Ultrasound in American Rheumatology Practice ... - Wiley Online Library

Arthritis Care & Research Vol. 62, No. 9, September 2010, pp 1206 –1219 DOI 10.1002/acr.20241 © 2010, American College of Rheumatology

SPECIAL ARTICLE

Ultrasound in American Rheumatology Practice: Report of the American College of Rheumatology Musculoskeletal Ultrasound Task Force AMERICAN COLLEGE OF RHEUMATOLOGY MUSCULOSKELETAL ULTRASOUND TASK FORCE

Introduction The current status of American rheumatologists with respect to the use of musculoskeletal ultrasound (US) considerably trails that of European peers. In Europe, the development of US applications by rheumatologists began nearly 2 decades ago (1). US is now routinely used by many European rheumatologists (2); however, only a few American rheumatologists use the technique regularly in their practices. This nascent interest is showing signs of maturing. In a recent survey of American College of Rheumatology (ACR) members and rheumatology fellows, 360 of 562 respondents replied that they utilize US, with 122 performing it themselves. (3). A number of factors drive rheumatologists’ interest in US. Since the first reported application of US to musculoMembers of the American College of Rheumatology Musculoskeletal Ultrasound Task Force are as follows: Robert Ike, MD: University of Michigan Health System, Ann Arbor; Erin Arnold, MD, William Arnold, MD: Illinois Bone and Joint Institute, Morton Grove; Jurgen Craig-Muller, MD: CentraCare Clinic, St. Cloud, Minnesota; Gurjit Kaeley, MBBS: University of Florida, Gainesville; Timothy McAlindon, MD, MPH: Tufts Medical Center, Boston, Massachusetts; Levon Nazarian, MD: Jefferson Medical College, Philadelphia, Pennsylvania; Antonio Reginato, PhD, MD: Brown University and Massachusetts General Hospital, Boston. The American College of Rheumatology is an independent, professional, medical and scientific society which does not guarantee, warrant, or endorse any commercial product or service. Dr. Ike has received consultant fees, speaking fees, and/or honoraria (less than $10,000) from Genzyme. Dr. CraigMuller is employed by CentraCare Rheumatology. Dr. Kaeley’s work was supported by an unrestricted equipment loan from Biosound Esaote and Sonosite. Dr. Reginato’s work was supported by a grant from the Robert Wood Johnson Foundation and he has received consultant fees, speaking fees, and/or honoraria (less than $10,000 each) from UCB, Takeda, URL Pharma, and Centocor. Address correspondence to Robert Ike, MD, Department of Internal Medicine, Division of Rheumatology, University of Michigan Health System, 1500 East Medical Center Drive, 3918 Taubman Center, Ann Arbor, MI 48109-0358. E-mail: [email protected]. Submitted for publication December 31, 2009; accepted in revised form April 19, 2010.

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skeletal diagnosis in 1972, differentiating Baker’s cysts from deep venous thrombosis (4), investigation of a wide range of pathologies affecting soft tissue and bone have demonstrated distinct US characteristics (5,6). Highquality machines produce sharply-defined images with a high degree of spatial resolution that have replaced the vague gray shadows of early US scans. Also, power Doppler capabilities showing blood movement in the microvasculature can serve as a surrogate marker for detecting local inflammation (7). US is patient friendly, noninvasive, radiation free, and relatively inexpensive when compared with other imaging modalities. It is directly applicable at the time of a patient’s visit, is capable of showing the relationships of structures during movement, can examine multiple joints in a single visit, and is readily repeatable. At the point of care, the clinician can gain an understanding of the patient’s unique structural pathology, describe the problem, and outline possible solutions. Besides enhancing the clinician’s physical examination skills, US holds tremendous promise in disease management, enabling both assessment and monitoring of inflammatory arthropathies. These are increasingly important capabilities, given the modern clinical goals of increasing emphasis on early identification of synovitis, implementing ever more effective (if expensive) treatments, and monitoring the effects of those treatments. While magnetic resonance imaging (MRI) has been proposed as a sensitive technique for monitoring disease (8), US may prove to be an attractive alternative in many cases. US is a technique that has near-equivalent accuracy to MRI in identifying many of the relevant pathologies in rheumatology, yet carries practical advantages such as far lower cost and portability. Obstacles remain that impede implementation of US in American rheumatology practices. Learning opportunities beyond introductory courses remain sparse, with the only path to acquiring added skills being self-directed efforts with a steep curve leading to implementation in the clinic, since preliminary hands-on practice is time consuming. To date, standards are lacking for what constitutes competence in this operator-dependent technique. In addition, not all radiologists agree that US should be within the purview of rheumatologists (9). Practically speaking, clin-

Ultrasound in American Rheumatology Practice ical use of US requires additional time, space, and data management capabilities that can challenge a busy rheumatology practice. The ACR Committee on Rheumatologic Care established a task force to address issues of musculoskeletal US as they may relate to American rheumatology practice. Members included American musculoskeletal US specialists from both academia and private practice, plus an experienced musculoskeletal radiologist. A “state-of-the-art” review was not created, given the existence of several excellent, extensive, and recently-published articles (6,7,10 –27). The ACR Musculoskeletal Ultrasound Task Force focused on the primary constituency of the ACR: the American rheumatologist considering US as an addition to his or her practice and needing related information. As a summary of the larger report, this manuscript describes some technical aspects of US and its capabilities, considers how implementation of US might impact clinical practice, and addresses educational issues.

Technical aspects of US Basics of US physics. US images are produced by sound waves with frequencies above 20 kHz, approximately the limit of human hearing, with a range of 2–20 MHz used for medical imaging. Waves are produced by piezoelectric elements in the transducer of the instrument that emit pulses of US waves of a specific frequency when electrically stimulated. Each pulse or US beam traverses a straight path until striking a tissue interface with differing acoustic impedances, after which an echo is reflected back to the transducer, generating the electric signals that provide the display image. Reflected echo intensity is proportionate to the amount of difference between tissue impedances at that interface, mainly due to differing water content in tissues, which provide the signals that define the edges of images. Intense echoes, such as from bone, calcium deposits, or metal appear whiter or “hyperechoic;” whereas weaker echoes from fluid or muscle make a darker, more “hypoechoic” image. Depth is also mapped. The longer it takes for the echo to return to the transducer, the deeper the echo will be mapped on the US image, producing the dimensional structure of the picture. Because the transducer sends out multiple scan lines simultaneously from many piezoelectric elements, a 2-dimensional (2-D) brightness mode (Bmode) gray-scale image is produced. Images appear to occur in real time, due to signal repetition at a rate of 20 – 40 times per second (28). Three-dimensional (3-D) images can be produced by transducers sending signals through multiple paths; early utilizers of this technique suggest that this advanced but costly processing allows the physician to see more detailed images with less operator effort (24). Frequencies required for musculoskeletal US. Higher frequencies yield better image resolution at the expense of depth penetration. Much lower frequencies can visualize a deep structure, such as a hip. Current transducers scan at multiple frequencies, so multiple transducers with differ-

1207 ent frequency ranges are no longer necessary. For example, a broadband 12-5 MHz transducer with a peak frequency of 12 MHz yields the best near-field resolution, while the 5 MHz frequency penetrates deep structures. Most useful for musculoskeletal US are linear array transducers with inline piezoelectric elements and a flat probe surface. This configuration provides optimal near-field imaging. It also helps avoid the phenomenon of anisotropy, where nonperpendicular US beams deflect away from the transducer when striking a smooth, “specular” (mirror-like) reflector such as tendon fibers, creating an artifact that appears black (29). Importance of color Doppler. Color flow Doppler US adds to the gray-scale evaluation of musculoskeletal structures by assessing blood flow. The frequency of a US pulse reflected from moving objects, such as erythrocytes, shifts higher if the objects are moving toward the transducer and lower if the objects are moving away. The signal magnitude is proportional to the object’s velocity (30). Doppler information can be depicted in one of several ways. In spectral Doppler, the frequency shift is plotted on a graph as a function of time. In color Doppler, the mean frequency shift is mapped in color onto the 2-D B-mode gray-scale image, with red or blue indicating flow direction, and color intensity representing velocity. In power Doppler, also called color amplitude imaging or energy mode Doppler imaging, the image intensity only depicts the total amplitude of frequency-shifted information received by the transducer, without velocity or directional information. In other words, the more erythrocytes there are causing a power Doppler shift, the stronger the signal (30). Comparative strengths of sensitivity between color Doppler and power Doppler are manufacturer dependent. Figure 1 demonstrates an example of RA synovitis shown by color Doppler in an affected metacarpophalangeal (MCP) joint. Additionally, use of Doppler during USguided procedures can help reduce vascular complications by locating blood vessels to avoid. Ways to quantify and enhance Doppler signals continue to be developed. There is semiquantitative power Doppler, based on the estimated number of blood vessels in a defined area (31). There is another method based on the resistive index, which promises to be a more precise measure of synovitis (32). Lastly, there is a method based on signal amplification through the use of US contrast agents with microencapsulated air bubbles that increases Doppler sensitivity, which is widely used in Europe but is not currently approved by the Food and Drug Administration (33). Color or power Doppler can identify low velocity bloodflow states that occur in inflamed sites. However, increased microvascular blood flow can also identify sites of injury and tissue repair in nonarthritic situations. Blood flow is influenced by conditions like room temperature, body temperature, physical activity, or alcohol consumption. These factors, as well as Doppler gain (if set too high), must be considered during any examination because they can provide artifactual signals (34).

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Figure 1. Metacarpophalangeal joint in a rheumatoid arthritis patient with active synovitis. Left image shows gray-scale ultrasound features, with area of synovial thickening highlighted. Right image shows power Doppler signal with increased flow in area of joint consistent with active synovitis. Images acquired with 12-7 Hz variable transducer on LogiqE ultrasound machine (GE) (courtesy of Drs. William J. Arnold and Erin L. Arnold).

US visualization of musculoskeletal structures Knowledge base in structural visualization. There is an extensive bibliography covering the musculoskeletal structures and anatomic sites that US can image, as well as definitions of structures (35) and pathologies involved (5) (Tables 1 and 2). A US special interest group, formed in 2004 under the auspices of OMERACT/EULAR (Outcome Measures in Rheumatology Clinical Trials/European League

Against Rheumatism), has worked to define the validity and reliability of US assessments. This group has developed a consensus set of definitions for pathologies seen in inflammatory joint diseases (36) (Table 3), and has stimulated systematic reviews of US assessments (37) and reliability studies (38). US reproducibility in diagnostic testing. Numerous studies testing the reproducibility of US diagnoses and

Table 1. Upper extremity pathologies identified by musculoskeletal ultrasound* Shoulder

Elbow

Wrist

Hand

Axillary recess Effusion Synovial proliferation Osteochondromatosis Rotator cuff Tear Calcific tendonitis Bursitis Subacromial Subdeltoid Cartilage lesions Calcifications Humeral head Bony lesion (erosion, osteophyte) Irregular contour Acromioclavicular joint Synovial proliferation Effusion Dislocation Loose body Deltoid muscle Hematoma Tear Biceps Tear Tenosynovitis Effusion Dislocation

Humeroradial and humeroulnar joints Synovial proliferation Effusion Bony lesions Loose joint body Lateral/medial epicondylitis Olecranon fossa Bursitis Synovial proliferation Olecranon bursa Bursitis Subcutaneous tissue Tophi Rheumatoid nodule Ulnar nerve Structural change Compression

Radioulnocarpal joint Synovial proliferation Effusion Calcifications Bony lesions Ganglion Triangular fibrocartilage Carpal tunnel Tenosynovitis Structural changes Ganglion Extensor tendons Tenosynovitis Structural changes Ganglion Rheumatoid nodule

Joints Effusion Synovial cysts Synovial proliferation Cartilage thinning/lesions Bone lesions erosion, osteophytes Ganglion Articular dislocation Periarticular lesions Calcinosis Crystal deposition Rheumatoid nodules Tendons Tenosynovitis Tendonitis Tear

* Adapted, with permission, from ref. 5.

Ultrasound in American Rheumatology Practice

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Table 2. Lower extremity pathologies identified by musculoskeletal ultrasound* Hip

Knee

Ankle

Foot

Joint effusion Synovial proliferation Osteochondromatosis Bursa Trochanteric Iliopectineal Bony lesion Erosion Osteophyte Irregular bone surface Slipped capital femoral epiphysis Cartilage lesion Calcifications Infection Loose prosthesis Loose body

Supra/parapatellar pouch Synovial proliferation Synovial folds Effusion Quadriceps tendon Tear, partial/complete Enthesopathy Femoropatellar joint Irregular contours Bony lesions Popliteal sulcus Bursitis Synovial proliferation Patellar ligament Tear, partial/complete Enthesopathy Deep infrapatellar bursa /subcutaneous prepatellar bursa Bursitis Tuberosity of tibia Irregular bony contour Infrapatellar bursitis Ligaments Tear or lesion Meniscus, lateral/medial Lesion or cyst Popliteal fossa Popliteal cyst Vessel compression

Talocalcaneonavicular joint Synovial proliferation Effusion Cartilage lesions Bony lesions Loose joint bodies Osteochondromatosis Muscles tibialis anterior/ posterior, peroneus Tenosynovitis Tear Achilles tendon nodules Tophi Rheumatoid Xanthomas Achilles tendon Calcification Tear Tendonitis/paratendonitis Enthesopathy Bursitis, retrocalcaneal/ superficial

Joints Effusion Synovial proliferation Cartilage lesions Bone lesions erosion, osteophytes Subcutaneous tissue Gout tophi Plantar fascia Plantar fasciitis Tendons Tenosynovitis Tear Enthesopathy Calcaneus Calcification plantar fascia Ossification calcaneus spur Bony lesions Erosions

* Adapted, with permission, from ref. 5.

measurement of musculoskeletal abnormalities show that there are generally high levels of reliability for US assessments (39 – 47). Given ultrasonographer credentials that include a range of experience levels and training, the data reveal an effect of operator experience on US precision and reproducibility. Although one study of OA found markedly variable levels of reproducibility among operators who had little to no training (40), others indicate that adequate reproducibility can be achieved by those who are not radiologists after relatively short training periods (41– 44). For example, when an experienced musculoskeletal ultrasonographer was compared with a rheumatologist whose US training consisted of a 3-hour course in hip US, they closely agreed on measurements of anatomic structures, as well as placement of target objects in a hip model (42). In another study, hip OA scores assigned to 100 patients by both a US specialist and a US-trained rheumatologist showed high concordance for global osteoarthritis (OA) and synovitis (43). Rheumatoid finger measurements evaluated by either an experienced musculoskeletal radiologist or a rheumatologist with limited US training had high absolute concordance, at 79 –91%, with acceptable correlation coefficients (47). A similar comparative study showed good reliability for US-detected erosions (48). Lastly, in an 8-patient examination exercise comparing US evaluations by highly experienced, formally trained

international rheumatologists with those done by selftaught American rheumatologists, both groups were able to differentiate among disease categories most of the time, but had equal difficulty with more specific disease diagnoses. The interreader reliability for detecting structural abnormalities was found to be fair for both groups, but it was slightly higher among the international rheumatologists (49).

US performance as a diagnostic test: validity Performance comparisons. The validity of US clinical assessments and anatomic measurements has been evaluated in a number of studies by comparing US with another imaging modality, clinical examination, and/or pathologic findings. US versus MRI. Many studies have compared US with MRI. Anatomic locations include the shoulder (41,45), forearm (50), wrist/finger (41,48,51), knee (41,49), and ankle/toe (41,51–53), while pathologies include rheumatoid arthritis (RA) (45,48), psoriatic arthritis (52), and tendon tears (52,53). One study of regional assessments showed a high level of concordance between US and MRI findings at the shoulder and knee, but less for the wrist/ finger and ankle/toe regions (41). In a rheumatoid shoulder study, agreement ranged from 31– 84% for various pathol-

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Table 3. Definitions of musculoskeletal pathologies shown by US in inflammatory joint diseases (OMERACT)* Pathology

Definition

RA bone erosion

An intraarticular discontinuity of the bone surface is visible in 2 perpendicular planes Abnormal hypoechoic or anechoic intraarticular material (relative to subdermal fat, but sometimes may be isoechoic or hyperechoic)† Displaceable, compressible, but without Doppler signal Abnormal hypoechoic (relative to subdermal fat, but at times may be isoechoic or hyperechoic) intraarticular tissue that is nondisplaceable and poorly compressible, which may exhibit Doppler signal Hypoechoic or anechoic thickened tissue, with or without fluid within the tendon sheath, seen in 2 perpendicular planes‡ May give Doppler signal Abnormally hypoechoic (loss of normal fibrillar architecture) and/ or thickened tendon or ligament at its bony attachment (may occasionally contain hyperechoic foci consistent with calcification), seen in 2 perpendicular planes that may exhibit Doppler signal and/or bony changes, including enthesophytes, erosions, or irregularity

Synovial fluid

Synovial hypertrophy

Tenosynovitis

Enthesopathy

* US ⫽ ultrasound; OMERACT ⫽ Outcome Measures in Rheumatology Clinical Trials; RA ⫽ rheumatoid arthritis. † Isoechoic: US signal similar to surrounding tissues. ‡ Anechoic: no US signal generated, visualized structure appears black.

ogies (45) and was highest for erosions and cuff tears. US assessment of OA knees in which MRI-detected effusion or synovial thickening identified nearly all effusions and approximately 66% of joints with synovial thickening (49). In one tendon lesion study (52), dynamic US had slightly lower sensitivity than MRI, while in another they were judged not significantly discrepant to alter clinical judgment (53). In a comparative erosion study, both psoriatic erosions and osteoproliferation were seen more by US than MRI (51). In patients with clinical heel enthesitis, US was superior to MRI in detecting early features of Achilles tendonitis and plantar fasciitis (54). In a study of MRIidentified retro-Achilles bursitis, US was deemed only 50% sensitive, but 100% specific (55). US versus radiography. Studies comparing these imaging modalities focus on rheumatoid erosions and occult fractures. US had greater sensitivity in detecting these pathologies, finding 2– 4 times more erosions than did radiographs. These differences were greatest in early dis-

ease (48,56). US was far superior to radiographs in detecting psoriatic arthritis pathologies, with the exception of osteoproliferation (51). Also, US detected fractures of the calcaneus (57), sternum (58), and scaphoid (59) in at-risk patients with normal radiographs. US versus clinical diagnosis. Several studies have examined the utility of US as an adjunct to clinical examination. In a study of rheumatoid finger and toe joints, US showed signs of inflammation in nearly 50% more joints than physical examination determined were tender or swollen (46). In patients with early oligoarthritis, US detected synovitis in 33% of painful joints that were not clinically inflamed, and 13% of asymptomatic joints (60). In joints exhibiting clinical synovitis, US confirmed the diagnosis in 79% of cases, suggested synovitis in 6% more, found tenosynovitis instead of synovitis in 7%, but declared that 8% were normal. Almost 66% of those study patients had subclinical disease detectable by US. Compared with physical examination in rheumatoid knees, US found ⬃5 times more Baker’s cysts, more than twice as much suprapatellar bursitis, and nearly one and a half times more effusions (61). With active enthesitis defined by US as the gold standard in one study, local tenderness was ⬃72% sensitive and 63% specific overall (62). US versus pathology. US assessment of anatomic structures correlates well with features on gross inspection. For example, in a study of cadaveric MCP joints, intricate structural characteristics seen by US, such as the sagittal bands of the extensor hood and first annular pulley, were confirmed on gross inspection. US could differentiate small benign depressions on the metacarpal heads from true erosions (46). US has accurately predicted the location, size, and thickness of supraspinatus tears seen at surgery (63). Also, US predicted supraspinatus tendon pathology seen at arthroscopy. US features of greater tuberosity, irregularity, and joint fluid predicted full-thickness tears. A combination of tendon nonvisualization, cortical irregularity, and a cartilage interface sign were associated with tendon disruptions (64). Several US shoulder dimensions matched well to direct measurements, including cartilage thickness (65), biceps tendon diameter (66), and capsular distension (67). US images of synovitis correlate well with features seen on gross and microscopic inspection. In knees examined clinically by US and then arthroscoped, US could identify synovial proliferation in a highly sensitive, specific, and accurate manner that proved far better than a clinical examination (68). In patients with unexplained arthritis or tenosynovitis who were referred for synovial biopsy, power Doppler identified edema or synovial proliferation in most instances. A positive Doppler signal was obtained in ⬃83% of cases with active synovitis. Doppler signal did correlate with subsynovial infiltration of polymorphonuclear leucocytes and surface fibrin, but not overall histopathology (69). Finally, US works well as a method of assessing vascularity, alone or with enhancers. Semiquantitative power

Ultrasound in American Rheumatology Practice Doppler scores prior to arthroplasty correlated with observed vascularity in synovial histopathology (70). In arthritic rabbit knees, microbubble contrast agent– enhanced power Doppler signals correlated with microvessel density in synovitis (71).

Potential impact of US on clinical practice The undiagnosed case. In patients with musculoskeletal pain, an initial step in diagnosis is to determine the anatomic source of the symptom and the nature of the pathology at that site. US can discern, with some precision, many relevant features of the process. For example, bursitis, various tendonopathies (including tears), tenosynovitis, and effusions of the acromioclavicular and glenohumeral joints can be distinguished on US, helping to identify soft tissue pathologies associated with shoulder pain (12). US can change a site-specific diagnosis. In one study, approximately one-half of the patients referred for injection of a certain region had US reveal that a different area was affected, most often when the foot was involved (72). On occasion, undiagnosed vague symptoms can be identified as true arthritis with US, allowing the clinician to focus further diagnostic and therapeutic efforts. On occasion, features identified at an affected site can have diagnostic implications, such as when prominent enthesopathy supports a diagnosis in the spondylarthropathy family (20). Visualization of various crystal-associated arthropathies can infer a diagnosis, even prior to radiographs or synovial fluid analysis. A tendon considered inflamed by clinical examination can instead show features of damage or overuse, such as partial tears (73). US assessment does not obviate the need for other imaging modalities. If certain anatomic pathology cannot be discerned from office US, referral to an experienced radiologist for MRI, or even further US imaging, for clarification is appropriate. Inflammatory arthropathies. US can detect inflammation before the clinical examination discerns such processes, finding synovial thickening or increased signal on power Doppler (7), and can identify subclinicallyinflamed joints (60). US detects many effusions missed by clinical examination (61). The diagnosis and management of inflammatory arthropathies can be influenced by US findings such as identification of the existence, type, and severity of synovial disease and visualization of the consequences of synovitis. For the elbow, ankle, and wrist, US can clarify a clinical examination that is unable to discern a joint effusion from tenosynovitis or other enthesopathies (13,16,17). Data from US studies examining joint inflammation suggest that clinical evaluation may underestimate inflammatory disease activity. In a study of RA patients using MRI as the gold standard, US found almost double the small joint synovitis than clinical assessment, with increased sensitivity coming without loss of specificity (74). In another study examining responses to infliximab, US baseline synovitis scoring could discern high and low response groups with greater sensitivity than conventional radiographic or clinical evaluation (75). In patients otherwise

1211 judged to be in complete clinical remission, US identified a patient subset with ongoing synovitis and a high likelihood of 2-year followup progression on radiography (76). Therefore, periodic US assessment of key joints, analogous to a clinical joint count, could become increasingly important in monitoring therapies. Regional flares in the established patient can provide the same sort of dilemmas as in the undiagnosed patient. US can usually discern whether a site is swollen because of effusion, synovial hypertrophy, adjacent soft issue swelling, tendonitis/tendonopathy, tenosynovitis, bursitis, or enthesitis/enthesopathy. In the spondylarthropathy patient, US can identify a swollen finger as dactylitis by showing fluid around the flexor tendon, diffuse extensor region edema, and increased periarticular blood flow (compared with intraarticular hypervascularity in active RA) (77). Semiquantitative scales are now available for enthesitis assessment at several standard sites (78,79). US is far more sensitive than radiography in detecting erosions, but the degree of sensitivity compared with MRI varies, depending on the location of the joint, and is worst in anatomically complicated joints. For example, US is very good for easily accessible joints such as the second and fifth MCP joints, but is less reliable for the third and fourth MCP joints (53,80). In addition, as is currently done with MRI, US can be used for prognosis, i.e., absence of baseline erosions predicts persistence of an erosion-free state at the 2-year followup (81). Conversely, erosion signs seen with power Doppler correlate strongly with radiographically-confirmed damage progression following a year of disease-modifying antirheumatic drug (DMARD) therapy in early RA (82). US assesses well certain features of juvenile idiopathic arthritis (JIA) otherwise poorly attainable by traditional clinical and imaging methods, including effusion, synovitis, tendonitis, enthesitis, or pannus (83,84). In children, changes in underlying bone do not readily appear by radiograph, since articular cartilage is in continuity with epiphyseal cartilage. As ossification centers develop, epiphyseal cartilage becomes refractile on US and therefore distinguishable from articular cartilage. Many soft tissue features of the knee detectable by MRI can be seen by US, although MRI remains superior at showing cartilage and internal ligament lesions (85). In JIA knees, Doppler US also can be used to assess response to treatment (86). Especially in children, US is more practical than MRI, since it avoids claustrophobia-related issues as well as the occasional need for general anesthesia. Finally, for pediatric transient hip synovitis, US is the imaging procedure of choice (87). Crystal-related arthropathies. Crystal deposition in articular cartilage, soft tissues, and bone produces characteristic US images. Urate crystals generate the “double contour sign,” as US signals reflect off both the crystal-covered cartilage surface and the chondro-osseous junction. The specificity for indicating gout is more than 90% (88). Increasing compaction of tophaceous deposits makes the surface highly reflective, with well-demarcated hyperechoic edges differentiating them from rheumatoid nodules

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(89). Tophi echogenicity diminishes during an inflammatory reaction and the structures become surrounded by fluid. Size of tophi diminishes with effective hypouricemic therapy. US sensitivity to change allows its use in determining outcomes in gout treatment trials (90). “Preclinical” gout can be diagnosed by US, since examination may reveal tophi in approximately one-third of asymptomatic hyperuricemic patients (91). As with rheumatoid erosions, many more gouty erosions are detected by US than by radiography (92). Calcific deposits in joints generate US signals that differ from those seen in gout, and can be seen by US before radiography can detect them. Calcium pyrophosphate dehydrate (CPPD) deposits within, rather than on top of, articular cartilage and usually appears as thin, homogenous, hyperechoic bands in the intermediate layer of hyaline cartilage, parallel to the surface, but they can be nodular or ovoid (93,94). In fibrocartilage and tendons, CPPD appears in a serial, thin, hyperechoic, punctuate pattern (95). Basic calcium phosphate (BCP) deposition appears most commonly in the shoulder, greater trochanter of the hip, lateral epicondyles of the elbow, and wrist tendons (96). Although not reliably distinguished from CPPD, BCP shows up as brightly refractile, globular, and discernible when as small as 2 mm. OA. US investigations in OA confirm that its pathology extends beyond bone and cartilage, showing abnormalities in synovium, entheses, and periarticular soft tissues (19). Some OA features can be detected earlier by US (97). While OA articular cartilage thickness and surface characteristics can be assessed by US, important load-bearing surfaces cannot be reached. In OA, useful diagnostic information comes from seeing US features that induce symptoms, such as crystal deposition or periarticular problems. US is particularly relevant to knee assessments, where it can identify Baker’s cysts, multiple bursae, and tendon pathology.

US as an outcome measure US use in determining outcome measures. US can be used to evaluate and follow disease activity in arthritis. The needs of clinical trials and daily practice differ. For example, contemporary trials evaluate early RA and a large number of joints. Some investigators propose that assessment of activity in a few sentinel joints could adequately reflect disease burden (98). OMERACT has devised a system to evaluate outcome measures in RA (99); the evaluation must assess feasibility, how the evaluation discriminates change, and whether it represents truth in terms of face, content, criterion, and construct validity. Based on the OMERACT filter, several analyses of US literature identify some important pitfalls (100 –104). Earlier studies did not employ standardized image acquisition or definitions of sonographic abnormalities; however, the procedural protocols and consensus sonopathologic definitions developed by the EULAR Musculoskeletal Group (Table 3) will help improve future studies.

Sonographic pathology and outcomes. US can identify erosions and signs of synovitis. Erosions can be described qualitatively by their presence or absence, but several features of synovitis are quantifiable. The quality of the assessment seems to be better at some joints than others. Although investigators have reported scores individually by modality or in a composited manner, it appears to be preferable to report activity and erosion scores both separately and composited. This allows for capture of the reversible components of disease activity and also tracking progression of erosive disease. The extent to which joints have been examined has varied, but a validated consensus model of US examination of MCP joints revealed good reliability when extended to the proximal interphalangeal, metatarsophalangeal, knee, and wrist joints (105). The same group of international experts also reported good intermachine reliability, following US examination of MCP joints (106).

Outcome issues in assessment of pathology, by type Erosions. Correlation of US-defined erosions with those seen on plain radiographs, computed tomography (CT), and MRI indicate reasonable content and criterion validity for US (100 –104). For erosion detection, US is more sensitive than plain radiography (48,107–110) and provides a high degree of reproducibility (47,48). US is comparable to MRI for detecting erosions in joints with good sonographic windows such as the fifth MCP joint, but does not perform as well in wrist joints, where acoustic windows are limited (42,48,110,111). US is more sensitive than radiography at detecting progression of erosions (107,108,112). There are limited data on concurrent histologic validation of erosions identified by US (113). Synovitis. Sonographic indications of synovitis include the ability to detect joint fluid, synovial hypertrophy, and vascularity. These features can also be seen in tendons and extraarticular structures such as tendon sheaths and bursae. The response to therapies has been followed in various ways, and US appears to be quite useful for this. Rapid reduction of the power Doppler signal, mirroring rapid clinical improvement, has been demonstrated in response to systemic glucocorticoid therapy (114,115), intraarticular injections of glucocorticoids (116 –120) and methotrexate (121), short-term biologic therapies (98,122–125), and nonsteroidal antiinflammatory drugs (86). It is possible that functional indices in US may be affected by chronic destructive changes and factors other than synovitis. With respect to reliable reproducibility in longitudinal studies, excellent interobserver and intraobserver reliability was demonstrated in a multicenter study using power Doppler to examine patients treated with traditional and biologic DMARDs (82,126). The predictive value of baseline US findings in estimating future erosive disease has also been evaluated. In one study, both the final Disease Activity Score in 28 joints and radiographically-determined erosion score correlated more strongly with the US synovitis score than with clinical and laboratory variables (82). US is more sensitive

Ultrasound in American Rheumatology Practice than clinical examinations in detecting synovitis in established and early RA (108,127–129). US features suggest that synovitis can persist in patients achieving clinical remission (130,131), suggesting that subclinical synovitis can progress to erosive disease. US examination can discern remission versus low disease activity (76). Synovial fluid. In OA, effusions may forecast outcome of disease. The presence of fluid and lack of osteophytes in hip OA may predict improvement following intraarticular glucocorticoid injection (132). US evidence of knee effusion, in addition to pain and radiologic severity, was found to predict progression to joint replacement (133).

US-guided procedures Blind injections and aspirations guided by external anatomic landmarks do not always enter the joint. When confirmed by arthrography, the accuracy of injection in one study ranged from 29% for subacromial injections to 71% for the knee (134). Even when synovial fluid was obtained, accuracy of subsequent injection was only 45% in one study (135). As accurate placement has been correlated with response to injection (134,136), methods that enhance accuracy should improve efficacy of local injection treatments. Comparisons of accuracy of US-guided injections with conventional methods consistently demonstrate superiority with US. In the hand, approximately 59% of palpationguided injections are placed accurately; however, there is a 96% accuracy rate when using US (137). A similar study involving many different joints demonstrates that 32% of blind aspirations were successfully completed, compared with 97% of US-guided aspirations; for knee aspirations, conventional methods give 40% success, with US providing a 95% success rate (134). This study also found that in joints where a previous blind aspiration was unsuccessful, all could be successfully aspirated using US guidance. US-guided injection has been correlated with response. For 41 patients with painful shoulders who were randomly assigned blind subacromial injections or US-guided ones, the outcome was significantly superior at 6 weeks when US guided (138). For a variety of different joints in 148 patients randomly assigned to receive injections guided either by US or palpation, outcome after US was significantly better than after blind injection. US also found more effusions, permitted collection of a significantly larger volume of synovial fluid, and was associated with far less procedure-related pain (139). The assurance that therapeutic compounds are delivered intraarticularly could prove even more important for biologic substances (e.g., hyaluronates, cytokine inhibitors, growth factors) that would not readily diffuse into the joint from an extraarticular placement, as do corticosteroids. By demonstrating in real time the structures within and around joints, US can not only enhance the safety of injections, but make it possible to access regions often deemed too risky to approach in an office setting. With US, a Baker’s cyst can be aspirated avoiding nearby neurovascular structures (140,141), steroids can be placed into the carpal tunnel away from nerves and tendons (142,143),

1213 and the hip joint can be entered accurately and safely (142,144). In obese patients with indiscernible landmarks, knee aspiration and injection can proceed due to US features indicating location and depth of the target area. Although still challenging to undertake, US-guided injection into the sacroiliac joint (145) and the lumbar facet joints (146) is possible. Although their efficacy compared with more traditionally guided methods has not been assessed, their lower cost and avoidance of radiation exposure could render them preferable to current high-cost measures such as fluoroscopy or CT. For all injections, accurate needle tip placement using US reduces the risk of damage from cartilage contact and from corticosteroid infiltration of tendons and extraarticular soft tissues. Detailed techniques for US-guided injection have been described (147). US can be used to guide penetration in 2 different ways. In a 2-step process, US first defines the coordinates for entry and the target structure depth, but site entry follows without concomitant US visualization. In a 1-step, more challenging method, the operator holds the US transducer in one hand and the needle in the other, obtaining a real-time image of the needle penetrating the structure. This latter method can show the injected material entering the structure, as well. Certain soft tissue disorders have been treated with USguided needle penetration of the affected structure, often followed by injection. For example, with deposits in calcific tendonitis of the shoulder, direct penetration, subsequent lavage, and steroid infiltration have been described as an effective, although technically challenging, intervention in recalcitrant cases (148,149). Techniques for US-guided synovial biopsy (150,151), which are less invasive than arthroscopic or open biopsy, have been described. Use of US assures that abnormal areas are sampled and that structures not readily discernible by clinical examination can be accessed.

Educational considerations Postgraduate training in musculoskeletal US is available to practicing rheumatologists. There are many short introductory-level courses offered in the US and Europe. These courses typically cover equipment use and image acquisition, review musculoskeletal pathologies US distinguishes, discuss US capabilities and findings, and offer some hands-on exposure. Also available are advancedlevel courses in US-guided procedures. Beyond that, selfdirected learning can proceed with input from an experienced ultrasonographer (152). The self-taught model shows promising results, as competence was found to be comparable between self-taught Americans and experienced international ultrasonographers (49). Currently, American rheumatologists have neither an official musculoskeletal US-regulating body nor a certification process in place. A set of UK-based rheumatologists has proposed rigorous, extensive guidelines for US training and has outlined the levels of competence (153–155). These guidelines are not currently used in any formal certification process. The American Institute of Ultrasound in Medicine (AIUM) has recently released the Training Guidelines for the Performance of Musculoskel-

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Table 4. Training guidelines for the performance of MSK US examinations* Physicians performing and/or interpreting diagnostic examinations who have not been trained in radiology should meet the following criteria 1. Completion of an ACGME- or AOA-accredited residency in a specialty practice 2. 100 hours of AMA PRA category 1 credits in MSK medicine, surgery, and/or imaging, of which at least 40 of these 100 hours need to be specific to MSK US 3. At least 1 MSK US course that includes hands-on training, supervision and/or performance, and interpretation. CME credits from course included in 40 hours 4. Reporting of 150 MSK US examinations within the last 36 months Physicians will not need to complete the 60 hours of non-MSK US-specific CME if they are within 2 years of residency and/or fellowship training in a specialty that focuses on MSK medicine and/or surgery Maintenance of competence All physicians performing MSK US examinations should demonstrate evidence of continuing competence in the interpretation and reporting of those examinations. A minimum of 50 diagnostic MSK US examinations per year is recommended to maintain the physician’s skills CME The physician should complete 30 hours of AMA PRA category 1 credits specific to MSK US every 3 years * Online at http://www.aium.org/publications/statements.aspx. MSK ⫽ musculoskeletal; US ⫽ ultrasound; ACGME ⫽ Accreditation Council for Graduate Medical Education; AOA ⫽ American Osteopathic Association; AMA ⫽ American Medical Association; PRA ⫽ Physician’s Recognition Award; CME ⫽ continuing medical education.

etal Ultrasound Examinations (Table 4). While development of these guidelines included input from ACR members, the ACR has not fully accepted the guidelines, which are still problematic and only identify one pathway that is not outcome driven. In an ongoing pilot program at American institutions with available US, rheumatology fellows collect images of normal and pathologic anatomy and submit these for review (Kissin E: unpublished observations). The same trainees are later tested in a hands-on exercise proctored by experienced ultrasonographers. This pilot program will help discern the training required for US competency and begin development of a certification and credentialing process. In many programs, US exposure is part of the curriculum. Of 42 program directors responding to a survey of all 110 US accredited adult programs, 17 indicated that their fellows gained some contact with US, with a rheumatologist as the main resource in 11 instances. Challenges cited included time constraints of the curriculum, equipment availability and cost, lack of experienced faculty on site with time to dedicate to this training, and objections from other specialties (156). Besides its impact on clinical rheumatology practice, US can aid in teaching the basics of musculoskeletal anatomy (157). Although the reading of radiographs, CT, and MRIs

does allow for some learning of anatomy, only US reveals the relationships between moving parts. US can also enhance undergraduate-level rheumatology teaching programs (158). Until US training is integrated into academic curricula, most trainees and practicing rheumatologists face the challenge of finding training elsewhere and teaching themselves. As a professional society dedicated to meeting the needs of its members, the ACR plans to advocate for the role of US in the practice of rheumatology and help promote its acceptance. Curriculum guidelines and competencies for practice should emerge, following cooperative efforts between the ACR and other specialties such as orthopedics and radiology (perhaps coordinated by the AIUM).

Discussions US is a powerful tool in the practice of rheumatology. Its utility is well established in Europe and is beginning to emerge in America. US is uniquely capable of visualizing a number of different anatomic structures and their coordinated motions; moreover, it can help elucidate the nature and severity of pathology within those structures. US can help establish diagnoses, guide procedures, and assess efficacy of ongoing treatments in patients with various rheumatic conditions. Currently, training in US is a mandatory part of the fellowship curriculum in both Germany and Italy (10). American trainees are beginning to appreciate that US could be a part of their future, but are uncertain how or where to learn these skills. The ACR recognizes the need to standardize and speed up the learning process, as well as to increase dissemination of this useful technique in American practice. Cost-effectiveness data for musculoskeletal US are therefore far lacking. Reimbursement issues also need to be clarified. While some radiologists have concerns about excessive and inappropriate use of US (9), a separate group estimates that Medicare savings of more than $6.9 billion in the period from 2006 to 2020 could be realized by the appropriate use of musculoskeletal US, rather than the more costly MRI, in situations where the 2 modalities would yield similar information (159). A future for US in American rheumatology seems certain. The improved clinical assessments and patient outcomes arising from the use of US should augment American rheumatology practice. In addition, US will impact clinical research. Use of US parameters and outcome measures in clinical trials will almost certainly expand, and with it the need for coordinated efforts to standardize assessment techniques among participating centers. Individual practitioners will not only need to learn US in its current status, but assess, adapt to, and incorporate emerging techniques such as high-resolution power Doppler and 3-D US. Questions regarding US to which investigators might apply their focus still seem limitless, despite more than a decade of research on musculoskeletal US. Such ways forth should proceed in cooperation with our radiology colleagues, sharing expertise in technology and clinical pathology that can play complementary roles in the development of musculoskeletal US. Finally, educators

Ultrasound in American Rheumatology Practice shoulder the task of developing and implementing both the curriculum to train rheumatologists in US and the methods to certify competence.

AUTHOR CONTRIBUTIONS All authors were involved in drafting the article or revising it critically for important intellectual content, and all authors approved the final version to be submitted for publication. Dr. Ike had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study conception and design. Ike, Erin Arnold, William Arnold, Kaeley, McAlindon, Nazarian, Reginato. Acquisition of data. Ike, Erin Arnold, William Arnold, CraigMuller, Reginato. Analysis and interpretation of data. Ike, Erin Arnold, Craig-Muller, McAlindon, Reginato.

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