Surgical Reconstructions for adult brachial plexus injuries. Part I: Treatments for combined C5 and C6 injuries, with or without C7 injuries

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Surgical Reconstructions for adult brachial plexus injuries. Part I: Treatments for combined C5 and C6 injuries, with or without C7 injuries Yu-Huan Hsueh , Yuan-Kun Tu PII: DOI: Reference:

S0020-1383(20)30151-0 https://doi.org/10.1016/j.injury.2020.02.076 JINJ 8632

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Injury

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15 February 2020

Please cite this article as: Yu-Huan Hsueh , Yuan-Kun Tu , Surgical Reconstructions for adult brachial plexus injuries. Part I: Treatments for combined C5 and C6 injuries, with or without C7 injuries, Injury (2020), doi: https://doi.org/10.1016/j.injury.2020.02.076

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Title: Surgical Reconstructions for adult brachial plexus injuries. Part I: Treatments for combined C5 and C6 injuries, with or without C7 injuries.

Authors: Yu-Huan Hsueh, MD, Yuan-Kun Tu, MD, PhD

Corresponding author: Yuan-Kun Tu, MD, PhD Institute: Orthopedic department, E-DA hospital / I-Shou university Address: No. 1, Yida Rd., Yanchao Dist., Kaohsiung City 824, Taiwan (R.O.C.) Tel: +886-7-615-0011-2971 Fax: +886-7-615-5581 E-mail: [email protected]

Keywords: Brachial plexus injury, upper arm type, nerve transfer, neurotization

[ Introduction ] Brachial plexus injuries (BPI) are devastating injuries that lead to both motor and sensory partial or complete function loss. (1,2,3) These injuries can be classified into upper arm type

(C5, 6 with or without C7 injuries) (Figure 1), lower arm type (C8, T1 injuries), and total arm type (C5, 6, 7, 8, T1 injuries). The upper arm type BPI result in loss function of shoulder elevation, abduction, rotation, and elbow flexion. Furthermore, the combined C7 injury may cause additional elbow, wrist and finger extension deficit. These injuries also lead to sensory loss, pain, psychological morbidity and poor quality of life. The brachial plexus reconstructive surgeries have developed with improving functional results from nerve repair with or without nerve graft, nerve transfer (neurotization), tendon transfer, muscle transfer, and free functioning muscle transfer (FFMT). Based on the severity of lesion, duration after trauma, and associated injuries, different treatments have been used to obtain optimal results. In treating adult upper arm BPI, restoration of elbow flexion is the first priority of treatment, followed by shoulder motor function and stability. Then the elbow, wrist, and finger extension need to be restored, if C7 root is involved. With recent advances in reconstructive surgeries, the adult upper arm type BPI can be treated successfully with satisfactory functional outcomes.

[ Clinical evaluation for upper arm type BPI ] The most common injury mechanism of upper arm type BPI is traction injury, in which the head is distracted away from the shoulder. This mechanism usually results in upper trunk (C5 and C6) injury with or without C7 injury, but the lower trunk (C8-T1) functions are preserved. The typical clinical presentations of upper arm type BPI are the loss of shoulder elevation, and elbow flexion function in C5-6 injury; and additional loss of elbow, wrist, and hand extension function when C7 root is also involved. The individual muscle function evaluations show that

paralysis or atrophy of biceps, brachialis, deltoid and rotator cuff in C5-6 injury. And the additional paralysis of triceps, wrist and hand extensors in C7 injury. To further confirm the diagnosis of upper arm BPI, electromyography (EMG) and nerve conduction velocity (NCV) studies are used. These electrodiagnosis tools are usually performed 6 weeks after injury and followed by the second EMG/NCV examination in another 6 weeks later. The CT myelogram (CTM) or magnetic resonance myelogram (MRM) can also be used before surgical exploration to further confirm the injury level and trauma zone of the brachial plexus, which may also help to make the detailed preoperative treatment plan.

[ Surgical treatments for upper arm type BPI ] Treatments for upper arm type BPI are complex and challenging. With the advancement of surgical reconstruction procedures in these three decades, the function of injured limb can be reliably restored. We systemically summarize the different reconstruction methods, including nerve repair, nerve grafting, nerve transfer (neurotization), tendon / muscle transfer, and FFMT, to restore the function of shoulder abduction / elevation / rotation, elbow flexion, and elbow / wrist / hand extension as well.

1. Nerve repair BPI are mostly caused by a traction mechanism which may lead to pre-ganglionic or postganglionic avulsion injuries, which may benefit from nerve transfer. However, nerve repair with direct end-to-end coaptation suture of the musculocutaneous nerve, the lateral cord, or the upper trunk still provide an optimal outcome in patients with sharp cutting or penetrating injuries. It is suitable in cases of acute localized injury, which the injured proximal and distal stumps can be sutured directly without tension.

2. Nerve grafting In the cases with cutting or traction injury with loss of nerve continuity, the direct nerve repair without tension may not be possible, and the nerve grafting is needed for the functional restoration. If the injury level is not preganglionic lesion and the length of nerve defect between proximal and distal stumps is adequately evaluated (usually less than 6 cm), the reconstruction can be performed by nerve grafting with an interposition nerve graft. The sural nerve can be

harvest as a nerve graft and it is most commonly used in treating BPI patients. (Figure 2) In addition, lateral antebrachial cutaneous nerve and medial antebrachial cutaneous nerve also can be used for nerve grafting (7,8). In consideration of intraneural topography, an adequate anatomical coaptation suture between proximal and distal nerve stump should be performed to obtain an optimal functional outcome. In the cases with injury zone between the level of C5, C6 roots and trunkal level, the nerve grafting should be performed to connect C5 proximal stump to the posterior division, and connecting C6 proximal stump to the anterior division. In the other hand, it is difficult to obtain an ideal distal stump in patients with wide injury zone and large nerve defect. These patients may have more benefits in nerve grafting from the proximal C5, C6 stump to distal branches (2,4,5,6,7,8). Although the current trends favor nerve transfer over nerve repair or nerve grafting, there are still some authors prefer nerve grafting as a primary reconstruction procedure, if there is an adequate proximal nerve stump. In fact, the total avulsion of all cervical roots is rare and only account for 16% in BPI (9). It is especially true in the upper arm type BPI, because of the ligament structure over C5-6 foraminal region which lead the C5 and C6 proximal stump more likely to be preserved for nerve grafting. (10) The nerve grafting has several advantages, including avoidance of the possibility of donor site morbidity in nerve transfer, avoidance of the need of brain reeducation, and offering sufficient number of motor fascicles. (11) In addition, further nerve transfer as the 2nd stage surgery still can be performed if necessary, before the neuromuscular junction dysfunction and muscle atrophy occur. In the cases with suitable indications, nerve grafting can provide good elbow flexion restoration with 69.2% in C5-6 injury and 66.7% in C5-6-7 injury (12).

3. Nerve transfer for Shoulder abduction, elevation, external rotation restoration Nerve transfer, or so-called neurotization, was firstly performed 70 years ago and became one of the most optimal treatment modality for the BPI with the advancement of associated knowledge and surgical technique within recent 30 years (13). There are several intraplexus and extraplexus donor nerves have been reported as neurotizers to treat the upper arm type BPI. The available intraplexus donor nerves are median nerve (MN), ulnar nerve (UN), radial nerve (RN), and medial pectorial nerve (MPN). The available extraplexus donor nerves are spinal accessory nerve (SAN), phrenic nerve (PN), and intercostal nerve (ICN). To restore the shoulder function, the reinnervation of suprascapular nerve (SSN), and axillary nerve (AXN) are crucial and commonly be targeted as recipient nerves. We summarized several nerve transfer procedures that are most commonly used in clinical practices.

Reinnervation of suprascapular nerve (SSN) Spinal accessory nerve (SAN) transfer SAN is the XI cranial nerve which innervates the trapezius muscle. In treating BPI patients, SAN is a useful neurotizer with sufficient motor axon and length. Up to 95% of BPI patients have preserved SAN and it is widely transferred to different target to restore function, such as SSN, MCN, AXN, or gracilis FFMT. (14) The SAN transfer to SSN can be performed directly without interposition nerve graft. This procedure can be performed either through anterior supraclavicular approach or through posterior approach with reliable and good outcomes.

(Figure 3) Although SAN to SSN transfer can restore both shoulder external rotation and abduction function, recovery of shoulder external rotation is usually inferior to shoulder abduction after SAN to SSN transfer. The possible explanation is that relative insufficient myelinated fibers in SAN and the supraspinatus muscle attracts more regenerating axon than the infraspinatus muscle. (15) By SAN to SSN transfer, shoulder function can be restored with 80% success rate (≥ M3). (16, 17) (Figure 4)

Phrenic nerve (PN) transfer Transferring PN to SSN is another method to restore shoulder function without interposition nerve graft. The PN contains abundant of motor fiber and provides comparable success rate of shoulder function recovery to the SSN transfer. One of the major concern of this method is pulmonary function compromise. After PN harvesting, the elevation of diaphragm is usually observed post-operatively for 1 to 2 years. However, the pulmonary capacity decreasing will recover by 2 years post-operatively. Gu et al. demonstrated a rat model to evaluate the effects of different nerve transfer procedures, including PN, SAN and ICN transfers. The result showed that PN transfer had superior neural regeneration than SAN, or ICNs transfer. (18, 19) In addition, some authors even performed the simultaneous PN and ICNs transfer, despite of considerable pulmonary function compromise after this surgical procedure. However, the clinical results showed no respiratory distress after surgery, but a decreased lung function was observed 2 years post-operatively. (20) The PN transfer has an acceptable success rate with 70% (≥ M3 shoulder abduction). In consideration of pulmonary comorbidity, patients with

coexist poor pulmonary function, such as chest trauma, obesity, chronic lung disease, may not be suitable for this transfer.

Reinnervation of axillary nerve (AXN) Triceps branch of radial nerve (TRN) transfer Original TRN transfer to AXN was introduced by Lurje. He described that transferring triceps branch of radial nerve to AXN at the proximal level. (13) However, the result was unsatisfied because of relative far distance between the TRN and the target AXN, and may need interposition nerve graft. An anatomical study revealed that the number of myelinated fibers of current possible neurotizer may not be sufficient to reinnervate of AXN at proximal level. The AXN is not only innervating deltoid muscle, but also teres minor muscle. In addition, AXN contains a part of sensory fibers that contribute to superior lateral cutaneous nerve. There are two major branches from AXN, including anterior branch which innervates deltoid muscle majorly, and posterior branch which innervates teres minor and forms superior lateral cutaneous nerve. Therefore, transferring TRN to anterior branch of AXN, so-called highly selective nerve transfer, may provide a more ideal way to overcome the shoulder elevation weakness problem. (21) Leechavengvongs et al. introduced a posterior based approach that transferring TRN to AXN in the quadrilateral space. (22) The branch of RN to long head of triceps is identified at the triangular space and is coaptated suture to the anterior branch of AXN. By transferring to anterior branch of AXN at more distal level, it can avoid the dilution of donor motor fibers. With this modification, the dissection is relative easy, and the coaptation can be performed more closely to the target nerve without interposition nerve graft. (Figure 5) They reported an

excellent result with 100% of functional recovery and no triceps deficit after harvesting the motor branch of RN to long head of triceps. (23) To obtain a better shoulder function, reinnervation of both SSN and AXN is recommended. A combination procedure of SAN to SSN transfer and TRN to AXN transfer provides an excellent result with 100% success rate, 92° shoulder abduction, and 93° shoulder rotation. (24) In treating upper arm type BPI with C5-6 injury, double nerve transfer (combined SSN and AXN neurotizations) become the most commonly used technique for shoulder function restoration. (Figure 6)

Intercostal nerves (ICNs) transfer Simultaneous reinnervation of SSN and AXN was suggested to obtain a better shoulder recovery. The combined SAN to SSN transfer and TRN to AXN may provide most optimal results for patients with C5-6 injury. However, TRN is not available for nerve transfer in patients with C5-6-7 injury. Many neurotizers had been reported to reinnervate AXN, such as PN, SAN, and MPN. However, the results of these transfers were limited due to the far distance between the neurotizers to the target nerve, and need of interposition nerve graft. (25, 26,27) Based on the similar concept of highly selective neurotization with targeting the anterior branch of AXN, Lerdsin group in Thailand introduced a method which using ICNs as neurotizers to coaptate with the anterior branch of AXN. (28) The 4th and 5th ICNs were identified through a curved incision over chest wall and the anterior branch of AXN was identified through a posterior approach. Then the ICNs were passed through a subcutaneous tunnel and coaptation sutured to the anterior branch of AXN. The cadaveric study demonstrated an adequate length of 4th and 5th ICNs could be obtained after ligation of sensory nerve. In addition, this nerve transfer

is expandable that post-operative shoulder range of motion can be trained without tension on the nerve coaptation site. Good result was obtained with ≥ M4 deltoid recovery in their study. This result was further confirmed by a prospective comparison study. The double nerve transfers with SAN to SSN transfer and ICNs to AXN transfer had a significant better shoulder recovery with 94.2% success rate (≥ M3) than single nerve transfer with 78.2% success rate (≥ M3). (29)

4. Tendon / muscle transfer for Shoulder abduction, elevation, external rotation restoration Although there are several neurotization methods provide a reliable and good shoulder functional outcome, patients with previous nerve surgery failure or neglected presentation will suffer from persisted shoulder dysfunction. Shoulder paralysis leads to an internal rotation position, so-called hand-on-belly position, which decreases the elbow and hand function by limiting forearm and hand anterior motion in coronal plane. To restore shoulder function in these circumstance, tendon or muscle transfer is one of salvage procedures. Trapezius muscle is usually preserved in BPI patients and can be transferred to restore the shoulder. The upper trapezius transfer to restore shoulder abduction has been reported with variable results. (30, 31) (Figure 7) Furthermore, lower part trapezius transfer to reconstruct infraspinatus to restore shoulder external rotation had been introduced with 90% success rate. (32) However, the shoulder function is complicated and isolated tendon transfer is not sufficient to restore an optimal shoulder function. (33) The combined procedures with latissimus dorsi muscle transfer to restore the supraspinatus, and trapezius transfer to restore the deltoid had been used to simultaneously reconstruct the shoulder flexion, abduction and external rotation function. (3, 31, 31, 34) In addition, Elhassan et al. demonstrated a multiple tendon transfers to reconstruct

rotator cuff and deltoid function. The outcome was promising with improvement of pain, stabilization of shoulder joint, and improvement of flexion, abduction, external rotation. (35) In some patients with failure previous SA transfer to SS, the ipsilateral trapezius is not available for transfer. In such circumstance, the contralateral trapezius transfer with interpositional tendon / fascia graft had been reported to restore external rotation of shoulder with reasonable result. (36)

5. Shoulder arthrodesis By the advancement of shoulder arthroplasty, the indications of shoulder arthrodesis become limited recently. However, shoulder arthrodesis is still an alternative salvage procedure to treat the patients with unsalvageable shoulder function. Patients with preserved scapulothoracic motion can obtained a stable, painless shoulder joint with some degree of active elevation of shoulder after shoulder arthrodesis. In treating upper arm type BPI, shoulder arthrodesis can further improve the functional outcome in patients with reserved or restored elbow flexion function. (37) Shoulder arthrodesis has been associated with high rates of complications, including nonunion, fracture, implant breakage, and infection. Therefore, arthroscopic assisted shoulder arthrodesis was introduced to decrease the complications. It provides a less intraoperative blood loss, higher bony union rate, and less infection rate. (38)

6. Nerve transfer (Neurotization) for elbow flexion restoration

The biceps and brachialis are two major muscles to provide the function of elbow flexion. These two muscles are innervated by the musculocutaneous nerve (MCN) and it is the most important recipient nerve for nerve transfer to restore the elbow flexion function. We summarized the nerve transfer procedures that are most commonly applied in clinical practices.

Oberlin method The Oberlin method was firstly described by Christophe Oberlin. (39) This procedure includes isolation of one or two fascicles of UN, identification of biceps branch of MCN, and then coaptation suture from fascicles of UN to the biceps branch of MCN. (39,40,41) (Figure 8) Furthermore, he reported a series with 75% of patients who received the surgery have more than M3 elbow flexion recovery. The study from Leechavengvongs showed similar result that 93% of patients obtained the ability to against resistance. (40) In addition, no permanent donor site morbidity was reported. (40, 41) During the surgery, a nerve stimulator can be used as a neuroguide. We recommend harvesting the nerve fascicles that innervate the extrinsic finger muscles or wrist flexion muscles; and avoid harvesting the fascicles which innervated intrinsic muscle to minimize the risk of donor site deficit, such as claw hand or intrinsic deficit of hand. Nowadays, the Oberlin method is the most commonly used procedure to restore the elbow flexion function in upper arm BPI. Double nerve transfer (Mackinnon’s method, Oberlin II method) Since the Oberlin method had been introduced in 1994, it provides a reliable outcome. However, Oberlin method is focusing on the reinnervation of biceps muscle which plays a role

of elbow supinator more than elbow flexor. In the other hands, the brachialis muscle provides the primary elbow flexion function, and hence the reinnervation of the brachialis muscle may provide a better elbow flexion recovery. The study mentioned that a part of patients who received Oberlin transfer may need an additional Steindler flexorplasty to restore the useful elbow flexion function. (42) To overcome the problem, Susan MacKinnon introduced the double nerve transfer technique to simultaneously reinnervate the biceps and brachialis. (43) The original procedure described the use of different donor nerves, such as medial pectoral nerve, intercostal nerve, thoracodorsal nerve, and triceps branch of radial nerve, to reinnervate the brachialis muscle with or without nerve graft. (43) Furthermore, the Oberlin II method was introduced by transferring a fascicle of median nerve to the brachialis branch of MCN and a fascicle of ulnar nerve to the biceps branch of MCN. (44) (Figure 9) The report from Mackinnon group and Oberlin group both showed 100% of M4 elbow flexion recovery. (43,44) And there was no patient suffered from any donor site morbidity. The double nerve transfer provides an increased success rate of elbow flexion restoration without the loss of donor nerve function in hand. (Figure 10)

Intercostal nerves (ICNs) transfer The ICNs transfer was firstly be described by Seddon, and he transferred the ICNs to MCN with ulnar nerve graft for elbow flexion restoration in treating total arm type BPI patients. The procedure was further modified by Nagano et al. They harvested 3 rd, and 4th ICNs more than 12cm and directly transferred to MCN without nerve graft. (45) Nowadays, the ICN is one of the ideal neurotizers in BPI reconstruction. In consideration of the intraneural topography, the

motor fascicles are located in the central and upper zones of MCN and the sensory fascicles are located in the peripheral and lower zones of MCN. Therefore, the motor nerves of ICN should be transferred to the central and upper zone of cross-section cut and the sensory nerves of ICN shoulder be transferred to the peripheral and lower zone of cross-section cut of MCN. (25) In the other hands, some surgeons may prefer direct transfer the motor branch of ICNs to the biceps branch of MCN, which is the same target as Oberlin transfer, to obtain a more reliable motor function recovery. (46,47) Since ICNs transfer has been used for almost 50 years, transfers of two, or three ICNs have been reported for elbow flexion restoration. (48,49) Theoretically, more motor fascicles be used for transfer, better result may be obtained. However, the most ideal number of ICNs to transfer is undetermined. Xiao et al. conducted a study to compare the different number of ICNs transferring to MCN to restore the elbow flexion function. Although the result showed using three ICNs to transfer provided better results than using two ICNs, the difference was not significant. In fact, nerve transfer with mismatched myelinated fibers still may provide sufficient functional outcomes, because of up to 80% of motor neuron loss can be compensated by the enlargement of motor unit. (50) Thus, using two ICNs to transfer to MCN can provide reasonable outcome with up to 97.1% success rate (≥ M3 elbow flexion). (29) It takes about 12 to 18 months in average to achieved M3 elbow flexion and the function can be continuously improved with persisted intensive rehabilitation. After 3 years post-operatively, the independent elbow flexion control is obtained without the initiation of respiration. However, the ICNs transfer to MCN is more complicate and technique demanding. The possible complications of ICNs harvesting include pneumothorax, hemothorax, and respiratory

distress. In the meantime, the harvesting of ICNs is a time consuming procedure. Therefore, the Oberlin method or double nerve transfer to MCN have gained more popularity than ICNs transfer for most surgeons.

Spinal accessory nerve (SAN) transfer SAN neurotization has been used to reinnervate MCN with an interposition nerve graft. A 72.5% success rate (≥ M3 elbow flexion) of elbow flexion recovery has been reported by using SAN transfer to MCN with a sural nerve graft. (51) Further comparison study was conducted to evaluate the efficacy of SAN transfer and ICN transfer for elbow flexion restoration. The result showed that 84.6% success rate (≥ M3 elbow flexion) in SAN transfer group compared to 64% success rate (≥ M3 elbow flexion) in ICN transfer group. (52) The advantages of SAN transfer include more myelinated fibers than ICN, and easier rehabilitation training. In the contrast, using the nerve graft lead the longer recovery time and the result is poor when using the nerve graft more than 10 cm. (53) The other disadvantage is that SAN is commonly used for shoulder restoration by transfer to suprascapular nerve, and shoulder arthrodesis may be needed for shoulder stability restoration after transferring SAN to MCN.

Phrenic nerve (PN) transfer PN is another possible neurotizer to treat the elbow flexion of BPI. It contains large numbers of motor axon and provides reasonable functional outcomes. Gu et al. reported an 84.6% success rate (≥ M3 elbow flexion) by using PN transfer to MCN with or without nerve graft. There was no respiratory distress except one case who received PN transfer and ICNs transfer simultaneously. (54) However, the respiratory insufficiency was transient. The lung function

test showed decreased within 1 year post-operatively but gradually improved. In consideration of respiratory function compromise, caution should be taken if simultaneously transfer ICN or patients have coexisted pulmonary disease or injuries. Due to the reliable clinical outcomes after Oberlin or double nerve transfer for elbow flexion, only few surgeons use PN transfer for elbow flexion function.

Medial pectoral nerve (MPN) transfer In addition to the Oberlin methods or double nerve transfer, MPN transfer is another intraplexus neurotization option. It can be transferred to either AXN or MCN. For elbow flexion restoration, it achieved 85.7% success rate (≥ M3 elbow flexion). (27) The MPN transfer is also been used in treating obstetric brachial plexus injury with acceptable result. (55) The one of major disadvantages of MPN transfer is the short length of neurotizer (MPN). The length insufficiency can be solved by retrograde intra-fascicle dissection of MCN to obtained longer MCN length, or by using the sural nerve graft to bridge the defect.

7. Tendon transfer / Muscle transfer / Free functioning muscle transfer (FFMT) for elbow flexion restoration Steindler flexorplasty Steindler flexorplasty was firstly described by Steindler in 1918. By transferring the common flexor mass origin from medial epicondyle of distal humerus to one or more inch proximally of humerus shaft, the elbow flexion can be restored by forearm flexor. (56) The surgical procedure is modified by moving a bony part of medial epicondyle along with flexor muscle, which can

enhance the healing and shortening the recovery time. (57) Although nerve transfer provides good result of elbow flexion restoration and become a trend, the Steindler flexorplasty still play a role in treating upper arm BPI. If the forearm flexor is functioning with strong muscle power (≥ M4), the Steindler flexorplasty is indicated in certain situations, including patients with delayed presentation, patients with previous reconstruction surgeries failure, or combined use with nerve transfer to reinforce the elbow flexion power. The patient received Steindler flexorplasty need to make a fist and pronation in order to flex the elbow joint, so-called “Steindler effect”. Further modification was introduced by Brunelli et al. by transferring the flexor mass with flexor digitorum superficialis left in place. they obtained an 81% useful elbow flexion without Steindler effect. (58)

Latissimus dorsi (LD) transfer Neurotization provides a most optimal result in treating the acute upper arm BPI. However, patients with delayed presentation or failure of previous neurotization may need a salvage procedure to restore an acceptable elbow flexion function. Using the LD transfer to restore elbow flexion has been reported for 60 years (59). LD is innervated by the thoracodorsal nerve which is mostly preserved in patients with C5-6 injury. In the other hand, in C5-6-7 complete injury, LD muscle may not be available for transfer. Careful pre-operative evaluation of LD function is crucial for the success of LD transfer. There are two types of transfer, including unipolar transfer and bipolar transfer. In bipolar transfer, the insertion of LD over humerus was mobilized and anchored to the coracoid and conjoin tendon with careful protection of neurovascular pedicles. The origin of LD then be transferred to the distal biceps tendon or radial

tuberosity. This bipolar transfer provides a more ideal vector of pull force. (60) However, similar elbow flexion strength regained was reported between unipolar transfer and bipolar transfer. (61) The success rate of LD transfer for restoring elbow flexion function is acceptable with 80 - 84.6% (≥ M3 elbow flexion) (62)

Gracilis free functioning muscle transfer (FFMT) FFMT transfer is a useful technique in BPI reconstruction by transferring an entire gracilis muscle with neurovascular bundle to act as a new motor function. The muscle part of gracilis is suture to the distal clavicle, coracoid process, or rib and the tendon part of gracilis is suture to distal tendon of biceps. The motor nerve of gracilis muscle (Obturator nerve) usually is sutured to ICNs or SAN and there was no significant difference in success rate between using ICNs and SAN as neurotizers. (63) (Figure 11) Reinnervation of transferred gracilis muscle will be observed within 6 to 9 months and gradually matured after 2 years. (3) Using a branch of MN as a neurotizer has been reported by Bertelli. A reversed positioned of gracilis FFMT transfer was introduced to avoid the difficulty of dissection over supraclavicle or infraclavicle region which is operated previously. The muscle part of gracilis muscle is sutured to the elbow region and is reinnervated by a branch of MN. This reversed gracilis FFMT combined with Steindler flexorplasty provides a 96% success rate (≥ M3 elbow flexion). (64) Although relative high technique demanded, elbow flexion can be restored with 75% to 80% ≥ M3 elbow flexion by gracilis FFMT. (3,65,66) (Figure 12) In the current trend, gracilis FFMT are mostly reserved for the secondary reconstruction of BPI.

8. Elbow, wrist, finger extension restoration In upper arm type BPI, many patients have combined C5-6 injury and C7 injury. The involvement of C7 root will cause loss of elbow extension, wrist extension, and hand extension function. The reconstruction of C5-6-7 injury is more challenge and the result is less satisfied. The intraplexus neurotization, such as TRN to AXN cannot be done, when the triceps muscle is weak. Instead, the extraplexus neurotization, such ICN to AXN, may be used to restore the deltoid muscle function. In patients without pre-ganglionic lesion, nerve grafting can be performed between C7 stump to posterior division of middle trunk or radial nerve. However, restoration of the elbow extension, wrist extension and hand extension in patients with post-ganglionic lesion may be benefit from other procedures which are described below.

Restoration of elbow extension function ICN transfer to TRN In treating the upper arm type BPI, elbow flexion and shoulder function restoration is generally in highest priority. However, restoration of elbow extension can obtain a more useful upper limb function which can reach out the hand with stable elbow extension function without aid of contralateral hand. Thus, direct ICNs transfer to TRN without interposition nerve graft was used to restore the elbow extension function. (Figure 13) By transferring two to three ICNs to TRN, elbow extension can be restored with acceptable result (56% to 80% ≥ M3) (67,68)

Restoration of wrist and hand extension function

Patients with C7 injury will loss the function of wrist, finger and thumb extension function which will compromise the functional outcome. To restore the wrist and hand extension function, several tendon transfer and nerve transfer methods can be used with a satisfied result. For wrist extension, the pronator teres (PT) can be transferred to the extensor carpi radialis brevis (ECRB) in simple radial nerve palsy patients. However, the PT function may be injured in upper arm type BPI, and the PT to ECRB transfer only be indicated when the function of PT is preserved or recovered after reconstruction. Recently, never transfer was also used to reinnervate ECRB muscle to restore wrist extension function. Nerve branch of anterior interosseous nerve (AIN) to pronator quadratus transfer to nerve branch of RN to ECRB was introduced to reinnervate ECRB muscle with a good result of 90% success rate (≥ M4 wrist extension). (69) For fingers and thumb extension, tendon transfer provides a reliable and good functional outcome, including palmaris longus (PL) transfer to extensor pollicis longus (EPL), and flexor carpi radialis (FCR) transfer to extensor digitorum communis (EDC). (Figure 14) The finger and thumb function can also be restored by transferring flexor carpi ulnaris (FCU) to EDC, and PL to EPL. However, the FCU transfer may lead wrist radial deviation and should be carefully considered. Other alternative method is transferring the long and ring finger tendon of flexor digitorum superficialis (FDS) to the extensor tendons. The long finger tendon of FDS is transferred to EPL together with transferring ring finger tendon of FDS to EDC. (Figure 15)

[ Pain management for upper arm type BPI ]

In consideration of the quality of life, pain management is one of the most important part in treating BPI patients. After nerve injury, pain usually occurs within weeks and then becomes chronic. The intolerable pain may result in poor compliance of rehabilitation program, limitation of social activity, and significantly decreased quality of life. The oral medications, such as NSAIDs (Non-steroid anti-inflammatory drug), narcotic and anticonvulsants, are usually the first-line treatment. However, a part of patients suffered from persisted intractable pain, despite of conservative treatments. For these patients, surgical intervention can be performed with dorsal root entry zone (DREZ) rhizotomy. By performing thermocoagulation (rhizotomy) at DREZ, the pain can be effectively relieved. The author reported a 80% excellent to good pain relief in early post-operative period and gradually dropped to 50% excellent to good pain relief in 10 years follow-up. (3,70) More studies are needed to improve the pain management in BPI patients.

[ Rehabilitation after reconstruction procedures ] To maximize the functional outcome of patients with upper arm type BPI, the proper reconstruction procedures is not the only key factor, but also the post-operative rehabilitation. The adequate initial post-operative protection is needed to avoid an incidental damage to the structure that just be restored. In addition, the protecting splint or brace should be well tolerated by patient. The passive range of motion exercise should be started as soon as possible once the surgical anatomic structure becomes stable. Electrical stimulation can also facilitate the functional recovery by enhancing the nerve regeneration after surgical repair. (71) The home electrical stimulation with a portable slow pulse stimulation device is applied 4 to 6 hours per

day for at least 2 years in every patient who receives nerve repair or transfer. The specific rehabilitation programs are also needed depend on the different neurotization methods that patients received. Patients receive elbow flexion restoration with Oberlin transfer or double nerve transfer need hand grip-power training. Patients receive SAN transfer need trapezius muscle training. Patients received ICNs or PN transfer need respiration training. Adequate physical training may enhance the functional outcome and shortening the recovery time.

[ Objective assessment of the motor recovery after reconstruction procedures ] The Medical Research Council (MRC) grading system for muscle power evaluation is widely be used, because it is quick and easy to use. It is also commonly used to evaluate the recovery of muscle strength after reconstruction procedures. However, the MRC grading system may not precisely describe the muscle strength improvement, because of it has only simple grading from M0 (no muscle contraction) to M5 (Normal muscle strength). In consideration of the fine improvement of muscle power during the recovery period, a more objective and detailed assessment method is needed. The Hand-held dynamometer (HHD) was introduced to evaluate the muscle strength improvement during the rehabilitation program and provided a more scientific assessment for the functional outcome. (72) The HHD evaluation demonstrated a good reliability for muscle power evaluation after neurotization procedures and it also revealed a better function restoration in patients with C5-6 injury than patients with C5-6-7 injury, which may not be found clearly by traditional MRC grading system. (73)

[ Summary ]

1. In upper arm type BPI reconstructions, restoration of elbow flexion is the first priority, followed by shoulder function restoration. Patients with additional C7 injury, restoration of elbow, wrist, and hand extension function are needed. 2. Current trends in upper arm type BPI reconstruction is neurotization methods. However, exploration of trauma site is still needed to confirm the extent of injury and the available stump that can be used for direct repair or grafting. 3. For elbow flexion restoration, intraplexus neurotization may provide a better outcome than extraplexus neurotization. The double nerve transfer (Oberlin II) seems to has a faster and better functional outcome than Oberlin I method. For patients with delayed presentations or previous procedures failure, LD transfer, Steindler flexorplasty, and gracilis FFMT can be used as salvage procedures. 4. For shoulder function restoration, simultaneously reinnervate the SSN and AXN can obtain an optimal result, such as SAN-SSN and TRN-AXN. In consideration of the complexity of shoulder function, restoring both rotator cuff muscle and deltoid muscle is a more ideal treatment through either nerve transfer or muscle / tendon transfer. 5. For elbow, wrist, and hand extension restoration in combined C7 injury, neurotization and tendon transfer can provide a reliable outcome and further enhance the functional outcome. 6. Adequate pain management will increase the quality of life in BPI patients. The DREZ rhizotomy is indicated for patients with medical treatment failure, for more efficient pain relief. 7. Post-operative rehabilitation is crucial. Continuously rehabilitation with physical therapy, electric stimulation, and specific training program will maximize the functional outcome.

8. Objective assessments of muscle power by HHD during the recovery period may reveal more precise improvement after reconstruction procedures. Conflict of interest statement The authors whose names are listed immediately below certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

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Figure 1: Through a supraclavicular approach, the ruptured stumps of SSN and C5-C6 were identified and debrided with a 2cm nerve defect. The clear cutting end is prepared for further sural nerve grafting.

Figure 2: The sural nerves were harvested as nerve grafts. Then the nerve defects of SSN and C5-C6 were repaired with coaptation suture and sural nerve interposition nerve grafts.

Figure 3: An extended reversed T-shape incision was designed and the SAN was identified as long as possible through anterior supraclavicular approach. Then the SAN was transferred (coaptation suture) to the SSN without tension.

Figure 4: The patient received left SAN to SSN transfer with an excellent shoulder function with elevation 150 degrees and M5 shoulder muscle power recovery.

Figure 5: The anterior branch of AXN and the TRN were identified through a posterior approach. The Somsak’s procedure was performed by transferring the TRN to the anterior branch of AXN without interpositional nerve graft.

Figure 6: The patient received the combined transfer with SAN to SSN transfer, and TRN to AXN transfer. An excellent shoulder function was obtained with elevation 150 degrees and M5 shoulder muscle power recovery. Figure 7:

Figure 7a: The deltoid muscle and trapezius muscle were identified and isolated.

Figure 7b: The trapezius muscle was transferred to the deltoid muscle with adequate tension to obtain an optimal result.

Figure 8: The biceps branch of MCN and fascicles of UN were identified. Then the Oberlin transfer was performed to reinnervate biceps muscle, and to restore elbow flexion function.

Figure 9: We identified the MCN branches to biceps and brachialis, and fascicles of UN and MN. Then the double nerve transfers were performed by transferring fascicles of UN to biceps branch of MCN, and fascicle of MN to brachialis branch of MCN. With the reinnervation of both biceps muscle and brachialis muscle, the elbow flexion function can be restored with an optimal result.

Figure 10: The patient received double nerve transfer to restore the right elbow flexion function. After surgery, patient obtained M5 elbow flexion recovery with full range of motion of elbow joint.

Figure 11:

Figure 11a: The gracilis muscle was harvested and transferred to right arm medial site. The distal tendon of gracilis was passed through the subcutaneous tunnel to reach the biceps distal tendon.

Figure 11b: The gracilis muscle was anchored to distal clavicle proximally and sutured to biceps tendon distally. Good perfusion of monitor flap of gracilis muscle was observed.

Figure 12: Good outcome (M4 elbow flexion power) was obtained after gracilis FFMT for right elbow flexion restoration. The shoulder function was reconstructed with double nerve transfer (SAN to SSN transfer and Somsak’s procedure)

Figure 13:

Figure 13a: two ICNs and TRN were identified with adequate length, and prepared for nerve coaptation suture.

Figure 13b: The ICNs can be sutured to the TRN without interposition nerve graft.

Figure 14:

Figure 14a: The FCR and PL were identified and harvested through minimal invasive approach.

Figure 14b: The FCR and PL were passed through the interosseous tunnel. Then the FCR was sutured to the EDC, the PL was sutured to the EPL, and PT was transferred to ECRB with adequate tension.

Figure 15: By transferring the FCR to EDC, PL to EPL, and PT to ECRB, the wrist and hand extension can be restored with good functional outcome.