Quantifying synovial inflammation by imaging techniques
DOI:
https://doi.org/10.15305/ijrci/v2iS1/89Keywords:
Synovitis, Imaging, diffusion tensor imaging, scintigraphy, ultrasound, Magnetic resonance imaging, positron emission tomographyAbstract
The past few decades have witnessed dramatic changes and advances in diagnostic imaging. In the field of arthritis, these changes have contributed to enhance the diagnostic accuracy and to conduct serial monitoring of synovial inflammation without synovial biopsy. Advanced imaging techniques employ target-specific probes to non-invasively assess molecular, cellular, and physiological abnormalities associated with the underlying pathology. Dynamic and diffusion magnetic resonance imaging (MRI) are being developed to evaluate the discrete aspects of specific inflammatory and destructive pathways of inflammatory arthritis. These newer imaging modalities provide an earlier and more reliable assessment of clinical outcome, disease activity, severity, location, and therapeutic response. These techniques will be incorporated soon in routine clinical practice, and their adoption may enable clinicians to measure the treatment response and tailor the therapeutic interventions accordingly. In this review, we have attempted to summarize the emerging non-invasive imaging techniques and their application in quantifying synovial inflammation.
References
Brown AK, Conaghan PG, Karim Z, Quinn MA, Ikeda K, Peterfy CG, et al. An explanation for the apparent dissociation between clinical remission and continued structural deterioration in rheumatoid arthritis. Arthritis Rheum. 2008 Oct;58(10):2958–67.
Manger B, Kalden JR. Joint and connective tissue ultrasonography--a rheumatologic bedside procedure? A German experience. Arthritis Rheum. 1995 Jun;38(6):736–42.
Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D’Agostino M-A, et al. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol. 2005 Dec 1;32(12):2485–7.
Meenagh G, Filippucci E, Delle Sedie A, Riente L, Iagnocco A, Scirè CA, et al. Ultrasound imaging for the rheumatologist XIX. Imaging modalities in rheumatoid arthritis. Clin Exp Rheumatol. 2009 Feb;27(1):3–6.
Agnocco A, Epis O, Delle SA et al.Ultrasound imaging for the rheumatologist. XVII. Role of colour Doppler and power Doppler. Clin Exp Rheumatol 2008;26:759–62.
Balsa A, de Miguel E, Castillo C, Peiteado D, Martín-Mola E. Superiority of SDAI over DAS-28 in assessment of remission in rheumatoid arthritis patients using power Doppler ultrasonography as a gold standard. Rheumatology (Oxford). 2010 Apr;49(4):683–90.
Foltz V, Gandjbakhch F, Etchepare F, Rosenberg C, Tanguy ML, 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 Jan;64(1):67–76.
Scire CA, Montecucco C, Codullo V et al. Ultrasonographic evaluation of joint involvement in early rheumatoid arthritis in clinical remission: power Doppler signal predicts short-term relapse. Rheumatology 2009;48:1092–1097.
Qvistgaard E, Rogind H, Torp-Pedersen S, Terslev L, Danneskiold-Samso... B, Bliddal H. Quantitative ultrasonography in rheumatoid arthritis: evaluation of inflammation by Doppler technique. Ann Rheum Dis. 2001 Jul;60(7):690–3.
Newman JS, Laing TJ, McCarthy CJ, Adler RS. Power Doppler sonography of synovitis: assessment of therapeutic response--preliminary observations. Radiology. 1996 Feb;198(2):582–4.
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 Sep;44(9):2018–23.
Terslev L, Torp-Pedersen S, Qvistgaard E, Danneskiold-Samso... B, Bliddal H. Estimation of inflammation by Doppler ultrasound: quantitative changes after intra-articular treatment in rheumatoid arthritis. Ann Rheum Dis. 2003 Nov;62(11):1049–53.
De Zordo T, Mlekusch SP, Feuchtner GM, Mur E, Schirmer M, Klauser AS. Value of contrast-enhanced ultrasound in rheumatoid arthritis. Eur J Radiol. 2007 Nov;64(2):222–30.
Canella C, Philippe P, Pansini V, Salleron J, Flipo R-M, Cotten A. Use of tomosynthesis for erosion evaluation in rheumatoid arthritic hands and wrists. Radiology. 2011 Jan;258(1):199–205.
Dohn UM, Ejbjerg BJ, Hasselquist M, Narvestad E, Court-Payen M, Szkudlarek M, et al. Rheumatoid arthritis bone erosion volumes on CT and MRI: reliability and correlations with erosion scores on CT, MRI and radiography. Ann Rheum Dis 2007;66(10):1388–92.
Perry D, Stewart N, Benton N, Robinson E, Yeoman S, Crabbe J, et al. Detection of erosions in the rheumatoid hand; a comparative study of multidetector computerized tomography versus magnetic resonance scanning. J Rheumatol. 2005 Feb;32(2):256–67.
Døhn UM, Ejbjerg BJ, Court-Payen M, Hasselquist M, Narvestad E, Szkudlarek M, et al. Are bone erosions detected by magnetic resonance imaging and ultrasonography true erosions? A comparison with computed tomography in rheumatoid arthritis metacarpophalangeal joints. Arthritis Res Ther. 2006;8(4):R110.
Døhn UM, Ejbjerg B, Boonen A, Hetland ML, Hansen MS, Knudsen LS, et al. No overall progression and occasional repair of erosions despite persistent inflammation in adalimumab-treated rheumatoid arthritis patients: results from a longitudinal comparative MRI, ultrasonography, CT and radiography study. Ann Rheum Dis. 2011 Feb;70(2):252–8.
Knevel R, Kwok KY, de Rooy DPC, Posthumus MD, Huizinga TWJ, Brouwer E, et al. Evaluating joint destruction in rheumatoid arthritis: is it necessary to radiograph both hands and feet? Ann Rheum Dis. 2013 Mar;72(3):345–9.
Stach CM, Bäuerle M, Englbrecht M, Kronke G, Engelke K, Manger B, et al. Periarticular bone structure in rheumatoid arthritis patients and healthy individuals assessed by high-resolution computed tomography. Arthritis Rheum. 010 Feb;62(2):330–9.
Finzel S, Rech J, Schmidt S, Engelke K, Englbrecht M, Schett G. Interleukin-6 receptor blockade induces limited repair of bone erosions in rheumatoid arthritis: a micro CT study. Ann Rheum Dis. 2013 Mar;72(3):396–400.
Finzel S, Rech J, Schmidt S, Engelke K, Englbrecht M, Schett G. Quantitative assessment of periarticular osteopenia in patients with early rheumatoid arthritis: a preliminary report. Scand J Rheumatol 2004;33(5): 307–11.
Meirer R, Müller-Gerbl M, Huemer GM, Schirmer M, Herold M, Kersting S, et al. Quantitative assessment of periarticular osteopenia in patients with early rheumatoid arthritis: a preliminary report. Scand J Rheumatol. 2004;33(5):307–11.
Rand T, Imhof H, Czerny C, Breitenseher M, Machold K, Turetschek K, et al. Discrimination between fluid, synovium, and cartilage in patients with rheumatoid arthritis: contrast enhanced Spin Echo versus non-contrast-enhanced fat-suppressed Gradient Echo MR imaging. Clin Radiol. 1999 Feb;54(2):107–10.
Narvaez JA, Narváez J, De Lama E, De Albert M. MR Imaging of Early Rheumatoid Arthritis. RadioGraphics. 2010 Jan 1;30(1):143–63.
Narváez JA, Narváez J, Roca Y, Aguilera C. MR imaging assessment of clinical problems in rheumatoid arthritis. Eur Radiol. 2002 Jul;12(7):1819–28.
Ostergaard M, Ejbjerg B. Magnetic resonance imaging of the synovium in rheumatoid arthritis. Semin. Musculoskelet. Radiol. 2004; 8:287–299.
Rand T, Imhof H, Czerny C, Breitenseher M, Machold K, Turetschek K, et al. Discrimination between fluid, synovium, and cartilage in patients with rheumatoid arthritis: contrast enhanced Spin Echo versus non-contrast-enhanced fat-suppressed Gradient Echo MR imaging. Clin Radiol. 1999 Feb;54(2):107–10.
Gilkeson G, Polisson R, Sinclair H, Vogler J, Rice J, Caldwell D, et al. Early detection of carpal erosions in patients with rheumatoid arthritis: a pilot study of magnetic resonance imaging. J Rheumatol. 1988 Sep;15(9):1361–6.
Foley-Nolan D, Stack JP, Ryan M, Redmond U, Barry C, Ennis J, et al. Magnetic resonance imaging in the assessment of rheumatoid arthritis--a comparison with plain film radiographs. Br J Rheumatol. 1991 Apr;30(2):101–6.
Foley-Nolan D, Stack JP, Ryan M, Redmond U, Barry C, Ennis J, et al. Magnetic resonance imaging in the assessment of rheumatoid arthritis--a comparison with plain film radiographs. Br J Rheumatol. 1991 Apr;30(2):101–6.
McGonagle D, Green MJ, Proudman S, Richardson C, Veale D, O'Connor P et al. The majority of patients with rheumatoid arthritis have erosive disease at presentation when magnetic resonance imaging of the dominant hand is employed. Br J Rheumatol1997;36(Suppl 1):121.
Jorgensen C, Cyteval C, Anaya JM, Baron MP, Lamarque JL, Sany J. Sensitivity of magnetic resonance imaging of the wrist in very early rheumatoid arthritis. Clin Exp Rheumatol. 1993 Apr;11(2):163–8.
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 Apr;41(4):694–700.
Van der Leij C, van de Sande MGH, 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 Oct;253(1):234–40.
Zierhut ML, Gardner JC, Spilker ME, Sharp JT, Vicini P. Kinetic modeling of contrast-enhanced MRI: an automated technique for assessing inflammation in the rheumatoid arthritis wrist. Ann Biomed Eng. 2007 May;35(5):781–95.
Boesen M, Østergaard M, Cimmino MA, Kubassova O, Jensen KE, Bliddal H. MRI quantification of rheumatoid arthritis: current knowledge and future perspectives. Eur J Radiol. 2009 Aug;71(2):189–96.
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 Jun;74(3):e67–72.
Peloschek P, Boesen M, Donner R, Kubassova O, Birngruber E, Patsch J, et al. Assessement of rheumatic diseases with computational radiology: current status and future potential. Eur J Radiol. 2009 Aug;71(2):211–6.
Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology. 1996 Dec;201(3):637–48.
Chen J, Liu W, Zhang H, Lacy L, Yang X, Song S-K, et al. Regional ventricular wall thickening reflects changes in cardiac fiber and sheet structure during contraction: quantification with diffusion tensor MRI. Am J Physiol Heart Circ Physiol. 2005 Nov;289(5):H1898–907.
Hsu EW, Setton LA. Diffusion tensor microscopy of the intervertebral disc anulus fibrosus. Magn Reson Med. 1999 May;41(5):992–9.
Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging. 2001 Apr;13(4):534–46.
Hasan KM, Parker DL, Alexander AL. Comparison of Optimization Procedures for Diffusion-Tensor Encoding Directions. J Magn Reson Imaging 2001;13:769-80.
Hasan KM, Alexander AL, Narayana PA. Does fractional anisotropy have better noise immunity characteristics than relative anisotropy in diffusion tensor MRI? An analytical approach. Magn Reson Med. 2004 Feb;51(2):413–7.
Pfefferbaum A, Sullivan EV. Disruption of brain white matter microstructure by excessive intracellular and extracellular fluid in alcoholism: evidence from diffusion tensor imaging. Neuropsychopharmacology. 2005 Feb;30(2):423–32.
Agarwal V, Kumar M, Singh JK, Rathore RKS, Misra R, Gupta RK. Diffusion tensor anisotropy magnetic resonance imaging: a new tool to assess synovial inflammation. Rheumatology (Oxford). 2009 Apr;48(4):378–82.
Buckland J. Imaging: Bye-bye biopsy? Nat Rev Rheumatol. 2009 May;5(5):236–236.
Zeman MN, Scott PJ. Current imaging strategies in rheumatoid arthritis. Am J Nucl Med Mol Imaging. 2012 Mar 28;2(2):174–220.
Palmer WE, Rosenthal DI, Schoenberg OI, Fischman AJ, Simon LS, Rubin RH, 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 Sep;196(3):647–55.
Elzinga EH, van der Laken CJ, Comans EFI, Lammertsma AA, Dijkmans B a. C, Voskuyl AE. 2-Deoxy-2-[F-18]fluoro-D-glucose joint uptake on positron emission tomography images: rheumatoid arthritis versus osteoarthritis. Mol Imaging Biol. 2007 Dec;9(6):357–60.
Elzinga EH, van der Laken CJ, Comans EFI, Lammertsma AA, Dijkmans B a. C, Voskuyl AE. 2-Deoxy-2-[F-18]fluoro-D-glucose joint uptake on positron emission tomography images: rheumatoid arthritis versus osteoarthritis. Mol Imaging Biol. 2007 Dec;9(6):357–60.
Van der Laken CJ, Elzinga EH, Kropholler MA, Molthoff CFM, van der Heijden JW, Maruyama K, et al. Noninvasive imaging of macrophages in rheumatoid synovitis using 11C-(R)-PK11195 and positron emission tomography. Arthritis Rheum. 2008 fNov;58(11):3350–5.
Kubota K, Ito K, Morooka M, Mitsumoto T, Kurihara K, Yamashita H, et al. Whole-body FDG-PET/CT on rheumatoid arthritis of large joints. Ann Nucl Med. 2009 Nov;23(9):783–91.
Beckers C, Jeukens X, Ribbens C, André B, Marcelis S, Leclercq P, et al. 18F-FDG PET imaging of rheumatoid knee synovitis correlates with dynamic magnetic resonance and sonographic assessments as well as with the serum level of metalloproteinase-3. Eur. J. Nucl. Med. Mol. Imaging 2006;33:275–80.
Van der Laken CJ, Huisman MH, Voskuyl AE. Nuclear imaging of rheumatic diseases. Best Pract Res Clin Rheumatol. 2012 Dec;26(6):787–804.
Gent YYJ, Voskuyl AE, Kloet RW, van Schaardenburg D, Hoekstra OS, Dijkmans BAC, et al. Macrophage positron emission tomography imaging as a biomarker for preclinical rheumatoid arthritis: findings of a prospective pilot study. Arthritis Rheum. 2012 Jan;64(1):62–6.
Published
Issue
Section
License
Copyright for articles published in this journal is retained by the authors, with first publication rights granted to the ‘Internet Journal of Rheumatology and Clinical Immunology’. All the published content, except where otherwise noted, is licensed under Creative Commons license (CC-BY).
Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) after the publication of the manuscript in IJRCI, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
