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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 23  |  Issue : 2  |  Page : 96-103

Assessment of synovitis in rheumatoid arthritis by enhanced magnetic resonance imaging (OMERACT RAMRIS score) and power Doppler ultrasound: a comparative study


1 Department of Radiology, Kasr El Aini Hospital, Cairo University, Cairo, Egypt
2 Department of Rheumatology, Kasr El Aini Hospital, Cairo University, Cairo, Egypt

Date of Submission31-Jan-2017
Date of Acceptance28-Feb-2017
Date of Web Publication22-Nov-2017

Correspondence Address:
Manar H Abdel Sattar
Department of Radiology, Kasr El Aini Hospital, Cairo University, 10 Omar Tousson Street, Mohandessen, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/kamj.kamj_12_17

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  Abstract 

Background and objectives
Disease activity in rheumatoid arthritis (RA) joints is conventionally assessed clinically in combination with the measurement of levels of biochemical surrogate markers. Plain radiography shows only late signs of preceding disease activity. Newer imaging modalities such as contrast-enhanced MRI and power Doppler ultrasonography (PDUS) may offer improved monitoring.
The aim of the study was to compare the role of PDUS with enhanced MRI in the assessment and scoring of synovitis of the wrist and hand joints in RA patients.
Patients and methods
Fifty patients (39 female patients and 11 male patients) with RA were subjected to a PDUS study and enhanced MRI examination of the clinically dominant wrist and hand joints. The mean age of the patients was 45.3 years and mean disease duration was 6.2 years. Power Doppler score of synovitis was correlated and compared with MRI OMERACT score.
Results
PDUS detected increased vascularity within 30 (60%) wrist joints denoting active synovitis and MRI detected synovial enhancement within 38 (76%) wrist joints denoting active synovitis; both scoring systems agreed in the assessment of synovitis degree in 20 wrist joints. PDUS missed detection of synovitis in nine joints detected by MRI, seven of them estimated by MRI to be of mild activity (grade 1).
PDUS detected synovial activity (increased vascularity) in metacarpophalangeal (MCP) joints of 21 patients, whereas MRI detected synovial activity (synovial enhancement) in MCP joints of nine patients. Both modalities agreed in eight patients as regards the total synovial activity score.
Statistical analysis of these results showed a statistically significant correlation (P<0.001) and good agreement between the two modalities in the assessment of synovial activity in the wrist and MCP joints. Comparison of ultrasonography and MRI yielded a κ value of 0.482 and 0.376, respectively.
Conclusion
Our results showed that both modalities are comparable and closely related in the assessment of synovial inflammatory process of the hand and wrist joints in RA patients.

Keywords: magnetic resonance imaging metacarpophalangeal joint, power Doppler ultrasound, rheumatoid arthritis, score of disease activity, wrist joint


How to cite this article:
Abdel Sattar MH, Alsherbini HH. Assessment of synovitis in rheumatoid arthritis by enhanced magnetic resonance imaging (OMERACT RAMRIS score) and power Doppler ultrasound: a comparative study. Kasr Al Ainy Med J 2017;23:96-103

How to cite this URL:
Abdel Sattar MH, Alsherbini HH. Assessment of synovitis in rheumatoid arthritis by enhanced magnetic resonance imaging (OMERACT RAMRIS score) and power Doppler ultrasound: a comparative study. Kasr Al Ainy Med J [serial online] 2017 [cited 2018 Dec 14];23:96-103. Available from: http://www.kamj.eg.net/text.asp?2017/23/2/96/218993


  Introduction Top


Rheumatoid arthritis (RA) is a form of autoimmune arthritis that can cause disability and pathological manifestations of synovitis that most often involves the finger joints in the hand and the wrist joints. In clinical practice, assessment of RA progression often requires clinical evaluation, inflammatory index measurement and imaging of the rheumatoid. These parameters contribute to the choice of treatment and are used in treatment monitoring and prognosis [1].

As subclinical synovitis can be missed by clinical assessment alone, synovitis is frequently found by imaging, such as by ultrasonography (US) or MRI in patients considered to be in remission, and is associated with adverse clinical and functional outcomes [2].

Gray scale US allows imaging of anatomic structures, which enables visualization of synovial hypertrophy and/or effusion. Power Doppler ultrasound (PDUS) allows blood flow detection, and visualization of the movement of blood vessels, therefore detecting increased microvascular blood flow seen in active synovitis [3].

PDUS can be used for grading severity of synovial activity by a semiquantitative scoring system in which the intensity of the synovial blood flow is graded on a four-step scale [4].

MRI scanning is used for imaging and quantifying joint inflammation and damage in RA. The OMERACT rheumatoid arthritis MRI scoring system (RAMRIS) provides a framework for scoring inflammation and damage in RA with T1-weighted images (T1WIs) acquired before and after the administration of gadolinium-based, intravenous contrast to demonstrate enhancing synovitis [5]. Synovitis is scored 0–3 in each of the radiocarpal, intercarpal–carpometacarpal, and second to fifth metacarpophalangeal (MCP) joints [6].

The aim of the present study was to compare the role of PDUS with enhanced MRI in the assessment of synovitis of the wrist and hand joints in RA patients.


  Patients and methods Top


Fifty patients clinically diagnosed with RA were enrolled in this prospective study. The study was approved by the ethical committee, and consents were taken from all patients enrolled in the study.

The patients were recruited from the Rheumatology and Rehabilitation Outpatient Clinic, Faculty of Medicine, Cairo University Hospitals during the period from March 2014 to January 2016.

Thirty-nine (78%) patients were women and 11 (22%) were men; their ages ranging from 22 to 68 years with a mean age of 45.3 years. Thirty-nine (78%) patients were seropositive Rheumatoid Factor (RF) and 11 (22%) patients were seronegative (RF). Thirty-one (60%) patients were positive for C-reactive protein.

Inclusion criteria

  1. Clinical diagnosis of RA according to the American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis [7].
  2. No apparent deformities of the wrist and hand joints clinically.
  3. Subtle changes or normal study by radiography.


Exclusion criteria

  1. Advanced deformities of the wrist and hand joints detected clinically.
  2. Renal impairment.
  3. Contraindications to MRI (e.g. claustrophobia, pacemakers).


The clinically dominant wrist and hand joints of the 50 patients were examined (50 wrists and 200 MCPs). All patients included in this study were subjected to US examination, as well as a study before and after contrast MRI.

Ultrasonography

US of the wrist joints were performed by using GE Logiq P6 Pro US machines (General Electric: Boston, Massachussets, USA) using a near-focused linear-array transducer with a center frequency of 7.5–12 MHz.

During examination of the hand and wrist joints, the patient was examined while sitting upright, with the hand placed on a cushion and fully pronated and then supinated.

Dorsal longitudinal scan followed by dorsal transverse scan were done followed by palmar examination in supination to evaluate presence of pannus (synovial hypertrophy) and assessment of synovial vascularity (synovitis) using power Doppler (PD).

US examination for joint effusion and synovitis was carried out by gray-scale imaging, and synovial vascularization was assessed by PD.

Gray-scale imaging evaluation confirmed the presence or absence of synovial hypertrophy, which was graded using a semiquantitative scoring method consisting of a scale of 0–3, where 0 represented no synovial hypertrophy, 1 mild hypertrophy, 2 moderate hypertrophy, and 3 severe hypertrophy. PD was graded using a semiquantitative scoring method, which consisted of a scale of 0–3 [6] ([Table 1]).
Table 1: Semiquantitative grading of severity of power Doppler signal in rheumatoid arthritis [6]

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Each patient evaluation took no more than 20 min, including documentation, and the images demonstrating maximal abnormalities were archived.

Magnetic resonance imaging study

Magnetic resonance examination of the dominant wrist and hand joints was performed using Gyroscan Intera Philips Medical Systems (1.5 T; Philips Healthcare: Amsterdam, Netherlands). Patients were placed in the prone position with the hand above the head and dedicated wrist coil was used. The position was maintained and movement avoided with the aid of sand bags.

Three-dimensional coronal T1WIs and Short Tau Inversion Recovery (STIR) WIs were acquired and axial T1WIs of the wrist using the parameters shown in [Table 2].
Table 2: Magnetic resonance imaging technical parameters

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Then, 0.05 mmole/kg body weight of Gadoteric acid (DOTAREM; Guerbet, France) were injected intravenously. Acquisition of three-dimensional coronal and axial T1WIs of the wrist and MCPs was performed.

Evaluation of magnetic resonance imaging

Synovitis in a joint on MRI was defined as an area in the synovial compartment that showed enhancement on the postcontrast images. The degree of synovitis in each joint examined was graded on a scale of 0–3 according to the OMERACT definitions (0, normal; 1–3, mild, moderate, severe) as estimated by thirds of presumed maximum volume of enhancing tissue in a synovial compartment [5].

Statistical analysis

Data were statistically described in terms of mean±SD, and range, or frequencies (number of cases) and percentages when appropriate. Comparison between MRI and US results was done using the McNemar test and the χ2 test when appropriate. Agreement was tested using κ statistics. Correlation between various variables was done using Spearman’s rank correlation equation for non-normal variables. P-values less than 0.05 were considered statistically significant. All statistical calculations were done using the statistical package for the social science (SPSS, version 15; SPSS Inc., Chicago, Illinois, USA) for Microsoft Windows.


  Results Top


The clinically dominant wrist and hand joints of 50 RA patients were examined (50 wrists and 200 MCPs) for synovial hypertrophy and synovitis.

Results of gray scale and power Doppler ultrasonography examination

Forty-two (84%) wrist joints were found to have pannus (both active and inactive); among them 30 (60%) wrist joints were found to have increased vascularity by PDUS, 13 (26%) wrist joints showed mild activity, 10 (20%) wrist joints had moderate activity, while seven (14%) wrist joints showed severe activity ([Figure 1],[Figure 2],[Figure 3],[Figure 4]).
Figure 1: A 42 years old female patient with RA for 7 years pre and post contrast axial T1WIs of the wrist joint (A and B) showing severe synovial thickening and enhancement. PDUS longitudinal images (C and D) showing marked increased vascularity within the hypertrophied synovium of the wrist denoting severe synovitis.

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Figure 2: A 37 years old female patient with RA for 4 years pre and post contrast axial T1WIs of the wrist joint (A and B) show marked synovial thickening with moderate enhancement in the post contrast study denoting moderate synovitis. PDUS longitudinal images of the wrist joint (C and D) show hypoechoic synovial thickening with increased vascularity suggestive of moderate synovitis.

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Figure 3: A male patient 35 yrs with RA for 3 years pre and post contrast axial T1WIs of the wrist joints (A and B) showing synovial hypertrophy with minimal enhancement in the post contrast study. PDUS of the wrist (C) showing intercarpal hypoechoic synovial thickening with minimal ncreased vascularity by Doppler study.

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Figure 4: Pre and post contrast axial T1WIs of the MCP joints (A and B) showing no appreciable enhancement. PDUS longitudinal images (C and D) showing hypoechoic synovial thickening of the 2nd and 3rd MCPs with no evidence of increased vascularity.

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Sixty-two (31%) MCP joints were found to have synovial hypertrophy (pannus) both active and inactive; among them 44 (22%) MCP joints were found to have increased vascularity by PDUS ([Table 3] and [Table 4]).
Table 3: Frequency of synovial hypertrophy (pannus) by ultrasound in metacarpophalangeal joints

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Table 4: Synovitis (increased vascularity) by power Doppler in metacarpophalangeal joints

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Results of magnetic resonance imaging examination

Fifty wrists and 200 MCP joints were scanned and then interpreted according to the OMERACT RAMRIS.
  1. Forty-six (92%) wrist joints were found to have pannus (synovial hypertrophy). Evaluation of synovial enhancement in the postcontrast study revealed 38 (76%) wrist joints had active synovitis; among them 24 (48%) wrist joints had mild activity, five (10%) wrist joints had moderate activity and nine (18%) wrist joints had severe activity.
  2. Fifteen (7.5%) MCP joints were active in nine patients, and the total MCP activity scoring for all of the nine patients was mild.


Comparison between ultrasonography and magnetic resonance imaging in the detection of wrist and hand joints pathology

US detected synovial hypertrophy (pannus) in 42 wrist joints, whereas MRI detected it in 46 wrist joints; both modalities agreed in 42 patients, and US missed synovial hypertrophy in four wrist joints, which was detected by MRI ([Table 5]).
Table 5: Comparison between ultrasonography and magnetic resonance imaging in the detection of synovial hypertrophy (pannus) of wrist joints

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Statistical analysis of these results showed statistically significant correlation (P=0.125) and significant agreement between the two modalities in the detection of synovial hypertrophy. Comparison between US and MRI yielded a weighted κ value of 0.627.

PDUS detected increased vascularity within 30 (60%) wrist joints denoting active synovitis, whereas MRI detected synovial enhancement within 38 (76%) wrist joints denoting active synovitis. Both scoring systems agreed in the assessment of degree of synovitis in 20 wrist joints. PDUS missed detection of synovitis in nine joints detected by MRI, seven of them estimated by MRI to be of mild activity (grade 1) ([Table 6]).
Table 6: Comparison between power Doppler and magnetic resonance imaging in the assessment of synovial activity (synovitis) in wrist joints

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Statistical analysis of these results showed statistically significant correlation (P<0.001) and agreement between the techniques in the assessment of synovial activity in the wrist joints. Comparison of US and MRI yielded a κ value of 0.482.

PDUS detected synovial activity (increased vascularity) in MCP joints of 21 patients, whereas MRI detected synovial activity (synovial enhancement) in MCP joints of nine patients. Both modalities agreed in eight patients as regards the total synovial activity score ([Table 7]).
Table 7: Comparison between power Doppler ultrasonography and magnetic resonance imaging in the assessment of total metacarpophalangeal synovial activity score

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Statistical analysis of these results showed no statistically significant difference (P=0.002) and good agreement between the two modalities in the assessment of total MCP activity score. Comparison of US and MRI yielded a weighted κ value of 0.376; correlation between both of them revealed P value of 0.001 and correlation coefficient 0.445, which is a relatively weak correlation.


  Discussion Top


RA is an inflammatory systemic autoimmune disease of unknown etiology that predominantly affects the synovial membrane of joints. It is characterized by polyarticular manifestation, typically with a symmetrical pattern of involvement. In most cases, the finger and the wrist joints are affected [8]. Conventional radiography is the most widely used imaging modality for the diagnosis of RA. Its advantages are its wide availability, good standardization and validated evaluation scales [9].

Synovitis is among the earliest abnormalities in early arthritis, but is identified on radiographs only indirectly or not at all [10].

This study was carried out to compare effectiveness of both PDUS and MRI of the wrist and hand joints in the assessment of synovial inflammation and degree of activity and to try to correlate the OMERACT RAMRIS synovitis score with PD activity score in RA patients.

Synovial hypertrophy is evaluated primarily on gray scale images, while PD images are utilized to demonstrate activity related to the synovial hypertrophy. The clinical significance of gray scale findings remains disputed, and there is also the problem of interobserver agreement. The presence of microvascular blood flow in synovial hypertrophy is interpreted as active synovitis and predicts ongoing joint damage even in patients in clinical remission [11]. Contrast-enhanced MRI is used for the visualization of the inflamed synovium in which there is increased blood flow and increased capillary permeability. A correlation between the thickness of the synovial membrane detected with contrast-enhanced MRI and joint destruction has been reported. Several assessments for synovitis have been used, such as RAMRIS, which provides semiquantitative assessment, measuring the maximum enhanced thickness of the synovium, and the total volume of the synovial membrane, calculated by summation of each slice [12].

In the present study, 30 (60%) wrist joints were found to have increased vascularity upon PD application, denoting active synovitis. By MRI, 38 (76%) wrist joints showed evidence of synovial enhancement in the postcontrast study, denoting active synovitis.

We found statistically significant correlation and agreement between the PD score and OMERACT RAMRIS score of synovial activity in the wrist joints.

These result were in agreement with those of Boesen et al. [13] who reported that the OMERACT RAMRIS scores of inflammation in RA patients (bone marrow edema and synovial enhancement) are comparable with US color fraction measurements. They studied 50 wrist joints in patients with RA and their aim was to compare MRI scores with US Doppler measurements. MRI was scored according to OMERACT RAMRIS recommendations for synovitis, bone marrow edema and erosions, and the Doppler activity was quantified using color fraction calculation.

They reported, in a study first of its kind to compare OMERACT RAMRIS score with US Color Flow (CF), a significant correlation between US CF and MRI synovitis score (P<0.005) [13]. This was in agreement with our results (P<0.001). They examined the dorsal aspect of the wrist joints and subdivided them into three compartments, taking the average calculated CF and compared it to the total MRI synovitis score. In our study, we examined both the palmar and dorsal surfaces of the wrist joints, as well as the radiocarpal articulations in transverse and sagittal planes and took the highest Doppler activity score detected to be compared with MRI; this may explain the stronger correlation between the two modalities in our study.

Taniguchi et al. [11] assessed synovitis with MRI using Maximum Intensity Projection (MIP) images and PD findings to examine the clinical usefulness of MIP images for RA in the hand; they studied 60 wrist joints in 30 patients. They assumed a scoring method for the presence of articular synovitis using a semiquantitative method with a scale from 0 to 2 (grade 0, no enhancement; grade 1, partial enhancement of the joint; grade 2,complete enhancement of the joint). For PD images, each joint was scored on a semiquantitative scale (0–3); they found a statistically significant correlation between the scores for MIP images and PD images for both wrists (P<0.001). The agreement on synovitis between MIP and PD images was moderate at 0.73 (κ=0.44). This was in agreement with our study as regards the strong correlation between both modalities; and yet we differed in the scoring methods.

Fukuba et al. [14] compared the effectiveness of PDUS with that of dynamic MRI for detecting active synovitis in the hands of RA patients. They studied 220 joints in ten patients; the relative synovial enhancement ratio map of dynamic MRI was compared with a semiquantitative score of PDUS. A statistically significant correlation was observed between the detection of synovial blood flow signals on PDUS and detection of early synovial enhancement by dynamic MRI (correlation coefficient P=0.001).

Terslev et al. [15] compared the quantitative and qualitative information obtained by Doppler US of the wrist joints and the small joints of the hand with the information obtained by postcontrast MRI in patients with RA. They studied 29 patients − 196 joints (29 wrists and 167 finger joints). The joints of the hands were examined by color Doppler US; a joint was considered inflamed if any color pixels are seen, and the image with maximum color activity was selected for analysis. Postcontrast axial and coronal MRI images of the wrist and hand joints were obtained and evaluated for synovial enhancement and the degree of synovitis was graded on a scale of 0–3.

They found total agreement between the two imaging modalities with κ values of 0.45 and 0.41 for the wrist and MCP joints, respectively, in detection of synovitis, and statistically significant correlation (P<0.001) between color fraction in Doppler US and synovial thickness in postcontrast MRI [15]. Those results were in agreement with those obtained in our study. We found good agreement between both imaging modalities with κ values of 0.482 and 0.376 for the wrist and MCP joints, respectively, in the detection of active synovitis, with significant correlation (P<0.001).


  Conclusion Top


The present study revealed agreement between the results of PDUS and the findings of enhanced MRI, which have been shown to closely reflect synovial membrane inflammation in the overall grading of RA joints. PDUS might have comparable potential to enhanced MRI for assessing synovitis in RA patients.

PDUS is easy to perform, requires relatively cheap equipment and is also less invasive compared with enhanced MRI, with no need for injection of contrast material. As a more accessible, cheaper and more patient-friendly method than MRI, US (including PDUS) may become a routine bedside tool in the future.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd et al. Rheumatoid arthritis classification criteria. An American College of Rheumatology/European League against Rheumatism collaborative initiative. Ann Rheum Dis 2010; 69:1580–1588.  Back to cited text no. 1
    
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Colebatch AN, Edwards CJ, Østergaard M, Van der Heijde D, Balint PV, D’Agostino MA et al. EULAR recommendations for the use of imaging of the joints in the clinical management of rheumatoid arthritis. Ann Rheum Dis 2013; 72:804–814.  Back to cited text no. 2
    
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Martinoli C, Pretolesi F, Crespi G, Bianchi S, Gandolfo N, Valle M, Derchi LE et al. Power Doppler sonography: clinical applications. Eur J Radiol 1998; 28:133–140.  Back to cited text no. 3
    
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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; 48:955–962.  Back to cited text no. 4
    
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Mc Queen F, Lassere M, Edmonds J, Conaghan P, Peterfy C, Bird P et al. OMERACT rheumatoid arthritis magnetic resonance imaging studies. Summary of OMERACT MR imaging module. J Rheumatol 2003; 30:1387–1392.  Back to cited text no. 5
    
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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 2008; 47:13–21.  Back to cited text no. 6
    
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Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31:315–324.  Back to cited text no. 7
    
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Schirmer C, Schell A, Althoff CH. Diagnostic quality and scoring of synovitis, tenosynovitis and erosions in low-field MRI of patients with rheumatoid arthritis: a comparison with conventional MRI. Ann Rheum Dis 2007; 66:522–529.  Back to cited text no. 8
    
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Heijde D. Quantification of radiological damage in inflammatory arthritis: rheumatoid arthritis, psoriatic arthritis and ankylosing spondylitis. Best Pract Res Clin Rheumatol 2004; 18:847–860.  Back to cited text no. 9
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Ostergaard M, Ejbjerg B. Magnetic resonance imaging of the synovium in rheumatoid arthritis. Semin Musculoskelet Radiol 2004; 8:287–299.  Back to cited text no. 10
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Taniguchi D, Tokunaga D, Oda R, Fujiwara H, Ikeda T, Ikoma K et al. Maximum intensity projection with magnetic resonance imaging for evaluating synovitis of the hand in rheumatoid arthritis: comparison with clinical and ultrasound findings. Clin Rheumatol 2014; 33:911–917.  Back to cited text no. 11
    
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Boutry N, Morel M, Flipo RM, Demondion X, Cotten A. Early rheumatoid arthritis: a review of MRI and sonographic findings. Am J Roentgenol 2007; 189:1502–1509.  Back to cited text no. 12
    
13.
Boesen M, Ellegaard K, Boesen L, Cimmino MA, Jensen PS, Terslev L et al. Ultrasound Doppler score correlates with OMERACT RAMRIS bone marrow oedema and synovitis score in the wrist joint of patients with rheumatoid arthritis. Ultraschall Med 2012; 33:166–172.  Back to cited text no. 13
    
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Fukuba E, Yoshizako T, Kitagaki H, Murakawa Y, Kondo M, Uchida N. Power Doppler ultrasonography for assessment of rheumatoid synovitis: comparison with dynamic magnetic resonance imaging. Clin Imaging 2013; 37:134–137.  Back to cited text no. 14
    
15.
Terslev L, Torp-Pedersen S, Savnik A, von der Recke P, Qvistgaard E, Danneskiold-Samsøe B, Bliddal H. Doppler ultrasound and magnetic resonance imaging of synovial inflammation of the hand in rheumatoid arthritis: a comparative study. Arthritis Rheum 2003; 48:2434–2441.  Back to cited text no. 15
    


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