Nerve Transfer Strategies for Spinal Cord Injury

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Nerve Transfer Strategies for Spinal Cord Injury Q5

Ferry Senjaya1 and Rajiv Midha2

Key words - Nerve transfer - Neurotization - Paraplegia - Restoration of function - Spinal cord injury - Tetraplegia Abbreviations and Acronyms AIN: Anterior interosseous nerve CNS: Central nervous system ECRB: Extensor carpi radialis brevis FDP: Flexor digitorum profundus FPL: Flexor pollicis longus LMN: Lower motor neuron MABCN: Medial antebrachial cutaneous nerve MRC: Medical Research Council PIN: Posterior interosseous nerve SCI: Spinal cord injury VR: Ventral root From the 1Neurosurgery Department, Siloam Hospitals Lippo Village, Pelita Harapan University, Tangerang, Indonesia; and 2Division of Neurosurgery, Department of Clinical Neurosciences, Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada To whom correspondence should be addressed: Rajiv Midha, M.D., M.Sc. [E-mail: [email protected]] Citation: World Neurosurg. (2012) . http://dx.doi.org/10.1016/j.wneu.2012.10.001 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2012 Elsevier Inc. All rights reserved.

INTRODUCTION The annual incidence of spinal cord injury (SCI) in the United States is approximately 40 cases per 1 million population or roughly 12,000 new cases each year, not including injured individuals who die at the scene of the accident (39). SCI occurs most commonly in young, previously healthy, and active individuals. Based on a survey in 2005, the most frequent neurologic deficit at discharge was incomplete tetraplegia (39.5%) (39). One of the most devastating effects of SCI at the cervical level is the loss of arm or hand functions, which has a significant impact on a patient’s independence (9). A need assessment survey in 565 tetraplegics revealed that 77% of subjects expected an

Spinal cord injury (SCI) is associated with long-term health issues. Nerve Q1 transfer is a feasible option for restoration of critical limb function in patients with SCI that potentially improves independence and quality of life. This article delineates the general principles of nerve transfer and its specific application pertinent to SCI. The available nerve transfer strategies are described based on the targeted limb function, mostly involving critical upper extremity function. The role of nerve transfer for paraplegia, diaphragm reanimation, and bladder reinnervation is also discussed.

essential improvement in quality of life if their hand functions improved (46); this is comparable to the expectation of these subjects with regard to improvement of bowel and bladder control. Sexual function, pressure sores, standing, and pain control all were scored lower. Even partial recovery of arm and hand functions can have an enormous impact on quality of life because of the invaluable roles of these functions in activities of daily living and mobility (9, 47). A more recent survey in 137 subjects with tetraplegia found similar findings (2). Greater than 90% of the respondents believed that recovery of their arm or hand function would improve their quality of life. However, only 39% of these subjects had been told about the availability of reconstructive procedures to enhance their potential level of independence, and only 9% underwent such procedures. The most critical functions targeted by reconstructive procedures in patients with cervical cord injury are the restoration of elbow extension, lateral thumb pinch (key pinch), grasp, and release (10, 25). The traditional approach for reconstructive surgery has consisted of tendon transfers (10, 12). Although this approach can offer functional gains for tetraplegic patients to some extent, there are obstacles to an ideal result. Muscle groups affected by lower motor neuron (LMN) damage undergo fibrosis over time, leading to joint contractures and interfering with the function of the reconstructed hand (9, 10). Spasticity in tetraplegic patients may also render the result of tendon transfer unpredictable (42).

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Although rarely used to date, nerve transfer is a viable method for restoration of function after SCI (10, 15). Nerve transfer involves the repair of a distal denervated nerve element by using a proximal foreign nerve as the donor of neurons and their axons to reinnervate the distal targets (1, 12, 36). The concept is to sacrifice the function of a lesser valued donor nerve to revive function in the recipient nerve and muscle, which is considered functionally more critical than the donor nerve. There are several fundamental principles to maximize outcome in motor nerve transfers, as follows (22, 36): (i) The recipient nerve should be repaired as close as possible to the target muscle to ensure the shortest amount of time for reinnervation in an attempt to minimize distal nerve denervation and motor endplate changes. (ii) The donor nerve should be from a muscle whose function is expendable or has redundant innervation. (iii) Nerve repair should be performed directly, without intervening graft. (iv) The use of a donor nerve with pure motor fibers maximizes muscle fiber reinnervation. (v) The donor nerve should have a large number of motor axons and be a reasonable size match to the recipient nerve. (vi) To facilitate motor reeducation, a donor nerve that has a function synergistic to the muscle to be reconstructed should be used because cortical readaptation is the physiologic basis of functional recovery. (vii) Motor reeducation improves functional recovery postoperatively. Nerve transfers offer several advantages over tendon transfers. Tendon transfers require significantly more dissection and

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extended postoperative limb immobilization while the tendon heals (10). Reconstruction of finger flexion and extension must be done in a separate phase, owing to conflicting positions for postoperative immobilization (42). For some patients, this may be problematic because it causes a patient who is already highly dependent on others to become utterly incapable of performing the most basic self-care for a significant time (4, 10, 20). More importantly, a tenotomy may cause detrimental effects on muscle function owing to the fact that reduced specific force is developed (18, 24). Nerve transfers require a shorter period of less restrictive immobilization, probably with less pain, and minimal loss of donor muscle function (10). Reconstruction of finger flexion and extension can be performed at the same time. The tensioninsertion balance of the muscle-tendon unit is preserved because there is no disruption to the insertion or attachment of the muscle in question, maintaining line of pull and excursion and avoiding scar-induced restrictions to movement (10). Nerve transfers also offer a greater functional gain for a given transfer (9, 10, 12). The transferred axon, which originally provided innervation to a single muscle, can reinnervate multiple motor fibers. Later on, with motor reeducation and central plasticity, it is possible to activate multiple functions independently by the same nerve that initially controls only a single function (9, 10, 36). An example is provided in the transfer of the distal extensor carpi radialis brevis (ECRB) motor branch (with preservation of the proximal motor branch to ECRB) to the flexor pollicis longus (FPL) motor branch. With successful reinnervation and muscle reeducation, a nerve that initially controls only wrist extension (ECRB) gains a function to flex the thumb as well (FPL). In another situation, a single nerve transfer can reinnervate multiple muscle groups (e.g., transfer of brachialis motor branch to anterior interosseous nerve). This procedure gains control for the thumb flexor (FPL) as well as long finger flexors (FDP). By contrast, with tendon transfers, only one movement can generally be produced per muscle-tendon group transferred. Reconstruction of thumb and finger flexion requires two separate tendon transfers (e.g., brachialis to FDP and brachioradialis to FPL).

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Nerve transfer can be accomplished without appreciable loss of function from the donor muscle group because nerve transfer can be performed with only a portion of the donor nerve, not entirely denervating the muscle associated with the donor nerve (9, 10). Although this partial denervation results in a reduced number of axons to the original muscle, the residual motor axons sprout within the muscle and innervate orphaned muscle fibers to enlarge the motor unit. Each motor axon can increase innervation five times the number of muscle fibers that it originally served (17); this phenomenon is termed “adoption” (13). In time, the donor muscle may regain its original strength. When patients are carefully selected, and functional recovery takes place, nerve transfer seems like a promising option for reconstruction procedures for SCI (1). Nonetheless, some drawbacks are related to nerve transfers, as follows (1): (i) When the donor nerve and its pertinent muscle sacrificed are of suboptimal function to begin with (e.g., Medical Research Council [MRC] grade 3 or 4), nerve transfer may significantly downgrade its function. This may not be an issue if the donor nerve used is “completely” expendable (e.g., sacrificing supinator motor branch of radial nerve in a patient with strong biceps, which can act as a highly capable forearm supinator). (ii) An entirely denervated muscle, as a result of sacrifice of its nerve for donor, is no longer suitable for muscle transfer donor. Examples are the posterior deltoid and brachialis muscles, which are potential muscle transfer donors for restoring elbow extension and finger flexion. (iii) Central motor reeducation is needed to achieve functional recovery. This reeducation can be challenging for patients, especially for nerve transfers from nonsynergistic nerve. SCI PATHOPHYSIOLOGY AND ITS IMPLICATIONS IN NERVE TRANSFERS Traumatic SCI results in three distinct zones of spinal cord: supralesional segment, injured metamere or lesional segment, and infralesional segment (9, 10, 12, 15). The supralesional segment includes all components of the central nervous system (CNS) cephalad to the injury site. The injured metamere is the region directly impacted by the trauma and may extend several levels above and below the actual

site of impact owing to injury from secondary swelling and secondary injury (15). The myotome at the lesional segment generally shows some degree of LMN dysfunction. The infralesional segment is the region below the injury site. In a complete SCI, the infralesional segment and its corresponding peripheral nerves Q 2 generally remain anatomically intact, although they lose their volitional control (9, 10, 15). Aside from the SCI, associated peripheral nerve injury may also be present (9, 10, 15). These associated lesions may occur with the initial trauma or result from secondary events such as cast application or wheelchair use (15). Diagnosis may be difficult if the involved nerve corresponds to the injured metamere segment, and careful history taking, neurologic examination, and supplemental electrodiagnostic studies may be informative (15). Severe LMN injury at the injured metamere level requires different management than an upper motor neuron injury (10). With prolonged denervation resulting from LMN injury, the distal nerve becomes progressively less permissive to regenerating axons owing to endoneural tube fibrosis and Schwann cell loss (10). The denervated muscle undergoes severe atrophy and fibrosis, which often contributes to the development of contractures (10, 15). Reinnervation of muscle groups of the injured metamere may restore volitional function and prevent atrophy, fibrosis, and contracture (9, 10). Restoration of nerve function at the injured metamere level should be performed as early as possible, as in the case of peripheral nerve injury. Although nerve transfer intervention for the injured metamere is time-critical, this is not the case when addressing muscle groups innervated by the infralesional segment (affected by upper motor neuron injury) (10, 15). Nerve transfer may restore these muscle groups years after injury as long as the mechanical properties of the limb, such as joint mobility, are preserved. This restoration is possible because the innervation to these muscle groups has remained intact throughout. The architecture of the nerve and its target muscles is preserved, making this nerve an excellent conduit for regenerating axons if a nerve transfer is undertaken (10). Brown (9) reported a successful nerve transfer procedure to reconstruct elbow extension, wrist flexion-extension, and finger flexion-extension in a tetraplegic

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patient 13 years after injury. Preoperative investigations revealed mostly intact LMN innervation in the reconstructed upper limb, which might result from a remarkably thin segment of injured metamere. When innervation must be restored but a supralesional donor is unavailable, such as in a high cervical cord injury, an infralesional donor can be used in very select circumstances (10). This donor has been found useful in restoring innervation to the diaphragm when a high SCI results in LMN injury to the motor pool corresponding to the phrenic nerve. In this case, the intercostal nerve from the infralesional segment is transferred to the phrenic nerve to reinnervate the diaphragm for later implementation of diaphragmatic pacing. TIMING OF SURGERY AND PREOPERATIVE CONSIDERATIONS Nerve transfers should be performed after the reinnervation window, to allow adequate waiting time to ensure optimal spontaneous recovery has been achieved for lesional level myotomes. Bertelli et al. (4) recommended waiting for at least 6 months. Although recovery of SCI may occur 2 years after injury, most of the recovery occurs in the first 6 months (50). Muscles that remain totally paralyzed at 6 months after injury are not likely to recover or do not attain significant functional recovery (25). However, reinnervation of muscles innervated by the infralesional segment is not time-dependent and can be performed years after injury. As discussed previously, the extent of LMN injury at the injured metamere must be adequately assessed. This assessment is particularly important when the nerve transfer is contemplated at a point in time when the reinnervation window has elapsed. Nerve transfer in a chronically denervated muscle should be avoided because this work would be in vain. A detailed clinical examination is an indispensable part of the evaluation (15). Each key muscle group should be evaluated to determine the type of motor neuron injury (upper motor neuron or LMN) by evaluating its tone, trophic status, and relevant deep tendon reflex evaluation. One should also evaluate joint range of motion and deformities. In addition to the standard clinical assessment,

NERVE TRANSFER STRATEGIES FOR SCI

electrodiagnostic studies (electromyography and nerve conduction study) are beneficial to determine the extent of SCI (15). The presence of large numbers of fibrillations and positive sharp waves indicates injury to the motor neuron pool in the spinal cord resulting in chronically denervated muscle. Reduced compound muscle action potential amplitude indicates axon or motor neuron loss. However, nerve conduction studies can examine only a limited number of muscles, and the results can be affected by peripheral nerve compression and neuropathy (15). Another examination technique that is probably more useful is surface electrical stimulation (12, 15). This technique uses a bipolar surface electrical stimulator to stimulate paralyzed muscles, allowing evaluation of LMN integrity. Surface electrical stimulation provides an understanding of the mechanical properties of muscle, which can be quantified using the MRC scale (10, 15). Surface electrical stimulation allows exploration of almost all the muscles in the limbs, although stimulating or dissociating some deep muscles can be difficult (e.g., flexor digitorum superficialis and profundus) (15). Muscle that produces no perceptible contraction or only a flicker of contraction when stimulated or a response from antagonist muscle indicates that the muscle is severely denervated (10, 12, 15). Surface electrical stimulation is generally performed at least 6 months after injury, after the patient is neurologically stable (15). After a complete evaluation, one can map the muscles and discern three types of the following (15): (i) functional muscles (innervated by supralesional segment); (ii) paralyzed and denervated muscles (innervated by injured metamere, with damage to LMN); and (iii) paralyzed but innervated muscles (innervated by infralesional segment, with preserved LMN). The boundaries between these three zones are not always clear-cut but are often present with transition zones of muscles that are partially denervated (15). Before contemplating nerve transfer, the clinician needs to decide what is the primary function that needs to be restored. This decision depends on the patient’s level of injury. The first priority is the restoration of elbow extension (25). Pinch restoration is the next most crucial hand function. For activities of daily living, more tasks are performed with side pinch rather than grasp (25). The next priority is restoration

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of grasp and release. In the context of nerve transfers, it is possible to obtain multiple functions such as pinch and grasp in a single procedure. It is possible to reconstruct the entire upper extremity functional elements as outlined earlier in a singlestage procedure. The donor muscle chosen should be of adequate strength (at least MRC grade 4) to avoid significant downgrading of its function. The donor nerve should be in proximity to the recipient nerve to obviate the necessity of intervening nerve graft, increasing the success rate. Distal nerve transfer might have a better result than a proximal transfer because of less time needed for the growing axons to reach the muscle, ensuring prompt reinnervation before permanent muscle damage occurs from chronic denervation. Before surgery, a subsequent fallback procedure (e.g., musculotendinous transfers) should also be considered in case the nerve transfer fails to achieve functional results. Whenever possible, the nerve sacrificed for transfer should not eliminate the options for fallback procedures. INTRAOPERATIVE CONSIDERATIONS Electrostimulation is critical during the nerve transfer procedure and includes direct nerve stimulation and intraoperative motor evoked potentials (transcranial stimulation) to confirm effective cortical activation (9). Transcranial stimulation is noteworthy because paralyzed muscles of the infralesional segment still respond with direct nerve stimulation but show no response on transcranial stimulation (9). It is especially indispensable in a case with a thin or small area of injured metamere segment and unclear boundary between the muscles with intact cortical connection (supralesional segment) and muscles with intact innervation but no cortical connection (infralesional segment). A bipolar nerve stimulator is preferred over a monopolar one to minimize current spreading (9). The lowest current, slightly above the stimulation threshold, should be used for the same reason. Q 3 Response can be evaluated by seeing actual muscle contraction, augmented by electromyography if necessary. The intact innervation of the infralesional segment provides an additional advantage by enabling intraoperative confirmation of targeted distal muscle (9, 34). General principles of nerve repair also apply here. Tension at the repair

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site should always be avoided. Donor nerve is divided as distal as possible, and recipient nerve should be divided as proximal as possible to achieve tension-free nerve coaptation. Nerve coaptation is performed using 8-0/9-0 nylon epineural suture, enforced with fibrin glue (38). ELBOW EXTENSION About two thirds of cervical spine injuries involve the C5 vertebra, typically with injury of the C6-C7 spinal cord (7, 28, 53). A patient with this injury often is left with generally preserved shoulder function and elbow flexion. In most cases (82%), wrist extension is largely preserved (53). Elbow extension is absent or weak. Hand functions are also absent or extremely weak. Restoration of elbow extension is an integral part of upper extremity reconstruction because recovery of this function improves elbow stability, ability to perform pressure relief maneuvers, ability to perform manual wheelchair propulsion, ability to reach objects above shoulder level, and ability for self-transfers (4, 7, 20, 25). The procedure commonly used to restore elbow extension is transfer of posterior deltoid or biceps muscle to triceps (20, 25). However, most patients who have undergone these procedures regained only antigravity muscle strength (7). A more recent anatomic study in cadavers by Bertelli et al. (7) observed the feasibility of using the teres minor motor branch and posterior deltoid motor branch of the axillary nerve to reinnervate the triceps motor branch and thoracodorsal nerve. This study showed that the nerves could be transferred in a tension-free fashion via a transaxillary approach. The size match was reasonable, and the nerves had little variation in the number of myelinated fibers. In C6 SCI, some of the motor neurons going to the teres minor and deltoid might have been lost, and the number of motor axons in the donor nerve was potentially reduced. Nevertheless, the authors contended that this loss does not preclude the potential for successful reinnervation because only 20%e30% reinnervation is necessary to gain functional motor strength (7, 17). Bertelli et al. (4) followed this study with a case report of bilateral teres minor motor branch transfers to the long head of triceps motor branch in a tetraplegic patient with absent triceps function 9 months after the injury. The patient recovered MRC grade 4 elbow extension 14

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months after the surgery. The authors pointed out the benefits of using the teres minor motor branch as donor nerve in such a case. Teres minor muscle denervation typically does not result in significant deficit because the infraspinatus muscle compensates for any deficit in external rotation. The teres minor muscle itself is not used as donor muscle in tendon transfer for tetraplegic patients. Sacrificing the teres minor motor branch does not eliminate the option for later tendon transfers of biceps or posterior deltoid muscle to triceps tendon to enhance elbow extension if the nerve transfer procedure yields only partial recovery or as rescue procedure in a case of total failure (4). The use of the posterior deltoid motor branch for donor nerve should be considered carefully (7). Denervation of the posterior deltoid muscle would preclude its availability for transfer to the triceps tendon. Although the biceps is still available for transfer to triceps, biceps transfer to triceps eliminates the potential for the supinator motor branch to the posterior interosseous nerve (PIN) transfer for thumb and fingers extension because arm supination is compromised if both the biceps and the supinator are sacrificed. The challenge of using the teres minor motor branch for a donor is the difficulty in clinically testing the strength of this muscle before surgery (4). Brown (9) reported a case of cervical SCI with weak elbow extension and wrist and finger flexor and extensor. The axillary nerve fascicles were used as donor nerve to reconstruct the elbow extensor and wrist and finger extensors. The nerve was explored and separated into five main fascicles. Three of the fascicles contributed to global deltoid contraction, and the remaining two provided contraction primarily from the posterior deltoid. Two fascicles were taken—one that gave global deltoid contraction and one that provided posterior deltoid contraction. The fascicles were transferred to two radial nerve fascicles. One fascicle primarily produced wrist and finger extension, and the other fascicle produced elbow extension. The result of the surgery was not mentioned, so we recommend great caution in considering this specific approach. PINCH (THUMB OPPOSITION) AND GRASP (FINGER FLEXION) The primary goal of reconstruction in the hands of a tetraplegic patient is the

restoration of ability to pinch using the thumb and the lateral side of the index finger, as in holding a key (8). In the 1940s, flexor tenodesis of the thumb and finger flexors was recommended by Bunnel to reconstruct pinch ability; however, this procedure never found favor because of the complexity of controlling the many joints of the thumb and fingers (47, 50). Moberg was the first to observe that a useful pinch can be obtained by a much simpler method (50). Rather than reconstructing pinch between the tips of the thumb and fingers, which requires a complex reconstruction procedure and precise control of the position of the fingers, Moberg demonstrated that a functional pinch between the thumb and the side of the index finger could be easily achieved by simply anchoring the FPL tendon to the distal radius. A side pinch does not require precise control of position of the fingers because any point at the side of the index finger is adequate for thumb opposition. However, the Moberg key-pinch procedure is a passive tenodesis, in which side pinch is achieved through active wrist extension; this eliminates a degree of freedom of hand placement and precision because wrist extension is required to perform a side pinch. An alternative to the Moberg procedure is brachioradialis tendon transfer to the FPL, which is now more commonly used (50). Bertelli et al. (8) proposed a procedure to reconstruct thumb pinch by transferring the distal terminal motor branch of the ECRB to the FPL motor branch. Their anatomic study showed that the ECRB motor branch sends collaterals to the muscle before its final branching at almost inside the muscle. Both the distal ECRB motor branch and the FPL motor branch had similar diameter (approximately 1 mm) and numbers of myelinated axons (approximately 180). Bertelli et al. (8) reported a case of a 24-year-old tetraplegic man with preserved motion in his shoulder, elbow, wrist, and finger extension but paralyzed thumb and finger flexion. Surgery was performed 7 months after the injury to transfer the distal motor branch of the ECRB to the FPL motor branch and brachialis muscle with a tendon graft to the FDP. At 14 months after surgery, pinching and grasping were restored and measured 2 kg and 8 kg strength. The authors highlighted the importance of using the distal motor branch to the ECRB and preserving the proximal branches, instead of taking the

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entire nerve. Wrist extension is often not normal in tetraplegics, and complete denervation should be avoided. An alternative to the above-mentioned procedures for reconstruction of thumb and finger flexion is transfer of the brachialis motor branch of the musculocutaneous nerve to the anterior interosseous nerve (AIN) fascicle of the median nerve at arm level (9, 11). This procedure requires internal neurolysis of the median nerve at arm level and identification of the target fascicle that predominantly provides thumb and finger flexion. With the knowledge of fascicular anatomy and the aid of a direct nerve stimulator, fascicular identification is possible without the necessity of exposing the AIN distally and then dissecting its fascicle from the main median nerve trunk proximally. The advantage of intact LMN innervation in the target muscle is highlighted; intact innervation provides relative ease in identifying recipient nerve, as opposed to surgery for peripheral nerve injury. Mackinnon et al. (34) described a case in which they transferred the brachialis motor branch to the AIN motor fascicle in a 71-year-old man with complete C7 SCI 23 months after the injury. At 15 months after surgery, the patient achieved MRC grade 3 for the FPL and FDP, leading to the ability for self-feeding and rudimentary writing. Another option is using the ECRB motor branch or supinator motor branch as donor nerve for transfer to the AIN (11, 21). Hsiao et al. (21) reported a case with severe high median nerve injury from a displaced proximal humerus neck fracture. Treatment was performed 5 months after the injury with transfers of the supinator branch of the radial nerve to the AIN and ECRB motor branch of the radial nerve to the pronator teres motor branch of the median nerve. The FPL and FDP showed evidence of reinnervation 8 months after surgery. At 1-year follow-up, grip strength was 11 lb, and pinch strength was 5 lb. This result is comparable to the result achieved by Bertelli et al. However, care should be taken when using the supinator motor branch as donor nerve in tetraplegics with weakness in the thumb and finger extension because this nerve is also a potential donor for reconstruction of these functions, as discussed subsequently.

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THUMB AND FINGER EXTENSION In a C6-C7 SCI, hand functions including finger and thumb extension are severely impaired. Finger extension is required for object acquisition and object release (25). Common orthopedic procedures to reanimate finger extension have not yielded satisfactory results (5). In this type of injury, the supinator muscle (C5-6) is usually of normal strength. A study in cadavers by Bertelli et al. (5) explored the feasibility of transferring the supinator motor branches to the PIN to restore thumb and finger extension. This study showed that before or at the level of the arcade of Fröhse, two main motor branches to the supinator muscle arose from the PIN to innervate the deep and superficial heads of the supinator. The total number of myelinated axons of both supinator motor branches combined corresponded to 73% of the number of myelinated axons within the PIN (approximately 745). Both supinator motor branches can be coapted directly to the PIN in a tension-free fashion and roughly corresponded to 80% of PIN diameter. Bertelli et al. (6) performed this procedure in a tetraplegic patient who had bilateral paralysis of thumb and finger extension 7 months after the injury. There was almost full extension of the thumb and finger 6 months after surgery. This result showed that supinator motor branch transfer is a promising alternative for the reconstruction of thumb and finger extension. Sacrificing the supinator motor branches for donor nerve does not result in weakness in supination. The biceps, usually preserved in C6-C7 SCI, is a strong supinator and compensates for the loss of supinator muscle function (3, 5). Brown (9) reported transfer of the axillary nerve fascicle to the radial nerve fascicle that mainly provides wrist and finger extension; however, this was a “proximal” nerve transfer, which inevitably requires a longer time for the regenerative axons to reach the target muscle compared with the transfer described by Bertelli. Palazzi et al. (40) reported a single case of C7-T1 avulsion injury with absent finger and thumb extension. Nerve transfer using the brachialis motor branch to the PIN employing 3 cm  9 cm interpositional nerve grafts was performed 4 months after the injury.

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The long finger extensors reached MRC grade 3 10 months after surgery, but there was only a flicker of contraction of the thumb extensor. The poor result for reinnervation of the thumb extensor in this case might have been related to the use of long interpositional nerve grafts.

NERVE TRANSFERS FOR DIAPHRAGM REANIMATION Patients who sustain high cervical cord injury usually have respiratory insufficiency requiring long-term positive pressure mechanical ventilation, with associated high morbidity secondary to various pulmonary complications (26, 27). An alternative to positive pressure mechanical ventilation is electrophrenic respiration, also known as “diaphragmatic pacing,” a method of pacing the phrenic nerve to effect diaphragm contraction. However, this method cannot work if the injury involves the C3-5 level with subsequent loss of the motor neuron pool associated with the phrenic nerve (27). Krieger et al. (26, 27) successfully described a procedure to reinnervate the diaphragm by transferring intercostal nerve to phrenic nerve for later implementation of diaphragmatic pacing. The phrenic nerve within the thoracic cavity is exposed with a posterolateral thoracotomy through the T5 interspace. After confirmation of diaphragm paralysis by direct electrical stimulation, the phrenic nerve is sectioned 5 cm proximal to its insertion into the diaphragm. The fourth intercostal nerve was chosen as donor nerve because of its proximity to the phrenic nerve, its similar function to the phrenic nerve (involved in respiratory function), and its good size match. The pacemaker’s monopolar electrode is applied to the phrenic nerve 1 cm distal to the coaptation site, and the receiver is placed in a subcutaneous pocket on the anterior chest wall. The pacemaker is activated 3 months after the procedure, and the diaphragm is evaluated weekly for responsiveness. This evaluation is repeated until the patient is noted to have sustained diaphragmatic activity. There were 10 intercostal to phrenic nerve transfers performed in six patients (27), with the interval from injury to nerve transfer ranging from 6 months to 3 years. The average interval from surgery to diaphragm response to electrical

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stimulation was 9 months. At the time of publication, 8 of 10 transfers had enough time for axonal regeneration, and all 8 were able to tolerate diaphragmatic pacing as an alternative to positive pressure ventilation, as judged by end-tidal carbon dioxide values, tidal volume, and patient comfort. No specific details were given regarding the actual value of the tidal volume and evidence of diaphragmatic excursion with stimulation. Tubbs et al. (48) described an anatomic feasibility study of transferring spinal accessory nerve to phrenic nerve. These authors argued that the spinal accessory nerve is a better donor for diaphragm reinnervation because theoretically with successful reinnervation it allows voluntary control of the diaphragm and obviates the need for diaphragmatic pacing with its associated complications. Technically, the procedure is easier to perform and obviates the need for thoracotomy and its related morbidity. However, with high cervical cord injury, the viability of the spinal accessory nerve is questionable because its motor neuron pool at the upper cervical cord and as low as C6 level might also be affected by the injury. NERVE TRANSFERS FOR PARAPLEGIA Nerve transfers for the lower extremity are far less common compared with nerve transfers for the upper extremity, owing to the limited availability of donor nerves. Attempts to reanimate lower extremities using intercostal nerve to the lumbosacral plexus have been reported by a few authors with various results. Patil (41) reported a single case of compression fracture of the first and second lumbar vertebral bodies resulting in complete paraplegia. The patient was treated subacutely with posterior spinal stabilization in conjunction with nerve transfer using bilateral T8 and T9 intercostal nerves to anterior nerve roots of L2 (identified at its exits) and two motor nerve roots that produced plantar flexion with direct nerve stimulation (presumably S1 motor nerve roots). The target of the surgery was to reinnervate the hip flexor and extensors; however, the result of the surgery was not reported. Zhang et al. (54) reported the use of two to four intercostal nerves above the level of injury for transfer to motor nerve roots of L1-2 or L3-4, which resulted in the ability to step forward and

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walk with crutches in 18 of 23 patients. Mean postoperative follow-up was 3.5 years. An anatomic feasibility study for transferring T9-T10 intercostal nerves to the femoral nerve has also been described (29). Brunelli and Brunelli (14) reported transfer of the entire ulnar nerve to reinnervate the gluteus maximus, gluteus medius, and quadriceps femoris in three patients with T8-T11 SCI. This particular subset of patients was chosen because an injury above the T8 level hinders the paravertebral and abdominal muscles, which are crucial for walking. An injury below T11 produces flaccid paralysis and atrophy of the target muscles. The targeted muscles were gluteus maximus, which is important for hip extension; gluteus medius for stabilization of the pelvis in the frontal plane; and quadriceps femoris for hip flexion and knee extension. The ulnar nerve was chosen as donor nerve because it is the longest in the upper limb and can reach the glutei without the use of interpositional nerve graft. In addition, ulnar nerve palsy can be managed with a classic musculotendinous reconstructive procedure. The full length and circumference of the ulnar nerve and its motor branches were elevated from the hand region all the way to the axilla and then tunneled subcutaneously to the lateral aspect of the trunk and coapted directly to the nerves of the gluteus maximus and gluteus medius, with an interpositional graft to the femoral nerve. Although evidence of reinnervation was documented with electromyography in the target muscles, only one patient attained rudimentary walking capacity, and the other two were still stated to be in the recovery period, so we would deem these heroic transfers as highly experimental. One potentially life-threatening complication of paraplegia is the development of pressure sore. Although musculocutaneous flaps can achieve closure of pressure sores, the lack of sensation of this flaps often leads to recurrent ulceration (35). Attempts have been made to restore sensory innervation to pressure-bearing areas in paraplegics. Hauge (19) demonstrated the feasibility of using various intercostal nerves to reinnervate the sensory nerve to the skin covering the ischial tuberosity and the motor nerve to the gluteus maximus. The author believed that reinnervation of gluteus maximus is important to improve blood flow and diminish ischemia. Other clinical studies

described transfer of intercostal nerves for sensory innervation of plantar fillet free flap (16) or medial gastrocnemius free flap (23). Mackinnon et al. (35) described a procedure to reinnervate the territory of the lateral femoral cutaneous nerve using the medial antebrachial cutaneous nerve (MABCN) as a donor in a 21-year-old paraplegic, who was plagued by multiple trochanteric and ischial pressure sores. The first procedure to transfer the MABCN was carried out 3 years after the injury. The MABCN was identified from its branching point from the medial cord to just distal to the elbow, transected distally, and tunneled underneath the anterior abdominal wall. The lateral femoral cutaneous nerve was divided near its origin at the spinal foramen and brought up into the subcutaneous tissue of the anterior abdominal wall. The MABCN was coapted to the lateral femoral cutaneous nerve using sural nerve grafts. Sensory reinnervation occurred within 19e20 months, after which a musculocutaneous flap was rotated to cover the pressure sore area. At 4-year follow-up, the patient was able to perceive light touch, pressure, and vibration, all referred to the MABCN distribution (33). The flaps remained well healed. A biopsy specimen of the reinnervated skin showed nerve fibers in proximity to a hair follicle. This finding is definitive evidence that the nerve fibers grew into the skin and found their appropriate receptor. NERVE TRANSFERS FOR BLADDER REINNERVATION Neurogenic bladder dysfunction after SCI imposes severe lifelong impairment on patients (37). It is a major contributor to the morbidity and mortality of SCI. With restoration of bladder function, patients can gain independence from present methods of bladder emptying, be free from associated medical complications, and enjoy an improvement in their quality of life (32). The pioneering work of using nerve transfer to bypass the area of spinal cord damage and reinnervate the bladder was first conceptualized in 1907, as reviewed by Vorstman et al. (49) in the mid-1980s. The landmark study in rats by Xiao and Godec (51) in 1994 confirmed that the efferent of a somatic reflex arc could regenerate into the parasympathetic efferent to the bladder. They successfully transferred the L4 ventral

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root (VR) to L6 VR. After allowing adequate time for axonal regeneration, they were able to elicit detrusor contraction by L4 VR electrical stimulation. Stimulation of distal sciatic nerve or scratching at the L4 dermatome produced detrusor contraction as well. An explanation for this phenomenon is that the nerve transfer created a new reflex arc, the so-called skin-CNS-bladder reflex, which uses cutaneous efferent signal to trigger the micturition. Xiao et al. (52) followed this work with a trial of nerve transfer from the L5 VR to S2-S3 VR in 15 patients with hyperreflexic neurogenic bladder and detrusoreexternal sphincter dyssynergia secondary to complete suprasacral SCI. Mean follow-up was 3 years. Bladder function was recovered in 10 of 15 patients, as assessed by urodynamic parameters. Similar to the animal model, stimulation of the L5 dermatome elicited the skin-CNS-bladder reflex, causing micturition. In 2009, Lin et al. (30) reported a similar study by unilaterally transferring the S1 VR to S2-S3 VR in 12 patients with hyperreflexic neurogenic bladder and detrusoreexternal sphincter dyssynergia secondary to complete suprasacral SCI. At 12 months after surgery, 9 of 12 patients had significant improvement in bladder capacity and post-voiding residual volume. Stimulation for micturition was performed by percussing the Achilles tendon. In conus medullary injury with atonic bladder, the aforementioned procedure would not work because the L5 and S1 segments are also damaged by the injury. Livshits et al. (32) reported 11 patients with conus medullary syndrome secondary to L1 level injury who underwent transfers of two lower thoracic intercostal nerves to proximal intradural S2-S3 nerve roots. After a 12-month follow-up, the authors reported that all patients exhibited reflex voiding ability, whereas several urodynamic parameters were significantly improved. Lin et al. (31) reported a series of 10 paraplegics with traumatic lesion of the conus medullaris where the T11 VR above the lesion was transferred to the S2 VR unilaterally through a 30-cm nerve graft. The T11 dorsal root was left intact as the trigger of micturition after axonal regeneration. The mean duration of injury before surgery was 8.7 months. Of 10 patients, 7 regained satisfactory bladder control and attained significant improvement in their urodynamic parameters

NERVE TRANSFER STRATEGIES FOR SCI

within 18e24 months after surgery. These patients voided by stimulating the skinCNS-bladder reflex (scratching or gently squeezing the T11 dermatome). This reflex became functional around 18 months postoperatively. More recent experiments, such as the ones by Ruggieri et al. (43e45), have demonstrated the feasibility of using several motor donors, such as intercostal, coccygeal, and genitofemoral nerves, directing them to sacral nerve roots or more distally to pelvic nerve recipients to reinnervate the canine bladder successfully. CONCLUSIONS Nerve transfer is a viable option for restoration of critical upper limb function in SCI, which potentially improves independence. Although the use of this technique for SCI is still in its infancy, it offers several advantages over the traditionally used tendon transfer. Nerve transfer does not require prolonged immobilization; it provides greater functional gain for a given transfer; and reconstruction of several facets of upper limb function, which is highly useful, can potentially be performed in a single stage. Nerve transfer also has a limited role for diaphragm reanimation and bladder reinnervation in select circumstances. The use of nerve transfers in very select cases of paraplegia for sensory reinnervation to prevent recurrent pressure sores seems reasonable, but nerve transfer for motor control of locomotion in paraplegics remains very experimental. The merits of nerve transfer warrant further study to evaluate its value for SCI in humans. REFERENCES 1. Addas BM, Midha R: Nerve transfers for severe nerve injury. Neurosurg Clin N Am 20:27-38, 2009: vi. 2. Anderson KD, Friden J, Lieber RL: Acceptable benefits and risks associated with surgically improving arm function in individuals living with cervical spinal cord injury. Spinal Cord 47:334-338, 2009. 3. Bertelli JA, Ghizoni MF: Transfer of supinator motor branches to the posterior interosseous nerve in C7-T1 brachial plexus palsy: case report. J Neurosurg 113:129-132, 2010. 4. Bertelli JA, Ghizoni MF, Tacca CP: Transfer of the teres minor motor branch for triceps reinnervation in tetraplegia. J Neurosurg 114:1457-1460, 2011.

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5. Bertelli JA, Kechele PR, Santos MA, Besen BA, Duarte H: Anatomical feasibility of transferring supinator motor branches to the posterior interosseous nerve in C7-T1 brachial plexus palsies: laboratory investigation. J Neurosurg 111:326-331, 2009. 6. Bertelli JA, Tacca CP, Ghizoni MF, Kechele PR, Santos MA: Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report. J Hand Surg Am 35:1647-1651, 2010. 7. Bertelli JA, Tacca CP, Duarte ECW, Ghizoni MF, Duarte H: Transfer of axillary nerve branches to reconstruct elbow extension in tetraplegics: a laboratory investigation of surgical feasibility. Microsurgery 31:376-381, 2011. 8. Bertelli JA, Lehm VLM, Tacca CP, Duarte ECW, Ghizoni MF, Duarte H: Transfer of the distal terminal motor branch of the extensor carpi radialis brevis to the nerve of the flexor pollicis longus: an anatomic study and clinical application in a tetraplegic patient. Neurosurgery 70: 1011-1016, 2012. 9. Brown JM: Nerve transfers in tetraplegia I: background and technique. Surg Neurol Int 2:121, 2011. 10. Brown JM: The reconstructive neurosurgery of spinal cord injury. In: Dimitrijevic MR, Kakulas BA, McKay WB, Vrbova G, eds. Restorative Neurology of Spinal Cord Injury. New York: Oxford University Press; 2012:134-168. 11. Brown JM, Mackinnon SE: Nerve transfers in the forearm and hand. Hand Clin 24:319-340, 2008:v. 12. Brown JM, Vivio N, Sheean GL: The clinical practice of reconstructive neurosurgery. Clin Neurol Neurosurg 114:506-514, 2012. 13. Brunelli G, Brunelli F: Partial selective denervation in spastic palsies (hyponeurotization). Microsurgery 4:221-224, 1983. 14. Brunelli GA, Brunelli GR: Restoration of walking in paraplegia by transferring the ulnar nerve to the hip: a report on the first patient. Microsurgery 19: 223-226, 1999. 15. Coulet B, Allieu Y, Chammas M: Injured metamere and functional surgery of the tetraplegic Q4 upper limb. Hand Clin 18:399-412, 2002:vi. 16. Goldberg JA, Barwick WJ, Levin LS: Restoration of sensation in paraplegia by a sensory innervated plantar fillet free flap: case report. Paraplegia 33: 116-119, 1995. 17. Gordon T, Yang JF, Ayer K, Stein RB, Tyreman N: Recovery potential of muscle after partial denervation: a comparison between rats and humans. Brain Res Bull 30(3-4):477-482, 1993. 18. Guelinckx PJ, Faulkner JA, Essig DA: Neurovascular-anastomosed muscle grafts in rabbits: functional deficits result from tendon repair. Muscle Nerve 11:745-751, 1988. 19. Hauge EN: The anatomical basis of a new method for re-innervation of the gluteal region in paraplegics. Acta Physiol Scand Suppl 603:19-21, 1991.

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Conflict of interest statement: F. Senjaya carried out this review during a peripheral nerve surgery fellowship at the University of Calgary. The fellowship is partially supported by a grant from Integra Foundation. Received 30 May 2012; accepted 2 October 2012 Citation: World Neurosurg. (2012) . http://dx.doi.org/10.1016/j.wneu.2012.10.001 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2012 Elsevier Inc. All rights reserved.

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