Injuries to the brachial plexus or other proximal peripheral nerves in the upper extremity can be functionally devastating. The second half of the last century witnessed remarkable advances in magnification, instrumentation, microsurgical techniques, and a greater understanding of nerve injury and repair. However, the expected functional recovery after proximal nerve injuries, even when a prompt and appropriate nerve repair was performed, remained poor. This was due to the limitations imposed by long reinnervation distances, especially in adults. Following an injury to a motor nerve, irreversible motor endplate damage begins immediately after denervation, and the longer the distance from injury to the neuromuscular junction, the longer time is needed to allow for regeneration, and the greater the motor endplate degredation.1 If the delay between injury and endplate reinnervation exceeds a few months, functional recovery will be poor. In upper extremity nerve surgery, “time is muscle.”2
An alternative to traditional nerve repair in proximal injuries is the restoration of function through nerve transfers, whereby a denervated peripheral target is reinnervated by a healthy, nonanatomic donor nerve. Nerve transfers have a long history, with sporadic reports in the literature as early as the 1920s when Harris3 described a radial to median nerve transfer to treat an injury sustained in battle during World War I. Nerve transfers experienced a revival and began to gain widespread acceptance in the 1990s when Brandt and Mackinnon4 and Oberlin et al5 described techniques for restoring elbow flexion. Over the ensuing 2 decades, numerous transfers have been described. Nerve transfer techniques have been nothing less than a revolution in peripheral nerve surgery, and functional outcomes have been achieved for brachial plexus and other proximal nerve injuries far exceeding those obtained from traditional nerve repair or tendon transfers.6–9 However, nerve transfer techniques have not been universally adopted by surgeons engaged in the care of upper extremity injuries. This is due in part to the large array of transfers described in the literature, which can be baffling to the novice, and to the misconception that nerve transfer procedures require skills and equipment available only at specialized centers. The purpose of this review was to present the indications for nerve transfers, the essential techniques and key transfers, to demystify the topic for the novice, and to further clarify the topic for the experienced.
The benefits of nerve transfers are manifold. They bring live axons close to the denervated target, essentially converting a high nerve injury to a more distal one, thus limiting motor endplate degradation. In addition, there is usually only one neurorrhaphy site, limiting the potential for axonal attrition due to scarring, foreign body, and fascicular misalignment. Finally, nerve transfers allow the surgeon to operate in an unscarred bed, allowing more precise anatomic identification, limiting operative times, and reducing the potential for iatrogenic injury.
In general, a nerve transfer is indicated in cases of proximal brachial plexus injuries where grafting is not possible and in proximal peripheral nerve injuries with long reinnervation distances. In the latter case, nerve transfers may be used in place of or as an adjunct to traditional neurorrhaphy or grafting. Nerve transfers are indicated in patients with extensive posttraumatic scarring, where exploration would risk damage to critical structures, as is commonly seen after proximal replantation or repair of severe crush or avulsion injuries. Nerve transfers may also be indicated in patients with a delayed reconstruction, as they can speed up reinnervation times, although it is generally understood that target muscles must be reinnervated before they are irreversibly atrophied, ideally before 12 to 18 months after injury, and certainly before 24 months.2,10 Nerve transfers for motor nerves are contraindicated beyond this time point, and patients are better served with tendon or functional muscle transfers (Table 1).
The preoperative planning for upper extremity nerve transfer procedures is similar to that for traditional tendon transfers. A thorough examination is performed to determine priorities as to which functions will be restored. In general, a proximal to distal approach is preferred, restoring shoulder and elbow motion, the key “positioning” functions, before restoring wrist and hand motion. A careful inventory must be made of functioning and nonfunctioning musculotendinous units in the extremity, to determine which nerves are available as donors. As with tendon transfers, the goal is to maximize the “return on investment,” sacrificing noncritical functions to restore essential ones. Suitable donor nerves include nerves to expendable muscles, such as the pronator quadratus branch of the anterior interosseous nerve, or nerves to muscles with redundant innervation.2 Examples of the latter include the distal accessory nerve, median nerve branches to the flexor digitorum superficialis (FDS), and ulnar nerve branches to the flexor carpi ulnaris (FCU). It is this redundancy in proximal nerve fibers that makes most nerve transfers possible.11
When possible, donor nerves which provide synergistic functions to the target muscle should be chosen, as this will facilitate postoperative motor unit retraining. For example, in median to radial transfers, Ray and Mackinnon have demonstrated better outcomes transferring the FDS branch of median nerve to the nerve to the extensor carpi radialis brevis (ECRB), rather than using it to innervate the nonsynergistic digital extensors. Likewise, the nerve to the flexor carpi radialis (FCR) is more effectively transferred to the posterior interosseous nerve, than it is to the nonsynergistic ECRB branch.12
KEY TECHNICAL POINTS
The performance of nerve transfer procedures is not technically difficult. In general, the procedures are more easily performed than traditional cable grafting, as nerve dissection is carried out in a pristine, unscarred bed. The surgical techniques are well within the abilities of a plastic surgeon familiar with microsurgery and upper extremity nerve repair. An inexpensive, disposable, handheld nerve stimulator is helpful for identifying motor fascicles, but no other specialized equipment is necessary. In addition, the stimulator can be used to verify redundancy of motor fascicles before a donor fascicle is harvested. To preserve intraoperative nerve function, it is important to avoid long-acting paralytic agents and local anesthetics. Likewise, tourniquet time during nerve dissection should be limited to 30 minutes to avoid ischemic compromise of nerve function.2
For motor transfers, the donor nerve is dissected out and stimulated to verify that the appropriate fascicle has been selected, and the remaining fascicles are stimulated to confirm preservation of critical functions. Donor and recipient nerves are mobilized sufficiently to provide a tension-free coaptation. The transfer should be performed as close to the target muscle as possible, to minimize the reinnervation distance.2
KEY MOTOR TRANSFERS
Transfers to Restore Shoulder Function I—Accessory to Suprascapular Nerve Transfer
Injury to the upper trunk of the brachial plexus commonly affects the suprascapular nerve (SSN), which provides motor innervation to the supraspinatus and infraspinatus muscles. These muscles are responsible for initiating arm abduction and performing external rotation, respectively. If the C5 to C6 nerve root is viable, cable grafting can restore function, as the reinnervation distance is relatively short. However, in an avulsion injury, there is no proximal nerve available, and the accessory nerve to SSN transfer is a good alternative.13,14 For this transfer, anterior or posterior approaches have been described. However, a posterior approach to the accessory nerve is generally preferred as it facilitates exposure of the distal portion of the nerve as well as permitting exposure of the radial and axillary nerves without patient repositioning (Table 2).
The accessory nerve can be located along a line parallel to the superior border of the scapula at a point two-fifths of the distance from the dorsal midline to the acromion. The SSN is also located along this line, at the midpoint between the superior angle of the scapula and the acromion.15 A transverse surgical incision is designed to expose both nerves. The trapezius muscle is split, exposing the suprascapular notch. Care is taken to avoid injury to the suprascapular artery, which passes over the scapula immediately lateral to the notch. The nerve is released from the notch and dissected as far proximally as possible. The distal spinal accessory nerve is then located in the medial aspect of the wound, deep to the trapezius muscle. Using the distal-most branch allows preservation of the proximal branches to the upper portions of the trapezius, preserving its function.8 The distal accessory branch is dissected as far distally as possible, divided, and transposed laterally. The SSN is divided as far proximal is possible, while still allowing a tension-free coaptation. Nerve grafting is not necessary (Fig. 1). In a recent functional outcomes study evaluating the results of the accessory to SSN nerve transfer, recovery of shoulder abduction and external rotation was achieved at an M3 or better modified Medical Research Council16 grade level in 8 of 9 patients at 28 months mean follow-up time9 (Table 3).
Transfers to Restore Shoulder Function II—Medial Triceps Nerve to Axillary Nerve Transfer
Upper trunk brachial plexus injuries and other proximal injuries often cause loss of axillary nerve function and denervation of the deltoid, the major abductor of the shoulder. In patients with preservation of radial nerve function, abduction can be effectively restored via transfer of one of the triceps branches of the radial nerve to the axillary nerve.8,17–19 This transfer is commonly performed in conjunction with the accessory to SSN transfer, described previously. Use of the lateral and long triceps branches has been described, but the medial triceps branch is preferable, due to its independence, long reach, and ease of dissection.8 Exposure for this transfer is provided through an incision extending from the quadrilateral space distally along the posterior arm to the midhumerus. At the proximal end of the incision, the axillary nerve is identified within the quadrilateral space and dissected as far proximal as possible, to ensure inclusion of the branch to the teres minor. Often, the lateral brachial cutaneous nerve, a branch of the axillary nerve, is encountered first, coursing around the posterior edge of the deltoid. It can then be traced back to the main nerve trunk.
The medial triceps branch of the radial nerve is easily identified in the posterior arm, running alongside the main radial nerve, in the interval between the long and lateral heads of the triceps. As the medial triceps branch runs independently for a long distance, it can be readily dissected free, verified with nerve stimulation, and transposed superiorly, where a tension-free coaptation is made to the axillary nerve at the level of its emergence from the quadrilateral space8 (Fig. 2). Of course, the radial nerve is often involved in brachial plexus injuries, and intact radial nerve function is a prerequisite for this transfer.
Double Fascicular Transfer to Restore Elbow Flexion
The results of nerve transfers to restore elbow function can be dramatic. Early efforts in this area involved the use of intercostal or pectoral nerves, with some success.4 In 1994, Oberlin described the use of branches of the ulnar nerve as the donor, transferred to the biceps branch of the musculocutaneous nerve at the level of the distal brachium, thus greatly shortening the reinnervation distance. His initial series consisted of 4 patients, 3 of whom achieved M4 level elbow flexion.5 Humphreys and Mackinnon have subsequently demonstrated that the classic Oberlin transfer can be augmented by transfer of a redundant median nerve fascicle to the FCR or FDS to the brachialis branch, the so-called “double-transfer.”20–22
The procedure is performed with the patient in the supine position with the arm extended. An incision is made over the biceptal groove in the medial arm. The brachial artery, median, and ulnar nerves are exposed. The musculocutaneous nerve is identified lateral to these structures, deep to the biceps muscle. It is dissected out distally, exposing the branches to biceps and brachialis. The donor nerves are then prepared. By careful nerve stimulation, a median nerve fascicle can be identified with FCR or FDS function. There is a great deal of redundancy in these functionalities; therefore, one fascicle can usually be harvested without yielding a donor deficit. However, once the fascicle is identified and teased away, the remaining fascicles should be tested to ensure preservation of function. In a likewise fashion, an FCU fascicle of the ulnar nerve is identified, tested, and prepared for transfer. Again, the donor fascicles should be dissected out for sufficient length so that the nerve coaptations can be performed without tension and as close to the recipient muscles as possible8 (Fig. 3).
Several studies have been published reporting excellent long-term results from both the classic Oberlin transfer and the double transfer for elbow flexion.5,7,23–25 However, by including the brachialis muscle, the double transfer seems to confer additional functional benefit, especially in terms of increased flexion strength.20,26 In 2005, Mackinnon et al20 presented a series of 6 patients, all of whom regained M4 or M4+ elbow flexion function after the double transfer, at a mean follow-up of 20.5 months. As a further testament to the value of the double transfer, Oberlin and colleagues have adopted the technique, publishing in 2006 a series of 10 patients who had undergone the procedure. All 10 recovered elbow flexion to the M4 level and were able to lift between 1 and 4 kg of weight, at 12 months mean follow-up.26
Anterior Interosseous Transfer to Restore Ulnar Intrinsic Function
Recovery of ulnar intrinsic function is typically poor after a proximal ulnar nerve injury, even with prompt and appropriate nerve repair.27,28 Tendon transfers can be used to augment or reproduce ulnar intrinsic function, but with variable results.29 Where median nerve function is intact, the distal anterior interosseous nerve (AIN) can be effectively transferred to the ulnar deep motor branch to restore function.30,31 The transfer was initially described with an end-to-end coaptation; however, the terminal AIN can be transferred in a reverse end-to-side fashion to the ulnar nerve, to “supercharge” the motor fascicle of a recovering ulnar nerve after proximal repair.32 In our practice, we perform this transfer regularly for any ulnar nerve repair proximal to the elbow.
A longitudinal palmar incision is used to expose the contents of Guyon canal, and it is extended proximally in a zigzag fashion across the wrist crease and into the distal forearm to provide exposure of the AIN.33 The ulnar motor branch is identified as it dives deep to the origin of the flexor digiti minimi muscle at the hamate hook. Under operative microscopy, the motor fascicle is readily separable from the remainder of the nerve into the distal forearm. The AIN is identified at the proximal border of the pronator quadratus muscle. The nerve is traced into the muscle a short distance and divided just before its terminal branches. Proximal dissection is performed to gain adequate length for a tension-free coaptation, either end-to-end or reverse end-to-side, as the clinical situation dictates33 (Fig. 4).
Anatomic studies have shown that there are more than 1200 motor axons in the ulnar motor branch at the wrist, compared to approximately 900 axons in the AIN, some of which are afferent sensory fibers.34 Despite this axonal mismatch, excellent results have been reported. In 1999, Battiston and Lanzetta reported the results of 7 cases of proximal ulnar nerve injury treated with an AIN to ulnar motor branch transfer. At a mean follow-up of 2.5 years, 5 patients experienced recovery to the M4 level, and 1 patient, an 11-year-old boy, had M5 level function.35 Three years later, Novak and Mackinnon reported a series of 8 patients, with a mean follow-up of 18 months. All patients experienced significant improvements in lateral pinch and gripping strength. Only 1 patient required subsequent tendon transfer, to restore small finger adduction.30
Numerous sensory transfers have been described, to restore sensation after ulnar, median, or radial nerve injuries, or to restore critical sensation after brachial plexus injuries.8,33,36–40 All of these transfers are based on the principle of sacrificing nerves that provide noncritical sensation to restore essential hand or digital sensation. For less critical sensory nerves, an end-to-side nerve transfer can be performed, thus preserving sensation in the donor dermatome. Experimental studies have shown that in the absence of injury to the donor nerve, only sensory axons will traverse such a repair.41–43 Most authors agree that the end-to-side technique can provide protective sensibility to noncritical areas, but higher levels of sensory recovery are not typical.33
Median nerve sensation is critical for fine manipulation and tip-to-tip pinch. Restoring sensation to the radial aspect of the thumb and ulnar side of the index finger are of utmost priority after median nerve injury, and in the past neurovascular island flaps have been used to restore sensibility to these areas. The fourth webspace and dorsum of the hand are less critical sensory distributions, and the nerves which provide sensation to these areas are potential donors for nerve transfers. Brown and Mackinnon describe a trio of nerve transfers designed to restore critical sensation after median nerve injury.33 In this procedure, the dorsal cutaneous branch of the ulnar nerve is transferred end-to-end to the branch of the median nerve to the thumb, first, and second webspaces. The ulnar nerve branch to the fourth webspace is transferred in an end-to-side fashion to the third webspace branch of median nerve. The ulnar sensory branch is also transferred in an end-to-side fashion to the distal cut end of the dorsal sensory branch of ulnar nerve, with an autograft, to preserve protective sensation in the donor site44 (Fig. 5).
The early phase of rehabilitation after nerve transfer is similar to any nerve injury, with a focus on range of motion and edema control. As function improves in the recipient muscle units, a program of reeducation is initiated, with intensive practice and repetition.45 Retraining is more easily achieved when a synergistic transfer is used. For sensory transfers, early behavioral reinforcement is of proven benefit, with patients who undergo early sensory reeducation having less severe paresthesias and better 2-point discrimination than those who do not.46 The process of cortical reorganization continues long after injury, so motor unit retraining with a certified therapist may be of benefit for many months, or even years, after injury.47
There is a large and rapidly growing body of literature regarding nerve transfers in the upper extremity. Despite this fact, and possibly because of it, there has been a slow adoption of these techniques by hand surgeons. A wide array of nerve transfers have been described, but there are a few for which the clinical evidence is very strong. These include the accessory to SSN and medial triceps to axillary nerve for shoulder abduction, the double fascicular transfer for elbow flexion, and the distal AIN to ulnar motor branch transfer for ulnar intrinsic function. These transfers are not technically challenging, require no extraordinary equipment or expertise, and have the potential to provide dramatic improvements in function for injuries which have been traditionally discouraging to treat. For complex injury patterns, such as brachial plexus avulsion injuries or multiple nerve injuries, nerve transfers form a therapeutic triad with tendon transfers and motor unit reeducation to achieve the fullest possible functional recovery (Fig. 6). The future will certainly bring the development of new nerve transfer procedures, as well as additional clarity regarding the value and indications for the transfers already described. The possible applications of nerve transfers are limited only by human anatomy and human imagination.
The author thanks Tom Dolan, MS, and Matt Hazard, Bio-Medical Illustrators with the University of Kentucky Academic Technology Group, for the preparation of illustrations.
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