Neurotization

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Neurotization is a surgical procedure that intentionally divides a physiologically intact nerve with little morbidity and transfers it to a distal more important but irreparably denervated nerve. The procedure is best done within a golden time period, which is defined as within 5 months of injury [8,9], to reactivate a paralyzed muscle or muscle groups early (4 to 6 months postoperatively), effectively, and successfully (M4 muscle strength). Neurotization can be broadly classified into four categories: extraplexus neurotization, intraplexus neurotization, close-target neurotization, and end-to-side neurorrhaphy neurotization. Combined neurotization such as combined extraplexus and intraplexus (Fig. 1A-C) for treatment of rupture and avulsion of brachial plexus injury, or combined extraplexus and close-target neurotization (Fig. 2A-C) for simultaneous treatment of the upper plexus avulsion injury, have now become options for a possible one-stage reconstruction.

Fig. 1. (A-C) An 18-year-old man who sustained rupture of C5 and avulsion of C6 of his right brachial plexus achieved good shoulder and elbow function 3 years after proximal C5 transfer to distal C6 with cable nerve grafts (intraplexus neurotization), and Ph and XI double neurotization to distal C5 (extraplexus neurotization).

Fig. 1. (A-C) An 18-year-old man who sustained rupture of C5 and avulsion of C6 of his right brachial plexus achieved good shoulder and elbow function 3 years after proximal C5 transfer to distal C6 with cable nerve grafts (intraplexus neurotization), and Ph and XI double neurotization to distal C5 (extraplexus neurotization).

Extraplexus neurotization

Extraplexus neurotization means transfer of a non-brachial plexus component nerve to the avulsed brachial plexus for neurotization of a de-nervated nerve. Donor nerves in common use mostly for motor reinnervation [7] include the phrenic nerve (Ph), spinal accessory nerve (XI), deep motor branches of the cervical plexus (CMB), intercostal nerves (IC), hypoglossal nerve (XII), and the contralateral C7 spinal nerve (CC7).

The Ph nerve is the motor nerve to the diaphragm, originating from C3 to C5, but mainly from C4. It lies on the ventral and medial surfaces of the anterior scalene muscle, but occasionally is found on the lateral surface of the muscle and descends obliquely toward the medial clavicle. It is always the first nerve encountered after dissection of the adipofascial tissue, below the transverse cervical vessels and nerve stimulation is required to identify it. The Ph nerve is such a powerful nerve that it has become an important donor nerve for transfer especially for shoulder elevation, although its transection can cause palsy of the diaphragm and a decrease in pulmonary capacity [7,10]. Ph nerve transection can cause severe respiratory distress in children younger than 2 years old, but in most adults, it causes no significant respiratory problem except for night dyspnea in a few cases. However, bilateral phrenic nerve palsies may cause orthopnea for 1 month in adults [7]. The Ph nerve is superior to hypoglossal and intercostal nerve transfers because of its characteristic of spontaneous rhythmic impulse discharge, which simulates a continuous internal nerve stimulator (termed "autophysiotherapy"). The Ph nerve can be dissected distally down to the medial clavicle by direct visualization with loupe magnification for direct coaptation to the distal C5 spinal nerve, suprascapular nerve, or posterior division of the upper trunk for shoulder function (see Figs. 1 and 2; Fig. 3). The Ph nerve can also be dissected distally to the diaphragm by endoscopic-assisted technique for direct coaptation to the radial nerve for elbow/wrist extension; to the musculocutaneous nerve for elbow flexion; or to the median or ulnar nerves for restoration of some intrinsic muscle function in the hand [11].

The XI nerve is the motor nerve of the sternocleidomastoid and trapezius muscles, lying behind the sternocleidomastoid muscle at a point within one finger breadth above the emergence of the greater auricular nerve, passing laterally, obliquely, and posteriorly in front of the trapezius muscle. Alternatively, the XI nerve can also be indentified subcutaneously on the anterior and lateral margins of the trapezius muscle after detaching the trapezius muscle from the clavicle. Nerve stimulation can confirm the location of the XI nerve. Dissection should be as distal as possible down to the two or three terminal rami that enter into the muscle, which are then divided

Fig. 2. An 18-year-old man had a C5 and C6 avulsion injury of his left upper limb. He underwent double neurotization with Ph nerve transfer to the posterior division of the upper trunk and XI nerve transfer to the suprascapular nerve (extraplexus neurotization) and part of the ulnar nerve transfer to the musculocutaneous nerve (close target neurotization). He achieved good shoulder function (A) and elbow flexion (B, C), but still showed subclinical deficits of the left ulnar nerve (hand grip strength, right: 52 kg, but left 32 kg) 3 years after surgery (D).

Fig. 2. An 18-year-old man had a C5 and C6 avulsion injury of his left upper limb. He underwent double neurotization with Ph nerve transfer to the posterior division of the upper trunk and XI nerve transfer to the suprascapular nerve (extraplexus neurotization) and part of the ulnar nerve transfer to the musculocutaneous nerve (close target neurotization). He achieved good shoulder function (A) and elbow flexion (B, C), but still showed subclinical deficits of the left ulnar nerve (hand grip strength, right: 52 kg, but left 32 kg) 3 years after surgery (D).

for transfer. The proximal stump can be transferred either to the retro- or supraclavicular region to coapt the suprascapular nerve (see Fig. 2; Fig. 4), or to the posterior division of the upper trunk directly, or to the infraclavicular region for free muscle transplantation. In addition to the main distal ramus being coapted to the recipient target nerve, the other two or three proxi-mally divided rami can also be elongated with a sural nerve graft (1 to 2 cm in length) to be coap-ted to the distal target nerve so no axons are wasted. The branches to the sternocleidomastoid muscle and the first branch to the upper trapezius are generally spared. The XI nerve is commonly transferred to the suprascapular nerve directly; or to the axillary or musculocutaneous nerves with a nerve graft; or to innervate a free muscle transfer and is considered to be more powerful than intercostal nerves [12,13].

The IC nerves are located beneath the periosteum of the ribs after dissection through the external and internal intercostal muscles. Each IC nerve has two main branches: the deep central and superficial lateral branches. The deep central

Fig. 3. An 18-year-old man suffered ruptured C5 and avulsed C6-7 injuries of the right brachial plexus. He achieved good shoulder elevation (A) and elbow flexion (B, C) 3 years after proximal C5 stump coapted to the musculocutaneous

and axillary nerves, even with long cable nerve grafts (14 axillary nerve 1/2).

branch is predominantly motor and commonly used for transfer. In T1 to T3, it lies on the upper margin of the rib; in T4 to T6, it lies at the lower margin of the rib; and in T7 and below, it is found in the intercostal and rectus abdominis muscles inferior to the rib. Two or three deep central branches are usually transected at the costochon-dral junction and transferred to neurotize the branch to the biceps; the branch to the long head of triceps; or a functioning free muscle

4 cm, two to the musculocutaneous nerve and two to the transfer. Mixed nerves including the deep central motor branches and superficial lateral branches are also often used to neurotize the mixed nerve of the musculocutaneous or median nerves. IC nerve transfer is quite effective in children more than in adult patients [14].

The CC7 spinal nerve has been proven to produce little significant loss of any specific muscle function [15,16]. There is no single muscle in the upper limb innervated by C7 only, and C7 innervated

Triple Nerve Transfer
Fig. 4. (A) A 23-year-old female had single C5 root avulsion. (B) She underwent triple neurotization with Ph, XI, and CMB nerves combined to the distal C5 stump and obtained good results one and half postoperatively.

muscles have cross-innervation with other spinal nerves. CC7, the most powerful donor nerve, is transected after the divisions and elongated either with a vascularized ulnar nerve graft to the median nerve in the total avulsion brachial plexus injury, or with cable nerve grafts to the C8 nerve in the lower plexus avulsion injury. These elongated nerve grafts are usually placed subcutaneously. CC7 nerve transfer can be performed in one stage with no need for a two-stage procedure. When performing a CC7 transfer, the contralateral Ph nerve should not be touched at all, otherwise a temporary palsy of the contralateral side of the diaphragm will result. This will produce bilateral phrenic nerve palsies in the patient with Ph nerve palsy or a Ph nerve that has been transected for transfer, and cause critical respiratory distress.

Cervical motor branches (CMBs) are deep branches of C4, passing posterolaterally to innervate the levator scapular, the rhomboids, and part of the trapezius. Nerve stimulation can help identify them. CMBs are often used as an adjuvant nerve to neurotize the suprascapular nerve or distal C5 for shoulder function with a nerve graft (see Fig. 3) [7]. Some surgeons use the CMBs for transfer to the long thoracic nerve, pectoral nerve, or the thoracodorsal nerve.

The XII cranial nerve, the hypoglossal nerve, is the motor nerve to the tongue and is located inferior to the submaxillary gland and deep to the tendon of the anterior belly of the digastric muscle. Nerve stimulation can distinguish it from the nearby lingual nerve, which is sensory. The author uses it for neurotization when the Ph nerve is avulsed; results have not been convincing [7]. It always requires a long nerve graft (> 10 cm) to coapt to the suprascapular nerve or distal C5 for shoulder function. Unilateral XII nerve transfer will cause half of the tongue to atrophy and deviation to the normal side when the tongue is protruded. It does not interfere with eating, drinking, or speech; however, the author has had the experience of bilateral partial XII nerve transfers in a patient with bilateral C4-T1 total root avulsion causing temporary but severe speech and swallowing disturbances.

Extraplexus sensory neurotization, such as IC nerve transfer or subclavicular nerve transfer to the median nerve, is sometimes used to restore sensation to the hand.

Intraplexus neurotization

Intraplexus neurotization is used in cases of nonglobal root avulsion, in which at least one of the spinal nerves is still available for transfer, not to its original pathway but to other more important nerves.

In a C5 rupture and C6 avulsion (see Fig. 1), or a C5 and C6 rupture at the upper trunk but the C5 stump is more healthy than C6, the C5 fibers are transferred to C6 or the anterior division of the upper trunk for elbow flexion. The posterior division of the upper trunk or suprascapular nerve is then innervated by the injured C6; or combined extraplexus neurotization with Ph and/or XI nerve transfer for shoulder function is performed.

In a C5 rupture and C6-T1 four-root avulsion, the C5 fibers are transferred to the distal C8 with cable nerve grafts, or transferred to the median nerve with a vascularized ulnar nerve graft for restoration of hand function, instead of nerve grafting to the distal C5 or upper trunk [5-7]. Such intraplexus neurotization is individualized depending on the intraoperative findings and judgment, surgeon's philosophy, patient's condition, and functional requirements [7].

Other donor nerves, called regional nerves by Samardzic and colleagues [17], have been used including the pectoral nerve [17,18], long thoracic nerve [17,19], thoracodorsal nerve [17,18,20], and branch of the subscapular nerve [17]. Intraplexus regional nerve neurotization is indicated in C5-6 avulsion of the brachial plexus. However, in C5-6 avulsion, C7 is usually not healthy either, and the regional nerves are therefore often partially denervated. In addition, a combined supra- and infraclavicular approach through a big incision is required for the intraplexus regional nerve neurotization. Because of these factors, in-traplexus regional nerve neurotization is not popular in the author's series.

Close-target neurotization

Close-target neurotization (CTN) is a procedure of nerve transfer providing direct coaptation at a more distal site closer to the end organ targets, muscle, or skin, thus achieving faster outcome of motor and sensory recovery. CTN is performed distal to the supra- and infraclavicular fossae because the donor nerve is not close to the target at this point. The recipient nerve should be close to the neuro-muscular junction for motor, or close to the sensory receptors for sensory reinnervation. The donor nerve should be functioning and close by for both motor and sensory nerve transfer. Examples of CTN include extraplexus neurotization such as XI nerve transfer to the suprascapular nerve through the upper back trunk approach; intraplexus neurotization, such as the long head of triceps nerve transfer to the axillary nerve through the posterior arm or axillary fossa approaches; partial ulnar nerve transfer to the musculocutaneous nerve through the medial upper arm approach; or partial median nerve transfer to the branch to brachialis in the arm or to the radial or posterior interosseous nerves in the forearm; and branch of the anterior interosseous nerve transfer to the deep motor branch of the ulnar nerve [21-23]. Sensory nerve transfers for restoration of sensation in the hand [22] are also examples ofCTN.

The advantages of proximal nerve neurotiza-tion versus close target neurotization are the subject of much debate. CTN has the advantages of direct nerve coaptation without the need for nerve grafting, a shorter operating time as dissection in the traumatized scar zone is avoided, and the nerve stumps are healthy with no scarring. Late-stage sensory and motor reeducation is, however, required because of the alteration in cortical mapping. The major disadvantage of the technique is the increased clinical or subclinical deficits resulting from dividing the donor nerve in a more distal region (Fig. 2D). The proximal source nerves such as the spinal nerves or brachial plexus nerves are more powerful, easier for brain cognition, and are mixed nerves for which partial division will produce fewer deficits than CTN. Intentional neglect of the proximal, original powerful mother nerve, and only performing direct distal coaptation is not theoretically accepted. CTN is most appropriate for cases of confirmed proximal brachial plexus avulsion, following excision of proximal brachial plexus neurofibromas (benign or malignant) for intrinsic nerve palsy of the median or ulnar nerves, and for single terminal nerve palsy such as an isolated axillary nerve palsy. It is not indicated in cases of rupture injury of the brachial plexus where the proximal stump is still available for neurotization (Fig. 3A-C).

End-to-side neurorraphy neurotization

End-to-side neurorrhaphy (terminolateral neurorrhaphy) neurotization is a technique to transfer the distal end of an irreparable nerve of a paralyzed muscle to the side of an intact nerve, with or without an epineurial window without needing any nerve transection. Its use has been reported for both motor and sensory reconstruction, but the author has never used this technique for brachial plexus injury. From the author's point of view, it is a functionless, but not functional regeneration. It might result in S2 or better sensation, but M2 or less motor function when applied in lower level distal nerve neurotiza-tion. M4 function is recognized as a functional reconstruction, which cannot be achieved by using this technique. For high-level brachial plexus injury, end-to-side neurotization will produce no effect.

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