Role of Functional Electrical Stimulation in Tetraplegia Hand Surgery

Archives of Physical Medicine and Rehabilitation journal homepage: www.archives-pmr.org Archives of Physical Medicine and Rehabilitation 2016;97(6 Suppl 2):S154-9

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Role of Functional Electrical Stimulation in Tetraplegia Hand Surgery Ines Bersch, PT, MSc,a Jan Fride´n, MD, PhDa,b,c From the aSwiss Paraplegic Center, Nottwil, Switzerland; bCenter for Advanced Reconstruction of Extremities, Sahlgrenska University Hospital, Gothenburg, Sweden; and cDepartment of Hand Surgery, Institute of Clinical Sciences, The Sahlgrenska Academy at Go¨teborg University, Gothenburg, Sweden.

Abstract The use of functional electrical stimulation (FES) to improve upper limb function is an established method in the rehabilitation of persons with tetraplegia after spinal cord injury. Surgical reconstruction is another well-established yet underused technique to improve the performance of the upper extremities. Hand surgery plays an essential role in restoring hand function, mobility, and quality of life in the tetraplegic population. The knowledge about the effects of FES on a structural and functional level is fundamental for understanding how and when FES can be used best to support the effect of hand surgery, both pre- and postoperatively. In this article we discuss principles of FES and how FES improves functional outcome after surgical reconstruction. The reported results are based on preliminary clinical observations. Archives of Physical Medicine and Rehabilitation 2016;97(6 Suppl 2):S154-9 ª 2016 by the American Congress of Rehabilitation Medicine

Functional electrical stimulation (FES) in rehabilitation of patients with spinal cord injury (SCI) opens up a wide field of possible treatments with multiple aims. FES treatment has been shown to improve lower1-3 and upper limb function4-6; improve trunk function7,8; improve breathing in high-level tetraplegia9-11; improve bladder, bowel, and sexual function12; improve cardiovascular fitness by increasing aerobic capacity13-16; decrease body fat mass17; and prevent pressure ulcers by increasing muscular blood flow and muscle mass.18-21 FES may also have an influence on synapses and motor neurons, as animal studies have shown.22 We also propose that FES could be a useful treatment modality before and after surgical reconstruction of upper limb function. One of the first applications of FES in combination with tendon transfer procedures was the freehand system, developed in Cleveland, Ohio.23 The freehand system was implanted in >250 persons with tetraplegia with a C5-6 lesion.24 It was reported that all patients with implants had better grasp and release, greater pinch force, and activities of daily living independence.25 To improve the outcome, implanting the system was combined with reconstructive hand and arm surgery. As surgical techniques for reconstructive procedures continue to be refined, the pre- and

Supported by the Swiss Paraplegic Centre, Nottwil, Switzerland. Publication of this article was supported by the American Congress of Rehabilitation Medicine. Disclosures: none.

postoperative rehabilitation protocols are evolving as well. Importantly, the combination of multiple procedures in a single-stage operation has led to shorter and more efficient postsurgery rehabilitation periods.25-28 Therefore, integrating the use of FES with surgical protocols may be of benefit on a structural and functional level to improve the preoperative condition of the donor and recipient muscles and even more to enhance the postoperative outcome and optimize the rehabilitation process. The aim of this article is to discuss how and when FES can be used to support the effect of hand and arm surgery in patients with tetraplegia. Preoperative strengthening of the transferred muscle is crucial for a satisfying functional outcome. Depending on the intended postoperative function of a donor muscle, FES may also be used to retrain the transferred muscle postoperatively under certain conditions. We will discuss the use of FES to achieve these goals and present preliminary findings based on our clinical experience.

Effects of FES on muscular physiology There are a few principles of FES that must be considered in order to configure an efficient/effective stimulation protocol. When creating individual stimulation protocols, the effectiveness of different stimulation parameters should be considered. An increasing current amplitude (mA) leads to an increased torque

0003-9993/16/$36 - see front matter ª 2016 by the American Congress of Rehabilitation Medicine http://dx.doi.org/10.1016/j.apmr.2016.01.035

Functional electrical stimulation in hand surgery (Nm) by recruitment of additional motor units. Increasing the pulse width has shown to increase the torque (Nm) by increasing motor unit activation. Furthermore, increasing the frequency (Hz) leads to an increased evoked torque (Nm) by increasing the torque per active muscle area.29

Activation and recruitment The stimulation current is transmitted via nerves; therefore, the lower motor neuron (LMN) must be intact.30 The propagation of action potentials and synaptic transmission occurs analog to the central nervous system. In FES, all reachable motor units are excited without physiological recruitment. The excitation follows the all-or-none principle. During physiological activation, type I fibers are recruited first, followed by type IIA fibers when additional force is needed and type IID fibers when the activation approaches the maximum.

Fatigue effects Muscle fatigue occurs because the same motor units are stimulated repeatedly under stable stimulation parameters.29,31 Fatigue can be decreased and endurance increased by using a welldesigned stimulation protocol. There are 2 types of fatigue mentioned in the literature. First, the high-frequency fatigue occurs at
50Hz. It compromises the neuromuscular transmission by reducing the deactivation of neurotransmitters at the neuromuscular junctions, and muscle force subsequently decreases.32 FES does not affect other processes known to cause fatigue (eg, excitation-contraction coupling).33 Recovery occurs quickly by reducing the frequency.29 Second, the low-frequency fatigue occurs in the range from 15 to 50Hz. The excitationcontraction coupling is reduced, and muscle force decreases. In this case, recovery is extended to hours or days.33 However, repetitive stimulation of a muscle with a normative frequency can achieve better muscle fatigue resistance.34 It has been observed in the quadriceps muscle that low-frequency stimulation can increase fatigue resistance.35 Gorgey et al29 have shown that only the frequency has an influence on fatigue and not the amplitude or the pulse width. In 7 healthy subjects who stimulated their quadriceps muscle, it was possible to reduce the fatigue from 76% to 39% by reducing the frequency of FES from 100 to 25Hz.29 On a structural level, FES can cause a change in muscle fibers from type IID to type IIA and partly to type I.36 That means that the altered fiber type composition can partly be reversed. Muscle fibers type I are more fatigue resistant. A muscle fiber shift from type I to type II occurs approximately 6 weeks after SCI.37 Therefore, muscle fiber type conversion after FES can increase the fatigue resistance of stimulated muscles. Furthermore, the training can be performed more efficiently taking into account the torque-frequency relation. If the contractile speed of a chronically paralyzed muscle decreases, it should be possible to get the same muscle force by decreasing the frequency (Hz).33

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Strength The power output of muscles or muscle groups can be increased by FES after SCI.2,38 Several studies in individuals with SCI have shown that it is possible to increase torque and power output by FES-supported exercises in the lower and upper extremities if the LMN is intact.39,40 Furthermore, there is an increase in the physiological cross-sectional area of the stimulated muscles. Stimulation parameters must be chosen carefully to achieve the intended effect. The pulse width should be between 250 and 400ms. The frequency should be between 20 and 50Hz, and the amplitude should be as high as possible to stimulate as many motor units as possible.

FES and reconstructive arm and hand surgery FES has a great potential to enhance hand surgery. It can be beneficial preoperatively because selective stimulation has a positive influence on the muscle structure, power output, cross-sectional area, and muscle fiber type adaptation. In postsurgical treatment, electromyography-triggered stimulation is applied with respect to retraining the transferred muscle to perform a new function and may affect neuroplastic changes that support motor learning. Additionally, strengthening of transferred muscles can be achieved.41 Furthermore, preoperative FES testing of potential donor muscles is a simple and reliable method to determine if the contraction of the muscle is sufficient or if the muscle shows signs of denervation.

FES before surgery Several issues must be addressed before a muscle can be selected as a donor to replace a lost function. First, it should develop sufficient force (M4 on British Medical Research Council Scale); second, it should have a sufficient physiological cross-sectional area. Similar criteria apply to the recipient muscles when they are considered for a nerve transfer.42 After SCI, the muscle structure changes as a result of disuse or denervation.33,37 The prerequisites for a recipient muscle are a certain number of contractible motor units and a sufficient cross-sectional area. The stimulation schedule of the donor muscle before surgery should contain low-frequency training to avoid muscle fatigue,29 if possible in a loaded position or acting against gravity or resistance. The preparation of the recipient muscle should be similar but if possible performed using a functional movement (table 1). The training has to be carried out 3 times a week for at least 30 minutes during each session.43 The training should start 12 weeks before surgery.32,39 The best training is FESsupported arm cranking. An advantage of FES arm cranking is the synchronization of the movement (ie, stimulation and resistance of each muscle). However, preoperative training usually has to be done in a domestic setting; therefore, FES with a 2-channel stimulator in combination with physical therapy exercises in a loaded position or against resistance with portable weights could be used alternatively to FES-supported arm cranking.

List of abbreviations: BR FES LMN SCI

brachioradialis functional electrical stimulation lower motor neuron spinal cord injury

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FES after surgery The recipient muscle has to be strengthened after the immobilization period. Training of the recipient muscle against resistance

I. Bersch, J. Fride´n

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Table 1 Stimulation protocol before surgery: Type of reconstruction, donor and recipient muscles with corresponding stimulation parameters and training procedure Reconstruction

Donor Muscle

Recipient Muscle

Stimulation Parameters

Training Procedure

Elbow extension

DEL

TRI

Wrist extension

BR

ECRB

Loaded Against resistance In function Against resistance In function

Key pinch

BR

FPL

300ms 20e35Hz 20e50mA 300ms 20e35Hz 15e40mA 300ms 20e35Hz 15e40mA

Against resistance In function

Abbreviations: DEL, deltoid; ECRB, extensor carpi radialis; FPL, flexor pollicis longus; TRI, triceps.

is possible approximately 6 to 8 weeks after surgery.42 After 4 weeks, it is possible to train the muscle against gravity. During this period, the stimulation schedule consists of dynamic arm cranking or movement without resistance, using a low frequency of approximately 20Hz. When training against resistance is possible, arm cranking against increasing resistance or functional movements against resistance or load can be performed. Furthermore, the frequency can be increased up to 50Hz (table 2). The training generally takes place in a clinical setting and can then be continued at home. We recommend training for 3 months with 3 sessions per week, each session lasting 30 minutes.

Motor learning The electromyography-triggered stimulation opens the field for motor learning and relearning. After reconstructive hand and arm surgery the patient has to learn to perform new functions with a muscle that previously had a different function, or in other words a forgotten function has to be relearned. The representation of the function of a paralyzed muscle on the motor cortex has been reported to disappear after disuse.44 For example, after transferring the brachioradialis (BR) muscle to the extensor carpi radialis brevis muscle to gain wrist extension, the treatment goal for the patient is to learn to extend the wrist without elbow flexion and pro- and supination (the original functions of the BR). In occupational therapy and physiotherapy, the goal is to teach the patient to activate the BR exclusively for wrist extension. This motor learning process is performed following the hands-on/hands-off

Table 2 Stimulation protocol after surgery, including training procedure and stimulation parameters Time

Training Procedure

4wk postsurgery

Dynamic arm cranking without resistance or dynamic movement without resistance Arm cranking against increasing resistance or functional movements against resistance or load

6e8wk postsurgery

Stimulation Parameters 300ms 20e35Hz 15e30mA 300ms 20e35Hz 20e60mA

principle45 in combination with repetitive task orientated exercises. Motor learning consists of 3 stages: (1) the cognitive stage, (2) the associative stage, and (3) the autonomous stage. The cognitive stage begins when the learner is first introduced to the motor task. In this stage a hands-on role of the therapist is recommended in order to support the learning process. The associative stage is characterized by performing and refining the skills. The important stimuli have been identified, and their meaning is known. The autonomous stage is characterized by a nearly automatic kind of performance. The therapist should take a hands-off approach in the last 2 stages mentioned.45,46 FES is supposed to have a supporting effect in functional tasks.6,47 By performing a certain task, in this case wrist extension, the motor area of the brain sends a command via the spinal cord and the efferent nerves to the target muscles (wrist). If this stimulation reaches a sufficient threshold, the BR contracts and a voluntary wrist extension occurs. Electromyography-triggered FES initiates and intensifies the muscular contraction (fig 1). Afferent nerves transmit the information concerning the BR activity via the spinal cord to the brain where the information is processed.

FES as a diagnostic tool After SCI, voluntary movement of the muscles below the lesion is not possible because of the damaged central nervous system. At the level of injury, there is often an upper motor neuron and LMN lesion. The effect on the affected muscles regarding atrophy and structural transformation is different. Atrophy as a result of disuse appears after an upper motor neuron lesion.48 The reflex arcs are intact; consequently, FES can be conducted via the nerve. If the LMN is affected, denervation atrophy appears and a structural transformation of muscle tissue into soft tissue (fat or connective tissue) occurs.49 In this case, electrical stimulation has to be applied directly to the muscle fibers. The excitation of a nerve is possible with very short impulses in the range of 200 to 400ms. In contrast, excitation of a muscle begins at 10 milliseconds. In reconstructive tetraplegia hand surgery, it is important to know which type of lesion is present in a donor or a recipient muscle. This is particularly imperative when considering the transfer of a functioning motor nerve to a target nerve in order to reinnervate a key muscle function. FES of a nerve is easily feasible with a 2-channel nerve stimulator, a pen electrode, and a reference electrode. In case of denervation, a 2-channel muscle stimulator with 2 electrodes is required to detect contractible muscle fibers. www.archives-pmr.org

Functional electrical stimulation in hand surgery

S157 fasciae latae muscle or the tibialis anterior muscle is commonly used. To improve hand function, muscle-tendon transfers of the BR to the flexor pollicis longus muscle and of the extensor carpi radialis longus muscle to the flexor digitorum profundus muscle, combined with a split tenodesis of the flexor pollicis longus muscle to the extensor pollicis longus muscle are performed. Furthermore, thumb metacarpophalangeal joint fusion or a transfer of the extensor digiti minimi muscle to the abductor pollicis brevis muscle is realized. In addition, a reconstruction of the interossei muscles may be performed.28

FES protocol Fig 1 Electromyography-triggered stimulation of the BR stimulator, STIWELL med4.

Methods In the Swiss Paraplegic Center, the following FES protocol was used in combination with reconstructive tetraplegia hand and arm surgery.

Tendon transfer procedures The participants (table 3) received
1 of the procedures subsequently described. In cases of triceps reconstruction to improve elbow extension, the insertion of the posterior deltoid muscle is moved to the olecranon. A tendon graft harvested from the tensor

Table 3

Patients’ characteristics

Patient Sex Diagnosis 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

F M F M M M M M M M M M M M M M M M M F

C5 Plexus lesion C6 C6 C4 C5 C5 C5 C4 C5 C7 C5 C5 C5 C6 C6 L3/TBI C6 C4 Locked-insyndrome

AIS Grade Procedure C A C A A C B B A C A D B A C C B D

Triceps reconstruction Hand reconstruction Hand reconstruction Triceps and hand reconstruction Triceps reconstruction Triceps and hand reconstruction Hand reconstruction Triceps reconstruction Triceps and hand reconstruction Triceps reconstruction Hand reconstruction Hand reconstruction Hand reconstruction Hand reconstruction Triceps reconstruction Hand reconstruction Hand reconstruction Triceps and hand reconstruction Hand reconstruction Hand reconstruction

Abbreviations: AIS, American Spinal Injury Association Impairment Scale; F, female; M, male; TBI, traumatic brain injury.

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All of the participants were treated with FES using the same protocol (see tables 1 and 2). The stimulation was performed preand postoperatively with a 2- or 8-channel stimulator (Motionstim 8 and Microstim 2a). Those who had arm surgery, mainly triceps reconstruction, underwent FES to strengthen the elbow extensor after surgery. Two of them stimulated the donor muscle (posterior deltoid) for 3 months before surgery. All who had reconstructive hand surgery performed electromyography-triggered electrical stimulation after surgery to support the process of motor learning. The electromyography-triggered stimulation was performed with the STIWELL med4.b The 2 electromyographic channels allow a biofeedback therapy. It was possible to differentiate between compensatory and voluntary activity of the donor muscle and therefore to achieve the targeted stimulation. The stimulation parameters were 300-ms pulse width at 20Hz with an individually chosen amplitude (mA) in the range between 15 and 40mA. The latter depended on the quality of the muscle contraction without a spillover effect to neighboring muscles.

Results The 2 patients who were stimulated before surgery and who received triceps reconstruction were able to increase the strength of the donor muscle and improve the preoperative condition. The improvement was assessed by observing the quality of transfer techniques and self-reported stability of the arm during bench to wheelchair transfers. The therapists observed that all who stimulated the recipient muscles after surgery built up strength easily and quickly despite the immobilization time. Those who received electromyography-triggered stimulation learned to activate the transferred muscle after 2 to 3 FES treatments. They were able to reach an object with either spontaneous elbow extension or were able to grasp during the first trial. The mentioned beneficial effects are only based on clinical observations.

Discussion Strengthening of the transferred muscle is an important prerequisite for a satisfying functional outcome. FES should be performed on the recipient and/or donor muscle before and after reconstructive tetraplegia surgery to increase muscle torque and power output. Several studies have shown that it is possible to increase torque and power output with FES-supported exercise in the lower and upper extremities of individuals with SCI.39,40 Therefore, FES can be used to improve the strength and number of available donor muscles before reconstructive surgery. Muscles

I. Bersch, J. Fride´n

S158 that are too weak to be used for transfer surgery can be strengthened with FES training to make them suitable candidates. Using FES during postoperative activities may improve the overall coordination with other muscles of the upper extremities. The patient has to learn a new function for a muscle that previously had another function. FES in functional tasks also has a motor learning effect.6,47 The idea is to help the patient who is unable to achieve voluntary activation to learn to use the transferred muscle with the external stimulus. Furthermore, building up additional muscle strength can be achieved by combining FES with exercises.50 FES-based exercises can be easily performed by the patient or with the help of caregivers at home. Until now there is no published study that either proves or disproves the positive effect of these 2 methods regarding strengthening and motor learning. The positive effects observed in our study are based on the clinical observations of the therapists who have expertise in treating this patient population. Based on this preliminary work, we intend to conduct additional studies to quantify the improvements and to differentiate the effects of FES from other forms of therapy (eg, strengthening). Furthermore, the effect of the FES-supported training before surgery should be measured. Preoperatively, this would include the measurement of the voluntary-evoked force (torque; Nm) of the stimulated muscles and the electrostimulated-evoked force (torque; Nm) of the donor and recipient muscles before FES training and after a training period. After surgery, the same measures should be performed as soon as possible to see how much of the FES-evoked force (torque; Nm) has been lost in comparison with the baseline values of the FES-trained muscle before surgery. The Canadian Occupational Performance Measure should be used to evaluate the patients’ perspective. The use of modalities (eg, FES) is not a routine part of conventional therapy, but appears to have the potential for improving upper limb function after SCI. Even if the effect of FES is beneficial, there are some limitations that need to be taken into account. FES is time-consuming with regard to the required preparation for the patient before the treatment. Electrodes have to be attached and wires have to be fixed so that they do not hinder the movement. The wish of therapists and patients to have small, portable, easy-to-handle, wireless systems must be acknowledged. Only in a small number of countries are FES devices refunded by insurance. The consequence is that FES cannot be continued in a domestic setting in all countries. Finally, studies are needed to provide evidence for the efficacy and efficiency of FES in tetraplegia hand surgery because the current knowledge is based on clinical observations.

Conclusions FES has a great potential as part of surgical reconstruction. It can be applied before and after tetraplegia reconstructive hand and arm surgery to strengthen the donor and/or recipient muscles. Furthermore, there is clinical evidence that electromyographytriggered FES used after reconstructive surgery improves the motor learning process.

Suppliers a. Krauth þ Timmermann GmbH, Germany. b. STIWELL med4; Otto Bock Suisse AG.

Keywords Electric stimulation therapy; Reconstructive surgical procedures; Rehabilitation; Spinal cord injuries; Tendon transfer

Corresponding author Ines Bersch, PT, MSc, Swiss Paraplegic Center, Guido A. Za¨ch Strasse, CH-6207 Nottwil, Switzerland. E-mail address: ines. [email protected].

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