaining to the use or application of an orthosis.

or·thot·ic
adj.
Of or relating to orthotics.
 Research & Locomotion Assessment Unit, Oswestry, England) (123). This system uses surface ES along with a hip-knee-ankle-foot orthoses but requires 3.5 times more energy consumption than that of the user's resting level (99). Improvements to the ParaWalker System where reported by Nene Nene (nēn, nĕn) or Nen (nĕn), river, c.90 mi (140 km) long, rising in the Northampton Uplands, central England, and flowing NE past Northampton, Oundle, Peterborough, and Wisbech to the Wash.  et al. (98) who found that energy cost reduced up to 8% when adding stimulation to the gluteal muscles on the same side of weight-bearing as compared to ambulation with the ParaWalker alone.

The Parastep System (Sigmedics Inc., Northfield IL, USA) is an FDA-approved hybrid system that uses a battery-powered microprocessor to enable independent standing and ambulation with a front-training program using the Parastep System, 92% stood and took steps, and 34% eventually ambulated independently (18). Approximately 82% continued to use the system regularly at 6 month follow-up (18). In average subjects walked for approximately 115 meters at 5 meters/minute without rest, and completed 12 weeks of exercise at 3 times per week while using the Parastep System (74).

Limitations of ES for the above applications include 1) electrode failure; 2) ES-induced muscle fatigue; 3) excessive energy expenditure; 4) ES-induced autonomic dysreflexia; 5) spasticity spasticity /spas·tic·i·ty/ (spas-tis´i-te) the state of being spastic; see spastic (2).

spas·tic·i·ty
n.
1. A spastic state or condition.

2. Spastic paralysis.
; and 6) cumbersome electrical hardware with an inefficient user-machine interface (85). Reasons for patients discontinuing use of these systems include 1) the time required to don and doff the system; 2) difficulties with operation of the system; and 3) problems incorporating use of the system into the home environment and living situation (75). These systems are less functional compared with wheelchair mobility, as the speed of ES assisted ambulation is slow, typically in the range of 0.1 to 0.4 meters per second, and the time to don and doff the braces can be quite significant. In addition, the average comfortable walking distance with these devices varies considerably between users and may be limited by the rapid onset of muscle fatigue and high energy cost.

It should be noted that prior to using an ES system for standing and gait, patients must undergo a training program to properly prepare them. This preparation generally addresses 1) strength and endurance training using ES to the leg muscles, 2) cardiovascular endurance training, and 3) posture and standing balance.

Bladder Function

ES is effective in improving and restoring bladder function, which reduces infections and improves continence continence /con·ti·nence/ (kon´tin-ens) the ability to control natural impulses.con´tinent

con·ti·nence
n.
1. Self-restraint; moderation.

2.
. Individuals with SCI that have difficulty with manual bladder management and who have frequent infections of the urinary tract and prone to autonomic dysreflexia are generally considered for ES bladder systems. ES bladder systems are generally applied to the pelvic nerve, spinal cord, bladder wall, or ventral sacral nerve roots (21, 115). Unfortunately, these systems are invasive with varying outcomes that depend to a significant degree on electrode location. The pelvic nerve stimulation, if placed incorrectly can cause reflexive external sphincter activity. Effective stimulation to the spinal cord requires the electrodes be implanted in the intermediolateral sacral sacral /sa·cral/ (sa´kral) pertaining to the sacrum.

sa·cral
adj.
In the region of or relating to the sacrum.


sacral,
adj pertaining to the sacrum.
 cord region; predisposing injury of the parasympathetic parasympathetic /para·sym·pa·thet·ic/ (-sim?pah-thet´ik) see under system.

par·a·sym·pa·thet·ic
adj.
Of, relating to, or affecting the parasympathetic nervous system.
 motor neurons (114). Electrical stimulation to the bladder wall requires placement of electrodes over the detrusor muscle Detrusor muscle
Bladder muscle.

Mentioned in: Urine Flow Test
, which in some individuals, the ES may cause pain, lower extremity muscle contraction, defecation defecation
 or bowel movement

Elimination of feces from the digestive tract. Peristalsis moves feces through the colon to the rectum, where they stimulate the urge to defecate.
, and erection. Ventral sacral root stimulation appears the most promising and is commonly uses for persons with SCI (114). The Finetech-Brindley Bladder System (FineTech Medical Ltd., England) stimulates the ventral sacral root to contract and relax the detrusor muscle using a sequence of ES pulse-train bursts (15). The stimulator is implanted subcutaneously and the electrodes are placed on the anterior sacral nerve roots S2-S4. A dorsal rhizotomy at S2-S5 is performed during implantation to eliminate reflex erection, ejaculation ejaculation /ejac·u·la·tion/ (e-jak?u-la´shun) forcible, sudden expulsion; especially expulsion of semen from the male urethra. , and bladder emptying. The user controls the unit externally via telemetry. This system is effective in individuals with SCI where follow-up reports show that approximately 85% of users affectively void using the system and 73% were having no incontinence issues during the day (136). Additional data regarding the clinical outcome of these systems may be found in work by Brindley et al. (14) and Vastenholt et al. (137).

Circulation

Muscle paralysis and impaired mobility contribute to reduction in blood flow and a compromise in overall circulation. Subsequently, circulatory stasis can result in the formation of blood clots that can develop in the vessels of the lower extremity. The results may eventually lead to the formation of deep vein thromboses (DVT See deep vein thrombosis. ) (100), (especially during acute and sub acute stage of recovery from SCI) a life-threatening condition. Natural muscle pumping of the lower limb muscles help prevent DVT occurrence (138).

Researchers have studied ES-induced muscle pumping action of calf muscles to determine if ES can facilitate venous blood return and prevention of DVT (34, 36, 39, 40, 42, 96). Phillip and colleagues (109) evaluated blood flow using a photoelectric Converting photons into electrons. When light is beamed onto a metal, electrons are released from its atoms. The higher the light frequency, the more electron energy released. Photonic sensors of all kinds work on this principle. They sense light and cause an electric current to flow.  plethysmography plethysmography /ple·thys·mog·ra·phy/ (ple?thiz-mog´rah-fe) the determination of changes in volume by means of a plethysmograph.

plethysmography

the determination of changes in volume by means of a plethysmograph.
 following ES-induced isometric isometric /iso·met·ric/ (-met´rik) maintaining, or pertaining to, the same measure of length; of equal dimensions.

i·so·met·ric
adj.
1.
 contraction of both lower extremities during arm ergometry in 8 SCI subjects and found reductions in venous blood pooling. Faghri et al. (42) evaluated the effects of ES of lower extremity muscles during standing on the hemodynamic response in persons with SCI and concluded that ES of the lower extremity could be used as an adjunct during standing to prevent orthostatic hypotension and circulatory hypokinesis. Merli and colleagues (88) studied prolonged ES to the tibialis tibialis /tib·i·a·lis/ (tib?e-a´lis) [L.] tibial.

tibialis

[L.] tibial.
 anterior and gastrocnemius gastrocnemius /gas·troc·ne·mi·us/ (gas?tro-ne´me-?s) (gas?trok-ne´me-us) see under muscle.

gas·troc·ne·mi·us
n. pl.
 muscles, in combination with low-dose heparin. Patients with acute SCI showed a significant decrease in the incidence of DVT in comparison with a group receiving a low-dose of the anti-coagulant alone. The effects were suggested to be in part to the effects of ES in increasing plasma fibrinolytic activity.

Strength/Endurance Training

The successful use of ES with various applications requires both muscle strength and endurance. Stein (125) reported increases in endurance and decreases in fatigue of the stimulated muscle to levels found in able-bodied control subjects. Positive changes in the muscle at the level of the muscle fiber and even at the intracellular level have been reported (29). Martin et al. (86) indicated that continuous low frequency ES of skeletal muscles results in transformation of the muscle fiber from type II fibers to fibers with type I characteristics. The implications of this change are significant in that the fast-twitch fibers are converted to slow-twitch, thus becoming more resistant to fatigue. The proportion of type I muscle fibers increased from 14% to 25% following continuous low frequency (20Hz) ES of the tibialis anterior in patients with SCI (86). According to Ragnarsson (111), ES to lower extremity muscles of individuals with chronic SCI increases thigh circumference, improves muscle strength and endurance, and increases quadriceps muscle protein synthesis rates. Petrofsky (106) documented improvements in muscle strength in a group of SCI individuals following slow ES-induced isokinetic isokinetic /iso·ki·net·ic/ (-ki-net´ik) maintaining constant torque or tension as muscles shorten or lengthen; see isokinetic exercise, under exercise.  weight lifting 3 times per week at 50% of a muscle's maximal strength.

Reports found significant improvements in bulk and muscle strength following approximately 3 months of ES-induced knee extension exercises (33, 46, 102, 103, 127). Exercise training using ES-induced leg cycle ergometry (ES-LCE) markedly improves muscle size and strength (112). Faghri and colleagues (37) reported that after 12 weeks of training with ES-LCE, power output increased from 6 to 30 W, and exercise tolerance increased from a few minutes to 30 minutes time.

Using computer tomography, Pacy et al. (101) recorded increases in mid-thigh muscle area by 27% after 10 weeks of ES knee exercise; an increase that coincided with a significantly higher quadriceps muscle protein synthesis rate. Hjeltnes et al. (62) measured body composition changes following ES-induced leg cycling exercise in 5 individuals with tetraplegia. Using dual-energy X-ray absorptiometry dual-energy x-ray absorptiometry,
n diagnostic test used to determine bone density and to diagnose and monitor osteoporosis.
, they noted increased lean body mass, and decreased whole body fat content following 2 months of exercise. They also reported increased cross-sectional area of the quadriceps, hamstring, and gluteal muscles after the training. In addition, Scremin et al. (119) found increased cross-sectional areas of thigh muscles following a multi-phase ESLCE exercise program. Using computer tomography, they recorded a 31% increase in cross-sectional area for quadriceps and a 26% increase for hamstrings, in 13 healthy males with complete SCI. They also demonstrated that increased muscle strength was associated with increased muscle bulk. Other studies reported similar findings with ES-induced strength training programs (33, 118).

Cardiovascular Fitness

Researchers found that ES-induced exercise promotes peripheral and central circulation (33) and elevates metabolic and cardiopulmonary responses (46, 47) to a magnitude exceeding those obtained by traditional arm exercises (45). Mohr and coworkers (90) investigated the effects of ES-LCE applications on 10 SCI individuals. Subjects were trained for 1 year between two and three times a week, 30 minutes on each occasion. After training, all subjects were able to perform 30 minutes of continuous training, and maximal oxygen uptake (V[O.sub.2]) uptake increased significantly from 1.20 [+ or -] 0.08 liters per minute to 1.43 [+ or -] 0.09 liters per minute. It was concluded that inactivity-associated changes in exercise performance capacity and in skeletal muscle, are reversible, even up to over 20 years after an initial SCI. It follows that electrically induced exercise training of the paralyzed limbs is an effective rehabilitation tool that should be offered to SCI individuals in the future. Hjeltnes and colleagues, (62) also found that levels of V[O.sub.2] during a cycling session increased 70% after 8 weeks of training.

Efforts to improve cardiovascular benefits from ES-induced leg cycle ergometry exercise are ongoing. The original ES-induced leg cycle ergometry system was based on work done by Petrofsky (105). Petrofsky developed closed-loop controls to provide timed ES to the quadriceps, gluteus maximus, and hamstring muscles during stationary leg cycling (105). The onset and offset of ES to these muscles were based on previous electromyography electromyography

Process of graphically recording the electrical activity of muscle, which normally generates an electric current only when contracting or when its nerve is stimulated.
 studies involving upright leg cycling (103-108). Rodgers et al. (117) studied the effects of stimulation to the lower leg musculature musculature /mus·cu·la·ture/ (mus´kul-ah-cher) the muscular apparatus of the body or of a part.

mus·cu·la·ture
n.
The arrangement of the muscles in a part or in the body as a whole.
 (i.e., tibialis anterior and gastrocnemius) and reported that the added muscles produced higher V[O.sub.2] when cycling without resistance (less efficient with higher V[O.sub.2] with same power output), suggesting that extra metabolic stress may be beneficial for aerobic/cardiovascular exercise. More recently, Trumbower et al. (133) found that changes in ES sequencing may be necessary to improve pedaling effectiveness and increase the number of individuals who may benefit from this exercise system.

Osteoporosis Management

Electrical stimulation has been studied for the management of osteoporosis in persons with SCI. A paucity of evidence supports the effects of ES on the skeletal system. Moreover, the literature reports that its clinical use as a modality to reverse bone loss is equivocal. Studies that support and refute the application for osteoporosis management are presented.

Loss of bone mineral density bone mineral density
n.
See bone density.


bone mineral density A measurement of bone mass, expressed as the amount of mineral–in grams divided by the area scanned in cm2. See Bone densitometry.
 (BMD BMD

In currencies, this is the abbreviation for the Bermudian Dollar.

Notes:
The currency market, also known as the Foreign Exchange market, is the largest financial market in the world, with a daily average volume of over US $1 trillion.
) in paralyzed limbs is well documented (72, 128). Decomposition of trabecular and cortical bone minerals and matrix matter occurs following SCI, increasing susceptibility to fractures (76). The greatest loss of BMD occurs within the unloaded paralyzed limbs.(143) Therefore, it is not surprising to find most frequent fractures occurring within the lower extremities(139) with rates as high as 39% 15 years post injury (17, 87). Approximately 25% of all SCI individuals are at risk of fracture (17).

It is believed that prevention of muscle atrophy and increasing muscle strength through ES-induced contraction may contribute to higher levels of stress on the bone and possible reversal of bone loss following SCI. An early study by Doyle et al. (28) reported a strong positive relation between muscle mass and BMD. It is thought by many that this association may hold for ES-induced strength training. Unfortunately, there are no prevailing experimental findings that application of ES has a positive impact on the skeletal system.

Few researchers have documented positive changes in BMD following ES. Belanger and colleagues (7) reported reversal of osteopenia in the proximal tibia tibia: see leg.  and distal femur following daily ES-assisted isokinetic exercise of the quadriceps for six months. Bloomfield (9) found an increase in BMD of the distal femur, but only at higher loads of ES-LCE exercise. Levels of serum osteocalcin, which is used as an indicator of bone resorption, increased 10% following 6 months of ES-LCE training (91).

Contrary to these studies, Leeds et al. (77) reported no changes in bone density at the femoral femoral /fem·o·ral/ (fem´or-al) pertaining to the femur or to the thigh.

fem·o·ral
adj.
Of or relating to the femur or thigh.
 neck, trochanter trochanter /tro·chan·ter/ (tro-kan´ter) a broad, flat process on the femur, at the upper end of its lateral surface (greater t.), or a short conical process on the posterior border of the base of its neck (lesser t.) . , or Ward's triangle following six months of ES-induced leg cycling in tetraplegics. Rodgers and colleagues (118) found that training with ES-induced knee extension may slow the rate of bone loss, but found no reversal of osteopenia. More recent findings found no attenuation Loss of signal power in a transmission.
Attenuation

The reduction in level of a transmitted quantity as a function of a parameter, usually distance. It is applied mainly to acoustic or electromagnetic waves and is expressed as the ratio of power densities.
 of bone loss when comparing BMD before and after ES-induced leg cycling exercise (6, 32, 60). Based on these results, ES is not a well-supported treatment option for osteoporosis management. However, future studies are still needed to fully explore the outcomes of ES on osteoporosis management in persons with acute and chronic SCI.

Wound and Pressure Sore Management

Pressure sores and skin wounds are common complications affecting approximately 80% of individuals with SCI (17). Skin breakdown can eventually lead to decubiti ulcers, and if left untreated can result in permanent tissue damage (17). Electrical stimulation applications may limit the major risk factors that influence an individual's susceptibility to skin lesions (10). A survey of 11 individuals with implanted neuroprostheses for standing and ambulation exercise 12 months post injury reported a reduction in pressure sore incidences, among other findings (1).

Unfortunately, few studies have documented the use of ES for prevention of pressure ulcers. Long-term use of ES has been reported to improve wound healing rates by as much as 50% (124) and to provide long-term adaptive improvements to muscle morphology (10). Fergusson et al. (43) measured ischial ischial /is·chi·al/ (is´ke-il) ischiatic; pertaining to the ischium.

ischiadic, ischial

ischiatic.
 pressures during quadriceps stimulation of 9 SCI individuals. Pulsed-ES with alternating polarity has been shown to be the most effective for wound healing (96). These studies suggest that therapeutic and functional ES could be used for prevention and management of wound healing and pressure sore development. Levine et al. (78, 79) reported ES to the gluteus maximus muscle The gluteus maximus is the largest and most superficial of the three gluteal muscles. It makes up a large portion of the shape and appearance of the buttocks.

It is a broad and thick fleshy mass of a quadrilateral shape, and forms the prominence of the nates.
 caused pressure redistribution and increased localized blood flow. However these studies were performed on healthy able-bodied individuals that do not have compromised muscle bulk. Considering this shortcoming, Bogie bo·gie 1 also bo·gy  
n. pl. bo·gies
1. One of several wheels or supporting and aligning rollers inside the tread of a tractor or tank.

2.
 et al. (11) studied the tissue effects of ES to the gluteal muscles in a small group of individuals with SCI and reported pressure reduction near the ischial tuberosity tuberosity /tu·be·ros·i·ty/ (-te) an elevation or protuberance, especially one on a bone where a muscle is attached.

tu·ber·os·i·ty
n.
1. The quality or condition of being tuberous.
. The reported increased muscle bulk around the buttock but·tock
n.
1. Either of the two rounded prominences on the human torso that are posterior to the hips and formed by the gluteal muscles and underlying structures.

2. buttocks The rear pelvic area of the human body.
 region likely provided more protective "cushioning". Still more research is needed that study a larger population of subjects and how tissue variability affects treatment outcomes with ES treatment.

FUTURE OPPORTUNITIES AND CHALLENGING ISSUES

ES technology impacts many areas of rehabilitation, and can be used as a therapeutic medium to augment functional independence of individuals with SCI. The technology has progressed significantly over the last 10 years, with several devices being developed or receiving FDA approval. Taking advantage of these opportunities requires inspection into the practicality of ES devices. Engineers (designers), healthcare professionals (prescribers), insurance companies (payers), and the SCI community (users) ultimately decide on whether an ES device is reasonable for clinical use. Future use of ES technology must face the challenges of cost, education, and machine-user interfacing.

I. Cost: The greatest challenge facing widespread use of ES applications is expense. The cost of ES applications includes initial fees for purchase, maintenance for electrode purchasing, repairs, and healthcare provider fees. Multi-purpose systems may be more cost-effective and their uses are more extensive with broader populations of users in mind. However, different kinds of costs and cost-savings that should be considered for effective implementation of this technology assuming that the outcomes are real and health benefits can be proven.

II. Education: User knowledge is another major challenge affecting ES applications. However, knowledge must be gained through accurate dissemination of research results that include the advantages and limitations. Comprehensive review of these studies should assist clinicians in their decision-making process on how best to prescribe and treat.

III. Machine-User Interfacing: Machine-user interfacing refers to the interaction of the ES system and user. As the sophistication so·phis·ti·cate  
v. so·phis·ti·cat·ed, so·phis·ti·cat·ing, so·phis·ti·cates

v.tr.
1. To cause to become less natural, especially to make less naive and more worldly.

2.
 of ES technology improves, user-friendly interfacing becomes an even greater clinical challenge. Fisekovic et al. (48) developed an all-purpose, easy to use controller that can stimulate many muscle groups to assist in functional tasks (i.e., transfers, ambulating, reaching, and grasping) using a PC-based software package integrated with the ES controller. User-friendly graphical interfaces acquire, analyze, and present these data on a standard PC that are interpretable to any user and compatible with standard universal ES systems. Future development of ES technology must consider user friendliness and the machine-user interfaces.

CONCLUSIONS

Electrical stimulation has potential to contribute to the rehabilitation of person with SCI and to reduce/prevent the secondary complications in these individuals. However, many of these systems are not widely used in the clinical setting primarily due to a lack of clear evidence, cost, and limited user knowledge. There is a growing need for evidence-based practice that clearly define ES applications and outcomes for a given physical disability. In order to maximize ES benefits as the rehabilitation tool of choice for individual with SCI, studies need to further document cost-benefit ratio, clinical outcomes, limitations, and adverse effects of these systems in order to truly determine how, where, and in whom it can be most beneficial.

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Pouran D. Faghri (1) and Randy D. Trumbower

(1) Department of Health Promotion & Biomedical Engineering Program, University of Connecticut The University of Connecticut is the State of Connecticut's land-grant university. It was founded in 1881 and serves more than 27,000 students on its six campuses, including more than 9,000 graduate students in multiple programs.

UConn's main campus is in Storrs, Connecticut.
, Storrs, CT and (2) Functional Performance Laboratory, School of Engineering, Biomedical Engineering Program, University of Connecticut, Storrs, CT

ADDRESS CORRESPONDENCE TO:

Pouran D. Faghri, MD, MS, FACSM FACSM Fellow of the American College of Sports Medicine.

FACSM
abbr.
Fellow of the American College of Sports Medicine
 

Department of Health Promotion

University of Connecticut

Koons Hall, U-2101

358 Mansfield Road, U-2101

Storrs, CT 06269-2101

Ph: (860) 486-0018

FAX: (860) 486-5375

E-mail: pouran.faghri@uconn.edu
Table 1: Advantages, Methods, Disadvantages, and Alternatives of
ES Applications

ES Applications        Advantages                  Methods

Cardiovascular         [up arrow] endurance,       1. ES-induced leg
fitness(71, 95, 110,   heart and lung function,       cycling
140)                   and muscle integrity        2. ES-induced
                                                      rowing
                                                      ergometer

Breathing and          Independence with lung      1. Functional
Coughing assistance    clearing and coughing,         magnetic
(80-82, 130)           stimulate activity of          stimulation
                       diaphragm and chest         2. Surface
                       muscles, less dependent        electrodes on
                       on ventilator                  abdomen
                                                   3. Phrenic nerve
                                                      stimulator
                                                   4. Intercostal
                                                      muscle pacer

Grasping and           [up arrow] independence     1. Freehand system
reaching activities    during activities of        2. Handmaster
(8, 20, 48, 93, 121,   daily living,               3. Bionic Glove
129, 135)              [down arrow] need for       4. NEC-ES system
                       assistance from others

Transfers and          [up arrow] independence     1. Hybrid orthoses
ambulation (1, 12,     and mobility, exercise,     2. Parawalker
74, 99)                [down arrow] need for       3. Walkaid
                       wheelchair and other        4. Parastep
                       walking devices

Bowel and bladder      Assists in bladder          1. spinal cord
assistance (52, 142)   emptying, [down arrow]         stimulation
                       frequency of UTI,              (dorsal column
                       [down arrow]                   stimulation)
                       constipation,               2. neuromodulation
                       [down arrow] bowel          3. pelvic floor
                       and bladder accidents          stimulation
                                                   4. Vocare system

Erection and           Penis erection,             1. electrode probe
electroejaculation     ejaculation of sperm for    in rectum
(13, 59)               artificial insemination

Wound care and         To prevent or treat         1. surface ES units
pressure sore          pressure sores              2. implantable ES
management (43,                                       units
124)

Circulation (35, 39,   [down arrow] DVT,           1. surface ES units
41, 42)                [down arrow] distal limb
                       swelling

Contracture            To help maintain or         1. surface ES units
management (38)        regain functional range
                       of motion (ROM)

Osteoporosis           [down arrow] bone loss in   1. surface ES units
management (7, 91)     lower extremities,
                       [down arrow] fracture
                       risk

ES Applications        Disadvantages          Alternatives

Cardiovascular         1. not readily         1. wheelchair
fitness(71, 95, 110,      accessible             propulsion
140)                   2. cost                2. swimming
                       3. setup time          3. arm ergometry
                       4. user-machine
                          interface

Breathing and          1. surgery             1. chest percussion
Coughing assistance    2. potentially         2. suctioning
(80-82, 130)              interfere with      3. positioning
                          other implanted     4. corset that inflates
                          devices                or deflates
                       3. training            5. ventilator
                          requirement

Grasping and           1. may require         1. orthoses and
reaching activities       extensive surgery      splinting
(8, 20, 48, 93, 121,   2. cost                2. tendon transfers
129, 135)              3. crude control       3. assistance from
                       4. man-machine            others
                          interfacing

Transfers and          1. setup time          1. Reciprocating gait
ambulation (1, 12,     2. cost                   orthoses
74, 99)                3. user-machine        2. HKAFO
                          interface           3. Assistance from
                                                 others
                                              4. Standup wheelchair
                                              5. Standing frame

Bowel and bladder      1. surgery             1. bladder management
assistance (52, 142)   2. erectile               -- catheters, condom
                          dysfunction            catheters,
                       3. cost                   medications
                                              2. bowel management
                                                 -- diet, stool
                                                 softeners and
                                                 suppositories,
                                                 digital rectal
                                                 stimulation,
                                                 medications

Erection and           1. autonomic           1. masturbation
electroejaculation        dysreflexia         2. vibrator
(13, 59)               2. no erection for     3. suction device
                          SCI below T10       4. medications
                       3. require a           5. prosthetic
                          clinical visit

Wound care and         1. may require         1. diet
pressure sore             surgery             2. positioning
management (43,        2. user-machine        3. manual pressure
124)                      interface              relief
                                              4. proper seat
                                                 cushioning

Circulation (35, 39,   1. user-machine        1. positioning
41, 42)                   interface           2. leg stocking
                                              3. anti-coagulant
                                                 medications
                                              4. physical therapy
                                              5. intermittent
                                                 pneumatic
                                                 compression

Contracture            1. user-machine        1. passive stretching
management (38)           interface           2. passive ROM
                                              3. splinting
                                              4. exercise
                                              5. medications to
                                                 reduce spasticity

Osteoporosis           1. conflicting         1. standing frame
management (7, 91)        outcomes            2. orthotics and bracing
                       2. user-machine        3. standup wheelchair
                          interface
                       3. setup time

Abbreviations: [down arrow], decrease; [up arrow], increase; DVT,
deep venous thrombosis; UTI, urinary tract infection.
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Author:Faghri, Pouran D.; Trumbower, Randy D.
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Date:Dec 22, 2005
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