Gross anatomy

The brachial plexus is formed by the anterior primary rami of the lower cervical (C5–8) and the first thoracic (T1) spinal nerves, which give motor innervation to muscles of the shoulder, including all anterior and posterior chest muscles related to glenohumeral joint movement, muscles of the entire upper limb, and sensory innervation of the entire upper limb, except the skin on some part of the medial aspect of the upper arm. In the “prefixed brachial plexus” C4 provides a significant contribution to C5, but T2 does not contribute. In the “postfixed brachial plexus” T2 has significant contributions to T1, but C4 does not. Clinically, the prefixed type is more common than the postfixed. A postfixed plexus in adult BPI has been rarely seen, probably because the injuries are either so extensive that further dissection of C8–T1 is hazadous and unnecessary, or the injuries are diagnosed not to involve C8–T1 so that further identification is also unnecessary.

Each spinal nerve is formed by the joining of the ventral root (motor fibers) and the dorsal root (sensory fibers). Each root is formed by a number of rootlets. The dorsal roots carry sensory information to the central nervous system, while the ventral roots convey motor fibers to the muscles. The cell bodies (neurons) of the motor fibers are located in the anterior horn of the spinal cord, while the cell bodies of the sensory fibers reside in the dorsal root ganglion located within the intervertebral foramen, immediately outside the dura mater of the spinal cord. The dorsal and ventral roots unite a few millimeters distal from the ganglion to form a spinal nerve, a mixed nerve, which goes through the interscalene space between the scalene anterior and middle muscles. Just out of the scalene muscles the five postganglionic spinal nerves make a first union to form the three trunks: upper (formed by C5 and C6), middle (C7 itself), and lower trunk (formed by C8 and T1 spinal nerves). Each trunk divides into anterior and posterior divisions just proximal to or directly under the clavicle. The nerves exchange fibers and form the second union, just distal to the clavicle, and are termed “cords.” Lateral and medial cords are anterior compartment nerves, passing anterior to the subclavian artery. The posterior cord is a posterior compartment nerve, passing posterior to the subclavian artery. The cords anterior to the subscapularis muscle run further distally behind the pectoralis minor muscle. Each cord has two or more terminal branches to the periphery (Fig. 36.1).

Fig. 36.1 Anatomy and numbered level of brachial plexus injury.

Disputed anatomy

Various classifications of the level of BPI have been proposed: two levels of injury described by Leffert¹ and Krakauer and Wood²; three levels by Terzis et al.³; four levels by Millesi,⁴ Alnot,⁵ and Chuang⁶; five levels by Narakas⁷; six levels by Mackinnon and Dellon⁸; and eight levels by Boome⁹ (Table 36.2). These numerous classifications have made the understanding of the anatomy of the brachial plexus complex and confusing. The most confusing aspect is the so-called postganglionic root (Fig. 36.2). Some anatomists term the part in the interscalene space before formation of the trunks to be “roots.”¹⁰ However, some call this part “spinal nerve.”¹¹ In fact, after the dorsal root ganglion, both ventral and dorsal roots continue for only a few millimeters (<5 mm) in distance and unite to become a mixed nerve where it is no longer a root (Fig. 36.2). Sunderland¹¹ has stated that “the term nerve root should be reserved for the paired anterior and posterior nerve roots in the spinal canal,” and that “the part of the plexus extending from the union of nerve roots to the formation of the trunks of the plexus should be referred to as a spinal nerve.” The author accepts this statement. Therefore, the components of the brachial plexus are roots, spinal nerves, trunks, divisions, cords, and terminal branches.

Table 36.2 Classifications for level of brachial plexus injury

Fig. 36.2 (A) The drawing shows that the postganglionic root is part a; postganglionic spinal nerve is part b from the anatomy point of view; (B) an avulsion C7 (distal stump) during dissection.

Numerous anatomical variations of the brachial plexus do exist^1,5 and should be always kept in mind. For example, the musculocutaneous nerve may sometimes arise from the median nerve and not from the lateral cord. In some rare cases of C5–6 root avulsion, the musculocutaneous nerve is still found to be functional because part of the musculocutaneous nerve derives from the median with its origins from C7.

Microanatomy

The microanatomy or internal topography of the brachial plexus has been extensively studied and described.^12,13 The monofascicular pattern is usually found in regions of: (1) the spinal nerves; (2) anterior and posterior divisions of the upper trunk; and (3) the origin of the suprascapular and musculocutaneous nerve. Marked changes in fascicular topography occur every 10 mm. It is especially true at the level of the upper trunk where interfascicular crossovers are so extensive that direct repair or repair with short nerve grafts will frequently lead to co-contractions due to aberrant regeneration of a group of muscles. This aberrant regeneration is mainly found in obstetrical brachial plexus palsy (OBPP) patients but rarely in adult BPI. In addition, plexus connective tissue is more abundant than neural tissue. All these factors are reasons why the results of brachial plexus nerve surgery are so unpredictable. Knowledge of the internal topography of the plexus can be helpful in connecting corresponding nerve fibers with bridging nerve grafts. However, localization within the spinal nerve to define specific axonal groups to supply specific muscles or specific branches is difficult and not practical.

Anatomy with level of injury

To avoid anatomical confusion, we have described brachial plexus lesions in terms of the level of injury 1–4 (Fig. 36.1). A total of 819 cases of adult BPI were included (1986–2003) in this new classification¹⁴ and the incidence at different levels was determined:

There are some relationships among the levels of injury:

There are two types of characteristic lesions seen in BPI: avulsion and rupture (Fig. 36.3). Both are traction injuries but with different characteristics. Avulsion refers to the nerve being torn from its attachment (proximal avulsion occurs at the spinal cord, distal avulsion at the muscle). Rupture is a nerve injury involving a traction force on an incompletely divided nerve, causing a complete division with irregular proximal and distal ends (Fig. 36.3C). In avulsion injury, only one disrupted end with a coiled spring-like appearance can be seen in the operative field in the acute stage (Fig. 36.3A or Fig. 36.4A), or a fusiform pattern (glioma) in the chronic stage (Fig. 36.3B or Fig. 36.4B). If a surgeon attempts to locate the other disrupted end, a second operative wound is usually required. However, in rupture injury the two nerve ends can be visualized in the same operative wound in the acute stage, or within a big neuroma noted in the chronic stage.

Fig. 36.3 The mechanism of (A,B) avulsion injury versus (C) rupture injury.

Fig. 36.4 (A) Coiled spring-like structure with irregularity of stumps of C5 and C6 avulsion (acute stage); (B) fusiform pattern neuroma (or glioma) of the distal C7 stump (chronic stage) during dissection.

Root avulsion is very common in BPI due to its weak supporting structures consisting of dura and dentate ligaments. A novel approach of performing spinal cord implantation with or without nerve graft^15,16 showed unsatisfactory clinical results. This implies that in avulsion injury only one end (distal end) is available, while the other end (proximal) end is absent or unsuitable for repair. “Root injury” is an obscure term which may mean avulsion from the cord (true avulsion), or rupture or stretch at rootlets or roots. Root avulsion in BPI is usually accompanied by dura tearing and a cerebrospinal fluid leak with cyst formation, called pseudomeningocele. However in some cases the root can be avulsed at its origin with an intact dura cone (called “avulsion in situ”). The nerve root may remain inside the spinal canal or at the dural orifice, giving a grossly normal appearance or loosening with curvature of the spinal nerve at the time of surgical intervention despite established paralysis. Most often, however, the entire avulsed root, including ventral, dorsal roots, and ganglia, retracts and migrates downward to the interscalene or preclavicular region.

Tinel’s sign

The Hoffman–Tinel’s sign is an important clinical sign to determine the location of a neuroma or to track the regeneration of the injured nerves. Palpation or percussion at the neck, at the supraclavicular Erb’s point (clavicular insertion of the sternocleidomastoid muscle), at the infraclavicular coracoid process of the scapula, or at the route of different nerves along their course may induce an electric current sensation (like pins and needles) running down to the shoulder or the hand (positive Tinel’s sign). If the Tinel’s sign remains at a fixed point, which means retardation of its progression, surgical exploration is warranted. If the Tinel’s sign advances from supraclavicular to infraclavicular and distally to the arm or forearm at successive examinations, observation is recommended, as this may indicate a Sunderland third-degree lesion. A weak or absent Tinel’s sign in the neck region usually indicates total root avulsion.

Horner’s syndrome

Horner’s syndrome (miosis, ptosis, enophthalmos, and anhidrosis) is a sign of sympathetic nervous system disturbance. It indirectly implies avulsion of the T1 and C8 roots because the sympathetic fibers from the T1–2 sympathetic ganglia are quite close to the preganglionic fibers of T1 and C8. This syndrome may regress with time. It is a more reliable sign in adult BPI, but less accurate in obstetric traction injury.

Plain X-ray and imaging studies

Plain X-rays of the chest and cervical spine are required. The chest X-ray should include inspiration and expiration views to exclude diaphragmatic palsy. Cervical spine X-rays are evaluated for any fracture of the transverse process, spinous process, or vertebrae body.

Cervical myelography and computed tomography (CT) myelography can provide valuable information related to the level 1 injury of the brachial plexus.²⁵ However, in recent years these studies have been gradually replaced by noninvasive magnetic resonance imaging (MRI).²⁶ The most useful MRI technique for the evaluation of a possible level 1 lesion is the three-dimensional (3D) fast imaging employing steady-state acquisition (FIESTA). These 3D source data are reconstructed along the planes of ventral and dorsal rootlets using a curve planar reformat technique to demonstrate the respective rootlets in a better perspective. Other MR techniques help in the imaging of the whole brachial plexus, notably of level 2 (Fig. 36.6).

Fig. 36.6 (A) Right C5–T1 avulsion cysts on the ventral view using magnetic resonance imaging (MRI) three-dimensional (3D) fast imaging employing steady-state acquisition (FIESTA) technique; (B) dorsal view, using MRI 3D FIESTA and curve planar reformat techniques; and (C) MRI cervical spine myelogram on the same patient; (D) MRI 3D, coronal view, avulsion cyst of the left C7, and (E) axial view for comparison; (F) MRI 3D diffusion-weighted imaging techniques to see the level 2 spinal nerves.

Level 1 injury: inside the (vertebral) bone (preganglionic root) injury, including spinal cord, rootlet, and root

The incidence of level 1 lesions is 70%. Nerves may be avulsed from the spinal cord (true avulsion), or ruptured at the preganglionic roots and rootlets. Partial Brown-Séquard syndrome is an example of true avulsion.²² One to all five roots may be avulsed. Root avulsion injuries lack central connection and are considered irreparable. Nerve transfer, pedicled muscle transfer, and FFMT provide the only possibilities for functional restoration.

Nerve transfer

Nerve transfer is a surgical option which intentionally divides a physiologically active nerve (with low donor morbidity) and transfers it to a distal, more important but irreparable paralyzed nerve. The procedure is best done within a golden time period, within 5 months of the injury,⁶ in order to reactivate the paralyzed muscle(s) effectively (aiming for M4). Nerve transfer can be broadly classified into four categories: (1) extraplexus; (2) intraplexus; (3) close-target nerve transfer; and (4) end-to-side neurorrhaphy nerve transfer.

Extraplexus nerve transfer

Extraplexus nerve transfer involves the transfer of a brachial plexus neighboring nerve (from either the ipsilateral or contralateral neck) to the avulsed brachial plexus for neurotization of a paralyzed nerve. The reported donor nerves in common use are mostly aimed at motor reinnervation.²⁹ These donor nerves include the phrenic (Ph) nerve, spinal accessory (XI) nerve (accessed by an anterior neck approach), deep motor branches of the cervical plexus (cervical motor branches, CMB), hypoglossal nerve (XII), and the contralateral C7 (CC7) spinal nerve. Extraplexus sensory nerve transfer such as supraclavicular sensory nerve to median nerve transfer is sometimes used to provide sensation to the paralyzed hand.

Intraplexus nerve transfer

Intraplexus nerve transfer is applicable in cases of nonglobal root avulsion, in which at least one of the spinal nerves is ruptured and still available for transfer – not to its original pathway, but to other more important nerves. For example, in a case of C5 and C6 rupture injury (level 2) in which the C5 stump is healthier than the C6 stump, the C5 fibers are intentionally transferred to C6 (or the anterior division of the upper trunk) for elbow flexion. The distal C5 (or the posterior division of the upper trunk and suprascapular nerve) is then innervated by the partially injured C6. This strategy acknowledges that elbow flexion has priority over shoulder reconstruction. Intraplexus nerve transfer is individualized depending upon the intraoperative findings, the surgeon’s philosophy, and the patient’s condition and requirements. Extraplexus and intraplexus nerve transfers are both considered as proximal nerve neurotization.

Closed-target nerve transfer

Closed-target nerve transfer is a procedure that provides a direct coaptation at a more distal site, closer to the neuromuscular junction, thus achieving faster recovery of motor outcomes. Closed-target nerve transfer is defined as a procedure outside the supra- and infraclavicular fossa. Examples include spinal accessory (XI) nerve transfer to the suprascapular nerve via a posterior approach; partial ulnar nerve transfer to the biceps nerve; partial median nerve transfer to the brachialis nerve; long head of triceps branch transfer to the axillary nerve; intercostal nerve transfer to the biceps nerve, the musculocutaneous nerve, or the nerve of the long head of triceps; anterior interosseus nerve transfer to the radial or posterior interosseus nerve; and branch of the anterior interosseus nerve transfer to the deep motor branch of the ulnar nerve in the forearm. Closed-target nerve transfer is considered as distal nerve transfer.³⁰ Selecting proximal or distal nerve transfer as a reconstructive strategy is now a subject of much debate (Table 36.4). Proximal nerve transfer (extraplexus and intraplexus nerve transfer) is traditionally still the main reconstructive procedure.

Table 36.4 Proximal nerve transfer versus distal nerve transfer in adult brachial plexus injury

	Proximal nerve transfer	Distal nerve transfer
Philosophy	Traditional	New strategy
Donor nerve	Supraclavicular, far from the target muscle	The nearby nerve close to the target muscle
Advantages	Diagnostic and treatment Proximal nerve(s), powerful Nerve cut, fewer functional deficits	A treatment procedure, but not diagnostic No scars, easy dissection Shorter operation time Nerve-cut stumps: healthy, no scar Direct repair; no need to graft nerve Short rehabilitation, faster recovery
Disadvantages	More scars, difficult dissection Health of cut stumps is unpredictable May need long nerve grafts Longer operation time Longer rehabilitation period	Nerve cut, risk of causing deficits Risk of iatrogenic injury May need multiple incisions
Indication	All kinds of avulsion/rupture injury of brachial plexus injury	Not global injury After brachial plexus neurofibroma (C5 and C6) resection Intrinsic palsy of the hand

End-to-side neurorrhaphy nerve transfer

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