Nerve Transfers: Indications and Techniques

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Chapter 198 Nerve Transfers: Indications and Techniques

Manish S. Sharma, Allen T. Bishop, Alexander Y. Shin, Robert J. Spinner

Traumatic brachial plexus injuries (BPIs) produce psychologically and functionally devastating handicaps afflicting, generally, a subset of young, healthy males in the prime of life. Seventy percent are caused by motor vehicle accidents, of which 70% are due to the use of two-wheelers.1 The disease burden is estimated to be about 2162 cases per annum in the United States; costs of treatment amount to about $34,733 per capita.2 It is prudent to mention at the outset that the management of traumatic BPI requires a complex multidisciplinary approach involving neurosurgeons, orthopedists, plastic/hand surgeons, neurologists, neuroradiologists, neurophysiologists, physiotherapists, and pain specialists.

Surgical repair for BPI involves either neurolysis (scar release) that may be external, internal, or both; nerve grafting using devascularized, vascularized, or pedicled nerve cables to bridge defects; or nerve transfers where healthy functioning donor nerve is coapted directly onto a damaged recipient nerve.

Nerve Transfers (Neurotizations)

Specifically, nerve transfers involve re-assigning an “expendable” or redundant working nerve, part of a nerve (fascicle), or a nerve branch (donor) to a more important, nonfunctioning nerve (recipient).

The use of and enthusiasm for nerve transfers have increased dramatically in the past two decades largely due to the creative contributions of innovators such as Drs. Christophe Oberlin and Susan Mackinnon. The introduction of a fascicular transfer by Oberlin et al. (1994)3 for upper trunk injuries catalyzed the transformation. This procedure introduced the concept of fascicular transfer by using functioning ulnar nerve fascicles supplying the flexor carpi ulnaris to be selectively transferred onto the nerve to biceps with excellent results.3–5

The new era of nerve transfer has created a major controversy in brachial plexus surgery now—the role of nerve grafts versus nerve transfers in postganglionic injuries. This issue remains largely unresolved. The advantages and disadvantages of performing nerve transfers over nerve grafts are listed in Tables 198-1 and 198-2. As can be seen, the advantages of performing nerve transfers may outweigh those of brachial plexus nerve grafting. In fact, in the event of patients sustaining panplexal nerve injuries secondary to multiple root avulsions, nerve transfers may be the only viable form of repair.

TABLE 198-1 Advantages of Performing Nerve Transfer versus Nerve Graft

Nerve Transfer Nerve Graft
A distal procedure performed close to the motor point of muscles. This decreases the time to reinnervation. The direct repair is at a single suture line. This improves reinnervation as well. Performed at the site of injury, typically proximally, and thus more anatomical. These are also more physiologic and make relearning when muscle power returns easier.
Surgical dissection occurs in uninvolved pristine tissue. These repairs make available more donor motor axons as nerve stumps are typically largest proximally.
Directed (selective) neurotization makes targeting motor recipient axons easier as it is closer to the motor end plate. As the entire cut surface is coapted with the injured stump, sensory reinnervation is also a possibility.
Is the only procedure possible after nerve root avulsion. Grafts enable entire motor groups to recover as opposed to single targeted muscles.
Can be performed with minimal technology.

TABLE 198-2 Disadvantages of Performing Nerve Transfer versus Nerve Graft

Nerve Transfer Nerve Graft
Involves some loss of existing function, by definition. Typically requires use of nerve grafts, e.g., non-degenerated sensory nerves like the sural. The harvest has cosmetic and functional sequelae.
Requires muscle re-education that can hamper autonomy because of co-contractions. Has to be performed at the site of injury. Dissection is more difficult, especially in the presence of a concomitant vascular repair.
Number of available donor nerves is limited especially in patients with panplexal injuries. Cannot be performed in patients with root avulsive injuries.
Number of available motor axons is necessarily limited. Directed (motor donor to motor recipient) repair is seldom possible, especially when the loss of length is high. All proximal components of the brachial plexus are mixed sensorimotor.
Longer grafts should be vascularized as free grafts may fibrose secondary to ischemic injury.
Grafts require axonal sprouts to cross two suture lines. This further delays repair. If the distal suture line scars densely, the entire repair may fail here.
Grafts ideally require the use of intraoperative sensory and motor-evoked potentials to determine the viability of the donor nerve stump (especially proximal cervical nerves) even if it appears structurally intact. These have several technical and observer-dependent confounding factors.

Indications

1. “Irreparable” nerves that are avulsed from the spinal cord.

Preganglionic injuries are not amenable to any other form of repair as the motor axon has been physically disconnected from the neuronal cell body across the intervertebral foramen. Reconnection via axonal regeneration is not physically possible. In such patients, motor end plate degeneration starts at the time of injury and may be irreversible after 12 to 18 months.6,7 To beat the biological clock, it is imperative to operate as soon as possible and transfer viable axons to as close to the motor end point as possible. This is the procedure of choice in this form of injury.

2. More rapid or reliable recovery of motor function.

Most experts have now begun to recognize that nerve transfers allow a faster and perhaps more reliable way of regaining function even in postganglionic injuries bucking the previous trend of using proximal nerve grafts (Table 198-3).

3. To power free-functioning muscle transfers (FFMT).

Free-functioning muscle transfer is a reliable way to reconstruct the damaged upper extremity by moving a functioning muscle with its nerve and blood supply to another location where it can subserve a new function. This can occur after a successful nerve repair and anastomosis of the artery and vein have been accomplished. This microsurgical technique therefore does not have a time window like typical nerve reconstruction. Most commonly, FFMTs have thereby been performed for delayed cases to provide elbow flexion (such as in neglected injuries or those with poor or incomplete recovery). FFMTs in this setting can augment motor function. The native anatomy of the transferred muscle/tendon unit (gracilis, for example) has important features which allow FFMTs to achieve more distal function, ordinarily unachievable with standard techniques of nerve reconstruction (e.g., recovery of prehension of the hand in patients with flail limbs). The nerve supply is relatively close to the muscle and the tendon is long (and can be prolonged). This technique then can also be incorporated into an armamentarium in combination with other nerve techniques in the early setting.

TABLE 198-3 Commonly and Uncommonly Performed Nerve Donors/Transfers

Recipient Nerve Common Donor Nerves Uncommon Donor Nerves
Suprascapular Spinal accessory
C5 nerve
C6 nerve		 C4 nerve
C7 nerve/middle trunk
Phrenic nerve
Contralateral C7
Dorsal scapular
Axillary Triceps branch of radial
Medial pectoral
Motor intercostals		 Thoracodorsal
Contralateral C7
MCN, biceps, or brachialis branch Ulnar nerve fascicle
Median nerve fascicle
Motor intercostal
Medial pectoral		 Thoracodorsal
Spinal accessory
Phrenic
Contralateral C7
Hemi-hypoglossal
Median Sensory intercostals
Contralateral C7
Ulnar nerve fascicle
Brachialis branch of MCN		 Supinator/ECRB branch of radial
Radial Motor intercostals
Proximal branches of radial		 Contralateral C7
Dorsal scapular nerve
Median nerve branches
Ulnar nerve Brachialis branch of MCN
Anterior interosseous		 Contralateral C7

ECRB, extensor carpi radialis brevis; MCN, musculocutaneous.

Contraindications

The only absolute contraindications for a nerve transfer are the absence of a donor nerve and the presence of a fibrosed atrophic recipient nerve with no viable fascicles seen under magnification on sequential cut sections at the motor point. Relative contraindications would include the availability of a poor quality donor as seen with direct electrical stimulation at surgery, the presence of a stimulatable motor nerve recipient at surgery, or a short segment rupture/neuroma that can easily be repaired end-to-end without the use of a graft.

Principles

Some basic principles must be respected while performing nerve transfers. These include the following:

1. Accurate documentation of pre-existing muscle power, vascular injury, and joint contractures

2. Clear, coherent, and exhaustive discussion of options and priorities with the patient

3. Fall-back planning and prior consent in case favored donors are poorly functioning

4. Elaboration of realistic goals prior to surgery, including risks related to possible donor morbidity (transient and permanent) and slow nature of recovery

5. Selection of the ideal donor nerve (Table 198-4)

6. Transection of recipient nerve as proximal as possible to determine adequacy before donor dissection

7. Donor nerve dissected distal to recipient to gain length

8. Selective neurotization based on knowledge of fascicular anatomy (Table 198-5)

9. Awareness of proximal and distal orientation of transected nerve segments

10. Tension-free direct repair under magnification

TABLE 198-4 Characteristics of Ideal Donor

Pure Motor or sensory.
Example: Medial pectoral nerve (motor); sensory intercostal nerves.
Adjacent Minimal donor dissection required to gain length.
Example: Double fascicular transfer for elbow flexion.
Expendable Unlikely to affect donor function.
Example: Intercostal nerve transfer.
Uninjured Donor fascicle muscle groups must have at least grade 4/5 MRC power.
Example: Spinal accessory transfer is contraindicated when shoulder function is poor.
Remote From zone of injury (dissection is easier).
Example: Oberlin’s transfer in upper trunk injury.
Proximate To motor point so reinnervation is faster and likely better.
Example: Triceps to axillary nerve transfer.
Adequate Diameter mismatch is prevented.
Example: Three motor intercostals are used to neurotize the nerve to biceps.
Educatable Same muscle compartment is ideal, as relearning and subsequent autonomy are better and faster as antagonistic co-contractions do not occur.

MRC, Medical Research Council.

TABLE 198-5 Fascicular Anatomy of Major Nerves

Nerve Donor/Recipient Fascicular Anatomy
CC7 Donor Posterior division has 2x motor axons.
Median (axilla) Recipient Lateral root is mainly sensory.
Median (arm) Donor FCR/FDS fascicle is medial.
Median (arm) Recipient Posterior fascicle (AIN).
Anterior fascicle (PT, FCR).
Middle fascicle (FDS, thenar, sensory).
Median (forearm) Donor Terminal AIN branch to PQ.
Nerve to biceps Recipient Lateral in musculocutaneous nerve.
Nerve to brachialis Donor/recipient Lateral to LABC.
Suprascapular Recipient Lateral within upper trunk.
Ulnar (arm) Donor FCU fascicle is posteromedial.

AIN, anterior interosseous nerve; CC7, contralateral C7; FCR, flexor carpi radialis; FCU, flexor carpi ulnaris; FDS, flexor digitorum superficialis; LABC, lateral antebrachial cutaneous nerve; PQ, pronator quadratus; PT, pronator teres.

Common Targets

The common recipient nerves for transfers are the suprascapular, axillary, and musculocutaneous nerves. A list of donors is provided in Table 198-3.

Surgical Anatomy

The brachial plexus is formed by the ventral rami of the fifth to eighth cervical and the first thoracic nerve roots. It is essential to remember that the nerves emerge between the scalenus anterior and medius (interscalene triangle) to form trunks in the supraclavicular fossa. The divisions of the brachial plexus are retroclavicular while the cords are infraclavicular and named as such in relation to the axillary artery.

Supraclavicular Exploration

The key muscles for the supraclavicular exploration of the brachial plexus are the omohyoid (deep to which lies the fat pad covering the plexus) and the scalenus anterior (deep to which lie the nerves). The latter is often difficult to identify especially when there is extensive scarring. They are then identified indirectly as the structures that lie beneath the phrenic nerve. The phrenic nerve may be identified visually as the only neural structure (other than the nerve to subclavius) that passes from lateral to medial in the root of the neck (Fig. 198-1). If scarring is extensive, blind neural stimulation using 0.1–2 mA of current may provoke capnographic changes if not frank diaphragmatic contraction that may guide the surgeon to the approximate location of this key structure before sharp dissection is commenced.8 The phrenic nerve can then be traced back to the C5 nerve via its contribution to the former. From here, the C5 nerve can then be traced to the upper trunk. Proximal and distal dissection allows identification of C6 and the divisions of the upper trunk. The suprascapular nerve is the key target in this exploration and can be found superior, lateral, and posterior to the upper trunk. Its direction confirms its identity. It parallels the omohyoid and runs posteriorly obliquely to the scapular notch. In the event of a complete rupture of the C5 and C6 nerves, the distal components of the plexus can be found near, behind, or even below the clavicle.

image

FIGURE 198-1 Intraoperative photograph. The phrenic nerve (black arrows) can be seen crossing from lateral to medial over the scalenus anterior (SA). The C5, C6 nerves and the upper trunk (asterisk) pass behind and lateral to this muscle but anterior to the scalenus medius (SM). The nerve to subclavius (black arrowheads) and the accessory phrenic nerve (white arrowhead) are also depicted.

The spinal accessory nerve can be identified by exposing the lateral aspect of the supraclavicular incision. The nerve can be identified reliably a few centimeters above the clavicle on the anterior surface of the trapezius at its medial border. Other smaller, mostly sensory nerves frequently seen in this location represent neural elements of the cervical plexus. These may produce weak contractions of the trapezius. In contrast, direct stimulation of the spinal accessory nerve produces powerful trapezius contraction.

Care has to be taken, during dissection, not to injure the lymphatic duct on the right and the chyle carrying thoracic duct on the left side. These elements are at risk during medial dissection such as with exposure of the lower trunk elements.

Infraclavicular Exploration

The key muscle in the infraclavicular exploration of the brachial plexus is the pectoralis minor. This may be approached either through the preferred corridor offered by the deltopectoral groove or a transpectoralis major (muscle splitting) exposure. The pectoralis minor is identified as the musculotendinous structure passing inferomedially from the coracoid process of the scapula to the third–fifth costochondral junctions. This anatomy also helps the surgeon to define ribs and the underlying intercostal nerves with a number. Division of the pectoralis minor muscle reveals the cords, terminal branches, and axillary vessels within the axillary sheath. Fat can treacherously encase these structures, especially the axillary and cephalic veins. Due care must be taken while retracting the pectoralis minor as the medial and lateral pectoral nerves arborize in the adjacent fat planes when penetrating this muscle.

The key neural structure to be identified here is the median nerve, which is characterized by a Y-shape at its take-off from both the lateral and medial cords. The median nerve helps navigation. The lateral root of the median nerve enters the lateral cord. The lateral cord can then be followed distally into the musculocutaneous nerve. Its medial root can be traced proximally into the medial cord and the medial cord can be traced to the ulnar nerve in the arm which lies in the biceps–triceps groove. The proximal median nerve is at first lateral to the brachial artery and crosses it ventrally in the mid-arm to gain its medial relation. At this point, the ulnar nerve, which lies medial to the brachial artery in the upper arm, begins descending posteriorly to eventually penetrate the medial intermuscular septum and pass behind the medial epicondyle.

It is important to realize that the musculocutaneous nerve provides its first branch to the coracobrachialis muscle and then penetrates this muscle. This must not be mistaken for the nerve to the biceps which is given off its lateral aspect in the mid-arm (typically 12 cm distal to the acromion). The nerve to the brachialis is given off further distally (approximately 17 cm distal to the acromion) and typically lies lateral to the terminal branch, the lateral antebrachial cutaneous nerve.9 The former is a pure motor branch, while the latter is a sensory nerve. The authors verify the nature of both these terminal divisions by tracing the brachialis branch until it arborizes on the muscle surface. A variation that has to be considered is the low take-off of the musculocutaneous nerve from the median nerve. This is important to consider especially when the median nerve is being considered as a donor for a simultaneous nerve transfer.

Anterior and Posterior Approaches for the Suprascapular and Axillary Nerves

The suprascapular and axillary nerves can be approached either anteriorly or posteriorly. The suprascapular nerve is typically identified in the supraclavicular dissection. Occasionally it can be identified and dissected further distally in the infraclavicular region. It lies lateral to the cords/divisions. It runs near the coracoid process as it heads toward the suprascapular notch.

A separate posterior incision can be done along the lateral aspect of the scapular spine. The trapezius can be elevated from the scapular spine or its fibers split in line with their course. The atrophic suprapinatus can be mobilized inferiorly. The shiny transverse scapular ligament can be seen and divided. The suprascapular nerve is deep to the ligament. This posterior approach can be used if a second site of injury is suspected or if a distal nerve transfer is performed (distal spinal accessory nerve to the distal suprascapular nerve).

The infraclavicular exposure allows anterior exposure of the axillary nerve. It can be located superior and lateral to the posterior cord at the level of the humeral head. For identifying the posterior cord, the axillary artery has to be mobilized, generally ventrally and laterally off the axillary vein. This is a delicate procedure and the access is made more difficult by the operating depth or by previous vascular injury and/or repair. The conjoined tendon can be taken down from the coracoid to allow more lateral and distal exposure, that is, more removed from the typical vascular injury. The conjoined tendon would need to be reapproximated at the end of the case.

A posterior approach allows easy dissection of the axillary nerve in the quadrangular space formed laterally by the long head of the triceps, medially by the proximal humerus, superiorly by the teres minor and inferiorly by the teres major. The axillary nerve here, follows the posterior circumflex humeral artery, and splits into the anterior and posterior divisions. The anterior division is generally targeted as it supplies the anterior and middle deltoid. The posterior division innervates the less important posterior deltoid and also gives rise to the superior lateral cutaneous nerve of the arm, which need not be reinnervated. The importance of the superior lateral cutaneous nerve of the arm lies in that it can be used, when traced retrogradely from the skin incision, for navigating to the posterior division and thereon to the anterior division of the axillary nerve. Sometimes, a combined anterior and posterior approach may be required to satisfactorily visualize the axillary nerve in its entirety or to find a healthy recipient nerve (the pull through procedure). The radial nerve exits the axilla inferior (more inferiorly) to the axillary nerve. It courses through the triangular space formed by the teres major superiorly, the long head of the triceps inferomedially and the shaft of the humerus laterally.

General Principles: Surgical Technique

Positioning and Anesthesia

Patients are operated on under general anesthesia. Strict instructions are issued to ensure that no neuromuscular blocking agents are used. The patient is typically placed in the supine position with the head slightly extended and turned to the opposite side. An interscapular towel roll can also be used to make the supraclavicular fossa more prominent. Occasionally, the patient is bumped up to provide access if a posterior approach is anticipated. The arm is placed, initially, in an adducted and depressed position to enhance the exposure. However, it should be draped in such a manner as to ensure that it can be freely abducted or crossed over the chest, so as to facilitate further surgery. The hands and fingers should be kept exposed for visual inspection of evoked movements. As a substantial part of the total body surface area has to be kept exposed, it is vital to ensure that patients do not slip into hypothermia. The appropriate use of blankets and warming units is encouraged. As nerve transfers may well be done in combination with nerve grafting, wide prepping of the neck, chest, arm, and both legs is always done for various exposures and harvest of nerve graft(s).

Technique of Nerve Coaption

First we prepare all of the donor and recipient nerves or fascicles and clip them with redundancy to green backgrounds, once transected, to ensure high visibility. Then we perform all of the microsurgery of the various nerves. We trim back on the recipient so that its length is as short as possible so as to minimize reinnervation time to the end organ. A repair with tension is avoided. The repair is tested in the maximum anticipated range of joint movements in all directions. Diameter mismatches are avoided wherever possible and selective neurotization is practiced when it is not. Donor and recipient nerve fascicles are further skeletonized and soft tissue is denuded at the coapting ends to prevent scar formation. The fascicular ends are finally sectioned using an ultrafine diamond knife. Coaption is then carried out using interrupted, nylon, monofilament 9-0 sutures passed through the epineurium of adjacent fascicles. An operating microscope with twin mobile opposable eyepieces is used so that two surgeons can operate simultaneously. Frequent heparinized saline flushes ensure adequate visibility at the time of coaption. Typically, two diametrically opposite sutures are used with three throws each. The initial knot is tensioned gradually so as to just appose the cut sections of the participating fascicles without buckling them. Knots are initially cut long so as to rotate the line of coaption to look for any unevenness. If the suture line is uneven or buckled, more sutures or else release of existing sutures and redo may be preferred as this is the most vital part of the operation. Once the suture line is observed to be satisfactory, we place a bivalved nerve tube of an appropriate diameter to protect the repair. This is then cemented in with the use of tissue adhesive.9

Common Presentations: Strategies and Nerve Transfers

Panplexal Injury

Management Rationale

The priorities for reconstruction are shoulder stability (abduction and external rotation) and elbow flexion. The targeted recipient nerves are suprascapular, axillary and musculocutaneous. The problem is the lack of donor nerves in this vicinity. It is worthwhile to explore the plexus in every case to determine whether the C5/C6/C7 nerves are viable or not. If somatosensory and motor-evoked potentials (SSEPs, MEPs) are positive, these nerves provide the best qualitative and quantitative motor axons for transfer. Grafts can then be placed to target the suprascapular and axillary nerves. Realistically, the limited number of donors represents valuable commodities. These resources expended on more distal targets are often lost due to the poor recovery obtained historically given the necessary prolonged time for reinnervation.

In the event of panroot avulsion, nerve transfers alone can provide the only solution. The authors’ preferred standard solution is the spinal accessory-suprascapular nerve (Fig. 198-2), motor intercostal-musculocutaneous nerve (Fig. 198-3) and sensory intercostal-lateral root of median nerve transfer. This algorithm provides stability of the shoulder, elbow flexion, and protective sensation in the hand. In many situations, a C5 stump is available for nerve grafting, even in the panplexal situation. This is why we recommend exploration of the brachial plexus and electrophysiologic monitoring of these patients. One or more donors may be available for use.

image

FIGURE 198-2 Spinal accessory nerve transfer to the suprascapular nerve. Anterior approach, single incision. The spinal accessory nerve is identified on the medial margin of the trapezius several finger breadths above the clavicle. It is transferred directly to the suprascapular nerve.

(From Mayo Foundation for Medical Education and Research, with permission. All rights reserved.)

image

FIGURE 198-3 Intraoperative photograph depicting the intercostal-musculocutaneous nerve transfer The pectoralis major (PM) tendon has been detached at its insertion and the muscle belly reflected medially to expose the chest wall. The harvested motor intercostal nerves (T2-4; solid black arrows) have been dissected back to the serratus anterior (SRA) and coapted directly (dashed black arrow) with the musculocutaneous nerve (black asterisk). The lateral root of the median nerve (black arrowhead) has been coapted with the sensory intercostal nerves (white arrowheads) behind the fat pad marked by a black star. The white arrow depicts the nerve to the coracobrachialis (CB).

We have also employed a technique to offer patients a chance of hand prehension. We have modified Doi’s original procedure detailing the double functioning free muscle transfer (FFMT) into a single-stage procedure to provide some chance of hand recovery in a patient with a flail anesthetic limb.10 If one cervical nerve is viable, it is used as a donor for nerve grafting to the suprascapular and axillary nerves. If it is not available, the shoulder is not reconstructed, or at a delayed stage, shoulder fusion or tendon transfer can be considered. Four intercostals (T3–T6) are harvested for nerve transfers for elbow flexion: two of these (T5 and T6) are transferred to the native nerve to biceps and the remaining two (T3 and T4) are used to power a FFMT destined for combined elbow flexion/finger flexion. The contralateral gracilis muscle is transferred with its neurovascular pedicle onto the clavicle and its tendon sutured into the long flexors of all five digits. Vascular anastomoses are then carried out and the nerve to gracilis is coapted. Sensory innervation is provided for by coapting all available sensory intercostal nerves with the lateral root of the median nerve (Fig. 198-4).9 The spinal accessory nerve is lengthened with a nerve graft and coapted to a triceps branch.

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FIGURE 198-4 Single-stage FFMT procedure in a panplexal injury. A, T3 and T4 are transferred to the FFMT for combined elbow flexion and finger flexion. T5 and T6 are transferred to the native biceps. Several sensory intercostals are transferred to the lateral root of the median nerve. The spinal accessory nerve is extended with a graft to a triceps branch. C5 if available is used to graft shoulder targets (not shown). B, Details of the transferred FFMT (gracilis) are shown, including the origin on the clavicle, its subcutaneous course in the arm, beneath a lacertus fibrosus pulley and woven into the finger flexors. The nerve, artery, and vein repairs have been done. LCCMN, lateral cord contribution to the median nerve; SPA, spinal accessory nerve; Lat, lateral cord; Post., posterior cord; Med., medial cord; S, sensory intercostals nerve; M, motor intercostals nerve.

(From Mayo Foundation for Medical Education and Research, with permission. All rights reserved.) FFMT, free functioning muscle transfer.

Approaches

The supraclavicular brachial plexus is explored through a transverse incision several finger breadths above the clavicle. A separate vertical limb extends through the deltopectoral groove to the proximal arm for exposure of terminal branches of the brachial plexus and is used for concomitant nerve transfers. An inframammary incision is incorporated for harvesting intercostal nerves. If a FFMT is performed, wider exposure has been helpful. A reverse hockey stick type incision is performed centered over the acromioclavicular joint combining the supra and infraclavicular incisions.

The supraclavicular approach is done first. Full-thickness flaps are raised and the clavicle is exposed. The lateral border of the sternocleidomastoid is identified, the wound is deepened and the omohyoid is divided and tagged. The fat pad is then reflected laterally and the scar dissected to identify the phrenic nerve and then the posterior border of the scalenus anterior. Here, the C5 and C6 nerves are identified and traced to the region of the intervertebral foramen,

The suprascapular nerve is identified during the exposure of C5 and C6 nerves. In the event of a total rupture the nerve may even lie behind the clavicle. It may be approached in this position, ventrally, by varying the line of vision, elevating the head end of the operating table, and depressing the ipsilateral upper limb. When encased in a neuroma-in-continuity, the nerve is seen as a fairly prominent branch coming off the superior surface of the upper trunk and heading posteriorly, laterally and inferiorly almost parallel to the posterior division of the upper trunk towards the suprascapular notch.

The spinal accessory nerve is then identified on the medial border of the trapezius, stimulated to confirm its identity and viability after detecting trapezius contraction, encircled with vessel loops, and then traced distally as far as is feasible. The proximal branch of the spinal accessory nerve to the trapezius is preserved to retain some of the muscle’s function.

Intraoperative recordings are then performed. Paralytic agents sometimes are necessary during the neurophysiological testing to minimize artifact from background muscle stimulated. We routinely check for the presence of somatosensory evoked potentials (SSEPs) and motor evoked potentials (MEPs). Negative recordings favor the performance of nerve transfers.

The spinal accessory nerve is then prepared. Distal branches will need to be sacrificed in order to pivot the nerve out of the operative depth toward the suprascapular nerve. Contributions from the cervical plexus to the spinal accessory nerve are maintained when possible. The transected tip of the nerve is passed through the fat pad and tagged with a clip to a green background for later identification.

The suprascapular nerve is then prepared. It is dissected off the neuroma/posterior division and its fascicle traced into the upper trunk to gain additional length. It is transected at that level. Good fascicular structure is obtained by trimming back as necessary. The donor and recipient fascicles are then secured on a green background. These nerves may be difficult to find later in a bloody field and the suprascapular nerve may retract inferiorly after being cut. This repair is then carried out using a standardized technique described in an earlier section (Fig. 198-2).

Intercostal–Musculocutaneous/Median Nerve Transfer

The inframammary part of the procedure begins using a curvilinear incision beneath the breast which skirts the anterior axillary line to enter the deltopectoral incision. Through this approach, the cephalic vein is first identified and protected. The chest wall is then exposed by first identifying the insertion of the pectoralis major tendon into the humerus and following this muscle across the anterior axillary fold onto the chest. In the majority of cases, this tendon is then divided at its insertion into the humerus and the muscle is lifted off, along with the skin and breast tissue, from the underlying ribs and intercostal muscles. This tendon is repaired at the end of the case if the pectoralis major had some function preoperatively or is targeted as part of the reconstruction. In cases where FFMT is performed, the pectoralis major tendon is not repaired as this muscle configuration interferes with the trajectory of the FFMT.

The pectoralis minor muscle is then encountered. It is followed to the coracoid process, released from this bone and then retracted with self-retainers to expose the axillary sheath. At this point in time we begin to dissect the intercostal nerves starting with the sixth rib. The presence of fractures may greatly endanger safe dissection. The rib surface is first exposed using monopolar cautery to incise the periosteum. The periosteum is then stripped away superiorly, inferiorly and mediolaterally using straight and curved periosteal elevators and rib raspatories. Care is taken during lateral exposure of the ribs to minimize risk of injury to the long thoracic nerve which may be functional in patients with postganglionic injury. The intercostal nerve harvest is best performed using two assistants. One raises the bare rib using either the raspatory or an umbilical tape passed under this bone to completely expose the periosteum below it. The second assistant retracts the periosteum and keeps it stretched. The surgeon then incises the periosteum starting medially where the donor nerve is most superficial and the intercostal muscles are generally deficient. The entire nerve, once identified, is then stimulated to confirm its motor identity. The nerve is then further dissected to skeletonize the motor versus the non-stimulatable sensory branches. Both nerves are then traced laterally to the midaxillary line and separated from the intercostal muscles with a combination of sharp and blunt dissection and gentle retraction with vessel loops. Intercostal vessels may be damaged at multiple spots during this procedure. Hemostasis should be secured with the minimal use of cautery to prevent thermal damage to these delicate nerves. This procedure is repeated at other ribs. Sensory intercostal nerves are dissected towards the skin as far as possible to create long lengths for direct, graft-less, transfers onto the median nerve. The intercostobrachial nerve is a large nerve and can be used for sensory neurotization. To prevent a diameter mismatch, we try to use at least three intercostal motor nerves for coaption with the musculocutaneous nerve and two for the nerve to the triceps long/lateral heads.

With the axillary sheath exposed, the lateral cord, its contribution to the median nerve and the take-off of the musculocutaneous nerve are identified. The musculocutaneous nerve is then followed to its biceps motor branch. This branch is then lengthened with retrograde dissection, separating it from the parent nerve until sufficient length is obtained to allow direct transfer of the prepared intercostal motor nerves. In a similar fashion, the lateral root of the median nerve is also skeletonized from the musculocutaneous nerve and the lateral cord itself to gain additional length to allow for a direct transfer of the previously harvested intercostal sensory nerves (Fig. 198-3). Nerve coaption is performed using the operating microscope with the arm abducted to 90 degrees in external rotation.

Upper Trunk (C5/C6) Brachial Plexus Injury Pattern

Management Rationale

In this pattern of partial brachial plexis injury (BPI), several intraplexal donors are available for nerve transfers. Most importantly, hand function remains intact as the C8, T1 nerves are viable. However, this hand function is of limited use in the absence of useful elbow and shoulder function. Thus, while the management priorities are the same as that for panplexal injuries (namely, shoulder abduction and external rotation and elbow flexion), the major difference is that more options exist. These include newer, better motor intraplexal donors that can be transferred closer to the end organ. Classical proximal nerve grafts or nerve transfers, which were previously performed for these injuries, are now being replaced by distal directed nerve transfers for reasons that have been discussed previously.11–39 In these cases, to optimize results, double reinnervation of shoulder and elbow flexor targets is attempted.

For shoulder function the suprascapular nerve is still targeted using the spinal accessory. For restoring axillary nerve function, the authors prefer to use the adjacent triceps branch of the radial nerve via a posterior approach (Leechavengvongs’ transfer; Figs. 198-5 and 198-6).40 Elbow flexion is gained using either the Oberlin transfer alone (ulnar nerve to biceps) or a double fascicular transfer (ulnar nerve to biceps and a simultaneous median—nerve to brachialis; Fig. 198-7).41 If the C7 nerve is injured in addition, the axillary nerve may be neurotized using the medial pectoral nerve (C8, T1) or the thoracodorsal nerves (C6–C8). The more common techniques are described below.

image

FIGURE 198-5 The posterior approach to the axillary nerve. The axillary nerve (anterior division depicted by black arrows; posterior division by black arrowhead) is seen exiting the quadrangular space between the teres major (TMa), the teres minor (TMi), the long head of the triceps (LT) and the humerus head (∗). The deltoid muscle (D) has been retracted anteriorly. The blue dotted line represents the skin incision over the posterior border of the deltoid muscle. The radial nerve (white arrow) can be seen exiting the triangular space formed by the TMa and the LT with the humeral shaft. The selected branch to the long head of the triceps is marked with a white arrowhead.

(From Mayo Foundation for Medical Education and Research, with permission. All rights reserved.)

image

FIGURE 198-6 Intraoperative photographs. Preparing for Leechavengvongs transfer. A, The superior lateral cutaneous nerve of the arm (double white asterisks) has been identified at the posterior border of the deltoid (D), which has been retracted ventrally. The radial nerve (white arrow in white rectangle) and a triceps branch (white arrowhead) can be seen inferiorly in the lower triangular space between the triceps long head (LT) and the teres major (TMa). The axillary nerve (black arrow in dotted white rectangle) can be seen above the teres major muscle and below the teres minor (TMi). B, Close-up photograph of the region of interest around the radial nerve (white rectangle in A). The selected triceps donor branch (white arrowhead) has been dissected free distally. C, Close-up photograph of the region of interest around the axillary nerve (dashed white rectangle in A). The posterior division (black arrowhead) is seen. The anterior division (black arrow) was selected as the recipient.

image

FIGURE 198-7 Double fascicular nerve transfer. A, The nerve to brachialis (recipient) and a redundant nerve fascicle from the median nerve (donor) are marked in green for future coaption. B, The nerve to biceps (recipient) and a redundant nerve fascicle from the ulnar nerve (donor) are marked in green for future coaption. C, Final orientation. LABC, lateral antebrachial cutaneous nerve.

(From Mayo Foundation for Medical Education and Research, with permission. All rights reserved.)

Spinal Accessory Nerve to Suprascapular Nerve Transfer

As described previously, this is most commonly done in the supraclavicular region (Fig. 198-2). Some surgeons are performing this more distally, that is, closer to the target supraspinatus muscle. The disadvantage of this procedure is that it entails a separate exposure. Moreover, the distal myelinated axon count of the donor spinal accessory nerve is reduced due to its terminal branching pattern. Through a separate posterior incision, one can harvest both the spinal accessory and the suprascapular nerves in the vicinity of the scapula. This technique will not be further discussed here.

Nerve to Triceps-Axillary Nerve (Leechavengvongs) Transfer

This may be performed in an isolated axillary nerve paralysis or in conjunction with other nerve grafts or nerve transfers for a C5/C6 BPI. This nerve transfer is most commonly performed using a posterior approach. The arm is placed across the patient’s chest and held by an assistant. The skin incision used parallels the posterior border of the affected deltoid muscle. The incision is deepened, taking care to preserve the cutaneous sensory branch of the axillary nerve. This is then followed down to the quadrangular space after reflecting the deltoid muscle anteriorly. At this point, the main stem of the nerve as well as its divisions (anterior and posterior) are identified. The anterior division is specifically dissected out from the adjacent soft tissue and is traced back into the main stem of the nerve to gain as much length as possible. Bleeding can be encountered here from the accompanying posterior circumflex humeral vessels. This should again be controlled delicately with a bipolar cautery forceps. The nerve is then transected deeply and clipped to a green background for future identification. We leave the posterior division of the axillary nerve intact, should spontaneous recovery ensue.

The radial nerve and its branches to the triceps are now identified in the triangular space. The interval between the long and lateral heads of the triceps is opened, and the radial nerve is readily exposed. Several triceps branches are identified, tagged with vessel loops and tested for function using a nerve stimulator. The longest, largest functioning motor radial branch to any of the triceps heads is identified. Other branches to the triceps and the main radial nerve are protected. The selected triceps branch is then traced distally to gain as much length as feasible. It is also traced proximally and separated from the main radial nerve so as to displace the pivot point closer towards the deltoid muscle. This permits not only adequate length to perform a direct graft-free nerve transfer but also provides a little extra length. The surgeon can trim the recipient nerve back closer to the motor point of the deltoid to enable faster and perhaps better muscle reinnervation. The suture line is later rechecked with the arm in a position of abduction and external rotation before final approximation (Figs. 198-5 and 198-6).

Double Fascicular Transfer for Elbow Flexion

The double fascicular transfer involves coaption of donors from the ulnar and median nerves onto the nerve to biceps and brachialis (Fig. 198-7). The theoretical advantage of performing this procedure is obvious as the brachialis is a more powerful elbow flexor than the biceps. The use of the additional donor and the inherent risk (albeit low) need to be carefully balanced. In our experience, clinical results have not demonstrated a functional advantage of the double fascicular transfer versus a single fascicular transfer.41

These donor and recipient nerves are found within the neurovascular bundle in the triceps-biceps groove of the mid-arm. A straight linear skin incision in the groove below the biceps, extending from the anterior axillary line to the distal one third–two thirds junction of the arm, is deepened through fat and fascia. The median nerve is generally the first structure to be reliably identified. The biceps muscle belly is then identified and retracted to look for the musculocutaneous nerve which lies on the deep surface of this muscle. Its separate branches to the biceps and brachialis muscles are then identified as is the lateral antebrachial cutaneous nerve. The ulnar nerve is then identified and dissected in the lower arm to a point 5 to 7 cm distal to the entry point of the musculocutaneous branch into the biceps muscle.

Once all nerves are identified, the biceps branch is mobilized in a proximal direction and transected. It is brought down to the ulnar nerve to help determine where the ulnar nerve should be dissected. With minimal internal neurolysis, a nerve stimulator is used to identify the fascicle(s) that gives mostly/only wrist flexion (the flexor carpi ulnaris fascicle). This is typically located in the 9 o’clock position of the ulnar nerve (closest to the biceps branch). The selected fascicle(s) comprising 10% to 20% of the ulnar nerve are then dissected as far proximally as possible within the substance of the ulnar nerve to gain maximal length before distal division for transfer onto the nerve to the biceps.

Slightly more distally, the median nerve fascicular transfer is performed. The brachialis branch is mobilized proximally, transected and swung towards the median nerve. We try to identify a median nerve fascicle for wrist flexion (i.e., the flexor carpi radialis); others use a flexor digitorum superficialis fascicle. Care should be taken to avoid use of the anterior interosseous nerve fascicle. The donor median nerve fascicle is transected distally and then coaption is accomplished.

Free-Functioning Muscle Transfer

An FFMT is based on the placement of a fasciomyocutaneous flap and its neurovascular pedicle in the region of the brachial plexus. The muscle classically transferred is the gracilis. The transverse cervical, suprascapular, thoracoacromial, and thoracodorsal arteries are amongst common donors. The venous outflow is channeled along the subclavian vein, the cephalic vein or venae comitantes of the donor blood vessels mentioned previously. The motor nerve to the muscle varies. The intercostals and the spinal accessory are favored when the patient has a panplexal injury.

In early reconstruction, the authors prefer to perform either a single gracilis FFMT for elbow and finger flexion (Fig 198-4) or a two-staged double gracilis FFMT performed 6 weeks apart for combined elbow flexion and wrist extension and finger flexion. Shoulder stability, elbow extension and hand sensation is also targeted in both reconstructive algorithms. FFMT, in the chronic setting for elbow flexion, can be done using any available donor (most commonly spinal accessory nerve or intercostals; occasionally an ulnar fascicle). Details of these microsurgical procedures are beyond the scope of this chapter and have been described elsewhere by our group.9 Secondary reconstructive procedures are often performed such as arthrodesis of the glenohumeral joint, carpometacarpal joint of the thumb and the wrist joint to optimize muscle pull vectors and are considered on an individual basis.

Other Rarely Performed Nerve Transfers

Medial Pectoral-Axillary/Musculocutaneous Nerve Transfer

This procedure is performed by some for neurotizing the axillary and musculocutaneous nerves in upper and middle trunk/C5,C6,C7 nerve level injuries. A direct transfer is feasible through the same infraclavicular approach and skin incision.37,38 The problems lie in that the donor nerve here is the sole functioning nerve supplying the pectoralis major, and sectioning it decreases shoulder function. Another major problem is the diameter mismatch between donor and recipients. The transfer onto the musculocutaneous nerve is satisfactory in most hands, but this procedure is being supplanted by the use of the Oberlin’s transfer, which decreases the time to reinnervation and can be performed solely within the arm.

Phrenico-Suprascapular/Axillary/Musculocutaneous Nerve Transfer

The advantages of using the phrenic nerve are several—it is easily accessible, fires continuously and is purely motor for all realistic purposes.42–48 Sufficiently long lengths can also be isolated especially with the use of endoscopy to harvest it in the chest.48 This, theoretically, enables direct nerve transfers without the use of grafts. Practically, when this nerve is harvested in the supraclavicular region, grafts are required for axillary and musculocutaneous nerve transfers. Though several reports indicate that the clinical effects of diaphragmatic palsy are transient, the authors’ experience indicates otherwise especially when simultaneous intercostal nerves are harvested. This may perhaps be related to racial variations in build and body mass indices as well as regional variations involving low- versus high-velocity motor vehicle accidents.

Contralateral C7 Transfer

This was initially developed as a significant source of remote extraplexal expendable motor neurons by Gu et al. especially in the restoration of hand function in patients with panplexal injuries.35,36,49–54 It is classically performed in two stages. In the first stage, standard nerve transfers aimed at gaining shoulder and elbow function are performed. Simultaneously, the normal contralateral plexus is explored and the C7 nerve/middle trunk is either used in toto or after hemisection as a donor coapted with either a reversed pedicled or a vascularized free ulnar (ipsilateral injured) nerve graft passed subcutaneously across the chest. Axonal growth is monitored clinically along the ulnar nerve graft using Tinel’s sign and SSEPs. Once the Tinel’s sign reaches the axilla, the patient undergoes the second stage of surgery when the distal part of the ulnar graft is connected to the injured median nerve. This theoretically provides for both sensory innervation of the hand as well as long finger flexor function. Although initial results were promising, they have not been reproducible, especially regarding independent hand function.55–60 Moreover, the risk to the only functioning extremity, though small, is not without significance. In the authors’ experience, results have been functionally disappointing.

Newer Directions

It would not be an exaggeration to state that the results obtained after performing nerve transfers have radically improved the formerly dismal prognosis after BPI (Table 198-6).61–75 Achieving hand function in patients with panplexal injury, once unobtainable, can now be achieved with aggressive techniques. We are using FFMT. Some groups are routinely using extended phrenic or contralateral C7 nerve transfers. Others are attempting direct reimplantation of ventral avulsed roots within the spinal cord.76

TABLE 198-6 Surgical Results Following Nerve Transfers

Recipient Nerve Donor Nerves Useful Postoperative Function (≥M3 MRC)
Suprascapular Spinal accessory
Phrenic
Contralateral C7		 70–100% 61–6366
75–100% 44,46,61,65
23.1*–100% 24
Axillary Triceps branch of radial
Spinal accessory
Medial pectoral
Motor intercostals
Thoracodorsal
Contralateral C7		 100% 40,63,67
75% 37
81.8% 75
63.2% 37
36v93.3% 62,74
20–23.1% *,19
MCN Ulnar nerve fascicle
Motor intercostal
Medial pectoral
Median nerve fascicle
Contralateral C7
Spinal accessory
Phrenic
Thoracodorsal		 64.7–100% 3–563
0–100% 37,61,62
85.7–90% 62,75
90–100% 72,73
52–100% 19,54,69–71
0–100% 61,64
16.6–100% 45,61
100% 74

*Mayo Clinic results (in press).

MCN, musculocutaneous nerve; MRC, Medical Research Council.

The extrapolation of nerve transfer techniques for single or distal nerves in the upper limb, to major nerves in the lower limb, or even the distal transected spinal cord can potentially change current management strategies.77–80 New pharmacologic agents, such as FK 506 may enhance neural regeneration and provide us with a new window of opportunity.81 The future for novel nerve transfers is bright.

Key References

Bertelli J.A., Ghizoni M.F. Reconstruction of C5 and C6 brachial plexus avulsion injury by multiple nerve transfers: spinal accessory to suprascapular, ulnar fascicles to biceps branch, and triceps long or lateral head branch to axillary nerve. J Hand Surg Am. 2004;29:131-139.

Carlsen B.T., Kircher M.F., Spinner R.J., et al. Comparison of single versus double nerve transfers for elbow flexion after brachial plexus injury. Plast Reconstr Surg. 2011;127:269-276.

Carlstedt T., Anand P., Hallin R., et al. Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J Neurosurg. 2000;93:237-247.

Chuang D.C. Contralateral C7 transfer (CC–7T) for avulsion injury of the brachial plexus. Tech Hand Up Extrem Surg. 1999;3:185-192.

Doi K., Muramatsu K., Hottori Y., Watanabe M. Reconstruction of upper extremity function in brachial plexopathy using double free gracilis flaps. Tech Hand Up Extrem Surg. 2000;4:34-43.

Gu Y., Xu J., Chen L., et al. Long term outcome of contralateral C7 transfer: a report of 32 cases. Chin Med J [Engl]. 2002;115:866-868.

Gu Y.D., Chen D.S., Zhang G.M., et al. Long-term functional results of contralateral C7 transfer. J Reconstr Microsurg. 1998;14:57-59.

Leechavengvongs S., Witoonchart K., Uerpairojkit C., Thuvasethakul P. Nerve transfer to deltoid muscle using the nerve to the long head of the triceps, part II: a report of 7 cases. J Hand Surg Am. 2003;28:633-638.

Loy S., Bhatia A., Asfazadourian H., Oberlin C. Ulnar nerve fascicle transfer onto to the biceps muscle nerve in C5–C6 or C5–C6–C7 avulsions of the brachial plexus. Eighteen cases. Ann Chir Main Memb Super. 1997;16:275-284. [French]

Mackinnon S.E., Novak C.B., Myckatyn T.M., Tung T.H. Results of reinnervation of the biceps and brachialis muscles with a double fascicular transfer for elbow flexion. J Hand Surg Am. 2005;30:978-985.

Mackinnon S.E., Novak C.B. Nerve transfers. New options for reconstruction following nerve injury. Hand Clin. 1999;15:643-666.

Merrell G.A., Barrie K.A., Katz D.L., Wolfe S.W. Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature. J Hand Surg Am. 2001;26:303-314.

Oberlin C., Beal D., Leechavengvongs S., et al. Nerve transfer to biceps muscle using a part of ulnar nerve for C5–C6 avulsion of the brachial plexus: anatomical study and report of four cases. J Hand Surg Am. 1994;19:232-237.

Samardzic M., Rasuli L., Grujici D., Milici B. Results of nerve transfers to the musculocutaneous and axillary nerves. Neurosurgery. 2000;46:93-101.

Samardzic M., Grujicic D., Rasulic L., Bacetic D. Transfer of the medial pectoral nerve: myth or reality? Neurosurgery. 2002;50:1277-1282.

Samii M. Nerve transfer. J Neurosurg. 2000;92:1068-1069.

Songcharoen P., Wongtrakul S., Mahaisavariya B., Spinner R.J. Hemi-contralateral C7 transfer to median nerve in the treatment of root avulsion brachial plexus injury. J Hand Surg Am. 2001;26:1058-1064.

Spinner R.J., Shin A.Y., Herbert-Blouin M., et al. Traumatic brachial plexus injury, Wolfe S.W., Hotchkiss R.N., Pederson W.C., Kozin S.H., editors. Green’s Operative Hand Surgery, 6th ed, vol. 2. Philadelphia: Elsevier Churchill Livingstone, 2010;1235-1295.

Sulaiman O.A., Kim D.D., Burkett C., Kline D.G. Nerve transfer surgery for adult brachial plexus injury: a 10-year experience at Louisiana State University. Neurosurgery. 2009;65:A55-A62.

Sungpet A., Suphachatwong C., Kawinwonggowit V. One-fascicle median nerve transfer to biceps muscle in C5 and C6 root avulsions of brachial plexus injury. Microsurgery. 2003;23:10-13.

Teboul F., Kakkar R., Ameur N., et al. Transfer of fascicles from the ulnar nerve to the nerve to the biceps in the treatment of upper brachial plexus palsy. J Bone Joint Surg (Am). 2004;86:1485-1490.

Terzis J.K., Kokkalis Z.T. Selective contralateral cC7 transfer in posttraumatic brachial plexus injuries: a report of 56 cases. Plast Reconstr Surg. 2009;123:927-938.

Terzis J.K., Konofaos P. Low-dose FK506 after contralateral C7 transfer to the musculocutaneous nerve using two different tubes: a study in rats. Ann Plast Surg. 2010;64:622-631.

Tung T.H., Mackinnon S.E. Nerve transfers: indications, techniques, and outcomes. J Hand Surg Am. 2010;35:332-341.

Witoonchart K., Leechavengvongs S., Uerpairojkit C., et al. Nerve transfer to deltoid muscle using the nerve to the long head of the triceps, part I: an anatomic feasibility study. J Hand Surg Am. 2003;28:628-632.

Numbered references appear on Expert Consult.

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