Musculoskeletal Sonography of the Tendon
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1 SOUND JUDGMENT SERIES Musculoskeletal Sonography of the Tendon Kenneth S. Lee, MD Invited paper The Sound Judgment Series consists of invited articles highlighting the clinical value of using ultrasound first in specific clinical diagnoses where ultrasound has shown comparative or superior value. The series is meant to serve as an educational tool for medical and sonography students and clinical practitioners and may help integrate ultrasound into clinical practice. Received September 4, 2012, from the Department of Musculoskeletal Radiology, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin USA. Revision requested September 17, Revised manuscript accepted for publication September 28, Address correspondence to Kenneth S. Lee, MD, Department of Musculoskeletal Radiology, University of Wisconsin School of Medicine and Public Health, 600 Highland Ave, CSC E3/366, Madison, WI USA. Abbreviations MRI, magnetic resonance imaging Tendon abnormalities are common musculoskeletal injuries that comprise 7% of all physician visits in the United States and up to 50% of all sports-related injuries. 1 3 Common tendon abnormalities include tendinopathy and tendon tears, which impose a substantial cost to society in the United States and abroad. According to the American Public Health Association, tendon disorders account for approximately $850 billion per year in health care costs and indirect lost wage expenditures. 4 Accurate and timely diagnosis of musculoskeletal tendon injuries is critical to ensure proper treatment and thus minimize societal costs. Magnetic resonance imaging (MRI) has been the imaging standard for musculoskeletal injuries. However, MRI is costly and overused. 5 Improvements in ultrasound technology have made sonography a rapidly growing imaging alternative and complementary tool to MRI for the diagnosis of common tendon injuries. 6 Sonography is both portable and cost-effective, with the potential to save $7 billion in health care costs over the next 15 years with increased use. 5 High-resolution and dynamic assessment advantages make sonography well suited for tendon evaluation and should be a first-line complementary diagnostic tool. Currently in clinical practice, musculoskeletal sonography is widely accepted and expanding in Europe. 7 Most recently, the use of musculoskeletal sonography is increasing among radiologists and nonradiologists in the United States, but especially by nonradiology groups. 8 Sonographic Appearance of the Tendon Tendons connect muscle to bone and are, therefore, unique structures that give a characteristic sonographic appearance. The tendon is made up of bundles of parallel linear fibers that contain, at a basic level, a relatively high percentage of type I collagen that is arranged in a cross-linked triple-helix structure. 9 The helical structure is stabilized by tightly bound water molecules. 10,11 The orientation of the collagen fibers is along the long axis of the tendon in keeping with the biomechanical strain placed between muscle and bone. 3 On sonography, this pattern is seen as multiple tightly spaced echogenic parallel lines in a fibrillar pattern (Figure 1A). 12 Transverse plane imaging shows multiple echogenic dots (Figure 1B). The normal tendon is uniform in echo texture and size by the American Institute of Ultrasound in Medicine J Ultrasound Med 2012; 31:
2 The ultrasound beam should be perpendicular to the orientation of the collagen fibers. If the beam is not perpendicular and off as little as 2 in angulation, the expected sonographic appearance is lost, simulating disease and increasing the likelihood of a false-positive diagnosis (Figure 2A). 13 This artifact is called anisotropy, unique to the musculoskeletal system. Therefore, great care should be given in imaging a tendon that is not parallel to the skin surface and for complex tendon structures that may change fiber orientation even within a tendon, such as seen in the rotator cuff (Figure 2B). While evaluating and documenting the tendon in orthogonal planes, the operator will often gently toggle the transducer or even indent the skin surface with one end of the transducer in what is known as a heel-toe maneuver to optimize tendon visualization by orienting the ultrasound beam perpendicular to the tendon structure. Figure 1. Normal sonograms of the tendon in a 32-year-old man. A, Longitudinal grayscale sonogram of the Achilles tendon (arrowheads) shows the parallel echogenic lines in a fibrillar pattern that is uniform in size and echo texture. B, Transverse grayscale sonogram of the normal Achilles tendon shows the tightly spaced network of tendon fibrils in a normal polka dot appearance in cross section. Star indicates calcaneus. A Advantages of Sonographic Evaluation Musculoskeletal sonography has come a long way over the past 30 years due to improved computer and transducer technology. The earliest sonographic reports of the tendon investigated patients with Achilles tendon rupture in Ultrasound technology advancements such as the development of linear array probes to decrease anisotropy and improvements in near-field high-resolution and focusing capabilities have helped propel musculoskeletal sonography as a viable imaging tool. 15 The most defining advantage of sonography over MRI is its real-time imaging capability, which allows for dynamic evaluation of the tendon using a variety of stress maneu- Figure 2. Anisotropy of the normal supraspinatus tendon in a 32-yearold man. A, Longitudinal grayscale sonogram of the normal supra - spinatus tendon (arrowheads) of the rotator cuff shows relative hypo echogenicity (arrow) of the deep tendon fibers as it angles away from the ultrasound beam to insert onto the footprint, mimicking tendon disease. B, Longitudinal grayscale sonogram of the same normal supraspinatus tendon without the hypoechogenicity after the transducer probe was gently adjusted shows normal tendon fibers (arrow). A B B 1880 J Ultrasound Med 2012; 31:
3 vers. 16,17 For example, in the neutral position, the long head of the biceps tendon may lie normally in the bicipital groove (Figure 3), only to dislocate medially once the arm, with elbow flexed, is externally rotated (Figure 4). In addition to tendon subluxation, other tendon abnormalities diagnosed dynamically include tendon snapping, friction between two structures such as in shoulder impingement, 18 and increasing conspicuity of tendon tears while stressing the tendon or with sonopalpation. 17 Real-time dynamic sonographic evaluation provides this unique diagnostic ability using controlled movements. Real-time imaging capability also allows for direct needle visualization during sonographically guided procedures. 16,19 Sonography can guide a needle to the target in any plane that is comfortable for both the patient and physician, while avoiding major neurovascular structures. Common sonographically guided procedures include tendon sheath and bursa steroid injections and lavage of calcium deposits seen in calcific tendinitis of the rotator cuff. 20 Innovations in sonographically guided therapy of the tendon such as platelet-rich plasma, percutaneous tenotomy, and sclerotherapy of neovessels to treat tendinopathy are only made possible because of the real-time capability and needle visualization under sonography (Figure 5). 21,22 Patient and referring provider satisfaction is also high because sonography can be used to both diagnose and treat various tendon abnormalities in one setting during a single appointment, requiring less days off work for the patient and accompanying family members. The therapeutic advantage of sonography clearly differentiates this imaging modality from others. High spatial resolution is another advantage of sonography, made possible by the emergence of high-frequency (10 12 MHz) linear array transducers. 23 High-frequency imaging can resolve finer detail within a tendon than MRI. For example, the axial resolution of a 10-MHz probe is about 150 μm, whereas a typical 1.5-T MRI scanner with a matrix of pixels and a 5-mm slice thickness is about μm. 24,25 This high-resolution advantage of sonography allows for a sensitive evaluation for tendinopathy and tendon tears. The power Doppler capability of sonography can give important information about hyperemia that can be associated with tendinopathy. 26 Tendinopathy is an overuse injury characterized by disorganization of fibers, tendon weakening, and abnormal tendon thickening from edema and fibroblast accumulation. 27 Hyperemia is increased vascularity that can also be seen with tendinopathy. 27 Typical sonographic findings of tendinopathy include loss of the normal fibrillar pattern, tendon thickening, and hypo - echogenicity. Increased Doppler flow helps increase specificity that the sonographic finding is likely correlated to the patient s site of pain (Figure 6). 16 Hyperemia can also be seen in tenosynovitis or bursitis closely associated with the tendon. Color Doppler imaging is also useful for detecting blood vessels that can be carefully avoided during sonographically guided procedures. 19 Accessibility of ultrasound equipment and lower cost are other advantages of musculoskeletal sonography. When a quick diagnosis to initiate early treatment coupled with increasing concerns of health care costs becomes a priority, sonography may be the preferred modality. 5 Figure 3. Dynamic sonographic evaluation of the long head of the biceps tendon in a 45-year-old woman. Transverse grayscale sonogram shows the long head of the biceps tendon (arrow) located within the bicipital groove. Figure 4. Dynamic sonographic evaluation of the long head of the biceps tendon in a 52-year-old woman. Transverse grayscale sonogram obtained during dynamic real-time evaluation of the long head of the biceps tendon (arrow) shows the tendon medially dislocating out of the bicipital groove. J Ultrasound Med 2012; 31:
4 Figure 5. Sonographically guided needle placement into the supra - spinatus tendon (arrowhead) during platelet-rich plasma treatment for rotator cuff tendinopathy in a 58-year-old man. Long-axis grayscale sonogram of the supraspinatus tendon shows in-plane needle placement (arrow) with the needle in the tendon and the needle tip placed on the footprint of the greater tuberosity (asterisk). A recent Medicare population study found that by the year 2020, the potential annual cost savings to Medicare by using musculoskeletal sonography instead of MRI, when appropriate, would be around $736 million. 5 Sonography Versus MRI Figure 6. Longitudinal power Doppler sonogram from a 25-year-old man with proximal patellar tendinopathy shows hyperemia (red) along the deep surface of the abnormally thickened and hypoechoic proximal patellar tendon (arrowheads). Star indicates patella. Although MRI is considered the imaging modality of choice for many musculoskeletal injuries, musculoskeletal sonography has been rapidly growing in popularity in the United States as a complementary or sometimes preferred imaging tool. This growth is in part due to increasing evidence-based literature stating that the diagnostic accuracy of musculoskeletal sonography is comparable to that of MRI. Magnetic resonance imaging has excellent soft tissue contrast and, therefore, is capable of evaluating the bone marrow and intra-articular structures such as cartilage and labrum that cannot be effectively imaged with sonography. However, sonography serves as a useful complementary tool that can quickly assess the integrity of superficial tendon structures as well as real-time dynamic evaluation for tendon snapping or dislocation. Many studies have investigated the accuracy of diagnosing tendon injuries using sonography. The best-studied tendon, and the most commonly imaged with sonography, is the shoulder rotator cuff. Recent metaanalyses that reviewed up to 62 sonographically based studies of the shoulder found that sonography had sensitivity of 92% to 96% and specificity of 93% to 96% for full-thickness tears compared to the reference standard of surgery (Figure 7) For partial-thickness rotator cuff tears, the sensitivity and specificity were 67% to 84% and 89% to 94%, respectively. Similarly, a metaanalysis of 67 MRI-based studies showed sensitivity of 92% and specificity of 93% for full-thickness tears compared to surgery and sensitivity of 64% and specificity of 92% for partial-thickness tears. 30 When comparing the accuracy of MRI and sonography for diagnosing rotator cuff tears, there was no statistically significant difference. Interestingly, however, patient satisfaction was significantly higher for sonography when receiving both MRI and sonography of the shoulder. 31 Because shoulder pain is most likely due to rotator cuff tears in the older population, 32 unlike labral tears in the younger population, sonography offers a quick, cost-effective, and accurate assessment of rotator cuff integrity. Studies have also investigated the accuracy of MRI and sonography for tendon tears of the ankle. Sonography has been shown to have sensitivity of 100% and specificity of 83% for differentiating partial- from full-thickness tears of the Achilles tendon (Figure 8). 33 Magnetic resonance imaging has shown a similar high level of sensitivity and specificity. However, for smaller ankle tendons such as the Figure 7. Full-thickness tear of the supraspinatus tendon in a 62-yearold man. Longitudinal grayscale sonogram of the supraspinatus tendon shows a large anechoic defect of a full-thickness tear (arrows). Arrowhead indicates articular cartilage of the humeral head J Ultrasound Med 2012; 31:
5 Figure 8. Partial-thickness tear of the Achilles tendon in a 56-year-old woman. Longitudinal grayscale sonogram of the distal Achilles tendon (arrowheads) shows a hypoechoic defect (arrow) involving the deep surface of the Achilles tendon near its calcaneal insertion. Asterisk indicates calcaneus. peroneal tendons, sonography compared to surgery was more sensitive (100% versus 83%) for detecting tears. 34,35 A meta-analysis for detecting gluteal tendon tears comparing MRI and sonography to surgery was also recently done. 36 The study found that the sensitivity of MRI for detecting gluteal tendon tears ranged from 33% to 100%, whereas specificity remained consistently high (92% 100%) across studies. Sonography was found to be consistently sensitive (79% 100%) compared to MRI, suggesting that sonography may be a first-line imaging tool for evaluating gluteal tendon tears. Tendinopathy is also a commonly imaged tendon abnormality. With respect to surgical correlation, sonography may be slightly more sensitive for detecting rotator cuff tendinopathy but less specific than MRI. However, Figure 9. Calcific tendinitis of the rotator cuff in a 48-year-old woman with chronic intermittent shoulder pain. Longitudinal grayscale sonogram of the supraspinatus tendon (arrowheads) shows a rounded hyperechoic calcium deposit (arrow) with some posterior acoustic shadowing within the supraspinatus tendon. Asterisk indicates greater tuberosity. sonography is highly sensitive for detecting shoulder calcific tendinitis, whereas MRI is not (Figure 9). 20,37 Another comparison study between MRI and sonography for patellar tendinopathy compared with clinical diagnosis showed sonography to be more sensitive than MRI. Specificity was also higher when power Doppler imaging was used to detect hyperemia. 38 Other studies comparing the sensitivity and specificity of MRI and sonography for Achilles tendinopathy and lateral epicondylosis had mixed results. 39,40 These discrepancies in results, however, may be limitations with regard to operator dependence, equipment differences, and the reference standard used. Musculoskeletal sonography is well suited for evaluating tendon abnormalities. In most cases, sonography and MRI have comparable diagnostic accuracy for detecting tendon tears or tendinopathy. However, the additional advantages of sonography such as accessibility, low cost, dynamic capability, and needle guidance make it a viable first-line imaging modality. Musculoskeletal sonography should be implemented as a complementary imaging tool in a growing musculoskeletal imaging practice that wants to offer integrated expertise across all modalities. References 1. Kannus P, Natri A. Etiology and pathophysiology of tendon ruptures in sports. Scand J Med Sci Sports 1997; 7: Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand J Med Sci Sports 1997; 7: Sharma P, Maffulli N. Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 2005; 87: Józsa L, Kannus P. Histopathological findings in spontaneous tendon ruptures. Scand J Med Sci Sports 1997; 7: Parker L, Nazarian LN, Carrino JA, et al. Musculoskeletal imaging: Medicare use, costs, and potential for cost substitution. J Am Coll Radiol 2008; 5: Adler RS, Finzel KC. The complementary roles of MR imaging and ultrasound of tendons. Radiol Clin North Am 2005; 43: , ix. 7. Klauser AS, Tagliafico A, Allen GM, et al. Clinical indications for musculoskeletal ultrasound: a Delphi-based consensus paper of the European Society of Musculoskeletal Radiology. Eur Radiol 2012; 22: Sharpe RE, Nazarian LN, Parker L, Rao VM, Levin DC. Dramatically increased musculoskeletal ultrasound utilization from 2000 to 2009, especially by podiatrists in private offices. J Am Coll Radiol 2012; 9: Rich A, Crick FH. The structure of collagen. Nature1955; 176: Fullerton GD, Rahal A. Collagen structure: the molecular source of the tendon magic angle effect. J Magn Reson Imaging 2007; 25: Ramachandran GN, Chandrasekharan R. Interchain hydrogen bonds via bound water molecules in the collagen triple helix. Biopolymers 1968; 6: J Ultrasound Med 2012; 31:
6 12. Robinson P. Sonography of common tendon injuries. AJR Am J Roentgenol 2009; 193: Crass JR, van de Vegte GL, Harkavy LA. Tendon echogenicity: ex vivo study. Radiology 1988; 167: Mayer R, Wilhelm K, Pfeifer KJ. Sonography of Achilles tendon rupture [in German]. Digitale Bilddiagnostik 1984; 4: McNally EG. The development and clinical applications of musculoskeletal ultrasound. Skeletal Radiol 2011; 40: Nazarian LN. The top 10 reasons musculoskeletal sonography is an important complementary or alternative technique to MRI. AJR Am J Roentgenol 2008; 190: Khoury V, Cardinal E, Bureau NJ. Musculoskeletal sonography: a dynamic tool for usual and unusual disorders. AJR Am J Roentgenol 2007; 188:W63 W Bureau NJ, Beauchamp M, Cardinal E, Brassard P. Dynamic sonography evaluation of shoulder impingement syndrome. AJR Am J Roentgenol 2006; 187: Joines MM, Motamedi K, Seeger LL, DiFiori JP. Musculoskeletal interventional ultrasound. Semin Musculoskelet Radiol 2007; 11: Lee KS, Rosas HG. Musculoskeletal ultrasound: how to treat calcific tendinitis of the rotator cuff by ultrasound-guided single-needle lavage technique. AJR Am J Roentgenol 2010; 195: McShane JM, Nazarian LN, Harwood MI. Sonographically guided percutaneous needle tenotomy for treatment of common extensor tendinosis in the elbow. J Ultrasound Med 2006; 25: Lee KS, Wilson JJ, Rabago DP, Baer GS, Jacobson JA, Borrero CG. Musculoskeletal applications of platelet-rich plasma: fad or future? AJR Am J Roentgenol 2011; 196: Hodgson RJ, O Connor PJ, Grainger AJ. Tendon and ligament imaging. Br J Radiol 2012; 85: Neumann T, Ermert H. Schlieren visualization of ultrasonic wave fields with high spatial resolution. Ultrasonics2006; 44(suppl 1):e1561 e Link TM, Majumdar S, Peterfy C, et al. High resolution MRI of small joints: impact of spatial resolution on diagnostic performance and SNR. Magn Reson Imaging 1998; 16: Zanetti M, Metzdorf A, Kundert HP, et al. Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US. Radiology 2003; 227: Abate M, Silbernagel KG, Siljeholm C, et al. Pathogenesis of tendinopathies: inflammation or degeneration? Arthritis Res Ther 2009; 11: Smith TO, Back T, Toms AP, Hing CB. Diagnostic accuracy of ultrasound for rotator cuff tears in adults: a systematic review and meta-analysis. Clin Radiol 2011; 66: Ottenheijm RP, Jansen MJ, Staal JB, et al. Accuracy of diagnostic ultrasound in patients with suspected subacromial disorders: a systematic review and meta-analysis. Arch Phys Med Rehabil 2010; 91: de Jesus JO, Parker L, Frangos AJ, Nazarian LN. Accuracy of MRI, MR arthrography, and ultrasound in the diagnosis of rotator cuff tears: a metaanalysis. AJR Am J Roentgenol 2009; 192: Middleton WD, Payne WT, Teefey SA, Hildebolt CF, Rubin DA, Yamaguchi K. Sonography and MRI of the shoulder: comparison of patient satisfaction. AJR Am J Roentgenol 2004; 183: Lin JC, Weintraub N, Aragaki DR. Nonsurgical treatment for rotator cuff injury in the elderly. J Am Med Dir Assoc 2008; 9: Hartgerink P, Fessell DP, Jacobson JA, van Holsbeeck MT. Full- versus partial-thickness Achilles tendon tears: sonographic accuracy and characterization in 26 cases with surgical correlation. Radiology 2001; 220: Lamm BM, Myers DT, Dombek M, Mendicino RW, Catanzariti AR, Saltrick K. Magnetic resonance imaging and surgical correlation of peroneus brevis tears. J Foot Ankle Surg 2004; 43: Grant TH, Kelikian AS, Jereb SE, McCarthy RJ. Ultrasound diagnosis of peroneal tendon tears: a surgical correlation. J Bone Joint Surg Am 2005; 87: Westacott DJ, Minns JI, Foguet P. The diagnostic accuracy of magnetic resonance imaging and ultrasonography in gluteal tendon tears: a systematic review. Hip Int 2011; 21: Martin-Hervas C, Romero J, Navas-Acien A, Reboiras JJ, Munuera L. Ultrasonographic and magnetic resonance images of rotator cuff lesions compared with arthroscopy or open surgery findings. J Shoulder Elbow Surg 2001; 10: Warden SJ, Kiss ZS, Malara FA, Ooi AB, Cook JL, Crossley KM. Comparative accuracy of magnetic resonance imaging and ultrasonography in confirming clinically diagnosed patellar tendinopathy. Am J Sports Med 2007; 35: Miller TT, Shapiro MA, Schultz E, Kalish PE. Comparison of sonography and MRI for diagnosing epicondylitis. J Clin Ultrasound 2002; 30: Aström M, Gentz CF, Nilsson P, Rausing A, Sjöberg S, Westlin N. Imaging in chronic Achilles tendinopathy: a comparison of ultrasonography, magnetic resonance imaging and surgical findings in 27 histologically verified cases. Skeletal Radiol 1996; 25: J Ultrasound Med 2012; 31:
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