Review Article Nerve Transfers for the Upper Extremity: New Horizons in Nerve Reconstruction

Abstract Steve K. Lee, MD Nerve transfers are key components of the surgeon’s Scott W. Wolfe, MD armamentarium in brachial plexus and complex nerve reconstruction. Advantages of nerve transfers are that nerve regeneration distances are shortened, pure motor or sensory nerve fascicles can be selected as donors, and nerve grafts are generally not required. Similar to the principle of tendon transfers, expendable donor nerves are transferred to denervated nerves with the goal of functional recovery. Transfers may be subdivided into intraplexal, extraplexal, and distal types; each has a unique role in From the Hospital for Special the reconstructive process. A thorough diagnostic workup and Surgery and Weill Cornell Medical intraoperative assessment help guide the surgeon in their use. College, New York, NY. Nerve transfers have made a positive impact on the outcomes of Dr. Lee or an immediate family nerve surgery and are essential tools in complex nerve member has received royalties from, is a member of a speakers’ bureau reconstruction. or has made paid presentations on behalf of, and serves as a paid consultant to or is an employee of Arthrex; serves as an unpaid lthough not a new concept, neurotization should be reserved to consultant to Synthes; has received Anerve transfers have become an describe the direct implantation of a research or institutional support from increasingly important technique in divided donor nerve into muscle, Arthrex, DePuy Mitek, Integra LifeSciences, Medartis, Axogen, and the strategic algorithm for nerve re- which has shown promise in an ani- 1,2 Checkpoint; and serves as a board construction. Pioneers such as mal model. member, owner, officer, or Flouren introduced the rooster committee member of the American plexus model in 1820, Balance de- Society for Surgery of the Hand. Indications and scribed the spinal accessory nerve Dr. Wolfe or an immediate family Contraindications member has received royalties from (SAN) transfer to the facial nerve in Extremity Medical; is a member of a 1903, Vulpius described use of the speakers’ bureau or has made paid A variety of indications exists for presentations on behalf of Small medial pectoral nerve in 1920, and nerve transfer, primarily when the Bone Innovations and TriMed; Seddon, the transfer of intercostal proximal nerve end is nonfunctional serves as a paid consultant to or is nerves (ICNs) in 1963.1 an employee of Extremity Medical or nerve reconstruction would re- and Small Bone Orthopedics; and The definition of nerve transfer is quire an excessively long nerve graft. serves as a board member, owner, the surgical coaptation of a healthy Nerve transfer may expedite reinner- officer, or committee member of the nerve donor to a denervated nerve. vation when traditional nerve graft- New York Society for Surgery of the Hand. The principle is similar to that of ing would exceed the expected via- tendon transfers in that a necessary bility of motor end plates and muscle J Am Acad Orthop Surg 2012;20: 3 506-517 distal function is recovered by sacri- (approximately 12 to 18 months). ficing another function that is less es- Nerve transfer may also be indicated http://dx.doi.org/10.5435/ JAAOS-20-08-506 sential to the patient. Synonyms for in patients in whom the zone of in- nerve transfer are nerve-to-nerve jury is very broad, with dense scar- Copyright 2012 by the American neurotization, heterotopic nerve su- Academy of Orthopaedic Surgeons. ring. Nerve transfer outside the zone ture, and nerve crossing. The term of injury is more surgically efficient

506 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD and outcomes, more predictable.4 nerve to the axillary nerve, a fascicle promised recipient nerve.7 End-to- In the upper extremity, nerve trans- of the ulnar nerve to the biceps mo- end transfer is preferable for all fer is most commonly used for recon- tor branch, a fascicle of the median transfers; reverse end-to-side trans- struction of brachial plexus injury. nerve to the brachialis motor branch, fers have not been demonstrated to Other indications include complex and triceps branches of the radial improve motor outcomes in humans injuries to peripheral nerves, espe- nerve to the axillary nerve and its but do show experimental promise.7,8 cially when associated with fractures branches. Extraplexal refers to do- End-to-side transfers have demon- and dislocations, lacerations, injuries nor nerves that originate outside the strated efficacy in sensory nerves.3,6 from projectiles, neoplasia, or, oc- plexus. Examples include the SAN to The most common upper extremity casionally, neuralgic amyotrophy the suprascapular nerve (SSN) and deficits that benefit from nerve trans- (Parsonage-Turner syndrome). the ICN or phrenic nerve to the mus- fer are elbow flexion and shoulder sta- Contraindications for nerve trans- culocutaneous nerve (MCN). bilization, abduction, and external ro- fer include the presence of a superior Distal transfer: Nerve transfer that tation. Other indications include reconstructive option, excessive time is at or distal to the elbow. scapular stabilization for winging, el- between injury and reinnervation (ie, Single versus dual transfer: Single bow extension, wrist extension, finger >18 months), or donor nerve motor transfer refers to the use of one nerve and thumb extension, finger flexion, strength of less than Medical Re- transfer to achieve one action. An and intrinsic hand function. Tables 1 to search Council grade M4. example of a single transfer is an ul- 3 describe intraplexal, extraplexal, and nar nerve fascicle to the biceps motor distal motor transfers. Sensory deficits branch to achieve elbow flexion. of the thumb, index, ring and small fin- Advantages of Nerve Dual transfer refers to the use of two ger and ulnar border of the hand are Transfer nerve transfers to achieve one action. treated by nerve transfers listed in Ta- An example is an ulnar nerve fascicle ble 4. Nerve transfer has the distinct ad- to the biceps motor branch and a Intraplexal donors include the fol- vantage over primary nerve repair median nerve fascicle to the brachia- lowing: ulnar nerve fascicle, median and long nerve grafting of shortening lis motor branch to achieve elbow nerve fascicle, medial pectoral nerve, the length that the nerve must regen- flexion. thoracodorsal nerve, triceps branches erate by bringing the donor nerve Direct nerve transfer: A direct nerve of the radial nerve, brachialis branch of closer to the target organ.3,5 With transfer connects the donor nerve to the MCN, and pectoral fascicle from nerve transfer, pure motor fascicles the recipient nerve without an inter- the middle trunk of C7. with maximal axonal counts are di- posed graft. If a tensionless nerve co- Extraplexal donors include the fol- rected to a recipient nerve. Opti- aptation is not possible, an interposi- lowing: SAN, ICNs, phrenic nerve, mally, nerves are directly transferred tion nerve graft must be used. and contralateral C7 nerve root. to the recipient nerve without an in- Motor versus sensory transfer: Distal transfer donors include the terposed nerve graft. As opposed to Transfers with the goal of recovering following: distal anterior interosse- tendon transfer, when nerve transfer motor or sensory function. Transfers ous nerve (AIN), radial nerve branch is successful, recovered function is performed to restore sensory func- to the extensor carpi radialis brevis, similar to the original muscle func- tion have the added benefit of de- supinator branches of the posterior tion because synchronous physio- creasing neuropathic pain.6 interosseous nerve (PIN), and radial logic motion may be achieved. With End-to-end, end-to-side, reverse end- nerve branch to the brachioradialis. quicker nerve recovery, more rapid to-side: End-to-end nerve transfer refers motor reeducation is also possible. to direct coaptation of the end of the donor nerve to the proximal end of the Common Transfers and Outcomes Nomenclature recipient nerve (Figure 1). End-to-side nerve transfer describes coaptation of Intraplexal versus extraplexal: Intra- the proximal end of the recipient nerve Intraplexal Transfers plexal refers to nerve transfers in to an epineural window in the side of Ulnar Nerve Fascicle to Biceps which the donor nerve originates in an intact and functioning donor nerve. Motor Branch the brachial plexus, including the ter- Reverse end-to-side is when the end of Transfer of the ulnar nerve fascicle to minal peripheral nerve branches a freshly divided donor nerve is the biceps motor branch, described above the elbow. Examples include coapted to an epineural window in the by Oberlin et al9 in 1994, critically the medial pectoral or thoracodorsal side of an intact but functionally com- altered the approach to modern

August 2012, Vol 20, No 8 507 Nerve Transfers for the Upper Extremity: New Horizons in Nerve Reconstruction

Figure 1

Illustrations of the types of nerve transfer. A, End-to-end. B, End-to-side. C, Reverse end-to-side.

nerve transfers. In this transfer, one individual fascicle (Checkpoint Sur- or central part of the nerve;10 any or two fascicles of the ulnar nerve gical Stimulator; Checkpoint Surgi- fascicles that give no response are are transferred directly to the motor cal, Cleveland, OH) and observing presumed to be sensory, and those branch of the biceps. In our practice, the distal muscular contraction. A that cause flexor digitorum profun- fascicles are identified intraopera- fascicle to the flexor carpi ulnaris is dus stimulation are avoided. Evi- tively by electrically stimulating an chosen, which is usually in the lateral dence suggests that any of the fasci-

508 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD

Table 1 Common Intraplexal Motor Transfers Motor Deficit Recipient Nerve or Nerves Donor Nerve or Nerves Comment

Elbow flexion Musculocutaneous nerve: bi- Ulnar nerve fascicle and me- Primary choice, if possible, in ceps and brachialis branches dian nerve fascicle upper nerve root brachial dual transfer plexus injury (C5-6, C5-7) Musculocutaneous nerve Medial pectoral nerve Secondary choice Musculocutaneous nerve Thoracodorsal nerve Secondary choice Shoulder stabilization/abduction/ Suprascapular nerve and axil- Spinal accessory nerve and Primary choice, if possible, com- external rotation lary nerve dual transfer triceps branches bination intraplexal and extra- plexal Shoulder stabilization/abduction Axillary nerve Medial pectoral nerve Secondary choice Axillary nerve Thoracodorsal nerve Secondary choice Scapular stabilization/anti- Long thoracic nerve Thoracodorsal nerve Primary choice if possible winging Long thoracic nerve Pectoral fascicle from middle Secondary choice trunk from C7 Thumb and index finger flexion Posterior fascicle of the median Brachialis branch of musculo- For lower trunk plexus injury or nerve in the arm which corre- cutaneous nerve or extensor high median nerve injury. Cou- sponds to the anterior in- carpi radialis brevis supinator pled with tenodesis of the four terosseous nerve branches of radial nerve flexor digitorum profundus ten- dons in the forearm Elbow extension Triceps branch of radial nerve Ulnar nerve fascicle to flexor — carpi ulnaris or median nerve fascicle to flexor digitorum superficialis

Table 2 Common Extraplexal Motor Transfers Motor Deficit Recipient Nerve or Nerves Donor Nerve or Nerves Comment

Elbow flexion Musculocutaneous nerve Intercostal nerves Primary choice if intraplexal nerve transfers not possible Musculocutaneous nerve Spinal accessory nerve Secondary choice Musculocutaneous nerve Phrenic nerve Infrequently performed given decreased exercise tolerance Shoulder stabilization/abduction/ Suprascapular nerve Spinal accessory nerve Primary choice as part of dual external rotation nerve transfer with triceps branches to axillary nerve Suprascapular nerve Intercostal nerves Secondary choice Shoulder stabilization/abduction Axillary nerve Intercostal nerves Secondary choice if triceps branch is not available Scapular stabilization/anti- Long thoracic nerve Intercostal nerves Secondary choice if thoracodor- winging sal nerve is not available Elbow extension Triceps branch of radial nerve Intercostal nerves — Elbow flexion, hand function Musculocutaneous nerve, me- Contralateral C7 For five-root avulsion in a young dian nerve patient, less commonly per- formed

cles of the ulnar nerve at the level of After 10 years of experience, (C5-6, C5-7). There were no deficits the proximal arm can be used for Teboul et al12 reported their out- in the donor ulnar nerve; 24 of 32 transfer without the loss of ulnar comes in 32 patients with upper patients achieved strength grade M3 nerve function.11 nerve root brachial plexus injuries or higher. A Steindler flexorplasty

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Table 3 Common Distal Motor Transfers Motor Deficit Recipient Nerve or Nerves Donor Nerve or Nerves Comments

Intrinsic hand Ulnar nerve motor branch Distal anterior interosseous For high ulnar nerve lesions nerve Thumb, finger extension Posterior interosseous nerve Nerve to supinator For C7-T1 plexus injuries branches of radial nerve Wrist, finger extension Radial nerve branch to exten- Median nerve fascicles to flexor Dual transfer sor carpi radialis brevis and digitorum superficialis and posterior interosseous nerve median nerve fascicles to flexor carpi radialis Thumb, finger flexion Anterior interosseous nerve Radial nerve branch to the Indicated for lower trunk plexus brachioradialis injury or high median nerve injury. Coupled with tenodesis of the four flexor digitorum profundus tendons in the fore- arm

Table 4 Common Sensory Transfers Sensibility Deficit Recipient Nerve or Nerves Donor Nerve or Nerves Comments

Radial hand Lateral cord contribution to the Intercostal sensory nerve Proximal transfer median nerve branches Thumb and index finger Common digital nerve to first Superficial radial nerve — web space, radial digital nerve to thumb Digital nerves of the ulnar as- Digital branches of superficial Very distal transfer pect of the thumb and radial radial nerve aspect of the index finger Common digital nerve to first Common digital nerve to third — web space, radial digital web space nerve to thumb Common digital nerve to first Common digital nerve to fourth — web space, radial digital web space nerve to thumb Common digital nerve to first Dorsal branch of the ulnar — web space, radial digital nerve nerve to thumb Ring and small fingers Ulnar nerve Lateral antebrachial cutaneous C7-T1 injuries nerve Common digital nerve to fourth Common digital nerve to third — web space, ulnar digital nerve web space to small finger Ulnar border of hand Dorsal branch of the ulnar Lateral antebrachial cutaneous — nerve nerve Dorsal branch of the ulnar Median nerve at distal forearm — nerve (end to side)

was performed as a secondary proce- Steindler flexorplasty, 30 of 32 pa- with M4 strength13 and, in a differ- dure in 10 patients with strength tients achieved a good (M4) or a fair ent series, 13 of 15 patients with M4 grade M3 or lower. Overall, includ- (M3) result. Leechavengvongs and strength, without using the comple- ing all patients with and without colleagues reported 30 of 32 patients mentary Steindler flexorplasty.13,14

510 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD

Figure 2 fers. However, these authors still use the dual nerve transfer in practice. Garg et al4 performed a systematic review comparing the outcomes of nerve transfers for elbow function with autogenous nerve grafting from C5 or C6; they found that 83% of nerve transfers achieved elbow flex- ion strength of grade M4 or higher, and that 96% achieved grade M3 or higher. By comparison, for nerve graft outcomes, 56% achieved grade M4 or higher and 82% achieved grade M3 or higher. The authors concluded that, compared with tra- ditional nerve grafting for restora- tion of elbow function, nerve trans- fers led to improved outcomes.4

Triceps Branch to Axillary Nerve Regarding shoulder function, a key transfer is the triceps branch of the Illustration of dual transfer to regain elbow flexion. Transfer of an ulnar nerve radial nerve to the axillary nerve.20,21 fascicle to the biceps motor branch, plus transfer of a median nerve fascicle The nerve branches to the long, me- to the brachialis motor branch. dial, or lateral head of the triceps are transferred to branches of the axil- lary nerve. Because of the critical im- Medial Pectoral or fascicle to the biceps motor branch, portance of external rotation, Ber- Thoracodorsal Nerve to as described above. This is followed telli and Ghizoni21 recommend Musculocutaneous Nerve by transfer of a median nerve fascicle transfer to both the anterior branch Brandt and Mackinnon15 reported on (generally, the branch to the flexor and the teres minor branch. Transfer five cases in which biceps/brachialis carpi radialis or flexor digitorum su- of the triceps branch to the axillary reinnervation was performed by us- perficialis) to the brachialis motor nerve may be combined with SSN re- ing one or more medial pectoral branch (Figure 2). In practice, either innervation,21,22 thereby making the nerve branches, which lie in close ulnar or median nerve fascicles may procedure a dual nerve transfer for proximity to the MCN. Novak be transferred to either the biceps or both shoulder abduction and exter- et al16 examined the feasibility and brachialis branches, depending on nal rotation (Figure 3). In seven pa- success of the thoracodorsal transfer the patient’s anatomy. Liverneaux tients who had dual transfers of SAN to the MCN; in five of six cases, the et al18 reported on 10 patients, all to SSN and of the triceps branch to patients recovered M4 or M5 with grade M4 elbow flexion the axillary nerve, Leechavengvongs strength of elbow flexion. strength. Ray et al10 reported on 29 et al20 reported all patients as having patients: 23 had strength of grade 4 Dual Transfer: Ulnar Nerve grade M4 deltoid function with 124° Fascicle to Biceps Transfer and or better, and 4 had grade 3. There of abduction. In 10 patients with Median Nerve Fascicle to were no donor deficits. C5-6 brachial plexus injury, Bertelli Brachialis Mackinnon et al17 and Liverneaux and Ghizoni21 reported that, with dual Given the initial 80% success rate et al18 make a strong argument for shoulder nerve transfers, 3 patients had with the single nerve transfer for el- dual transfer for elbow flexion, espe- grade M4 abduction, 7 had grade M3 bow flexion, Ray et al,10 Mackinnon cially compared with previous pub- shoulder abduction (average, 92°), 2 et al,17 and Liverneaux et al18 pro- lished results of single transfer. had grade M4 external rotation, and 5 posed a dual transfer to regain elbow Carlsen et al19 reported that, with the had grade M3 external rotation; aver- flexion. The first part of the dual numbers tested, there was no differ- age external rotation was 93° from full transfer is transfer of an ulnar nerve ence between single and dual trans- internal rotation. In their systematic re-

August 2012, Vol 20, No 8 511 Nerve Transfers for the Upper Extremity: New Horizons in Nerve Reconstruction

Figure 3

Illustrations of dual nerve transfer for shoulder stabilization, abduction, and external rotation. Transfer of the spinal accessory nerve to the suprascapular nerve (A), plus transfer of triceps branches to the anterior division of the axillary nerve and teres minor branch (B). CN XI = cranial nerve XI

view, Garg et al4 found that 74% of tively, two patients had no scapular Extraplexal Transfers patients with dual nerve transfers winging, and three had decreased Spinal Accessory Nerve to had shoulder abduction strength of scapular winging. These patients also Suprascapular Nerve grade M4 or higher, compared with had transfers of the SAN to SSN and The SAN (ie, cranial nerve XI) inner- 35% of patients with single nerve of the triceps branch to the axillary vates the sternocleidomastoid and transfer and 46% of patients with nerve. Average shoulder external ro- trapezius muscles. Transferring the nerve grafts. They concluded that tation from the fully internally ro- dual nerve transfers are associated tated resting position improved to distal fascicles of the SAN to the SSN with improved outcomes for shoul- 124°. The authors concluded that re- is part of a key nerve transfer set for der abduction. innervating the serratus anterior regaining shoulder function. In this muscle is beneficial for shoulder transfer, the inferior branch of the Thoracodorsal Nerve to Long function.24 This finding may be par- SAN is divided distally and directly Thoracic Nerve ticularly important in managing pa- transferred to the SSN. Superior Raksakulkiat et al23 have shown the tients with C5-7 injuries and conse- branches to the trapezius are left in- feasibility and value of reinnervating quent complete denervation of the tact, which preserves strong trape- the serratus anterior muscle using the serratus anterior; reinnervation zius function. It is best to transfer thoracodorsal nerve in five patients should be considered critical to res- without a nerve graft; interposed with C5-6 root avulsion. Postopera- toration of shoulder function. nerve grafting worsens results.22,25

512 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD

Figure 4 ing takes dedicated patient effort and considerable time (12 to 24 months). The sensory branches of the ICNs may also be used for recovery of lim- ited hand sensation and relief of neu- ropathic pain.28 Kovachevich et al29 reported a 15% complication rate with ICN transfers, the most com- mon being pleural tears. They stated that the current literature shows minimal effect of ICN harvest on pulmonary function. Giddins et al30 reported no pulmonary dysfunction after intercostal harvest, even with concomitant phrenic nerve palsy. ICNs may also be used as the motor nerve for free-functioning muscle transfers.31

Phrenic Nerve to Musculocutaneous Nerve The phrenic nerve is most commonly Illustration of transfer of intercostal nerves to the musculocutaneous nerve. used as a donor to regain elbow flex- ion when other donor nerves are not available. Exposure of the phrenic Segmental injury of the SSN can and C5-8 levels, with mean out- nerve is rapid, but it must be length- occur; patients with upper trunk or comes of 77° abduction and 17° ex- ened by a nerve graft to reach the C5 root injuries can also have a dis- ternal rotation. With less severe, iso- MCN or the median nerve. Endo- tal injury to the SSN at the supra- lated C5-6 injury, patients have scopic harvest has been described to scapular notch, especially those who better results.21 lengthen the donor phrenic nerve to have sustained scapular fractures, allow for direct transfer to the MCN scapulothoracic dissociation, and Intercostal Nerve or median nerve.32 Gu and Ma33 re- clavicle dislocations. In these situa- ICNs are among the most useful and ported on results of this technique in tions, Bertelli and Ghizoni26 pro- dependable extraplexal donors. Used 65 patients; 85% achieved a strength posed to dissect both the SAN and most frequently in cases of five-level grade of M3 or higher, and 50% SSN via a distal oblique supraclavic- (C5-T1) plexus palsy, up to seven achieved a grade of M4 or M5. Pul- ular incision, prolonged up to the ICNs can be transferred to regain monary function tests showed de- scapular notch, so that the SSN can some control of the upper extremity. creased pulmonary capacities within be decompressed and the nerve in- ICNs are most frequently used for 1 year of surgery, improving toward spected for continuity. As discussed, restoration of elbow flexion, but 2 years. Disadvantages of this trans- dual transfers for shoulder function other recipients include the axillary fer are that, in young, active patients, lead to improved results over iso- nerve, long thoracic nerve, and SSN the donor defect may permanently lated transfers to the axillary (Figure 4). A systematic review by affect aerobic performance. Also, nerve.4,22,25,26 However, poor recovery Merrell et al22 showed that 72% of considerable retraining is required. of external rotation continues to af- patients achieved elbow flexion re- Because of this, the phrenic nerve fect outcomes, especially with more covery of grade M3 or better when transfer has diminished in popularity extensive injury patterns. Bertelli and direct transfer of ICNs to MCNs was in the last several years. Ghizoni26 showed that no patient performed; only 47% achieved grade with a five-level plexus palsy recov- M3 or better when interposed nerve Contralateral C7 ered external rotation. Suzuki et al27 grafts were used. Given the original The contralateral C7 nerve root or reported results in 12 patients with a function of the ICNs, it is not con- its posterior division may be pro- mix of injuries at the C5-6, C5-7, sidered a synergistic transfer; retrain- longed with a nerve graft and

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Figure 5 tralateral latissimus dorsi muscle to represent the AIN fascicles. This flex the elbow. These authors re- transfer must be coupled with side- ported no functional median nerve to-side flexor digitorum profundus recovery in the four median nerve tenodesis to transmit forces from the patients. median-innervated index and middle 35 Liu et al reported on two cases fingers to the ulnar-innervated ring with severe donor C7 motor and sen- and small fingers. Zheng et al38 re- sory deficits. Full functional recovery ported that five of six patients had was documented at 6 months. How- recovery of digital flexion at 18- ever, objective qualitative and quan- month follow-up. Grip strength aver- titative differences in the motor and aged 66 lb. sensory deficits in the donor limbs were still present at 1.5 to 2 years. Distal Anterior Interosseous 36 Songcharoen et al reported on 21 Nerve to Ulnar Nerve Motor patients with transfer of the contra- Branch lateral C7 to the median nerve; 6 pa- For patients with high ulnar nerve le- tients (29%) obtained grade M3 re- sions, the AIN branch to the prona- covery of the wrist and finger tor quadratus can be transferred to flexors, and 4 (19%) achieved grade the motor branch of the ulnar M2. Ten of the 21 patients (48%) nerve39,40 (Figure 5). In a series of achieved British Medical Research eight patients, all had reinnervation Council grade S3, and 7 (33%) had of their intrinsic muscles at 18 Illustration of transfer of the distal grade S2 recovery in the median months. Pinch increased from 2.2 lb anterior interosseous nerve (AIN) nerve distribution. Average time to preoperatively to 13.8 lb postopera- to the ulnar motor nerve. recovery was 34 months. Three of 6 tively. Grip strength increased from patients aged <18 years had grade 8.8 lb to 61.2 lb.39 crossed over the chest to the injured M3 finger flexion; 3% of the original side, to be used as a donor nerve 111 patient cohort had motor defi- Supinator Branches to Posterior when there is a paucity of other cits in the donor extremity, with per- Interosseous Nerve nerve donors. The best results have manent wrist extension weakness in In the uncommon C7-T1 palsies of been reported in young patients with one patient. Sammer at al37 recom- the brachial plexus, shoulder and el- complete five-level (C5-T1) root mended against the use of this proce- bow function is preserved, but digital avulsions. In this transfer, the ipsilat- dure, given its poor outcomes and function is absent. Supinator muscle eral full-length vascularized ulnar risk of permanent donor site morbid- function is preserved because inner- nerve graft is raised on a pedicle ity. Enthusiasm for this transfer has vation arises from the C6 nerve root. based on the superior ulnar collateral waned in recent years. Sacrifice of the supinator motor artery and is reversed to cross the branches does not eliminate supina- chest to the contralateral brachial Distal Transfers tion because biceps muscle function plexus. Usually several fascicles of is preserved in C7-T1 palsies. Bertelli Brachialis Motor Branch to the 41 C7 are isolated, identified as fascicles Anterior Interosseous Nerve, et al performed a cadaver feasibility to the shoulder, then divided and Coupled With Tenodesis of study and showed that one or two coapted to the ulnar nerve. Usual tar- the Flexor Digitorum Profundus branches of the PIN to the supinator gets include the median nerve and/or For patients with the rare C8-T1 or can be transferred to the PIN the MCN. Hierner and Berger34 re- lower trunk plexus injury, and po- branches that innervate the extensor ported on 10 cases—6 to the MCN, tentially for patients with a high me- pollicis longus and the extensor digi- 4 to the median nerve. All 10 pa- dian nerve injury, the brachialis mo- torum communis muscles (Figure 6). tients had temporary donor sensory tor branch of the MCN can be These authors later reported that deficits but no donor motor deficits. transferred to the posterior third of four of four patients had full meta- All six of the MCN transfer patients the median nerve in the arm to re- carpophalangeal joint extension after had M3 or M4 elbow flexion return, store median motor function.3,38 The this transfer.42 Dong et al43 also re- but two required a “start” com- posterior third of the median nerve ported good results with this trans- mand—that is, contracting the con- was identified by Zheng et al38 to fer.

514 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD

Figure 6 Figure 7

Illustration of transfer of median Illustration of transfer of supinator branches to the posterior interosseous nerve branches to the posterior nerve (PIN). (Adapted with permission from Bertelli JA, Ghizoni MF: Transfer interosseous nerve (PIN) and of supinator motor branches to the posterior interosseous nerve in C7-T1 extensor carpi radialis brevis brachial plexus palsy. J Neurosurg 2010;113[1]:129-132.) (ECRB) branches. FCR = flexor carpi radialis, FDS = flexor digitorum superficialis, MN = me- dian nerve, PL = palmaris Median Nerve Branches to distal superficial radial nerve trans- longus, RN = radial nerve. Radial Nerve Branches fers to the digital nerves of the ulnar (Adapted with permission from Ray This procedure is a dual transfer set aspect of the thumb and radial as- WZ, Mackinnon SE: Clinical in which median nerve branches to pect of the index finger in eight pa- outcomes following median to radial nerve transfers. J Hand Surg the flexor digitorum superficialis are tients with high median nerve le- Am 2011;36[2]:201-208.) transferred to the radial nerve sions. Protective or better sensation branch to the extensor carpi radialis was recovered in all patients. Ducic brevis, and median nerve branches to et al48 presented two successful cases intraoperative electrodiagnostic stud- the flexor carpi radialis are trans- of radial sensory nerve transfers to ies and histopathologic frozen-tissue ferred to the PIN.44,45 Ray and Mac- the thumb and index finger. In examination to further evaluate po- kinnon46 reported that 18 of 19 pa- C7-T1 injuries, the lateral antebra- tential donor root viability. Each re- tients had good to excellent wrist chial cutaneous nerve can be trans- constructive strategy is individual- extension; 9 patients also had prona- ferred to the ulnar nerve in the arm ized. tor teres to extensor carpi radialis to regain distal sensory function. Our main goals for reinnervation brevis tendon transfer. Twelve of 19 are (1) elbow flexion, (2) shoulder patients had good to excellent finger abduction and external rotation, (3) and thumb extension (grade M4 or Authors’ Preferred Nerve scapular stabilization, (4) elbow ex- M4+), 2 of 19 had fair recovery Transfers and tension, (5) sensory reinnervation for (M3), and 5 of 19 had poor recovery Reconstructive Strategies control of neuropathic pain, and (6) (M0 to M2) (Figure 7). A compara- restoration of distal (below-elbow) tive functional study of nerve trans- Nerve transfers are part of our arma- function. For elbow flexion, we pre- fers versus tendon transfers for resto- mentarium for nerve reconstruction, fer the double fascicular transfer of ration of PIN function has not been along with nerve grafting and sec- ulnar and median fascicles to biceps performed. ondary procedures. When we evalu- and brachialis. We perform double ate a patient with brachial plexus in- nerve transfers whenever possible for Sensory Transfers jury, the physical examination, shoulder recovery—generally, trans- Sensory transfers are employed to re- imaging studies, and electrodiagnos- fer of the SAN to the SSN and of the gain essential zones of sensibility and tic studies help us define whether vi- triceps, medial pectoral, thoracodor- to decrease neuropathic pain.6 Ber- able roots are present to use for rein- sal, or ICN to the axillary nerve. telli and Ghizoni47 reported on very nervation. We routinely employ Whenever possible, reinnervation of

August 2012, Vol 20, No 8 515 Nerve Transfers for the Upper Extremity: New Horizons in Nerve Reconstruction the teres minor branch of the axillary contents. In this article, references 2, in brachial plexus injuries. J Hand Surg nerve is performed to improve exter- 4, 7, 8, 19, and 22 are level III studies. Am 2011;36(12):2002-2009. nal rotation. If there is an intact C5 References 6, 9-18, 20, 21, and 23-48 12. Teboul F, Kakkar R, Ameur N, Beaulieu nerve root, the target will often be JY, Oberlin C: Transfer of fascicles from are level IV studies. References 1, 3, the ulnar nerve to the nerve to the biceps the axillary nerve or the posterior and 5 are level V expert opinion. in the treatment of upper brachial plexus cord, lengthened by sural nerve palsy. J Bone Joint Surg Am 2004;86(7): References printed in bold type are grafts. 1485-1490. those published in the past 5 years. ICNs are our extraplexal source of 13. Leechavengvongs S, Witoonchart K, Uerpairojkit C, Thuvasethakul P, 1. Meals RA, Nelissen RG: The origin and choice, especially in five-level plexus Ketmalasiri W: Nerve transfer to biceps meaning of “neurotization.” J Hand muscle using a part of the ulnar nerve in injuries. Common intercostal targets Surg Am 1995;20(1):144-146. are the MCN, axillary nerve, and brachial plexus injury (upper arm type): 2. Swanson AN, Wolfe SW, Khazzam M, A report of 32 cases. J Hand Surg Am long thoracic nerve. Intercostal sen- Feinberg J, Ehteshami J, Doty S: 1998;23(4):711-716. sory nerves are often transferred to Comparison of neurotization versus 14. Leechavengvongs S, Witoonchart K, the lateral cord contribution of the nerve repair in an animal model of chronically denervated muscle. J Hand Uerpairojkit C, Thuvasethakul P, median nerve for pain relief and pro- Surg Am 2008;33(7):1093-1099. Malungpaishrope K: Combined nerve transfers for C5 and C6 brachial plexus tective sensibility. “Crossing the el- 3. Tung TH, Mackinnon SE: Nerve avulsion injury. J Hand Surg Am 2006; bow” for hand and wrist reanima- transfers: Indications, techniques, and 31(2):183-189. tion with nerve reconstruction is outcomes. J Hand Surg Am 2010;35(2): 332-341. 15. Brandt KE, Mackinnon SE: A technique relatively ineffective in adult total for maximizing biceps recovery in 4. Garg R, Merrell GA, Hillstrom HJ, brachial plexus reconstruction. J Hand plexus palsies; if there is insufficient Wolfe SW: Comparison of nerve Surg Am 1993;18(4):726-733. nerve regeneration 2 years after transfers and nerve grafting for 16. Novak CB, Mackinnon SE, Tung TH: nerve reconstruction, we generally traumatic upper plexus palsy: A systematic review and analysis. J Bone Patient outcome following a employ a combination of tendon Joint Surg Am 2011;93(9):819-829. thoracodorsal to musculocutaneous nerve transfer for reconstruction of transfers, joint fusions, and free- 5. Rohde RS, Wolfe SW: Nerve transfers elbow flexion. Br J Plast Surg 2002; functioning muscle transfers to im- for adult traumatic brachial plexus palsy 55(5):416-419. prove the position and function of (brachial plexus nerve transfer). HSS J 2007;3(1):77-82. 17. Mackinnon SE, Novak CB, Myckatyn the wrist and hand. The phrenic TM, Tung TH: Results of reinnervation 6. Leechavengvongs S, Ngamlamiat K, of the biceps and brachialis muscles with nerve and contralateral C7 are not Malungpaishrope K, Uerpairotkit C, a double fascicular transfer for elbow common donor sources in our prac- Witoonchart K, Kulkittiya S: End-to-side flexion. J Hand Surg Am 2005;30(5): tice. radial sensory to median nerve transfer 978-985. to restore sensation and relieve pain in C5 and C6 nerve root avulsion. J Hand 18. Liverneaux PA, Diaz LC, Beaulieu JY, Surg Am 2011;36(2):209-215. Durand S, Oberlin C: Preliminary results of double nerve transfer to restore elbow 7. Isaacs JE, Cheatham S, Gagnon EB, flexion in upper type brachial plexus Summary Razavi A, McDowell CL: Reverse end- palsies. Plast Reconstr Surg 2006;117(3): to-side neurotization in a regenerating 915-919. Nerve transfers are a vital part of the nerve. J Reconstr Microsurg 2008;24(7): 489-496. 19. Carlsen BT, Kircher MF, Spinner RJ, global strategy for the surgical treat- Bishop AT, Shin AY: Comparison of ment of brachial plexus and complex 8. Kale SS, Glaus SW, Yee A, et al: Reverse single versus double nerve transfers for end-to-side nerve transfer: From animal elbow flexion after brachial plexus nerve injuries. All of the various model to clinical use. J Hand Surg Am injury. Plast Reconstr Surg 2011;127(1): types of transfers may be used for a 2011;36(10):1631-1639, e2. 269-276. variety of indications, including in- 9. Oberlin C, Béal D, Leechavengvongs S, 20. Leechavengvongs S, Witoonchart K, traplexal, extraplexal, and distal, Salon A, Dauge MC, Sarcy JJ: Nerve Uerpairojkit C, Thuvasethakul P: Nerve transfer to biceps muscle using a part of transfer to deltoid muscle using the nerve and for recovery of motor and sen- ulnar nerve for C5-C6 avulsion of the to the long head of the triceps, part II: A sory function. Knowledge of and the brachial plexus: Anatomical study and report of 7 cases. J Hand Surg Am 2003; report of four cases. J Hand Surg Am 28(4):633-638. ability to perform these transfers is 1994;19(2):232-237. paramount to the success of these 21. Bertelli JA, Ghizoni MF: Reconstruction 10. Ray WZ, Pet MA, Yee A, Mackinnon of C5 and C6 brachial plexus avulsion complex reconstructions. SE: Double fascicular nerve transfer to injury by multiple nerve transfers: Spinal the biceps and brachialis muscles after accessory to suprascapular, ulnar brachial plexus injury: Clinical outcomes fascicles to biceps branch, and triceps References in a series of 29 cases. J Neurosurg 2011; long or lateral head branch to axillary 114(6):1520-1528. nerve. J Hand Surg Am 2004;29(1):131- 139. 11. Bhandari PS, Deb P: Fascicular selection Evidence-based Medicine: Levels of for nerve transfers: The role of the nerve 22. Merrell GA, Barrie KA, Katz DL, Wolfe evidence are described in the table of stimulator when restoring elbow flexion SW: Results of nerve transfer techniques

516 Journal of the American Academy of Orthopaedic Surgeons Steve K. Lee, MD, and Scott W. Wolfe, MD

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