Novel Imaging Techniques in Rheumatic Diseases

Robert Hemke; Vasco Mascarenhas; Mario Maas

doi:10.1055/s-0038-1641160

Seminars in Musculoskeletal Radiology, Table of Contents

Semin Musculoskelet Radiol 2018; 22(02): 237-244
DOI: 10.1055/s-0038-1641160

Review Article

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

Novel Imaging Techniques in Rheumatic Diseases

Authors

Robert Hemke

¹Department of Radiology and Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam Movement Sciences, Amsterdam, The Netherlands

²Musculoskeletal Imaging Quantification Center (MIQC), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
Vasco Mascarenhas

³MSK imaging Unit (UIME), Imaging Center, Hospital da Luz, Lisbon, Portugal
Mario Maas

¹Department of Radiology and Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam Movement Sciences, Amsterdam, The Netherlands

²Musculoskeletal Imaging Quantification Center (MIQC), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands

Abstract

Since the introduction of new MR imaging techniques within the past two decades, the imaging assessment of joints in rheumatic diseases has changed considerably. MRI enables to evaluate both the inflamed synovial membrane as well as early structural damage. In the last few years, several new functional/metabolic MR imaging techniques have applied in rheumatic diseases, making it possible to evaluate the pathophysiology of the disease in greater detail. Moreover, they permit a more quantitative approach for the evaluation of disease activity and damage. Several functional imaging techniques in rheumatic diseases have been proposed for the evaluation and monitoring of disease status.

Keywords

magnetic resonance imaging - positron emission tomography - rheumatoid arthritis - juvenile idiopathic arthritis - spondylarthropathy

Full Text

References

References
1 O'Connor JP, Tofts PS, Miles KA, Parkes LM, Thompson G, Jackson A. Dynamic contrast-enhanced imaging techniques: CT and MRI. Br J Radiol 2011; 84 (Spec No 2): S112-S120
2 Sourbron S. Technical aspects of MR perfusion. Eur J Radiol 2010; 76 (03) 304-313
3 Khalifa F, Soliman A, El-Baz A. , et al. Models and methods for analyzing DCE-MRI: a review. Med Phys 2014; 41 (12) 124301
4 van de Sande MG, van der Leij C, Lavini C, Wijbrandts CA, Maas M, Tak PP. Characteristics of synovial inflammation in early arthritis analysed by pixel-by-pixel time-intensity curve shape analysis. Rheumatology (Oxford) 2012; 51 (07) 1240-1245
5 van der Leij C, van de Sande MG, Lavini C, Tak PP, Maas M. Rheumatoid synovial inflammation: pixel-by-pixel dynamic contrast-enhanced MR imaging time-intensity curve shape analysis--a feasibility study. Radiology 2009; 253 (01) 234-240
6 Cimmino MA, Innocenti S, Livrone F, Magnaguagno F, Silvestri E, Garlaschi G. Dynamic gadolinium-enhanced magnetic resonance imaging of the wrist in patients with rheumatoid arthritis can discriminate active from inactive disease. Arthritis Rheum 2003; 48 (05) 1207-1213
7 Axelsen MB, Stoltenberg M, Poggenborg RP. , et al. Dynamic gadolinium-enhanced magnetic resonance imaging allows accurate assessment of the synovial inflammatory activity in rheumatoid arthritis knee joints: a comparison with synovial histology. Scand J Rheumatol 2012; 41 (02) 89-94
8 Hemke R, Lavini C, Nusman CM. , et al. Pixel-by-pixel analysis of DCE-MRI curve shape patterns in knees of active and inactive juvenile idiopathic arthritis patients. Eur Radiol 2014; 24 (07) 1686-1693
9 Tofts PS, Brix G, Buckley DL. , et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 1999; 10 (03) 223-232
10 Lavini C, de Jonge MC, van de Sande MG, Tak PP, Nederveen AJ, Maas M. Pixel-by-pixel analysis of DCE MRI curve patterns and an illustration of its application to the imaging of the musculoskeletal system. Magn Reson Imaging 2007; 25 (05) 604-612
11 Kubassova O, Boesen M, Boyle RD. , et al. Fast and robust analysis of dynamic contrast enhanced MRI datasets. Med Image Comput Comput Assist Interv 2007; 10 (Pt 2): 261-269
12 Kubassova O, Boesen M, Cimmino MA, Bliddal H. A computer-aided detection system for rheumatoid arthritis MRI data interpretation and quantification of synovial activity. Eur J Radiol 2010; 74 (03) e67-e72
13 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
14 Ostergaard M, Stoltenberg M, Løvgreen-Nielsen P, Volck B, Sonne-Holm S, Lorenzen I. Quantification of synovistis by MRI: correlation between dynamic and static gadolinium-enhanced magnetic resonance imaging and microscopic and macroscopic signs of synovial inflammation. Magn Reson Imaging 1998; 16 (07) 743-754
15 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
16 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
17 Maijer KI, van der Leij C, de Hair MJ. , et al. Dynamic Contrast-Enhanced Magnetic Resonance Imaging Using Pharmacokinetic Modeling: Initial Experience in Patients With Early Arthritis. Arthritis Rheumatol 2016; 68 (03) 587-596
18 Cimmino MA, Barbieri F, Boesen M. , et al. Dynamic contrast-enhanced magnetic resonance imaging of articular and extraarticular synovial structures of the hands in patients with psoriatic arthritis. J Rheumatol Suppl 2012; 89: 44-48
19 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
20 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
21 Hodgson RJ, O'Connor P, Moots R. MRI of rheumatoid arthritis image quantitation for the assessment of disease activity, progression and response to therapy. Rheumatology (Oxford) 2008; 47 (01) 13-21
22 Axelsen MB, Eshed I, Hørslev-Petersen K. , et al; OPERA study group. A treat-to-target strategy with methotrexate and intra-articular triamcinolone with or without adalimumab effectively reduces MRI synovitis, osteitis and tenosynovitis and halts structural damage progression in early rheumatoid arthritis: results from the OPERA randomised controlled trial. Ann Rheum Dis 2015; 74 (05) 867-875
23 Conaghan PG, Østergaard M, Bowes MA. , et al. Comparing the effects of tofacitinib, methotrexate and the combination, on bone marrow oedema, synovitis and bone erosion in methotrexate-naive, early active rheumatoid arthritis: results of an exploratory randomised MRI study incorporating semiquantitative and quantitative techniques. Ann Rheum Dis 2016; 75 (06) 1024-1033
24 Boesen M, Kubassova O, Parodi M. , et al. Comparison of the manual and computer-aided techniques for evaluation of wrist synovitis using dynamic contrast-enhanced MRI on a dedicated scanner. Eur J Radiol 2011; 77 (02) 202-206
25 Boesen M, Kubassova O, Bouert R. , et al. Correlation between computer-aided dynamic gadolinium-enhanced MRI assessment of inflammation and semi-quantitative synovitis and bone marrow oedema scores of the wrist in patients with rheumatoid arthritis--a cohort study. Rheumatology (Oxford) 2012; 51 (01) 134-143
26 Malattia C, Damasio MB, Basso C. , et al. Dynamic contrast-enhanced magnetic resonance imaging in the assessment of disease activity in patients with juvenile idiopathic arthritis. Rheumatology (Oxford) 2010; 49 (01) 178-185
27 Workie DW, Graham TB, Laor T. , et al. Quantitative MR characterization of disease activity in the knee in children with juvenile idiopathic arthritis: a longitudinal pilot study. Pediatr Radiol 2007; 37 (06) 535-543
28 Nusman CM, Lavini C, Hemke R. , et al. Dynamic contrast-enhanced magnetic resonance imaging of the wrist in children with juvenile idiopathic arthritis. Pediatr Radiol 2017; 47 (02) 205-213
29 Hemke R, Nusman CM, van den Berg JM. , et al. Construct validity of pixel-by-pixel DCE-MRI: Correlation with conventional MRI scores in juvenile idiopathic arthritis. Eur J Radiol 2017; 94: 1-5
30 Hemke R, van Rossum MA, van Veenendaal M. , et al. Reliability and responsiveness of the Juvenile Arthritis MRI Scoring (JAMRIS) system for the knee. Eur Radiol 2013; 23 (04) 1075-1083
31 Gaspersic N, Sersa I, Jevtic V, Tomsic M, Praprotnik S. Monitoring ankylosing spondylitis therapy by dynamic contrast-enhanced and diffusion-weighted magnetic resonance imaging. Skeletal Radiol 2008; 37 (02) 123-131
32 Rudwaleit M, Jurik AG, Hermann KG. , et al. Defining active sacroiliitis on magnetic resonance imaging (MRI) for classification of axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI group. Ann Rheum Dis 2009; 68 (10) 1520-1527
33 Bozgeyik Z, Ozgocmen S, Kocakoc E. Role of diffusion-weighted MRI in the detection of early active sacroiliitis. AJR Am J Roentgenol 2008; 191 (04) 980-986
34 Ai F, Ai T, Li X, Hu D, Zhang W, Morelli JN. Value of diffusion-weighted magnetic resonance imaging in early diagnosis of ankylosing spondylitis. Rheumatol Int 2012; 32 (12) 4005-4013
35 Sanal HT, Yilmaz S, Kalyoncu U. , et al. Value of DWI in visual assessment of activity of sacroiliitis in longstanding ankylosing spondylitis patients. Skeletal Radiol 2013; 42 (02) 289-293
36 Sahin N, Hacibeyoglu H, Ince O. , et al. Is there a role for DWI in the diagnosis of sacroiliitis based on ASAS criteria?. Int J Clin Exp Med 2015; 8 (05) 7544-7552
37 Zhao YH, Li SL, Liu ZY. , et al. Detection of Active Sacroiliitis with Ankylosing Spondylitis through Intravoxel Incoherent Motion Diffusion-Weighted MR Imaging. Eur Radiol 2015; 25 (09) 2754-2763
38 Sun H, Liu K, Liu H. , et al. Comparison of bi-exponential and mono-exponential models of diffusion-weighted imaging for detecting active sacroiliitis in ankylosing spondylitis. Acta Radiol 2018; 59 (04) 468-477
39 Gezmis E, Donmez FY, Agildere M. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol 2013; 82 (12) 2316-2321
40 Dallaudière B, Dautry R, Preux PM. , et al. Comparison of apparent diffusion coefficient in spondylarthritis axial active inflammatory lesions and type 1 Modic changes. Eur J Radiol 2014; 83 (02) 366-370
41 Agarwal V, Kumar M, Singh JK, Rathore RK, Misra R, Gupta RK. Diffusion tensor anisotropy magnetic resonance imaging: a new tool to assess synovial inflammation. Rheumatology (Oxford) 2009; 48 (04) 378-382
42 Jeromel M, Jevtič V, Serša I, Ambrožič A, Tomšič M. Quantification of synovitis in the cranio-cervical region: dynamic contrast enhanced and diffusion weighted magnetic resonance imaging in early rheumatoid arthritis--a feasibility follow up study. Eur J Radiol 2012; 81 (11) 3412-3419
43 Li X, Liu X, Du X, Ye Z. Diffusion-weighted MR imaging for assessing synovitis of wrist and hand in patients with rheumatoid arthritis: a feasibility study. Magn Reson Imaging 2014; 32 (04) 350-353
44 Neubauer H, Evangelista L, Morbach H. , et al. Diffusion-weighted MRI of bone marrow oedema, soft tissue oedema and synovitis in paediatric patients: feasibility and initial experience. Pediatr Rheumatol Online J 2012; 10 (01) 20
45 Barendregt AM, Nusman CM, Hemke R. , et al. Feasibility of diffusion-weighted magnetic resonance imaging in patients with juvenile idiopathic arthritis on 1.0-T open-bore MRI. Skeletal Radiol 2015; 44 (12) 1805-1811
46 Barendregt AM, van Gulik EC, Lavini C. , et al. Diffusion-weighted imaging for assessment of synovial inflammation in juvenile idiopathic arthritis: a promising imaging biomarker as an alternative to gadolinium-based contrast agents. Eur Radiol 2017; 27 (11) 4889-4899 . Doi: 10.1007/s00330-017-4876-y
47 Hilbert F, Holl-Wieden A, Sauer A, Köstler H, Neubauer H. Intravoxel incoherent motion magnetic resonance imaging of the knee joint in children with juvenile idiopathic arthritis. Pediatr Radiol 2017; 47 (06) 681-690 . Doi: 10.1007/s00247-017-3800-6
48 J P Bray T, Vendhan K, Ambrose N. , et al. Diffusion-weighted imaging is a sensitive biomarker of response to biologic therapy in enthesitis-related arthritis. Rheumatology (Oxford) 2017; 56 (03) 399-407
49 Vendhan K, Bray TJ, Atkinson D. , et al. A diffusion-based quantification technique for assessment of sacroiliitis in adolescents with enthesitis-related arthritis. Br J Radiol 2016; 89 (1059): 20150775
50 Yoo HJ, Hong SH, Oh HY. , et al. Diagnostic Accuracy of a Fluid-attenuated Inversion-Recovery Sequence with Fat Suppression for Assessment of Peripatellar Synovitis: Preliminary Results and Comparison with Contrast-enhanced MR Imaging. Radiology 2017; 283 (03) 769-778
51 Son YN, Jin W, Jahng GH. , et al. Efficacy of double inversion recovery magnetic resonance imaging for the evaluation of the synovium in the femoro-patellar joint without contrast enhancement. Eur Radiol 2018; 28 (02) 459-467
52 Crymes Jr WB, Demos H, Gordon L. Detection of musculoskeletal infection with 18F-FDG PET: review of the current literature. J Nucl Med Technol 2004; 32 (01) 12-15
53 Carey K, Saboury B, Basu S. , et al. Evolving role of FDG PET imaging in assessing joint disorders: a systematic review. Eur J Nucl Med Mol Imaging 2011; 38 (10) 1939-1955
54 Costelloe CM, Murphy Jr WA, Chasen BA. Musculoskeletal pitfalls in 18F-FDG PET/CT: pictorial review. AJR Am J Roentgenol 2009; 193 (3, Suppl) WS1-WS13 , Quiz S26–S30
55 Zeisel SH. Dietary choline: biochemistry, physiology, and pharmacology. Annu Rev Nutr 1981; 1: 95-121
56 Roivainen A, Parkkola R, Yli-Kerttula T. , et al. Use of positron emission tomography with methyl-11C-choline and 2-18F-fluoro-2-deoxy-D-glucose in comparison with magnetic resonance imaging for the assessment of inflammatory proliferation of synovium. Arthritis Rheum 2003; 48 (11) 3077-3084
57 van der Laken CJ, Elzinga EH, Kropholler MA. , et al. Noninvasive imaging of macrophages in rheumatoid synovitis using 11C-(R)-PK11195 and positron emission tomography. Arthritis Rheum 2008; 58 (11) 3350-3355
58 Damasio MB, Malattia C, Tanturri de Horatio L. , et al. MRI of the wrist in juvenile idiopathic arthritis: proposal of a paediatric synovitis score by a consensus of an international working group. Results of a multicentre reliability study. Pediatr Radiol 2012; 42 (09) 1047-1055
59 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
60 Miese F, Scherer A, Ostendorf B. , et al. Hybrid 18F-FDG PET-MRI of the hand in rheumatoid arthritis: initial results. Clin Rheumatol 2011; 30 (09) 1247-1250
61 Buchbender C, Ostendorf B, Ruhlmann V. , et al. Hybrid 18F-labeled Fluoride Positron Emission Tomography/Magnetic Resonance (MR) Imaging of the Sacroiliac Joints and the Spine in Patients with Axial Spondyloarthritis: A Pilot Study Exploring the Link of MR Bone Pathologies and Increased Osteoblastic Activity. J Rheumatol 2015; 42 (09) 1631-1637