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Intraoperative testing and monitoring during brachial plexus surgery
Intraoperative Monitoring of Neural Function Handbook of Clinical Neurophysiology, Vol. 8 M.R. Nuwer (Ed.) # 2008 Elsevier B.V. All rights reserved
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CHAPTER 51
Intraoperative testing and monitoring during brachial plexus surgery Huan Wanga, Allen T. Bishopb, Alexander Y. Shinb and Robert J. Spinnerb,* a
Visiting Fellow, Mayo Clinic, and Department of Hand Surgery, Huashan Hospital, Fudan University, Shanghai, People’s Republic of China b
Mayo Clinic, Brachial Plexus Clinic, Rochester, MN 55905, USA
Brachial plexus surgery can be challenging for a number of reasons: intricate and somewhat variable neuroanatomy, presence of scar or tumor obscuring the anatomy, and limited proximal nerve resources resulting in complex decision making. The preoperative assessment of the nerves is imperfect in cases of injury or suspected entrapment, and even the location of the nerve(s) in relation to tumor is suboptimal with current state-of-the-art examinations and studies. Operative assessment and intervention for brachial plexus pathology can be optimized by intraoperative electrophysiological techniques. These techniques may be used in surgery of the brachial plexus or its terminal branches, whether for injury, entrapment, or tumor. In cases of injury, intraoperative electrophysiological testing allows surgeons to better judge the function of nerve, the severity of injury, and the potential for neural recovery. The intraoperative testing can help determine the severity of compression (e.g., thoracic outlet syndrome) as well as assisting in the avoidance of accidental injury to neighboring nerves. Intraoperative electrophysiological testing can assist the surgeon to preserve critical nerve function when resecting a tumor, and help select nonfunctional fascicles when a nerve biopsy is needed. Transfer of a portion of normal nerve for muscle reanimation is also assisted by such tests, by identifying appropriate motor fascicles. In short, intraoperative electrophysiology techniques play an important role, assisting the surgeon in understanding of pathophysiology of nerve injury. Further, these studies are *
Correspondence to: Robert J. Spinner, M.D., Mayo Clinic, Brachial Plexus Clinic, Gonda 8S, 200 First Street SW, Rochester, MN 55905, USA. Tel.: þ1-507-284-2376; fax: þ1-507-284-5206. E-mail: [email protected] (R.J. Spinner).
helpful to preserve critical functions in incomplete injuries or lesions requiring exploration, nerve biopsy, or tumor resection. Finally, they are helpful in appropriate fascicle selection when intra- or extraplexal nerve transfers are used for the reanimation of paralyzed muscle. 51.1. Traumatic lesions For brachial plexus injuries, there are a variety of different techniques available to the surgeon. These techniques include neurolysis, nerve grafting, nerve transfers, and/or free functioning muscle transfer — depending on the pathology identified and defined at surgery as well as the goals of the surgery (Spinner and Kline, 2000; Kandenwein et al., 2005; Shin et al., 2005). Because of the numerous different potential lesions (or combinations of lesions) and corrective strategies, intraoperative decision making is often difficult. As surgical techniques rely on knowledge of the type and extent of neural pathology, it is imperative to determine as accurately as possible the extent of injury. Intraoperative electrophysiological testing adds useful information to the overall decision making in brachial plexus trauma. This includes evaluation of proximal nerve integrity with the central nervous system (preganglionic lesion), and the assessment of more distal lesions-in-continuity. In such cases, little reliable information can be obtained from direct inspection of the external surface of the nerve unless dorsal root ganglion and/or avulsed rootlets are seen and confirmed by histology. Histologic examination, while helpful, demands sampling (or sacrifice) of a piece of the nerve. Additionally, patients with a postganglionic rupture may still have preganglionic injury. Before surgery, an adequate history, physical examination, electrophysiological testing, and imaging
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studies are required to: (1) confirm the diagnosis of a brachial plexus lesion and determine the roots involved, (2) localize the level of injury (preganglionic vs. postganglionic), and (3) allow some determination of the severity of nerve injury. However, there are limitations to all of these examinations and studies. Intraoperative electrophysiological testing is used in such cases to provide information unobtainable with noninvasive means, which can be integrated with tests and imaging studies. For example, the electrophysiological integrity of motor and sensory pathways in individual spinal nerve ventral and dorsal rami can best be evaluated at surgery. This information, when correlated with preoperative computed tomography (CT) myelography, can be critical when considering the use of nerve grafts from individual roots. In some cases, nerve root injury is not detected by preoperative studies. For example, Kline and Hudson (1995) found a nonfunctioning C7 nerve root in 10% of cases by intraoperative electrophysiological testing, when preoperative testing would not have predicted this. This observation attests to the “expendable” nature of C7 due to the overlapping innervation of muscles innervated by this nerve. 51.1.1. Distinguishing preganglionic from postganglionic lesions Standard brachial plexus exploration is performed at a supraclavicular level, exposing neural elements proximally to an extraforaminal level; more proximal exposure of nerve roots is not typically obtained from this exposure. The appearance of the neural elements may be deceiving. At times, there may be little scarring present at the level of the scalene muscles in patients with preganglionic injury, due to the more proximal nature of the injury. In contrast, in other cases of preganglionic injury, retracted avulsed dorsal root ganglia may contribute to dense scarring. In cases of combined pre- and postganglionic injury, the operative appearance may be more suggestive of an isolated postganglionic injury with a neuroma in continuity (see below); sectioning of the nerve near the foramen however may reveal lack of normal fascicular structure. Several studies have documented the difficulty distinguishing pre- and postganglionic injury. One recent study demonstrated that combining physical examination and both routine and paraspinal electromyography (EMG) yielded an 80% diagnostic rate for intraforaminal lesion, 80% for extraforaminal lesion, and 67% for combined lesions (Balakrishnan and Kadadi, 2004).
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It should be noted that paraspinal fibrillations are not specific for an affected nerve. CT-myelography and magnetic resonance imaging (MRI) are only accurate in 85% and 52% of the cases, respectively, as verified by intradural exploration (Carvalho et al., 1997). Combined myelography and CT-myelography had 23% false findings in judging ventral root lesions and 27% false findings in judging dorsal root lesions when compared with findings on intradural inspection (Oberle et al., 1998). Intraoperative evoked potential recording, on the other hand, has been shown to have 100% sensitivity for ventral root avulsion with a negative evoked motor action potential from neck muscles and 100% sensitivity for dorsal root avulsion with a negative somatosensory evoked potential (SEP) when compared with intradural exploration (Oberle et al., 2002). The incidence of partial root avulsion at one or more levels has been reported to be as high as 11% in patients with brachial plexus root avulsions (Carvalho et al., 1997). Regardless, without intraoperative electrophysiology, it is difficult, if not impossible, to accurately assess these nerve roots. Given the limitations with individual techniques, we typically employ a combination of them, including SEPs, motor evoked potentials (MEPs), and nerve action potentials (NAPs) during supraclavicular brachial plexus exposures to distinguish pre- and postganglionic injuries (Kline and Hudson, 1995; Turkof et al., 1997; Burkholder et al., 2003; Hattori et al., 2004). The distinction between a pre- and postganglionic injury is clinically important in determination of which reconstructive surgery to perform. Nerve grafting to specific roots with evidence of preganglionic injury is not an option, for the obvious reason that continuity of the intraspinal rootlets with the spinal cord has been disrupted. Reimplantation of avulsed nerve roots has been reported (Carlstedt et al., 2000) but is only being performed at a few centers. Many brachial plexus surgeons feel that widespread clinical application of this technique is not yet warranted because of lack of clinical data and risk of substantial complications (Thomeer et al., 2002). At present, other methods including nerve transfers (neurotization) alone or combined with functioning free muscle transfer should be considered for reconstruction of these preganglionic injuries (Fig. 1). It should be remembered that each ventral ramus (nerve root) is assessed individually for avulsion (preganglionic injury) or rupture (postganglionic injury), and a final reconstructive plan then developed that makes use of available resources.
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Fig. 1. This patient had evidence of a left C5 and C6 brachial plexopathy without evidence of recovery when he was first evaluated at 3 months. He had denervation in the rhomboids and midcervical paraspinal muscles. Tinel’s sign was absent. CT myelogram suggested C5 and C6 avulsions. Rapid conductions on nerve action potentials (NAP) recordings and absent motor evoked potentials (MEPs) and somatosensory evoked potentials (SEPs) from C5 (shown here) and C6 suggested preganglionic injuries. Normal responses were obtained from C7. Correlating the preoperative and intraoperative assessment, we concluded that there was no functional integrity between the rootlets and the spinal cord in C5 and C6 and elected to perform nerve transfers for our reconstruction efforts. In an attempt to restore shoulder abduction and elbow flexion, we performed spinal accessory nerve to suprascapular nerve transfer; triceps branch to anterior branch of axillary nerve; ulnar nerve fascicle to biceps branch; median nerve fascicle to brachialis branch. UT, upper trunk; P, phrenic nerve.
51.1.2. Assessment of neuromas in continuity Intraoperative electrophysiology can be used to evaluate neuromas in continuity. Evaluation will determine the potential of spontaneous useful regeneration of the nerve. The assessment should provide guidance on the choice between neurolysis or resection of the neuroma and nerve grafting. We believe that the most useful intraoperative testing in this setting in adults with brachial plexus lesions is NAP recording (Kline and Happel, 1993) (Fig. 2). The presence of a NAP has clinical significance. Large operative series have demonstrated that 92% of neuromas in continuity with a present NAP result in good or better functional results with neurolysis (Kline and Hudson, 1995). Recovery has been demonstrated even in nerves with typically less favorable outcomes such as those supplying distal muscles (the lower trunk or the medial cord) when NAPs are recorded. In such a circumstance, neuroma
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Fig. 2. This patient had a left C5 and C6 brachial plexopathy without evidence of reinnervation over 6 months. In contrast to the patient in Fig. 1, examination of the rhomboids and cervical paraspinals was normal and a Tinel’s sign was present at Erb’s point. There was no sign of avulsion based on magnetic resonance imaging (MRI). At surgery, a bulbous neuroma (arrow) of the upper trunk (UT) was identified. Nerve action potential (NAP) recordings were performed across the lesion and were obtained, including from C5 to posterior division of the upper trunk (illustrated here). Based on this neurophysiologic assessment, neurolysis alone was performed. The patient made good clinical recovery over the ensuing 18 months. SSN, suprascapular nerve.
resection is ill-advised, likely resulting in a poorer clinical result than neurolysis alone. 51.1.3. Guiding selection of nerve branch or fascicles for transfer Nerve transfer, sometimes termed “neurotization,” refers to the use of all or a portion of a functioning nerve to restore crucial missing function by transfer to a specific distal motor or sensory target nerve (Figs. 3 and 4). The development of new distal nerve transfers, and the demonstration of results superior to conventional grafting, has revolutionized brachial
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Fig. 3. An innovative nerve transfer for shoulder abduction has been the introduction of the triceps branch to the axillary nerve by Leechavengvongs et al. (2003). This technique moves the reconstruction closer to the distal end-organ and can be accomplished safely in patients (A–D, with permission, Mayo Foundation 2006). A: The exposure is done along the posterior aspect of the proximal arm. B: The axillary (anterior and posterior branches to the deltoid) and radial nerves (particularly the triceps branches) are identified. An expendable functioning triceps branch is selected. C: In order to facilitate direct nerve repair, the triceps branch is sectioned distally and the anterior branch of the axillary nerve is sectioned proximally. D: The direct nerve transfer can then be accomplished.
plexus surgery. Such nerve transfers may come from extraplexal sources, or from functioning portions of the plexus and/or its terminal branches. For several decades, intercostal nerves have been the workhorse of nerve transfers, most commonly to restore elbow flexion. Other nerve transfers were then introduced, including the transfer of cervical plexus nerves, the spinal accessory nerve, and pectoral nerves. Other more controversial extraplexal nerve donors in use include the ipsilateral phrenic nerve, hypoglossal nerve and even the opposite, normal side (contralateral) C7 root.
Recently, several new nerve transfers from terminal (distal) plexus branches have been described. In most cases, these involve selection of a group of fascicles which are dissected from a large mixed nerve and transferred with direct coaptation to a specific muscle motor nerve (Oberlin et al., 1994; Teboul et al., 2004). The major advantage of this technique is that it allows the nerve repair to be done close to the target muscle, resulting in a shorter reinnervation time. This feature can be exploited in patients who present late after injury (9–15 months). These patients are generally poor candidates for conventional nerve
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Fig. 4. This technique as described by Leechavengvongs et al. (2003) and illustrated in Fig. 3 is demonstrated in this patient with a C5 and C6 lesion. The operative photograph was taken from an inferior to superior perspective compared to the Fig. 3 position. He underwent the same reconstructive strategy involving nerve transfers, as did the patient described in Fig. 1. A: The anterior branch of the axillary nerve (A) is sectioned proximally. B: The sectioned axillary nerve (A) was brought superficially and distally. The radial nerve (R) was exposed. The use of the nerve stimulator allowed us to select an expendable triceps branch (T). C: The triceps branch (T) has been sectioned and was brought near the axillary nerve (A). D: The nerve ends have been coapted without tension (arrow).
grafting because of the long distance and time required for nerve regeneration, together with ongoing irreversible changes in paralyzed muscles following the lower motor neuron injury. In order to minimize the risk of causing a new problem with motor weakness and/or permanent
sensory loss created by such use of a normal nerve, intraoperative electric stimulation of the nerve is required to select an expendable fascicle. A disposable hand-held or fine-tip monopolar stimulator is used to test portions of the nerve or individual fascicles. The fascicle for transfer is chosen according to
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the muscle contractions elicited. We typically use a qualitative approach to select noncritical muscles. Alternatively, one could perform compound muscle action potential (CMAP) recordings with surface or needle electrodes to take a more quantitative approach. These techniques can be used for determining whether a nerve or a portion of it, such as contralateral C7 (Holland and Belzberg, 1997), a triceps branch, or a fascicle from the ulnar or median nerve, is expendable. In some such transfers, a fascicle supplying a specific function is preferentially chosen. In the case of nerve transfers for elbow flexion for example, fascicles supplying the wrist flexors from ulnar or median nerve are directly transferred to the biceps and/or brachialis motor branches of the musculocutaneous nerve. These transfers are synergistic and can be learned independently with minimal effort. Such distal nerve transfers have improved outcomes for elbow flexion reconstruction and for many, have become the procedure of choice in C5 and C6 and even C5, C6, and C7 lesions. In several series, this type of reconstruction has led to >90% recovery at M3 or better for elbow flexion (Teboul et al., 2004). Improved results can be achieved with double reinnervation techniques by reinnervating both the biceps and brachialis muscles (Mackinnon et al., 2005). Microvascular surgery techniques, such as freefunctioning muscle transfers, have also been applied to brachial plexus reconstruction. This is a microsurgical
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procedure, transferring a muscle such as the gracilis, together with its vascular pedicle and motor nerve to the upper extremity to restore function of one or more denervated muscles. A common indication includes restoration of distal function (grasp) when patients are seen shortly after injury. Wrist and hand function is seldom restored by nerve graft or nerve transfer procedures. Free muscle transfer also allows reconstruction of elbow flexion in late presentations when irreversible muscle atrophy has occurred. We have also used free muscle after nerve surgery when the final result for a specific function has proved inadequate. Microvascular repair is performed and the muscle reinnervated by direct nerve transfer, most commonly using 2–3 intercostal or spinal accessory nerves. The donor nerve (or fascicle) is identified and selected using a nerve stimulator (similar to the method described above). 51.2. Entrapments The use of NAP recordings in thoracic outlet syndrome surgery provides confirmation of brachial plexus involvement close to the spine, involving C8 and T1 roots and the lower trunk. The severity of the compression can be determined, and any functional deficit resulting from previous surgeries demonstrated. Decrement of NAP amplitude and NAP conduction velocity is found in most cases for responses recorded from T1 to the lower trunk and
Fig. 5. Gilliatt–Sumner hand. A: Atrophy of the first dorsal web space. B: Atrophy of the thenar and hypothenar eminences.
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Fig. 6. This patient presented with progressive hand weakness and ulnar 2 digit numbness over the past 2 years and had a Gilliatt–Sumner hand. A: Elongated right C7 transverse process (arrow). B: The lower trunk (LT) was compressed and bowed over a fascial edge of the middle scalene muscle (arrow). SA, subclavian artery. C: The fascial band was released, scalenotomies were performed, and the elongated transverse process was resected. The lower trunk (LT), C8, and T1 nerves were decompressed. SA, subclavian artery.
C8 to the lower trunk, and occasionally for responses recorded from C7 to the middle trunk. These findings are particularly striking in patients who have neurogenic thoracic outlet syndrome with the typical Gilliatt–Sumner hand (Figs. 5 and 6) (Kline and Hudson, 1995; Tender et al., 2004). We do not typically use NAPs in routine cases of nerve compression, however, as the results do not change our course of treatment, namely decompression. 51.3. Tumors/lesions in and around nerve 51.3.1. Neural tumors Brachial plexus tumors are relatively rare. Reports of large series have therefore come from centers with a large referral practice (Ganju et al., 2001; Huang et al., 2004). Benign nerve sheath tumors are most common, including schwannomas and the less common neurofibromas. Malignant peripheral nerve sheath tumors (MPNSTs) can occur in this region as well, however. Resecting these neural tumors demand special skill, expertise, and experience as the potential for downgrading function is relatively high. The path of nerve fibers across a tumor can be mapped by intrafield stimulation at various places of the tumor/nerve tissue mass and/or recording CMAPs from a group of possible target muscles. A safe zone free or relatively free of motor fibers can then be outlined and resection of the tumor carried out through that area. In schwannomas, the tumor can often be dissected from the majority of functioning fascicles. A single fascicle or two may be seen entering and exiting the tumor. NAP recordings across these entering and exiting fascicles have demonstrated them to be
nonfunctional. Thus the tumor can be resected entirely and safely (Kline and Hudson, 1995). When a benign tumor involves additional fascicles or is intermingled with the nerve, efforts should be made to preserve fascicles that produce an NAP recording or a distal EMG response; those that do not produce a response may be sacrificed. In some cases of nerve tumors with unfavorable fascicular or entire neural involvement, monitoring may help predict postoperative outcome. In some tumors, resection of the nerve may be necessary. Monitoring may help predict overlap and ultimately, outcomes in these cases (Fig. 7). When functioning fascicles are sacrificed and provide a necessary function, a spanning nerve graft may then be applied. By applying these techniques, good or excellent results may be achieved in even large tumors, providing both pain relief and functional preservation (Press et al., 1992; Kline and Hudson, 1995). 51.3.2. Biopsy of neural lesions or tumors Intraoperative monitoring may be employed to aid safe selection of a fascicular biopsy when an unknown lesion affects the brachial plexus. The use of a portable stimulator or a hand-held fine probe with sterile EMG needles is recommended. This technique is similar to that described in the nerve transfer selection. Here, the difference is that many of the fascicles are nonfunctional due to the nature of the underlying process. In the past 5 years, we have performed fascicular biopsy in more than 40 cases of brachial plexus lesions (excluding obvious neurogenic tumors). Extrapolated from techniques we have performed
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Fig. 7. This 35-year-old woman presented to a head and neck surgeon with a painless neck mass. Open biopsy was done without the benefit of preoperative imaging and was consistent with a schwannoma. The patient experienced new paresthesias after the biopsy, which was fortunately aborted once the extent and nature of the (brachial plexus) mass was discovered. A: After the biopsy, T2-weighted MR image without fat saturation demonstrates a large dumbbell tumor extending out the C7 neural foramen. The mass is displacing the thecal sac and has mass effect on the vertebral artery. It extends into the supraclavicular fossa, displacing neighboring neural elements. Based on the appearance of this tumor, a two-stage procedure was planned and carried out. A posterior approach was first undertaken to decompress the cervical cord, resect the posterior component of the tumor, and stabilize the cervical spine. The C7 nerve root was transected. Intraoperative electromyography (EMG) monitoring confirmed the overlap in the upper limb muscles by other neural elements and predicted the lack of functional deficit with nerve resection. B: An anterior supraclavicular approach was then performed. The brachial plexus was then exposed and protected in vasoloops. The large mass had displaced the upper trunk (UT) and the lower trunk (LT). At the distal pole, the entire cross-sectional area of the posterior division is involved in the tumor. C: The mass and the involved middle trunk were resected. D: Resected specimen.
for other peripheral nerve lesions with indeterminate, but severe and progressive neuropathies, we have targeted fascicles localized by clinical examination and/or high-resolution MRI imaging. In these cases, we have had an 70% diagnostic rate. This type of biopsy is particularly difficult as obtaining a fascicle of sufficient length is challenging because of the plexal interchange of individual fascicles. We have successfully diagnosed and treated conditions such as inflammatory lesions, vasculitis, perineurioma, neurolymphoma, breast cancer (Fig. 8), and radiation plexitis, among others, with this technique (Dyck et al., 2003). Neurological downgrading was present in 10% of patients, though some cases were
temporary. Paresthesias and neuropathic pain were typically transient. 51.3.3. Tumors in the vicinity of nerves of the brachial plexus In selected cases, monitoring of the brachial plexus during resection of tumors extrinsic to nerve may also be helpful. It is helpful in certain cases of benign infiltrative processes such as desmoids tumors, malignant processes, and especially in recurrent tumors (Fig. 9). In these cases, scarring may impede definition of tissue planes. Electrophysiology facilitates identification, mobilization, and protection of neighboring nerves
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Fig. 8. This 71-year-old woman presented with a 4-year history of painless weakness and numbness in the left upper limb. Twenty-three years earlier, she had been diagnosed with breast cancer and had 14/17 positive lymph nodes. She underwent left modified radical mastectomy and received chemotherapy. She also had a history of monoclonal gammopathy of undetermined significance (MGUS). On examination, she had a flail left shoulder and elbow with moderate weakness in the fingers and hand. She had percussion tenderness over the supraclavicular region radiating into C5 and C6 distributions. Electromyography (EMG) showed evidence of a severe left brachial plexopathy, most severely affecting the upper trunk, but involving all elements and miming conduction block in the lower trunk. Magnetic resonance imaging (MRI) and positron emission tomographic (PET) scans done at other institutions were thought to have been unchanged over the years. A: Sagittal T1-weighted MR image with fat saturation post gadolinium shows enlarged nerves with peripheral enhancement (arrow). B: PET scan shows increased uptake along the course of the brachial plexus. C: Exploration of the brachial plexus was performed. A fascicular biopsy of a fibrotic upper trunk was undertaken. D: The resected fascicle (inset) demonstrated metastatic adenocarcinoma, consistent with a primary breast cancer; estrogen and progesterone receptors were positive. She received radiation therapy to the involved field followed by hormonal therapy and noted moderate improvement in function.
that might otherwise be difficult to identify or avoid. Ultimately, this may enhance preservation of function and extent of tumor resection. Similar monitoring
of nerves at risk is useful in other elective or reconstructive procedures as well (see peripheral nerve Chapter 56).
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Fig. 9. This 65-year-old woman presented with left shoulder and arm pain associated with an enlarging recurrent supraclavicular mass. She had undergone previous resection of a lipoma around the brachial plexus done through a partial claviculectomy. The mass initially was not encapsulated and was intertwined with the neural elements and subclavian artery. A: Coronal T1-weighted image demonstrates a large encapsulated recurrent lipoma (*) displacing the brachial plexus and the subclavian vessels. It extends between the scalene anterior and scalene middle. B: At reoperation, scarring was dense. The mass was encountered early in the dissection. The neurovascular elements were identified, mobilized, and protected. C: The mass could then be easily dissected. D: The supraclavicular and retroclavicular course of the brachial plexus and subclavian artery (SA) is seen following tumor removal. The previous claviculectomy is seen. Despite intraoperative monitoring that was extremely helpful in the deep dissection, the patient experienced a neurapraxia of the musculocutaneous nerve; elbow flexion was still strong through the preserved brachioradialis. At 1-year follow-up, she had complete relief of her pain, was neurologically intact, and had no evidence of tumor recurrence on magnetic resonance imaging (MRI).
51.4. Conclusion
References
Although intraoperative monitoring is labor intensive, expensive, and time consuming, it provides critical additional information in brachial plexus lesions that cannot be obtained by other methods or studies. It is indispensable for posttraumatic reconstruction for both diagnostic evaluation and surgical management. Electrophysiological monitoring provides a greater margin of safety in tumor surgery that, at least for us, makes it invaluable in our surgical practice.
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CHAPTER 51
Intraoperative testing and monitoring during brachial plexus surgery Huan Wanga, Allen T. Bishopb, Alexander Y. Shinb and Robert J. Spinnerb,* a
Visiting Fellow, Mayo Clinic, and Department of Hand Surgery, Huashan Hospital, Fudan University, Shanghai, People’s Republic of China b
Mayo Clinic, Brachial Plexus Clinic, Rochester, MN 55905, USA
Brachial plexus surgery can be challenging for a number of reasons: intricate and somewhat variable neuroanatomy, presence of scar or tumor obscuring the anatomy, and limited proximal nerve resources resulting in complex decision making. The preoperative assessment of the nerves is imperfect in cases of injury or suspected entrapment, and even the location of the nerve(s) in relation to tumor is suboptimal with current state-of-the-art examinations and studies. Operative assessment and intervention for brachial plexus pathology can be optimized by intraoperative electrophysiological techniques. These techniques may be used in surgery of the brachial plexus or its terminal branches, whether for injury, entrapment, or tumor. In cases of injury, intraoperative electrophysiological testing allows surgeons to better judge the function of nerve, the severity of injury, and the potential for neural recovery. The intraoperative testing can help determine the severity of compression (e.g., thoracic outlet syndrome) as well as assisting in the avoidance of accidental injury to neighboring nerves. Intraoperative electrophysiological testing can assist the surgeon to preserve critical nerve function when resecting a tumor, and help select nonfunctional fascicles when a nerve biopsy is needed. Transfer of a portion of normal nerve for muscle reanimation is also assisted by such tests, by identifying appropriate motor fascicles. In short, intraoperative electrophysiology techniques play an important role, assisting the surgeon in understanding of pathophysiology of nerve injury. Further, these studies are *
Correspondence to: Robert J. Spinner, M.D., Mayo Clinic, Brachial Plexus Clinic, Gonda 8S, 200 First Street SW, Rochester, MN 55905, USA. Tel.: þ1-507-284-2376; fax: þ1-507-284-5206. E-mail: [email protected] (R.J. Spinner).
helpful to preserve critical functions in incomplete injuries or lesions requiring exploration, nerve biopsy, or tumor resection. Finally, they are helpful in appropriate fascicle selection when intra- or extraplexal nerve transfers are used for the reanimation of paralyzed muscle. 51.1. Traumatic lesions For brachial plexus injuries, there are a variety of different techniques available to the surgeon. These techniques include neurolysis, nerve grafting, nerve transfers, and/or free functioning muscle transfer — depending on the pathology identified and defined at surgery as well as the goals of the surgery (Spinner and Kline, 2000; Kandenwein et al., 2005; Shin et al., 2005). Because of the numerous different potential lesions (or combinations of lesions) and corrective strategies, intraoperative decision making is often difficult. As surgical techniques rely on knowledge of the type and extent of neural pathology, it is imperative to determine as accurately as possible the extent of injury. Intraoperative electrophysiological testing adds useful information to the overall decision making in brachial plexus trauma. This includes evaluation of proximal nerve integrity with the central nervous system (preganglionic lesion), and the assessment of more distal lesions-in-continuity. In such cases, little reliable information can be obtained from direct inspection of the external surface of the nerve unless dorsal root ganglion and/or avulsed rootlets are seen and confirmed by histology. Histologic examination, while helpful, demands sampling (or sacrifice) of a piece of the nerve. Additionally, patients with a postganglionic rupture may still have preganglionic injury. Before surgery, an adequate history, physical examination, electrophysiological testing, and imaging
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studies are required to: (1) confirm the diagnosis of a brachial plexus lesion and determine the roots involved, (2) localize the level of injury (preganglionic vs. postganglionic), and (3) allow some determination of the severity of nerve injury. However, there are limitations to all of these examinations and studies. Intraoperative electrophysiological testing is used in such cases to provide information unobtainable with noninvasive means, which can be integrated with tests and imaging studies. For example, the electrophysiological integrity of motor and sensory pathways in individual spinal nerve ventral and dorsal rami can best be evaluated at surgery. This information, when correlated with preoperative computed tomography (CT) myelography, can be critical when considering the use of nerve grafts from individual roots. In some cases, nerve root injury is not detected by preoperative studies. For example, Kline and Hudson (1995) found a nonfunctioning C7 nerve root in 10% of cases by intraoperative electrophysiological testing, when preoperative testing would not have predicted this. This observation attests to the “expendable” nature of C7 due to the overlapping innervation of muscles innervated by this nerve. 51.1.1. Distinguishing preganglionic from postganglionic lesions Standard brachial plexus exploration is performed at a supraclavicular level, exposing neural elements proximally to an extraforaminal level; more proximal exposure of nerve roots is not typically obtained from this exposure. The appearance of the neural elements may be deceiving. At times, there may be little scarring present at the level of the scalene muscles in patients with preganglionic injury, due to the more proximal nature of the injury. In contrast, in other cases of preganglionic injury, retracted avulsed dorsal root ganglia may contribute to dense scarring. In cases of combined pre- and postganglionic injury, the operative appearance may be more suggestive of an isolated postganglionic injury with a neuroma in continuity (see below); sectioning of the nerve near the foramen however may reveal lack of normal fascicular structure. Several studies have documented the difficulty distinguishing pre- and postganglionic injury. One recent study demonstrated that combining physical examination and both routine and paraspinal electromyography (EMG) yielded an 80% diagnostic rate for intraforaminal lesion, 80% for extraforaminal lesion, and 67% for combined lesions (Balakrishnan and Kadadi, 2004).
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It should be noted that paraspinal fibrillations are not specific for an affected nerve. CT-myelography and magnetic resonance imaging (MRI) are only accurate in 85% and 52% of the cases, respectively, as verified by intradural exploration (Carvalho et al., 1997). Combined myelography and CT-myelography had 23% false findings in judging ventral root lesions and 27% false findings in judging dorsal root lesions when compared with findings on intradural inspection (Oberle et al., 1998). Intraoperative evoked potential recording, on the other hand, has been shown to have 100% sensitivity for ventral root avulsion with a negative evoked motor action potential from neck muscles and 100% sensitivity for dorsal root avulsion with a negative somatosensory evoked potential (SEP) when compared with intradural exploration (Oberle et al., 2002). The incidence of partial root avulsion at one or more levels has been reported to be as high as 11% in patients with brachial plexus root avulsions (Carvalho et al., 1997). Regardless, without intraoperative electrophysiology, it is difficult, if not impossible, to accurately assess these nerve roots. Given the limitations with individual techniques, we typically employ a combination of them, including SEPs, motor evoked potentials (MEPs), and nerve action potentials (NAPs) during supraclavicular brachial plexus exposures to distinguish pre- and postganglionic injuries (Kline and Hudson, 1995; Turkof et al., 1997; Burkholder et al., 2003; Hattori et al., 2004). The distinction between a pre- and postganglionic injury is clinically important in determination of which reconstructive surgery to perform. Nerve grafting to specific roots with evidence of preganglionic injury is not an option, for the obvious reason that continuity of the intraspinal rootlets with the spinal cord has been disrupted. Reimplantation of avulsed nerve roots has been reported (Carlstedt et al., 2000) but is only being performed at a few centers. Many brachial plexus surgeons feel that widespread clinical application of this technique is not yet warranted because of lack of clinical data and risk of substantial complications (Thomeer et al., 2002). At present, other methods including nerve transfers (neurotization) alone or combined with functioning free muscle transfer should be considered for reconstruction of these preganglionic injuries (Fig. 1). It should be remembered that each ventral ramus (nerve root) is assessed individually for avulsion (preganglionic injury) or rupture (postganglionic injury), and a final reconstructive plan then developed that makes use of available resources.
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Fig. 1. This patient had evidence of a left C5 and C6 brachial plexopathy without evidence of recovery when he was first evaluated at 3 months. He had denervation in the rhomboids and midcervical paraspinal muscles. Tinel’s sign was absent. CT myelogram suggested C5 and C6 avulsions. Rapid conductions on nerve action potentials (NAP) recordings and absent motor evoked potentials (MEPs) and somatosensory evoked potentials (SEPs) from C5 (shown here) and C6 suggested preganglionic injuries. Normal responses were obtained from C7. Correlating the preoperative and intraoperative assessment, we concluded that there was no functional integrity between the rootlets and the spinal cord in C5 and C6 and elected to perform nerve transfers for our reconstruction efforts. In an attempt to restore shoulder abduction and elbow flexion, we performed spinal accessory nerve to suprascapular nerve transfer; triceps branch to anterior branch of axillary nerve; ulnar nerve fascicle to biceps branch; median nerve fascicle to brachialis branch. UT, upper trunk; P, phrenic nerve.
51.1.2. Assessment of neuromas in continuity Intraoperative electrophysiology can be used to evaluate neuromas in continuity. Evaluation will determine the potential of spontaneous useful regeneration of the nerve. The assessment should provide guidance on the choice between neurolysis or resection of the neuroma and nerve grafting. We believe that the most useful intraoperative testing in this setting in adults with brachial plexus lesions is NAP recording (Kline and Happel, 1993) (Fig. 2). The presence of a NAP has clinical significance. Large operative series have demonstrated that 92% of neuromas in continuity with a present NAP result in good or better functional results with neurolysis (Kline and Hudson, 1995). Recovery has been demonstrated even in nerves with typically less favorable outcomes such as those supplying distal muscles (the lower trunk or the medial cord) when NAPs are recorded. In such a circumstance, neuroma
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Fig. 2. This patient had a left C5 and C6 brachial plexopathy without evidence of reinnervation over 6 months. In contrast to the patient in Fig. 1, examination of the rhomboids and cervical paraspinals was normal and a Tinel’s sign was present at Erb’s point. There was no sign of avulsion based on magnetic resonance imaging (MRI). At surgery, a bulbous neuroma (arrow) of the upper trunk (UT) was identified. Nerve action potential (NAP) recordings were performed across the lesion and were obtained, including from C5 to posterior division of the upper trunk (illustrated here). Based on this neurophysiologic assessment, neurolysis alone was performed. The patient made good clinical recovery over the ensuing 18 months. SSN, suprascapular nerve.
resection is ill-advised, likely resulting in a poorer clinical result than neurolysis alone. 51.1.3. Guiding selection of nerve branch or fascicles for transfer Nerve transfer, sometimes termed “neurotization,” refers to the use of all or a portion of a functioning nerve to restore crucial missing function by transfer to a specific distal motor or sensory target nerve (Figs. 3 and 4). The development of new distal nerve transfers, and the demonstration of results superior to conventional grafting, has revolutionized brachial
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Fig. 3. An innovative nerve transfer for shoulder abduction has been the introduction of the triceps branch to the axillary nerve by Leechavengvongs et al. (2003). This technique moves the reconstruction closer to the distal end-organ and can be accomplished safely in patients (A–D, with permission, Mayo Foundation 2006). A: The exposure is done along the posterior aspect of the proximal arm. B: The axillary (anterior and posterior branches to the deltoid) and radial nerves (particularly the triceps branches) are identified. An expendable functioning triceps branch is selected. C: In order to facilitate direct nerve repair, the triceps branch is sectioned distally and the anterior branch of the axillary nerve is sectioned proximally. D: The direct nerve transfer can then be accomplished.
plexus surgery. Such nerve transfers may come from extraplexal sources, or from functioning portions of the plexus and/or its terminal branches. For several decades, intercostal nerves have been the workhorse of nerve transfers, most commonly to restore elbow flexion. Other nerve transfers were then introduced, including the transfer of cervical plexus nerves, the spinal accessory nerve, and pectoral nerves. Other more controversial extraplexal nerve donors in use include the ipsilateral phrenic nerve, hypoglossal nerve and even the opposite, normal side (contralateral) C7 root.
Recently, several new nerve transfers from terminal (distal) plexus branches have been described. In most cases, these involve selection of a group of fascicles which are dissected from a large mixed nerve and transferred with direct coaptation to a specific muscle motor nerve (Oberlin et al., 1994; Teboul et al., 2004). The major advantage of this technique is that it allows the nerve repair to be done close to the target muscle, resulting in a shorter reinnervation time. This feature can be exploited in patients who present late after injury (9–15 months). These patients are generally poor candidates for conventional nerve
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Fig. 4. This technique as described by Leechavengvongs et al. (2003) and illustrated in Fig. 3 is demonstrated in this patient with a C5 and C6 lesion. The operative photograph was taken from an inferior to superior perspective compared to the Fig. 3 position. He underwent the same reconstructive strategy involving nerve transfers, as did the patient described in Fig. 1. A: The anterior branch of the axillary nerve (A) is sectioned proximally. B: The sectioned axillary nerve (A) was brought superficially and distally. The radial nerve (R) was exposed. The use of the nerve stimulator allowed us to select an expendable triceps branch (T). C: The triceps branch (T) has been sectioned and was brought near the axillary nerve (A). D: The nerve ends have been coapted without tension (arrow).
grafting because of the long distance and time required for nerve regeneration, together with ongoing irreversible changes in paralyzed muscles following the lower motor neuron injury. In order to minimize the risk of causing a new problem with motor weakness and/or permanent
sensory loss created by such use of a normal nerve, intraoperative electric stimulation of the nerve is required to select an expendable fascicle. A disposable hand-held or fine-tip monopolar stimulator is used to test portions of the nerve or individual fascicles. The fascicle for transfer is chosen according to
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the muscle contractions elicited. We typically use a qualitative approach to select noncritical muscles. Alternatively, one could perform compound muscle action potential (CMAP) recordings with surface or needle electrodes to take a more quantitative approach. These techniques can be used for determining whether a nerve or a portion of it, such as contralateral C7 (Holland and Belzberg, 1997), a triceps branch, or a fascicle from the ulnar or median nerve, is expendable. In some such transfers, a fascicle supplying a specific function is preferentially chosen. In the case of nerve transfers for elbow flexion for example, fascicles supplying the wrist flexors from ulnar or median nerve are directly transferred to the biceps and/or brachialis motor branches of the musculocutaneous nerve. These transfers are synergistic and can be learned independently with minimal effort. Such distal nerve transfers have improved outcomes for elbow flexion reconstruction and for many, have become the procedure of choice in C5 and C6 and even C5, C6, and C7 lesions. In several series, this type of reconstruction has led to >90% recovery at M3 or better for elbow flexion (Teboul et al., 2004). Improved results can be achieved with double reinnervation techniques by reinnervating both the biceps and brachialis muscles (Mackinnon et al., 2005). Microvascular surgery techniques, such as freefunctioning muscle transfers, have also been applied to brachial plexus reconstruction. This is a microsurgical
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procedure, transferring a muscle such as the gracilis, together with its vascular pedicle and motor nerve to the upper extremity to restore function of one or more denervated muscles. A common indication includes restoration of distal function (grasp) when patients are seen shortly after injury. Wrist and hand function is seldom restored by nerve graft or nerve transfer procedures. Free muscle transfer also allows reconstruction of elbow flexion in late presentations when irreversible muscle atrophy has occurred. We have also used free muscle after nerve surgery when the final result for a specific function has proved inadequate. Microvascular repair is performed and the muscle reinnervated by direct nerve transfer, most commonly using 2–3 intercostal or spinal accessory nerves. The donor nerve (or fascicle) is identified and selected using a nerve stimulator (similar to the method described above). 51.2. Entrapments The use of NAP recordings in thoracic outlet syndrome surgery provides confirmation of brachial plexus involvement close to the spine, involving C8 and T1 roots and the lower trunk. The severity of the compression can be determined, and any functional deficit resulting from previous surgeries demonstrated. Decrement of NAP amplitude and NAP conduction velocity is found in most cases for responses recorded from T1 to the lower trunk and
Fig. 5. Gilliatt–Sumner hand. A: Atrophy of the first dorsal web space. B: Atrophy of the thenar and hypothenar eminences.
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Fig. 6. This patient presented with progressive hand weakness and ulnar 2 digit numbness over the past 2 years and had a Gilliatt–Sumner hand. A: Elongated right C7 transverse process (arrow). B: The lower trunk (LT) was compressed and bowed over a fascial edge of the middle scalene muscle (arrow). SA, subclavian artery. C: The fascial band was released, scalenotomies were performed, and the elongated transverse process was resected. The lower trunk (LT), C8, and T1 nerves were decompressed. SA, subclavian artery.
C8 to the lower trunk, and occasionally for responses recorded from C7 to the middle trunk. These findings are particularly striking in patients who have neurogenic thoracic outlet syndrome with the typical Gilliatt–Sumner hand (Figs. 5 and 6) (Kline and Hudson, 1995; Tender et al., 2004). We do not typically use NAPs in routine cases of nerve compression, however, as the results do not change our course of treatment, namely decompression. 51.3. Tumors/lesions in and around nerve 51.3.1. Neural tumors Brachial plexus tumors are relatively rare. Reports of large series have therefore come from centers with a large referral practice (Ganju et al., 2001; Huang et al., 2004). Benign nerve sheath tumors are most common, including schwannomas and the less common neurofibromas. Malignant peripheral nerve sheath tumors (MPNSTs) can occur in this region as well, however. Resecting these neural tumors demand special skill, expertise, and experience as the potential for downgrading function is relatively high. The path of nerve fibers across a tumor can be mapped by intrafield stimulation at various places of the tumor/nerve tissue mass and/or recording CMAPs from a group of possible target muscles. A safe zone free or relatively free of motor fibers can then be outlined and resection of the tumor carried out through that area. In schwannomas, the tumor can often be dissected from the majority of functioning fascicles. A single fascicle or two may be seen entering and exiting the tumor. NAP recordings across these entering and exiting fascicles have demonstrated them to be
nonfunctional. Thus the tumor can be resected entirely and safely (Kline and Hudson, 1995). When a benign tumor involves additional fascicles or is intermingled with the nerve, efforts should be made to preserve fascicles that produce an NAP recording or a distal EMG response; those that do not produce a response may be sacrificed. In some cases of nerve tumors with unfavorable fascicular or entire neural involvement, monitoring may help predict postoperative outcome. In some tumors, resection of the nerve may be necessary. Monitoring may help predict overlap and ultimately, outcomes in these cases (Fig. 7). When functioning fascicles are sacrificed and provide a necessary function, a spanning nerve graft may then be applied. By applying these techniques, good or excellent results may be achieved in even large tumors, providing both pain relief and functional preservation (Press et al., 1992; Kline and Hudson, 1995). 51.3.2. Biopsy of neural lesions or tumors Intraoperative monitoring may be employed to aid safe selection of a fascicular biopsy when an unknown lesion affects the brachial plexus. The use of a portable stimulator or a hand-held fine probe with sterile EMG needles is recommended. This technique is similar to that described in the nerve transfer selection. Here, the difference is that many of the fascicles are nonfunctional due to the nature of the underlying process. In the past 5 years, we have performed fascicular biopsy in more than 40 cases of brachial plexus lesions (excluding obvious neurogenic tumors). Extrapolated from techniques we have performed
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Fig. 7. This 35-year-old woman presented to a head and neck surgeon with a painless neck mass. Open biopsy was done without the benefit of preoperative imaging and was consistent with a schwannoma. The patient experienced new paresthesias after the biopsy, which was fortunately aborted once the extent and nature of the (brachial plexus) mass was discovered. A: After the biopsy, T2-weighted MR image without fat saturation demonstrates a large dumbbell tumor extending out the C7 neural foramen. The mass is displacing the thecal sac and has mass effect on the vertebral artery. It extends into the supraclavicular fossa, displacing neighboring neural elements. Based on the appearance of this tumor, a two-stage procedure was planned and carried out. A posterior approach was first undertaken to decompress the cervical cord, resect the posterior component of the tumor, and stabilize the cervical spine. The C7 nerve root was transected. Intraoperative electromyography (EMG) monitoring confirmed the overlap in the upper limb muscles by other neural elements and predicted the lack of functional deficit with nerve resection. B: An anterior supraclavicular approach was then performed. The brachial plexus was then exposed and protected in vasoloops. The large mass had displaced the upper trunk (UT) and the lower trunk (LT). At the distal pole, the entire cross-sectional area of the posterior division is involved in the tumor. C: The mass and the involved middle trunk were resected. D: Resected specimen.
for other peripheral nerve lesions with indeterminate, but severe and progressive neuropathies, we have targeted fascicles localized by clinical examination and/or high-resolution MRI imaging. In these cases, we have had an 70% diagnostic rate. This type of biopsy is particularly difficult as obtaining a fascicle of sufficient length is challenging because of the plexal interchange of individual fascicles. We have successfully diagnosed and treated conditions such as inflammatory lesions, vasculitis, perineurioma, neurolymphoma, breast cancer (Fig. 8), and radiation plexitis, among others, with this technique (Dyck et al., 2003). Neurological downgrading was present in 10% of patients, though some cases were
temporary. Paresthesias and neuropathic pain were typically transient. 51.3.3. Tumors in the vicinity of nerves of the brachial plexus In selected cases, monitoring of the brachial plexus during resection of tumors extrinsic to nerve may also be helpful. It is helpful in certain cases of benign infiltrative processes such as desmoids tumors, malignant processes, and especially in recurrent tumors (Fig. 9). In these cases, scarring may impede definition of tissue planes. Electrophysiology facilitates identification, mobilization, and protection of neighboring nerves
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Fig. 8. This 71-year-old woman presented with a 4-year history of painless weakness and numbness in the left upper limb. Twenty-three years earlier, she had been diagnosed with breast cancer and had 14/17 positive lymph nodes. She underwent left modified radical mastectomy and received chemotherapy. She also had a history of monoclonal gammopathy of undetermined significance (MGUS). On examination, she had a flail left shoulder and elbow with moderate weakness in the fingers and hand. She had percussion tenderness over the supraclavicular region radiating into C5 and C6 distributions. Electromyography (EMG) showed evidence of a severe left brachial plexopathy, most severely affecting the upper trunk, but involving all elements and miming conduction block in the lower trunk. Magnetic resonance imaging (MRI) and positron emission tomographic (PET) scans done at other institutions were thought to have been unchanged over the years. A: Sagittal T1-weighted MR image with fat saturation post gadolinium shows enlarged nerves with peripheral enhancement (arrow). B: PET scan shows increased uptake along the course of the brachial plexus. C: Exploration of the brachial plexus was performed. A fascicular biopsy of a fibrotic upper trunk was undertaken. D: The resected fascicle (inset) demonstrated metastatic adenocarcinoma, consistent with a primary breast cancer; estrogen and progesterone receptors were positive. She received radiation therapy to the involved field followed by hormonal therapy and noted moderate improvement in function.
that might otherwise be difficult to identify or avoid. Ultimately, this may enhance preservation of function and extent of tumor resection. Similar monitoring
of nerves at risk is useful in other elective or reconstructive procedures as well (see peripheral nerve Chapter 56).
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Fig. 9. This 65-year-old woman presented with left shoulder and arm pain associated with an enlarging recurrent supraclavicular mass. She had undergone previous resection of a lipoma around the brachial plexus done through a partial claviculectomy. The mass initially was not encapsulated and was intertwined with the neural elements and subclavian artery. A: Coronal T1-weighted image demonstrates a large encapsulated recurrent lipoma (*) displacing the brachial plexus and the subclavian vessels. It extends between the scalene anterior and scalene middle. B: At reoperation, scarring was dense. The mass was encountered early in the dissection. The neurovascular elements were identified, mobilized, and protected. C: The mass could then be easily dissected. D: The supraclavicular and retroclavicular course of the brachial plexus and subclavian artery (SA) is seen following tumor removal. The previous claviculectomy is seen. Despite intraoperative monitoring that was extremely helpful in the deep dissection, the patient experienced a neurapraxia of the musculocutaneous nerve; elbow flexion was still strong through the preserved brachioradialis. At 1-year follow-up, she had complete relief of her pain, was neurologically intact, and had no evidence of tumor recurrence on magnetic resonance imaging (MRI).
51.4. Conclusion
References
Although intraoperative monitoring is labor intensive, expensive, and time consuming, it provides critical additional information in brachial plexus lesions that cannot be obtained by other methods or studies. It is indispensable for posttraumatic reconstruction for both diagnostic evaluation and surgical management. Electrophysiological monitoring provides a greater margin of safety in tumor surgery that, at least for us, makes it invaluable in our surgical practice.
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