Magnetic Resonance Imaging of Rheumatoid Arthritis: Peripheral Joints and Spine

Monique Reijnierse; Annette van der Helm-Mil; Iris Eshed; Claudia Schueller-Weidekamm

doi:10.1055/s-0038-1639474

Seminars in Musculoskeletal Radiology, Inhaltsverzeichnis

Semin Musculoskelet Radiol 2018; 22(02): 127-146
DOI: 10.1055/s-0038-1639474

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Magnetic Resonance Imaging of Rheumatoid Arthritis: Peripheral Joints and Spine

Autor*innen

Monique Reijnierse

¹Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
Annette van der Helm-Mil

²Department of Rheumatology, Leiden University Medical Center, Leiden, The Netherlands
Iris Eshed

³Department of Radiology, Sheba Medical Center, affiliated with the Tel Aviv University, Tel Aviv, Israel
Claudia Schueller-Weidekamm

⁴Division of Neuroradiology and Musculoskeletal Radiology, Department of Biomedical Imaging und Image-guided Therapy, Medical University of Vienna/Vienna General Hospital, Vienna, Austria

Abstract

Both the fields of rheumatology and radiology are changing rapidly. Effective medication has become available for rheumatoid arthritis (RA) and transformed it from a progressive disabling disease into a chronic disease. Indications for magnetic resonance imaging (MRI) have changed accordingly, shifting toward early detection. There is also an overall increased clinical demand for high-end imaging. Together with improvement of MRI units and sequences, MRI protocols are adapted based on clinical indications. This article addresses (1) the clinical background and present role of MRI in early disease detection, (2) RA involvement of peripheral joints, (3) RA involvement of the spine, and (4) state-of-the-art RA MRI protocols. The key toward cost-effective MRI examination in RA is communication between radiologist and rheumatologist as well as awareness and knowledge of the basics and advancements in both fields.

Keywords

rheumatoid arthritis - magnetic resonance imaging - joints - spine - inflammation

Volltext

Referenzen

References
1 Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010; 376 (9746): 1094-1108
2 Ajeganova S, van Steenbergen HW, van Nies JA, Burgers LE, Huizinga TW, van der Helm-van Mil AH. Disease-modifying antirheumatic drug-free sustained remission in rheumatoid arthritis: an increasingly achievable outcome with subsidence of disease symptoms. Ann Rheum Dis 2016; 75 (05) 867-873
3 Smolen JS, Breedveld FC, Burmester GR. , et al. Treating rheumatoid arthritis to target: 2014 update of the recommendations of an international task force. Ann Rheum Dis 2016; 75 (01) 3-15
4 van Nies JA, Krabben A, Schoones JW, Huizinga TW, Kloppenburg M, van der Helm-van Mil AH. What is the evidence for the presence of a therapeutic window of opportunity in rheumatoid arthritis? A systematic literature review. Ann Rheum Dis 2014; 73 (05) 861-870
5 Nell VP, Machold KP, Eberl G, Stamm TA, Uffmann M, Smolen JS. Benefit of very early referral and very early therapy with disease-modifying anti-rheumatic drugs in patients with early rheumatoid arthritis. Rheumatology (Oxford) 2004; 43 (07) 906-914
6 Finckh A, Liang MH, van Herckenrode CM, de Pablo P. Long-term impact of early treatment on radiographic progression in rheumatoid arthritis: a meta-analysis. Arthritis Rheum 2006; 55 (06) 864-872
7 Gerlag DM, Raza K, van Baarsen LGM. , et al. EULAR recommendations for terminology and research in individuals at risk of rheumatoid arthritis: report from the Study Group for Risk Factors for Rheumatoid Arthritis. Ann Rheum Dis 2012; 71 (05) 638-641
8 van Steenbergen HW, Aletaha D, Beaart-van de Voorde LJ. , et al. EULAR definition of arthralgia suspicious for progression to rheumatoid arthritis. Ann Rheum Dis 2017; 76 (03) 491-496
9 Burgers LE, Siljehult F, Ten Brinck RM. , et al. Validation of the EULAR definition of arthralgia suspicious for progression to rheumatoid arthritis. Rheumatology (Oxford) 2017; 56 (12) 2123-2128
10 Knevel R, Huizinga TWJ, Kurreeman F. Genomic influences on susceptibility and severity of rheumatoid arthritis. Rheum Dis Clin North Am 2017; 43 (03) 347-361
11 van de Stadt LA, Witte BI, Bos WH, van Schaardenburg D. A prediction rule for the development of arthritis in seropositive arthralgia patients. Ann Rheum Dis 2013; 72 (12) 1920-1926
12 van Zanten A, Arends S, Roozendaal C. , et al. Presence of anticitrullinated protein antibodies in a large population-based cohort from the Netherlands. Ann Rheum Dis 2017; 76 (07) 1184-1190
13 Aletaha D, Neogi T, Silman AJ. , et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2010; 62 (09) 2569-2581
14 van Steenbergen HW, van Nies JA, Huizinga TW, Bloem JL, Reijnierse M, van der Helm-van Mil AH. Characterising arthralgia in the preclinical phase of rheumatoid arthritis using MRI. Ann Rheum Dis 2015; 74 (06) 1225-1232
15 van Steenbergen HW, Mangnus L, Reijnierse M, Huizinga TW, van der Helm-van Mil AH. Clinical factors, anticitrullinated peptide antibodies and MRI-detected subclinical inflammation in relation to progression from clinically suspect arthralgia to arthritis. Ann Rheum Dis 2016; 75 (10) 1824-1830
16 Nieuwenhuis WP, van Steenbergen HW, Mangnus L. , et al. Evaluation of the diagnostic accuracy of hand and foot MRI for early rheumatoid arthritis. Rheumatology (Oxford) 2017; 56 (08) 1367-1377
17 Nieuwenhuis WP, van Steenbergen HW, Stomp W. , et al. The course of bone marrow edema in early undifferentiated arthritis and rheumatoid arthritis: a longitudinal magnetic resonance imaging study at bone level. Arthritis Rheumatol 2016; 68 (05) 1080-1088
18 Nieuwenhuis WP, Mangnus L, van Steenbergen HW. , et al. Older age is associated with more MRI-detected inflammation in hand and foot joints. Rheumatology (Oxford) 2016; 55 (12) 2212-2219
19 Boer AC, Burgers LE, Mangnus L. , et al. Using a reference when defining an abnormal MRI reduces false-positive MRI results—a longitudinal study in two cohorts at risk for rheumatoid arthritis. Rheumatology (Oxford) 2017; 56 (10) 1700-1706
20 Backhaus M, Burmester GR, 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 (10) 895-904
21 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 (06) 1232-1245
22 Lindegaard HM, Vallø J, Hørslev-Petersen K, Junker P, Østergaard M. Low-cost, low-field dedicated extremity magnetic resonance imaging in early rheumatoid arthritis: a 1-year follow-up study. Ann Rheum Dis 2006; 65 (09) 1208-1212
23 Eshed I, Althoff CE, Schink T. , et al. Low-field MRI for assessing synovitis in patients with rheumatoid arthritis. Impact of Gd-DTPA dose on synovitis scoring. Scand J Rheumatol 2006; 35 (04) 277-282
24 Duer-Jensen A, Ejbjerg B, Albrecht-Beste E. , et al. Does low-field dedicated extremity MRI (E-MRI) reliably detect bone erosions in rheumatoid arthritis? A comparison of two different E-MRI units and conventional radiography with high-resolution CT scanning. Ann Rheum Dis 2009; 68 (08) 1296-1302
25 Østergaard M, Peterfy C, Conaghan P. , et al. OMERACT rheumatoid arthritis magnetic resonance imaging studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERACT RA-MRI scoring system. J Rheumatol 2003; 30 (06) 1385-1386
26 Sudoł-Szopińska I, Jurik AG, Eshed I. , et al. Recommendations of the ESSR Arthritis Subcommittee for the use of magnetic resonance imaging in musculoskeletal rheumatic diseases. Semin Musculoskelet Radiol 2015; 19 (04) 396-411
27 Stomp W, Krabben A, van der Heijde D. , et al. Aiming for a shorter rheumatoid arthritis MRI protocol: can contrast-enhanced MRI replace T2 for the detection of bone marrow oedema?. Eur Radiol 2014; 24 (10) 2614-2622
28 Mayerhoefer ME, Breitenseher MJ, Kramer J, Aigner N, Norden C, Hofmann S. STIR vs. T1-weighted fat-suppressed gadolinium-enhanced MRI of bone marrow edema of the knee: computer-assisted quantitative comparison and influence of injected contrast media volume and acquisition parameters. J Magn Reson Imaging 2005; 22 (06) 788-793
29 Schmid MR, Hodler J, Vienne P, Binkert CA, Zanetti M. Bone marrow abnormalities of foot and ankle: STIR versus T1-weighted contrast-enhanced fat-suppressed spin-echo MR imaging. Radiology 2002; 224 (02) 463-469
30 Tamai M, Kawakami A, Uetani M. , et al. Magnetic resonance imaging (MRI) detection of synovitis and bone lesions of the wrists and finger joints in early-stage rheumatoid arthritis: comparison of the accuracy of plain MRI-based findings and gadolinium-diethylenetriamine pentaacetic acid-enhanced MRI-based findings. Mod Rheumatol 2012; 22 (05) 654-658
31 Hetland ML, Ejbjerg B, Hørslev-Petersen K. , et al; CIMESTRA study group. MRI bone oedema is the strongest predictor of subsequent radiographic progression in early rheumatoid arthritis. Results from a 2-year randomised controlled trial (CIMESTRA). Ann Rheum Dis 2009; 68 (03) 384-390
32 Hetland ML, Stengaard-Pedersen K, Junker P. , et al; CIMESTRA study group. Radiographic progression and remission rates in early rheumatoid arthritis—MRI bone oedema and anti-CCP predicted radiographic progression in the 5-year extension of the double-blind randomised CIMESTRA trial. Ann Rheum Dis 2010; 69 (10) 1789-1795
33 Bøyesen P, Haavardsholm EA, Ostergaard M, van der Heijde D, Sesseng S, Kvien TK. MRI in early rheumatoid arthritis: synovitis and bone marrow oedema are independent predictors of subsequent radiographic progression. Ann Rheum Dis 2011; 70 (03) 428-433
34 McQueen FM, Benton N, Perry D. , et al. Bone edema scored on magnetic resonance imaging scans of the dominant carpus at presentation predicts radiographic joint damage of the hands and feet six years later in patients with rheumatoid arthritis. Arthritis Rheum 2003; 48 (07) 1814-1827
35 McQueen FM, 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 (03) 156-163
36 Whitten CG, Moore TE, Yuh WT, Kathol MH, Renfrew DL, Walker CW. The use of intravenous gadopentetate dimeglumine in magnetic resonance imaging of synovial lesions. Skeletal Radiol 1992; 21 (04) 215-218
37 Peterfy C, Edmonds J, Lassere M. , et al. OMERACT Rheumatoid Arthritis MRI Studies Module. J Rheumatol 2003; 30 (06) 1364-1365
38 McQueen FM. The MRI view of synovitis and tenosynovitis in inflammatory arthritis: implications for diagnosis and management. Ann N Y Acad Sci 2009; 1154: 21-34
39 Ostergaard M, Stoltenberg M, Løvgreen-Nielsen P, Volck B, Jensen CH, 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 (10) 1856-1867
40 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 (11) 2492-2502
41 Krabben A, Stomp W, Huizinga TW. , et al. Concordance between inflammation at physical examination and on MRI in patients with early arthritis. Ann Rheum Dis 2015; 74 (03) 506-512
42 Haavardsholm EA, Østergaard M, Ejbjerg BJ, Kvan NP, Kvien TK. Introduction of a novel magnetic resonance imaging tenosynovitis score for rheumatoid arthritis: reliability in a multireader longitudinal study. Ann Rheum Dis 2007; 66 (09) 1216-1220
43 Eshed I, Feist E, Althoff CE. , et al. Tenosynovitis of the flexor tendons of the hand detected by MRI: an early indicator of rheumatoid arthritis. Rheumatology (Oxford) 2009; 48 (08) 887-891
44 Nieuwenhuis WP, Krabben A, Stomp W. , et al. Evaluation of magnetic resonance imaging-detected tenosynovitis in the hand and wrist in early arthritis. Arthritis Rheumatol 2015; 67 (04) 869-876
45 Navalho M, Resende C, Rodrigues AM. , et al. Bilateral MR imaging of the hand and wrist in early and very early inflammatory arthritis: tenosynovitis is associated with progression to rheumatoid arthritis. Radiology 2012; 264 (03) 823-833
46 Möttönen TT. Prediction of erosiveness and rate of development of new erosions in early rheumatoid arthritis. Ann Rheum Dis 1988; 47 (08) 648-653
47 Ertel AN, Millender LH, Nalebuff E, McKay D, Leslie B. Flexor tendon ruptures in patients with rheumatoid arthritis. J Hand Surg Am 1988; 13 (06) 860-866
48 Visser H, le Cessie S, Vos K, Breedveld FC, Hazes JM. How to diagnose rheumatoid arthritis early: a prediction model for persistent (erosive) arthritis. Arthritis Rheum 2002; 46 (02) 357-365
49 van der Heijde DM. Joint erosions and patients with early rheumatoid arthritis. Br J Rheumatol 1995; 34 (02) (Suppl. 02) 74-78
50 McQueen FM, Stewart N, Crabbe J. , et al. Magnetic resonance imaging of the wrist in early rheumatoid arthritis reveals a high prevalence of erosions at four months after symptom onset. Ann Rheum Dis 1998; 57 (06) 350-356
51 Perry D, Stewart N, Benton N. , et al. Detection of erosions in the rheumatoid hand; a comparative study of multidetector computerized tomography versus magnetic resonance scanning. J Rheumatol 2005; 32 (02) 256-267
52 Døhn UM, Ejbjerg BJ, Hasselquist M. , et al. Detection of bone erosions in rheumatoid arthritis wrist joints with magnetic resonance imaging, computed tomography and radiography. Arthritis Res Ther 2008; 10 (01) R25
53 Smolen JS, van der Heijde DM, Aletaha D. , et al. Progression of radiographic joint damage in rheumatoid arthritis: independence of erosions and joint space narrowing. Ann Rheum Dis 2009; 68 (10) 1535-1540
54 Smolen JS, van der Heijde DM, Keystone EC. , et al. Association of joint space narrowing with impairment of physical function and work ability in patients with early rheumatoid arthritis: protection beyond disease control by adalimumab plus methotrexate. Ann Rheum Dis 2013; 72 (07) 1156-1162
55 Ostergaard M, Bøyesen P, Eshed I. , et al. Development and preliminary validation of a magnetic resonance imaging joint space narrowing score for use in rheumatoid arthritis: potential adjunct to the OMERACT RA MRI scoring system. J Rheumatol 2011; 38 (09) 2045-2050
56 Døhn UM, Conaghan PG, Eshed I. , et al. The OMERACT-RAMRIS rheumatoid arthritis magnetic resonance imaging joint space narrowing score: intrareader and interreader reliability and agreement with computed tomography and conventional radiography. J Rheumatol 2014; 41 (02) 392-397
57 Glinatsi D, Lillegraven S, Haavardsholm EA. , et al. Validation of the OMERACT Magnetic Resonance Imaging Joint Space Narrowing Score for the Wrist in a multireader longitudinal trial. J Rheumatol 2015; 42 (12) 2480-2485
58 Thevenon A, Cocheteux P, Duquesnoy B, Mestdagh H, Lecomte-Houcke M, Delcambre B. Subacromial bursitis with rice bodies as a presenting feature of seronegative rheumatoid arthritis. Arthritis Rheum 1987; 30 (06) 715-716
59 Popert AJ, Scott DL, Wainwright AC, Walton KW, Williamson N, Chapman JH. Frequency of occurrence, mode of development, and significance or rice bodies in rheumatoid joints. Ann Rheum Dis 1982; 41 (02) 109-117
60 Smith HJ, Larheim TA, Aspestrand F. Rheumatic and nonrheumatic disease in the temporomandibular joint: gadolinium-enhanced MR imaging. Radiology 1992; 185 (01) 229-234
61 Witulski S, Vogl TJ, Rehart S, Ottl P. Evaluation of the TMJ by means of clinical TMD examination and MRI diagnostics in patients with rheumatoid arthritis. BioMed Res Int 2014; 2014: 328560
62 Maijer KI, van der Leij C, de Hair MJ. , et al. Dynamic contrast-enhanced magnetic resonance imaging using pharmacokinetic modeling: initial experience in early arthritis patients. Arthritis Rheumatol 2016; 68: 587-596
63 Gaffney K, Cookson J, Blake D, Coumbe A, Blades S. Quantification of rheumatoid synovitis by magnetic resonance imaging. Arthritis Rheum 1995; 38 (11) 1610-1617
64 Ostergaard M, Stoltenberg M, Henriksen O, Lorenzen I. Quantitative assessment of synovial inflammation by dynamic gadolinium-enhanced magnetic resonance imaging. A study of the effect of intra-articular methylprednisolone on the rate of early synovial enhancement. Br J Rheumatol 1996; 35 (01) 50-59
65 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 (08) 1151-1157
66 König H, Sieper J, Wolf KJ. Rheumatoid arthritis: evaluation of hypervascular and fibrous pannus with dynamic MR imaging enhanced with Gd-DTPA. Radiology 1990; 176 (02) 473-477
67 Reece RJ, Kraan MC, 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 (02) 366-372
68 Axelsen MB, Poggenborg RP, Stoltenberg M. , et al. Reliability and responsiveness of dynamic contrast-enhanced magnetic resonance imaging in rheumatoid arthritis. Scand J Rheumatol 2013; 42 (02) 115-122
69 Rastogi A, Kubassova O, Krasnosselskaia LV. , et al. Evaluating automated dynamic contrast enhanced wrist 3T MRI in healthy volunteers: one-year longitudinal observational study. Eur J Radiol 2013; 82 (08) 1286-1291
70 Weber U, Hodler J, Jurik AG. , et al. Assessment of active spinal inflammatory changes in patients with axial spondyloarthritis: validation of whole body MRI against conventional MRI. Ann Rheum Dis 2010; 69 (04) 648-653
71 Althoff CE, Sieper J, Song IH. , et al. Active inflammation and structural change in early active axial spondyloarthritis as detected by whole-body MRI. Ann Rheum Dis 2013; 72 (06) 967-973
72 Axelsen MB, Eshed I, Duer-Jensen A, Møller JM, Pedersen SJ, Østergaard M. Whole-body MRI assessment of disease activity and structural damage in rheumatoid arthritis: first step towards an MRI joint count. Rheumatology (Oxford) 2014; 53 (05) 845-853
73 Arnett FC, Edworthy SM, Bloch DA. , et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31 (03) 315-324
74 Saraux A, Berthelot JM, Chalès G. , et al. Ability of the American College of Rheumatology 1987 criteria to predict rheumatoid arthritis in patients with early arthritis and classification of these patients two years later. Arthritis Rheum 2001; 44 (11) 2485-2491
75 Aletaha D, Neogi T, Silman AJ. , et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 2010; 62 (09) 2569-2581
76 Mjaavatten MD, Bykerk VP. Early rheumatoid arthritis: the performance of the 2010 ACR/EULAR criteria for diagnosing RA. Best Pract Res Clin Rheumatol 2013; 27 (04) 451-466
77 Sugimoto H, Takeda A, Hyodoh K. Early-stage rheumatoid arthritis: prospective study of the effectiveness of MR imaging for diagnosis. Radiology 2000; 216 (02) 569-575
78 Tamai M, Kita J, Nakashima Y. , et al. Combination of MRI-detected bone marrow oedema with 2010 rheumatoid arthritis classification criteria improves the diagnostic probability of early rheumatoid arthritis. Ann Rheum Dis 2014; 73 (12) 2219-2220
79 Nguyen HV, Ludwig SC, Silber J. , et al. Rheumatoid arthritis of the cervical spine. Spine J 2004; 4 (03) 329-334
80 Wasserman BR, Moskovich R, Razi AE. Rheumatoid arthritis of the cervical spine—clinical considerations. Bull NYU Hosp Jt Dis 2011; 69 (02) 136-148
81 Neva MH, Isomäki P, Hannonen P, Kauppi M, Krishnan E, Sokka T. Early and extensive erosiveness in peripheral joints predicts atlantoaxial subluxations in patients with rheumatoid arthritis. Arthritis Rheum 2003; 48 (07) 1808-1813
82 Paimela L, Laasonen L, Kankaanpää E, Leirisalo-Repo M. Progression of cervical spine changes in patients with early rheumatoid arthritis. J Rheumatol 1997; 24 (07) 1280-1284
83 Kauppi M, Anttila P. A stiff collar for the treatment of rheumatoid atlantoaxial subluxation. Br J Rheumatol 1996; 35 (08) 771-774
84 Laiho K, Soini I, Kautiainen H, Kauppi M. Can we rely on magnetic resonance imaging when evaluating unstable atlantoaxial subluxation?. Ann Rheum Dis 2003; 62 (03) 254-256
85 Reijnierse M, Breedveld FC, Kroon HM, Hansen B, Pope TL, Bloem JL. Are magnetic resonance flexion views useful in evaluating the cervical spine of patients with rheumatoid arthritis?. Skeletal Radiol 2000; 29 (02) 85-89
86 Vordenbäumen S, Schleich C, Lögters T. , et al. Dynamic contrast-enhanced magnetic resonance imaging of metacarpophalangeal joints reflects histological signs of synovitis in rheumatoid arthritis. Arthritis Res Ther 2014; 16 (05) 452
87 Currier B, Coblyn J. Cervical subluxation in rheumatoid arthritis. Available at: https://www.uptodate.com/contents/cervical-subluxation-in-rheumatoid-arthritis . Accessed March 23, 2018
88 Ranawat CS, O'Leary P, Pellicci P, Tsairis P, Marchisello P, Dorr L. Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am 1979; 61 (07) 1003-1010
89 Jurik AG. Imaging the spine in arthritis—a pictorial review. Insights Imaging 2011; 2 (02) 177-191
90 Younes M, Belghali S, Kriâa S. , et al. Compared imaging of the rheumatoid cervical spine: prevalence study and associated factors. Joint Bone Spine 2009; 76 (04) 361-368
91 Riew KD, Hilibrand AS, Palumbo MA, Sethi N, Bohlman HH. Diagnosing basilar invagination in the rheumatoid patient. The reliability of radiographic criteria. J Bone Joint Surg Am 2001; 83-A (02) 194-200
92 Aggarwal A, Kulshreshtha A, Chaturvedi V, Misra R. Cervical spine involvement in rheumatoid arthritis: prevalence and relationship with overall disease severity. J Assoc Physicians India 1996; 44 (07) 468-471
93 Joaquim AF, Ghizoni E, Tedeschi H, Appenzeller S, Riew KD. Radiological evaluation of cervical spine involvement in rheumatoid arthritis. Neurosurg Focus 2015; 38 (04) E4
94 Narváez JA, Narváez J, Serrallonga M. , et al. Cervical spine involvement in rheumatoid arthritis: correlation between neurological manifestations and magnetic resonance imaging findings. Rheumatology (Oxford) 2008; 47 (12) 1814-1819
95 Narváez JA, Narváez J, Roca Y, Aguilera C. MR imaging assessment of clinical problems in rheumatoid arthritis. Eur Radiol 2002; 12 (07) 1819-1828
96 Raskin RJ, Schnapf DJ, Wolf CR, Killian PJ, Lawless OJ. Computerized tomography in evaluation of atlantoaxial subluxation in rheumatoid arthritis. J Rheumatol 1983; 10 (01) 33-41
97 Sugiura T, Nagamoto Y, Iwasaki M. , et al. In vivo 3D kinematics of the upper cervical spine during head rotation in rheumatoid arthritis. J Neurosurg Spine 2014; 20 (04) 404-410
98 Czerny C, Grampp S, Henk CB, Neuhold A, Stiskal M, Smolen J. Rheumatoid arthritis of the craniocervical region: assessment and characterization of inflammatory soft tissue proliferations with unenhanced and contrast-enhanced CT. Eur Radiol 2000; 10 (09) 1416-1422
99 Ishii K, Matsumoto M, Takahashi Y. , et al. Risk factors for development of subaxial subluxations following atlantoaxial arthrodesis for atlantoaxial subluxations in rheumatoid arthritis. Spine 2010; 35 (16) 1551-1555
100 Matsunaga S, Sakou T, Onishi T. , et al. Prognosis of patients with upper cervical lesions caused by rheumatoid arthritis: comparison of occipitocervical fusion between c1 laminectomy and nonsurgical management. Spine 2003; 28 (14) 1581-1587 ; discussion 1587
101 Kim HJ, Nemani VM, Riew KD, Brasington R. Cervical spine disease in rheumatoid arthritis: incidence, manifestations, and therapy. Curr Rheumatol Rep 2015; 17 (02) 9