Selection for surgery

In the Leiden Nerve Center, the Netherlands, surgery for NBPL is rarely performed before 3 months of age, but it is almost always done before the age of 7 months. In selecting infants for surgery, all cases of neurotmesis or avulsion are identified using the criteria discussed next. Infants are selected for surgery when external shoulder rotation and elbow flexion with supination remain paralytic after a 3- to 4-month period to await spontaneous recovery. ¹⁷ Impaired hand function is an absolute indication for nerve surgery as soon as the infant turns 3 months old. ¹⁸ If there is doubt about the quality of shoulder and elbow joint movements, surgical exploration is performed in the hope that errors would consist of not finding neurotmesis or avulsion during surgery rather than letting such lesions go without surgical treatment. Preoperative ancillary investigations in all patients consist of ultrasound of diaphragm excursions to assess phrenic nerve function and MRI myelography under general anesthesia to detect root avulsions. ^{19,​ 20}

19.3 Surgical exposure

19.3.1 Supraclavicular exposure

The surgical approach to NBPL inevitably begins in the supraclavicular region for exploration of the proximal brachial plexus. In the vast majority of patients, the supraclavicular exposure alone will suffice for a proper nerve repair and reconstruction. Surgery is performed under general anesthesia without the use of muscle blocking agents. The supraclavicular brachial plexus is exposed in the posterior triangle of the neck. Appropriate positioning of the patient is extremely important to facilitate the operation: the patient is supine, and the head is turned toward the opposite direction with the neck in gentle extension. The head is supported by a silicone ring, where the contralateral ear is placed in the recess of the ring; the nonaffected shoulder is positioned caudally to avoid compressing the cervical vascular structures. Neck extension is encouraged by placing a folded cotton cloth at the level of the lower cervical spine and upper thoracic spine in order to support the plane of the brachial plexus parallel to the floor; avoid narrowing the costoclavicular space with an excessively thick folded cloth. The affected arm lies completely in the sterile field and is supported as close as possible to the edge of the operating table in 0-degree abduction during exploration and in 45 degrees of abduction during nerve repair. For easier access to the dorsal aspect of the legs for the harvesting of sural nerve grafts, the length of the operating table is reduced as much as possible. The lower part of the face, neck, shoulder, chest, and legs are prepared for surgery. A linear incision just lateral to the sternocleidomastoid muscle is made approximately 0.5 cm (in case the lower plexus is affected as well) to 1.5 cm (for upper plexus lesions) above and parallel to the clavicle. The platysma is incised perpendicular to its fibers, and a generous subplatysmal dissection is performed. The external jugular vein is often encountered and must be retracted or ligated when necessary. The position of the spinal accessory nerve is relatively superficial as it courses from the posterior aspect of the sternocleidomastoid muscle (two-thirds of the distance from the sternum to the mastoid) toward its insertion in the trapezius. Identification of the spinal accessory nerve along its course is crucial to preserve trapezius function or to use its terminal branches as donor for nerve transfer. An intraoperative nerve stimulator can be used to identify and confirm the course of the spinal accessory nerve.

The lateral margin of the sternocleidomastoid muscle is identified, with its sternal and clavicular heads. The lateral aspect of the clavicular head is released to facilitate exposure. The supraclavicular nerves (sensory nerves branches of the ansa cervicalis, C2–C4) are identified along their superficial cranial–caudal course. These nerves are likewise preserved for anatomical landmarks, or used as donors for sensible extraplexal to intraplexal transfers in total plexus lesions ²¹ and, occasionally, for potential donors for nerve graft material. The supraclavicular nerves are followed proximally until the C4 spinal nerve root is identified. The cervical fascia/scalene fat pad is released parallel to the sternocleidomastoid starting at the level of C4 in a cranial to caudal direction; at the retroclavicular level, the dissection of the fat pad turns 90 degrees lateral and parallel to the clavicle. The resulting cervical fascia/scalene fat pad can be mobilized for the exploration, then replaced at closure to cover the nerve grafts and nerve coaptation sites after the reconstruction. The cervical fascia/scalene fat pad should be preserved as much as possible, that is, coagulation should be avoided, as it may contribute to the revascularization of nerve grafts and may provide the optimal environment for the nerve elements. The thoracic duct should be preserved or ligated to avoid chyle leakage if the fat pad is released to expose the left supraclavicular brachial plexus. The transverse cervical artery and vein running parallel to the clavicle ventral to the BP elements are retracted or ligated. The omohyoid muscle is identified between the superficial and the deep cervical fascia along its course toward the suprascapular notch, and it can be tagged and retracted. Note that preserving this muscle to identify the suprascapular notch can facilitate the identification of the suprascapular nerve, especially in patients whose anatomy is distorted by trauma.

After the C4 spinal nerve root has been identified, its branch to the phrenic nerve is followed. The phrenic nerve is dissected along its length on the ventral aspect of the anterior scalene muscle. One should carefully mobilize the phrenic nerve to preserve the function of the diaphragm, which is especially important to infant respiration. Four pointers to facilitate the safe identification of the phrenic nerve follow. (1) The phrenic nerve cannot always be macroscopically seen directly because it may be covered by the deep transverse cervical fascia; the transparency of this fascia varies depending on its thickness and any scar present. Nerve stimulation to identify the course of the phrenic nerve from medial to lateral over the surface of the anterior scalene muscle is extremely helpful and is, in our opinion, indispensable. (2) the phrenic nerve origin can be located at the caudal aspect of C4; the phrenic nerve usually originates from C3 and C4; often there is a connecting branch from C4–C5. ²² Traction to the brachial plexus may result in a concurrent traction injury of the phrenic nerve via this connection. (3) The artery and vein that are adjacent to the phrenic nerve should not be identified erroneously as the nerve. (4) The authors have occasionally encountered a separate auxiliary phrenic nerve at higher cervical levels.

The phrenic nerve courses lateral to medial toward the diaphragm, while the contents of the plexus and the surrounding nerves course from medial to lateral. As the phrenic nerve approaches the lateral edge of the anterior scalene, the C5 spinal nerve root emerges; this is a reliable location for the identification of the C5 nerve root. The phrenic nerve is completely neurolyzed in its trajectory ventral to the anterior scalene muscle to allow gentle medial retraction without significant traction. In some patients, the phrenic nerve may be adherent to the neuroma of C5. Some neuroma scar tissue should deliberately left on the phrenic nerve instead of dissecting flush on the phrenic nerve and remove all the C5 neuroma in order to maximize preservation of diaphragmatic function. Resection or partial resection of the anterior scalene muscle is always performed to allow for optimal exposure of the proximal, intraforaminal part of the spinal nerve roots. A pseudomeningocele that extends extraforaminally may be encountered during such proximal exposure. Extraforaminal expansion of cells should be preoperatively identified on MRI.

Following the C5 root distally leads to the upper trunk, and following the upper trunk proximally will lead to the C6 spinal nerve root. The C6 spinal nerve root is located caudal and dorsal to the C5 spinal nerve root. The anterior tubercle of C6 can be very prominent (Chassaignac’s tubercle). The C7, C8, and T1 spinal nerve roots are sequentially more caudal and dorsal. A transverse cervical artery and vein cross the C7 spinal nerve root and can be ligated. Following the C7 spinal nerve distally will reveal the middle trunk. The C8 and T1 spinal nerves combine quickly to form the lower trunk, which is adjacent to the subclavian vessels. The roots of the lower trunk surround the first rib; therefore, care should be taken to avoid injury to the pleura. Special attention should be given to the vertebral artery, as in proximal dissection it runs unprotected at the level of the roots C8/T1 before it enters the vertebral canal in the lateral mass of C7. ²³

The next step is to identify the suprascapular nerve and the divisions of the upper trunk. The upper trunk can be seen to “split” into three separate structures—from lateral to medial, the suprascapular nerve, the posterior division, and the anterior division. ^{24,​ 25} The suprascapular nerve originates from the lateral aspect of the upper trunk and normally follows a slightly oblique cranial–caudal course toward the suprascapular notch (the omohyoid also attaches at the suprascapular notch). Caudal displacement of the superior trunk will alter the trajectory of the suprascapular nerve to a more horizontal direction. It may be necessary to extend the surgical exposure to the retroclavicular region to improve exposure of the distal stumps. To facilitate adequate exposure, the retroclavicular space can be easily expanded by suspension of the clavicle by retraction using a Penrose drain or gauze passed immediately underneath the clavicle ( ▶ Fig. 19.1). ²⁶ Suspension of the clavicle additionally facilitates the proximal dissection of the lower roots when indicated. Should a more extensive exposure be necessary, a clavicle osteotomy may be considered, although the authors have never done so and managed well without so far.

19.3.2 Infraclavicular exposure

Infraclavicular extension of the lesion in NBPL is quite rare. It may be indicated to explore donor nerves for transfers originating from the infraclavicular brachial plexus. The infraclavicular brachial plexus is exposed through the deltoideopectoral groove. A linear incision is made from the clavicle toward the axilla, overlying the deltoideopectoral groove. The cephalic vein is visualized within the groove, and it can be retracted laterally or ligated. If needed, a portion of the pectoralis major muscle can be detached from the inferior surface of the clavicle and from the humerus. The cuff of tendon from the humerus is tagged to facilitate later repair. The pectoralis major muscle is retracted caudally and the deltoid laterally, revealing the underlying coracoid process with its muscle attachments. Blunt dissection will separate the pectoralis minor from the coracobrachialis and the surrounding tissues. Once the pectoralis minor tendon has been isolated, it may be divided with later reapproximation, but usually muscle retraction will suffice. The infraclavicular brachial plexus elements lie immediately dorsal and caudal to the pectoralis minor. When the arm is at or lower than the plane of the shoulder, the most superficial structures are the lateral cord with its lateral branch leading to the musculocutaneous nerve and its medial branch leading to the median nerve. The medial cord may be identified medial and slightly posterior to the axillary artery, and the lateral branch of the medial cord will lead to the median nerve (the medial branch continues down the arm as the ulnar nerve). Exposure of the posterior cord and its axillary and radial nerve branches is best accomplished in the region lateral and posterior to the axillary artery, in contrast to the medial posterior course, which is frequently and erroneously depicted in schematic anatomical drawings. ²⁷ The axillary nerve branches from the posterior cord runs through the quadrilateral space above the latissimus dorsi and teres major tendons; this nerve can be identified more easily by externally rotating the humerus.

19.3.3 Exposure and technique for nerve transfers

If nerve transfers are indicated, ²⁸ the donor nerves must be exposed. It is imperative that donor nerves have normal function; direct electrical stimulation intraoperatively can assess their function and aid in their identification.

The spinal accessory nerve (SAN) is a commonly employed donor nerve for neurotization to the suprascapular nerve (SSN) for restoration of shoulder function. The SAN can be located as it approaches and enters the anterior surface of the trapezius muscle as described earlier. The nerve gives off a proximal branch to the superior part of the trapezius muscle, which must be kept intact. The SAN is mobilized, then transected as distally as possibly. The proximal stump is then passed through the cervical fascia/scalene fat pad to allow for the direct coaptation with the SSN. The caliber of the SAN usually corresponds well to that of the SSN. Alternatively, a dorsal approach can be applied to perform a SAN to SSN transfer. ²⁹ Theoretically, this transfer carries the advantage that the nerve coaptation is performed closer to the target muscle, leading to shorter recovery time. A proper comparison between both techniques has not yet been performed.

Another commonly used donor nerve is the medial pectoral nerve (MPN) ²¹; it is used for nerve transfer to the musculocutaneous nerve (MCN) for restoration of elbow flexion. The MCN can be identified in its course dorsal to the pectoralis major and minor muscles. Generally, the MPNs can be reached by retracting the pectoralis major muscle cranially through an incision in the lower part of the deltopectoral groove, which further extends distally over the proximal medial bicipital groove. The MPN originates from the medial cord, and its function remains intact in C5–C6 or C5–C6–C7 lesions. ³⁰ Intraoperative nerve stimulation is indispensable step for the identification of the MPNs since small vessels simulate their appearance and course. There are usually two individual MPN branches, and they should be cut as distally as possible, then coapted to the MCN. The total cross-sectional area of the MPN branches is usually less than that of the MCN. If so, the epineurium of the MCN is opened approximately 270 degrees and subsequently the perineurium is opened and the cross-sectional diameter of the individual fascicles is assessed. Subsequently, the MCN fascicle with a diameter comparable to the MPNs is cut and a direct coaptation is made between the MCN fascicle and the MPNs. Usually, more than half of the MCN can be covered with the MPN donor.

Another nerve transfer technique for restoration of elbow flexion uses intercostal nerves (ICNs) as donors and the MCN as recipient. The technique for ICN transfer in adults has been described previously. ³¹ The same surgical technique is applied in infants with NBPL. Either ICN 3 to 5 or 4 to 6 are exposed by means of an undulating, skin incision over the ipsilateral chest: the incision starts at the anterior axillary line at the inferior border of the pectoralis major muscle and continues beneath the nipple, extending medially to the costosternal junction. The inferior part of the pectoralis major muscle is shifted upward, with partial detachment of its sternal insertion if necessary. The rib attachments of the serratus anterior muscle usually remain intact. The main branch of the ICN is identified halfway in its ventral course between the external and internal interosseus intercostal muscle by means of blunt dissection in the muscle fiber direction and dissected free over its entire anterior course. Care should be taken to keep the periosteum of the ribs intact in order to avoid rib cage deformities during growth. ICN motor responses are assessed by using electrical nerve stimulation. If feasible, sensory branches are identified by their course toward the skin and left intact after they have been interfascicularly dissected from the main nerve. The three ICNs are then transected as close as possible to the sternum to obtain sufficient length for direct coaptation to the MCN and are tunneled to the axilla. The infraclavicular and intercostal wounds remain separated from each other by an area of intact skin at the anterior axilla, facilitating wound closure and healing. In female infants, if the anatomical localization of sensory innervation to the nipple is uncertain, the third ICN is left untouched to preserve at least partial sensation to the breast. The MC nerve is cut proximally after freeing it from the lateral cord until fascicular intermingling is encountered. No attempt is made to identify the motor branches within the MC nerve. However, the epineurium of the MCN is carefully dissected at the site of the stump in order to perform a targeted coaptation of the ICNs to the MCN fascicles. Before coaptation, the infant’s arm is abducted 90 degrees. The ICNs are coapted to the centrally located MC nerve fascicles by means of fibrin glue.

Other nerve transfer techniques have been described in literature using the phrenic nerve as donor, or an isolated fascicle of the ulnar or median nerve, or an intact nerve in an end-to-side fashion. ³² The use of the phrenic nerve at an early age might carry the risk of pulmonary problems in the immediate postoperative period lasting to adulthood, so it is not employed in our center. The authors do not routinely use the ulnar nerve fascicle to MCN (biceps muscle branch) transfer nor the median nerve fascicle to the MCN (brachialis muscle branch) transfer, as alternative options as described earlier have always sufficed. The technique and results in NBPL have extensively been described. ^{33,​ 34,​ 35} These techniques theoretically carry potential risks for hand function, although this has not been investigated systematically. Some authors employ the triceps branch to axillary nerve transfer for augmentation of shoulder function, but large series have not been published yet. The end-to-side option is not reliable enough for routine use. ³² The use of the hypoglossal nerve as donor was abandoned after it became apparent that volitional control after reinnervation does not restore. The reinnervated muscle contracts only when the tongue is pushed against the hard palate. Consequently, when patients talk or eat, they cannot move the limb. ^{36,​ 37} Much less is known about the quality of central control following transfer of the contralateral C7 spinal nerve in NBPL infants. Therefore, the authors have not used the contralateral C7 spinal nerve as a donor so far. ^{38,​ 39} This transfer might be a salvage option in those rare cases with avulsion of all five roots.

19.4 Assessment of the severity of the lesion

The severity of the NBPL lesion of each clinically involved spinal nerve is assessed. A distinction is made between axonotmesis, neurotmesis, and root avulsion on the basis of (1) inspection of the status of nerve continuity at the intraforaminal level in combination with presence or absence of root filaments on MRI myelography; (2) the extent and location of neuroma formation; and (3) selective electrical stimulation of all of the involved spinal nerves using a bipolar forceps in combination with a 2.5-Hz pulse generator with increasing voltage (maximum 6 V). Intraoperative nerve action potential (NAP) and compound motor action potential (CMAP) recordings did not add to the decision-making during surgery in infants with NBPL in our experience. ⁴⁰ Systematically recording from damaged nerves and control nerves of the upper brachial plexus showed statistically significant differences between normal, axonotmesis, neurotmesis, or root avulsion groups. For the individual patient, however, a clinically useful cut-off point for NAP and CMAP recordings to differentiate between avulsion, neurotmesis, axonotmesis, and normal could not be found. The sensitivity for an absent NAP or CMAP was too low for clinical use.

A spinal nerve root is considered avulsed when the nerve at the intraforaminal and juxtaforaminal level exhibits root filaments, the dorsal root ganglion is visible, neuroma formation is absent, and there are no muscle contractions after direct stimulation. During surgery for NBPL, it is unusual to find the avulsed nerve completely out of its foramen; it remains often attached with a pseudocontinuity, which is lost as one progressively dissects further proximally into the foramen. For this reason, it is indispensable to perform a very proximal dissection, with adequate resection of the anterior scalene muscle. These findings usually correspond with the absence of root filaments on MRI or CT myelography. Avulsions are found quite frequently; even in supposedly simple C5–C6 lesions, radiological examination showed a root avulsion or partial avulsion in 11/26 of patients. ⁴¹ Avulsed roots are cut as proximally as possible. When the dorsal root ganglion can be morphologically identified, it is dissected from the ventral root and removed. After confirmation by frozen section of the presence of ganglion cells, it is certain that the distal stump consists only of the ventral root. This ventral root can be the target for nerve grafting, or the ventral root can be attached to a qualitatively good nerve stump directly without a nerve graft.

A spinal nerve is considered neurotmetic when the following features are present: a normal appearance at the intraforaminal level, a clear increase of the cross-sectional diameter at the juxtaforaminal level ( ▶ Fig. 19.2), abundant epineurial fibrosis, loss of fascicular continuity, and increased consistency and increase of the length of the nerve elements with concomitant distal displacement of the trunk divisions. Electrical stimulation of the spinal nerve proximal to the neuroma may cause weak muscle contractions that are detectable with palpation but are not strong enough to move the limb. Resection of neurotmetic tissue is performed, and the proximal and distal stumps are prepared for nerve reconstruction. After resection of the neuroma, the proximal and distal stumps are examined with frozen section histology. The quality of the proximal stump is evaluated by the percentage of myelination, and corresponds with outcome. ⁴² Additionally, amount of scar tissue and architecture of the proximal and distal stumps are evaluated, to decide whether further resection is indicated. ⁴³ A spinal nerve is considered axonotmetic when neurolysis reveals no substantial increase of the cross-sectional diameter, only limited epineurial fibrosis, and intact fascicular continuity. Furthermore, on C5 stimulation, abduction with movement of the limb and some external rotation should be present, and on C6 stimulation, elbow flexion against gravity with supination should be found. Axonotmetic nerves are left in situ because spontaneous nerve regeneration is in process, although as yet clinically not clearly apparent. Axonotmesis is confirmed by the occurrence of good spontaneous recovery after at least 2 years of follow-up.

19.5 Principles underlying strategies for surgical reconstruction

The primary goal of nerve repair in patients with NBPL is restoration of hand grasp function, when indicated. The second priority is restoration of elbow flexion; the third is the restoration of shoulder movements; and the fourth is extension of the elbow, wrist, and fingers. The surgical repair/reconstruction strategy depends on the number of available viable proximal spinal nerve stumps for grafting, the cross-sectional area of the stumps, and the availability of donor nerves for neurotization. The resultant functional outcome is determined by integrity of the specific surgical connections made between proximal and distal stumps. For the purposes of the discussion of surgical strategies, the most common lesions are divided as shown in ▶ Table 19.1.

In the majority of NBPL lesions, nerve traction has resulted in neurotmesis of the upper and/or middle trunk. The classic approach to these lesions is to resect the neuroma and bridge the deficit with autologous nerve grafts. Recently, in adult brachial plexus lesions, the use of nerve transfers has become more popular, as results are at least equal to traditional nerve grafting, or may be superior. ⁴⁴ Advantages of this strategy consist of a shorter distance to the target muscle resulting in quicker recovery, and shorter operating time. The strategy to perform nerve transfers without exploring the brachial plexus, however, carries a number of drawbacks. The first is that it is not logical to leave a repairable lesion in place, and repairs only part of the functions of the superior trunk with nerve transfers. For instance, recovery of elbow flexion may be regained by a fascicular ulnar transfer to the biceps branch of the MCN, but by nerve reconstruction at the brachial plexus level additionally the brachialis muscle, the brachioradialis muscle, and the superior pectoral muscle are reinnervated, and sensation to the thumb is restored. Moreover, results of nerve grafting at adequate timing has led to very satisfying results in NBPL patients (contrary to adults, in whom nerve reconstruction results are modest—except for elbow flexion), which diminishes the drive to seek surgical alternatives.

At present, only small series have been published or presented with relatively short follow-up. ^{45,​ 46} Nerve transfers can only be applied if the ulnar nerve function is intact, and in case of a triple transfer the radial nerve. The use of the SAN partially sacrifices trapezius muscle function, which may have an effect on scapula stabilization. All in all, the authors do not favor sole application of distal transfers for routine use. It may be a viable option in infants who were referred late, as delayed nerve grafting beyond the age of 12 to 18 months is assumed to lead to declining results.

19.5.1 Group 1: C5, C6/Upper Trunk Lesions

C5, C6/upper trunk lesions comprise the lesions in the majority of NBPL patients. Three different types of C5, C6 lesions are observed clinically. In type 1, neurotmetic lesions of C5, C6/upper trunk are present. Since hand grasp function is essentially normal, the first priority of surgical intervention is restoration of elbow flexion, followed by reanimation of shoulder movements. The most common lesion observed intraoperatively is a C5, C6/upper trunk neuroma-in-continuity. ⁴⁷ The neuroma should be resected and nerve repair using sural nerve grafts is performed ( ▶ Fig. 19.2). At 4 to 5 months of age, the gap between the proximal and distal stumps is usually 2.5 to 3.5 cm, necessitating the harvest of the sural nerves from both legs. The authors always harvest sural nerves endoscopically using three small horizontal incisions, allowing for improved cosmesis; the length of each harvested nerve is usually 11 to 13 cm ( ▶ Fig. 19.3). Endoscopic harvesting of the sural nerve is facilitated by attaching the leg with sticky tape in a vertical position on a 90-degree iron bar. The usual strategy for nerve repair includes the use of one graft from C5 to SSN (placed at the rostroventral quadrant of the proximal stump of C5), ²⁵ two grafts from C5 to the posterior division of the upper trunk, and four grafts from C6 to the anterior division of the upper trunk. Depending on the size of the proximal stumps and the availability of nerve graft, an alternate strategy may involve a SAN to SSN transfer. Our results indicate that no difference in external rotation exists between nerve repair and nerve transfer to the SSN, which has been confirmed by other surgeons. ^{48,​ 49}

Related posts:

Clinical Aspects of Traumatic Peripheral Nerve Lesions in the Lower Limb Surgical Repair of Nerve Lesions: Neurolysis and Neurorrhaphy with Grafts or Tubes Nerve Injuries: Anatomy, Pathophysiology, and Classification Malignant Peripheral Nerve Sheath Tumors Ultrasound in Peripheral Nerve Surgery Nerve Anatomy of the Upper Limbs

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