Offering real-time, high-resolution images via intraoperative ultrasound is advantageous for a variety of peripheral nerve applications. To highlight the advantages of ultrasound, its extraoperative uses are reviewed. The current intraoperative uses, including nerve localization, real-time evaluation of peripheral nerve tumors, and implantation of leads for peripheral nerve stimulation, are reviewed. Although intraoperative peripheral nerve localization has been performed previously using guide wires and surgical dyes, the authors’ approach using ultrasound-guided instrument clamps helps guide surgical dissection to the target nerve, which could lead to more timely operations and shorter incisions.
Key points
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Evaluation of peripheral nerve pathology via ultrasound imaging is helpful in a variety of pathologic entities, including but not limited to nerve entrapments, mass lesions, and trauma.
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Advantages of ultrasound over other imaging modalities, such as MRI, include the ability to obtain real-time images and to obtain dynamic images.
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Intraoperative, ultrasound-guided nerve localization is a promising new technique that is particularly useful for nerves with a deep or varying anatomic course.
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Although there are several localization methods, the authors prefer placement of surgical clamps under ultrasound guidance to aid surgical dissection directly to the target nerve.
Introduction
Ultrasound has long been used in neurosurgery. With the advent of high-frequency ultrasound transducers, spatial resolution has improved to the point that peripheral nerves can be easily visualized. Most modern ultrasound systems equipped with high-frequency probes (at least 10 MHz) allow for spatial resolution of 150 μm. In contrast, MRI performed at 1.5 T allows a spatial resolution of 469 μm. This has opened the door to several extraoperative and intraoperative uses for ultrasound related to peripheral nerve disorders. Use of ultrasound has several advantages over alternative imaging modalities, including reduced cost and the ability to use ultrasound intraoperatively to gather real-time data and assess structures in a dynamic fashion. Ultrasound is mainly limited by depth of penetration and operator experience. Uses for ultrasound in peripheral nerve disorders continue to expand but include imaging of traumatic lesions, including neonatal brachial plexus palsy (NBPP), peripheral nerve tumors, nerve entrapment, and intraoperative localization of nerves for transection or stimulator placement.
Expedited and ideal visualization of nerves is dependent on a variety of factors, including operator experience, knowledge of typical nerve structure, and utilization of nearby landmarks such as muscles, tendons, and blood vessels. Proximal portions of the nerve present a larger cross-sectional area and a greater number of fascicles compared with distal portions of the nerve and are typically easier to visualize, particularly for a novice ultrasonographer. The normal appearance of peripheral nerves on ultrasound is similar to a honeycomb, with hypoechoic fascicles and hyperechoic connective tissue when viewed on the short axis ( Fig. 1 ), acquired by imaging the nerve perpendicular to the length of the probe. Similarly, in the long axis view obtained by placing the long axis of the probe parallel to the pathway of the nerve, hypoechoic nerve fascicles surrounded by hyperechoic connective tissue can be visualized.
Use of ultrasound in neurosurgery in general and, more specifically, for peripheral nerve disorders, continues to expand. The use of ultrasound began extraoperatively but is quickly finding new uses intraoperatively. The use of ultrasound extraoperatively for peripheral nerve disorders, localization of peripheral nerves intraoperatively using non–imaging-based techniques, and intraoperative localization of peripheral nerves using ultrasonography are reviewed. Furthermore, new ways in intraoperative ultrasound is used to improve peripheral nerve surgery are described.
Introduction
Ultrasound has long been used in neurosurgery. With the advent of high-frequency ultrasound transducers, spatial resolution has improved to the point that peripheral nerves can be easily visualized. Most modern ultrasound systems equipped with high-frequency probes (at least 10 MHz) allow for spatial resolution of 150 μm. In contrast, MRI performed at 1.5 T allows a spatial resolution of 469 μm. This has opened the door to several extraoperative and intraoperative uses for ultrasound related to peripheral nerve disorders. Use of ultrasound has several advantages over alternative imaging modalities, including reduced cost and the ability to use ultrasound intraoperatively to gather real-time data and assess structures in a dynamic fashion. Ultrasound is mainly limited by depth of penetration and operator experience. Uses for ultrasound in peripheral nerve disorders continue to expand but include imaging of traumatic lesions, including neonatal brachial plexus palsy (NBPP), peripheral nerve tumors, nerve entrapment, and intraoperative localization of nerves for transection or stimulator placement.
Expedited and ideal visualization of nerves is dependent on a variety of factors, including operator experience, knowledge of typical nerve structure, and utilization of nearby landmarks such as muscles, tendons, and blood vessels. Proximal portions of the nerve present a larger cross-sectional area and a greater number of fascicles compared with distal portions of the nerve and are typically easier to visualize, particularly for a novice ultrasonographer. The normal appearance of peripheral nerves on ultrasound is similar to a honeycomb, with hypoechoic fascicles and hyperechoic connective tissue when viewed on the short axis ( Fig. 1 ), acquired by imaging the nerve perpendicular to the length of the probe. Similarly, in the long axis view obtained by placing the long axis of the probe parallel to the pathway of the nerve, hypoechoic nerve fascicles surrounded by hyperechoic connective tissue can be visualized.
Use of ultrasound in neurosurgery in general and, more specifically, for peripheral nerve disorders, continues to expand. The use of ultrasound began extraoperatively but is quickly finding new uses intraoperatively. The use of ultrasound extraoperatively for peripheral nerve disorders, localization of peripheral nerves intraoperatively using non–imaging-based techniques, and intraoperative localization of peripheral nerves using ultrasonography are reviewed. Furthermore, new ways in intraoperative ultrasound is used to improve peripheral nerve surgery are described.
Extraoperative utilization of ultrasound for peripheral nerve disorders
Extraoperatively, ultrasound has a variety of diagnostic uses. Nerve entrapments, traumatic lesions, and peripheral nerve tumors can all be visualized and diagnosed using ultrasound. Studies continue to expand and report standardized diagnostic criteria.
Nerve Entrapments
The key finding to suggest peripheral nerve entrapment is hypoechoic enlargement of the nerve, both at the site of compression and proximal to the site of compression. Typically, loss of hyperechoic connective tissue occurs first, followed by nerve enlargement. Tinel sign elicited by pressing or tapping over the nerve at the site of compression, is a common clinical examination finding. The sonographic equivalent occurs when pressure over the nerve from the ultrasound transducer recreates the symptoms, typically pain or paresthesias. Although ultrasound can theoretically be used to examine any peripheral nerve at typical or even atypical sites of compression, it is best studied in the common entrapment syndromes, including carpal tunnel syndrome (CTS) with entrapment of the median nerve and cubital tunnel syndrome with entrapment of the ulnar nerve. Ultrasound does, however, offer some advantages when an atypical nerve becomes entrapped or a typical nerve becomes entrapped at an unusual site or by unusual pathology.
A common site of nerve entrapment is entrapment of the median nerve at the carpal tunnel. Causes of CTS include osteophyte formation, bony fractures, flexor tendon disease/tenosynovitis, accessory muscles, masses, trauma, pathologic enlargement of the median nerve, and various medical conditions (eg, diabetes, pregnancy, thyroid disease, amyloid, and multiple myeloma). Typical of entrapment neuropathies, in CTS the median nerve loses its hyperechoic connective tissue and becomes hypoechoic throughout. The nerve is enlarged proximal to the carpal tunnel and at the site, where it dives beneath the flexor retinaculum. Distal to the carpal tunnel, the nerve regains a normal caliber. The cross-sectional area of the median nerve is typically approximately 9 mm. Measuring the cross-sectional area of the median nerve at the volar wrist crease, 8 mm 2 to 12 mm 2 , is considered borderline for CTS whereas greater than 12 mm 2 is considered abnormal. Rather than measuring the absolute cross-sectional area of the nerve at the volar wrist crease, it can be measured at the proximal 1/3 of the pronator quadratus and compared to the maximal size of the nerve in the carpal tunnel. An increase of more than 2 mm 2 is highly diagnostic of CTS, approaching 99% sensitivity and approximately 100% specificity. Furthermore, cross-sectional measurements have been shown to correspond to severity of CTS based on nerve conduction studies. Additional studies are needed to evaluate whether imaging of the median nerve following release correlates to successful surgical outcomes.
Ulnar nerve entrapment around the elbow is referred to as cubital tunnel syndrome. Compression in this syndrome commonly occurs at 5 points: the medial intermuscular septum, arcade of Struthers, postcondylar groove, Osborne ligament (spanning from the olecranon process of the ulna to the medial epicondyle of the humerus), and Osborne fascia (connecting the ulnar and humeral heads of the flexor carpi ulnaris). Ultrasound evaluation of the ulnar nerve about the elbow has higher sensitivity than MRI with similar specificity and also offers the ability to dynamically image the nerve to assess for subluxation. Enlargement of the ulnar nerve proximal to the site of compression and hypoechoic appearance characterize this syndrome by ultrasonography. A cross-sectional area of 7.5 mm 2 to 9 mm 2 at the site of entrapment or 1.5 times that of the ulnar nerve at the midhumerus is diagnostic of cubital syndrome, although some studies make the diagnosis with areas greater than 8 mm 2 .
Ultrasound displays a high sensitivity and specificity for the diagnosis of cubital tunnel syndrome. In addition to being useful in the diagnosis of cubital tunnel syndrome, ultrasound can provide information that may alter the surgical treatment plan. Ultrasound can be used dynamically to visualize subluxation of the ulnar nerve over the edge of the medial epicondyle. The authors use this as an indication for transposition rather than simple neurolysis. Furthermore, snapping triceps syndrome can be diagnosed whereby the medial head of the triceps is abnormally displaced anteriorly during elbow flexion leading to 2 palpable snaps. When present, this prompts the authors to pay close attention to the area surrounding the intermuscular septum intraoperatively. Ultrasound seems of limited utility in the postoperative period, because the cross-sectional area of the ulnar nerve after decompression has not been shown to correlate with outcomes.
Ultrasound can also be extremely useful in atypical entrapment syndromes to identify the site of compression and to perform an ultrasound-guided diagnostic injection of local anesthetic. One case where when the authors commonly used this technique is when considering meralgia paresthetica with entrapment of the lateral femoral cutaneous nerve. Prior to offering any surgical intervention, an ultrasound is obtained to identify the nerve and then a diagnostic test injection is performed. The authors use improvement in symptoms as an indication for surgical decompression or neurectomy. A similar technique can be used when considering posttraumatic entrapment, such as with superficial peroneal nerve entrapment after foot trauma or saphenous nerve entrapment after knee trauma. The nerve can be identified using ultrasound, with a positive diagnostic test injection, suggesting that symptoms will improve with neurectomy or decompression, when feasible.
Mass Lesions
Ultrasound can detect and visualize a wide variety of masses that involve or encroach on peripheral nerves, including benign peripheral nerve sheath tumors, malignant peripheral nerve sheath tumors, and fibrofatty tumors of the extremities. Due to poor contrast resolution, however, ultrasound cannot reliably distinguish between benign and malignant lesions. Nerve sheath tumors, including schwannomas and neurofibromas, appear as hypoechoic masses continuous with the nerve. Although distinguishing between nerve sheath tumors is a challenge, sonography does reveal structural differences in preserved fascicles in schwannomas and disrupted fascicles in neurofibromas. Simon and colleagues used this intralesional structure revealed by ultrasound to avoid iatrogenic injury during resection surgery.
Although ultrasound provides some useful information for nerve sheath tumors, one mass lesion where ultrasound is particularly useful is intraneural ganglion cysts of the peroneal nerve. Peroneal neuropathy commonly occurs due to entrapment where the peroneal nerve wraps around the fibular neck and dives beneath the deep fascia of the peroneus longus. Ultrasound is particularly useful in the evaluation of this disorder for 2 reasons. First, ultrasound has been shown to have high sensitivity and specificity relative to electrodiagnostic studies for the diagnosis of peroneal neuropathy. Second, ultrasound can be used to diagnose mass lesions related to the peroneal nerve at this site, most commonly intraneural peroneal ganglion cysts. Recognition of intraneural ganglion cysts is particularly important, given that it changes the intraoperative management. When present, rather than simple neurolysis, the articular branch to the superior tibiofibular joint must be disconnected to prevent recurrence. Although MRI likely remains the imaging modality of choice for these lesions, ultrasound can readily identify them. Given the high sensitivity and specificity for peroneal neuropathy in general and the common occurrence of intraneural ganglion cysts (occurring in approximately 1 in 5 patients with peroneal neuropathy), ultrasound plays an important role in the evaluation of peroneal neuropathy.
Sonography has also become a mainstay in the evaluation of Morton neuroma. Morton neuroma results from fibrosis and inflammatory changes of entrapped interdigital nerves at the metatarsal heads under intermetatarsal ligaments, and patients typically present with burning pain in the second and third web space that is exacerbated by narrow-toed shoes or high heels. Classically, applying pressure to the plantar surface of the foot while compressing together the metatarsals produces a palpable click called Mulder sign. Appropriate imaging of the web space is required because in 28% of cases the neuroma is in the web space adjacent to the symptomatic web space. Ultrasound has been shown to have a sensitivity between 85% and 98%. Most studies have shown comparable sensitivity of ultrasound and MRI, although the specificity of MRI is higher compared with ultrasound—1.0 versus 0.854, respectively. Ultrasonic findings include a hypoechoic mass between and in line with the metatarsal bones that is in continuity with an interdigital nerve.
Peripheral Nerve Trauma
Peripheral nerve trauma ranges from mild neurapraxic injury to complete transection. In cases of severe stretch injury or transection, a neuroma forms as misguided axons attempt to grow distally. The neuroma appears as an abnormally enlarged segment of nerve that is hypoechoic ( Fig. 2 ). Determining whether the neuroma is present due to a transected nerve or is a neuroma-in-continuity requires tracing the nerve in question distally to ascertain if the neuroma is in continuity with the rest of the unaffected nerve. Sonographic evaluation provides useful information for preoperative planning regardless of the diagnosis. When a neuroma-in-continuity is present, there is hope of spontaneous recovery and a period of watchful waiting is typically undertaken. Conversely, in the case of a transected nerve, there is no hope of spontaneous recovery and early nerve reconstruction is optimal. Additionally, when a nerve is transected, retraction of the 2 ends of the nerve occurs over time. Ultrasound can be useful in both localizing the ends to help facilitate intraoperative localization and can also provide some guidance as to the likelihood of the need for a nerve graft.
Ultrasound is particularly useful for the evaluation of NBPP. Although magnetic resonance myelography and CT myelography are the workhorses of NBPP evaluation, both are limited in their ability to evaluate the extraforaminal brachial plexus; however, ultrasound evaluation has major advantages. Ultrasound can be used to evaluate the extraforaminal brachial plexus while simultaneously evaluating the nerves for continuity and neuroma formation, the muscles for evidence of denervation changes, and the glenohumeral joint for stability. Determining continuity of the nerve or the extent of neuroma formation in cases of neuroma-in-continuity is important for preoperative planning. This information facilitates localization of nerve ends intraoperatively and also helps determine the extent of nerve graft material required. Ultrasound evaluation of the rhomboids and serratus anterior can also provide information on the likely location of injury. Given that the takeoff of the dorsal scapular and long thoracic nerves is very proximal, atrophy and denervation changes in these muscles seen on ultrasound suggest a proximal injury that may not be amenable to nerve grafting.
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