Magnetic Resonance Imaging of the Synovium in Rheumatoid Arthritis

ABSTRACT

Early diagnosis, followed by early initiation and optimal adjustments of aggressive therapies, are acknowledged as essential to optimize long-term clinical and radiological outcome in rheumatoid arthritis (RA). This requires sensitive methods for detection and monitoring of the primary feature of RA-the synovitis. In comparison with conventional methods, magnetic resonance imaging (MRI) offers assessment of the rheumatoid synovium with improved sensitivity to early pathology and to change. Various aspects such as volume, vascularity, and edema can be assessed by different metrological approaches. MRI findings are of prognostic value to the long-term radiological outcome. This article reviews current knowledge on MRI for assessment of the synovium in RA, focusing on the validity of MRI measures of synovitis. Future perspectives and suggested research priorities are described. The rationale is provided for MRI becoming the new gold standard for assessment of RA joints and for MRI assessments of synovitis being reliable and valid measures of rheumatoid disease activity.

Rheumatoid arthritis - synovitis - magnetic resonance imaging

REFERENCES

• 1 Boers M, Verhoeven A C, Markusse H M et al.. Randomised comparison of combined step-down prednisolone, methotrexate and sulphasalazine with sulphasalazine alone in early rheumatoid arthritis.  Lancet. 1997;  350 309-318
• 2 Egsmose C, Lund B, Borg G et al.. Patients with rheumatoid arthritis benefit from early 2nd line therapy: 5 year followup of a prospective double blind placebo controlled study.  J Rheumatol. 1995;  22 2208-2213
• 3 Landewe R B, Boers M, Verhoeven A C et al.. COBRA combination therapy in patients with early rheumatoid arthritis: long-term structural benefits of a brief intervention.  Arthritis Rheum. 2002;  46 347-356
• 4 O'Dell J R. Treating rheumatoid arthritis early: a window of opportunity?.  Arthritis Rheum. 2002;  46 283-285
• 5 Lipsky P E, van der Heijde D M FM, StClair E W et al.. Infliximab and methotrexate in the treatment of rheumatoid arthritis.  N Engl J Med. 2000;  343 1594-1602
• 6 Bathon J M, Martin R W, Fleischmann R M et al.. A comparison of etanercept and methotrexate in patients with early rheumatoid arthritis.  N Engl J Med. 2000;  343 1586-1593
• 7 Cohen S, Hurd E, Cush J et al.. Treatment of rheumatoid arthritis with anakinra, a recombinant human interleukin-1 receptor antagonist, in combination with methotrexate: results of a twenty-four-week, multicenter, randomized, double-blind, placebo-controlled trial.  Arthritis Rheum. 2002;  46 614-624
• 8 Emery P. The optimal management of early rheumatoid disease: the key to preventing disability.  Br J Rheumatol. 1994;  33 765-768
• 9 Keystone E, Kavanaugh A, Sharp J et al.. Adalimumab (D2E7), a fully human anti-TNF-alfa monoclonal antibody, inhibits the progression of structural joint damage in patients with active RA despite concomitant methotrexate therapy. Arthritis Rheum 2002 46: S205 (Abstract)
• 10 Klarlund M, Østergaard M, Jensen K E et al.. Magnetic resonance imaging, radiography and scintigraphy of the finger joints: one year follow up of patients with early arthritis.  Ann Rheum Dis. 2000;  59 521-528
• 11 Backhaus M, Kamradt T, Sandrock D et al.. Arthritis of the finger joints. A comprehensive approach comparing conventional radiography, scintigraphy, ultrasound, and contrast-enhanced magnetic resonance imaging.  Arthritis Rheum. 1999;  42 1232-1245
• 12 Backhaus M, Burmester G R, Sandrock D et al.. Prospective two year follow up study comparing novel and conventional imaging procedures in patients with arthritic finger joints.  Ann Rheum Dis. 2002;  61 895-904
• 13 Szkudlarek M, Østergaard M, Court-Payen M et al.. Evaluation of erosions, synovitis and effusions in hand and finger joints in rheumatoid arthritis: a comparison of high resolution ultrasonography, magnetic resonance imaging and conventional radiography. Arthritis Rheum 1999 42(Suppl.): S133 (Abstract)
• 14 Scott D L, Grindulis K A, Struthers G R, Coulton B L, Popert A J, Bacon P A. Progression of radiological changes in rheumatoid arthritis.  Ann Rheum Dis. 1984;  43 8-17
• 15 Brower A C. Rheumatoid arthritis. Imaging. In: Klippel JH, Dieppe PA, editors. Rheumatology. London: Mosby-Year Book Europe Limited. 1994: 3.6.1-3.6.8
• 16 McQueen F M, Stewart N, Crabbe J et al.. Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals a high prevalence of erosion at four months after symptom onset.  Ann Rheum Dis. 1998;  57 350-356
• 17 Østergaard M. Magnetisk resonans billeddannelse ved reumatoid artrit. En sammenligning med ultralydundersøgelse og konventionel røntgenundersøgelse [Magnetic resonance imaging in rheumatoid arthritis. A comparison with ultrasonography and conventional radiography]. University of Copenhagen Denmark; 1996 (Ph.D. dissertation)
• 18 Klarlund M. Magnetic resonance imaging of wrist and finger joints in rheumatoid arthritis and early unclassified polyarthritis. University of Copenhagen Denmark; 2000 (Ph.D. dissertation)
• 19 Østergaard M. Magnetic resonance imaging in rheumatoid arthritis. Quantitative methods for assessment of the inflammatory process in peripheral joints (thesis). Dan Med Bull 1999 46: 313-344
• 20 Østergaard M, Hansen M, Stoltenberg M et al.. Magnetic resonance imaging-determined synovial membrane volume as a marker of disease activity and a predictor of progressive joint destruction in the wrists of patients with rheumatoid arthritis.  Arthritis Rheum. 1999;  42 918-929
• 21 McGonagle D, Conaghan P, O'Connor P et al.. The relationship between synovitis and bone changes in early untreated rheumatoid arthritis. A controlled magnetic resonance imaging study.  Arthritis Rheum. 1999;  42 1706-1711
• 22 Conaghan P G, O'Connor P, McGonagle D et al.. Elucidation of the relationship between synovitis and bone damage: a randomized magnetic resonance imaging study of individual joints in patients with early rheumatoid arthritis.  Arthritis Rheum. 2003;  48 64-71
• 23 McQueen F M, Stewart N, Crabbe J et al.. Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals progression of erosions despite clinical improvement.  Ann Rheum Dis. 1999;  58 156-163
• 24 Lindegaard H, Hørslev-Petersen K, Vallø J, Junker P, Østergaard M.. Baseline MRI erosions in early rheumatoid arthritis MCP- and wrist joint bones markedly increase the risk of radiographic erosions at 1 year follow-up. Arthritis Rheum 2002 46(Suppl.): S521 (Abstract)
• 25 Østergaard M, Hansen M, Stoltenberg M et al.. New radiographic bone erosions in rheumatoid arthritis wrists are detectable with MRI a median of 2 years earlier.  Arthritis Rheum. 2003;  48 2128-2131
• 26 Benton N M, Perry D, Crabbe J, Stewart N, Robinson E, Yeoman S et al.. Magnetic resonance scanning at first presentation predicts modified sharp score at six years in patients with rheumatoid arthritis. Arthritis Rheum 2002 46(Suppl.): S370 (Abstract)
• 27 Felson D T, Anderson J J, Boers M et al.. The American College of Rheumatology preliminary core set of disease activity measures for rheumatoid arthritis clinical trials.  Arthritis Rheum. 1993;  36 729-740
• 28 Resnick D. Common disorders of synovium-lined joints: pathogenesis, imaging abnormalities, and complications.  AJR Am J Roentgenol. 1988;  151 1079-1093
• 29 Harris Jr E D. Etiology and pathogenesis of rheumatoid arthritis. In: Kelley WN, Harris ED Jr, Ruddy S, Sledge CB Textbook of Rheumatology Philadelphia, PA; W.B. Saunders Company 1993: 833-873
• 30 Firestein G. Rheumatoid arthritis. Rheumatoid synovitis and pannus. In: Klippel JH, Dieppe PA Rheumatology London; Mosby-Year Book Europe Limited 1994: 3.12.1-3.12.30
• 31 Reiser M F, Bongartz G P, Erlemann R et al.. Gadolinium-DTPA in rheumatoid arthritis and related diseases: first results with dynamic magnetic resonance imaging.  Skeletal Radiol. 1989;  18 591-597
• 32 König H, Sieper J, Wolf K J. Rheumatoid arthritis: evaluation of hypervascular and fibrous pannus with dynamic MR imaging enhanced with gd-DTPA.  Radiology. 1990;  176 473-477
• 33 Yamato M, Tamai K, Yamaguchi T, Ohno W. MRI of the knee in rheumatoid arthritis: Gd-DTPA perfusion dynamics.  J Comput Assist Tomogr. 1993;  17 781-785
• 34 Østergaard M, Lorenzen I, Henriksen O. Dynamic gadolinium-enhanced MR imaging in active and inactive immunoinflammatory gonarthritis.  Acta Radiol. 1994;  35 275-281
• 35 Weinmann H-J, Brasch R C. Press W-R, Wesbye GE. Characteristics of gadolinium-DTPA complex: a potential NMR contrast agent.  AJR Am J Roentgenol. 1984;  142 619-624
• 36 Simkin P A, Pizzorno J E. Synovial permeability in rheumatoid arthritis.  Arthritis Rheum. 1979;  22 689-696
• 37 Levick J R. Permeability of rheumatoid and normal human synovium to specific plasma proteins.  Arthritis Rheum. 1981;  24 1550-1560
• 38 Østergaard M, Stoltenberg M, Henriksen O, Lorenzen I. Quantitative assessment of synovial inflammation by dynamic gadolinium-enhanced MRI. A study of the effect of intraarticular methylprednisolone on the rate of early synovial enhancement.  Br J Rheumatol. 1996;  35 50-59
• 39 Østergaard M, Stoltenberg M, Løvgreen-Nielsen P, Volck B, Sonne-Holm S, Lorenzen I. Quantification of synovitis by MRI: correlation between dynamic and static gadolinium-enhanced MRI and microscopic and macroscopic signs of synovial inflammation.  Mag Reson Imaging. 1998;  16 743-754
• 40 Gaffney K, Cookson J, Blake D, Coumbe A, Blades S. Quantification of rheumatoid synovitis by magnetic resonance imaging.  Arthritis Rheum. 1995;  38 1610-1617
• 41 Tamai K, Yamato M, Yamaguchi T, Ohno W. Dynamic magnetic resonance imaging for the evaluation of synovitis in patients with rheumatoid arthritis.  Arthritis Rheum. 1994;  37 1151-1157
• 42 Nakahara N, Uetani M, Hayashi K, Kawashara Y, Matsumoto T, Oda J. Gadolinium-enhanced MR imaging of the wrist in rheumatoid arthritis: value of fat suppression pulse sequences.  Skeletal Radiol. 1996;  25 639-647
• 43 Østergaard M, O'Connor P, Conaghan P et al.. Is intravenous contrast injection necessary for MRI assessment of inflammatory and destructive changes in rheumatoid arthritis wrist and MCP-joints? ESSR 2002 Book of abstracts. 2002: 141 (Abstract)
• 44 Rinck P A, Jones R A, Kværness J, Southon T E. Magnetic resonance in medicine. The basic textbook of the European Magnetic Resonance Forum. 3rd ed. Oxford Blackwell Scientific Publications 1993
• 45 Østergaard M, Gideon P, Henriksen O, Lorenzen I. Synovial volume-a marker of disease severity in rheumatoid arthritis? Quantification by MRI.  Scand J Rheumatol. 1994;  23 197-202
• 46 Waterton J C, Rajanayagam V, Ross B D, Brown D, Whittemore A, Johnstone D. Magnetic resonance methods for measurement of disease progression in rheumatoid arthritis.  Magn Reson Imaging. 1993;  11 1033-1038
• 47 Østergaard M, Stoltenberg M, Gideon P et al.. Effect of intraarticular osmic acid on synovial membrane volume and inflammation, determined by magnetic resonance imaging.  Scand J Rheumatol. 1995;  24 5-12
• 48 Østergaard M, Stoltenberg M, Henriksen O, Lorenzen I. The accuracy of MRI-determined synovial membrane and joint effusion volumes in arthritis. A comparison of pre- and post-aspiration volumes.  Scand J Rheumatol. 1995;  24 305-311
• 49 Østergaard M, Hansen M, Stoltenberg M, Lorenzen I. Quantitative assessment of the synovial membrane in the rheumatoid wrist. An easily obtained MRI-score reflects the synovial volume.  Br J Rheumatol. 1996;  35 965-971
• 50 Østergaard M, Stoltenberg M, Gideon P, Sørensen K, Henriksen O, Lorenzen I. Changes in synovial membrane and joint effusion volumes following intraarticular methylprednisolone. Quantitative assessment of inflammatory and destructive changes in rheumatoid arthritis by MRI.  J Rheumatol. 1996;  23 1151-1161
• 51 Polisson R P, Schoenberg O I, Fischman A et al.. Use of magnetic resonance imaging and positron emission tomography in the assessment of synovial volume and glucose metabolism in patients with rheumatoid arthritis.  Arthritis Rheum. 1995;  38 819-825
• 52 Palmer W E, Rosenthal D I, Schoenberg O I et al.. Quantification of inflammation in the wrist with gadolinium-enhanced MR imaging and PET with 2-[F-18]-fluoro-2-deoxy-D-glucose.  Radiology. 1995;  196 647-655
• 53 Østergaard M, Stoltenberg M, Løvgreen-Nielsen P, Volck B, Jensen C H, Lorenzen I. Magnetic resonance imaging-determined synovial membrane and joint effusion volumes in rheumatoid arthritis and osteoarthritis. Comparison with the macroscopic and microscopic appearance of the synovium.  Arthritis Rheum. 1997;  40 1856-1867
• 54 Sugimoto H, Takeda A, Kano S. Assessment of disease activity in rheumatoid arthritis using magnetic resonance imaging: quantification of pannus volume in the hands.  Br J Rheumatol. 1998;  37 854-861
• 55 Clunie G, Hall-Craggs M A, Paley M N et al.. Measurement of synovial lining volume by magnetic resonance imaging of the knee in chronic synovitis.  Ann Rheum Dis. 1997;  56 526-534
• 56 Clunie G, Wilkinson I D, Lui D et al.. Changes in articular synovial lining volume measured by magnetic resonance in a randomized, double-blind, controlled trial of intraarticular samarium-153 particulate hydroxyapatite for chronic knee synovitis.  Rheumatology. 1999;  38 113-117
• 57 Klarlund M, Østergaard M, Lorenzen I. Finger joint synovitis in rheumatoid arthritis: quantitative assessment by magnetic resonance imaging.  Rheumatology (Oxford). 1999;  38 66-72
• 58 Creamer P, Keen M, Zananiri F et al.. Quantitative magnetic resonance imaging of the knee: a method of measuring response to intra-articular treatments.  Ann Rheum Dis. 1997;  56 378-381
• 59 Rominger M B, Bernreuter W K, Kenney P J, Morgan S L, Blackburn W D, Alarcon G S. MR imaging of the hands in early rheumatoid arthritis: preliminary results.  Radiographics. 1993;  13 37-46
• 60 Yanagawa A, Takano K, Nishioka K, Shimada J, Mizushima Y, Ashida H. Clinical staging and gadolinium-DTPA enhanced images of the wrist in rheumatoid arthritis.  J Rheumatol. 1993;  20 781-784
• 61 Østergaard M, Gideon P, Sørensen K et al.. Scoring of synovial membrane hypertrophy and bone erosions by MR imaging in clinically active and inactive rheumatoid arthritis of the wrist.  Scand J Rheumatol. 1995;  24 212-218
• 62 Østergaard M, Klarlund M, Lassere M et al.. Interreader agreement in the assessment of magnetic resonance images of rheumatoid arthritis wrist and finger joints-an international multicenter study.  J Rheumatol. 2001;  28 1143-1150
• 63 Conaghan P, Lassere M, Østergaard M et al.. OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Exercise 4: An International Multicenter Longitudinal Study using the RA-MRI Score (RAMRIS).  J Rheumatol. 2003;  30 1376-1379
• 64 Lassere M, McQueen F, Østergaard M et al.. OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Exercise 3: An International Multicenter Reliability Study using the RA-MRI Score (RAMRIS).  J Rheumatol. 2003;  30 1366-1375
• 65 McQueen F, Lassere M, Edmonds J et al.. OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Development Of A Scoring System For MRI In Rheumatoid Arthritis: Summary of OMERACT 6 MR Imaging Module Magnetic resonance imaging of soft tissue changes in rheumatoid arthritis wrist joints.  J Rheumatol. 2003;  30 1387-1392
• 66 Østergaard M, Peterfy C, Conaghan P et al.. OMERACT Rheumatoid Arthritis Magnetic Resonance Imaging Studies. Core Set of MRI Acquisitions, Joint Pathology Definitions and Scoring System (OMERACT 2002 RAMRIS).  J Rheumatol. 2003;  30 1385-1386
• 67 Bird P, Lassere M, Shnier R, Edmonds J. Computerized measurement of magnetic resonance imaging erosion volumes in patients with rheumatoid arthritis: a comparison with existing magnetic resonance imaging scoring systems and standard clinical outcome measures.  Arthritis Rheum. 2003;  48 614-624
• 68 Corvetta A, Giovagnoni A, Baldelli S et al.. MR imaging of rheumatoid hand lesions: comparison with conventional radiology in 31 patients.  Clin Exp Rheumatol. 1992;  10 217-222
• 69 Jevtic V, Watt I, Rozman B et al.. Precontrast and postcontrast (Gd-DTPA) magnetic resonance imaging of hand joints in patients with rheumatoid arthritis.  Clin Radiol. 1993;  48 176-181
• 70 Jorgensen C, Cyteval C, Anaya J M, Baron M P, Lamarque J L, Sany J. Sensitivity of magnetic resonance imaging of the wrist in very early rheumatoid arthritis.  Clin Exp Rheumatol. 1993;  11 163-168
• 71 Sugimoto H, Takeda A, Masuyama J, Furuse M. Early-stage rheumatoid arthritis: diagnostic accuracy of MR imaging.  Radiology. 1996;  198 185-192
• 72 Sugimoto H, Takeda A, Hyodoh K. Early stage rheumatoid arthritis: Prospective study of the effectiveness of MR imaging for diagnosis.  Radiology. 2000;  216 569-575
• 73 Ostendorf B, Peters R, Dann P et al.. Magnetic resonance imaging and miniarthroscopy of metacarpophalangeal joints: sensitive detection of morphologic changes in rheumatoid arthritis.  Arthritis Rheum. 2001;  44 2492-2502
• 74 Szkudlarek M, Court-Payen M, Strandberg C, Klarlund M, Klausen T, Østergaard 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 2018-2023
• 75 Savnik A, Malmskov H, Thomsen H S et al.. MRI of the wrist and finger joints in inflammatory joint diseases at 1-year interval: MRI features to predict bone erosions.  Eur Radiol. 2002;  12 1203-1210
• 76 Huang J, Stewart N, Crabbe J et al.. A 1-year follow-up study of dynamic magnetic resonance imaging in early rheumatoid arthritis reveals synovitis to be increased in shared-epitope patients and predictive of erosions at 1 year.  Rheumatology (Oxford). 2000;  39 407-416
• 77 Reece R J, Kraan M C, Radjenovic A et al.. Comparative assessment of leflunomide and methotrexate for the treatment of rheumatoid arthritis, by dynamic enhanced magnetic resonance imaging.  Arthritis Rheum. 2002;  46 366-372
• 78 Rückmann A, Ehle B, Trampisch H-J. How to evaluate measuring methods in the case of non-defined external validity.  J Rheumatol. 1995;  22 1998-2000
• 79 Bruynesteyn K, van der Heijde D, Boers M et al.. Determination of the minimal clinically important difference in rheumatoid arthritis joint damage of the Sharp /van der Heijde and Larsen/Scott scoring methods by clinical experts and comparison with the smallest detectable difference.  Arthritis Rheum. 2002;  46 913-920
• 80 Arnett F C, Edworthy S M, Bloch D A et al.. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis.  Arthritis Rheum. 1988;  31 315-324
• 81 Jevtic V, Watt I, Rozman B, Kos-Golja M, Demsar F, Jarh O. Distinctive radiological features of small hand joints in rheumatoid arthritis and seronegative spondyloarthritis by contrast-enhanced (Gd-DTPA) magnetic resonance imaging.  Skeletal Radiol. 1995;  24 351-355
• 82 McGonagle D, Gibbon W, O'Connor P, Green M, Pease C, Emery P. Characteristic magnetic resonance imaging entheseal changes of knee synovitis in spondylarthropathy.  Arthritis Rheum. 1998;  41 694-700
• 83 Giovagnoni A, Grassi W, Terelli F et al.. MRI of the hand in psoriatic and rheumatical arthritis.  Eur Radiol. 1995;  5 590-595
• 84 Savnik A, Malmskov H, Thomsen H S et al.. MRI of the arthritic small joints: comparison of extremity MRI (0.2 T) vs high-field MRI (1.5 T).  Eur Radiol. 2001;  11 1030-1038
• 85 Lindegaard H, Vallø J, Hørslev-Petersen K, Junker P, Østergaard M. Low field dedicated magnetic resonance imaging in untreated rheumatoid arthritis of recent onset.  Ann Rheum Dis. 2001;  60 770-776
• 86 Ejbjerg B, Narvestad E, Szkudlarek M, Thomsen H S, Østergaard M. The sensitivity and specificity of low-field dedicated extremity MRI in patients with rheumatoid arthritis-a comparison with “conventional” high-field MRI.  Arthritis Rheum. 2001;  44 , (Abstract) S223
• 87 McQueen F M, Benton N, Crabbe J et al.. What is the fate of erosions in early rheumatoid arthritis? Tracking individual lesions using x rays and magnetic resonance imaging over the first two years of disease.  Ann Rheum Dis. 2001;  60 859-868