Top

02-08-2018 | Rheumatoid arthritis | Review | Article

Ultrasound and its clinical use in rheumatoid arthritis: where do we stand?

Journal: Advances in Rheumatology

Authors: Aline Defaveri do Prado, Henrique Luiz Staub, Melissa Cláudia Bisi, Inês Guimarães da Silveira, José Alexandre Mendonça, Joaquim Polido-Pereira, João Eurico Fonseca

Publisher: BioMed Central

Abstract

High-resolution musculoskeletal ultrasound (MSUS) has been increasingly employed in daily rheumatological practice and in clinical research. In rheumatoid arthritis (RA), MSUS can be now considered a complement to physical examination. This method evaluates synovitis through gray-scale and power Doppler and it is also able to identify bone erosions. The utilization of MSUS as a marker of RA activity has received attention in recent literature. Current data account for good correlation of MSUS with classical measures of clinical activity; in some instances, MSUS appears to perform even better. Diagnosis of subclinical synovitis by MSUS might help the physician in RA management. With some variation, interobserver MSUS agreement seems excellent for erosion and good for synovitis. However, lack of MSUS score standardization is still an unmet need. In this review, we describe several MSUS scores, as well as their correlation with clinical RA activity and response to therapy. Finally, we look at the relationship of MSUS with synovial tissue inflammation and discuss future perspectives for a better interpretation and integration of this imaging method into clinical practice.

Scott D, Wolfe F, Huizinga T. Rheumatoid arthritis. Lancet. 2010;376:1094–108.PubMedCrossRef

McInnes I, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007;7:429–42.PubMedCrossRef

Ohrndorf S, Backhaus M. Pro musculoskeletal ultrasonography in rheumatoid arthritis. Clin Exp Rheumatol. 2015;33:S50–3.PubMed

Filippucci E, Iagnocco A, Meenagh G. Ultrasound imaging for the rheumatologist. Clin Exp Rheumatol. 2006;24:1–5.PubMed

Zayat AS, Ellegaard K, Conaghan PG, Terslev L, EM a H, Freeston JE, et al. The specificity of ultrasound-detected bone erosions for rheumatoid arthritis. Ann Rheum Dis. 2015;74:897–903.PubMedCrossRef

Iwamoto T, Ikeda K, Hosokawa J, Yamagata M, Tanaka S, Norimoto A, Sanayama Y, Nakagomi D, et al. Prediction of relapse after discontinuation of biologic agents by ultrasonographic assessment in patients with rheumatoid arthritis in clinical remission: high predictive values of total gray-scale and power Doppler scores that represent residual synovial. Arthritis Care Res. 2014;66:1576–81.CrossRef

Pineda C, Reginato AM, Flores V, Aliste M, Alva M, Aragón-Laínez RA, et al. Pan-American league of associations for rheumatology (PANLAR) recommendations and guidelines for musculoskeletal ultrasound training in the Americas for rheumatologists. J Clin Rheumatol. 2010;16:113–8.PubMedCrossRef

Colebatch A, Edwards C, Østergaard M, van der Heijde D, Balint P, D’Agostino M, et al. EULAR recommendations for the use of imaging of the joints in the clinical management of rheumatoid arthritis. Ann Rheum Dis. 2013;72:804–14.PubMedCrossRef

Andersen M, Ellegaard K, Hebsgaard JB, Christensen R, Torp-Pedersen S, Kvist PH, et al. Ultrasound colour Doppler is associated with synovial pathology in biopsies from hand joints in rheumatoid arthritis patients: a cross-sectional study. Ann Rheum Dis. 2014;73:678–83.PubMedCrossRef

10.

Alivernini S, Peluso G, Fedele AL, Tolusso B, Gremese E, Ferraccioli G. Tapering and discontinuation of TNF-α blockers without disease relapse using ultrasonography as a tool to identify patients with rheumatoid arthritis in clinical and histological remission. Arthritis Res Ther. 2016;18:39.PubMedPubMedCentralCrossRef

11.

Anandarajah A, Thiele R, Giampoli E, Monu J, Seo GS, Feng C, et al. Patients with rheumatoid arthritis in clinical remission manifest persistent joint inflammation on histology and imaging studies. J Rheumatol. 2014;41:2153–60.PubMedCrossRef

12.

Takase K, Ohno S, Takeno M, Hama M, Kirino Y, Ihata A, et al. Simultaneous evaluation of long-lasting knee synovitis in patients undergoing arthroplasty by power Dopplerultrasonography and contrast-enhanced MRI in comparison with histopathology. Clin Exp Rheumatol. 2012;30:85–92.PubMed

13.

Koski J. Doppler Imaging and Histology of the Synovium. J Rheumatol. 2012;39:452–3.PubMedCrossRef

14.

Paleolog EM. The vasculature in rheumatoid arthritis: cause or consequence? Int J Exp Pathol. 2009;90:249–61.PubMedPubMedCentralCrossRef

15.

Koski JM, Saarakkala S, Helle M, Hakulinen U, Heikkinen JO, Hermunen H. Power Doppler ultrasonography and synovitis: correlating ultrasound imaging with histopathological findings and evaluating the performance of ultrasound equipments. Ann Rheum Dis. 2006;65:1590–5.PubMedPubMedCentralCrossRef

16.

Koski JM, Saarakkala S, Helle M, Hakulinen U, Heikkinen JO, Hermunen H, et al. Assessing the intra- and inter-reader reliability of dynamic ultrasound images in power Doppler ultrasonography. Ann Rheum Dis. 2006;65:1658–60.PubMedPubMedCentralCrossRef

17.

Walther M, Harms H, Krenn V, Radke S, Faehndrich TP, Gohlke F. Correlation of power Doppler sonography with vascularity of the synovial tissue of the knee joint in patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum. 2001;44:331–8.PubMedCrossRef

18.

Kitchen J, Kane D. Greyscale and power Doppler ultrasonographic evaluation of normal synovial joints: correlation with pro- and anti-inflammatory cytokines and angiogenic factors. Rheumatology (Oxford). 2015;54:458–62.CrossRef

19.

Ramirez J, Ruiz-Esquide V, Pomes I, Celis R, Cuervo A, Hernandez M, et al. Patients with rheumatoid arthritis in clinical remission and ultrasound-defined active synovitis exhibit higher disease activity and incresed serum levels of angiogenic biomarkers. Arthritis Res Ther. 2014;16:R5.PubMedPubMedCentralCrossRef

20.

Strunk J, Heineman E, Neeck G, Schmidt KL, Lange U. A new approach to studying angiogenesis in rheumatoid arthritis by means of power Doppler ultrasonography and measurement of serum vascular endothelial growth factor. Rheumatology. 2004;43:1480–3.PubMedCrossRef

21.

Terslev L, Torp-Pedersen S, Bang N, Koenig MJ, Nielsen MB, Bliddal H. Doppler ultrasound findings in healthy wrists and finger joints before and after use of two different contrast agents. Ann Rheum Dis. 2005;64:824–7.PubMedPubMedCentralCrossRef

22.

Klauser A, Frauscher F, Schirmer M, Halpern E, Pallwein L, Herold 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.PubMedCrossRef

23.

Fiocco U, Ferro F, Cozzi L, Vezzù M, Sfriso P, Checchetto C, et al. Contrast medium in power Doppler ultrasound for assessment of synovial vascularity: comparison with arthroscopy. J Rheumatol. 2003;30:2170–6.PubMed

24.

Szkudlarek M, Court-Payen M, Strandberg C, Klarlund M, Klausen T, Østergaard M. Contrast-enhanced power Doppler ultrasonography of the metacarpophalangeal joints in rheumatoid arthritis. Eur Radiol. 2003;13:163–8.PubMed

25.

Andersen M, Boesen M, Ellegaard K, Christensen R, Söderström K, Søe N, et al. Synovial explant inflammatory mediator production corresponds to rheumatoid arthritis imaging hallmarks: a cross-sectional study. Arthritis Res Ther. 2014;16:R107.PubMedPubMedCentralCrossRef

26.

Do Prado AD, Bisi MC, Piovesan DM, Bredemeier M, Batista TS, Petersen L, et al. Ultrasound power Doppler synovitis is associated with plasma IL-6 in established rheumatoid arthritis. Cytokine. 2016;83:27–32.PubMedCrossRef

27.

Ball E, Gibson D, Rooney AB. Plasma IL-6 levels correlate with clinical and ultrasound measures of arthritis in patients with systemic lupus erythematosus. Lupus. 2014;23:46–56.PubMedCrossRef

28.

Brzustewicz E, Bryl E. The role of cytokines in the pathogenesis of rheumatoid arthritis. Practical and potential application of cytokines as biomarkers and targets of personalized therapy. Cytokine. 2015;76:527–36.PubMedCrossRef

29.

Baillet A, Gossec L, Paternotte L, Paternotte S, Etcheto A, Combe B, et al. Evaluation of serum Interleukin-6 level as a surrogate marker of synovial inflammation and as a factor of structural progression in early rheumatoid arthritis: results from a French National Multicenter Cohort. Arthritis Care Res (Hoboken). 2015;67:905–12.CrossRef

30.

Fazaa A, Ben Abdelghani K, Abdeladhim M, Laatar A, Ben Ahmed M, Zakraoui L. The level of interleukin-17 in serum is linked to synovial hypervascularization in rheumatoid arthritis. Jt Bone Spine. 2014;81:550–1.CrossRef

31.

Gullick N, Evans H, Church L, Javaraj D, Filer A. Linking power Doppler ultrasound to the presence of Th17 cells in the rheumatoid. PLoS One. 2010;5:e12516.PubMedPubMedCentralCrossRef

32.

Van der Heijde D, van ‘t Hof M, van Riel P, Theunisse L, Lubberts E, van Leeuwen M, et al. Judging disease activity in clinical practice in rheumatoid arthritis: first step in the development of a disease activity score. Ann Rheum Dis. 1990;49:916–20.PubMedPubMedCentralCrossRef

33.

Vlad V, Berghea F, Libianu S, Balanescu A, Bojinca V, Constantinescu C, Abobului M, Predeteanu D, Ionescu R. Ultrasound in rheumatoid arthritis: volar versus dorsal synovitis evaluation and scoring. BMC Musculoskelet Disord. 2011;12:124.PubMedPubMedCentralCrossRef

34.

Szkudlarek M, Narvestad E, Klarlund M, Court-Payen M, Thomsen HS, Østergaard M. Ultrasonography of the metatarsophalangeal joints in rheumatoid arthritis: comparison with magnetic resonance imaging, conventional radiography, and clinical examination. Arthritis Rheum. 2004;50:2103–12.PubMedCrossRef

35.

Salaffi F, Filippucci E, Carotti M, Naredo E, Meenagh G, Ciapetti A, et al. Inter-observer agreement of standard joint counts in early rheumatoid arthritis: a comparison with grey scale ultrasonography - a preliminary study. Rheumatology (Oxford). 2008;47:54–8.CrossRef

36.

Ogishima H, Tsuboi H, Umeda N, Horikoshi M, Kondo Y, Sugihara M. Analysis of subclinical synovitis detected by ultrasonography and low-field magnetic resonance imaging in patients with rheumatoid arthritis. Mod Rheumatol. 2014;24:60–8.PubMedCrossRef

37.

Mendonca J, Yazbek M, Laurindo I, Bertolo M. Wrist ultrasound analysis of patients with early rheumatoid arthritis. Braz J Med Biol Res. 2011;44:11–5.PubMedCrossRef

38.

Rezaei H, Torp-Pedersen S, af Klint E, Backheden M, Kisten Y, Gyori N, et al. Diagnostic utility of musculoskeletal ultrasound in patients with suspected arthritis - a probabilistic approach. Arthritis Res Ther. 2014;16:448–55.PubMedPubMedCentralCrossRef

39.

Ceponis A, Onishi M, Bluestein H, Kalunian K, Townsend J, Kavanaugh A. Utility of the ultrasound examination of the hand and wrist joints in the management of established rheumatoid arthritis. Arthritis Care Res. 2014;66:236–44.CrossRef

40.

Nakagomi D, Ikeda K, Okubo A, Iwamoto T, Sanayama Y, Takahashi K, et al. Ultrasound can improve the accuracy of the 2010 American College of Rheumatology/European league against rheumatism classification criteria for rheumatoid arthritis to predict the requirement for methotrexate treatment. Arthritis Rheum. 2013;65:890–8.PubMedCrossRef

41.

Szkudlarek M, Court-Payen M, Strandberg C, Klarlund M, Klausen T, Ostergaard M. Power Doppler ultrasonography for assessment of synovitis in the metacarpophalangeal joints of patients with rheumatoid arthritis: a comparison with dynamic magnetic resonance imaging. Arthritis Rheum. 2001;44:2018–23.PubMedCrossRef

42.

Baillet A, Gaujoux-Viala C, Mouterde G, Pham T, Tebib J, Saraux A, Fautrel B, Cantagrel A, Le Loët X, Gaudin P. Comparison of the efficacy of sonography, magnetic resonance imaging and conventional radiography for the detection of bone erosions in rheumatoid arthritis patients: a systematic review and meta-analysis. Rheumatology (Oxford). 2011;50:1137–47.CrossRef

43.

Ten Cate DF, Luime JJ, Swen N, Gerards AH, De Jager MH, Basoski NM. Role of ultrasonography in diagnosing early rheumatoid arthritis and remission of rheumatoid arthritis - a systematic review of the literature. Arthritis Res Ther. 2013;15:R4.PubMedPubMedCentralCrossRef

44.

Dougados M, DEvauchelle-Pensec V, Ferlet J, Jousse-Joulin S, D’Agostino M, Backhaus M. The ability of synovitis to predict structural damage in rheumatoid arthritis: a comparative study between clinical examination and ultrasound. Ann Rheum Dis. 2013;72:665–71.PubMedCrossRef

45.

Brown A, Conaghan P, Karim Z, Quinn M, Ikeda K, Peterfy C, et al. An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis. Arthritis Rheum. 2008;58:2958–67.PubMedCrossRef

46.

Peluso G, Michelutti A, Bosello S, Gremese E, Toluso B, Ferraccioli G. Clinical and ultrasonographic remission determines different changes of relapse in early and long standing rheumatoid arthritis. Ann Rheum Dis. 2011;70:172–5.PubMedCrossRef

47.

Do Prado AD, Bisi M, Piovesan D, Bredemeieir M, Silveira I, Mendonça J, et al. Association of clinical examination with gray scale and power Doppler ultrassonography in established rheumatoid arthritis. J Clin Rheumatol. 2016; in press

48.

Yoshimi R, Toyota Y, Tsuchida N, Sugiyama Y, Kunishita Y, Kishimoto D, et al. Considerable discrepancy between Patient’s assessment and ultrasonography assessment on the most affected joint in rheumatoid arthritis [abstract]. Arthritis Rheumatol. 2015;67:S10.

49.

Filer A, de Pablo P, Allen G, Nightingale P, Jordan A, Jobanputra P. Utility of ultrasound joint counts in the prediction of rheumatoid arthritis in patients with very early synovitis. Ann Rheum Dis. 2011;70:500–7.PubMedCrossRef

50.

Smolen J, Van Der Heijde D, St Clair E, Emery P, Bathon J, Keystone E, et al. Predictors of joint damage in patients with early rheumatoid arthritis treated with high-dose methotrexate with or without concomitant infliximab: results from the ASPIRE trial. Arthritis Rheum. 2006;54:702–10.PubMedCrossRef

51.

Damjanov N, Radunovic G, Prodanovic S, Vukovic V, Milic V, SimicPasalic K. Construct validity and reliability of ultrasound disease activity score in assessing joint inflammation in RA: comparison with DAS-28. Rheumatology (Oxford). 2012;51:120–8.CrossRef

52.

Dale J, Purves D, McConnachie A, McInnes I, Porter D. Tightening up? Impact of musculoskeletal ultrasound disease activity assessment on early rheumatoid arthritis patients treated using a treat to target strategy. Arthritis Care Res. 2014;66:19–26.CrossRef

53.

Gärtner M, Mandl P, Radner H, Supp G, Machold K, Aletaha D, et al. Sonographic joint assessment in rheumatoid arthritis: associations with clinical joint assessment during a state of remission. Arthritis Rheum. 2013;65:2005–14.PubMedCrossRef

54.

Backhaus T, Ohrndorf S, Kellner H, Strunk J, Hartung W, Sattler H, et al. The US7 score is sensitive to change in a large cohort of patients with rheumatoid arthritis over 12 months of therapy. Ann Rheum Dis. 2013;72:1163–9.PubMedCrossRef

55.

Nguyen H, Ruyssen-Witrand A, Gandjbakhch F, Constantin A, Foltz V, Cantagrel A. Prevalence of ultrasound-detected residual synovitis and risk of relapse and structural progression in rheumatoid arthritis patients in clinical remission: a systematic review and meta-analysis. Rheumatology. 2014;53:2110–8.PubMedCrossRef

56.

Saleem B, Brown A, Quinn M, Karim Z, Hensor E, Conaghan P, et al. Can flare be predicted in DMARD treated RA patients in remission, and is it important? A cohort study. Ann Rheum Dis. 2012;71:1316–21.PubMedCrossRef

57.

Naredo E, Valor L, De la Torre I, Montoro M, Bello N, Martinez-Barrio J, et al. Predictive value of Doppler ultrasound-detected synovitis in relation to failed tapering of biologic therapy in patients with rheumatoid arthritis. Rheumatology. 2015;54:1408–14.PubMedCrossRef

58.

Marks J, Holroyd C, Dimitrov B, Armstrong R, Calogeras A, Cooper C, et al. Does combined clinical and ultrasound assessment allow selection of individuals with rheumatoid arthritis for susteined reduction of anti-tumor necrosis factor therapy? Arthritis Care Res. 2015;67:746–53.CrossRef

59.

Gärtner M, Alasti F, Supp G, Mandl P, Smolen J, Aletaha D. Persistence of subclinical sonographic joint activity in rheumatoid arthritis in sustained clinical remission. Ann Rheum Dis. 2015;74:2050–3.PubMedCrossRef

60.

Foltz V, Gandjbakhch F, Etchepare F, Rosenberg C, Tanguy M, Rozenberg S, et al. Power Doppler ultrasound, but not low-field magnetic resonance imaging, predicts relapse and radiographic disease progression in rheumatoid arthritis patients with low levels of disease activity. Arthritis Rheum. 2012;64:67–76.PubMedCrossRef

61.

Scirè C, Montecucco C, Codullo V, Epis O, Todoerti M, Caporali R. Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatol. 2009;48:1092–7.CrossRef

62.

Zufferey P, Möller B, Brulhart L, Tamborrini G, Scherer A, Finckh A, et al. Persistence of ultrasound synovitis in patients with rheumatoid arthritis fulfilling the DAS28 and/or the new ACR/EULAR RA remission definitions: results of an observational cohort study. Joint Bone Spine. 2014;81:426–32.PubMedCrossRef

63.

Yoshimi R, Hama M, Takase K, Ihata A, Kishimoto D, Terauchi K, et al. Ultrasonography is a potent tool for the prediction of progressive joint destruction during clinical remission of rheumatoid arthritis. Mod Rheumatol. 2013;23:456–65.PubMedCrossRef

64.

da Silva Chakr RM, Brenol JC, Behar M, Mendonça JA, Kohem CL, Monticielo OA, et al. Is ultrasound a better target than clinical disease activity scores in rheumatoid arthritis with fibromyalgia? A case-control study. PLoS One. 2015;10:e0118620.PubMedPubMedCentralCrossRef

65.

Iagnocco A, Finucci A, Ceccarelli F, Perricone C, Iorgoveanu V, Valesini G. Power Doppler ultrasound monitoring of response to anti-tumour necrosis factor alpha treatment in patients with rheumatoid arthritis. Rheumatology (Oxford). 2015;54:1890–6.CrossRef

66.

Montoro Alvarez M, Chong OY, Janta I, González C, López-Longo J, Monteagudo I, Valor L, et al. Relation of Doppler ultrasound synovitis versus clinical synovitis with changes in native complement component levels in rheumatoid arthritis patients treated with biologic disease-modifying anti-rheumatic drugs. Clin Exp Rheumatol. 2015;33:141–5.PubMed

67.

Haavardsholm E, Aga A, Olsen I, Hammer H, Uhlig T, Fremstad H, et al. Aiming for remission in rheumatoid arthritis: clinical and radiographic outcomes from a randomized controlled strategy trial investigating the added value of ultrasonography in a treat-to-target regimen [abstract]. Arthritis Rheumatol. 2015;67:S10.

68.

Hart LE, Tugwell P, Buchanan WW, Norman GR, Grace EM, Southwell D. Grading of tenderness as a source of interrater error in the Ritchie articular index. J Rheumatol. 1985;12:716–7.PubMed

69.

Thompson PW, Hart LE, Goldsmith CH, Spector TD, Bell MJ, Ramsden MF. Comparison of four articular indices for use in clinical trials in rheumatoid arthritis: patient, order and observer variation. J Rheumatol. 1991;18:661–5.PubMed

70.

Strunk J, Strube K, Rumbaur C, Lange U, Müller-Ladner U. Interobserver agreement in two- and three-dimensional power Doppler sonographic assessment of synovial vascularity during anti-inflammatory treatment in patients with rheumatoid arthritis. Ultraschall Med. 2007;28:409–15.PubMedCrossRef

71.

Fodor D, Felea I, Popescu D, Motei A, Ene P, Serban O, Micu M. Ultrasonography of the metacarpophalangeal joints in healthy subjects using an 18 MHz transducer. Med Ultrason. 2015;17:185–91.PubMedCrossRef

72.

Filippucci E, da Luz KR, Di Geso L, Salaffi F, Tardella M, Carotti M, et al. Interobserver reliability of ultrasonography in the assessment of cartilage damage in rheumatoid arthritis. Ann Rheum Dis. 2010;69:1845–8.PubMedCrossRef

73.

Sant'Ana Petterle G, Natour J, Rodrigues da Luz K, Soares Machado F, dos Santos MF, da Rocha Correa Fernandes A, et al. Usefulness of US to show subclinical joint abnormalities in asymptomatic feet of RA patients compared to healthy controls. Clin Exp Rheumatol. 2013;31:904–12.PubMed

74.

Luz KR, Furtado R, Mitraud SV, Porglhof J, Nunes C, Fernandes AR, Natour J. Interobserver reliability in ultrasound assessment of rheumatoid wrist joints. ActaReumatol Port. 2011;36:245–50.

75.

Szkudlarek M, Court-Payen M, Jacobsen S, Klarlund M, Thomsen HS, Østergaard M. Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum. 2003;48:955–62.PubMedCrossRef

76.

Zufferey P, Brulhart L, Tamborrini G, Finckh A, Scherer A, Moller B, et al. Ultrasound evaluation of synovitis in RA: correlation with clinical disease activity and sensitivity to change in an observational cohort study. Jt Bone Spine. 2014;81:222–7.CrossRef

77.

Brulhart L, Ziswiler HR, Tamborrini G, Zufferey P, SONAR/SCQM programmes. The importance of sonographer experience and machine quality with regards to the role of musculoskeletal ultrasound in routine care of rheumatoid arthritis patients. Clin Exp Rheumatol. 2015;33:98–101.PubMed

78.

Scheel AK, Schmidt WA, Hermann KG, Bruyn GA, D'Agostino MA, Grassi W, et al. Interobserver reliability of rheumatologists performing musculoskeletal ultrasonography: results from a EULAR "train the trainers" course. Ann Rheum Dis. 2005;64:1043–9.PubMedPubMedCentralCrossRef

79.

Ohrndorf S, Fischer IU, Kellner H, Strunk J, Hartung W, Reiche B, et al. Reliability of the novel 7-joint ultrasound score: results from an inter- and intraobserver study performed by rheumatologists. Arthritis Care Res (Hoboken). 2012;64:1238–43.

80.

Bisi M, do Prado A, Rabelo C, Brollo F, da Silveira I, JA M, et al. Articular ultrasonography: interobserver reliability in rheumatoid arthritis. Rev Bras Reumatol. 2014;54:250–4.PubMedCrossRef

81.

Vlad V, Berghea F, Iagnocco A, Micu M, Damjanov N, Skakic V, et al. Inter & intra-observer reliability of grading ultrasound videoclips with hand pathology in rheumatoid arthritis by using non- sophisticated internet tools (LUMINA study). Med Ultrason. 2014;16:32–6.PubMedCrossRef

82.

Cheung PP, Kong KO, Chew LC, Chia FL, Law WG, Lian TY, Tan YK, Cheng YK. Achieving consensus in ultrasonography synovitis scoring in rheumatoid arthritis. Int J Rheum Dis. 2014;17:776–81.PubMedCrossRef

83.

Naredo E, Bonilla G, Gamero F, Uson J, Carmona L, Laffon A. Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrassonography. Ann Rheum Dis. 2005;64:375–81.PubMedPubMedCentralCrossRef

84.

Carotti M, Salaffi F, Morbiducci J, Ciapetti A, Bartolucci L, Gasparini S, et al. Colour Doppler ultrasonography evaluation of vascularization in the wrist and finger joints in rheumatoid arthritis patients and healthy subjects. Eur J Radiol. 2012;81:1834–8.PubMedCrossRef

85.

Wakefield R, Balint P, Szkudlarek M, Fillipucci E, Backhaus M, D’Agostino M. OMERACT 7 Special Interest Group. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol. 2005;32:2485–7.PubMed

86.

Scheel AK, Hermann KG, Kahler E, et al. A novel ultrasonografic synovitis scoring system suitable for analyzing finger joint inflammation in rheumatoid arthritis. Arthritis Rheum. 2005;52:733–43.PubMedCrossRef

87.

Loeuille D, Sommier JP. ScUSI, an ultrasound inflammatory score, predicts sharp progression at 7 months in RA patients. Arthritis Rheum. 2006;54:S139.

88.

Hensch A, Hermann KG. Impact of B mode, power Doppler and contrast enhanced ultrasonography in RA patients on anti-TNF alfa therapy. Arthritis Rheum. 2007;56:S280.CrossRef

89.

Iagnocco A, Filippucci E, Perella C, Ceccarelli F, Cassarà E, Alessandri C, et al. Clinical and ultrasonographic monitoring of response to adalimumabe treatment in rheumatoid arthritis. J Rheumatol. 2008;35:35–40.PubMed

90.

Naredo E, Rodríguez M, Campos C, Rodríguez-Heredia JM, Medina JA, Giner E, Martínez O, et al. Validity, reproducibility, and responsiveness of a twelve-joint simplified power dopplerultrasonographic assessment of joint inflammation in rheumatoid arthritis. Arthritis Rheum. 2008;59:515–22.PubMedCrossRef

91.

Backhaus M, Ohrndorf S, Kellner H, Strunk J, Backhaus T, Hartung W. Evaluation of a novel 7-joint ultrasound score in daily rheumatologic practise: a pilot project. Arthritis Rheum. 2009;61:1194–201.PubMedCrossRef

92.

Hammer HB, Sveinsson M, Kongtorp AK, Kvien TK. A 78-joints ultrasonographic assessment is associated with clinical assessments and is highly responsive to improvement in a longitudinal study of patients with rheumatoid arthritis starting adalimumab treatment. Ann Rheum Dis. 2010;69:1349–51.PubMedCrossRef

93.

Perricone C, Ceccarelli F, Modesti M, Vavala C, Di Franco M, Valesini G, Iagnocco A. The 6-joint ultrasonographic assessment: a valid, sensitive-to-change and feasible method for evaluating joint inflammation in RA. Rheumatology (Oxford). 2012;51:866–73.CrossRef

94.

Seymour M, Pétavy F, Chiesa F, Perry H, Lukey PT, Binks M, et al. Ultrasonographic measures of synovitis in an early phase clinical trial: a double-blind, randomized, placebo and comparator controlled phase IIa trial of GW274150 (a selective inducible nitric oxide synthase inhibitor in rheumatoid arthritis. Clin Exp Rheumatol. 2012;30:254-61.

95.

Mendonça JA, Yazbek MA, Costallat BL, Gutiérrez M, Bértolo MB. The modified US7 score in the assessment of synovitis in early rheumatoid arthritis. Rev Bras Reumatol. 2014;54:287–94.PubMedCrossRef

96.

Yoshimi R, Ihata A, Kunishita Y, Kishimoto D, Kamiyama R, Minegishi K, et al. A novel 8-joint ultrasound score is useful in daily practice for rheumatoid arthritis. Mod Rheumatol. 2015;25:379–85.PubMedCrossRef

97.

Janta I, Valor L, De la Torre I, MartínezEstupiñán L, Nieto JC, Ovalles-Bonilla JG, et al. Ultrasound-detected activity in rheumatoid arthritis on methotrexate therapy: which joints and tendons should be assessed to predict unstable remission? Rheumatol Int. 2016;36:387–96.PubMedCrossRef

98.

Leng X, Xiao W, Xu Z, Zhu X, Liu Y, Zhao D, et al. Ultrasound7 versus ultrasound12 in monitoring the response to infliximab in patients with rheumatoid arthritis. Clin Rheumatol. 2016;35:587–95.PubMedCrossRef

99.

Aga A, Lie E, Olsen I, Hammer H, Uhlig T, van der Heijde D, et al. Development of an ultrasound joint inflammation score for rheumatoid arthritis through a data-driven approach. Arthritis Rheumatol. 2015;67:S10.

100.

Aga AB, Hammer HB, Olsen IC, Uhlig T, Kvien TK, van der Heijde D, et al. First step in the development of an ultrasound joint inflammation score for rheumatoid arthritis using a data-driven approach. Ann Rheum Dis. 2016;75:1444–51.PubMedCrossRef

101.

Mandl P, Naredo E, Wakefield R, Conaghan P, D’Agostino M, OMERACT Ultrasound Task Force, et al. A systematic literature review analysis of ultrasound joint count and scoring systems to assess synovitis in rheumatoid arthritis according to the OMERACT filter. J Rheumatol. 2011;38:2055–62.PubMedCrossRef

102.

Wakefield RJ, D'Agostino MA, Naredo E, Buch MH, Iagnocco A, Terslev L, et al. After treat-to-target: can a targeted ultrasound initiative improve RA outcomes? Ann Rheum Dis. 2012;71:799–803.PubMedCrossRef

103.

Gutierrez M, Okano T, Reginato AM, Cazenave T, Ventura-Rios L, Bertolazzi C, Pineda C. Pan-American League Against Rheumatisms (PANLAR) Ultrasound Study Group. New Ultrasound Modalities in Rheumatology. J Clin Rheumatol. 2015;21:427–34.PubMedCrossRef

104.

Terslev L, Torp-Pedersen E, Qvistgaard E, von der Recke P, Bliddal H. Doppler ultrasound findings in healthy wrists and finger joints. Ann Rheum Dis. 2004;63:644–8.PubMedPubMedCentralCrossRef

105.

Vlad V, Micu M, Porta F, Radunovic G, Nestorova R, Petranova T, et al. Ultrasound of the hand and wrist in rheumatology. Med Ultrason. 2012;14:42–8.PubMed

Medicine Matters Rheumatology

Abstract