GENERAL SCIENTIFIC SESSION 4 GENERAL SCIENTIFIC SESSION 4
Advances in the Repair of Peripheral Nerve Injury Robert J. Spinner, MD*‡ Alexander Y. Shin, MD‡ Allen T. Bishop, MD‡ *Department of Neurologic Surgery and ‡Orthopedics, Mayo Clinic, Rochester, Minnesota Correspondence: Robert J. Spinner, MD, Mayo Clinic, Gonda 8-214, Rochester, MN. E-mail: [email protected]
Copyright © 2015 by the Congress of Neurological Surgeons.
T
he armamentarium of a peripheral nerve surgeon includes neurolysis, nerve repair, nerve grafting, nerve transfers, and other soft tissue and bony procedures. Nerve transfers (neurotization) are increasingly being performed. By exploiting anatomy and neurobiology, peripheral nerve surgeons have introduced new techniques that are changing the way we think about and perform nerve reconstruction and improving clinical outcomes.
RECENT PAST Over the past several decades, considerable strides have been made in peripheral nerve surgery, which improved clinical results. Techniques such as intraoperative electrophysiology, microneurosurgery, and nerve grafting techniques allowed surgeons to better assess and repair or reconstruct nerves that had been injured. Results plateaued, often at a suboptimal level. In some cases, results have been adequate; in others cases, poor. New interest in and enthusiasm for nerve transfers (neurotization), a technique introduced approximately a century ago, are providing peripheral nerve surgeons with innovative ways to find opportunities when faced with the inherent challenges and limitations posed by neurobiology.
NERVE TRANSFERS: A PARADIGM SHIFT, A NEW CONSTRUCT
The 2014 CNS Annual Meeting presentation on which this article is based is available at http://bit.ly/1FfQmNV.
Nerve grafting represents a method to bridge nerve gaps. A nerve transfer allows the opportunity to bypass the zone of injury altogether. A functioning nerve, part of a nerve (fascicle), or nerve branch that is expendable or redundant is redirected to a more important but nonfunctioning nerve (ie, “robbing from the rich and giving to the poor”). This technique offers many important advantages that facilitate, expedite, and improve recovery and extend the time for the surgical window of opportunity to remain open: It can be done closer to the end organ; it allows a relatively large number of “pure” axons to be transferred to a target; and whenever possible, the donor nerve transferred is synergistic with the recipient nerve so that the
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individual can relearn the new function easily and independently. A wide variety of nerve transfers have been introduced to subserve different functions. Outcomes, whether for shoulder, elbow, or even hand function, have improved. Surgeons, once satisfied with M3 or better results (active motion through a full range, against gravity), are now consistently striving for and typically obtaining M4 results (active motion against resistance, through a full range, against gravity) at an earlier time; the need for secondary procedures to augment results and function has greatly diminished. The indications for nerve transfers are expanding. This technique once was performed only in preganglionic injuries when nerve grafting could not be considered because of the irreparable injury. Nerve transfer is now being done preferably in postganglionic injury situations rather than nerve grafting. Nerve transfer can also be done to power a free-functioning muscle transfer (FFMT). Nerve transfer has created a resurgence of interest (ie, a renaissance) in peripheral nerve surgery. It offers a new novel approach to exploit anatomy in the hope of improving clinical outcomes to another level.
NERVE TRANSFER: TACKLING THE NEUROBIOLOGICAL CHALLENGES AND CREATING CLINICAL OPPORTUNITIES For successful nerve regeneration, we need to consider 3 important and interrelated variables: time, distance, and quality. Time By and large, nerve regeneration occurs at a slow rate (1 in/mo). Although surgeons have not been able to accelerate nerve regeneration, earlier surgery can be performed. Surgery 3 to 6 months after closed injury is routinely recommended; in many cases and for many reasons, surgery may be performed after 6 months. In these situations, early (2-3 months) and even “ultraearly” (,1 month) surgery is being performed by some groups of experienced surgeons for patients with severe
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PERIPHERAL NERVE INJURY REPAIR ADVANCES
brachial plexus lesions in whom there is a high clinical suspicion of rupture or avulsion. The major benefits of this approach include reconstruction at a physiologically beneficial time frame for lesions that would not otherwise recover and performance of surgery before scarring ensued. The advantages of operating early must be weighed against the disadvantages of operating too early, including operating unnecessarily if a nerve were to recovery spontaneously and making operative decisions without having all of the available information such as reliable intraoperative electrophysiology. Distance Injuries to peripheral nerve often occur proximally such as in the neck or axilla, and the target organ may be in the hand. The long distance necessary for regeneration compounds the slow rate of regeneration. In these cases, recovery typically takes years to occur—when it occurs. Not surprisingly, it is often incomplete. Although we cannot change the location of the injury, we can change the location of the reconstruction and decrease the distance/time for regeneration. Quality Quality of regeneration is disappointing. Alpha motor neurons in the spinal cord die quickly after injury. Dispersion (axonal confusion) occurs at the repair site.1 Target muscles undergo secondary changes. Even if the nerve reaches the end organ, the muscle end organ may not be able to be reinnervated. Although we have not been able to enhance regeneration by improving the interface between nerve ends by decreasing scarring, nerve transfer has allowed a more targeted type of reconstruction with a favorable ratio of motor axons of the donor and recipient close to the muscle for example.
APPLICATION OF NERVE TRANSFERS TO BRACHIAL PLEXUS SURGERY Brachial Plexus Surgery Brachial plexus surgery, because of the proximal site of preganglionic or postganglionic injury and distal targets, represents an extremely challenging situation. In many cases, nerve transfer can be performed safely and easily in a pristine location away from the zone of injury and scarring. Ideally, it can be done distally. Nerve transfer is increasingly being used in many different circumstances: for brachial plexus and peripheral nerves, for adult and obstetrical cases, and for motor and sensory nerves. Nerve transfer is being performed around the world with increasing enthusiasm. We can apply the use of nerve transfers in 2 common situations: upper plexus pattern and complete brachial plexus injuries. Upper Plexus Pattern Patients with an upper pattern (C5-6 or C5-7 injuries) have paralysis of shoulder abduction/external rotation and elbow flexion. Elbow flexion is considered by most surgeons to be the
CLINICAL NEUROSURGERY
most important goal of reconstruction. The standard operation for preganglionic injuries by many historically entails 3 or 4 intercostal nerves being transferred to the musculocutaneous nerve but with varying degrees of success for elbow flexion. A novel technique described by Christophe Oberlin in 1994 involves transfer of 1 to 2 fascicles of the intact ulnar nerve (destined to the flexor carpi ulnaris) directly to the biceps motor branch of the musculocutaneous nerve in the proximal arm.2 He and then others have shown that the so-called Oberlin technique can be done not only effectively but safely (without donor morbidity). A modified set of nerve transfers, double fascicular transfer, was introduced separately by Susan Mackinnon and Oberlin.3,4 This combines the Oberlin transfer concomitantly with a second nerve reconstruction: transfer of a fascicle of the intact median nerve (to either the flexor carpi radialis or flexor digitorum superficialis) to the brachialis motor branch of the musculocutaneous nerve in the mid arm (Note that the brachialis muscle, akin to the biceps brachii, is a strong elbow flexor; Figure 1). The rationale for this double fascicular transfer approach is that 2 repairs are better than 1.5 Both the single (Oberlin procedure) and double fascicular nerve transfer techniques for elbow flexion allow .75% to 90% M4 recovery and early recovery beginning within several months without objective or subjective donor morbidity.6,7 They have been quickly adopted. These nerve transfer techniques have been used preferentially even in situations of postganglionic injury in which nerve grafting could be done and with better outcomes.8-11 Similar strategies are regularly applied to shoulder reinnervation. Patients with preganglionic injuries can be treated with single or preferably double nerve transfers.12 Typically, the spinal accessory (via an anterior or posterior approach) is transferred to the suprascapular nerve, and a triceps branch is transferred to the anterior division of axillary nerve.13 In patients with postganglionic injuries, many surgeons would perform nerve grafting, whereas others would opt for nerve transfers. Because of the success and ease of these types of nerve transfers, many surgeons are using a nerve transfer distally rather than nerve grafts proximally for isolated nerve (ie, musculocutaneous or axillary) injuries.14 These techniques have also been applied to novel circumstances (eg, after tumor reconstruction, radiation, inflammation, etc; Figure 2). Complete Brachial Plexus Injuries Patients with complete lesions (C5-T1) have a flail limb with an insensate hand. In some of these cases, there may only be 1 available nerve for grafting; in some cases, the lesions are all preganglionic, and there are no nerves available for grafting. Because of the paucity of suitable intraplexal or extraplexal donor nerves, there are limited options for reconstruction (nerve grafting or conventional nerve transfers). In the past, some surgeons would offer a trans-humeral amputation. A common nerve reconstructive approach would be to attempt to restore a stable shoulder and elbow flexion with nerve grafting or nerve transfers and/or shoulder arthrodesis. In general, hand function could not be
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FIGURE 1. Illustration shows double fascicular nerve transfer. A, median nerve fascicular transfer to the biceps (overlying insets a-c). B, ulnar nerve fascicular transfer to the biceps (overlying insets a-c). C, the completed double nerve transfers for elbow flexion. br, branch; LABC, lateral antebrachial cutaneous nerve; n, nerve. Reproduced with permission from the Mayo Foundation (2015).
achieved with nerve grafting or standard nerve transfers (ie, intercostals and spinal accessory) because regeneration is too slow and the distal target is too far away.15 More aggressive nerve transfer techniques are being used by some groups with some success at restoring hand function. These include contralateral C7 or extended phrenic nerve transfer and FFMT. Contralateral C7 offers a large number of potentially untapped axons. The phrenic nerve is readily available in the surgical field and likewise is typically available (ie, functioning), even in severe panplexal lesions; because it is always firing, it may have an intrinsic advantage to its use. The morbidity of the use of these nerves, although somewhat controversial, seems acceptable on the basis of reports in the literature. Truly independent use of contralateral C7 may be difficult to obtain. Long-term risks of phrenic nerve harvest in adults are not fully known. Novel
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techniques are being used to improve regeneration: prespinal routes for contralateral C716 and an extended phrenic nerve17 harvested endoscopically in the chest near the diaphragm. Both techniques effectively shorten the distances to target organs. The Mayo Brachial Plexus team has opted to use a combination of techniques, including FFMT,18 in patients with panplexal injury who desire an attempt at hand function. The anatomy of the gracilis is favorable for FFMT, especially for recovery of distal function. The muscle belly of the gracilis is innervated relatively proximally; it has a long tendon that can be further extended. These attributes can be exploited to target distal recovery (Figure 3). We have modified a 2-stage FFMT procedure by Doi et al19 into a single procedure. Our approach combines nerve grafting, when available, with nerve transfers and a single-stage FFMT. We explore and record from upper elements of the
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PERIPHERAL NERVE INJURY REPAIR ADVANCES
CLINICAL NEUROSURGERY
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FIGURE 2. A 60-year-old woman with a history of a radiation-induced malignant peripheral nerve sheath tumor 2 decades after treatment of a tongue squamous cell carcinoma. She had local and regional metastases at the time. She had undergone multiple surgeries, including flap coverage for infections and osteomyelitis. She had done well in the intervening years until she presented with progressive pain in the right volar forearm and paralysis of shoulder abduction and severe weakness in elbow flexion over 3 months. A, coronal short T1 inversion recovery image revealed a fusiform, irregularly shaped mass involving the brachial plexus. Biopsy confirmed a grade 2 malignant peripheral nerve sheath tumor. B, at operation, an infiltrative lesion (arrow) was seen in the upper trunk (UT). C, a wide resection of the extensive tumor (Tm) was performed involving C5-7 proximally to the level of the divisions distally. AD, anterior division of upper trunk; PN, phrenic nerve; SSN, suprascapular nerve. D, resected specimen with negative margins. One week later, she underwent a double fascicular transfer using ulnar and median nerve fascicles to biceps and brachialis muscles. E and F, she regained Medical Research Council grade 4 elbow flexion at 1 year followup and was able to perform activities of daily living quite effectively. She has done well from an oncological perspective 5 years after the resection. Radiation-induced changes to the neck are observed.
brachial plexus. If no nerve is available, then secondary reconstruction is used for the shoulder. If a spinal nerve is available, nerve grafting is done for shoulder function. Two
motor intercostals are transferred to the biceps motor branch and 2 to the FFMT (gracilis). Vascular repairs are done with the thoracoacromial vessels. The FFMT provides an opportunity for further elbow flexion and some finger flexion. The gracilis muscle is fixed to the clavicle and passed subcutaneously in the arm, and its tendon is passed deep to the bicipital aponeurosis and prolonged, woven into the finger flexors in the forearm. Sensory intercostals are also harvested and transferred to the lateral cord contribution of the median nerve to provide some protective radial-side finger sensation. Spinal accessory nerve is lengthened with a graft to innervate a triceps branch. At a later date, the wrist and thumb are fused to improve finger flexion. This complex form of microsurgical reconstruction can restore some useful and meaningful function.
FORMULA FOR SUCCESS We believe that nerve transfer offers the ability to exploit surgical anatomy against the limitations of neurobiology. By
FIGURE 3. This illustration shows a modified 1-stage free-functioning muscle transfer (FFMT) technique used to obtain finger flexion. The gracilis muscle with its skin paddle is anchored to the clavicle and passed in the arm; its long tendon is passed beneath the bicipital aponeurosis in the elbow region and woven into the finger flexors in the forearm. Intercostal neurotization of the FFMT and the native biceps is shown, along with the vascular repair with the thoracoacromial vessels. Reproduced with permission from the Mayo Foundation (2015).
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FIGURE 4. A formula for nerve regeneration.
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manipulating the variables of time, distance, and quality, one can improve clinical outcomes and value (Figure 4).
CONCLUSION Restoration of function in peripheral nerve injuries often involves bridging (grafting) or bypassing (nerve transfers) zones of injury. Improved nerve reconstructive strategies are necessary to improve clinical outcomes. By thinking creatively and exploiting anatomy, surgeons have introduced novel techniques, expanded clinical applications, and improved outcomes. The introduction of nerve transfers, particularly distal ones, has revolutionized the way in which peripheral nerve surgeons are thinking about problems and proposing potential solutions. The future of peripheral nerve surgery is bright. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Brushart TM, Mathur V, Sood R, Koschorke GM. Joseph H. Boyes Award: dispersion of regenerating axon across enclosed neural gaps. J Hand Surg Am. 1995;20(4):557-564. 2. Oberlin C, Béal D, Leechavengvongs S, Salon A, Dauge MC, Sarcy JJ. Nerve transfer to biceps muscle using a part of ulnar nerve for C5-6 avulsions of the brachial plexus: anatomical study and report of four cases. J Hand Surg Am. 1994; 19(2):232-237. 3. Mackinnon SE, Novak CB, Myckatyn TM, Tung TH. Results of reinnervation of the biceps and brachialis muscles with a double fascicular transfer for elbow flexion. J Hand Surg Am. 2005;30(5):978-985. 4. Liverneaux PA, Diaz LC, Beaulieu JY, Durand S, Oberlin C. Preliminary results of double nerve transfer to restore elbow flexion in upper trunk brachial plexus palsies. Plast Reconstr Surg. 2006;117:915-919. 5. Tung TH, Novak CB, Mackinnon SE. Nerve transfers to the biceps and brachialis branches to improve elbow flexion strength after brachial plexus injuries. J Neurosurg. 2003;98(2):313-318.
CLINICAL NEUROSURGERY
6. Sungpet A, Suphachatwong C, Kawinwonggowit V, Patradul A. Transfer of a single fascicle from the ulnar nerve to the biceps muscle after avulsions of upper roots of the brachial plexus. J Hand Surg Br. 2000;25(4):325-328. 7. Teboul F, Kakkar R, Ameur N, Beaulieu JY, Oberlin C. 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-A(7):1485-1490. 8. Garg R, Merrell GA, Hillstrom HJ, Wolfe SW. Comparison of nerve transfers and nerve grafting for traumatic upper plexus palsy: a systematic review and analysis. J Bone Joint Surg Am. 2011;93(9):819-829. 9. Yang LJ, Chang KW, Chung KC. A systematic review of nerve transfer and nerve repair for the treatment of adult upper brachial plexus injury. Neurosurgery. 2012; 71(2):417-429. 10. Dy CJ, Garg R, Lee SK, Tow P, Mancuso CA, Wolfe SW. A systematic review of outcomes reporting for brachial plexus reconstruction. J Hand Surg Am. 2015;40 (2):308-313. 11. Socolovsky M, Martins RS, Di Masi G, Siqueira M. Upper brachial plexus injuries: grafts vs ulnar fascicle transfer to restore biceps muscle function. Neurosurgery. 2012;71(2 suppl operative):ons227-ons232. 12. Merrell GA, Barrie KA, Katz DL, Wolfe SW. 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(2):303-314. 13. 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(4):633-638. 14. Lee JY, Kircher MF, Spinner RJ, Bishop AT, Shin AY. Factors affecting outcomes of triceps motor branch transfer for isolated axillary nerve injury. J Hand Surg Am. 2012;37(11):2350-2356. 15. Narakas AO, Hentz VR. Neurotization in brachial plexus injuries: indication and results. Clin Orthop Relat Res. 1988;(237):43-56. 16. Xu L, Gu Y, Xu J, Lin S, Chen L, Lu J. Contralateral C7 transfer via the prespinal and retropharyngeal route to repair brachial plexus avulsion: a preliminary report. Neurosurgery. 2008;63(3):553–558. 17. Xu WD, Gu YD, Xu JG, Tan LJ. Full-length phrenic nerve transfer by means of video-assisted thoracic surgery in treating brachial plexus avulsion injury. Plast Reconstr Surg. 2002;110(1):104-109. 18. Barrie KA, Steinmann SP, Shin AY, Spinner RJ, Bishop AT. Gracilis free muscle transfer for restoration of function after complete brachial plexus avulsion. Neurosurg Focus. 2004;16(5):E8. 19. Doi K, Muramatsu K, Hattori Y, et al. Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexus. Indications and long-term results. J Bone Joint Surg Am. 2000;82(5): 652-666.
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Advances in the Repair of Peripheral Nerve Injury Robert J. Spinner, MD*‡ Alexander Y. Shin, MD‡ Allen T. Bishop, MD‡ *Department of Neurologic Surgery and ‡Orthopedics, Mayo Clinic, Rochester, Minnesota Correspondence: Robert J. Spinner, MD, Mayo Clinic, Gonda 8-214, Rochester, MN. E-mail: [email protected]
Copyright © 2015 by the Congress of Neurological Surgeons.
T
he armamentarium of a peripheral nerve surgeon includes neurolysis, nerve repair, nerve grafting, nerve transfers, and other soft tissue and bony procedures. Nerve transfers (neurotization) are increasingly being performed. By exploiting anatomy and neurobiology, peripheral nerve surgeons have introduced new techniques that are changing the way we think about and perform nerve reconstruction and improving clinical outcomes.
RECENT PAST Over the past several decades, considerable strides have been made in peripheral nerve surgery, which improved clinical results. Techniques such as intraoperative electrophysiology, microneurosurgery, and nerve grafting techniques allowed surgeons to better assess and repair or reconstruct nerves that had been injured. Results plateaued, often at a suboptimal level. In some cases, results have been adequate; in others cases, poor. New interest in and enthusiasm for nerve transfers (neurotization), a technique introduced approximately a century ago, are providing peripheral nerve surgeons with innovative ways to find opportunities when faced with the inherent challenges and limitations posed by neurobiology.
NERVE TRANSFERS: A PARADIGM SHIFT, A NEW CONSTRUCT
The 2014 CNS Annual Meeting presentation on which this article is based is available at http://bit.ly/1FfQmNV.
Nerve grafting represents a method to bridge nerve gaps. A nerve transfer allows the opportunity to bypass the zone of injury altogether. A functioning nerve, part of a nerve (fascicle), or nerve branch that is expendable or redundant is redirected to a more important but nonfunctioning nerve (ie, “robbing from the rich and giving to the poor”). This technique offers many important advantages that facilitate, expedite, and improve recovery and extend the time for the surgical window of opportunity to remain open: It can be done closer to the end organ; it allows a relatively large number of “pure” axons to be transferred to a target; and whenever possible, the donor nerve transferred is synergistic with the recipient nerve so that the
146 | VOLUME 62 | NUMBER 1 | AUGUST 2015
individual can relearn the new function easily and independently. A wide variety of nerve transfers have been introduced to subserve different functions. Outcomes, whether for shoulder, elbow, or even hand function, have improved. Surgeons, once satisfied with M3 or better results (active motion through a full range, against gravity), are now consistently striving for and typically obtaining M4 results (active motion against resistance, through a full range, against gravity) at an earlier time; the need for secondary procedures to augment results and function has greatly diminished. The indications for nerve transfers are expanding. This technique once was performed only in preganglionic injuries when nerve grafting could not be considered because of the irreparable injury. Nerve transfer is now being done preferably in postganglionic injury situations rather than nerve grafting. Nerve transfer can also be done to power a free-functioning muscle transfer (FFMT). Nerve transfer has created a resurgence of interest (ie, a renaissance) in peripheral nerve surgery. It offers a new novel approach to exploit anatomy in the hope of improving clinical outcomes to another level.
NERVE TRANSFER: TACKLING THE NEUROBIOLOGICAL CHALLENGES AND CREATING CLINICAL OPPORTUNITIES For successful nerve regeneration, we need to consider 3 important and interrelated variables: time, distance, and quality. Time By and large, nerve regeneration occurs at a slow rate (1 in/mo). Although surgeons have not been able to accelerate nerve regeneration, earlier surgery can be performed. Surgery 3 to 6 months after closed injury is routinely recommended; in many cases and for many reasons, surgery may be performed after 6 months. In these situations, early (2-3 months) and even “ultraearly” (,1 month) surgery is being performed by some groups of experienced surgeons for patients with severe
www.neurosurgery-online.com
Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
PERIPHERAL NERVE INJURY REPAIR ADVANCES
brachial plexus lesions in whom there is a high clinical suspicion of rupture or avulsion. The major benefits of this approach include reconstruction at a physiologically beneficial time frame for lesions that would not otherwise recover and performance of surgery before scarring ensued. The advantages of operating early must be weighed against the disadvantages of operating too early, including operating unnecessarily if a nerve were to recovery spontaneously and making operative decisions without having all of the available information such as reliable intraoperative electrophysiology. Distance Injuries to peripheral nerve often occur proximally such as in the neck or axilla, and the target organ may be in the hand. The long distance necessary for regeneration compounds the slow rate of regeneration. In these cases, recovery typically takes years to occur—when it occurs. Not surprisingly, it is often incomplete. Although we cannot change the location of the injury, we can change the location of the reconstruction and decrease the distance/time for regeneration. Quality Quality of regeneration is disappointing. Alpha motor neurons in the spinal cord die quickly after injury. Dispersion (axonal confusion) occurs at the repair site.1 Target muscles undergo secondary changes. Even if the nerve reaches the end organ, the muscle end organ may not be able to be reinnervated. Although we have not been able to enhance regeneration by improving the interface between nerve ends by decreasing scarring, nerve transfer has allowed a more targeted type of reconstruction with a favorable ratio of motor axons of the donor and recipient close to the muscle for example.
APPLICATION OF NERVE TRANSFERS TO BRACHIAL PLEXUS SURGERY Brachial Plexus Surgery Brachial plexus surgery, because of the proximal site of preganglionic or postganglionic injury and distal targets, represents an extremely challenging situation. In many cases, nerve transfer can be performed safely and easily in a pristine location away from the zone of injury and scarring. Ideally, it can be done distally. Nerve transfer is increasingly being used in many different circumstances: for brachial plexus and peripheral nerves, for adult and obstetrical cases, and for motor and sensory nerves. Nerve transfer is being performed around the world with increasing enthusiasm. We can apply the use of nerve transfers in 2 common situations: upper plexus pattern and complete brachial plexus injuries. Upper Plexus Pattern Patients with an upper pattern (C5-6 or C5-7 injuries) have paralysis of shoulder abduction/external rotation and elbow flexion. Elbow flexion is considered by most surgeons to be the
CLINICAL NEUROSURGERY
most important goal of reconstruction. The standard operation for preganglionic injuries by many historically entails 3 or 4 intercostal nerves being transferred to the musculocutaneous nerve but with varying degrees of success for elbow flexion. A novel technique described by Christophe Oberlin in 1994 involves transfer of 1 to 2 fascicles of the intact ulnar nerve (destined to the flexor carpi ulnaris) directly to the biceps motor branch of the musculocutaneous nerve in the proximal arm.2 He and then others have shown that the so-called Oberlin technique can be done not only effectively but safely (without donor morbidity). A modified set of nerve transfers, double fascicular transfer, was introduced separately by Susan Mackinnon and Oberlin.3,4 This combines the Oberlin transfer concomitantly with a second nerve reconstruction: transfer of a fascicle of the intact median nerve (to either the flexor carpi radialis or flexor digitorum superficialis) to the brachialis motor branch of the musculocutaneous nerve in the mid arm (Note that the brachialis muscle, akin to the biceps brachii, is a strong elbow flexor; Figure 1). The rationale for this double fascicular transfer approach is that 2 repairs are better than 1.5 Both the single (Oberlin procedure) and double fascicular nerve transfer techniques for elbow flexion allow .75% to 90% M4 recovery and early recovery beginning within several months without objective or subjective donor morbidity.6,7 They have been quickly adopted. These nerve transfer techniques have been used preferentially even in situations of postganglionic injury in which nerve grafting could be done and with better outcomes.8-11 Similar strategies are regularly applied to shoulder reinnervation. Patients with preganglionic injuries can be treated with single or preferably double nerve transfers.12 Typically, the spinal accessory (via an anterior or posterior approach) is transferred to the suprascapular nerve, and a triceps branch is transferred to the anterior division of axillary nerve.13 In patients with postganglionic injuries, many surgeons would perform nerve grafting, whereas others would opt for nerve transfers. Because of the success and ease of these types of nerve transfers, many surgeons are using a nerve transfer distally rather than nerve grafts proximally for isolated nerve (ie, musculocutaneous or axillary) injuries.14 These techniques have also been applied to novel circumstances (eg, after tumor reconstruction, radiation, inflammation, etc; Figure 2). Complete Brachial Plexus Injuries Patients with complete lesions (C5-T1) have a flail limb with an insensate hand. In some of these cases, there may only be 1 available nerve for grafting; in some cases, the lesions are all preganglionic, and there are no nerves available for grafting. Because of the paucity of suitable intraplexal or extraplexal donor nerves, there are limited options for reconstruction (nerve grafting or conventional nerve transfers). In the past, some surgeons would offer a trans-humeral amputation. A common nerve reconstructive approach would be to attempt to restore a stable shoulder and elbow flexion with nerve grafting or nerve transfers and/or shoulder arthrodesis. In general, hand function could not be
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SPINNER ET AL
FIGURE 1. Illustration shows double fascicular nerve transfer. A, median nerve fascicular transfer to the biceps (overlying insets a-c). B, ulnar nerve fascicular transfer to the biceps (overlying insets a-c). C, the completed double nerve transfers for elbow flexion. br, branch; LABC, lateral antebrachial cutaneous nerve; n, nerve. Reproduced with permission from the Mayo Foundation (2015).
achieved with nerve grafting or standard nerve transfers (ie, intercostals and spinal accessory) because regeneration is too slow and the distal target is too far away.15 More aggressive nerve transfer techniques are being used by some groups with some success at restoring hand function. These include contralateral C7 or extended phrenic nerve transfer and FFMT. Contralateral C7 offers a large number of potentially untapped axons. The phrenic nerve is readily available in the surgical field and likewise is typically available (ie, functioning), even in severe panplexal lesions; because it is always firing, it may have an intrinsic advantage to its use. The morbidity of the use of these nerves, although somewhat controversial, seems acceptable on the basis of reports in the literature. Truly independent use of contralateral C7 may be difficult to obtain. Long-term risks of phrenic nerve harvest in adults are not fully known. Novel
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techniques are being used to improve regeneration: prespinal routes for contralateral C716 and an extended phrenic nerve17 harvested endoscopically in the chest near the diaphragm. Both techniques effectively shorten the distances to target organs. The Mayo Brachial Plexus team has opted to use a combination of techniques, including FFMT,18 in patients with panplexal injury who desire an attempt at hand function. The anatomy of the gracilis is favorable for FFMT, especially for recovery of distal function. The muscle belly of the gracilis is innervated relatively proximally; it has a long tendon that can be further extended. These attributes can be exploited to target distal recovery (Figure 3). We have modified a 2-stage FFMT procedure by Doi et al19 into a single procedure. Our approach combines nerve grafting, when available, with nerve transfers and a single-stage FFMT. We explore and record from upper elements of the
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Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
PERIPHERAL NERVE INJURY REPAIR ADVANCES
CLINICAL NEUROSURGERY
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SPINNER ET AL
FIGURE 2. A 60-year-old woman with a history of a radiation-induced malignant peripheral nerve sheath tumor 2 decades after treatment of a tongue squamous cell carcinoma. She had local and regional metastases at the time. She had undergone multiple surgeries, including flap coverage for infections and osteomyelitis. She had done well in the intervening years until she presented with progressive pain in the right volar forearm and paralysis of shoulder abduction and severe weakness in elbow flexion over 3 months. A, coronal short T1 inversion recovery image revealed a fusiform, irregularly shaped mass involving the brachial plexus. Biopsy confirmed a grade 2 malignant peripheral nerve sheath tumor. B, at operation, an infiltrative lesion (arrow) was seen in the upper trunk (UT). C, a wide resection of the extensive tumor (Tm) was performed involving C5-7 proximally to the level of the divisions distally. AD, anterior division of upper trunk; PN, phrenic nerve; SSN, suprascapular nerve. D, resected specimen with negative margins. One week later, she underwent a double fascicular transfer using ulnar and median nerve fascicles to biceps and brachialis muscles. E and F, she regained Medical Research Council grade 4 elbow flexion at 1 year followup and was able to perform activities of daily living quite effectively. She has done well from an oncological perspective 5 years after the resection. Radiation-induced changes to the neck are observed.
brachial plexus. If no nerve is available, then secondary reconstruction is used for the shoulder. If a spinal nerve is available, nerve grafting is done for shoulder function. Two
motor intercostals are transferred to the biceps motor branch and 2 to the FFMT (gracilis). Vascular repairs are done with the thoracoacromial vessels. The FFMT provides an opportunity for further elbow flexion and some finger flexion. The gracilis muscle is fixed to the clavicle and passed subcutaneously in the arm, and its tendon is passed deep to the bicipital aponeurosis and prolonged, woven into the finger flexors in the forearm. Sensory intercostals are also harvested and transferred to the lateral cord contribution of the median nerve to provide some protective radial-side finger sensation. Spinal accessory nerve is lengthened with a graft to innervate a triceps branch. At a later date, the wrist and thumb are fused to improve finger flexion. This complex form of microsurgical reconstruction can restore some useful and meaningful function.
FORMULA FOR SUCCESS We believe that nerve transfer offers the ability to exploit surgical anatomy against the limitations of neurobiology. By
FIGURE 3. This illustration shows a modified 1-stage free-functioning muscle transfer (FFMT) technique used to obtain finger flexion. The gracilis muscle with its skin paddle is anchored to the clavicle and passed in the arm; its long tendon is passed beneath the bicipital aponeurosis in the elbow region and woven into the finger flexors in the forearm. Intercostal neurotization of the FFMT and the native biceps is shown, along with the vascular repair with the thoracoacromial vessels. Reproduced with permission from the Mayo Foundation (2015).
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FIGURE 4. A formula for nerve regeneration.
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PERIPHERAL NERVE INJURY REPAIR ADVANCES
manipulating the variables of time, distance, and quality, one can improve clinical outcomes and value (Figure 4).
CONCLUSION Restoration of function in peripheral nerve injuries often involves bridging (grafting) or bypassing (nerve transfers) zones of injury. Improved nerve reconstructive strategies are necessary to improve clinical outcomes. By thinking creatively and exploiting anatomy, surgeons have introduced novel techniques, expanded clinical applications, and improved outcomes. The introduction of nerve transfers, particularly distal ones, has revolutionized the way in which peripheral nerve surgeons are thinking about problems and proposing potential solutions. The future of peripheral nerve surgery is bright. Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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CLINICAL NEUROSURGERY
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