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Five Operations That Give the Best Results after Brachial Plexus Injury

Maldonado, Andrés A. M.D., Ph.D.; Bishop, Allen T. M.D.; Spinner, Robert J. M.D.; Shin, Alexander Y. M.D.

Plastic and Reconstructive Surgery: September 2017 - Volume 140 - Issue 3 - p 545–556
doi: 10.1097/PRS.0000000000003620
Hand/Peripheral Nerve: Original Article
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Summary: Treatment of brachial plexus injuries has improved slowly over the past 45 years. Changes in strategy, techniques, microsurgical equipment, and technology have expanded the surgical options for reconstructing these life-altering, highly complex injuries. The surgical techniques available include neurolysis, nerve repair, nerve grafting, nerve transfers, tendon transfer, muscle transfer, and other soft- and bony-tissue procedures. In this article, the authors have selected five surgical procedures (i.e., Oberlin procedure, Leechavengvongs procedure, free functional muscle transfer, radial nerve tendon transfers, and C5-C6 nerve grafting in obstetric birth palsy) that have consistently yielded good results in patients who require surgical reconstruction.

Supplemental Digital Content is available in the text.

Rochester, Minn.; and Frankfurt, Germany

From the Department of Neurologic Surgery and the Department of Orthopedic Surgery, Division of Hand Surgery, Mayo Clinic; and the Department of Plastic, Hand and Reconstructive Surgery, BG Unfallklinik Frankfurt.

Received for publication December 30, 2016; accepted March 2, 2017.

Disclosure: The authors have no financial interest to declare in relation to the content of this article. No external funding was received.

Supplemental digital content is available for this article. Direct URL citations appear in the text; simply type the URL address into any Web browser to access this content. Clickable links to the material are provided in the HTML text of this article on the Journal’s website (www.PRSJournal.com).

Alexander Y. Shin, M.D., Department of Orthopedic Surgery, Division of Hand Surgery, Mayo Clinic, 200 1st Street South West, Rochester, Minn. 55905, shin.alexander@mayo.edu

Treatment of brachial plexus injuries has improved slowly during the past 45 years, mainly because of improvement in strategy, techniques, microsurgical equipment, understanding anatomy, and technology. The techniques available to a surgeon include neurolysis, nerve repair, nerve grafting, nerve transfers, tendon transfer, muscle transfer, and other soft- and bony-tissue procedures. In this article, we present five operations (i.e., Oberlin procedure, Leechavengvongs procedure, free functional muscle transfer, radial nerve tendon transfers, and C5-C6 nerve grafting in obstetric palsy) that have consistently given good outcomes in patients undergoing brachial plexus reconstruction.

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OBERLIN PROCEDURE

Injury to the upper trunk (C5-C6) of the brachial plexus results in the loss of elbow flexion and shoulder abduction/external rotation.1 Restoration of elbow flexion is the primary goal in the reconstruction of upper extremity function. In 1994, Oberlin et al.2 described a novel nerve transfer of a portion of the normal ulnar nerve to the biceps motor branch of the musculocutaneous nerve to restore elbow flexion (Fig. 1). The outcome of this procedure [which today carries the eponym of that article’s senior author, and is often referred to as the “Oberlin procedure” (i.e., ulnar nerve fascicle transfer to the biceps motor branch in adult upper trunk or upper trunk and C7 injuries)] has resulted in excellent elbow flexion recovery with minimal deficits in the ulnar nerve distribution for patients with C5-C6 or even C5-C7 brachial plexus injuries.3

Fig. 1

Fig. 1

In 2005, Mackinnon et al.4 described a double nerve transfer whereby a portion of the median nerve is transferred to the brachialis branch of the musculocutaneous nerve in addition to the ulnar nerve transfer to the biceps branch of the musculocutaneous nerve (Figs. 2 and 3). Six of six patients achieved British Medical Research Council grade 4 or better elbow flexion strength. In 2006, Liverneaux et al. reported their findings in 10 patients treated with double nerve transfer to restore elbow flexion. They reported all 10 patients achieving British Medical Research Council grade 4 or better elbow flexion strength. In 2011, Carlsen et al.5 reported their experience comparing the single versus double fascicular transfer with respect to motor outcomes. The double nerve transfer group did not have statistically significant differences in elbow flexion or supination torque strength. Similar results were found by Martins et al.6 in a prospective randomized study. Based on these studies, we have recommended the single ulnar nerve fascicle transfer to the biceps motor branch with preservation of the median nerve. Occasionally, the double fascicular transfer may be considered when there is a recovering ulnar nerve lesion or patient preference or request for a double transfer.

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The idea introduced first by Brandt and Mac kinnon7 (medial pectoral nerves to reconstruct the musculocutaneous nerve in patients with proximal brachial plexus injuries) and then by Oberlin with the Oberlin procedure2 was a revolutionary concept: brachial plexus injuries were not treated where the injury was (in the nerve roots), but distal to it. This allowed for earlier recovery and improved outcomes, and expanded the time window for surgery in patients with late presentation. Even 20 years later, we still recognize distal nerve transfers as one of the best ways to improve elbow flexion after a C5-C6 brachial plexus injury. [See Video, Supplemental Digital Content 1, which demonstrates 1-year follow-up results after single fascicular transfer for elbow flexion (Oberlin procedure) performed 11 months after upper trunk injury in a 28-year-old man with an upper trunk injury where the shoulder recovered spontaneously and the musculocutaneous nerve did not. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C340. See Video, Supplemental Digital Content 2, which demonstrates 2.5-year follow-up results after double fascicular nerve transfer performed 7 months after upper trunk. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C341.]

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LEECHAVENGVONGS PROCEDURE

Injuries to the upper trunk (C5-C6) of the brachial plexus result in the loss of shoulder abduction and external rotation and elbow flexion.1 Restoration of shoulder abduction and external rotation is the second goal in reconstruction upper extremity function, after elbow flexion. In 2003, Leechavengvongs et al.8 described a novel nerve transfer of a triceps branch of the radial nerve to the axillary nerve to restore shoulder abduction [i.e., Leechavengvongs procedure (triceps nerve fascicle transfer to axillary motor branch in adult upper trunk injury)].

Seven patients with loss of shoulder abduction secondary to upper brachial plexus injuries were reported. All patients recovered deltoid power against resistance (M4), and no notable weakness of elbow extension was observed. The outcome of this procedure (which carries the eponym of the author, is known as the “Leechavengvongs” or “Somsak” procedure) has resulted in good shoulder abduction recovery without significant motor deficits in the triceps muscle after a C5-C6 brachial plexus injuries.9 We reported 21 patients who underwent triceps motor branch transfer for the treatment of isolated axillary nerve injury. The average Medical Research Council grade of deltoid muscle strength was 3.5. In the multiple linear regression model, the delay from injury to surgery, age of the patient, and body mass index of the patient were the important factors, in that order, that affected the outcome of this procedure.10 This procedure has become a preferred reconstruction in patients with C5-C6 root avulsions with loss of deltoid function (Figs. 4 through 6). [See Video, Supplemental Digital Content 3, which demonstrates triceps branch selection for the Leechavengvongs procedure. Note how we test different radial nerve branches, selecting the one with a stronger triceps contraction. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C342. See Video, Supplemental Digital Content 4, which demonstrates 2-year follow-up results after the Leechavengvongs procedure performed 9 months after isolated axillary nerve injury in an 8-year-old boy. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C343. See Video, Supplemental Digital Content 5, which demonstrates 2.5-year follow-up results after the Leechavengvongs procedure performed 6 months after upper trunk injury. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C344.] The triceps branch used remains a topic of debate as well; most surgeons select a sizable nerve branch that can be mobilized for direct repair. Triceps transfer is typically combined with concomitant spinal accessory nerve transfer to the suprascapular nerve, a procedure that can be performed from an anterior or posterior approach.

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There is controversy regarding the best treatment for postganglionic injury to C5 or a neuroma-in-continuity affecting the upper trunk and axillary nerve. In a patient with a viable spinal C5 or C6 nerve who is less than 6 months from injury, we prefer using it with cable nerve grafting to the posterior division of the upper trunk. In isolated axillary nerve injuries, the Leechavengvongs procedure and interpositional nerve grafting are the most commonly used techniques to restore isolated axillary nerve defects.10–12 Advocates of nerve grafting believe that a greater number of axons are being redirected to the axillary nerve, with improved motor function; however, this necessitates a meticulous axillary nerve exploration in a scarred bed to localize the location of the injury, careful attention to the blind zone of the axillary nerve, and harvest of an autologous sural nerve graft.13,14 The triceps branch nerve transfer is a relatively quick and straightforward operation with dissection outside the zone of injury, requires no nerve graft and associated donor-site morbidity, and in theory has quicker deltoid muscle reinnervation. Wolfe et al.12 demonstrated that in a mixed cohort of isolated axillary and combined nerve injuries, there was no statistically significant difference in functional outcomes between patients that had either the Leechavengvongs procedure or long nerve grafts (mean, 13.5 cm). A recent study from our institution of isolated axillary nerve injuries15 failed to demonstrate earlier reinnervation or better functional recovery with the triceps motor nerve transfer. The functional recovery was statistically superior in the axillary nerve grafting group compared with the nerve transfer group (British Medical Research Council grade, 4.3 versus 3.05; p < 0.05). This improved functional outcome with nerve grafting versus transfer could be a result of a more appropriate ratio of proximal nerve fibers to distal fibers (approximately 1:1 for nerve grafting and 0.46:1 for nerve transfer), a critical component of nerve repair. However, for scenarios in which a fast reinnervation is critical (injuries between 6 and 12 months or very proximal axillary nerve injuries), this nerve transfer permits a more direct deltoid reinnervation.

Injuries to the upper trunk (C5-C6) of the brachial plexus are usually treated combining both of the aforementioned procedures (Oberlin and Leechavengvongs nerve transfers) in addition to transfer of the spinal accessory nerve to the suprascapular nerve. These two innovative techniques offer the potential for superior functional recovery in patients with C5-C6 avulsion injuries.

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FREE FUNCTIONAL MUSCLE TRANSFER FOR ELBOW FLEXION AND RUDIMENTARY HAND FUNCTION RECONSTRUCTION

The pan-plexus injury (C5-T1) is the most challenging pattern in brachial plexus reconstruction, and a multidisciplinary approach combining all types of reconstruction modalities is fundamental to optimize the results of surgery. Elbow flexion is widely accepted as the most important function to restore after this type of complex injury.16 Traditionally, nerve grafting and transfer techniques have resulted in reliable restoration of elbow flexion when the procedure is undertaken within 6 to 9 months of injury.17–20 In many instances, however, delay in treatment or complete avulsion of the brachial plexus limits the reconstruction options. This has resulted in the use of free functional muscle transfer in conjunction with extraplexus motor nerves to restore function in the setting of brachial plexus avulsions or when the interval between injury and surgery is greater than 1 year.21–31 Free muscle transfer procedures produce reliable elbow flexion when treatment delay prevents nerve grafting or nerve transfers for restoration of biceps function, or when previous nerve grafting and/or nerve transfer has yielded unsatisfactory results and proximal muscle strength is insufficient to allow tendon transfers.19,21–29

A variety of muscles have been used for elbow flexion reconstruction (latissimus dorsi,28,32,33 rectus femoris33–36 or, more recently, medial gastrocnemius muscle37). The gracilis muscle for free functional muscle transfer has become our muscle of choice, with reliable outcomes over the past 15 years.21,38 We have previously reported our technique for harvesting the entire gracilis muscle and tendon through three incisions.39 Doi et al.25 described a double gracilis transfer to provide combined elbow flexion and extension, hand sensibility, and rudimentary hand grasp and release. In the first muscle transfer, the gracilis muscle is innervated by the spinal accessory nerve and anastomosed to the thoracoacromial trunk to produce elbow flexion and finger or wrist extension. In the second transfer, the gracilis is innervated by the motor intercostal nerves and anastomosed to the thoracodorsal artery to create finger flexion. The triceps is innervated with two additional motor intercostal nerves. [See Video, Supplemental Digital Content 6, which demonstrates 3-year follow-up results after a pan-plexus injury reconstructed with two gracilis free functional muscles transfer (Doi procedure). (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C345.] The sensory intercostal nerves are transferred to the median nerve for hand sensation (Fig. 7). At our institution, we have made modifications to the gracilis free functional muscle transfer originally described by Doi. We perform a single gracilis muscle transfer to restore elbow flexion and finger flexion, as our patients do not want two major operations in 6 weeks, and we attempt to gain similar function with a single operation. The muscle is tunneled into the forearm, beneath the lacertus fibrosis, to create a pulley effect, and is provisionally placed in its final position. The vascular anastomoses are preferentially performed end-to-end to the thoracoacromial artery and vein. The neurorrhaphy is completed with two motor intercostal nerves (third and fourth). Distally, the flexor digitorum profundus and flexor pollicis longus tendons are identified and sutured en masse in a position that creates key pinch and grasp. The gracilis tendon is Pulvertaft woven into the prepared flexor digitorum profundus and flexor pollicis longus tendons. Tension is placed on the graft to allow the fingers and thumb to close with elbow extension (Fig. 8). [See Video, Supplemental Digital Content 7, which demonstrates 14-month follow-up results after a pan-plexus injury reconstructed with a single gracilis free functional muscle transfer for elbow flexion and finger/thumb flexion. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C346.] A recent study has shown clinically and biomechanically that this distal attachment of the gracilis free functional muscle transfer to the flexor digitorum profundus and flexor pollicis longus tendons was superior in achieving elbow flexion strength, compared with the traditional gracilis-to-biceps tendon attachment.40

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In late presentation over 1 year from injury, free functional muscle transfer is ideal for restoring elbow flexion. [See Video, Supplemental Digital Content 8, which demonstrates 4-year follow-up results after a late pan-plexus injury reconstructed with one gracilis free functional muscle transfer for elbow flexion. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C347.] In injuries more recent than 9 months, we have reinnervated the biceps muscle simultaneously. A comparison of the outcome of intercostal nerve transfer to a gracilis free functional muscle transfer versus the musculocutaneous nerve demonstrated that 67.7 percent of patients in the free functional muscle transfer group achieved M3 or M4 elbow flexion compared with 41.9 percent of patients in the intercostal nerve–to–musculocutaneous nerve group.41 The difference was statistically significant (p < 0.05). Based on this study, the role of free functional muscle transfer in acute pan–brachial plexus avulsions should be seriously considered in lieu of nerve transfer alone for elbow flexion. Although we continue to use the intercostal nerves–to–musculocutaneous nerve transfer as a sole means of obtaining elbow flexion in selected cases (i.e., vascular injury), it is now often performed in combination with free functional muscle transfer when possible (intercostal nerve transfers–to–free functional muscle and musculocutaneous nerve).

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RADIAL NERVE TENDON TRANSFERS AFTER POSTERIOR CORD INJURY

Lesions of the posterior cord of the brachial plexus usually present with a very specific clinical picture. The mechanism of injury is still unclear, although it is considered quite similar to the mechanism for axillary nerve trauma, which consists usually of a direct blow to the shoulder.42 An axillary nerve and high radial neuropathy result in motor deficits, including loss of deltoid function, elbow extension, wrist extension, finger extension at the metacarpophalangeal joints, thumb extension, and thumb radial abduction; and sensory deficits in the posterior proximal and distal arm, forearm, and wrist. Patients also present with weak grip strength caused by the transmission of flexion force through an unstable wrist.43

Our experience, and that of others,42 has demonstrated that a combination of nerve grafts for proximal function (deltoid and triceps muscles) and tendon transfers for distal reconstruction (hand function) provide the most reliable and consistent results. We perform this set of procedures concomitantly, typically using two sets of surgeons. Nerve grafting of the radial nerve provides inconsistent results for distal targets and takes several years. The classic triple tendon transfer to restore wrist, thumb, and finger extension has been well described. The pronator teres is transferred to the extensor carpi radialis brevis for wrist extension, and the palmaris longus (or flexor digitorum superficialis if the palmaris longus is absent) is transferred to the rerouted extensor pollicis longus, and a wrist flexor (flexor carpi radialis or flexor carpi ulnaris) is used to restore finger extension. It is our preference to use the flexor carpi radialis rather than the flexor carpi ulnaris, as the important movement of wrist flexion and ulnar deviation (power grip) is preserved.44 These tendon transfers are highly reliable, with excellent long-term results in wrist, finger, and thumb mobility and in patient satisfaction.45

Some authors prefer to use nerve transfers instead of the classic tendon transfers for wrist, finger, and thumb extension. Nerve branches of the flexor digitorum superficialis to the extensor carpi radialis brevis nerve branch and branches of the flexor carpi radialis and palmaris longus to the posterior interosseous nerve are the most common ones. Ray and Mackinnon46 report greater than M4 wrist and finger extension in 11 of 19 patients; however, five of the 19 patients obtained minimal finger extension and one patient failed to recover either wrist or finger extension. Nine of these patients underwent simultaneous pronator teres–to–extensor carpi radialis brevis tendon transfers and nerve transfers, confounding the results of nerve transfers versus tendon transfers. Our concern related to these nerve transfers is that if they failed, there are limited options for tendon transfer that remain because the nerve branches to the usual donor tendons have been sacrificed by the nerve transfer; in addition, unacceptable weak tendon-muscle groups may result. Given the excellent functional results with tendon transfers and the significantly faster recovery, we have preferred radial nerve tendon transfers over nerve transfers. We typically perform tendon transfers for residual radial neuropathy after brachial plexus injuries in lieu of nerve transfers for the reasons listed above. [See Video, Supplemental Digital Content 9, which demonstrates a 27-year-old woman with posterior cord injury who underwent reconstruction with posterior cord sural nerve grafting for triceps function and radial nerve tendon transfers performed 4 months after injury. Two months after radial nerve tendon transfer (pronator teres–to–extensor carpi radialis brevis, flexor carpi radialis–to–extensor digitorum communis, and palmaris longus–to–extensor pollicis longus), hand function is excellent. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C348. See Video, Supplemental Digital Content 10, which demonstrates the same patient 12 months after posterior cord sural nerve grafting to the triceps; triceps function is antigravity. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C349.]

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C5-C6 NERVE GRAFTING AFTER OBSTETRIC BRACHIAL PALSY INJURY

The origin of newborn palsies is traumatic and not congenital. Lesions are caused by traction applied on the roots during the combined lowering of the shoulder and inclination of the cervical spine to the contralateral side. Two clinical appearances predominate: paralysis of the upper roots and complete paralysis. Paralysis of the upper roots (Erb palsy47) involves C5 and C6 with or without C7 roots. The upper limb is held in internal rotation and pronation, and active abduction is not possible. The elbow is slightly flexed (paralysis of C5-C7) or fully extended (paralysis of C5 and C6), and the wrist and sometimes the fingers are flexed.47

The major clinical dilemma resulting from the uncertainty regarding spontaneous neurologic recovery is to determine whether surgical exploration and nerve reconstruction are warranted in infants without antigravity return of C5-C7 function at 3, 4, 5, or 6 months of age. Disagreement among surgeons is common regarding surgical indications.48 This lack of clarity creates large regional variations in care and makes decision-making difficult for parents. During the observation period, elbow flexion movement possibly returns by 3 months, with antigravity flexion by 6 months. If the patient does not achieve active elbow flexion by 6 months, surgical exploration is with nerve reconstruction or transfer as indicated and/or preferred.

Priorities in pediatric reconstruction are as follows: hand, elbow flexion, and shoulder external rotation/abduction. In patients with an upper trunk injury, the goals of reconstruction are elbow flexion and shoulder external rotation and abduction. We routinely explore the brachial plexus through a supraclavicular approach. In the presence of a viable C5 nerve as confirmed through intraoperative electrophysiologic testing, cabled sural nerve grafts to the posterior division of the upper trunk (which would include the axillary nerve) and typically the suprascapular nerve are used to reinnervate the shoulder. In the presence of a functional C6 nerve as confirmed through intraoperative electrophysiologic testing, cabled sural nerve grafts to the anterior division of the upper trunk (targeting the musculocutaneous nerve) are performed. Two main theories have been postulated regarding the better results with nerve grafting in children compared with adults: the enhanced regenerative capacity of nerves and the shorter distances for regeneration in children. Experimental studies in animals have shown that the number of larger myelinated fibers crossing the repair site is superior in fetal compared with adult animals, with a higher total percentage of remyelinated nerves at the experimental endpoint.49,50 We tend to perform nerve grafting over nerve transfers in patients with postganglionic obstetric brachial plexus palsy when surgery is performed relatively early (before 9 months) based on the good or excellent results of this type of reconstruction; in addition, we avoid the possible donor-site morbidity that can occur with nerve transfers (including exacerbated winging of the scapula following use of the spinal accessory nerve) and attempt to achieve sensory recovery in the hand.

According to Gilbert et al.,51 elbow results should be good even in cases with severe or even complete paralysis: 81 percent show good or excellent results after 8 years. For shoulder, at 4 years, 80 percent of children have good or excellent results in C5-C6 lesions; in C5-C7 lesions, only 61 percent have good or excellent results; in complete palsy, the results after 8 years are 77 percent with average, good, or excellent results. [See Video, Supplemental Digital Content 11, which demonstrates 6-year follow-up after upper trunk obstetric brachial plexus reconstructed with grafting of C5 to the posterior division of the upper trunk, C6 to the anterior division of the upper trunk, and spinal accessory–to–suprascapular nerve transfer. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C350. See Video, Supplemental Digital Content 12, which demonstrates 4-year follow-up after upper trunk obstetric brachial plexus reconstructed with grafting of C5 to the posterior division of the upper trunk and suprascapular nerve and C6 to the anterior division of the upper trunk. (Copyright Mayo Foundation for Medical Education and Research.) See http://links.lww.com/PRS/C351.]

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CONCLUSIONS

We have described five operations based on nerve grafting, nerve transfers, tendon transfer, and free muscle transfer that have completely changed the prognosis and recovery of different brachial plexus injuries. However, to offer the entire spectrum of reconstructive options and possibly achieve the best outcomes, it is important to critically evaluate patients as soon as possible by a multidisciplinary team of surgeons. Although new techniques may continue to be developed and new therapies (such as tissue engineering and stem cell technology) may emerge as future options, the five operations described (some new and some old) have given consistently good outcomes and have made significant changes in the lives of our patients.

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