Acta Neurochirurgica https://doi.org/10.1007/s00701-018-3671-0 CASE REPORT - PERIPHERAL NERVES Double nerve transfer for restoration of hand grasp and release in C7 tetraplegia following complete cervical spinal cord injury Mohammadreza Emamhadi 1 & Sasan Andalib 2,3 Received: 19 August 2018 / Accepted: 31 August 2018 # Springer-Verlag GmbH Austria, part of Springer Nature 2018 Abstract Cervical spinal cord injury (SCI) can cause tetraplegia. Nerve transfer has been routinely utilized for reconstruction of hand in brachial plexus injuries. Here, we report reconstruction of finger flexion (hand grasp) and extension (hand release) in a victim of cervical spinal cord injury with tetraplegia. We also focus on importance of extension phase in restoration of hand function in the tetraplegic case, in addition to provision of a detailed description of both operations including text, photographs, and a video. We used double nerve transfer, namely brachialis branches of musculocutaneous nerve to anterior interosseous nerve (AIN) and supinator branch of radial nerve to posterior interosseous nerve (PIN). We found that brachialis nerve transfer to AIN (for finger flexion) and supinator branch nerve transfer to PIN (for finger extension) can provide finger flexion and extension simultaneously. Brachialis nerve transfer to AIN and supinator branch nerve transfer to PIN may be an acceptable surgical technique to restore hand grasp and release in tetraplegia after SCI. Keywords Tetraplegia . Nerve transfer . Neurotization Introduction Cervical spinal cord injury (SCI) may lead to tetraplegia. The upper extremity dysfunctions in tetraplegic patients impair daily living activities such as eating, personal hygiene, and self-protection. Hand function is even of higher importance than walking, bowel and bladder control, and sexual function in these patients. Thus, restoration of some hand function can indeed improve quality of the life of tetraplegic patients. This article is part of the Topical Collection on Peripheral Nerves Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00701-018-3671-0) contains supplementary material, which is available to authorized users. * Mohammadreza Emamhadi mr.emamhadi@gmail.com 1 Brachial Plexus and Peripheral Nerve Injury Center, Guilan University of Medical Sciences, Rasht, Iran 2 Neuroscience Research Center, Poursina Hospital, Guilan University of Medical Sciences, Rasht, Iran 3 Department of Neurosurgery, Poursina Hospital, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran Surgical techniques such as tendon transfers, nerve grafts, and nerve transfers may restore some motor functions [9]. Tendon transfers aiming to regain active wrist extension and thumb flexion have yielded clear benefits in tetraplegia resulting from cervical cord injury. Nerve transfers offer new options of pain, motor, and sensory recoveries [7, 8, 10]. In comparison with tendon transfers, nerve transfers provide a better functional outcome as they are less invasive, maintain the original anatomy and biomechanics of the upper limb, do not require prolonged immobilization, and offer functional improvement even when no tendon transfer options are available. Moreover, they may restore multiple functions with sacrifice of only one donor nerve. Initially applied in cases of brachial plexus injuries, these techniques have provided rewarding functional outcomes never hoped before [16]. The basic functional movements such as lateral thumb pinch (key pinch), finger flexion (hand grasp), and finger extension (hand release) are considered necessary for tetraplegic patients. If the abovementioned movements in combination with elbow extension are regained, the patient’s independency is remarkably increased. It should also be emphasized that in tetraplegia, careful evaluation of the donors is an absolute prerequisite of nerve transfer and this procedure is contraindicated when the muscle is innervated by a donor nerve scoring less than M4. Acta Neurochir A few published reports have so far confirmed nerve transfer in tetraplegic upper extremity [1, 4–6, 15]; albeit, there exists only one single report concerning hand reconstruction for both grasp and release phases [17]. Here, we report a case of complete cervical SCI with tetraplegia undergoing transfer of brachialis branch of musculocutaneous nerve to anterior interosseous nerve (AIN) for finger flexion and supinator branch nerve to posterior interosseous nerve (PIN) for finger extension. Cervical SCIs of C5 or below are normally candidates for the procedure since there are intact musculocutaneous and axillary nerves to be used as donors. Clinical presentation A 30-year-old right-handed male patient was referred to our center. The patient had a motorcycle accident with C6 burst fracture leading to tetraplegia and undergone C6 corpectomy and C5C7 stabilization 12 months before admission to our center. Our aim was to provide functional improvement in his hand. Preoperative clinical evaluation and electrodiagnostic tests According to the Medical Research Council (MRC) [14], on motor examination, both trapezius muscles scored M5; biceps/brachialis, deltoid, and brachioradialis muscles were M4 bilaterally. Triceps strength was M4 and M3 on the right and left side, respectively, and pronation of forearms scored M4. Wrist extension was M4 bilaterally and wrist flexion scored M4 on the right side and M3 on the left side. Supinator muscles scored M4. Finger and thumb extensors and flexors were M0 and the right thumb was flexed into the palm (Fig. 1). No spasticity was observed in the involved muscles. According to the clinical examination, the patient was classified in group 5 of the international classification of surgery of the hand in tetraplegia [11] in the right side (Video 1) and group 4 in the left side. Fig. 1 Preoperative clinical examination showing that finger and thumb extensors and flexors were completely paralyzed and right thumb was flexed into the palm Preoperative electromyography of brachialis and supinator muscles showed a relatively normal recruitment. Fibrillations were observed in the nerve transfer target muscles, but no voluntary activity was confirmed. Indication of surgery was given, planning to perform a brachialis branch to AIN transfer to restore finger flexion [6], and supinator branch to PIN transfer to regain finger extension [15] on the right upper limb. Surgical technique Double nerve transfer included tranbrachialis branch of musculocutaneous nerve to AIN for finger flexion (Figs. 2 and 3) and supinator branch nerve to PIN for finger extension (Fig. 4). Nerve surgery was carried out under general anesthesia without muscle relaxation agent aiming to restore function on the right upper limb. The patient was supine with his right arm abducted, supinated, and placed on an arm board. A vertical incision on the medial surface of the arm allowed exposure and identification of the musculocutaneous nerve and its branches to the biceps and brachialis muscles. The brachialis branch (donor nerve) was isolated with a vessel loop. Exploration of the right median nerve was performed via an S-shaped incision on the volar surface of forearm. The median nerve was identified proximal to the lacertus fibrosus and its course was followed between the two heads of the pronator teres. Then, the AIN (recipient) was identified and its course was followed proximally. A vessel loop was used to isolate it. Response in flexor pollicis longus muscle was confirmed by using intraoperative electrostimulation. The brachialis nerve and AIN were sharply severed and under microscope, a tension-free nerve coaptation between these nerves was made by 9–0 epineural sutures (Fig. 2). Then, the forearm was placed prone on the surgical table. A 10-cm-long incision was made on the proximal third dorsal side of the forearm and the supinator muscle exposed by laterally displacing the extensor carpi radialis brevis muscle and extensor digitorum communis muscle. The superficial portion of supinator muscle was divided in order to expose the PIN and the motor branches of the supinator muscle. The function of supinator muscle was confirmed by neurostimulatation. Contraction of the extensor digitorum communis, extensor carpi ulnaris, extensors of the thumb, and index muscles could be assessed on electric stimulation of PIN. The contraction appeared as in upper motor neuron paralyzed muscles, because the connection between muscles and spinal cord is often intact; hence, the muscles below injury are kept alive. Then, supinator branches were distally cut and the PIN was proximally sectioned (Fig. 3). A tension-free coaptation was done with 9–0 mononylon sutures under microscope. The Acta Neurochir Fig. 2 Intrafascicular dissection of the median nerve at arm level to explore AIN subcutaneous tissue was finally approximated and the skin was sutured. Postoperative management Immobilization of the forearm and the elbow (the wrist and the forearm in neutral and the elbow flexed to 90°) in a splint was done for 4 weeks. Once the splint was removed, the patient was neurologically re-evaluated and no additional functional deficit was detected. In particular, postoperative elbow flexion force was unchanged. A month after the surgery, for motor reeducation, a hand therapist commenced physiotherapy and aided the patient with exercising passive flexion of the fingers and the thumb coinciding with elbow flexion, and also passive extension of the fingers and the thumb concurrently with forearm supination. Following motor reeducation (due to brain neuroplasticity) and reinnervation of the target muscles, the patient regained flexion and extension of the fingers and the thumb as natural voluntary actions. Follow-up and surgical outcome Neurological follow-up was carried out every month lasting for 20 months after surgery. Electrophysiological follow-up was done every 2 months starting 6 months after surgery. Postoperative electrodiagnostic tests showed early reinnervation of the extensors 6 months after surgery whereas the reinnervation was detected 8 months after the procedure in the flexors. In the following 2 months, flexor pollicis longus and flexor digitorum profundus also showed initial signs of recovery. Nine months after the surgery, finger extension was seen by supination of the forearm. The patient recovered flexor pollicis longus and first- and second-digit flexor digitorum profundus scoring M3 15 months after the surgery. The patient finally achieved M4 on thumb and finger flexion, M3 on thumb extension, and M4 on finger extension and became able to pick up object and feed himself with his right hand 20 months after surgery (Video 1 and Figs. 4, 5 and 6). Fig. 3 Transfer of brachialis branch of musculocutaneous nerve to AIN for finger flexion Acta Neurochir Fig. 6 Follow-up examination: the patient became able to feed himself with his right hand Fig. 4 Supinator branches were cut distally and the PIN was sectioned proximally Given the favorable results on the right upper extremity, nerve transfers were then performed on the left upper extremity wherein follow-up is still in progress. Discussion In tetraplegic patients, the main goals of nerve reconstruction are to restore elbow extension, wrist extension, finger flexion, finger extension, and intrinsic hand function. A few published reports have so far confirmed nerve transfer in tetraplegic upper extremity [1, 4–6, 15]; albeit, there exists only one Fig. 5 Right-hand grip reconstruction (a grasp phase, b release phase) single report concerning hand reconstruction of both finger flexion and extension [17]. Friden et al. [12] reported nerve transfer to regain wrist extension in a subject with C5 tetraplegia. He transferred brachialis muscle branch of the musculocutaneous nerve to the extensor carpi radialis longus muscle branch of the radial nerve, achieving active wrist extension. Bertelli et al. [5] could restore only finger and thumb extension by transferring the supinator motor branch to the PIN in a case of complete C6 SCI with preoperatively intact function in the brachioradialis, radial wrist extensors, and supinator muscles and elsewhere, Bertelli et al. [4] carried out a transfer of the teres minor nerve branch of axillary nerve to long head of triceps nerve branch to restore elbow extension in a C6 tetraplegic patient. Fourteen months after the procedure, the patient achieved a M4 triceps. In seven tetraplegic patients, Bertelli et al. [2] utilized one of axillary nerve division to reinnervate the triceps long and upper medial head motor branches in 13 patients and transfer of the nerve to the supinator to the PIN was carried out to reconstruct thumb and finger extension. Consequently, after followup of 19 months, elbow extension force scored M4 in most of patients. Thumb extension scored M4 in 8 upper limbs and finger extension scored M4 in 12 hands. In the abovementioned papers, the authors did not perform a nerve transfer to restore finger flexion. However, Bertelli et al. [1] later reported a tetraplegic case undergoing nerve transfers for elbow extension and thumb and finger extension, but they carried out a tendon transfer for finger flexion. He transferred tendon of brachioradialis to the flexor pollicis longus and flexor digitorum superficialis for the index finger flexion. On the other hand, there are reports of nerve transfer for restoration of thumb and finger flexion without reconstruction of finger extension. Bertelli et al. [3] attempted to restore only finger flexion in a tetraplegic case by transferring nerve to the brachialis or brachioradialis or extensor carpi radialis brevis (ECRB) to AIN and concluded that nerve to ECRB is a better donor than the other two nerves. Mackinnon et al. [15] Acta Neurochir reported a single case of C7 cervical SCI undergoing restoration of finger and thumb flexion following brachialis branch to AIN transfer. The authors reported that flexor pollicis longus and flexor digitorum profundus showed M3 muscle force 15 months after the surgery. Hawasli et al. [13] reported a 21-year-old male subject with complete C7 tetraplegia. The patient underwent brachialis muscle branch to AIN transfer and showed precocious reinnervation within 3 months after the procedure with M2-M3 in the first- and second-digit flexor digitorum profundus and flexor pollicis longus. A few reports have been dedicated to both phases (flexion and extension) of hand reconstruction. Brown [6] performed brachialis branch of musculocutaneous transfer to the median fascicle and restored wrist and finger flexion to allow pinch and grasp and also transferred donor fascicles from the axillary nerve to recipient fascicles of the radial nerve, one corresponding to wrist and finger extension and the other corresponding to elbow extension via triceps function. Although he did not report any results, it appears that use of a recipient in proximal of radial nerve, which has a marked distance from target muscles, takes a longer time for reinnervation in contrast to the technique we used, that is to say, transfer of supinator branch to PIN. The report by Van Zyl et al. [17] pertained to restoring both phases of hand function, along with elbow extension reconstruction by using nerve transfer in a man with C6 tetraplegia. The authors transferred teres minor nerve branch to long head of triceps nerve branch, brachialis nerve branch to anterior interosseous nerve, and supinator nerve branch to posterior interosseous nerve and achieved elbow extension, key pinch, grasp, and release. Ethical approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Guilan University of Medical Sciences) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent Informed consent was obtained. References 1. 2. 3. 4. 5. 6. 7. 8. 9. Conclusion In tetraplegic patients, nerve transfers are safe and reliable procedures for the reconstruction of elbow and wrist extension and finger flexion and extension. Finger flexion and extension should be simultaneously restored to achieve the best hand function. It should be mentioned that finger extension is an important phase of hand function because this function is required for object acquisition and release. In our case, we found that brachialis nerve transfer to AIN (for finger flexion) and supinator branch nerve transfer to PIN (for finger extension) can provide a functional hand with grasp and release. Inasmuch as most daily living activities could be performed through hand grasp and release, such double nerve transfer can be an acceptable surgical approach in tetraplegic patients after cervical SCI. 10. 11. 12. 13. 14. 15. 16. Compliance ethical standards 17. Conflict of interest The authors declare that they have no conflict of interest. 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J Hand Surg 39:1779–1783 Acta Neurochir Comments A well planned, executed, documented, and described clinical case report addressing a challenging spinal cord injury problem with very good restoration of important and useful hand function. Michel Kliot California, USA Doctors Emamhadi and Andalib report on a C7 quadriplegic patient who benefited significantly from nerve transfers. As outlined in their discussion section, there has been sparse literature on using nerve transfers to improve the life of quadriplegic patients. The results published thus far are very encouraging. Figures 5 and 6 demonstrate the benefit the patient received from the procedure. Other nerve transfers that have been reported in quadriplegic patients are a transfer of the AIN to the ECRL for improvement of wrist extension and stabilization of the hand. To improve wrist extension transfer of the teres or deltoid branches on the axillary nerve to triceps branches of the radial nerve to restore elbow extension. If this latter transfer proved to be successful, quadriplegic patients that were wheel chair bound could use their triceps to help transfer from their wheel chairs to the bed. I congratulate the authors on their excellent results. I will be following this literature to try to determine the optimal time for transfers and also to judge the efficacy of these transfers. The alternate strategy for improving hand grip in quadriplegic patients is spinal cord stimulation. Both of these techniques open new doors for improving the lives of this unfortunate group of patients. Allan Friedman North Carolina, USA