- Email: [email protected]
Applications of Doppler Imaging in the Musculoskeletal System
Pictorial Review
Applications of Doppler Imaging in the Musculoskeletal System James Teh, BSc, MBBS, MRCP, FRCR
Pathological conditions affecting the musculoskeletal system often result in alterations of regional blood flow. The assessment of a Doppler signal in inflammatory or infective processes complements the grayscale findings, helping to evaluate the severity of disease. Doppler imaging can also be used to determine therapeutic response or help guide injections. In addition, Doppler interrogation enables vascular characterization of solid masses. The presence of a Doppler signal can also help differentiate solid from cystic lesions. This article reviews the wide range of applications for Doppler imaging of the musculoskeletal system.
Ultrasound has an invaluable role in the imaging of the musculoskeletal system, holding an advantage over other cross-sectional modalities in many circumstances due to its superior spatial resolution and ability to allow dynamic assessment. Combining grayscale ultrasound with Doppler imaging allows unique realtime evaluation of regional blood flow, which may be altered in a variety of disease processes. The assessment of Doppler signal in inflammatory or infective processes complements the grayscale findings, helping to evaluate the severity of disease. Doppler imaging can also be used to determine therapeutic response or guide injections. In addition Doppler interrogation enables vascular characterization of solid masses. The presence of Doppler signal can also help differentiate From the Nuffield Orthopaedic Centre, Headington, Oxford, United Kingdom. Reprint requests: James Teh, BSc, MBBS, MRCP, FRCR, Nuffield Orthopaedic Centre, Windmill Road, Headington, Oxford OX3 7LD, United Kingdom. E-mail: [email protected]. Curr Probl Diagn Radiol 2006;35:22-34. © 2006 Mosby, Inc. All rights reserved. 0363-0188/2006/$32.00 ⫹ 0 doi:10.1067/j.cpradiol.2005.10.003
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solid from cystic lesions. This article will review the wide range of applications for Doppler imaging of the musculoskeletal system.
Basic Physics Doppler shift is the change of frequency in a wave when a source moves relative to the given receiver. An example from day-to-day life is the drop in the pitch of a siren as an ambulance approaches and passes. With ultrasound imaging, the change of frequency detected between the transmitted and received ultrasound frequency is the Doppler shift.
What Is Color Doppler? Color Doppler is real-time imaging with the mean Doppler shift at a specified point depicted in color and superimposed on the grayscale image.
What Is Power Doppler? Unlike color Doppler, power Doppler depicts the total integrated power of the signal in color superimposed on the grayscale image.
What Are the Disadvantages of Color Doppler versus Power Doppler Imaging? The main problems that may arise from using color Doppler for imaging the musculoskeletal system which are not encountered with power Doppler are background noise, aliasing, and angle dependency.1 Background Noise. Color Doppler has a random direction of flow on the image as noise has a random frequency shift. Power Doppler on the other hand has a uniformly low noise. Increasing the gain on color
Curr Probl Diagn Radiol, January/February 2006
FIG 1. (A) Color Doppler US of the lower arm demonstrating the effect of high gain on background noise. (B) Power Doppler US demonstrating true flow on a background of noise. Note the improved visualization of the vessels compared with color Doppler (A). (Color version of figure is available online.)
Doppler increases the noise and thereby the image is degraded. When power Doppler gain is increased, there is a uniformly colored background with an enhanced signal from true flow. The sensitivity and dynamic range of power Doppler is therefore greater than color Doppler (Fig 1). Aliasing. Aliasing is a phenomenon that occurs when an analog signal is sampled at a frequency that is lower than half of its maximum frequency. This causes all the frequencies above half of the sampling frequency (the Nyquist frequency) to be folded back in the low-frequency region. With color Doppler, aliasing may cause vessels to appear discontinuous with possible distortion of direction and speed. Power Doppler is free from aliasing, as the signal is calculated from the integral of the Doppler spectrum. As a consequence, however, power Dopp-
Curr Probl Diagn Radiol, January/February 2006
ler does not display any information on direction and velocity. Angle Dependency. In color Doppler imaging the angle of insonation is crucial to avoid loss of signal and spurious results. The closer the angle of insonation is to 90°, the less the distortion. Power Doppler has the advantage of being relatively independent of angle. As the main interest is in detecting low-velocity microvascular flow in musculoskeletal imaging, power Doppler is generally preferred to color Doppler, although on new ultrasound machines, the difference is often negligible.
Ultrasound Settings Modern ultrasound machines have preset parameters that vary according to the region being examined.
23
FIG 2. Arteriovenous malformation of the thigh. (A) Color Doppler showing a large serpiginous feeding vessel. (B) Spectral Doppler trace confirms phasic, arterial flow. (Color version of figure is available online.)
These settings may require further customization and therefore an understanding of these parameters is necessary.
Sample Volume The sample volume should be kept as small as possible, as a large sample volume results in increased motion sensitivity.
Doppler Gain The bony cortex is a strong specular reflector and spurious Doppler signal may therefore occur at the cortical–soft-tissue interface. The Doppler gain threshold in musculoskeletal imaging should thus be set such that there is no signal seen within bone.2
Color Persistence The level of frame-averaging that occurs in obtaining an image is called persistence. High persistence results in the summation of several frames results in less information on pulsatile flow. A low persistence
24
allows better evaluation of pulsatile flow, but results in a poor signal-to-noise ratio.
Doppler Filter Level The Doppler filter reduces the amount of background noise, resulting in a clearer signal. However, if the filter level is set too high, slow flow may be missed. The filter should therefore be set at the lowest level and then gradually increased until a clear image is obtained.
Doppler Imaging Technique Use the Spectral Doppler Trace The use of a spectral Doppler trace can confirm if the Doppler signal is artifactual, as a phasic waveform should be obtained if there is true flow. Furthermore the spectral trace allows differentiation of arterial from venous flow and allows measurement of parameters such as the resistive index (Fig 2).
Curr Probl Diagn Radiol, January/February 2006
FIG 3. Ganglion. (A) Coronal gradient echo MR image demonstrating a fluid signal mass on the dorsum of the wrist. (B) Power Doppler US shows no internal Doppler signal and posterior acoustic enhancement. (Color version of figure is available online.)
FIG 4. Giant cell tumor of tendon sheath on the flexor aspect of the finger. (A) Extended field of view demonstrating a low echogenicity nodule in a digit. (B) Power Doppler ultrasound shows internal Doppler signal, confirming its solid nature. (Color version of figure is available online.)
FIG 5. Thigh abscess. (A) Extended field of view image demonstrating an echogenic mass in the thigh. (B) Peripheral flow is seen on color Doppler in the wall of the abscess indicating an inflammatory collection. (Color version of figure is available online.)
Curr Probl Diagn Radiol, January/February 2006
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FIG 6. Achilles tendinosis. (A) Power Doppler imaging demonstrates tendon neovascularity (arrows) and retro-Achilles inflammatory change. (B) Axial color Doppler image demonstrates flow within the tendon. (Color version of figure is available online.)
FIG 7. Lateral epicondylitis. Power Doppler demonstrates increased vascularity at the common extensor origin indicating tendinosis. (Color version of figure is available online.)
Use the Correct Angle of Insonation The angle of insonation is of particular importance when using color Doppler. To ensure an accurate representation of blood flow, the angle should be greater than 60°, which can be achieved by angling either the probe or the sample box. One of the advantages of power Doppler is that it is not angle dependent.
Use Light Transducer Pressure If the soft tissues are compressed, the vascular structures can become compromised, leading to an underestimation of blood flow. Ideally minimal transducer pressure should be exerted while still maintaining good contact. The most effective way to achieve this is to use copious jelly.
state of contraction. For example, when performing Doppler assessment of the patellar tendon, the knee should be extended rather than flexed.
Use Doppler for Dynamic Localization The motion sensitivity of Doppler imaging can be advantageous. For example, flexing the great toe may help localize the flexor hallucis longus tendon at the ankle.
Ensure a Constant Ambient Temperature The ambient temperature may affect regional blood flow.3 Serial scans should therefore ideally be performed in the same environment. A temperature-controlled water bath may be useful if an extremity is to be serially scanned.
Examine Structures in a Relaxed State
Compare with the Normal Side
Blood flow can be underestimated due to compression of vessels if a tendon or muscle is examined in a
Comparing the normal opposite limb is useful if there is uncertainty regarding the significance of Doppler flow.
26
Curr Probl Diagn Radiol, January/February 2006
FIG 8. Wrist flexor compartment tenosynovitis. There is marked synovial hypertrophy with increased flow on power Doppler. Note that the tendon itself appears relatively normal. (Color version of figure is available online.)
FIG 9. Granuloma surrounding a rose-thorn foreign body in the finger tip. (A) Grayscale ultrasound demonstrates a well-defined low-signal mass around a linear foreign body. (B) Extensive neovascularity on power Doppler ultrasound indicating a solid granuloma rather than an abscess. (Color version of figure is available online.)
FIG 10. Acute myositis in fibrodysplasia ossificans progressiva. (A) Extended field of view in the transverse plane showing marked swelling of the left rectus abdominis muscle (arrows) compared with the normal right side (arrowheads). (B) Increased flow is seen on color Doppler interrogation indicating an acute myositis. (Color version of figure is available online.)
Curr Probl Diagn Radiol, January/February 2006
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FIG 11. Carpal synovitis in psoriasis arthritis. Synovial hypertrophy and neovascularity at the carpus demonstrated power Doppler. (Color version of figure is available online.)
FIG 12. Infective arthritis of the elbow. (A) Extended field of view scan showing effusion and synovial hypertrophy. (B) Power Doppler demonstrates increased flow in a region of synovial hypertrophy. (Color version of figure is available online.)
Clinical Applications Distinguishing Solid from Fluid-Containing Structures Cysts or fluid-containing lesions are usually anechoic with posterior acoustic enhancement and no internal Doppler signal (Fig 3). Compressibility may be a feature. However, the presence of low-level internal echoes may make differentiation between a low-echogenicity solid mass and an echogenic fluid collection difficult. Under these circumstances, the
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presence of internal Doppler signal allows confirmation of a solid lesion4 (Fig 4). Similarly synovial hypertrophy can be differentiated from synovial fluid by the presence of Doppler signal.5
The Use of Doppler in Musculoskeletal Disorders Detailed structural information can be obtained by grayscale imaging but the addition of Doppler allows a more functional assessment, demonstrating disease activity and often confirming the diagnosis. Increased
Curr Probl Diagn Radiol, January/February 2006
FIG 13. (A and B) Metacarpophalangeal synovitis in rheumatoid arthritis. Power Doppler pre- and poststeroid therapy, respectively, showing a decrease in Doppler signal post-therapy, corresponding to clinical improvement. (Color version of figure is available online.)
Doppler signal may be generated by increased vascularity, increased perfusion, or hyperemia, which may occur in a variety of inflammatory, traumatic, degenerative, and neoplastic conditions.6,7 Differentiating Inflammatory from Noninflammatory Collections. Grayscale sonography is usually unable to distinguish inflammatory from noninflammatory collections. With Doppler imaging, however, increased blood flow may be seen around inflammatory collections8 (Fig 5). It should be noted that Doppler imaging is unreliable for distinguishing between infective and noninfective collections and that chronic, walled-off abscesses and tuberculous cold
Curr Probl Diagn Radiol, January/February 2006
abscesses may not demonstrate surrounding increased flow. Trauma. After soft-tissue injury, wound healing occurs in three main phases,9 as follows: The inflammatory phase, during which there is coagulation and leukocyte migration; the proliferative phase, when there is angiogenesis and fibrous proliferation; and the remodeling phase, when the tissue attempts return to its preinjury phenotype. After soft-tissue injury, increased Doppler signal may therefore be seen as part of a normal healing response. Tendon Disease. Tendinosis is a degenerative condition resulting from chronic repetitive trauma, char-
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FIG 14. Glomus tumor of the finger pulp. These are small highly vascular soft-tissue tumors that involve the neuromyoarterial glomus, usually in the fingertip or nail-bed. They present with exquisite tenderness, which may fluctuate with ambient temperature. (A) Grayscale ultrasound shows typical position of the mass in the finger pulp. (B) Color Doppler shows a hypervascular mass. (Color version of figure is available online.)
FIG 15. Synovial sarcoma of the foot. (A) Axial T2-weighted fat-saturated MRI demonstrating a lobulated high signal mass (arrowheads). (B) Power Doppler image demonstrating an anarchic vessel pattern with caliber changes and branching vessels. (Color version of figure is available online.)
acterized by loss of normal architecture, microtears, and tenocyte hyperplasia with angiogenesis.10 Doppler interrogation may reveal neovascularization, which occurs as part of a chronic reparative process11 (Figs 6 and 7). Sclerosing the vessels in tendinosis may help alleviate symptoms, suggesting that angiogenesis is related to the pathogenesis of pain.12,13 Tenosynovitis is an inflammatory or infective process characterized by low-echogenicity synovial hypertrophy and/or fluid in the synovial sheath. The tendon may appear normal or thickened. Doppler can reveal the relative proportion of vascularized synovium to fluid5 (Fig 8).
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Cellulitis. Cellulitis is characterized by thickening and induration of the skin and subcutaneous tissues.14 On ultrasound there is loss of normal architecture of the subcutaneous fat, with increased echogenicity and poor ultrasound penetration. Increased blood flow in the thickened tissues may be used to differentiate the edema of cellulitis from fluid overload. Inflammatory masses and granulomas may be also be distinguished from abscesses by the presence of internal Doppler signal (Fig 9). Posttraumatic regional pain syndrome or reflex sympathetic dystrophy is a painful condition comprising hyperesthesia and vasomotor disturbance. Eventually
Curr Probl Diagn Radiol, January/February 2006
FIG 16. Ewing’s sarcoma of femur. (A) Large lobulated mass with anarchic vessel pattern demonstrating trifurcations. (B) Conventional radiograph showing a large mass with cortical destruction and ossification. (Color version of figure is available online.)
FIG 17. Benign nerve sheath tumor. (A) Low echogenicity mass with dural tail (arrows). (B) Simple nonbranching vessel in the mass shown on power Doppler. (Color version of figure is available online.)
it may lead to muscle atrophy and trophic skin changes. Doppler may reveal increased flow in the skin and subcutaneous tissues of these patients.15 Muscle Inflammation. Myositis can be the result of a variety of disease processes including autoimmune disease, infection, and trauma. The normal muscle architecture is disrupted with edema, swelling, and increased blood flow on Doppler imaging (Fig 10). The ultrasound appearances, however, are usually nonspecific and biopsy may be required for diagnosis. Muscle contusion may be followed by myositis ossificans.16 During the initial inflammatory phase, there may be muscle edema with increased flow on Doppler imaging. Echogenic foci may be seen, indicating mineralization. This phase is followed by progressive calcification starting in the periphery, which matures into ossification. Once ossification is mature,
Curr Probl Diagn Radiol, January/February 2006
there is usually no evidence of increased flow. The lesion may eventually diminish in size and resorb.17 Synovitis. Synovitis may occur with infective, degenerative, or inflammatory arthropathies. Grayscale sonography reveals low-echogenicity material within the joint, which may indicate fluid or synovial hypertrophy (Fig 11). Although Doppler imaging is useful for confirmation of inflammatory change, it is unhelpful in differentiating between infective and noninfective conditions18 (Fig 12). Furthermore, it should be remembered that the absence of periarticular flow on Doppler does not exclude septic arthritis. Early Detection of Inflammatory Arthropathy. Ultrasound has an established role in detecting early synovitis and erosions in inflammatory arthropathy.19-21 The erosive phase of rheumatoid arthritis is preceded by production of pannus, which is associated
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FIG 18. Hemangioma overlying trapezius. (A) Extended field of view demonstrating a heterogeneous ovoid mass. (B) Color Doppler demonstrates slow-flowing large-caliber vessels. (Color version of figure is available online.)
with angiogenesis.22 The early detection of vascular pannus therefore has an important role in determining if and when disease-modifying drugs should be introduced. In patients with established inflammatory arthritis, the degree of blood flow in areas of synovitis is greater during exacerbations.21,23 The use of a microbubble ultrasound contrast agent can improve the detection of intraarticular blood flow at finger joints,24 but in practice, contrast is not routinely required. Monitoring Therapeutic Response. Monitoring therapeutic response has a key role in evaluating the effectiveness of different treatments for inflammatory rheumatological conditions. Traditionally, the clinical
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examination, self-assessment questionnaires, and serological markers of inflammation such as the ESR have been used to assess response to treatment, but these methods are not always reliable. Several researchers have therefore used Doppler ultrasound to qualitatively monitor therapeutic response.7,25 Using techniques such as flow mapping, Doppler signal can also be quantified. As long as the Doppler settings are unchanged, serial studies can be used to objectively quantify response to treatment23 (Fig 13). One of the difficulties with using ultrasound for serial studies is that exact repositioning of the probe may be difficult to achieve even with the scrupulous use of landmarks. Tumor Characterization. Ultrasound is often the first imaging modality used in the investigation of
Curr Probl Diagn Radiol, January/February 2006
musculoskeletal soft-tissue masses. It provides a quick and effective means of confirming the presence of a lesion, and providing valuable information on the site, size, morphology, and anatomical relations. Certain benign lesions, such as superficial lipomas and glomus tumors, have a characteristic appearance on ultrasound26 (Fig 14). Grayscale ultrasound however cannot reliably distinguish malignant from benign masses.26-29 Using a combination of color and power Doppler imaging with spectral wave analysis, researchers have attempted to differentiate benign from malignant lesions.30 The vessels in malignant tumors have an irregular margin and lack a muscle layer. With Doppler imaging, these vessels often demonstrate an anarchic pattern, with occlusions, stenoses, arteriovenous shunts, and loops31 (Figs 15 and 16). Benign tumors tend to have a simple branching vascular morphology (Fig 17). The morphologic analysis of tumor vessels appears to be more reliable than quantitative parameters such as flow velocities or resistive indices.32,33 Although meticulous Doppler examination may help differentiate benign from malignant lesions, in practice, a cautious approach should be taken as not all malignant soft-tissue tumors have an anarchic pattern. Furthermore some necrotic lesions and low-grade neoplasms may not demonstrate neovascularity and therefore the absence of flow does not necessarily indicate benignity. Ultimately, ultrasound is unable to provide a histological diagnosis, which can only be obtained by biopsy. Soft-tissue vascular anomalies are usually easily recognized by a combination of grayscale and Doppler imaging. The presence of a solid component can help distinguish hemangiomas from arteriovenous malformations34 (Fig 18). Hemangiomas however have a very variable appearance, sometimes showing no flow on Doppler imaging.34 Arterial flow characteristics and vessel density have been shown to be similar in hemangiomas and arteriovenous malformations. In the latter however there is a significantly higher mean venous peak velocity (Fig 2). Doppler ultrasound has also been shown to be useful in assessing response of tumors such as Ewing’s sarcoma and osteosarcoma to chemotherapy.35 If the vascularity decreases within the lesion and there is an increase in the resistive index in the feeding vessel, then this can be considered a good response, indicating a successful treatment regimen.
Curr Probl Diagn Radiol, January/February 2006
REFERENCES 1. Rubin JM. Musculoskeletal power doppler. Eur Radiol 1999; 9:S403-6. 2. Rubin JM. Spectral Doppler US. Radiographics 1994;14:13950. 3. Keberle M, Tony HP, Jahns R, et al. Assessment of microvascular changes in Raynaud’s phenomenon and connective tissue disease using colour doppler ultrasound. Rheumatology (Oxford) 2000;39:1206-13. 4. Fornage BD. Role of color Doppler imaging in differentiating between pseudocystic malignant tumors and fluid collections. J Ultrasound Med 1995;14:125-8. 5. Breidahl WH, Stafford Johnson DB, Newman JS, et al. Power Doppler sonography in tenosynovitis: significance of the peritendinous hypoechoic rim. J Ultrasound Med 1998;17: 103-7. 6. Newman JS, Adler RS, Bude RO, et al. Detection of softtissue hyperemia: value of power Doppler sonography. AJR 1994;163:385-9. 7. Newman JS, Laing TJ, McCarthy CJ, et al. Power Doppler sonography of synovitis: assessment of therapeutic response— preliminary observations. Radiology 1996;198:582-4. 8. Breidahl WH, Newman JS, Taljanovic MS, et al. Power Doppler sonography in the assessment of musculoskeletal fluid collections. AJR 1996;166:1443-6. 9. Kirsner RS, Eaglstein WH. The wound healing process. Dermatol Clin 1993;11:629-40. 10. Yu JS, Popp JE, Kaeding CC, et al. Correlation of MR imaging and pathologic findings in athletes undergoing surgery for chronic patellar tendinitis. AJR 1995;165:115-8. 11. Weinberg EP, Adams MJ, Hollenberg GM. Color Doppler sonography of patellar tendinosis. AJR 1998;171:743-4. 12. Ohberg L, Alfredson H. Ultrasound guided sclerosis of neovessels in painful chronic Achilles tendinosis: pilot study of a new treatment. Br J Sports Med 2002;36:173-5; discussion 176-7. 13. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 2001;9:233-8. 14. Chao HC, Lin SJ, Huang YC, et al. Sonographic evaluation of cellulitis in children. J Ultrasound Med 2000;19:743-9. 15. Nazarian LN, Schweitzer ME, Mandel S, et al. Increased soft-tissue blood flow in patients with reflex sympathetic dystrophy of the lower extremity revealed by power Doppler sonography. AJR 1998;171:1245-50. 16. Beiner JM, Jokl P. Muscle contusion injury and myositis ossificans traumatica. Clin Orthop Relat Res 2002;403(suppl): S110-9. 17. Peetrons P. Ultrasound of muscles. Eur Radiol 2002;12:35-43. 18. Strouse PJ, DiPietro MA, Adler RS. Pediatric hip effusions: evaluation with power Doppler sonography. Radiology 1998; 206:731-5. 19. Backhaus M, Kamradt T, Sandrock D, et al. Arthritis of the finger joints: a comprehensive approach comparing conventional radiography, scintigraphy, ultrasound, and contrastenhanced magnetic resonance imaging. Arthritis Rheum 1999; 42:1232-45.
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20. Giovagnoni A, Valeri G, Burroni E, et al. Rheumatoid arthritis: follow-up and response to treatment. Eur J Radiol 1998;27(suppl 1):S25-30. 21. Hau M, Schultz H, Tony HP, et al. Evaluation of pannus and vascularization of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis by high-resolution ultrasound (multidimensional linear array). Arthritis Rheum 1999;42:2303-8. 22. Taylor PC. VEGF and imaging of vessels in rheumatoid arthritis. Arthritis Res 2002;4:S99-107. 23. Teh J, Stevens K, Williamson L, et al. Power Doppler ultrasound of rheumatoid synovitis: quantification of therapeutic response. Br J Radiol 2003;76:875-9. 24. Klauser A, Frauscher F, Schirmer M, et al. The value of contrast-enhanced color Doppler ultrasound in the detection of vascularization of finger joints in patients with rheumatoid arthritis. Arthritis Rheum 2002;46:647-53. 25. Stone M, Bergin D, Whelan B, et al. Power Doppler ultrasound assessment of rheumatoid hand synovitis. J Rheumatol 2001;28:1979-82. 26. Belli P, Costantini M, Mirk P, et al. Role of color Doppler sonography in the assessment of musculoskeletal soft tissue masses. J Ultrasound Med 2000;19:823-30. 27. Alexander AA, Nazarian LN, Feld RI. Superficial soft-tissue masses suggestive of recurrent malignancy: sonographic localization and biopsy. AJR 1997;169:1449-51.
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28. Lagalla R, Iovane A, Caruso G, et al. Color Doppler ultrasonography of soft-tissue masses. Acta Radiol 1998;39:421-6. 29. Kransdorf MJ, Murphey MD. Radiologic evaluation of softtissue masses: a current perspective. AJR 2000;175:575-87. 30. Bodner G, Schocke MF, Rachbauer F, et al. Differentiation of malignant and benign musculoskeletal tumors: combined color and power Doppler US and spectral wave analysis. Radiology 2002;223:410-6. 31. Less JR, Skalak TC, Sevick EM, et al. Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer Res 1991;51:265-73. 32. Schroeder RJ, Maeurer J, Gath HJ, et al. Vascularization of reactively enlarged lymph nodes analyzed by color duplex sonography. J Oral Maxillofac Surg 1999;57:1090-5. 33. Schroeder RJ, Maeurer J, Vogl TJ, et al. D-galactose-based signal-enhanced color Doppler sonography of breast tumors and tumorlike lesions. Invest Radiol 1999;34:109-15. 34. Paltiel HJ, Burrows PE, Kozakewich HP, et al. Soft-tissue vascular anomalies: utility of US for diagnosis. Radiology 2000;214:747-54. 35. van der Woude HJ, Bloem JL, van Oostayen JA, et al. Treatment of high-grade bone sarcomas with neoadjuvant chemotherapy: the utility of sequential color Doppler sonography in predicting histopathologic response. AJR 1995;165: 125-33.
Curr Probl Diagn Radiol, January/February 2006
Applications of Doppler Imaging in the Musculoskeletal System James Teh, BSc, MBBS, MRCP, FRCR
Pathological conditions affecting the musculoskeletal system often result in alterations of regional blood flow. The assessment of a Doppler signal in inflammatory or infective processes complements the grayscale findings, helping to evaluate the severity of disease. Doppler imaging can also be used to determine therapeutic response or help guide injections. In addition, Doppler interrogation enables vascular characterization of solid masses. The presence of a Doppler signal can also help differentiate solid from cystic lesions. This article reviews the wide range of applications for Doppler imaging of the musculoskeletal system.
Ultrasound has an invaluable role in the imaging of the musculoskeletal system, holding an advantage over other cross-sectional modalities in many circumstances due to its superior spatial resolution and ability to allow dynamic assessment. Combining grayscale ultrasound with Doppler imaging allows unique realtime evaluation of regional blood flow, which may be altered in a variety of disease processes. The assessment of Doppler signal in inflammatory or infective processes complements the grayscale findings, helping to evaluate the severity of disease. Doppler imaging can also be used to determine therapeutic response or guide injections. In addition Doppler interrogation enables vascular characterization of solid masses. The presence of Doppler signal can also help differentiate From the Nuffield Orthopaedic Centre, Headington, Oxford, United Kingdom. Reprint requests: James Teh, BSc, MBBS, MRCP, FRCR, Nuffield Orthopaedic Centre, Windmill Road, Headington, Oxford OX3 7LD, United Kingdom. E-mail: [email protected]. Curr Probl Diagn Radiol 2006;35:22-34. © 2006 Mosby, Inc. All rights reserved. 0363-0188/2006/$32.00 ⫹ 0 doi:10.1067/j.cpradiol.2005.10.003
22
solid from cystic lesions. This article will review the wide range of applications for Doppler imaging of the musculoskeletal system.
Basic Physics Doppler shift is the change of frequency in a wave when a source moves relative to the given receiver. An example from day-to-day life is the drop in the pitch of a siren as an ambulance approaches and passes. With ultrasound imaging, the change of frequency detected between the transmitted and received ultrasound frequency is the Doppler shift.
What Is Color Doppler? Color Doppler is real-time imaging with the mean Doppler shift at a specified point depicted in color and superimposed on the grayscale image.
What Is Power Doppler? Unlike color Doppler, power Doppler depicts the total integrated power of the signal in color superimposed on the grayscale image.
What Are the Disadvantages of Color Doppler versus Power Doppler Imaging? The main problems that may arise from using color Doppler for imaging the musculoskeletal system which are not encountered with power Doppler are background noise, aliasing, and angle dependency.1 Background Noise. Color Doppler has a random direction of flow on the image as noise has a random frequency shift. Power Doppler on the other hand has a uniformly low noise. Increasing the gain on color
Curr Probl Diagn Radiol, January/February 2006
FIG 1. (A) Color Doppler US of the lower arm demonstrating the effect of high gain on background noise. (B) Power Doppler US demonstrating true flow on a background of noise. Note the improved visualization of the vessels compared with color Doppler (A). (Color version of figure is available online.)
Doppler increases the noise and thereby the image is degraded. When power Doppler gain is increased, there is a uniformly colored background with an enhanced signal from true flow. The sensitivity and dynamic range of power Doppler is therefore greater than color Doppler (Fig 1). Aliasing. Aliasing is a phenomenon that occurs when an analog signal is sampled at a frequency that is lower than half of its maximum frequency. This causes all the frequencies above half of the sampling frequency (the Nyquist frequency) to be folded back in the low-frequency region. With color Doppler, aliasing may cause vessels to appear discontinuous with possible distortion of direction and speed. Power Doppler is free from aliasing, as the signal is calculated from the integral of the Doppler spectrum. As a consequence, however, power Dopp-
Curr Probl Diagn Radiol, January/February 2006
ler does not display any information on direction and velocity. Angle Dependency. In color Doppler imaging the angle of insonation is crucial to avoid loss of signal and spurious results. The closer the angle of insonation is to 90°, the less the distortion. Power Doppler has the advantage of being relatively independent of angle. As the main interest is in detecting low-velocity microvascular flow in musculoskeletal imaging, power Doppler is generally preferred to color Doppler, although on new ultrasound machines, the difference is often negligible.
Ultrasound Settings Modern ultrasound machines have preset parameters that vary according to the region being examined.
23
FIG 2. Arteriovenous malformation of the thigh. (A) Color Doppler showing a large serpiginous feeding vessel. (B) Spectral Doppler trace confirms phasic, arterial flow. (Color version of figure is available online.)
These settings may require further customization and therefore an understanding of these parameters is necessary.
Sample Volume The sample volume should be kept as small as possible, as a large sample volume results in increased motion sensitivity.
Doppler Gain The bony cortex is a strong specular reflector and spurious Doppler signal may therefore occur at the cortical–soft-tissue interface. The Doppler gain threshold in musculoskeletal imaging should thus be set such that there is no signal seen within bone.2
Color Persistence The level of frame-averaging that occurs in obtaining an image is called persistence. High persistence results in the summation of several frames results in less information on pulsatile flow. A low persistence
24
allows better evaluation of pulsatile flow, but results in a poor signal-to-noise ratio.
Doppler Filter Level The Doppler filter reduces the amount of background noise, resulting in a clearer signal. However, if the filter level is set too high, slow flow may be missed. The filter should therefore be set at the lowest level and then gradually increased until a clear image is obtained.
Doppler Imaging Technique Use the Spectral Doppler Trace The use of a spectral Doppler trace can confirm if the Doppler signal is artifactual, as a phasic waveform should be obtained if there is true flow. Furthermore the spectral trace allows differentiation of arterial from venous flow and allows measurement of parameters such as the resistive index (Fig 2).
Curr Probl Diagn Radiol, January/February 2006
FIG 3. Ganglion. (A) Coronal gradient echo MR image demonstrating a fluid signal mass on the dorsum of the wrist. (B) Power Doppler US shows no internal Doppler signal and posterior acoustic enhancement. (Color version of figure is available online.)
FIG 4. Giant cell tumor of tendon sheath on the flexor aspect of the finger. (A) Extended field of view demonstrating a low echogenicity nodule in a digit. (B) Power Doppler ultrasound shows internal Doppler signal, confirming its solid nature. (Color version of figure is available online.)
FIG 5. Thigh abscess. (A) Extended field of view image demonstrating an echogenic mass in the thigh. (B) Peripheral flow is seen on color Doppler in the wall of the abscess indicating an inflammatory collection. (Color version of figure is available online.)
Curr Probl Diagn Radiol, January/February 2006
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FIG 6. Achilles tendinosis. (A) Power Doppler imaging demonstrates tendon neovascularity (arrows) and retro-Achilles inflammatory change. (B) Axial color Doppler image demonstrates flow within the tendon. (Color version of figure is available online.)
FIG 7. Lateral epicondylitis. Power Doppler demonstrates increased vascularity at the common extensor origin indicating tendinosis. (Color version of figure is available online.)
Use the Correct Angle of Insonation The angle of insonation is of particular importance when using color Doppler. To ensure an accurate representation of blood flow, the angle should be greater than 60°, which can be achieved by angling either the probe or the sample box. One of the advantages of power Doppler is that it is not angle dependent.
Use Light Transducer Pressure If the soft tissues are compressed, the vascular structures can become compromised, leading to an underestimation of blood flow. Ideally minimal transducer pressure should be exerted while still maintaining good contact. The most effective way to achieve this is to use copious jelly.
state of contraction. For example, when performing Doppler assessment of the patellar tendon, the knee should be extended rather than flexed.
Use Doppler for Dynamic Localization The motion sensitivity of Doppler imaging can be advantageous. For example, flexing the great toe may help localize the flexor hallucis longus tendon at the ankle.
Ensure a Constant Ambient Temperature The ambient temperature may affect regional blood flow.3 Serial scans should therefore ideally be performed in the same environment. A temperature-controlled water bath may be useful if an extremity is to be serially scanned.
Examine Structures in a Relaxed State
Compare with the Normal Side
Blood flow can be underestimated due to compression of vessels if a tendon or muscle is examined in a
Comparing the normal opposite limb is useful if there is uncertainty regarding the significance of Doppler flow.
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Curr Probl Diagn Radiol, January/February 2006
FIG 8. Wrist flexor compartment tenosynovitis. There is marked synovial hypertrophy with increased flow on power Doppler. Note that the tendon itself appears relatively normal. (Color version of figure is available online.)
FIG 9. Granuloma surrounding a rose-thorn foreign body in the finger tip. (A) Grayscale ultrasound demonstrates a well-defined low-signal mass around a linear foreign body. (B) Extensive neovascularity on power Doppler ultrasound indicating a solid granuloma rather than an abscess. (Color version of figure is available online.)
FIG 10. Acute myositis in fibrodysplasia ossificans progressiva. (A) Extended field of view in the transverse plane showing marked swelling of the left rectus abdominis muscle (arrows) compared with the normal right side (arrowheads). (B) Increased flow is seen on color Doppler interrogation indicating an acute myositis. (Color version of figure is available online.)
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FIG 11. Carpal synovitis in psoriasis arthritis. Synovial hypertrophy and neovascularity at the carpus demonstrated power Doppler. (Color version of figure is available online.)
FIG 12. Infective arthritis of the elbow. (A) Extended field of view scan showing effusion and synovial hypertrophy. (B) Power Doppler demonstrates increased flow in a region of synovial hypertrophy. (Color version of figure is available online.)
Clinical Applications Distinguishing Solid from Fluid-Containing Structures Cysts or fluid-containing lesions are usually anechoic with posterior acoustic enhancement and no internal Doppler signal (Fig 3). Compressibility may be a feature. However, the presence of low-level internal echoes may make differentiation between a low-echogenicity solid mass and an echogenic fluid collection difficult. Under these circumstances, the
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presence of internal Doppler signal allows confirmation of a solid lesion4 (Fig 4). Similarly synovial hypertrophy can be differentiated from synovial fluid by the presence of Doppler signal.5
The Use of Doppler in Musculoskeletal Disorders Detailed structural information can be obtained by grayscale imaging but the addition of Doppler allows a more functional assessment, demonstrating disease activity and often confirming the diagnosis. Increased
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FIG 13. (A and B) Metacarpophalangeal synovitis in rheumatoid arthritis. Power Doppler pre- and poststeroid therapy, respectively, showing a decrease in Doppler signal post-therapy, corresponding to clinical improvement. (Color version of figure is available online.)
Doppler signal may be generated by increased vascularity, increased perfusion, or hyperemia, which may occur in a variety of inflammatory, traumatic, degenerative, and neoplastic conditions.6,7 Differentiating Inflammatory from Noninflammatory Collections. Grayscale sonography is usually unable to distinguish inflammatory from noninflammatory collections. With Doppler imaging, however, increased blood flow may be seen around inflammatory collections8 (Fig 5). It should be noted that Doppler imaging is unreliable for distinguishing between infective and noninfective collections and that chronic, walled-off abscesses and tuberculous cold
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abscesses may not demonstrate surrounding increased flow. Trauma. After soft-tissue injury, wound healing occurs in three main phases,9 as follows: The inflammatory phase, during which there is coagulation and leukocyte migration; the proliferative phase, when there is angiogenesis and fibrous proliferation; and the remodeling phase, when the tissue attempts return to its preinjury phenotype. After soft-tissue injury, increased Doppler signal may therefore be seen as part of a normal healing response. Tendon Disease. Tendinosis is a degenerative condition resulting from chronic repetitive trauma, char-
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FIG 14. Glomus tumor of the finger pulp. These are small highly vascular soft-tissue tumors that involve the neuromyoarterial glomus, usually in the fingertip or nail-bed. They present with exquisite tenderness, which may fluctuate with ambient temperature. (A) Grayscale ultrasound shows typical position of the mass in the finger pulp. (B) Color Doppler shows a hypervascular mass. (Color version of figure is available online.)
FIG 15. Synovial sarcoma of the foot. (A) Axial T2-weighted fat-saturated MRI demonstrating a lobulated high signal mass (arrowheads). (B) Power Doppler image demonstrating an anarchic vessel pattern with caliber changes and branching vessels. (Color version of figure is available online.)
acterized by loss of normal architecture, microtears, and tenocyte hyperplasia with angiogenesis.10 Doppler interrogation may reveal neovascularization, which occurs as part of a chronic reparative process11 (Figs 6 and 7). Sclerosing the vessels in tendinosis may help alleviate symptoms, suggesting that angiogenesis is related to the pathogenesis of pain.12,13 Tenosynovitis is an inflammatory or infective process characterized by low-echogenicity synovial hypertrophy and/or fluid in the synovial sheath. The tendon may appear normal or thickened. Doppler can reveal the relative proportion of vascularized synovium to fluid5 (Fig 8).
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Cellulitis. Cellulitis is characterized by thickening and induration of the skin and subcutaneous tissues.14 On ultrasound there is loss of normal architecture of the subcutaneous fat, with increased echogenicity and poor ultrasound penetration. Increased blood flow in the thickened tissues may be used to differentiate the edema of cellulitis from fluid overload. Inflammatory masses and granulomas may be also be distinguished from abscesses by the presence of internal Doppler signal (Fig 9). Posttraumatic regional pain syndrome or reflex sympathetic dystrophy is a painful condition comprising hyperesthesia and vasomotor disturbance. Eventually
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FIG 16. Ewing’s sarcoma of femur. (A) Large lobulated mass with anarchic vessel pattern demonstrating trifurcations. (B) Conventional radiograph showing a large mass with cortical destruction and ossification. (Color version of figure is available online.)
FIG 17. Benign nerve sheath tumor. (A) Low echogenicity mass with dural tail (arrows). (B) Simple nonbranching vessel in the mass shown on power Doppler. (Color version of figure is available online.)
it may lead to muscle atrophy and trophic skin changes. Doppler may reveal increased flow in the skin and subcutaneous tissues of these patients.15 Muscle Inflammation. Myositis can be the result of a variety of disease processes including autoimmune disease, infection, and trauma. The normal muscle architecture is disrupted with edema, swelling, and increased blood flow on Doppler imaging (Fig 10). The ultrasound appearances, however, are usually nonspecific and biopsy may be required for diagnosis. Muscle contusion may be followed by myositis ossificans.16 During the initial inflammatory phase, there may be muscle edema with increased flow on Doppler imaging. Echogenic foci may be seen, indicating mineralization. This phase is followed by progressive calcification starting in the periphery, which matures into ossification. Once ossification is mature,
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there is usually no evidence of increased flow. The lesion may eventually diminish in size and resorb.17 Synovitis. Synovitis may occur with infective, degenerative, or inflammatory arthropathies. Grayscale sonography reveals low-echogenicity material within the joint, which may indicate fluid or synovial hypertrophy (Fig 11). Although Doppler imaging is useful for confirmation of inflammatory change, it is unhelpful in differentiating between infective and noninfective conditions18 (Fig 12). Furthermore, it should be remembered that the absence of periarticular flow on Doppler does not exclude septic arthritis. Early Detection of Inflammatory Arthropathy. Ultrasound has an established role in detecting early synovitis and erosions in inflammatory arthropathy.19-21 The erosive phase of rheumatoid arthritis is preceded by production of pannus, which is associated
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FIG 18. Hemangioma overlying trapezius. (A) Extended field of view demonstrating a heterogeneous ovoid mass. (B) Color Doppler demonstrates slow-flowing large-caliber vessels. (Color version of figure is available online.)
with angiogenesis.22 The early detection of vascular pannus therefore has an important role in determining if and when disease-modifying drugs should be introduced. In patients with established inflammatory arthritis, the degree of blood flow in areas of synovitis is greater during exacerbations.21,23 The use of a microbubble ultrasound contrast agent can improve the detection of intraarticular blood flow at finger joints,24 but in practice, contrast is not routinely required. Monitoring Therapeutic Response. Monitoring therapeutic response has a key role in evaluating the effectiveness of different treatments for inflammatory rheumatological conditions. Traditionally, the clinical
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examination, self-assessment questionnaires, and serological markers of inflammation such as the ESR have been used to assess response to treatment, but these methods are not always reliable. Several researchers have therefore used Doppler ultrasound to qualitatively monitor therapeutic response.7,25 Using techniques such as flow mapping, Doppler signal can also be quantified. As long as the Doppler settings are unchanged, serial studies can be used to objectively quantify response to treatment23 (Fig 13). One of the difficulties with using ultrasound for serial studies is that exact repositioning of the probe may be difficult to achieve even with the scrupulous use of landmarks. Tumor Characterization. Ultrasound is often the first imaging modality used in the investigation of
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musculoskeletal soft-tissue masses. It provides a quick and effective means of confirming the presence of a lesion, and providing valuable information on the site, size, morphology, and anatomical relations. Certain benign lesions, such as superficial lipomas and glomus tumors, have a characteristic appearance on ultrasound26 (Fig 14). Grayscale ultrasound however cannot reliably distinguish malignant from benign masses.26-29 Using a combination of color and power Doppler imaging with spectral wave analysis, researchers have attempted to differentiate benign from malignant lesions.30 The vessels in malignant tumors have an irregular margin and lack a muscle layer. With Doppler imaging, these vessels often demonstrate an anarchic pattern, with occlusions, stenoses, arteriovenous shunts, and loops31 (Figs 15 and 16). Benign tumors tend to have a simple branching vascular morphology (Fig 17). The morphologic analysis of tumor vessels appears to be more reliable than quantitative parameters such as flow velocities or resistive indices.32,33 Although meticulous Doppler examination may help differentiate benign from malignant lesions, in practice, a cautious approach should be taken as not all malignant soft-tissue tumors have an anarchic pattern. Furthermore some necrotic lesions and low-grade neoplasms may not demonstrate neovascularity and therefore the absence of flow does not necessarily indicate benignity. Ultimately, ultrasound is unable to provide a histological diagnosis, which can only be obtained by biopsy. Soft-tissue vascular anomalies are usually easily recognized by a combination of grayscale and Doppler imaging. The presence of a solid component can help distinguish hemangiomas from arteriovenous malformations34 (Fig 18). Hemangiomas however have a very variable appearance, sometimes showing no flow on Doppler imaging.34 Arterial flow characteristics and vessel density have been shown to be similar in hemangiomas and arteriovenous malformations. In the latter however there is a significantly higher mean venous peak velocity (Fig 2). Doppler ultrasound has also been shown to be useful in assessing response of tumors such as Ewing’s sarcoma and osteosarcoma to chemotherapy.35 If the vascularity decreases within the lesion and there is an increase in the resistive index in the feeding vessel, then this can be considered a good response, indicating a successful treatment regimen.
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