Brachial Plexus and Nerves about the Shoulder

Carlo Martinoli, M.D.,1 Nicola Gandolfo, M.D.,2 Maribel Miguel Perez, M.D.,3 Andrea Klauser, M.D.,4 Federigo Palmieri, M.D.,1 Luca Padua, M.D.,5,6 and Alberto Tagliafico, M.D.1

ABSTRACT

Ultrasound (US) and MR imaging have been shown able to detect in-depth features of brachial plexus anatomy and to localize pathological lesions in disorders where electrophysiology and physical findings are nonspecific or nonlocalizing. High-end gradient technology, phased array coils, and selection of an appropriate protocol of pulse sequences are the main requirements to evaluate the brachial plexus nerves with MR imaging and to distinguish between intrinsic and extrinsic pathological changes. A careful scanning technique based on anatomical landmarks is required to image the brachial plexus nerves with US. In traumatic injuries, MR imaging and myelographic techniques can exclude nerve lesions at the level of neural foramina and at intradural location. Outside the spinal canal, US is an excellent alternative to MR imaging to determine the presence of a lesion, to establish the site and the level of nerve involvement, as well as to confirm or exclude major nerve injuries. In addition to brachial plexus injuries, MR imaging and US can be contributory in avarietyofnontraumaticbrachialplexopathiesofacompressive,neoplastic,andinflam- matory nature. In the thoracic outlet syndrome, imaging performed in association with postural maneuvers can help diagnose dynamic compressions. MR imaging and US are also effective to recognize neuropathies about the shoulder girdle involving the suprascapular, axillary, long thoracic, and spinal accessory nerves that may mimic brachial plexopathy. In this article, the clinical entities just listed are discussed independently, providing an overview of the current status of knowledge regarding imaging assessment.

KEYWORDS: Brachial plexus, Parsonage-Turner syndrome, brachial plexopathies, Downloaded by: Rutgers University. Copyrighted material. thoracic outlet syndrome, magnetic resonance imaging, ultrasound, MR myelography

Evaluation of the brachial plexus represents a tion is essential to understand which part or parts of the great challenge to the clinician and the radiologist, plexus are involved.2,3 Electrophysiology, including posing difficulties in patient management, the timing nerve conduction studies and electromyography and range of investigation, as well as the indication for (EMG), may serve to confirm and extend clinical in- surgery.1 In the diagnostic workup for brachial plexus formation, to assess whether a lesion is pre- or post- pathology, a preliminary meticulous physical examina- ganglionic based on the pattern of involvement.2,3

1Cattedra di Radiologia–DISC, Universita` di Genova, Genova, Italy; M.D., Cattedra di Radiologia–DISC, Universita` di Genova, Largo 2IM2S–Institut Mone´gasque de Me´decine and chirurgie Sportive, Rosanna Benzi 8, I-16132 Genova, Italy (e-mail: carlo.martinoli@ Montecarlo, Monaco; 3Unit of Human Anatomy and Embryology, libero.it). Department of Pathology and Experimental Therapy, Faculty of Imaging of the Peripheral Nerves; Guest Editor, Carlo Martinoli, Medicine (C Bellvitge), University of Barcelona, Barcelona, Spain; M.D. 4Department of Diagnostic Radiology, Medical University Innsbruck, Semin Musculoskelet Radiol 2010;14:523–546. Copyright # 2010 Innsbruck, Austria; 5Fondazione Don Gnocchi Onlus; 6Department of Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY Neurology, Policlinico ‘‘A. Gemelli,’’ Universita` Cattolica del Sacro 10001, USA. Tel: + 1(212) 584-4662. Cuore, Rome, Italy. DOI: http://dx.doi.org/10.1055/s-0030-1268072. Address for correspondence and reprint requests: Carlo Martinoli, ISSN 1089-7860. 523 524 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

However, functional studiesareoftennonspecificor brachial plexus pathologies, including traumatic injuries, nonlocalizing, especially at the early stage of some entrapment syndrome at the thoracic outlet, Parsonage- brachial plexopathies or in cases of mild abnormalities.4 Turner syndrome, secondary and primary tumors, and Imaging modalities, therefore, are a necessary comple- radiation therapy. In addition to the plexus, some ment to conclude the diagnostic assessment of most frequently missed uncommon neuropathies about the brachial plexus disorders. Imaging is currently based on shoulder girdle affecting the suprascapular, the axillary, magnetic resonance (MR) imaging, computed tomog- the long thoracic and the spinal accessory nerves are raphy (CT), ultrasound (US), myelographic techniques, discussed.9,10 and radiography.5–7 Although MR imaging is widely regarded as the method of choice in the workup of many brachial plexus disorders, this technique has NORMAL ANATOMY inherent limitations in specific clinical settings and The brachial plexus has a complex anatomy with many can be variably supported by other modalities depend- nerves involved that interconnect.11 At each vertebral ing on the underlying clinical problem but also on the level, anterior (motor) and posterior (sensory) nerve equipment used and the management policy of periph- rootlets exit the spinal cord and merge at the dorsal eral nerve surgeons. root ganglion at the level of the neural foramina. There- In the last decade, the diagnostic workup for after, each ganglion gives off a large ventral and a small evaluation of brachial plexus pathology has been con- dorsal branch, each including motor and sensory fibers. tinually reviewed with technological refinements in The dorsal branch provides nerve supply to the para- progress and the introduction of novel cutting-edge spinal muscles but does not take part in the brachial imaging algorithms.1,8 Light must be shed, therefore, plexus (Fig. 1A). Instead, the plexus is formed by the on where imaging is going to draw the current optimal contribution of the ventral branches coming from the imaging strategy for any indication, thereby avoiding four cervical (C5, C6, C7, and C8) and the first thoracic underutilization or inappropriate use of the available (T1) level (Fig. 1B). These branches are referred to as the imaging techniques. In this article, we discuss and proper ‘‘nerve roots’’ and extend from the neural fora- illustrate the imaging appearance of a wide spectrum of mina to the interscalene triangle. Downloaded by: Rutgers University. Copyrighted material.

Figure 1 Brachial plexus anatomy. (A) Schematic drawing of a cross-sectional view of the fifth cervical vertebra showing the spinal cord (black arrow). The spinal nerve arises from the spinal cord by dorsal (outlined arrowhead) and ventral (black arrowhead) rootlets. The spinal ganglion (G) is located on the dorsal root within the intervertebral foramen. The dorsal and ventral rootlets join at about the level of the intervertebral foramen to form a spinal nerve. Just outside the foramen, the spinal nerve divides into ventral (1) and dorsal (2) branches. The ventral branches participate in the brachial plexus, the dorsal ones direct posteriorly to supply the paraspinal muscles, including the multifidus (MF), the semispinalis cervicis (SS), the semispinalis capitis (SC), and the longus colli (LC). The spinal cord, the rootlets, the ganglion, and the spinal nerve are invested by the arachnoid and dura mater (white arrow). a, vertebral artery. Note that the sixth cervical nerve leaves the intervertebral foramen superior to the transverse process of C6. (B) Schematic drawing of the general structure of the brachial plexus. C5, fifth nerve root; C6, sixth nerve root; C7, seventh nerve root; C8, eighth nerve root; T1, first thoracic nerve root. Moving away from the spine, C5 and C6 join to form the upper trunk, C7 continues as the middle trunk, and C8 and T1 constitute the lower trunk. Each of the trunks splits into anterior and posterior divisions that further anastomose to give origin to the lateral, medial, and posterior cords. The level of origin of the long thoracic, suprascapular, musculocutaneous, axillary, radial, ulnar, and median nerves is shown. BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 525

At the external border of the interscalene triangle, pectoralis minor muscle, the cords continue as the five the roots unite to form three trunks: The roots of C5 and peripheral nerves of the upper limb. The axillary and C6 join together to form the upper trunk, the root of C7 radial nerves originate from the posterior cord, the continues as the middle trunk, and, in the lower neck, musculocutaneous and part of the median nerve arise the roots of C8 and T1 form the lower trunk of the from the lateral cord, whereas the other contributions of brachial plexus. More distally, in the supraclavicular fibers to the median nerve and the ulnar nerve originate region, each trunk gives off two divisional branches, from the medial cord. named anterior and posterior divisions, which innervate Clinically relevant spaces along the course of the flexor and extensor muscles of the upper extremity, brachial plexus nerves are (1) the interscalene triangle, respectively. In the axilla, these divisions join in various (2) the costoclavicular space, and (3) the retropectoralis combinations to form the cords of the brachial plexus. minor space (subcoracoid tunnel).12 The interscalene The lateral cord is formed by the anterior division of the triangle is bordered by the anterior and middle scalene upper and middle trunks, the medial cord by the anterior muscles on each side and the first rib inferiorly division of the lower trunk, and the posterior cord by the (Figs. 2A, B). The subclavian artery travels through posterior divisions of all the trunks. Distal to the the lower part of this space, and the lower trunk of the Downloaded by: Rutgers University. Copyrighted material.

Figure 2 Brachial plexus anatomy: interscalene triangle. (A) Schematic drawing illustrates the trunks as they exit the interscalene space, a passageway delimited by the anterior scalene (AS), the middle scalene (MS), and the first rib. The trunks are located superior to the subclavian artery (white arrow). Note the phrenic nerve (arrowhead) as it winds through the anterior scalene muscle. The posterior scalene muscle (PS) is also demonstrated in close proximity to the middle scalene. Black arrow, subclavian vein. (B) Cadaveric view shows the brachial plexus trunks passing through the interscalene triangle. The phrenic (arrowheads) and the suprascapular nerves are demonstrated in relationship to the nerve trunks. (C) Sagittal turbo spin-echo T1- weighted image of the interscalene space reveals the roots from C5 through T1 as aligned hypoechoic dots passing deep to the anterior scalene muscle and posterior to the subclavian artery (SA). (D) Oblique transverse ultrasound image demonstrates the brachial plexus nerves as hypoechoic dots embedded in the hyperechoic fatty space lying between the scalene muscles. The more external the nerve bundles, the higher the level of the plexus. SCM, sternocleidomastoid muscle. 526 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

plexus crosses the inferior part of the triangle behind rib, structural changes in the subclavius muscle, change the subclavian artery. This space may be responsible for in shoulder position, and trauma.12,13 Crossing down upper extremity neurovascular compression. A narrow the clavicle, the nerve cords enter the retropectoralis triangle may often be due to anatomical variants of minor space (Figs. 4A, B). During upper limb eleva- size, shape, and attachment of the scalene muscles on tion, the cords may lean tightly against the posterior the first rib, and they can cause a scissoring effect on side of the pectoralis minor, which may be predispos- the plexus nerves and the vessels.12,13 Distal to the ing to compression, especially in short, stocky muscular interscalene triangle, the costoclavicular space is a young men, leading to numbness and tingling in the triangular space bounded anteriorly by the inner half hands and weakness in the arms during hyperabduc- of the clavicle, underlying the subclavius muscle and tion. The most common anatomical variants of bra- the costoclavicular ligament, and posteromedially by chial plexus nerves are the passage of the C5 root the first rib and insertion of the anterior and the completely in front of (3%) or piercing (13%) the middle scalene muscles (Figs. 3A, B). In this space, anterior scalene muscle and the course of the C8 and neurovascular compression may occur as a result of T1 roots behind the middle scalene muscle rather than congenital or acquired changes in the clavicle and first passing anterior to it.14,15 Downloaded by: Rutgers University. Copyrighted material.

Figure 3 Brachial plexus anatomy: costoclavicular space. (A) Schematic drawing illustrates the relevant anatomical structures of the costoclavicular space, a rectangular passageway delimited by the clavicle (1) and the first rib (2). Note the insertion of the anterior (4) and middle (3) scalene muscles on the first rib, the transversely oriented subclavius muscle (5), and, in a more medial position, the costoclavicular ligament (6), also known as the rhomboid ligament. The fascicles of the different nerve cords (arrow) and the subclavian artery (A) cross this space passing between the scalene muscles and underneath the subclavius. The subclavian vein (V) runs more anteriorly. (B) Cadaveric slice in the short axis of the costoclavicular space with (C), corresponding T1-weighted turbo spin-echo magnetic resonance image demonstrates the nerve cords (arrows), the subclavian artery (A) and vein (V) between the clavicle and the first rib. Note the subclavius (5) and the pectoralis major (PMj). BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 527

Figure 4 Brachial plexus anatomy: retropectoralis minor space and axillary region. (A) Schematic drawing with (B), anatomic correlation, illustrates the arrangement of the lateral (LC), medial (MC), and posterior (PC) cords of the plexus relative to the axillary artery (A), the coracobrachialis (CoB), and the pectoralis minor (Pmin) muscle. Note the origin of the axillary, musculocutaneous, radial, medial (MN), and ulnar (UN) nerves. (C) Oblique sagittal T1-weighted turbo spin-echo magnetic resonance image of the retropectoralis minor space. Deep to the pectoralis major (PMj) and minor (Pmin) muscles, the position

of the LC, MC, and PC cords of the plexus relative to the axillary artery (A) and vein (V) is shown. (D) Corresponding ultrasound Downloaded by: Rutgers University. Copyrighted material. image depicts the hypoechoic fascicles of the different nerve cords distributed around the axillary artery.

MAGNETIC RESONANCE IMAGING contraindications to MR imaging or whenever MR TECHNIQUE imaging provides insufficient preoperative data.1 MR imaging of the brachial plexus is best performed by Compared with CT myelography, MR myelog- using a multielement phased-array radiofrequency re- raphy is noninvasive, does not use ionizing radiation, and ceiver coil to span the neck-to-shoulder area with the is superior to depict pseudomeningoceles because some aim of imaging either the right or the left plexus at high of them do not communicate with the dural sac and spatial resolution, rather than a bilateral examination cannot be filled in with contrast medium.6 For the with lower resolution.16 For imaging the preganglionic examination of the postganglionic plexus, a comprehen- segment of brachial plexus nerves, gadolinium (Gd)- sive MR imaging examination should extend from the enhanced MR imaging and three-dimensional (3D) cervical spine to the cords in the axilla, just distal to the heavily T2-weighted MR imaging with fat- and flow pectoralis minor muscle16 (Fig. 5). At field strengths suppression (MR myelography) are the most valuable from 1T to 3T, the brachial plexus can be evaluated techniques for identifying root avulsions and pseudome- based on its appearance on T1- and T2-weighted images ningoceles.17 Concerning the rootlets, the ganglionic with flow compensation. area and initial segment of the roots, MR myelography Concerning sequence protocols, standard 2D has become the reference modality in the last few years, turbo spin-echo (TSE) sequences are valuable to gen- limiting the use of CT myelography to patients with erate images with T1 contrast. These images display 528 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

On T2-weighted images, obliquely oriented saturation bands over the heart and thoracic aorta may contribute to further improve MR image quality by arterial flow saturation. 3D acquisitions have recently been imple- mented to image the plexus, including CISS 3D, true fast imaging with steady-state precession 3D, and 3D STIR sequences.19–22 As technology advances, these sequences and new ones in progress are increasingly gaining ground to provide a more flexible delineation of the out-of-plane course of brachial plexus nerves. The image data set of these sequences, with <1 mm isotropic resolution, can be reformatted in any plane, regardless of the prescribed plane during the image acquisition, thus allowing visual- ization of long nerve segments in a single image and giving better depiction of diffuse pathological processes affecting them. In specific clinical settings (e.g., sus- pected tumors, radiation injury, neuritis, or after regional surgery), Gd-enhanced fat-suppressed TSE T1- Figure 5 Normal brachial plexus. Coronal T1-weighted 18,23 turbo spin-echo magnetic resonance image of a normal weighted sequences can be used. brachial plexus (outlined arrows) using a wide field of view Diffusion tensor imaging (DTI) with tractogra- and phased array coil. The numbers indicate the approximate phy has recently been proven to provide indirect 3D sagittal locations for the roots (1), trunks (2), divisions (3), images of nerves.24 However, the application of DTI to cords (4), and peripheral nerves (5). The divisions and cords get reproducible tracking of brachial plexus fibers ap- run alongside the subclavian/axillary artery (a). pears to be technically challenging due to the small size of nerves, the changing orientation of the fibers, the nerves as linear low signal intensity structures outlined peculiar location of the plexus between the neck and the by surrounding fat and allow assessment of their rela- shoulder, where relevant geometric distortion and arti- tionship with relevant regional structures, including fact may occur, as well as the intrinsic low signal-to- bones, muscles, and blood vessels18 (Figs. 2C, 3C, 4C, noise ratio of echo-planar imaging technique.24 In addi- and 5). Fluid-sensitive sequences with T2 contrast tion, current reconstruction algorithms are time con- including fat-suppressed T2-weighted TSE or short suming and have poor reproducibility. tau inversion recovery (STIR) sequences are then ob- Concerning image parameters, an in-plane reso- tained to detect pathological changes within plexus lution of 2 mm2 with 3-mm slice thickness provides components. Although STIR sequences are able to sufficient signal-to-noise ratio for brachial plexus trac- give more uniform and consistent suppression of fat tography. In perspective, DTI is the only method that can

signal across the field of view (FOV), they have lower offer an indirect view of the nerve microstructure in Downloaded by: Rutgers University. Copyrighted material. signal-to-noise ratio, are more sensitive to blood flow addition to the information on fibers trajectory. With artifacts, and allow acquisition of a lower number of DTI, nerves are depicted because water diffusion pref- slices rather than TSE T2-weighted sequences.18 On erably follows the long axis of the fibers and is restricted fat-suppressed TSE T2-weighted images, shimming of transversely (inherent anisotropic diffusion). Similar to the magnetic field over the volume encompassing the other nerves, the representation of brachial plexus nerves region of interest may be helpful to reduce areas of with this technique reflects lines of fast water diffusion incomplete suppression of fat signal or with water that probably give a representation of the axonal archi- saturation rather than fat saturation. Placing a bag tecture and transport25 (Fig. 6). Tractography is a prom- containing clay suspensions against the ipsilateral neck ising method to visualize the 3D course of brachial plexus and suprascapular region has also been proposed to nerves and provide important information about the site reduce magnetic susceptibility effects. MR imaging of swelling and loss of water due to nerve abnormalities or typically includes true coronal planes over the neck-to- entrapment.26 Further experience is needed, however, to shoulder area using a wide FOV and double oblique solve technical challenges and evaluate the ultimate role (oblique-sagittal oblique-coronal) planes oriented in the of this technique for brachial plexus imaging. true short-axis of brachial plexus nerves.11 These latter planes are acquired with a smaller FOV. Instead of true sagittal images, double oblique planes can better approx- ULTRASOUND SCANNING TECHNIQUE imate the real cross-section of brachial plexus fascicles, US has recently proved to be an effective means to offering a better display of subtle nerve abnormalities. depict normal brachial plexus anatomy at several levels, BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 529

be systematic and should reveal the C7 vertebra as the first landmark. The C7 root is detected on the same plane of the C7 vertebra because it is bordered by the posterior tubercle only. Given that, the probe may move either up or down on axial planes depending on the root the examiner wants to image.31 Shifting the probe upward, the C6 vertebra is recognized due to the presence of prominent anterior and posterior tubercles: The C6 root appears as a hypoechoic structure held in between them. The transverse processes of C5 have basically the same shape of C6 and can be identified as the successive step cranial to the C6 level by taking into account the number of transverse processes encountered while sweeping the transducer cranially from C7. As a rule, the higher the level, the closer the space intervening between the tubercles. Shifting the probe downward from C7, the lateral aspect of the T1 vertebra appears flat without any tubercle; at this level, the C8 root can be appreciated while exiting the foramen. More caudally, visualization of the T1 root is unfeasible with US due to aproblemofaccessrelatedtoatoodeeplocationofthe intervertebral foramen between the T1 and T2 vertebra and the interposition of the first rib. In the paravertebral area, coronal planes are able to depict the nerve roots using the same scanning planes for the study of vertebral vessels. On these planes, the picture of vertebral vessels is obscured at regular intervals by the acoustic shadowing Figure 6 New magnetic resonance imaging techniques. from the anterior tubercles of the transverse processes. (A) Coronal reformatted diffusion-weighted image shows Moving the transducer slightly on the back, the vessels nerves of the brachial plexus. On either side, the nerve roots disappear and the roots appear as curved elongated (arrowheads) are depicted as individual structures. Dorsal ganglia (arrow) are also seen as a series of paraforaminal hypoechoic images exiting the neural foramina and nodular swellings. (B) Coronal view of the spine and brachial descending the lateral neck spaces. At the level of the plexus nerves imaged with diffusion tensor imaging tracto- interscalene triangle, the roots appear as aligned hypo- graphy in a volunteer showing the three-dimensional course echoic dots passing between the anterior and middle of the brachial plexus nerves from the C5 through C8 level. scalene muscles (Fig. 2D). In this space, the most superficial fascicles belong to C5 and the deepest to C8.

The ability of US to recognize the exact level of Downloaded by: Rutgers University. Copyrighted material. including the paravertebral area, the interscalene tri- the roots in the paravertebral area also leads to a con- angle, the supraclavicular region, and the retropector- fident identification of the trunks by simply following alis minor space.11,27–32 The US examination of the nerve bundles from where they arise. Between the brachial plexus nerves is based on detection of some interscalene triangle and the costoclavicular space, the anatomical landmarks in the neck, including bones divisions and the initial part of the cords are visualized as (roots), muscles (trunks), and vessels (divisions and aclusterofhypoechoicroundedimages,mostofwhich cords). As the roots exit the neural foramina, they slide running alongside the posterior aspect of the subclavian between two apophyses of the transverse processes of artery, just over the first rib and the apical pleura. The the cervical vertebrae, the anterior and posterior tu- dorsal scapular artery, a small vessel arising from the bercles (Fig. 7). Each root emerges from the foramen as subclavian artery, may be seen encroaching the nerve amonofascicularhypoechoicstructure,anappearance divisions and cords in the supraclavicular region. This quite different from that of nerves in the extremities vessel may pass posterior to or among the fascicles, in that is made of clusters of hypoechoic fascicles.27,31 this latter case forming a cleavage plane that is frequently Imaging based on scanning planes is ideal to located between the middle and the lower plexus com- depict the relationship of the roots with the transverse ponents. More distally, the costoclavicular space is blind processes at any given level. Based on the peculiar to US examination due to the interposition of the appearance of the transverse process of C7, in which clavicle and the lack of an acoustic window. The inability the posterior tubercle is absent, US is able to establish to image this important space represents one of the main the level of nerve roots.31 The scanning technique must limitations of a US approach. Crossing down the 530 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

Figure 7 Normal brachial plexus. (A) Transverse ultrasound image over the left anterolateral neck demonstrates the main landmarks for identification of the nerve roots. Note the position of the left lobe of the thyroid (Thy) and the common carotid artery (CA) located between the superficial sternocleidomastoid (scm) and the deep longus colli (lc) muscles. Deep to these structures, the lateral aspect of the C6 vertebra shows a wavy hyperechoic contour that delineates the vertebral body (1), the pedicle (2), and the transverse process (3), which exhibits in turn two prominent anterior (4) and posterior (5) tubercles. The C6 root (arrow) appears as a hypoechoic image lying in between these tubercles. (B) Cadaveric slice shows the relevant anatomical structures depicted in (A) including the common carotid artery, the longus colli muscle, and the transverse process of the C6 vertebra, characterized by anterior and posterior tubercles. Note the nerve root (arrow) located in between the tubercles, the superficial internal jugular vein (IJV) and the vertebral artery (VA) in a deeper position.

clavicle, in the retropectoralis minor space, the nerve young.1,33 After traffic accidents, the second most com- cords continue their course around the axillary artery.11 mon cause is obstetric trauma that may occur from The fascicles belonging to the posterior cord course mechanical injury involving shoulder dystocia during behind the artery; the lateral cord runs external and the difficult childbirth.34 Brachial plexus injuries are typi- medial cord internal to it (Fig. 4D). On short-axis cally related to a violent excessive nerve stretching as it planes, the axillary artery is the main landmark to occurs during simultaneous traction of the arm and identify the nerves in this area. This arrangement is throwing of the head to the opposite shoulder.33 De- maintained across these spaces like a ‘‘three-point’’ star pending on trauma characteristics, brachial plexus le- with the artery centered in the middle. sions can be divided into complete (when C5 through T1 Finally, the examination of the most distal part of components are involved) and incomplete injuries.

brachial plexus nerves is completed using an axillary Incomplete injuries can be further subdivided into Downloaded by: Rutgers University. Copyrighted material. approach as these nerves assume a deeper course. Espe- two types: upper and lower brachial plexus lesions. cially in overweight people or patients with hypertro- Upper lesions involve damage of C5 and C6 roots and phied regional musculature, the nerves in the axillary lead to Erb’s palsy, producing the so-called waiter’s tip area may be too deep and undefined using an anterior deformity, due to loss of the external rotators of the approach. With an axillary approach, nerves appear more shoulder (suprascapular, axillary), arm flexors (musculo- superficial in this area and can be accurately evaluated. cutaneous), and hand extensors (radial); lower lesions US scanning should first start at the proximal arm to involve C8 and T1 either before or after they have joined identify the median, ulnar, and radial nerves as they to form the lower trunk. This latter condition, known as surround the brachial artery. Then the probe is swept up Klumpke’s palsy, is less frequent and mainly affects the along the short axis of the nerves to reach the distal part intrinsic muscles of the hand and the flexors of the wrist of the cords. and fingers (ulnar, median). An early assessment of the extent and severity of the injury is essential for deciding treatment strategies.1,4 TRAUMATIC PLEXOPATHIES Several types of injury may occur at the brachial Closed brachial plexus injuries are relatively infrequent, plexus level, including nerve stretching (neurapraxia), affecting 1% of all multitrauma patients and approach- the most common and least severe form, rootlets avul-  ing 5% in high-velocity motor vehicle accidents, primar- sion (preganglionic separation from the spinal cord), ily motorcycle accidents, but result in debilitating pseudomeningocele (tear in the meningeal sheath consequences in a patient group that is relatively around the nerve roots with leakage of cerebrospinal BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 531

fluid), and postganglionic injury (discontinuity of the The first task of imaging is distinguishing intra- brachial plexus nerves distal to the ganglion). Differ- spinal nerve root avulsion, theso-calledpreganglionic entiation between intraspinal nerve root avulsion, the injuries, from extraforaminal lesions, or postganglionic so-called preganglionic injuries, from extraforaminal injuries because the surgical treatment differs in each lesions, or postganglionic injuries is aided by electro- case.4,36 In preganglionic injuries, the lesion is intra- physiological studies based on detection of abnormalities dural and located proximal to the dorsal root ganglion. in the paraspinal muscles, and especially the multifidus, Despite some attempts to subdivide these lesions into in injuries located proximal to the brachial plexus.35 A central and peripheral, in most cases they are not substantial number of root avulsions occur, however, considered amenable to direct repair and the prognosis without denervation signs in the paraspinal muscles is unfavorable.37 Nerve transfers are usually performed due to the multisegmental level of innervation of these to restore function, using intercostal transfer to the muscles. Somatosensory evoked potentials can be used to musculocutaneous to regain elbow function or spinal diagnose intraforaminal nerve injuries, but because these accessory to suprascapular to reestablish flexion. In do not enable physicians to discriminate between in- cervical nerve root avulsion, the finding of a traumatic complete avulsions and intact roots or between intra- pseudomeningocele indicates an extradural collection foraminal root avulsion and rootlet avulsion from the of cerebrospinal fluid due to laceration of the dural spinal cord, conventional MR imaging and myelo- sleeve17 (Fig. 8). This is the main landmark that graphic techniques based on CT/MR imaging play an indicates a preganglionic injury is present, although important role in the diagnostic workup.1,4 pseudomeningocele may occur without nerve root Downloaded by: Rutgers University. Copyrighted material.

Figure 8 Pseudomeningocele. (A, B) Twenty-six-year-old man with a traumatic pseudomeningocele after a motorcycle accident. (A) Axial turbo spin-echo (TSE) T2-weighted magnetic resonance (MR) image shows the retracted right C7 nerve root (outlined arrow) and the leakage of cerebral spinal fluid (arrowheads). Note mild denervation signs (white arrow) in the right multifidus and semispinalis capitis muscles. (B) Coronal short tau inversion recovery MR image of the distal plexus reveals a wavy appearance of the retracted nerve cords (outlined arrows). (C) Transverse TSE T1-weighted MR image and (D) corresponding three-dimensional MR myelogram in a 17-year-old young man with chronic root avulsion demonstrate a prominent pseudomeningocele (outlined arrowheads) extending laterally to form a sac (asterisk) in the postscalenic area. Observe the normal contralateral root (black arrowhead, C) at the same vertebral level. 532 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

avulsion ( 15% of cases) and, conversely, avulsion may  38–40 occur without meningocele (20% of cases). Other signs of preganglionic injury include Gd enhancement of intradural roots, intramedullary edema (T2-weighted sequences), lateral displacement of the spinal cord, intracanal hematoma, and secondary dener- vation signs.4,41,42 These signs are found in 20% of 38  cases. Comparing the results of CT myelography and MR myelography, current literature reports that both imaging modalities have similar sensitivity for detecting intraspinal nerve injuries.17 After excluding preganglionic injuries, an early assessment of the extent and severity of the injury outside the spine is essential for determining treatment. In contrast to preganglionic injuries, postganglionic lesions with defects in nerve continuity can be repaired with nerve grafting that involves excision of the dam- aged segment and autograft between two nerve ends, or neurolysis to remove perineural scar and adhesions.4 If nerve fascicles are intact, spontaneous recovery is usu- ally expected. In postganglionic injuries, lesions must be further subdivided in supraclavicular and infracla- vicular based on their location.4 Preoperative electro- physiological studies are routinely performed to assess the status of brachial plexus nerves outside the spine but often yield ambiguous findings.2,43 Because patients suffering from major postganglionic nerve injuries are known to recover better if operated on early (within 3monthsafterinjury),diagnosticimagingwithUSand MR imaging has critical value for assessing the status of nerves outside the neural foramina.1,4,17,43 In patients with severe extraspinal injuries, signs of nerve disconti- nuity are most often observed (1) at the interscalene triangle, as a result of the tethering effect exerted by Figure 9 Acute brachial plexus injury in a 25-year-old the scalene muscles on the stretched nerves; and, more motorcyclist with total plexus palsy following a traffic acci- dent. The examination was performed 1 week after trauma. distally, (2) at the costoclavicular space, especially in (A) Long-axis ultrasound (US) image over the C5 (white patients with clavicular fracture when bony fragments arrowheads) and C6 (outlined arrowheads) components of Downloaded by: Rutgers University. Copyrighted material. directly impinge the underlying cords. Diagnostic the upper trunk of the right brachial plexus. Both nerves are imaging may provide an early categorization of extra- transected and exhibit a wavy course. At their end, bulbous spinal plexus pathology and define surgical candidates neuromas (asterisks) are starting to develop. (B) Three- by identifying the exact site of the injury, how many and dimensional gradient-recalled echo MR imaging acquisition which are the nerves involved, the severity of involve- with multiplanar reconstruction obtained along the axis of the ment, and the position of the retracted wavy nerve ends right roots demonstrates discontinuity (outlined arrows) of in cases of neurotmesis. C5 through C8 roots. Distal to the transection level, hetero- In the acute phase, the information provided by geneous signal in the soft tissues (asterisk) of the supracla- US seems even more detailed than the one provided by vicular area is seen. When compared with the left side, note the swollen appearance and more vertical course of the MR imaging to distinguish theinterruptednervesfrom affected right roots. the adjacent deranged soft tissue with hemorrhage and edema.43–45 However, the interpretation of imaging findings becomes more accurate and informative after levels, US and MR imaging can assess the relationship afewweekswhenhematomasorareasofsubcutaneous of fibrotic areas with brachial plexus nerves. When the emphysema are reabsorbed and stump neuromas are traction injury is not strong enough to determine developing at the nerve ends (Fig. 9). In chronic complete interruption of nervebundles,segmentalfusi- injuries, fibrous scar arising from damaged fascicles form thickening of the involved nerves reflecting a may also be seen encasing normal fascicles and causing spindle neuroma may occur as a result of traction late worsening of symptoms (Fig. 10). At the different trauma (Fig. 11). Spindle traction neuromas usually BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 533

Figure 11 Brachial plexus injury in a 25-year-old man following a motorcycle accident. (A) Long-axis ultrasound image of the C5 (outlined arrowheads) and C6 (white arrow- heads) roots in the paravertebral region reveals nerve ab- normalities related to a stretching injury (axonotmesis). Both nerve roots are continuous but have wavy and irregular contours and less defined fascicular echotexture. (B) Normal contralateral side for comparison. Figure 10 Chronic brachial plexus injury in a 47-year-old man with median nerve palsy following a closed trauma 1yearbefore.Inthelast3months,thepatientpresented For the diagnostic workup, a combined approach progressive worsening of pain and neurogenic symptoms in with MR imaging and US can be used to evaluate the the territory of ulnar nerve distribution. (A) Oblique sagittal traumatized patient, the first technique to evaluate the turbo spin-echo T2-weighted magnetic resonance image of spine and the foraminal region, the second to assess the supraclavicular space demonstrates swollen hyperin- 43 tense cords of the plexus (white arrowhead) grouped to- the nerves outside the spine. Detection of extraspinal gether and encased by a peripheral fibrous scar (arrows). nerve abnormalities with US may have important clinical Downloaded by: Rutgers University. Copyrighted material. Outlined arrowhead, subclavian vessels. (B) Corresponding implications. It may give an early assessment of the status short-axis ultrasound image confirms the presence of scar of the plexus in the immediate phases after the trauma tissue (arrows) derived from a previous nerve injury. Within when clinical findings are not yet conclusive on whether the scar, intact hyperechoic fascicles (arrowheads) with abrachialplexusdamagewillrequiresurgery.USseems preserved fascicular echotexture are seen. Cl, clavicle; sa, to be particularly effective in patients with supraclavic- subclavian artery. ular postganglionic injuries, a difficult-to-explore area with MR imaging. develop at the interscalene triangle and in the space intervening between it and the costoclavicular space. Depending on the severity of traction injury, a faint NEUROGENIC THORACIC OUTLET fascicular pattern with swollen fascicles can be still SYNDROME visible within the neuroma orahomogeneousfusiform Thoracic outlet syndrome is a range of disorders arising hypoechoic mass is found in continuity with the from the passage of the subclavian artery and vein and nerve.46 In injuries associated with clavicle fracture, brachial plexus nerves through the three anatomical the involvement of the nerve cords typically occur at the spaces of the thoracic outlet: the interscalene triangle, costoclavicular space (Fig. 12). Following open surgery the costoclavicular space, and the retropectoralis minor around the shoulder or glenohumeral joint dislocation, space, the narrowing of which can variably lead to the involvement of the nerve cords is found more arterial, venous, or nervous compression.12,38,47,48 A distally, at the level of the retropectoralis minor space. pure neurogenic syndrome is disputed in the literature 534 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

Figure 12 Brachial plexus injury in a 51-year-old woman who had a right clavicular fracture following a car accident and subsequent motor and sensory disturbances in the territory of radial nerve distribution. (A) Radiograph shows right clavicular fracture with detachment of some pointed fragments (arrowheads). (B, C) Short-axis ultrasound (US) image of the supraclavicular space obtained in (B) neutral position and (C) during external rotation of the right arm. In (B), US demonstrates the subclavian artery (sa) and some apparently normal nerve cords (arrow). In (C), the external rotation of the arm makes the posterior cord (arrowheads) visible by displacing it from underneath the clavicle. Note the swollen and hypoechoic appearance of this cord, partially damaged by the pointed fracture fragments. (D) Sagittal turbo spin-echo T1-weighted magnetic resonance (MR) image obtained at the fracture level reveals heterogeneous hypointense tissue (arrow) located deep to the clavicle and posterior to the subclavian artery (outlined arrowhead) and vein (white arrowhead). Coexisting deltoid (asterisk) injury is also depicted.

and seems to occur more frequently at the interscalene affected nerves at the costoclavicular space is exceptional triangle and the costoclavicular space rather than at the with MR imaging. level of the retropectoralis minor space.47,49 In many Some authors found good correlation between

cases, the nerve involvement is not isolated but associ- distortion of brachial plexus nerves seen on MR imaging Downloaded by: Rutgers University. Copyrighted material. ated with arterial disease, as a possible result of common and clinical symptoms.50 Using multiplanar reformatting neurovascular compression and/or arterial disease caus- of 3D gradient-recalled echo MR acquisitions or volu- ing secondary disturbances in the intranervous micro- metric CT scan with planes reconstructed in the short vasculature.12 axis of the interscalene and costoclavicular spaces, imag- The clinical diagnosis is difficult because symp- ing is able to directly measure the size of these spaces toms are vague and nonspecific. In upper plexus involve- with the arm alongside the body or during a postural ment, pain typically radiates in the ipsilateral neck up to maneuver, such as holding the arm 130 degrees abducted the occipital region, and it may involve the rhomboid and rotated externally (Wright’s test).51,52 Patients with area, the upper pectoralis area, and the deltoid and thoracic outlet syndrome showed a significantly smaller trapezius down to the external aspect of the arm. Lower costoclavicular distance and a wider retropectoralis mi- plexus pain distributes around the shoulder and radiates nor space after arm abduction (Fig. 13A). In addition, down the medial arm and the medial forearm, with an they exhibited a thicker subclavius muscle at rest and ulnar nerve distribution.12,49 Detection of nerve com- during postural maneuver than did normal volunteers.51 pression is very difficult to detect with imaging modal- MR imaging may occasionally depict fibrous bands ities both in its isolated form or in association with causing nerve distortion.50 Ahypertrophiedanterior vascular disease. In fact, US is unable to evaluate nerve scalene muscle, possibly accompanied by or fused with changes about the costoclavicular space due to problems ahypertrophiedmiddlescalenecompressingtheplexus of access of the US beam. Similarly, direct visualization against the first rib (scalenus anticus syndrome), can also of focal swelling and signal intensity changes in the be depicted on MR imaging and multislice CT.16,53 In BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 535

Figure 13 Thoracic outlet syndrome in a 24-year-old woman with neurovascular symptoms. (A) Sagittal turbo spin-echo (TSE) T1-weighted image of the costoclavicular space obtained in the short axis with arm hyperabduction reveals a reduced distance between the clavicle (1) and the first rib (2) with compacted neurovascular structures (outlined arrow). a, subclavian artery. (B) Magnetic resonance angiography image obtained with maximum-intensity projection reconstruction algorithm while keeping the patient’s arm hyperabducted demonstrates flow signal in the right brachiocephalic vein (outlined arrow) but not in the right subclavian (arrowheads). some instances, compression may be related to the severe shoulder burning pain followed shortly by pro- anomalous insertion of the middle scalene into almost found muscle weakness and flaccid paralysis of at least the entire length of the first rib, thus overlapping the one of the shoulder girdle muscles.57 Typically, there is anterior scalene and creating a very narrow window for no loss of sensation associated with the weakness. This the neurovascular bundle.12 In this compression, the uncommon but not rare disorder (incidence rate: Adson’s test is positive when the patient’s head is turned 1.64 105 people) has a peak incidence between the  outward. Finally, care should be taken not to miss a 3rd and the 5th decades and male predominance (male- cervical rib or an elongated transverse process of the C7 to-female ratio ranges from 2:1 to 11.5:1), is often vertebra. Both structures are often associated with fi- bilateral (a third of cases), and may mimic other more brous bands.7,12,54 For this purpose, a plain film should common pathological conditions (e.g., cervical radicul- be always obtained before other imaging studies. opathy, shoulder impingement syndrome, nerve entrap- Supernumerary cervical ribs account for 0.5 to ment due to local mass effect, and rotator cuff tear).58  0.6% of normal people, and in more than half of the cases Although different factors, including viral infec- they are bilateral. Conventionally, cervical ribs can be tion, trauma, surgery, and autoimmunity have been Downloaded by: Rutgers University. Copyrighted material. grouped into four types: type I, <2.5 cm in length; type implicated to play a causative role, the precise etiology II, >2.5 cm with free tip; type III, full-size cervical rib of Parsonage-Turner syndrome still remains controver- with fibrous connection to the first rib; and type IV, full- sial.58 Electrodiagnostic studies may demonstrate size cervical rib with a chondral attachment to the first changes related to acute denervation in the brachial rib.55 Depending on the rib size, symptoms are present plexus distribution, especially in the C5 and C6 terri- along the C7-T1 distribution with a positive Adson’s tory.59 The suprascapular nerve (supplying the supra- test when the patient’s head is rotated inward. In these spinatus and the infraspinatus) is the most commonly patients, dynamic US may reveal a tight contact and involved. Among other nerves of the shoulder girdle, the impingement of the nerve divisions with the tip of the axillary (deltoid and teres minor), long thoracic (serratus cervical rib while performing the postural maneuver anterior), and musculocutaneous (coracobrachialis, bi- (Fig. 14). US has proved to be a useful tool to demon- ceps brachii and brachialis) may be affected individually strate cervical ribs in children, thus avoiding ionizing or in combination. Imaging studies may help confirm the radiation.56 diagnosis.59–61 Although US is able to suggest denervation by showing loss in bulk and hyperechoic appearance of the PARSONAGE-TURNER SYNDROME affected muscles in the absence of tendon tears, MR Parsonage-Turner syndrome, also known as ‘‘acute bra- imaging seems more reliable and gives a comprehensive chial plexus neuritis’’ or ‘‘neuralgic amyotrophy,’’ is a self- view of the complex pattern of muscle involvement that limiting clinical entity consisting of a sudden onset of characterizes the Parsonage-Turner syndrome. It may 536 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

Figure 14 Thoracic outlet syndrome in a 66-year-old woman with a cervical rib and sensory disturbances in the area of the median nerve. (A) Schematic drawing simulates the position of a type 4 supernumerary rib (arrows). Note the interscalene triangle delimited by the anterior scalene muscle (1), the middle scalene muscle (2), and the first rib (5). The distal tip (black arrow) of the cervical rib protrudes within the triangle thus narrowing its space and possibly impinging the nerve roots (arrowhead). Other relevant regional structures are the posterior scalene (3), the clavicle (4), and the second rib (6). C7 and T1 indicate the vertebral levels. (B) Plain film demonstrates the supernumerary rib (white arrow) joining a prominent accessory process (outlined arrow) of the first rib by a synchondrosis (outlined arrowhead). (C) Cranial and (D) caudal short-axis ultrasound images obtained over the supernumerary rib (asterisk) demonstrate the C7 root (arrow) snapping over the bone.

47 also rule out cervical radiculopathy. Early MR imaging tumors. Concerning metastatic disease, a wide variety Downloaded by: Rutgers University. Copyrighted material. studies demonstrate intramuscular increased T2 signal of histotypes have been reported to involve the brachial intensity as a possible result of the increased extracellular plexus secondarily. Among them, breast cancer is more water content and/or increased intramuscular capillary common by far, accounting for approximately <1to blood volume that occur during partial denervation60,61 1.8% of patients because one of the most relevant (Fig. 15). Later on, intramuscular fatty infiltration and lymphatic drainage paths of the breast passes through decrease in muscle bulk can be observed. In most the axillary region.62 The onset of metastatic plexus instances, brachial plexus nerves retain normal size, disease varies widely with a mean of 5.5 years. MR appearance, and signal intensity. Focal areas of increased imaging demonstrates metastases as definite space-oc- Gd enhancement and higher T2 signal intensity may cupying lesions along the course of brachial plexus seldom be seen in the nerves supplying denervated nerves, characterized by low intensity signal on muscles as a nonspecific sign of inflammation (neuritis). T1-weighted images, increased signal intensity (higher Prognosis is generally benign, with 75% recovery than that of muscle) on T2-weighted images and Gd  54 within 2 years, and treatment is symptomatic (analgesic enhancement; however, the signal intensity may vary drug and physical therapy). (Fig. 16). Pleural and vertebral involvement can be also assessed with this technique. US may reveal a well- defined solid mass with irregular margins and hypoechoic TUMORS AND POSTRADIATION IMAGING echotexture encasing nerves with an abrupt nerve- Brachial plexus tumors include two main classes of to-tumor interface.44 Alternatively, the neoplasm may disorder: metastatic disease and neurogenic primary cause segmental thickening and hypoechoic appearance BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 537

Figure 15 Parsonage-Turner syndrome in a 40-year-old patient. (A) Photograph from above shows obvious atrophy of the right supraspinatus (1) and infraspinatus (2) muscles and winged scapula (curved arrow). The patient also had weakness of the trapezius. (B, C) Corresponding axial fat-suppressed turbo spin-echo (TSE) T2-weighted magnetic resonance (MR) images reveal reduced volume and hyperintense appearance of the supraspinatus (outlined arrows) and the infraspinatus (outlined Downloaded by: Rutgers University. Copyrighted material. arrowheads). (D) Oblique sagittal short tau inversion recovery MR image shows hyperintense appearance of the trapezius, supraspinatus (SS), infraspinatus (IS) relative to the subscapularis (SubS) and the teres minor (Tm). of the involved nerves without causing a clear mass the presenting symptom in 98% of patients with meta- effect.44 Satellite lymph nodes are often associated. static plexopathy.62,63 Based on location, the upper plexus Distinguishing between metastatic plexopathy and (C5-C6) seems more frequently involved in radiation radiation injury is critical to determine both prognosis and injury, the lower trunk (C8-T1) in metastatic disease.62 treatment, but the distinction is not easy to make, and Horner’s syndrome is also more likely found in metastatic both electrophysiology and imaging studies have met with plexopathy rather than in radiation disease. In radiation limited success.7 The incidence of radiation-induced plexopathy, MR imaging reveals diffuse thickening of the brachial plexopathy is significantly higher when the axil- involved nerves without a focal mass and soft tissue lary dose of radiation therapy is >60 Gy.62 The dose changes with low signal intensity on both T1- and T2- alone, however, does not determine whether a given weighted sequences.16,47,64 Gd does not help differentiate patient will develop radiation damage: the treatment between tumor and radiation fibrosis because both con- technique and the concomitant use of chemotherapy ditions show some degree of enhancement.54 US demon- seem also to play a role. Sensory symptoms, such as strates diffuse thickening of nerve fascicles in the absence numbness and paresthesias (55%) along with swelling of a focal mass. Different from neoplastic infiltration, the and weakness of the arm (45%), are the initial symptoms nerve thickening is more uniform, and some faint fasci- in patients with radiation plexopathy. In contrast, pain is cular pattern is preserved in radiation fibrosis.44 However, 538 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

Figure 16 Brachial plexus metastasis from breast cancer in a 65-year-old woman. (A) Oblique sagittal turbo spin-echo (TSE) T1-weighted and (B) fat-suppressed TSE T2-weighted magnetic resonance images of the infraclavicular region show an infiltrating mass (white arrows) encasing the subclavian artery (arrowhead) and brachial plexus nerves (outlined arrow). (C) Long-axis ultrasound image demonstrates markedly swollen and hypoechoic appearance of the nerve cords (arrows) as a result of the infiltrative spreading of cancer. Some nerve fascicles (arrowheads) are preserved and retain a normal appearance. Asterisk, subclavius muscle; cl, clavicle. Downloaded by: Rutgers University. Copyrighted material.

this finding is far from being specific to the diagnosis, and often, vertebral body involvement. 3D MR imaging and such a differentiation remains problematic with both multislice CT have markedly improved the visualization modalities. 18F-fluorodeoxyglucose positron emission to- of this tumor and its relationship with brachial plexus mography (FDG-PET) and 18FDG-CT-PET have been nerves and the subclavian vessels. Primary neurogenic used for this purpose.65,66 The results seem promising, tumors of the brachial plexus, including neurofibromas particularly if other imaging studies are indeterminate and schwannomas, are far less common than metastatic despite clear clinical evidence of brachial plexopathy and disorders. The MR imaging and US characteristics of for depicting metastases outside the axilla.16,65,66 these tumors are equal to those already described in other Among other malignant histotypes, Pancoast’s locations47 (Fig. 17). The feature of value in distinguish- tumor (superior sulcus tumor) characteristically presents ing these tumors from other soft tissue masses—and with a syndrome of pain around the shoulder and in the especially from enlarged supraclavicular lymph nodes— arm derived from involvement of the C8, T1, and T2 is demonstration of the continuity between the tumor root distribution.54 The main features associated with and the nerve of origin. this syndrome are Horner’s syndrome (i.e., ptosis of the upper eyelid, miosis, anhydrosis, enophthalmos, and loss of ciliospinal reflex), muscle atrophy in the territory of NERVES AROUND THE SHOULDER ulnar nerve distribution, radiographic detection of an In some clinical settings, other neuropathies around the opacity at the lung apex with first rib destruction, and, shoulder may be added to the differential diagnosis list BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 539

Figure 17 Schwannoma of the brachial plexus. (A) Short-axis ultrasound (US) image over the brachial plexus in a patient presenting with a palpable mass in the supraclavicular region. Note a solid hypoechoic mass (asterisk) located posterior to the axillary artery (ax). The mass is surrounded by intact nerve fascicles (arrowheads) and, on long-axis planes (not shown), was in continuity with one of them. (B) Correlative turbo spin-echo (TSE) T1-weighted and (C) fat-suppressed TSE T2-weighted images show the mass (asterisk) in close relationship with the axillary artery (arrow). for a suspected brachial plexus disorder. A brief focus on ities, even relatively small space-occupying lesions like these frequently missed conditions affecting the supra- paralabral ganglion cysts, and brachial plexus disorders scapular, axillary, long thoracic, and spinal accessory (Parsonage-Turner syndrome) have been reported as nerves is therefore needed to remind the radiologist of potential causes of suprascapular neuropathy.9 Regard- these problems when evaluating patients with suspected less of the cause, if the nerve is entrapped at the brachial plexus pathology that does not fit typical diag- supraspinous notch, the supraspinatus and the infra- noses. spinatus muscles undergo denervation changes. By contrast, if the nerve is compressed more distally, at the spinoglenoid notch, denervation is limited to the Suprascapular Neuropathy infraspinatus or part of it, whereas the supraspinatus From an anatomical point of view, the suprascapular is a remains spared. Symptoms are insidious at onset unless purely motor nerve that takes its origin from the upper there is a history of acute trauma and may mimic trunk (C5 and C6) of the plexus.9 It descends the neck glenohumeral instability. Late in the process, wasting with an oblique lateral course passing beneath the or atrophy of the involved muscles become more easily trapezius and the omohyoideus and enters the supra- manifest. In many instances, however, the patient does spinous fossa through the suprascapular notch not complain of weakness because of compensation of (Fig. 18A). This notch has variable shape and is roofed the posterior deltoid and teres minor. by the transverse scapular ligament. After crossing this The diagnosis of suprascapular neuropathy is Downloaded by: Rutgers University. Copyrighted material. ligament, the suprascapular nerve gives off motor essentially based on a careful and thorough history and branches to the supraspinatus muscle. The nerve then physical examination. Neurophysiology, including travels obliquely along the floor of the supraspinous EMG and nerve conduction studies, may help confirm fossa, deep to the supraspinatus, until 2cmfromthe the diagnosis, but there are false negatives and it may not  glenoid rim, and curves around the lateral margin of the always define the nature of the abnormal findings and base of the scapular spine, an area also referred to as the localize the site of compression.67 Imaging may be useful spinoglenoid notch, to enter the infraspinous fossa9 to evaluate patients with suprascapular neuropathy, es- (Fig. 18A). At the spinoglenoid notch, the nerve may pecially to determine the presence of paralabral cysts be roofed by the inferior transverse scapular ligament. compressing the nerve and to assess the rotator cuff Along its course, the suprascapular nerve is accompanied muscles for atrophy.68 Paralabral cysts are usually asso- by the suprascapular vessels. ciated with tears of the superior and posterior glenoid Due to its relatively fixed position combined labrum (from 8- to 11-o’clock positions), related to the with its lying under the rotator cuff muscles, the supra- passage of joint fluid into the cyst through a thin scapular nerve is particularly susceptible to compres- pedicle.61,69,70 During their growth, paralabral cysts sion. The suprascapular notch and the spinoglenoid may spread into the spinoglenoid notch, the suprascap- notch are the most frequent sites of nerve entrapment. ular notch, or both, possibly causing nerve entrapment Anarrowsuprascapularnotch,anabnormaltransverse and muscle denervation.69 US and MR imaging can scapular ligament, mechanical stretching of the nerve identify the cyst and recognize secondary changes of by repeated overhead activities, spinoglenoid varicos- nerve damage, including loss in bulk and echotextural/ 540 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

onset of denervation symptoms, with an average volume of the cysts causing muscle denervation significantly greater (6.0 cm3 versus 2.2 cm3 of all other paralabral cysts).69 Due to their deep location, depiction of parala- bral cysts requires a careful scanning technique with US.71 Varicose veins in the spinoglenoid notch is the main differential diagnosis. Although enlarged spino- glenoid notch veins look like a cyst because they appear as fluid-filled images, they change their shape, collapsing in internal rotation of the arm and dilating maximally in external rotation. Some relationship between spinoglenoid varicos- ities and suprascapular neuropathy has been sug- gested.61,68,72 It is unclear, however, if these two entities are separate expression of a narrow suprascapular tunnel or if the varicosities may actually lead to nerve impingement. Percutaneous needle aspiration of the cyst content can be attempted under US guidance to treat suprascapular nerve compression.73,74 For this purpose, repeated ‘‘to-and-fro’’ passage movements of the needle tip are helpful to avoid recurrence. This procedure has reported to lead to marked relief of symptoms in >86% of patients.74

Axillary Neuropathy The axillary nerve arises from the posterior cord of the brachial plexus receiving fibers from C5 and C6 levels.9 It travels below the coracoid process and then along the inferolateral border of the subscapularis to curve inferior to the glenohumeral joint and pass through the quadri- lateral space, a squared passageway bounded by the long head of the triceps medially, the surgical neck of the humerus laterally, the teres minor cranially and the teres major and latissimus dorsi caudally. After crossing this space, the axillary nerve enters the posterior aspect of the

Figure 18 Suprascapular nerve. (A) Schematic drawing shoulder and divides into two terminal branches: ante- Downloaded by: Rutgers University. Copyrighted material. illustrates the anatomy of the suprascapular nerve as seen rior and posterior. The anterior branch supplies the from the posterior aspect of the shoulder. Note the nerve anterior and middle deltoid muscle and overlying skin; (arrowheads) traveling under the transverse scapular liga- the posterior branch innervates the teres minor and the ment (1) at the supraspinous notch and then under the posterior deltoid muscle and distributes to the skin spinoglenoid ligament (2) at the spinoglenoid notch. The overlying the distal deltoid and the proximal triceps9 nerve gives off branches for the supraspinatus (a) in the (Figs. 19A, B). Along its course, the nerve is accom- supraspinous fossa and for the infraspinatus (b) in the infra- panied by the posterior circumflex artery. The axillary spinous fossa. Along its course, the nerve is accompanied by neuropathy may be secondary to stretching injures or the suprascapular artery (arrows). (B) Axial fat-suppressed extrinsic compression in the quadrilateral space caused turbo spin-echo T2-weighted magnetic resonance image of the shoulder in a 43-year-old manual worker with chronic by humeral fractures, improper use of crutches, casts, shoulder pain. A ganglion cyst (asterisk) is shown in the fibrous bands, space-occupying masses, and inferior 9,61 spinoglenoid notch causing selective denervation of the paraglenoid cysts (from the 9- to 7-o’clock positions). infraspinatus muscle (arrows). Iatrogenic nerve damage during arthroscopic procedures around the coracoid or by posterior surgical arthroscopic signal intensity changes in the innervated muscles due to portals has been reported.9 When entrapment of the edema and fatty replacement54 (Fig. 18B). The continu- axillary nerve occurs in the quadrilateral space, there is ity of the cyst with a defect in the labrum can be revealed selective denervation of the teres minor muscle because with these techniques as well. A direct correlation has the anterior branch of the nerve (supplying the deltoid) is been found between the size of paralabral cysts and the spared. BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 541

Figure 19 Axillary nerve. Schematic drawings illustrate the anatomy of the axillary nerve in relation to some relevant muscles of the shoulder girdle and the quadrilateral space as seen from (A) the anterior and (B) the posterior aspect of the shoulder. After arising from the posterior cord of the brachial plexus, the axillary nerve (arrow) traverses the inferior border of the subscapularis muscle (2) and then passes through the quadrilateral space, a narrow passageway delimited by the humerus, the teres major (3), the long head of the triceps (4), and the teres minor (5) muscles to enter the posterior aspect of the shoulder. The axillary nerve splits into an anterior branch (black arrowhead) that provides motor supply to the anterior and middle parts of the deltoid

(1), and a posterior branch (outlined arrowhead) that supplies the teres minor and the posterior part of the deltoid continuing Downloaded by: Rutgers University. Copyrighted material. down as the superior lateral cutaneous nerve of the arm. Along its course, the nerve is accompanied by the posterior circumflex artery. (C) Sagittal ultrasound image over the infraspinous fossa in a 35-year-old professional volleyball player with axillary neuropathy. Note the atrophy of the deltoid and teres minor compared with the infraspinatus. The teres minor appears hyperechoic as a result of fatty replacement. (D) Oblique sagittal short tau inversion recovery magnetic resonance image reveals intramuscular edema with increased signal intensity in the deltoid (1) and teres minor (5).

The axillary neuropathy may be discovered inci- changes of the involved muscles in the absence of a dentally during routine examination of the shoulder tendon tear (Figs. 19C, D). MR imaging is superior to because the action of the teres minor cannot be clearly US to depict any space-occupying lesion in the quadri- separated from the contribution of the infraspinatus. lateral space, such as paralabral cysts extending off the This would suggest that the disease may exist in a inferior aspect of the glenoid in association with a tear of subclinical form. When symptomatic, the axillary neuro- the inferior labrum.71,75,76 pathy presents with vague, often nonspecific, posterior shoulder pain, sensory disturbances over the external aspect of the shoulder, and weakness exacerbated by Long Thoracic Neuropathy overhead activity and heavy lifting. Even without any From an anatomical point of view, the long thoracic detectable soft tissue abnormality along the nerve course, nerve takes its origin from C5 through C7 and occa- the imaging diagnosis of axillary neuropathy is based on sionally (8%) C8.10 After traveling anteriorly to the the evidence of volume loss and echotextural/signal posterior scalene muscle, it traverses distally and laterally 542 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

to pass below the clavicle and under the first and the injury. This typically occurs in athletes (e.g., throwing second rib. More distally, the long thoracic nerve de- sports like baseball, javelin, or when spiking or serving a scends along the chest wall in the midaxillary line to the volleyball or a tennis ball) when the head is tilted and outer border of the serratus anterior, sending branches to rotated laterally away from the affected extremity and each of the digitations of this muscle10 (Fig. 20A). The the arm is raised overhead.10 Direct trauma over the serratus anterior, which forms the medial wall of the upper anterior chest and whiplash injury may also cause axilla, originates from the first through ninth ribs and nerve compression.77 Nontraumatic causes include com- inserts into the costomedial border of the scapula. It acts pression by distended bursae, such as the subcoracoid as a stabilizer of the scapula during the initial stages of bursa or the subscapularis recess. Regardless of the abduction (Fig. 20B). pathomechanism, it is still unclear where the injury Long thoracic neuropathy most often derives occurs along the course of the nerve. Physical examina- from repeated microtrauma as a result of a stretching tion reveals a distinct clinical picture with scapular Downloaded by: Rutgers University. Copyrighted material.

Figure 20 Long thoracic nerve. (A) Schematic drawing illustrates the anatomy of the long thoracic nerve. After branching off before the brachial plexus, note the long thoracic nerve (arrows) piercing the middle scalene muscle (MS) and then becoming subcutaneous about the level of the first or second rib and sending off branches to the different digitations (asterisks) of the serratus anterior muscle. AS, anterior scalene muscle; I–IV, rib levels. (B) Schematic drawing shows the action of the serratus anterior in stabilizing the scapula against the chest wall. Arrows, vector forces during serratus anterior muscle contraction. (C) Winged scapula in a 24-year-old woman with long thoracic nerve palsy following a car accident. Winging (arrows) involves the entire medial border of the left scapula. (D) Axial fat-suppressed turbo spin-echo T2-weighted image of the posterior chest wall obtained in the same patient shown in (B). Note increased intensity signal in the left serratus anterior muscle (white arrow) compared with the right one (outlined arrow). BRACHIAL PLEXUS AND NERVES ABOUT THE SHOULDER/MARTINOLI ET AL 543 winging, particularly when the patient extends his or her with the vagus; the external is mainly a motor nerve arms and pushes against a wall78 (Fig. 20C). Direct containing some sensory fibers coming from C1 through evaluation of the long thoracic nerve is feasible only in C3.10 This latter branch courses underneath the digastric part and for limited segments with US. The diagnosis and the sternocleidomastoid and, more distally, crosses basically relies on detection of denervation signs in the in diagonal the posterior cervical triangle bordered by the serratus anterior muscle. MR imaging is superior to US sternocleidomastoid anteriorly, the trapezius posteriorly, to recognize these signs (Fig. 20D). and the clavicle caudally (Fig. 21A). In this area, the spinal accessory nerve has a superficial course beneath the superficial cervical fascia and passes adjacent to Spinal Accessory Neuropathy lymph nodes. Thus it is vulnerable to blunt trauma, Although not a true peripheral nerve, the spinal acces- traction, and penetrating wounds or surgical procedures, sory nerve (CN XI) can be acceptably included in the list such as radical neck dissection for neoplasm, carotid of nerves around the shoulder because it supplies the endarterectomy, and cervical lymph node biopsy. trapezius and sternocleidomastoid. After exiting the Spinal accessory palsy causes a clinically distinct skull through the jugular foramen, the spinal accessory picture resulting from the paralysis of the trapezius, with nerve divides into two branches. The internal one joins drooping shoulder, asymmetry of the neckline, weakness Downloaded by: Rutgers University. Copyrighted material.

Figure 21 Spinal accessory nerve. (A) Schematic drawing shows the pertinent anatomy of the spinal accessory nerve (arrowhead) that emerges underneath the sternocleidomastoid muscle (1), becomes superficial at the posterior cervical triangle (2), and then enters and supplies the trapezius muscle (3). (B) Winged scapula in a 27-year-old woman with spinal accessory nerve palsy after cervical lymph node biopsy. Winging (arrow) involves the superomedial scapula. (C) Longitudinal ultrasound image obtained over the left cervical region in the same patient shown in (B). The spinal accessory nerve (outlined arrows) is seen crossing the sternocleidomastoid muscle and ending in a small fusiform neuroma (white arrow) suggesting complete nerve transection. 544 SEMINARS IN MUSCULOSKELETAL RADIOLOGY/VOLUME 14, NUMBER 5 2010

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