Doppler Techniques E

Doppler techniques E. Naredo, I. Monteagudo

Department of Rheumatology. Hospital ABSTRACT real time US imaging. In CD mode, General Universitario Gregorio Marañón Over the last decade, there has been a the information from Doppler tech- and Universidad Complutense, Madrid, growing body of evidence on the valid- nique is integrated in the B-mode (i.e. Spain. ity of Doppler ultrasound for assess- grey-scale) image as a colour signal. Esperanza Naredo, MD, PhD ing inflammatory changes in target Real-time flow information as a colour Indalecio Monteagudo, MD, PhD anatomic structures involved in rheu- signal is superimposed on the B-mode Please address correspondence to: matic diseases such as joints, tendons, (i.e. grey-scale) image. Colours indicate Esperanza Nardo, MD, PhD, entheses and vessels. The enhanced Dr Alvarez Sierra 4, 4º A, direction of flow. Red usually indicates 28033 Madrid, Spain. sensitivity for detecting low-velocity flow towards the transducer i.e( . artery) E-mail: [email protected] flow in synovium vessels achieved by and blue indicates flow away from the Received on July 29, 2013; accepted in current Doppler techniques has lead to transducer (i.e. vein). revised form on September 14, 2013. the incorporation of Doppler US in the Power Doppler (PD) mode is the most Clin Exp Rheumatol 2014; 32 (Suppl. 80): assessment of joint and inflammatory recent Doppler mode, which has been S12-S19. enthesis lesions. This review offers an available in US technique since the 90s © Copyright Clinical and overview of the key aspects of current (2-5). While CD displays mean Dop- Experimental Rheumatology 2014. applications and limitations of Dop- pler shift, PD displays power of the pler ultrasound in inflammatory rheu- Doppler shift in each cell, represent- Key words: Doppler, ultrasound, matic diseases. The basic principles ing only signal intensity (i.e. amount of synovitis, tenosynovitis, enthesitis, of Doppler modes, Doppler scanning red blood cells flowing). Consequently, rheumatoid arthritis, spondyloarthritis, method, and Doppler artefacts and pit- PD potentially increased the sensitivity vasculitis falls in rheumatology ultrasound are to detect low velocity flow from small also described. vessels such as those involved in inflammatory processes, which are the Doppler physics and modes key areas in rheumatic diseases (2-5). Doppler ultrasound (US) is based on the In addition, PD is almost angle inde- Doppler effect, which was described by pendent, displays poorer delineation the Austrian physicist Christian Dop- of the flow profile and pursatility and pler in 1842. This physical phenomenon is more vulnerable to motion artefacts consists of a change in the frequency of than CD. In recent years, the sensitiv- a sound wave (i.e. Doppler shift) result- ity of CD mode for detecting flow at ing from motion of either the source or the microvascular level has greatly im- the receiver. In medical Doppler US, proved in many high-end US machines. the Doppler effect allows us to detect Thus, currently the choice of PD versus movement of red blood cells in vessels. CD should be taken for each particular Thus, Doppler US provides information US machine. Nevertheless, PD is still on blood flow, which is related to the recommended for use in rheumatology vascularisation of the anatomic struc- in many mid-range and entry-level US tures (1). machines. Spectral Doppler was the first mode available in Doppler US. In this Dop- Doppler settings pler mode, the spectrum of flow veloci- Optimal adjustment of CD or PD Dop- ties is represented graphically on the pler setting is essential to enhance the y-axis and time on the x-axis. Thus quality of Doppler US assessment. spectral mode allows us to measure dif- Doppler settings should be adjusted to Competing interests: ferent blood flow parameters, some of obtain the highest sensitivity for detect- E. Naredo has received a research grant which (e.g. resistive index) can be use- ing flow with or without minimal arte- from MSD and speaker fees from AbbVie, ful in rheumatology US. facts. These parameters depend on the Roche Farma, BMS, Pfizer, UCB, General

Electric, and Esaote; Later, colour flow imaging or colour US equipment and are different accord- I. Monteagudo has received a research Doppler (CD) mode was developed ing to the depth of the studied anatomic grant from Pfizer and speaker fees from in Doppler US. CD technique is the area. We can create some presets with AbbVie and Roche. combination of the Doppler effect and appropriate Doppler parameters for dif-

S-12 Applications of Doppler techniques in rheumatology / E. Naredo & I. Monteagudo ferent anatomic area (e.g. deep, inter- Table I. Principal artefacts in rheumatology Doppler US. mediate and superficial joints), which Artefacts Technical basis How to avoid or minimise are very helpful and save time in daily practice. The principal Doppler settings Motion or random flashes Too low PRF produces detection Adjusting PRF to maximise Doppler that we need to know for rheumatology of slight movements of the sensitivity with no or minimal Doppler US, either CD or PD, are de- patients or the examiner, artery artefacts walls or patient’s voice scribed below (6). – Focusing Ramdon noise Too high Doppler gain Adjusting Doppler gain at or just below the level that generates no or As on B-mode, the focal point should minimal random noise be placed at the level of the target area. – Doppler frequency Mirror Mirror colour images under The real vessel and its mirror image highly reflecting surfaces such under the bone surface are easily In general, high Doppler frequencies as bones recognised should be used for superficial anatomic Blooming Colour beyond the vessel wall This artifact is recognised by areas and low Doppler frequencies for due to high gain temporarily reducing the gain deep anatomic areas. However, optimal Reverberation Superficial vessels produce false This artifact is recognised extending frequencies for different depths depend color signals at deeper locations the colour box to the top of the image on the US machines. such as within synovial spaces – Pulse repetition frequency (PRF) A low PRF enhances the sensitivity US: ultrasound; PRF: pulse repetition frequency. of Doppler to detect low velocity flow from small vessels in inflammatory dis- – Colour priority – Scanning of joints and entheses orders. However, a too low PRF produc- This setting should be maximised over Joints should be scanned in neutral po- es motion artefacts due to movement of grey-scale priority when detecting sition instead of in extended or flexed the patients, probe or artery wall or pa- blood flow is the primary objective of position; overextension or flexion of tient’s voice. These artefacts can make the US investigation. the joint can tighten the joint capsule the interpretation of real flow in the US resulting in compression of vessels images very difficult. Therefore, opti- Doppler scanning method and consequent reduction of detectable mal PRF should be the lowest value that Doppler examination should be per- flow (7). Entheses should be scanned maximises Doppler sensitivity with no formed after morphological B-mode with the joint in neutral position, oth- or minimal motion artefacts. This value examination of the investigated ana- erwise increase in the intratendinous usually ranges from 500 to 900 Hz de- tomic structures. The valuable informa- tension can produce entheseal vessel pending on the US equipment. tion about blood perfusion provided by collapse (8). – Doppler gain Doppler US is always complementary – Scanning pressure A high Doppler gain increases the Dop- to the morphological information pro- Care should be taken not to apply too pler sensitivity but also the noise arte- vided by B-mode US. much pressure with the probe in super- facts. Hence, Doppler gain should be – Training ficial joints so as not to compress the increased until random noise appears. A thorough knowledge of musculoskel- vessels and overlook the colour signal. As stated by Rubin (2), because no etal US on B-mode is necessary before A thick layer of gel should be applied flow should be visualised in the bone, starting the training on Doppler modes. between the probe and the patient’s colour gain should be set just below the The morphological information of the skin which should be visible in the level at which colour noise appeared anatomic structures provided by the US image to ensure minimal scanning underlying bone. Optimal Doppler gain B-mode images allows us to know the pressure. is highly dependent on the machine. location of the vascularisation detected – Knowledge of anatomy – Wall filter by Doppler mode and thus interpret the Knowledge of the location of the feed- Low wall filters enhance the sensitiv- nature, normal (i.e. feeding vessels) or ing vessels of joints, tendon and en- ity of Doppler for detecting flow from pathological, of blood perfusion. theses avoid misinterpretation of these small vessels. – Patient and examiner positioning normal vessels as pathologic vasculari- – Doppler box The patient and the examiner must be sation (Online Fig. 1). The colour box should be adjusted to comfortable to avoid motion artefacts. the region of interest, which should The patient should be quiet because Doppler artefacts include the studied anatomic structure voice can produce motion artefacts. Correct use of Doppler US requires (e.g. joints, entheses), the bony margins The examined area must be relaxed; recognition of artefacts, which can and a variable view of surrounding tis- tension in muscle, tendons and joints lead to misinterpretation of relevant sues. This box can be extended to the produces motion artefacts. The scan- findings in rheumatic diseases (Online top of the image (i.e. patient’s skin) to ning arm and hand of the examiner Figs. 5-8). Table I shows the principal recognise reverberation artefacts pro- must rest in a comfortable way to avoid artefacts in rheumatology Doppler US duced by superficial vessels (6). motion artefacts. (6).

S-13 Applications of Doppler techniques in rheumatology / E. Naredo & I. Monteagudo

Applications of Doppler ultrasound synovitis has shown predictive value in of Doppler signal at the anatomic loca- in rheumatology relation to disease flare or relapse in RA tions of the entheses (i.e. very close to Synovitis and tenosynovitis patients in clinical remission (15, 18, or at the bone profile) has demonstrated Synovial inflammation consists of 20, 24). high specificity for diagnosing SpA in periarticular vasodilatation followed patients with early axial or peripheral by synovial proliferation, which is ac- Reliability symptoms (65, 68, 69). In patients with companied by angiogenesis resulting in Despite the high operator dependence psoriasis, the presence of entheseal intra-articular blood vessel formation of US, Doppler technique has shown Doppler signal seems to be associated (9). Angiogenesis of the synovial and good interobserver and intraobserver with the development of psoriatic ar- tenosynovial membrane is considered reliability in synovitis and tenosyno- thritis (70). Doppler-detected enthesitis to be a primary pathogenic mechanism vitis detection and scoring. This reli- has shown good reliability (71) and re- responsible for the joint and tendon ability was similar using quantitative sponsiveness (72) in SpA patients. aggressiveness in rheumatoid arthritis or semiquantitative scoring systems (RA) and other inflammatory arthritis (43-47). Vasculitis (9,10). CD and PD US techniques de- Colour Doppler US of superficial arter- tect pathologic flow within the synovial Responsiveness ies has been widely used to detect vas- and tenosynovial hypertrophy, which is Many longitudinal studies have dem- culitis (73-79). Hypoechoic thickening a sign of inflammatory activity (Figs. onstrated a significant reduction of of the artery wall (i.e. circumferential 1-3). This has led to Doppler US play- joint inflammation evaluated by - Dop halo detected in transverse and longi- ing an increasingly important role in the pler US (e.g. PD or CD) in different tudinal plane) is the most specific sign evaluation and monitoring of patients joints and joint combinations of RA for vessel inflammation (specificity with inflammatory arthritis in clinical patients on different treatments, includ- >90%). In addition, turbulent flow and practice and clinical trials (11). Inter- ing intra-articular corticosteroid injec- arterial stenosis or occlusion are more estingly, recent studies have reported tions, systemic corticosteroid therapy, sensitive signs (sensitivity >75%) but the presence of subclinical synovi- synthetic and biologic DMARDs (32, less specific for arteritis (76). These tis with Doppler-detected activity in 36-38, 40, 44, 48-58). In these studies, colour Doppler findings have been de- around 50% of RA patients in clinical changes in Doppler-detected synovitis scribed in the temporal, occipital, and remission treated with synthetic or bio- were associated with clinical and labo- facial arteries, as well as in extracrane- logic disease-modifying anti-rheumatic ratory response to therapy. la arteries such as axillary, subclavian, drugs (DMARDs) (12-24). However, common carotid arteries and other pe- the impact of Doppler-targeted therapy Diagnostic value ripheral arteries in giant cell arteritis on RA outcomes in these patients has In a small number of studies, the pres- (GCA) (73-75, 78). Some experienced not been established yet. ence of synovial Doppler signal has ultrasonographer have proposed that In addition to inflammatory arthritis, shown diagnostic value in relation to US Doppler performed with an appro- synovial Doppler signal can be found the development of chronic arthritis or priate machine can replace the temporal in other conditions such as pigmented RA in patients with early undifferenti- artery biopsy as complementary tools villonodular synovitis (Online Fig. 2), ated synovitis (59-62). However, more in the clinical diagnosis of the above microcrystalline arthropathies or osteo- studies are needed to establish the diag- disease. Alternatively, colour Doppler arthritis. nostic and therapeutic impact of Dop- can be very helpful in guiding the bi- pler findings in patients with arthralgia opsy of the most involved and the most Validity or very early arthritis. accessible area of the temporal artery There is an increasing number of studies to enhance the diagnostic capability of on the concurrent validity of Doppler- Enthesitis these diagnostic tools in GCA. Colour detected synovial inflammation using Entheses are the sites where tendons, Doppler US has shown responsiveness histology (25-28) or contrast-enhanced ligaments, muscle, fascia or joint cap- in GCA after few weeks of appropriate magnetic resonance imaging as gold sules attached to the bone (63). Inflam- corticosteroid treatment (80). standard (29, 30). Other studies have mation of entheses or enthesitis is the shown close association between Dop- principal pathological feature of spon- Soft tissue diseases pler-detected synovitis and clinical or dyloarthritis (SpA) (64). Histological The presence of abnormal blood flow laboratory markers of inflammation in studies on enthesitis have described lo- detected with Doppler US has been de- RA (31-35). Synovial Doppler signal cal inflammation, fibrosis, erosion, os- scribed around or inside soft tissue le- has demonstrated predictive value in re- sification and adjacent bursitis (64). sions (e.g. tendinosis, tendon tear, bur- lation to structural damage progression Abnormal blood flow in peripheral en- sitis) (81) (Online Fig. 3). More recent- in both clinically active (36-42) and in- theses detected with Doppler US has ly, Doppler US has been used to distin- active (14, 22, 24) RA patients treated been described in active SpA patients, guish active tendinosis (i.e. increased with synthetic or biologic DMARDs. In mainly in the lower limbs (65-69) (Fig. Doppler-detected blood flow inside addition, subclinical Doppler-detected 4). Even more important, the presence the tendon degenerative area) from

S-14 Applications of Doppler techniques in rheumatology / E. Naredo & I. Monteagudo inactive tendinosis (i.e. no or minimal normal Doppler-detected blood flow inside the tendon degenerative area) (82). These active areas in tendinosis seem to correspond with proliferation of new vessels, which may be part of a healing process and/or an inflammatory process. This distinction can be useful to choose the most appropriate treatment for tendinosis.

Methods of quantification of inflammatory findings in rheumatology Doppler US Pathologic blood flow can be detected with Doppler US in different synovial recesses accessible by US evaluation in peripheral joints. In inflammatory arthritis, colour or power Doppler sig- Fig. 1. Longitudinal ultrasound image of the dorsal aspect of a metacarpophalangeal joint that shows nal within synovial hypertrophy is the severe power Doppler signal within the synovial hypertrophy. main pathologic marker of inflammatory activity (25-30). Several systems for quantifying Doppler-detected synovitis in RA joints have been used in published studies (83). These systems have been qualitative (29), semiquantitative (12, 14, 15, 17, 20, 23-26, 31, 32, 34, 38, 41, 43, 50-55, 58) or quantitative (25, 30, 36, 44, 49, 84) and have included any number of scanned joints ranging from 78 joints to a reduced number of target RA joints such as wrist, hand, or toe joints (85). These variables have made comparison of study results difficult. A binary scoring of synovitis according to the presence or absence of synovial Doppler signal at synovial sites can be feasible, easy and reliable but not sensitive to change. Most research groups have used a four-grade semiquantitative scoring system (i.e. 0, no Dop- pler signal; 1, isolated Doppler signal; 2, moderate Doppler signal; 3, severe Doppler signal) for synovial Doppler signal. This system is easily applica- ble in clinical practice and clinical tri- Fig. 2. Transverse ultrasound image of the tibialis posterior tendon that shows tenosynovitis on als, and is reliable and responsive to B-mode and power Doppler mode (diffuse Doppler signal within the distended synovial sheath). therapeutic interventions. In fact, the eular-omeract (European League chine reliability in RA patients (86-88). clude computer-assisted measurement Against Rheumatism-Outcome Meas- Quantitative assessment of synovial of colour pixels in a specific area of ures in Rheumatology) group for mus- Doppler signal has the advantages of interest (Online Fig. 4) (25, 30, 36, 44, culoskeletal US has agreed on the use being more objectives than semiquan- 49, 84) and spectral Doppler analysis of four-grade semiquantitative scoring titative assessment. In addition, quanti- with measurement of the resistive in- systems for both, B-mode-detected and tative systems use continuous variables dex (30, 44, 49, 84). Low values of RI Doppler-detected synovitis, which have which can be more sensitive to change indicate an inflammation process. Both demonstrated good multi-examiner in- than semiquantitative variables. Quan- Doppler parameters have been shown traobserver, interobserver and intera- titative Doppler scoring systems in- highly reliable and responsive to thera-

S-15 Applications of Doppler techniques in rheumatology / E. Naredo & I. Monteagudo

py (44-46, 84). However, they are time consuming and not feasible in clinical practice. Thus, they are probably more suitable for US research. In clinical practice, spectral Doppler can be useful to distinguish real flow versus artefacts in some occasional doubtful cases. Recently, the eular-omeract group for musculoskeletal US has developed a scoring system for tenosynovitis in RA (47). A four-grade semiquantitative scoring system (i.e. grade 0, no Doppler signal; grade 1, focal Doppler signal; grade 2, multifocal Doppler signal; grade 3, diffuse Doppler signal) was agreed upon for scoring pathologic peritendinous (i.e. intra-sheath) Dop- pler signal in RA tenosynovitis (47). Intratendinous Doppler signal was not included in the elementary lesions of tenosynovitis because it could correspond to intratendinous tenosynovial angiogenesis, vasodilatation of intratendinous feeding vessels or hypervas- cularisation in areas of tendon repair. Nevertheless, the presence of intratendinous signal in addition to peritendinous signal was considered in the teno- Fig. 3. Longitudinal ultrasound image of the tibialis posterior tendon that shows tenosynovitis on B-mode and power Doppler mode (diffuse Doppler signal within the distended synovial sheath). synovitis scoring system (i.e. intratendinous signal increases the grades 1 and 2 by one point). Regarding the global scoring of Dop- pler-detected synovitis (i.e. patient level), most published studies have included a limited number of target rheumatoid joints and few studies have included tenosynovitis as synovial sites assessed by Doppler US (85). The global score for Doppler synovitis was usually obtained from the sum of the Doppler score of each studied joint. Some studies have proposed reduced- joint Doppler US assessments (23, 54, 55, 62, 89). These studies have demonstrated appropriate metric properties of reduced-joint scoring systems for monitoring therapeutic response (54, 55, 89, 90), evaluating subclinical synovitis in RA patients in clinical remission (23), and diagnosing RA (62). At the patient level, wrist-hand and ankle-foot tendons should be selected for scoring tenosynovitis because of their frequent involvement in inflammatory Fig. 4. Longitudinal ultrasound image of the Achilles tendon in a patient with spondyloarthritis. arthritis and their superficial location B-mode enthesopathy and power Doppler signal within a calcaneal bone erosion, the retrocalcaneal bursa area and the tendon substance are detected. which is optimal for Doppler sensitivity (47, 91).

S-16 Applications of Doppler techniques in rheumatology / E. Naredo & I. Monteagudo

Some studies have included the pres- ADLER RS: Power Doppler sonography of power Doppler ultrasonography as a gold ence of entheseal Doppler signal in the synovitis: assessment of therapeutic re- standard. Rheumatology 2010; 49: 683-90. sponse. Preliminary observations. Radiology 18. PELUSO G, MICHELUTTI A, BOSELLO S et US assessment of SpA enthesopathy 1996; 198: 582-4. al.: Clinical and ultrasonographic remission (65-69). However, there is no agree- 4. MURPHY KJ, RUBIN JM: Power Doppler: determines different chances of relapse in ment on a scoring system for Doppler it’s a good thing. Semin Ultrasound CT MRI early and long standing rheumatoid arthritis. enthesitis in SpA patients. 1997; 18: 13-21. Ann Rheum Dis 2011; 70: 172-5. 5. MARTINOLI C, PRETOLESI F, CRESPI G et al.: 19. SALEEM B, BROWN AK, KEEN H et al.: Power Doppler sonography: clinical appli- Should imaging be a component of rheuma- Limitations of Doppler ultrasound cations. Eur J Radiol 1998; 28: S133-40. toid arthritis remission criteria? A compari- in rheumatology 6. TORP-PEDERSEN ST, TERSLEV L: Settings son between traditional and modified com- and artefacts relevant in colour/power Dop- posite remission scores and imaging assess- A number of technical limitations of pler ultrasound in rheumatology. Ann Rheum ments. Ann Rheum Dis 2011; 70: 792-8. Doppler US should be mentioned. The Dis 2008: 67: 143-9. 20. SALEEM B, BROWN AJ, QUINN M et al.: lower sensitivity of CD and PD to de- 7. LEE V, ZAYAT A, WAKEFIELD RJ: The effect Can flare be predicted in DMARD treated tect flow from small vessels in deep of joint position on Doppler flow in finger RA patients in remission, and is it important? synovitis. Ann Rheum Dis 2009; 68: 603-4. A cohort study. Ann Rheum Dis 2012; 71: anatomic areas as compared with su- 8. GUTIERREZ M, FILIPPUCCI E, GRASSI W, 1316-21. perficial areas limits the assessment of ROSEMFFET M: Intratendinous power Dop- 21. SAKELLARIOU G, SCIRÈ CA, VERSTAPPEN inflammatory activity in deep joints, pler changes related to patient position in SMM, MONTECUCCO C, CAPORALI R: In tendons or entheses. In addition, ad- seronegative spondyloarthritis. J Rheumatol patients with early rheumatoid arthritis, the 2010; 37: 1057-9. new ACR/EULAR definition of remission justing the settings for optimal balance 9. PAP T, DISTLER O: Linking angiogenesis to identifies patients with persistent absence between high Doppler sensitivity and bone destruction in arthritis. Arthritis Rheum of functional disability and suppression of minimal artefacts is not easy in all US 2005; 52: 1346-8. ultrasonographic synovitis. Ann Rheum Dis machines. Furthermore, the difficulty 10. JAIN A, NANCHAHAL J, TROEBERG L, 2013; 72: 245-9. GREEN P, BRENNAN F: Production of cyto- 22. YOSHIMI R, HAMA M, TAKASE K et al.: in standardising Doppler parameters kines, vascular endothelial growth factor, Ultrasonogarphy is a potent tool for the pre- among different US equipments lim- matrix metalloproteinases, and tissue inhibi- diction of progressive joint destruction dur- its both comparison between Doppler tor of metalloproteinases by tenosynovium ing clinical remission of rheumatoid arthritis. studies and the development of multi- demonstrates its potential for tendon destruc- Mod Rheumatol 2013; 23: 456-65. tion in rheumatoid arthritis. Arthritis Rheum 23. NAREDO E, VALOR L, de la TORRE I et al.: centre Doppler studies performed with 2001; 44: 1754-60. Ultrasound joint inflammation in rheumatoid different machines. 11. JOSHUA M, EDMONDS J, LASSERE M: Power arthritis in clinical remission: how many and Doppler ultrasound in musculoskeletal dis- which joints should be assessed?. Arthritis eases: a systematic review. Semin Arthritis Care Res 2013; 65: 512-7. Conclusions Rheum 2006; 36: 99-108. 24. FOLTZ V, GANDJBAKHCH F, ETCHEPARE F et Doppler ultrasound is a valid imaging 12. BROWN AK, QUINN MA, KARIM Z et al.: al.: Power Doppler ultrasound, but not low- modality in assessment and monitoring Presence of significant synovitis in rheuma- field magnetic resonance imaging, predicts of inflammatory arthritis with proven toid arthritis patients with disease-modifying relapse and radiographic disease progression antirheumatic drug-induced clinical remis- in rheumatoid arthritis patients with low lev- predictive value in relation to disease sion: evidence from an imaging study may els of disease activity. Arthritis Rheum 2012; outcomes and has a promising diag- explain structural progression. Arthritis 64: 67-76. nostic value. Doppler ultrasound of su- Rheum 2006; 54: 3761-73. 25. WALTHER M, HARMS H, KRENN V, RADKE S, perficial vessels can also be used as a 13. WAKEFIELD RJ, FREESTON JE, HENSOR EM, FAEHNDRICH TP, GOHLKE F: Correlation of BRYER D, QUINN MA, EMERY P: Delay in im- Power Doppler Sonography with vascular- diagnostic tool in vasculitis. However, aging versus clinical response: a rationale for ity of the synovial tissue of the knee joint in some technical issues such as the low prolonged treatment with anti-tumor necrosis patients with osteoarthritis and rheumatoid sensitivity of Doppler in deep joints, the factor medication in early rheumatoid arthri- arthritis. Arthritis Rheum 2001; 44: 331-8. tis. Arthritis Rheum 2007; 57: 1564-7. 26. SCHMIDT WA, VÖLKER L, ZACHER J, inability to standardise Doppler settings 14. BROWN AK, CONAGHAN PG, KARIM Z et al.: SCHLÄFKE M, RUHNKE M, GROMMICA- among different ultrasound machines, An Explanation for the Apparent Dissocia- IHLE E: Colour Doppler ultrasonography to and the difficulty in adjusting maximal tion Between Clinical Remission and Contin- detect pannus in knee joint synovitis. 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68. D’AGOSTINO MA, AEGERTER P, BECHARA et al.: Diagnostic performance of ultrasonog- SEN S, TERSLEV L, DANNESKIOLD-SAMSOE K et al.: How to diagnose spondyloarthritis raphy for giant-cell arteritis: a meta-analysis. B, BLIDDAL H: Quantitative ultrasonography early? Accuracy of peripheral enthesitis de- Ann Intern Med 2005; 142: 359-69. in rheumatoid arthritis: evaluation of inflam- tection by power Doppler ultrasonography. 77. PÉREZ LÓPEZ J, SOLANS LAQUÉ R, BOSCH mation by Doppler technique. Ann Rheum Ann Rheum Dis 2011; 70: 1433-40. GIL JA, MOLINA CATERIANO C, HUGUET RE- Dis 2001; 60: 690-3. 69. D’AGOSTINO MA, SARAUX A, CHARY-VAL- DECILLA P, VILARDELL TARRÉS M: Colour- 85. MANDL P, NAREDO E, WAKEFIELD RJ, CON- CKENAERE I et al.: Can we improve the di- duplex ultrasonography of the temporal and AGHAN PG, D’AGOSTINO MA: A systematic agnosis of spondyloarthritis in patients with ophthalmic arteries in the diagnosis and fol- litterature review analysis of ultrasound joint uncertain diagnosis? The EchoSpA prospec- low-up of giant cell arteritis. Clin Exp Rheu- count and scoring systems used to assess tive multicenter French cohort. Joint Bone matol 2009; 27 (Suppl. 52): S77-82. synovitis in rheumatoid arthritis, according Spine 2012; 79: 586-90. 78. SCHMIDT WA, SEIFERT A, GROMNICA-IHLE to the OMERACT filter. J Rheumatol 2011; 70. AYDIN SZ, ASH ZR, TINAZZI I et al.: The link E et al.: Ultrasound of proximal upper ex- 38: 2055-62. between enthesitis and arthritis in psoriatic tremity arteries to increase the diagnostic 86. WAKEFIELD RJ, D’AGOSTINO MA, IAGNOC- arthritis: a switch to a vascular phenotype at yield in large-vessel giant cell arteritis. Rheu- CO A et al.: The OMERACT Ultrasound insertions may play a role in arthritis devel- matology 2008; 47: 96-101. Group: status of current activities and research opment. Ann Rheum Dis 2013; 72: 992-5. 79. Delle SEDIE A, RIENTE L, FILIPPUCCI E et directions. J Rheumatol 2007; 34: 848-51. 71. D’AGOSTINO MA, AEGERTER P, JOUSSE- al.: Ultrasound imaging for the rheumatolo- 87. D’AGOSTINO MA, CONAGHAN PG, NAREDO JOULIN S et al.: How to evaluate and im- gist. XV. Ultrasound imaging in vasculitis. E et al.: The OMERACT ultrasound task prove the reliability of power Doppler ultra- Clin Exp Rheumatol 2008; 26: 391-4. force - Advances and priorities. J Rheumatol sonography for assessing enthesitis in spon- 80. de MIGUEL E, ROXO A, CASTILLO C, PEI- 2009; 36: 1829-32. dylarthritis. Arthritis Rheum 2009; 61: 61-9. TEADO D, VILLALBA A, MARTÍN-MOLA E: 88. NAREDO E, WAKEFIELD RJ, IAGNOCCO A et 72. NAREDO E, BATLLE-GUALDA E, GARCÍA- The utility and sensitivity of colour Doppler al.: The OMERACT ultrasound task force. VIVAR ML et al.: Power Doppler ultrasono- ultrasound in monitoring changes in giant Summary of advances and priorities. J Rheu- graphic assessment of entheses in spondy- cell arteritis. Clin Exp Rheumatol 2012; 30: matol 2011; 38: 2063-7. loarthropathies: response to therapy of en- (Suppl. 70): 34-8. 89. PERRICONE C, CECCARELLI F, MODESTI M theseal abnormalities. J Rheumatol 2010; 37: 81. BOESEN MI, BOESEN M, LANGBERG H et al.: et al.: The 6-joint ultrasonographic assess- 2110-7. Musculoskeletal colour/power Doppler in ment: a valid, sensitive-to-change and feasi- 73. SCHMIDT WA, KRAFT HE, VORPAHL K et al.: sports medicine: image parameters, artefacts, ble method for evaluating joint inflammation Color Duplex ultrasonography in the diagno- image interpretation and therapy. Clin Exp in RA. Rheumatology 2012; 51: 866-73. sis of temporal arteritis. N Engl J Med 1997; Rheumatol 2010; 28: 103-13. 90. COLLADO P, NAREDO E, CALVO C et al.: 337: 1336-42. 82. RICHARDS PJ, WIN T, JONES PW: The distri- Reduced joint assessment vs comprehensive 74. SCHMIDT WA: Doppler ultrasonography in bution of microvascular response in Achilles assessment for ultrasound detection of syno- the diagnosis of giant cell arteritis. Clin Exp tendonopathy assessed by colour and power vitis in juvenile idiopathic arthritis. Rheuma- Rheumatol 2000; 18 (Suppl. 29): S40-S42. Doppler. Skeletal Radiol 2005; 34: 336-42. tology 2013; 52: 1477-84. 75. SCHMIDT WA, NATUSCH A, MÖLLER DE, 83. ALBRECHT K, MÜLLER-LADNER U, STRUNK 91. BRUYN GW, MÖLLER I, GARRIDO J et al.: VORPAHL K, GROMNICA-IHLE E: Involve- J: Quantification of the synovial perfusion Reliability testing of tendon disease using ment of peripheral arteries in giant cell arte- in rheumatoid arthritis using Doppler ultra- two different scanning methods in patients ritis: A color Doppler sonography study. Clin sonography. Clin Exp Rheumatol 2007; 25: with rheumatoid arthritis. First step towards Exp Rheumatol 2002; 20: 309-318. 630-8. an ultrasonography scoring index. Rheuma- 76. KARASSA FB, MATSAGAS MI, SCHMIDT WA 84. QVISTGAARD E, ROGIND H, TORP-PEDER- tology 2012; 51:1655-61.

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