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Ultrasonography and Electrodiagnosis: Are They Complementary Techniques?
Electrodiagnostics Supplement
Ultrasonography and Electrodiagnosis: Are They Complementary Techniques? Andrea Boon, MBChB Abstract: In this review, the role of high-resolution ultrasound in the diagnosis of neuromuscular disease as a tool complementary to electrodiagnostic techniques will be discussed, including indications, advantages, limitations, and potential for future research. Ultrasound-guided needle placement can be used to increase accuracy and safety of nerve conduction studies and needle electromyography. Ultrasound imaging of nerve and muscle can provide additional diagnostic information when performed in conjunction with nerve conduction studies and needle electromyography in the setting of nerve entrapment, nerve inflammation, and muscle disease. Its unique features include the ability to image structures dynamically in real time and the technique of sonopalpation. Because neuromuscular ultrasound is a rapidly evolving diagnostic tool with significant changes in technology, which facilitates its increased use, there is a steadily growing body of literature in this area. However, there remains an ongoing need for high-quality studies that evaluate the role and cost-effectiveness of neuromuscular ultrasound, both when used alone and in combination with electrodiagnosis. PM R 2013;5:S100-S106
INTRODUCTION In recent years, high-frequency ultrasound has become increasingly used by physiatrists for diagnostic and therapeutic purposes. With advances in technology, high-resolution portable units have become more affordable and increasingly prevalent as physiatrists develop the skill to use ultrasound in clinical practice. As a result, this modality is now a potential adjunctive tool in the evaluation of neuromuscular disease that is an ideal complement to electrodiagnosis. Prerequisites to successful implementation include an in-depth knowledge of anatomy, sound knowledge of ultrasound physics, and comfort with the machine itself to recognize and minimize artifacts and to facilitate image optimization. A detailed review of basic ultrasound principles and technique is outside the scope of this article, and interested readers are referred to recently published articles for more information [1,2]. Ultrasound allows one to image in real time and provides diagnostic anatomic and functional information concurrent with electrodiagnosis, without exposing the patient to radiation. Advantages of ultrasound in the clinical setting, compared with magnetic resonance imaging (MRI), include cost, accessibility, speed of the examination, ability to image the entire length of a nerve in a single study, and the capability to image both statically and dynamically. In addition, there is minimal artifact related to metal and no known contraindications, and ultrasound provides equivalent or better spatial resolution than MRI, with individual fascicles visible in many peripheral nerves [3,4]. One of the disadvantages of needle EMG is its invasive and sometimes painful nature, with a small but finite risk of direct injury to nerves, blood vessels, and vital structures. Ultrasound provides high-resolution imaging of soft tissue, fascial planes, and neurovascular structures, and the use of real-time ultrasound guidance for needle placement during nerve conduction studies (NCS) and needle electromyography (EMG) can increase accuracy and decrease risk in certain settings [5]. In addition to facilitating NCS and EMG, in the hands of a skilled operator, ultrasound provides detailed anatomic and pathophysiological information about nerve and muscle disease and real-time information regarding muscle activation and movement patterns. PM&R
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A.B. Department of Physical Medicine and Rehabilitation, Mayo Clinic and Foundation, 200 1st St SW, Rochester, MN 55905. Address correspondence to: A.B.; e-mail: boon. [email protected] Disclosure: nothing to disclose
© 2013 by the American Academy of Physical Medicine and Rehabilitation Suppl. 1, S100-S106, May 2013 http://dx.doi.org/10.1016/j.pmrj.2013.03.014
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Ultrasound should be considered complementary to electrodiagnosis; the latter provides physiological information, whereas the former provides both structural and, in some cases, additional physiological information. Just as the electrodiagnostic examination must be individualized for each patient and modified based on ongoing findings, the ultrasound examination is also dynamic; the sonographer can dynamically rule in or out various diagnoses based on the information acquired while performing the study. The sonographer also has the ability to use sonopalpation (direct pressure over structures of interest) and to receive real-time feedback from the patient: this ability to palpate and visualize simultaneously is a unique and potentially helpful feature. Besides operator dependence, a limitation of ultrasound is limited penetration, which can be problematic when imaging deeper structures such as cranial nerves, sympathetic chains, and nerve roots, and in patients who are obese [2]. Many applications in nerve and muscle disease involve appendicular imaging in which obesity and consequent limited penetration is not as problematic; nonetheless, image resolution is dependent on the specific ultrasound machine and transducer, and may vary considerably among manufacturers. The frequency of the ultrasound beam is inversely related to image resolution, such that lower frequencies allow for greater depth of penetration but less resolution than can be achieved when imaging superficial structures. Lower frequencies are sometimes necessary to evaluate deeper nerves, particularly in subjects who are obese, and, in such cases, a curvilinear probe provides a wider depth of field as well as deeper penetration of the beam. With ongoing developments in technology and a rapidly increasing body of supportive literature, the role of ultrasound in the diagnosis of neuromuscular disease will continue to evolve. The goal of this article is to review the current indications for ultrasound as it relates to localization of nerve and muscle to highlight the additional information ultrasound can provide in neuromuscular disease diagnosed electrophysiologically and to discuss the potential for future research.
APPLICATIONS OF ULTRASOUND IN NCS AND NEEDLE EMG Most nerves that are amenable to electrophysiological testing can also be visualized with ultrasound, depending on the skill and experience of the examiner. Larger, superficial nerves (such as the median at the wrist and the ulnar at the elbow) are easier to identify, but smaller nerves can also be quickly identified with current ultrasound technology [6]. Due to the penetration limitations of ultrasound imaging, deeper nerves can be more challenging, particularly in patients who are obese. For example, the sciatic nerve in the gluteal region and even in the thigh usually requires a curvilinear transducer with a lower frequency, which allows
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deeper penetration [7]. Cervical nerve roots and the brachial plexus can be visualized, although it may be challenging to identify all components, particularly in certain regions [8]. Many experienced electromyographers would argue that using ultrasound to facilitate NCS is unnecessary and merely adds time and expense. In the vast majority of routine NCS, this is true; however, there are certain settings in which ultrasound may be helpful to accurately localize a nerve at the stimulation or recording site. For example, when anatomy is altered or the usual anatomic landmarks are not palpable due to body habitus, it may not be clear whether an absent response is due to true pathology or to technical factors. In such cases, the targeted nerve can be localized sonographically before proceeding with standard surface stimulation directly over the nerve, for example, after ulnar nerve transposition surgery in which the postsurgical position of the nerve can be mapped out in the antecubital fossa and segmental studies performed along the relocated course of the nerve. Ultrasound-guided NCS has also allowed more accurate and reliable evaluation of nerves that are typically challenging for technical or anatomical reasons. Examples of these nerves include the lateral femoral cutaneous in the proximal thigh and the saphenous in the calf [9-11]. Nearnerve needle stimulation or recording can be performed more quickly, accurately, and safely, and with lower current and less patient discomfort when needles are placed under direct ultrasound guidance. This can be important when confirming that a proximal drop in amplitude represents true conduction block and is not due to submaximal stimulation of the nerve proximally [12]. Examples include the radial nerve at the spiral groove or elbow, the sciatic nerve in the thigh, the tibial nerve at the knee, the femoral nerve in the groin, the brachial plexus, and the cervical roots [13]. Ultrasound-guided needle placement is a clear advantage in anticoagulated patients, in which power-Doppler ultrasound can facilitate identification of blood vessels. Furthermore, ultrasound can be used for postprocedure surveillance if there is clinical concern for bleeding [5,14-16]. Similar to NCS, ultrasound guidance has a role in needle EMG in certain clinical scenarios, the most apparent of which is facilitating accurate muscle localization. Although clinicians are trained to use various techniques, including anatomic landmarks, palpation during muscle activation, and the proximity of motor unit firing with activation, for accurate localization during needle EMG, there are clinical scenarios that challenge one’s ability to isolate the targeted muscle. There are multiple examples in which inadvertent needle placement in an adjacent muscle (with different peripheral nerve or nerve root supply) will lead to an erroneous conclusion. Most experienced electromyographers are comfortable localizing muscles for needle EMG without using image guidance; however, muscles rarely examined can be more challenging as can deeper muscles, particularly in patients who are obese, or in cases in which the anatomy is
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altered from an operation or trauma. Several studies have shown that needle placement is not as accurate as might be expected in specific muscles, even in the hands of an experienced electromyographer [17-19]. Accuracy can be enhanced by the use of ultrasound guidance, and, as in the case of NCS, this adds little time and effort once the electromyographer is adequately skilled in ultrasound-guided needle placement [20]. Ultrasound-guided needle placement may also be indicated for patients who are unresponsive or uncooperative, those with severe denervation or spasticity that prevents voluntary muscle activation, or when patient feedback with voluntary contraction is not possible. As with needle placement for challenging NCS, ultrasound guidance for needle EMG can be used to mitigate risk in anticoagulated patients when examining muscles in proximity to vascular structures such as the iliopsoas, flexor pollicis longus, or tibialis posterior. Another high-risk situation in which ultrasound is advantageous is needle EMG of muscles in close proximity to vital structures, especially the lung. Needle EMG of the diaphragm is typically performed without image guidance; however, risks include pneumothorax, penetration of abdominal viscera, and hemorrhage. Due to these risks and the fact that the diaphragm can be extremely thin when atrophic, needle examination is often suboptimal, with inaccurate localization. This is more likely in patients who are obese or in those with altered anatomy or advanced obstructive pulmonary disease and associated lung hyperinflation. Even in relatively straightforward cases, the optimal intercostal space for needle entry, where the diaphragm is thickest and there is little or no encroachment of the lung during inspiration, can be identified before needle placement, and the depth of the diaphragm noted. Thus, if one is using a standard nonguided technique with needle insertion perpendicular to the skin– chest wall, then knowing the anticipated depth of the diaphragm is helpful [21,22]. In more technically challenging patients, direct real-time visualization of the needle with ultrasound throughout insertion can minimize risk and maximize the chance of entering the diaphragm. Use of an oblique stand-off technique can significantly enhance needle visualization throughout the procedure [1,2]. Although the greatest concern during needle EMG of the diaphragm is pneumothorax, the actual risk of this complication is very low and is more likely to occur during needle EMG of chest wall muscles, such as the serratus anterior, rhomboid, and thoracic paraspinals [23-25]. Ultrasound can also be used to localize these muscles, particularly in subjects who are obese and in whom ribs and other anatomic landmarks cannot be palpated. Image guidance ensures accurate identification of the targeted muscle, because chest wall muscles are often difficult to activate in isolation, particularly when denervated. It also allows qualitative evaluation for atrophy or signs of denervation in cases in which needle examination is technically difficult or contraindicated, particularly in unilat-
eral disease in which the patient can serve as his or her own control, in comparison with the contralateral side.
DIAGNOSTIC IMAGING OF MUSCLE Ultrasound imaging has been used for many years to diagnose muscle disease but may become more widely applicable in the future with the development of quantitative grayscale imaging [26-30]. Muscle size, the presence of atrophy or hypertrophy, changes in echotexture, and the pattern of muscle involvement can be evaluated. The dynamic aspect of ultrasound makes this a unique imaging modality, with the capacity to assess muscle function and to identify spontaneous activity such as fasciculations and, with increasing levels of resolution, even fibrillation potentials [31]. The role of sonographic assessment of spontaneous activity is unclear at this time and may only be clinically applicable in the evaluation of neuromuscular disease in pediatric patients in whom EMG is challenging. However, given that a larger area of muscle can be examined for fasciculation potentials by using ultrasound compared with needle EMG, this has potential application when testing for certain diseases, for example, amyotrophic lateral sclerosis [32,33]. Normal muscle has a “starry night” appearance when imaged in the short-axis plane and a pennate or feather-like appearance in the long-axis plane. The echointensity of a muscle changes as it develops myopathic or neurogenic changes and manifests as increasing homogeneity and/or an overall increase in signal intensity, accompanied by muscle atrophy in some cases [26]. Both neurogenic and myopathic disorders cause increased echointensity; however, there are qualitative differences that may help to differentiate the two. Neuropathies are often associated with atrophy, whereas muscle bulk is typically preserved in myopathies. Primary myopathic disorders tend to show homogeneously increased echointensity within a muscle group, whereas primary neuropathic processes usually show more heterogeneous changes [26]. Muscle echointensity can be assessed via grayscale analysis, but visual evaluation of a grayscale signal has been shown to have poor reproducibility [28]. Therefore, grayscale analysis via computer-assisted quantification of muscle echointensity has been developed as a reliable means of identifying changes in homogeneity as well as in overall echotexture [31]. Primarily on the basis of grayscale analysis, ultrasound has been shown to have high sensitivity in screening children who present with symptoms suggestive of neuromuscular disease, with ⬎90% sensitivity demonstrated by some investigators, by using final diagnosis as the criterion standard (based on clinical impression and results of various testing, including EMG, biochemical and genetic testing, and/or muscle biopsy) [26,31,34]. This has a particularly useful potential role in children, in whom standard electrodiagnostic evaluation can be challenging. When changes can be
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recognized on ultrasound, such as increased homogeneity or atrophy, this can help select the biopsy site and increase its yield. This could be helpful in diseases with patchy involvement of muscle, such as some inflammatory, metabolic, and inherited myopathies, and could decrease the risk of sampling areas of muscle that are either uninvolved or too severely affected to provide diagnostic information. Clinical utility of grayscale analysis is currently limited by the need for normal values, which are dependent on the particular ultrasound machine. System settings adjustments for each machine as well as correction models may allow for transposition of normal values to different machines in the future, but such software is not yet widely available. Other issues to account for when incorporating such techniques into clinical practice include standardization of testing, for example, by ensuring the use of the same anatomic landmarks and standardized muscle positions and by maintaining consistent machine settings for serial examinations. Quantitative imaging of muscle is a relatively simple technique to learn, and once normal values and technology to apply those values to different machines and transducers become more available, it has the potential for widespread use in screening for nerve and muscle disease and in targeting biopsies.
IMAGING OF NERVE Ultrasound imaging of nerve in isolation or in conjunction with electrodiagnostic testing is a rapidly evolving field, with many potential applications but also some limitations related to operator dependence and the lack of robust normal values in many cases. Electrodiagnosis provides diagnostic information regarding the presence of neuropathy and useful prognostic information based on the severity of axon loss and demyelination. In contrast to electrodiagnosis, high-resolution ultrasound in nerve disease provides anatomic information about the nerve itself and surrounding structures. It can be used to identify many types of nerve pathology, including focal entrapment, nerve transection, neuroma, nerve tumor, intraneural ganglion, and more diffuse involvement of the nerve, as seen in multifocal motor neuropathy with conduction block, hereditary motor sensory neuropathy (Charcot– Marie–Tooth disease), and acute and chronic inflammatory demyelinating polyradiculoneuropathy [35-40]. Structural lesions, such as fascial bands, anomalous muscles, hematomas, pseudoaneurysms, lipomas, fibromas, and hemangiomas, that can result in focal neuropathies can also be identified [37,39,41,42]. Ultrasound is useful in identifying anatomic variants, such as a bifid median nerve or persistent median artery, which may have implications for surgical treatment. Sonopalpation (direct pressure from the transducer applied over the area of interest) is a unique feature that can help to determine whether a neuroma is symptomatic [42,43]. The dynamic aspect of ultrasound can also be used
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to advantage in certain settings, such as diagnosing a subluxing ulnar nerve and simultaneously evaluating for a snapping head of the medial triceps, an entity that commonly goes unrecognized and that has implications in the surgical treatment of ulnar neuropathy [44-46]. Dynamic entrapment related to anomalous muscle or compressive lesions, for example, fascial bands, can be visualized by using real-time ultrasound, which allows the clinician to more confidently implicate the lesion as a cause of entrapment [47]. A normal peripheral nerve on ultrasound has a honeycomb appearance in cross-section (short axis), which represents the hypoechoic nerve fascicles surrounded by more hyperechoic connective tissue stroma or epineurium. In the long axis, nerves have a striated (fascicular) appearance, which consists of hypoechoic (ie, dark) linear fascicles that alternate with hyperechoic (ie, white or bright) interfascicular connective tissue [3,48]. Nerves are less anisotropic than tendons, more compressible, and more mobile, and usually course very close to vessels; these properties can facilitate differentiation of tendon from nerve [2,3,48]. When entrapped, nerves show changes in mobility, shape, and echotexture, likely related to intraneural edema, venous congestion, and/or fibrosis. Entrapped nerves typically show focal enlargement; although, in cases of severe compression, the nerve may be atrophied. At the site of focal compression, the nerve may be flattened, with fusiform hypoechoic (ie, dark) swelling just proximal, but, in other situations, the nerve will be swollen right at the site of entrapment. This variation may reflect different causes of entrapment (and varying pathologic changes in the nerve) or may just reflect the capacity of the nerve to swell at that site of entrapment [38]. Inflammatory hyperemia within the nerve is evident on ultrasound as an increased signal on color-Doppler ultrasound imaging, and qualitative changes in echogenicity, hyperemia, mobility, and fascicular pattern are often present. The cross-sectional area is currently the most reliable measure for sonographic diagnosis of nerve pathology, although, in some cases, it may be necessary to use the patient as his or her own control when evaluating for focal or unilateral pathology [49]. Nerve entrapment is the most well-studied area of nerve ultrasound to date, with a particular focus on median and ulnar neuropathies. Most studies have focused on median neuropathy at the wrist and, to a lesser extent, ulnar neuropathy at the elbow, with considerable overlap demonstrated between normal controls and those individuals with the condition [41,49,50-55]. Although, for the most part, electrodiagnostic testing remains the criterion standard in diagnosing neuropathy, ultrasound can be helpful in certain situations, particularly when electrodiagnostic studies are inconclusive. For example, an ulnar neuropathy may be nonlocalizable on the basis of NCS and needle EMG, but focal swelling may be present at the elbow on ultrasound [56,57].
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In carpal tunnel syndrome (CTS), if electrodiagnostic studies are inconclusive or negative, then ultrasound may be positive, and, in patients with coexisting peripheral neuropathy or radiculopathy, the use of patient-derived control measurements may allow one to make the diagnosis of CTS [49,58]. The potential role of ultrasound in electrodiagnosis is highlighted in a study in which diagnostic ultrasound was performed in a series of 77 patients after various mononeuropathies were diagnosed on NCS and needle EMG. In 26% of cases, an underlying cause for the neuropathy was identified with ultrasound, which resulted in modification of the management of those cases [39]. In another study, intraneural ganglion cysts, which should be surgically resected, were seen on ultrasound in 18% of patients with electrophysiological evidence of common peroneal (fibular) neuropathy at the fibular head [59]. In 1 series of 77 patients (96 wrists) with clinical and electrophysiological evidence of CTS, 17% had underlying flexor tenosynovitis evident on ultrasound [41]. In another study, in which ultrasound was performed in patients who presented with electrophysiological evidence of unilateral CTS, 35% had evidence of an underlying structural abnormality [60]. The advantages of ultrasound over electrodiagnosis include cost, depending on how extensive the electrodiagnostic testing is, its noninvasive nature, and the ability to identify underlying causes of entrapment neuropathies [50,51,56]. However, to promote more widespread integration of neuromuscular ultrasound into the electrodiagnostic laboratory setting and in isolation as a stand-alone diagnostic tool, there is a need for ongoing research.
Findings may well be diagnosis or region specific, and it is possible that each laboratory and/or practitioner needs to develop normal values for their laboratory setting and patient population.
THE FUTURE OF NEUROMUSCULAR ULTRASOUND
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To develop this unique imaging modality to its greatest potential in the realm of neuromuscular disease, there is a need for ongoing research that evaluates normal and diseased controls, the most appropriate site for nerve measurement, the utility of patient-derived control measures, the effect of various body metrics, and more detailed evaluation of changes in nerves over time with different disease processes. There is little information to date regarding the spectrum of changes seen in relation to the duration and severity of disease in response to various interventions, including surgery, and in cases of normal electrodiagnostic testing. There is a continuing need for validation of predefined diagnostic criteria and of measures of sensitivity, specificity, and positive and negative predictive values, with close attention to reproducibility, to help refine the utility of this modality in the realm of electrodiagnosis, specifically with including comparison of either electrodiagnosis or ultrasound alone versus when used in combination. Cost-effectiveness measures are also necessary, given that the use of these 2 modalities together is more expensive than either one in isolation.
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A curvilinear probe and the use of lower frequencies can help evaluate deeper nerves, for example, the sciatic nerve, in the gluteal and thigh regions as well as in obese or technically challenging subjects. After ulnar nerve transposition surgery, ultrasound can be used to locate the postsurgical position of the nerve and subsequently perform electrodiagnostic segmental studies along the relocated course of the nerve. In near-nerve needle stimulation studies, ultrasoundguided needle placement can be used to avoid other structures and to accurately stimulate nerves (such as radial nerve at the spiral groove, the sciatic nerve in the thigh, the tibial nerve at the knee, the femoral nerve in the groin, the brachial plexus, and the cervical roots) with lower currents. Ultrasound guidance for needle EMG can be used to mitigate risk in anticoagulated patients when examining muscles in proximity to vascular structures such as the iliopsoas, flexor pollicis longus, or tibialis posterior. Even in relatively straightforward cases, the optimal intercostal space for needle entry, where the diaphragm is thickest and there is little or no encroachment of the lung during inspiration, can be identified before needle placement, and the depth of the diaphragm noted. Ultrasound imaging has been used for many years to diagnose muscle disease but may become more widely applicable in the future with the development of quantitative grayscale imaging. The dynamic aspect of ultrasound can also be used to diagnose a subluxing ulnar nerve, a snapping head of the medial triceps on the ulnar nerve, and anomalous fascial bands. Sonopalpation reveals that nerves are less anisotropic than tendons, more compressible, and more mobile, and usually course very close to vessels. A cross-sectional area is the most reliable measure for sonographic diagnosis of nerve pathology currently, particularly when a side-to-side comparison is made.
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47. Sucher BM. Ultrasound imaging of the carpal tunnel during median nerve compression. Curr Rev Musculoskelet Med 2009;2:134-146. 48. Martinoli C, Bianchi S, Dahmane M, Pugliese F, Bianchi-Zamorani MP, Valle M. Ultrasound of tendons and nerves. Eur Radiol 2002;12:44-55. 49. Hobson-Webb LD, Massey JM, Juel VC, Sanders DB. The ultrasonographic wrist-to-forearm median nerve area ratio in carpal tunnel syndrome. Clin Neurophysiol 2008;119:1353-1357. 50. Beekman R, Schoemaker MC, Van Der Plas JP, et al. Diagnostic value of high-resolution sonography in ulnar neuropathy at the elbow. Neurology 2004;62:767-773. 51. Beekman R, Visser LH. Sonography in the diagnosis of carpal tunnel syndrome: A critical review of the literature. Muscle Nerve 2003;27:26-33. 52. Kamolz LP, Schrogendorfer KF, Rab M, Girsch W, Gruber H, Frey M. The precision of ultrasound imaging and its relevance for carpal tunnel syndrome. Surg Radiol Anat 2001;23:117-121. 53. Mondelli M, Filippou G, Frediani B, Aretini A. Ultrasonography in ulnar neuropathy at the elbow: Relationships to clinical and electrophysiological findings. Neurophysiol Clin 2008;38:217-226. 54. Visser LH, Smidt MH, Lee ML. High-resolution sonography versus EMG in the diagnosis of carpal tunnel syndrome. J Neurol Neurosurg Psychiatry 2008;79:63-67.
55. Yoon JS, Walker FO, Cartwright MS. Ultrasonographic swelling ratio in the diagnosis of ulnar neuropathy at the elbow. Muscle Nerve 2008;38: 1231-1235. 56. Bayrak AO, Bayrak IK, Turker H, Elmali M, Nural MS. Ultrasonography in patients with ulnar neuropathy at the elbow: Comparison of crosssectional area and swelling ratio with electrophysiological severity. Muscle Nerve 2010;41:661-666. 57. Padua L, Marjanovic I, Pasquale AD, Liotta G, Tonali PA. Ultrasonography in patients with ulnar neuropathy at the elbow: Comparison of cross-sectional area and swelling ratio with electrophysiological severity. Muscle Nerve 2011;43:298-299. 58. Visser LH, Smidt MH, Lee ML. Diagnostic value of wrist median nerve cross sectional area versus wrist-to-forearm ratio in carpal tunnel syndrome. Clin Neurophysiol 2008;119:2898-2899; author reply 2899. 59. Visser LH. High-resolution sonography of the common peroneal nerve: Detection of intraneural ganglia. Neurology 2006;67:14731475. 60. Nakamichi K, Tachibana S. Unilateral carpal tunnel syndrome and space-occupying lesions. J Hand Surg Br 1993;18:748-749.
Ultrasonography and Electrodiagnosis: Are They Complementary Techniques? Andrea Boon, MBChB Abstract: In this review, the role of high-resolution ultrasound in the diagnosis of neuromuscular disease as a tool complementary to electrodiagnostic techniques will be discussed, including indications, advantages, limitations, and potential for future research. Ultrasound-guided needle placement can be used to increase accuracy and safety of nerve conduction studies and needle electromyography. Ultrasound imaging of nerve and muscle can provide additional diagnostic information when performed in conjunction with nerve conduction studies and needle electromyography in the setting of nerve entrapment, nerve inflammation, and muscle disease. Its unique features include the ability to image structures dynamically in real time and the technique of sonopalpation. Because neuromuscular ultrasound is a rapidly evolving diagnostic tool with significant changes in technology, which facilitates its increased use, there is a steadily growing body of literature in this area. However, there remains an ongoing need for high-quality studies that evaluate the role and cost-effectiveness of neuromuscular ultrasound, both when used alone and in combination with electrodiagnosis. PM R 2013;5:S100-S106
INTRODUCTION In recent years, high-frequency ultrasound has become increasingly used by physiatrists for diagnostic and therapeutic purposes. With advances in technology, high-resolution portable units have become more affordable and increasingly prevalent as physiatrists develop the skill to use ultrasound in clinical practice. As a result, this modality is now a potential adjunctive tool in the evaluation of neuromuscular disease that is an ideal complement to electrodiagnosis. Prerequisites to successful implementation include an in-depth knowledge of anatomy, sound knowledge of ultrasound physics, and comfort with the machine itself to recognize and minimize artifacts and to facilitate image optimization. A detailed review of basic ultrasound principles and technique is outside the scope of this article, and interested readers are referred to recently published articles for more information [1,2]. Ultrasound allows one to image in real time and provides diagnostic anatomic and functional information concurrent with electrodiagnosis, without exposing the patient to radiation. Advantages of ultrasound in the clinical setting, compared with magnetic resonance imaging (MRI), include cost, accessibility, speed of the examination, ability to image the entire length of a nerve in a single study, and the capability to image both statically and dynamically. In addition, there is minimal artifact related to metal and no known contraindications, and ultrasound provides equivalent or better spatial resolution than MRI, with individual fascicles visible in many peripheral nerves [3,4]. One of the disadvantages of needle EMG is its invasive and sometimes painful nature, with a small but finite risk of direct injury to nerves, blood vessels, and vital structures. Ultrasound provides high-resolution imaging of soft tissue, fascial planes, and neurovascular structures, and the use of real-time ultrasound guidance for needle placement during nerve conduction studies (NCS) and needle electromyography (EMG) can increase accuracy and decrease risk in certain settings [5]. In addition to facilitating NCS and EMG, in the hands of a skilled operator, ultrasound provides detailed anatomic and pathophysiological information about nerve and muscle disease and real-time information regarding muscle activation and movement patterns. PM&R
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A.B. Department of Physical Medicine and Rehabilitation, Mayo Clinic and Foundation, 200 1st St SW, Rochester, MN 55905. Address correspondence to: A.B.; e-mail: boon. [email protected] Disclosure: nothing to disclose
© 2013 by the American Academy of Physical Medicine and Rehabilitation Suppl. 1, S100-S106, May 2013 http://dx.doi.org/10.1016/j.pmrj.2013.03.014
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Ultrasound should be considered complementary to electrodiagnosis; the latter provides physiological information, whereas the former provides both structural and, in some cases, additional physiological information. Just as the electrodiagnostic examination must be individualized for each patient and modified based on ongoing findings, the ultrasound examination is also dynamic; the sonographer can dynamically rule in or out various diagnoses based on the information acquired while performing the study. The sonographer also has the ability to use sonopalpation (direct pressure over structures of interest) and to receive real-time feedback from the patient: this ability to palpate and visualize simultaneously is a unique and potentially helpful feature. Besides operator dependence, a limitation of ultrasound is limited penetration, which can be problematic when imaging deeper structures such as cranial nerves, sympathetic chains, and nerve roots, and in patients who are obese [2]. Many applications in nerve and muscle disease involve appendicular imaging in which obesity and consequent limited penetration is not as problematic; nonetheless, image resolution is dependent on the specific ultrasound machine and transducer, and may vary considerably among manufacturers. The frequency of the ultrasound beam is inversely related to image resolution, such that lower frequencies allow for greater depth of penetration but less resolution than can be achieved when imaging superficial structures. Lower frequencies are sometimes necessary to evaluate deeper nerves, particularly in subjects who are obese, and, in such cases, a curvilinear probe provides a wider depth of field as well as deeper penetration of the beam. With ongoing developments in technology and a rapidly increasing body of supportive literature, the role of ultrasound in the diagnosis of neuromuscular disease will continue to evolve. The goal of this article is to review the current indications for ultrasound as it relates to localization of nerve and muscle to highlight the additional information ultrasound can provide in neuromuscular disease diagnosed electrophysiologically and to discuss the potential for future research.
APPLICATIONS OF ULTRASOUND IN NCS AND NEEDLE EMG Most nerves that are amenable to electrophysiological testing can also be visualized with ultrasound, depending on the skill and experience of the examiner. Larger, superficial nerves (such as the median at the wrist and the ulnar at the elbow) are easier to identify, but smaller nerves can also be quickly identified with current ultrasound technology [6]. Due to the penetration limitations of ultrasound imaging, deeper nerves can be more challenging, particularly in patients who are obese. For example, the sciatic nerve in the gluteal region and even in the thigh usually requires a curvilinear transducer with a lower frequency, which allows
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deeper penetration [7]. Cervical nerve roots and the brachial plexus can be visualized, although it may be challenging to identify all components, particularly in certain regions [8]. Many experienced electromyographers would argue that using ultrasound to facilitate NCS is unnecessary and merely adds time and expense. In the vast majority of routine NCS, this is true; however, there are certain settings in which ultrasound may be helpful to accurately localize a nerve at the stimulation or recording site. For example, when anatomy is altered or the usual anatomic landmarks are not palpable due to body habitus, it may not be clear whether an absent response is due to true pathology or to technical factors. In such cases, the targeted nerve can be localized sonographically before proceeding with standard surface stimulation directly over the nerve, for example, after ulnar nerve transposition surgery in which the postsurgical position of the nerve can be mapped out in the antecubital fossa and segmental studies performed along the relocated course of the nerve. Ultrasound-guided NCS has also allowed more accurate and reliable evaluation of nerves that are typically challenging for technical or anatomical reasons. Examples of these nerves include the lateral femoral cutaneous in the proximal thigh and the saphenous in the calf [9-11]. Nearnerve needle stimulation or recording can be performed more quickly, accurately, and safely, and with lower current and less patient discomfort when needles are placed under direct ultrasound guidance. This can be important when confirming that a proximal drop in amplitude represents true conduction block and is not due to submaximal stimulation of the nerve proximally [12]. Examples include the radial nerve at the spiral groove or elbow, the sciatic nerve in the thigh, the tibial nerve at the knee, the femoral nerve in the groin, the brachial plexus, and the cervical roots [13]. Ultrasound-guided needle placement is a clear advantage in anticoagulated patients, in which power-Doppler ultrasound can facilitate identification of blood vessels. Furthermore, ultrasound can be used for postprocedure surveillance if there is clinical concern for bleeding [5,14-16]. Similar to NCS, ultrasound guidance has a role in needle EMG in certain clinical scenarios, the most apparent of which is facilitating accurate muscle localization. Although clinicians are trained to use various techniques, including anatomic landmarks, palpation during muscle activation, and the proximity of motor unit firing with activation, for accurate localization during needle EMG, there are clinical scenarios that challenge one’s ability to isolate the targeted muscle. There are multiple examples in which inadvertent needle placement in an adjacent muscle (with different peripheral nerve or nerve root supply) will lead to an erroneous conclusion. Most experienced electromyographers are comfortable localizing muscles for needle EMG without using image guidance; however, muscles rarely examined can be more challenging as can deeper muscles, particularly in patients who are obese, or in cases in which the anatomy is
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altered from an operation or trauma. Several studies have shown that needle placement is not as accurate as might be expected in specific muscles, even in the hands of an experienced electromyographer [17-19]. Accuracy can be enhanced by the use of ultrasound guidance, and, as in the case of NCS, this adds little time and effort once the electromyographer is adequately skilled in ultrasound-guided needle placement [20]. Ultrasound-guided needle placement may also be indicated for patients who are unresponsive or uncooperative, those with severe denervation or spasticity that prevents voluntary muscle activation, or when patient feedback with voluntary contraction is not possible. As with needle placement for challenging NCS, ultrasound guidance for needle EMG can be used to mitigate risk in anticoagulated patients when examining muscles in proximity to vascular structures such as the iliopsoas, flexor pollicis longus, or tibialis posterior. Another high-risk situation in which ultrasound is advantageous is needle EMG of muscles in close proximity to vital structures, especially the lung. Needle EMG of the diaphragm is typically performed without image guidance; however, risks include pneumothorax, penetration of abdominal viscera, and hemorrhage. Due to these risks and the fact that the diaphragm can be extremely thin when atrophic, needle examination is often suboptimal, with inaccurate localization. This is more likely in patients who are obese or in those with altered anatomy or advanced obstructive pulmonary disease and associated lung hyperinflation. Even in relatively straightforward cases, the optimal intercostal space for needle entry, where the diaphragm is thickest and there is little or no encroachment of the lung during inspiration, can be identified before needle placement, and the depth of the diaphragm noted. Thus, if one is using a standard nonguided technique with needle insertion perpendicular to the skin– chest wall, then knowing the anticipated depth of the diaphragm is helpful [21,22]. In more technically challenging patients, direct real-time visualization of the needle with ultrasound throughout insertion can minimize risk and maximize the chance of entering the diaphragm. Use of an oblique stand-off technique can significantly enhance needle visualization throughout the procedure [1,2]. Although the greatest concern during needle EMG of the diaphragm is pneumothorax, the actual risk of this complication is very low and is more likely to occur during needle EMG of chest wall muscles, such as the serratus anterior, rhomboid, and thoracic paraspinals [23-25]. Ultrasound can also be used to localize these muscles, particularly in subjects who are obese and in whom ribs and other anatomic landmarks cannot be palpated. Image guidance ensures accurate identification of the targeted muscle, because chest wall muscles are often difficult to activate in isolation, particularly when denervated. It also allows qualitative evaluation for atrophy or signs of denervation in cases in which needle examination is technically difficult or contraindicated, particularly in unilat-
eral disease in which the patient can serve as his or her own control, in comparison with the contralateral side.
DIAGNOSTIC IMAGING OF MUSCLE Ultrasound imaging has been used for many years to diagnose muscle disease but may become more widely applicable in the future with the development of quantitative grayscale imaging [26-30]. Muscle size, the presence of atrophy or hypertrophy, changes in echotexture, and the pattern of muscle involvement can be evaluated. The dynamic aspect of ultrasound makes this a unique imaging modality, with the capacity to assess muscle function and to identify spontaneous activity such as fasciculations and, with increasing levels of resolution, even fibrillation potentials [31]. The role of sonographic assessment of spontaneous activity is unclear at this time and may only be clinically applicable in the evaluation of neuromuscular disease in pediatric patients in whom EMG is challenging. However, given that a larger area of muscle can be examined for fasciculation potentials by using ultrasound compared with needle EMG, this has potential application when testing for certain diseases, for example, amyotrophic lateral sclerosis [32,33]. Normal muscle has a “starry night” appearance when imaged in the short-axis plane and a pennate or feather-like appearance in the long-axis plane. The echointensity of a muscle changes as it develops myopathic or neurogenic changes and manifests as increasing homogeneity and/or an overall increase in signal intensity, accompanied by muscle atrophy in some cases [26]. Both neurogenic and myopathic disorders cause increased echointensity; however, there are qualitative differences that may help to differentiate the two. Neuropathies are often associated with atrophy, whereas muscle bulk is typically preserved in myopathies. Primary myopathic disorders tend to show homogeneously increased echointensity within a muscle group, whereas primary neuropathic processes usually show more heterogeneous changes [26]. Muscle echointensity can be assessed via grayscale analysis, but visual evaluation of a grayscale signal has been shown to have poor reproducibility [28]. Therefore, grayscale analysis via computer-assisted quantification of muscle echointensity has been developed as a reliable means of identifying changes in homogeneity as well as in overall echotexture [31]. Primarily on the basis of grayscale analysis, ultrasound has been shown to have high sensitivity in screening children who present with symptoms suggestive of neuromuscular disease, with ⬎90% sensitivity demonstrated by some investigators, by using final diagnosis as the criterion standard (based on clinical impression and results of various testing, including EMG, biochemical and genetic testing, and/or muscle biopsy) [26,31,34]. This has a particularly useful potential role in children, in whom standard electrodiagnostic evaluation can be challenging. When changes can be
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recognized on ultrasound, such as increased homogeneity or atrophy, this can help select the biopsy site and increase its yield. This could be helpful in diseases with patchy involvement of muscle, such as some inflammatory, metabolic, and inherited myopathies, and could decrease the risk of sampling areas of muscle that are either uninvolved or too severely affected to provide diagnostic information. Clinical utility of grayscale analysis is currently limited by the need for normal values, which are dependent on the particular ultrasound machine. System settings adjustments for each machine as well as correction models may allow for transposition of normal values to different machines in the future, but such software is not yet widely available. Other issues to account for when incorporating such techniques into clinical practice include standardization of testing, for example, by ensuring the use of the same anatomic landmarks and standardized muscle positions and by maintaining consistent machine settings for serial examinations. Quantitative imaging of muscle is a relatively simple technique to learn, and once normal values and technology to apply those values to different machines and transducers become more available, it has the potential for widespread use in screening for nerve and muscle disease and in targeting biopsies.
IMAGING OF NERVE Ultrasound imaging of nerve in isolation or in conjunction with electrodiagnostic testing is a rapidly evolving field, with many potential applications but also some limitations related to operator dependence and the lack of robust normal values in many cases. Electrodiagnosis provides diagnostic information regarding the presence of neuropathy and useful prognostic information based on the severity of axon loss and demyelination. In contrast to electrodiagnosis, high-resolution ultrasound in nerve disease provides anatomic information about the nerve itself and surrounding structures. It can be used to identify many types of nerve pathology, including focal entrapment, nerve transection, neuroma, nerve tumor, intraneural ganglion, and more diffuse involvement of the nerve, as seen in multifocal motor neuropathy with conduction block, hereditary motor sensory neuropathy (Charcot– Marie–Tooth disease), and acute and chronic inflammatory demyelinating polyradiculoneuropathy [35-40]. Structural lesions, such as fascial bands, anomalous muscles, hematomas, pseudoaneurysms, lipomas, fibromas, and hemangiomas, that can result in focal neuropathies can also be identified [37,39,41,42]. Ultrasound is useful in identifying anatomic variants, such as a bifid median nerve or persistent median artery, which may have implications for surgical treatment. Sonopalpation (direct pressure from the transducer applied over the area of interest) is a unique feature that can help to determine whether a neuroma is symptomatic [42,43]. The dynamic aspect of ultrasound can also be used
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to advantage in certain settings, such as diagnosing a subluxing ulnar nerve and simultaneously evaluating for a snapping head of the medial triceps, an entity that commonly goes unrecognized and that has implications in the surgical treatment of ulnar neuropathy [44-46]. Dynamic entrapment related to anomalous muscle or compressive lesions, for example, fascial bands, can be visualized by using real-time ultrasound, which allows the clinician to more confidently implicate the lesion as a cause of entrapment [47]. A normal peripheral nerve on ultrasound has a honeycomb appearance in cross-section (short axis), which represents the hypoechoic nerve fascicles surrounded by more hyperechoic connective tissue stroma or epineurium. In the long axis, nerves have a striated (fascicular) appearance, which consists of hypoechoic (ie, dark) linear fascicles that alternate with hyperechoic (ie, white or bright) interfascicular connective tissue [3,48]. Nerves are less anisotropic than tendons, more compressible, and more mobile, and usually course very close to vessels; these properties can facilitate differentiation of tendon from nerve [2,3,48]. When entrapped, nerves show changes in mobility, shape, and echotexture, likely related to intraneural edema, venous congestion, and/or fibrosis. Entrapped nerves typically show focal enlargement; although, in cases of severe compression, the nerve may be atrophied. At the site of focal compression, the nerve may be flattened, with fusiform hypoechoic (ie, dark) swelling just proximal, but, in other situations, the nerve will be swollen right at the site of entrapment. This variation may reflect different causes of entrapment (and varying pathologic changes in the nerve) or may just reflect the capacity of the nerve to swell at that site of entrapment [38]. Inflammatory hyperemia within the nerve is evident on ultrasound as an increased signal on color-Doppler ultrasound imaging, and qualitative changes in echogenicity, hyperemia, mobility, and fascicular pattern are often present. The cross-sectional area is currently the most reliable measure for sonographic diagnosis of nerve pathology, although, in some cases, it may be necessary to use the patient as his or her own control when evaluating for focal or unilateral pathology [49]. Nerve entrapment is the most well-studied area of nerve ultrasound to date, with a particular focus on median and ulnar neuropathies. Most studies have focused on median neuropathy at the wrist and, to a lesser extent, ulnar neuropathy at the elbow, with considerable overlap demonstrated between normal controls and those individuals with the condition [41,49,50-55]. Although, for the most part, electrodiagnostic testing remains the criterion standard in diagnosing neuropathy, ultrasound can be helpful in certain situations, particularly when electrodiagnostic studies are inconclusive. For example, an ulnar neuropathy may be nonlocalizable on the basis of NCS and needle EMG, but focal swelling may be present at the elbow on ultrasound [56,57].
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In carpal tunnel syndrome (CTS), if electrodiagnostic studies are inconclusive or negative, then ultrasound may be positive, and, in patients with coexisting peripheral neuropathy or radiculopathy, the use of patient-derived control measurements may allow one to make the diagnosis of CTS [49,58]. The potential role of ultrasound in electrodiagnosis is highlighted in a study in which diagnostic ultrasound was performed in a series of 77 patients after various mononeuropathies were diagnosed on NCS and needle EMG. In 26% of cases, an underlying cause for the neuropathy was identified with ultrasound, which resulted in modification of the management of those cases [39]. In another study, intraneural ganglion cysts, which should be surgically resected, were seen on ultrasound in 18% of patients with electrophysiological evidence of common peroneal (fibular) neuropathy at the fibular head [59]. In 1 series of 77 patients (96 wrists) with clinical and electrophysiological evidence of CTS, 17% had underlying flexor tenosynovitis evident on ultrasound [41]. In another study, in which ultrasound was performed in patients who presented with electrophysiological evidence of unilateral CTS, 35% had evidence of an underlying structural abnormality [60]. The advantages of ultrasound over electrodiagnosis include cost, depending on how extensive the electrodiagnostic testing is, its noninvasive nature, and the ability to identify underlying causes of entrapment neuropathies [50,51,56]. However, to promote more widespread integration of neuromuscular ultrasound into the electrodiagnostic laboratory setting and in isolation as a stand-alone diagnostic tool, there is a need for ongoing research.
Findings may well be diagnosis or region specific, and it is possible that each laboratory and/or practitioner needs to develop normal values for their laboratory setting and patient population.
THE FUTURE OF NEUROMUSCULAR ULTRASOUND
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To develop this unique imaging modality to its greatest potential in the realm of neuromuscular disease, there is a need for ongoing research that evaluates normal and diseased controls, the most appropriate site for nerve measurement, the utility of patient-derived control measures, the effect of various body metrics, and more detailed evaluation of changes in nerves over time with different disease processes. There is little information to date regarding the spectrum of changes seen in relation to the duration and severity of disease in response to various interventions, including surgery, and in cases of normal electrodiagnostic testing. There is a continuing need for validation of predefined diagnostic criteria and of measures of sensitivity, specificity, and positive and negative predictive values, with close attention to reproducibility, to help refine the utility of this modality in the realm of electrodiagnosis, specifically with including comparison of either electrodiagnosis or ultrasound alone versus when used in combination. Cost-effectiveness measures are also necessary, given that the use of these 2 modalities together is more expensive than either one in isolation.
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A curvilinear probe and the use of lower frequencies can help evaluate deeper nerves, for example, the sciatic nerve, in the gluteal and thigh regions as well as in obese or technically challenging subjects. After ulnar nerve transposition surgery, ultrasound can be used to locate the postsurgical position of the nerve and subsequently perform electrodiagnostic segmental studies along the relocated course of the nerve. In near-nerve needle stimulation studies, ultrasoundguided needle placement can be used to avoid other structures and to accurately stimulate nerves (such as radial nerve at the spiral groove, the sciatic nerve in the thigh, the tibial nerve at the knee, the femoral nerve in the groin, the brachial plexus, and the cervical roots) with lower currents. Ultrasound guidance for needle EMG can be used to mitigate risk in anticoagulated patients when examining muscles in proximity to vascular structures such as the iliopsoas, flexor pollicis longus, or tibialis posterior. Even in relatively straightforward cases, the optimal intercostal space for needle entry, where the diaphragm is thickest and there is little or no encroachment of the lung during inspiration, can be identified before needle placement, and the depth of the diaphragm noted. Ultrasound imaging has been used for many years to diagnose muscle disease but may become more widely applicable in the future with the development of quantitative grayscale imaging. The dynamic aspect of ultrasound can also be used to diagnose a subluxing ulnar nerve, a snapping head of the medial triceps on the ulnar nerve, and anomalous fascial bands. Sonopalpation reveals that nerves are less anisotropic than tendons, more compressible, and more mobile, and usually course very close to vessels. A cross-sectional area is the most reliable measure for sonographic diagnosis of nerve pathology currently, particularly when a side-to-side comparison is made.
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