Role of Ultrasound and MRI in Detection of Hand and Wrist Joints Erosions in Rheumatoid Arthritis Patients, Comparative Study

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1 Med. J. Cairo Univ., Vol. 83, No. 1, September: , Role of Ultrasound and MRI in Detection of Hand and Wrist Joints Erosions in Rheumatoid Arthritis Patients, Comparative Study MOHAMED EL-GHOBASHY, M.Sc.*; HATEM EL-AZIZY, M.D.*; MANAR HUSSEIN, M.D.* and HEND HELAL, M.D.** The Departments of Diagnostic Radiology* and Rheumatology**, Faculty of Medicine, Cairo University Abstract Objective: To compare the role of musculoskeletal ultrasonography and MRI in the detection of erosions of the wrist and hand joints in Rheumatoid arthritis patients. Patients and Methods: This study included fifty patients (39 females and 11 males) with rheumatoid arthritis. They were subjected to high resolution grey scale ultrasound study and MRI examination of the clinically dominant wrist joints. Mean age was 45.3 years and mean disease duration was 6.2 years. Comparison and correlation between both modalities was done. Results: Our results showed that both modalities are comparable and closely related in the detection of erosions in hand and wrist joints in rheumatoid arthritis patients. Key Words: MRI Rheumatoid arthritis Ultrasound Erosions. Introduction RHEUMATOID arthritis is a chronic disease affecting approximately 1% of the world's population. It is a systemic autoimmune disease involving mainly joints and targeting the synovium, with progression of the disease and lack of proper treatment, permanent disorganization and destruction of the joints will occur with subsequent severe deformity and disability [1]. New effective treatments aiming to prevent joint destruction are available now increasing the demand for more sensitive imaging tools especially at an early stage of the disease to monitor and predict disease progression and thus reduce burden on the patients [2,3]. Correspondence to: Dr. Mohamed El-Ghobashy, The Department of Diagnostic Radiology, Faculty of Medicine, Cairo University Bone erosions are the hallmark of severe progressive arthritis leading to joint destruction and deformity. Most of the erosions occur during the first two years of the disease [4]. In 1987, radiographic erosions were included in the diagnostic criteria for rheumatoid arthritis by the American College of Rheumatology and were thought to be both sensitive and specific for the condition, the presence of bone erosions at the time of diagnosis has been shown to be related to a poor long-term clinical outcome [1]. Bone erosions result from proliferative synovitis. They are less frequently bilateral than synovitis or tenosynovitis. The capitate, triquetrum, and lunate bones & the radial aspect of the second and third metacarpal bones are commonly affected [2]. Assessment of disease activity in the joints of RA patients includes clinical examination as well as measurement of the levels of markers such as serum C-reactive protein (CRP). The presence of joint erosions is generally assessed by traditional X-rays, but recently more sensitive techniques have been employed to study bone erosions in RA patients, particularly at diagnosis [5,6]. Evaluation of hand arthritis being the most common site of rheumatoid arthritis (RA) is important for diagnosis and evaluation of disease activity. As new imaging methods, magnetic resonance imaging (MRI) and joint ultrasonography (US) are currently used in RA [1]. Magnetic resonance imaging (MRI) is an excellent tool for detecting synovitis and is better than X-rays for showing bone changes in the majority of patients with early RA [8,9]. 615

2 616 Role of Ultrasound & MRI in Detection of Hand & Wrist Joints Erosions Ultrasonography (US), thanks to the introduction of the multi-frequency linear array transducer and advanced software updates, became a promising tool in bone erosion detection. Comparison with MRI and retrospective reviews of radiographs have confirmed the specificity of the additional lesions detected by sonography [4,10]. The purpose of the present study is to compare the role of grey scale musculoskeletal ultrasonography and MRI in detection of erosions in the wrist and hand joints in Rheumatoid arthritis patients. Patients and Methods Fifty Rheumatoid Arthritis (RA) patients were recruited for this study, from the Rheumatology and Rehabilitation outpatient clinic, Faculty of Medicine, Cairo University Hospitals through the period from March 2012 to November This study included 39 females and 1 1 males, their age ranged from 22 to 68 years with a mean age of 45.3, the duration of the disease ranged from one year to 18 years. Inclusion criteria: - Clinical diagnosis of rheumatoid arthritis (RA) according to the American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis [11]. - No apparent deformities of the wrist and hand joints clinically. - X-ray revealed either subtle changes or normal study. Exclusion criteria: - Advanced deformities of the wrist and hand joints were detected clinically. - Renal impairment. - Contraindications to MRI (e.g. claustrophobia, pacemakers). All patients included in this study were subjected to ultrasonography examination as well as MRI study. I- Ultrasonography (US): Ultrasonography of the wrist joints were performed by GE LOGIQ P6 Pro ultrasound machines using a near focused linear array transducer with a center frequency of MHz. During examination of hand joints and wrists: The patient was examined while sitting upright, with the hand placed on a cushion and fully pronated then supinated. Dorsal longitudinal scan followed by dorsal transverse scan were done followed by palmar examination in supination. Grey-scale imaging evaluation confirmed the presence or absence of erosions according to the OMERACT definition of an erosion seen on ultrasound imaging being an intra articular discontinuity of the bone surface that is visible in two perpendicular planes [1,12]. Each patient evaluation took no more than 20 min, including documentation, and the images demonstrating maximal abnormalities were archived. II- MRI study: Magnetic resonance examination of the dominant wrist joint was performed using Philips Intera 1.5T (closed) patients were placed in 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 STIR WIs were acquired and axial T1WIs of the wrist using the parameters in (Table 1). Table (1): MRI technical parameters. TR TE Matrix Average time T1WIs X 150 (coronal) 90 8mins (axial) STIR WIs X 150 (coronal) 90 8mins (axial) Evaluation of MRI images: FOV Flip angle The OMERACT definition of an erosion on MRI is a sharply marginated bone lesion with correct juxta articular location and typical signal characteristics that is visible in at least two planes with a cortical break seen in at least one plane. In addition to breach of the cortex, the erosion itself generally contains inflammatory tissue or fluid showing high signal on STIR WI weighted images [12]. Statistical analysis: Data were statistically described in terms of mean ± standard deviation ( ±SD), and range, or frequencies (number of cases) and percentages when appropriate. Comparison between MRI and US results was done using McNemar test and Chi square (χ 2) test when appropriate. Agreement was tested using kappa statistic. Correlation between

3 Mohamed El-Ghobashy, et al. 617 various variables was done using Spearman rank correlation equation for non-normal variables. p- values less than 0.05 was considered statistically significant. All statistical calculations were done using computer programs SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA) version 15 for Microsoft Windows. Results Fifty adult Rheumatoid Arthritis patients diagnosed as RA according to the 1987 revised American College of Rheumatology (ACR) criteria for classification of Rheumatoid Arthritis, [11] were inclued in the study. They were 39 females (78%) and 11 males (22%), their ages ranged from 22 to 68 years with a mean age of 45.3 years ± The disease duration ranged from one year to 18 years with a mean of 6.20 years ±4.2 thirty nine patients (78%) were seropostive (RF) and eleven patients (22%) were seronegative (RF). Thirty one patients were positive for CRP (60%). Results of ultrasonography examination: Erosions were found in, 30 wrist joints (60%) and 27 MCPs (13.5%) as demonstrated in (Tables 2,3). Table (2): Frequency of erosions in wrist joints by ultrasound. No. of erosions Frequency Percent Table (3): Distribution of erosions among MCPs by ultrasound. Effusion 2 nd MCP 3 rd MCP 4th MCP 5th MCP Positive Negative Table (5): Distribution of erosions among wrist joints by MRI. No. of Erosions Number of wrist joints Percent Comparison between US & MRI in the detection of hand joints pathology: Comparison between US and MRI in the detection of erosions of wrist joints (Table 6). Erosions-MRI: Erosions ultrasound Absent Percent Total Absent N Present N Total N Ultrasound detected erosions in 35 wrist joints and MRI detected erosions in 37 wrist joints Figs. (1-3). Both modalities agreed in 30 wrist joints, ultrasound missed erosions in 7 joints detected by MRI and MRI missed erosions in 5 joints detected by ultrasound Results of Magnetic Resonance Imaging (MRI) examination: Erosions were detected in 37 wrist joints (74%) and 25 MCP joints (12.5%), (Tables 4,5). 5 0 Absent Erosions ultrasound Present Erosions-MRI Table (4): Frequency of erosions among wrist and MCP joints by MRI. Fig. (1): Comparison between US and MRI in the detection of erosions of wrist joints. Erosions Positive Negative Wrist 2 nd MCP 3rd MCP 4th MCP 5th MCP Statistical analysis of these results showed significant agreement between the two modalities in the detection of erosions. Comparison of US and MRI yielded a weighted Kappa value of

4 618 Role of Ultrasound & MRI in Detection of Hand & Wrist Joints Erosions (A) Fig. (2-A,B): Coronal T 1WIs of the wrist joint and longitudinal ultrasound image showing multiple erosions of the carpal bones. (B) Ultrasound detected erosions in 27 MCP joints and MRI detected erosions in 25 MCP joints Fig. (4). Both modalities agreed in 15 joints, ultrasound missed 10 joints detected by MRI (Table 7). Table (7): Comparison between US and MRI in the detection of erosions of MCPs joints. Erosions ultrasound Absent Percent Total Erosions-MRI: Absent N Present N Total N (A) (B) (A) (C) Fig. (3-A,B,C): Coronal MRI T1WIs A and longitudinal ultrasound images B,C revealed multiple erosions involving the carpal bones. (B) Fig. (4-A,B): Coronal T1WIs and longitudinal ultrasound image showing 2 nd MCP erosion.

5 Mohamed El-Ghobashy, et al. 619 Discussion The higher sensitivity of MRI and US compared to conventional X-ray examination had already been established in many studies [8,10,13,14]. Owing to its limited availability and high cost, MRI role became limited despite being the standard practice in the diagnostic assessment of early arthritis in patients with negative radiographic findings [4]. Therefore, the use of US might represent a feasible alternative. Our study demonstrates that US is comparable to MRI in erosion detection as regards the wrist and hand joints, in this study ultrasound detected erosions in 57/250 joints (22.8%) and MRI detected erosions in 62/250 joints (24.8%). Scheel and his coworkers [15] studied the MCPs and PIPs II-V (128 joints) of the clinically dominant hand of 16 patients with RA, the number of erosions and the presence of synovitis were determined for each joint and graded as either normal (0) or abnormal (1). They demonstrated that US had detected erosions in 12 joints (9%) while MRI did so in 34 joints (27%) which is even lower than our results, however they explained the small number of erosions detected by US, by possibly the significantly low resolution of US device and the need to use an acoustic standoff pad. Also, by that neither ulnar nor radial aspects of the joints were evaluated by US, raising the possibility that some erosions might have been missed. As for detection of bone erosions, Szkudlarek and his coworkers, [16] found that US and MRI were similar, in their study at least one modality detected bone erosions in 10 1 quadrants of MCPs, there was agreement between both modalities regarding the presence of erosions in 49 quadrants (49%), and MRI identified bone erosions in only 26 quadrants (26%). In our study at least one modality detected signs of bone destruction in 27 MCP joints, agreement between both modalities in 15 joints (55.6%), and MRI identified erosions in only 10 MCP joints (3 7%), they studied joints using the quadrant as a unit while in our study we used the joint as a unit. Another study conducted by Magnani and his coworkers, [4] compared the Ultrasonography and MRI in their capability to detect bone erosions in RA patients, they examined thirteen patients with advanced RA, the wrist joints as well as the MCPs were examined by MRI with contrast and ultra- sound, they found no significant difference between both modalities in detecting erosions in wrist joints, and this matches with our results, where both modalities agreed in detecting erosions in 30 wrist joints (8 1 %) out of 3 7 joints detected by MRI. US examination is less expensive than other imaging modalities; the time required to perform it is similar to MRI, but longer than conventional X-ray. Conclusion: We conclude that both modalities are comparable and closely related as regards detection of bone destructive changes in hand and wrist joints of rheumatoid arthritis patients and we consider that US examination is a useful tool in detection of erosions during the early phase in all rheumatoid arthritis patients or, at least, in those without erosions on conventional X-ray examination. In addition, US examination could be utilized in the follow-up and monitoring of patients with established diagnosis of rheumatoid arthritis. References 1- ROWBOTHAM E.L. and GRAINGER A.J.: Rheumatoid arthritis: Ultrasound versus MRI. American Journal of Roentgenology, 197: 541-6, BOUTRY N., MOREL M., FLIPO R.M., DEMONDION X. and COTTEN A.: Early rheumatoid arthritis: A review of MRI and sonographic findings. American Journal of Roentgenology, 189: , QUINN M.A., CONAGHAN P.G., O'CONNOR P.J., KARIM Z., GREENSTEIN A., BROWN A., et al.: Very early treatment with infliximab in addition to methotrexate in early, poor-prognosis rheumatoid arthritis reduces magnetic resonance imaging evidence of synovitis and damage, with sustained benefit after infliximab withdrawal: Results from a twelve-m. Arthritis and Rheumatism, 52: 27-35, MAGNANI M., SALIZZONI E., MULÈ R., FUSCONI M., MELICONI R. and GALLETTI S.: Ultrasonography detection of early bone erosions in the metacarpophalangeal joints of patients with rheumatoid arthritis. Clinical and Experimental Rheumatology, 22: 743-8, GRAUDAL N.A., JURIK A.G., De CARVALHO A. and GRAUDAL H.K.: Radiographic progression in rheumatoid arthritis: A long-term prospective study of 109 patients. Arthritis and Rheumatism, 41: , BOESEN M., ELLEGAARD K., BOESEN L., CIMMINO M.A., JENSEN P.S., 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 in der Medizin, 33: , COLEBATCH A.N., EDWARDS C.J., ØSTERGAARD M., VAN DER HEIJDE D., BALINT P.V., D'AGOSTINO

6 620 Role of Ultrasound & MRI in Detection of Hand & Wrist Joints Erosions M.A., et al.: EULAR recommendations for the use of imaging of the joints in the clinical management of rheumatoid arthritis. Annals of the rheumatic diseases, 72: , BACKHAUS M., BURMESTER G.R., SANDROCK D., LORECK D., HESS D., SCHOLZ A., et al.: Prospective two year follow-up study comparing novel and conventional imaging procedures in patients with arthritic finger joints. Annals of the rheumatic diseases, 61: , KLARLUND M., OSTERGAARD M., JENSEN K.E., MADSEN J.L., SKJØDT H. and LORENZEN I.: Magnetic resonance imaging, radiography, and scintigraphy of the finger joints: One year follow-up of patients with early arthritis. The TIRA Group. Annals of the rheumatic diseases, 59: 521-8, KARIM Z., WAKEFIELD R.J., CONAGHAN P.G., LAW- SON C.A., GOH E., QUINN M.A., et al.: The impact of ultrasonography on diagnosis and management of patients with musculoskeletal conditions. Arthritis and Rheumatism, 44: , ARNETT F.C., EDWORTHY S.M., BLOCH D.A., MC- SHANE D.J., FRIES J.F., COOPER N.S., et al.: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis and rheumatism, 31: , ØSTERGAARD M., PETERFY C., CONAGHAN P., MCQUEEN F., BIRD P., EJBJERG B., et al.: OMERACT rheumatoid arthritis magnetic resonance imaging studies. Core set of MRI acquisitions, joint pathology definitions, and the OMERACT RA-MRI scoring system. In Journal of Rheumatology, Volume 30. pp , WAKEFIELD R.J., GIBBON W.W., CONAGHAN P.G., O'CONNOR P., McGONAGLE D., PEASE C., et al.: The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: A comparison with conventional radiography. Arthritis and Rheumatism, 43: , GRASSI W., FILIPPUCCI E., FARINA A., SALAFFI F. and CERVINI C.: Ultrasonography in the evaluation of bone erosions. Annals of the rheumatic diseases, 60: , SCHEEL A.K., HERMANN K.G.A., OHRNDORF S., WERNER C., SCHIRMER C., DETERT J., et al.: Prospective 7 year follow-up imaging study comparing radiography, ultrasonography, and magnetic resonance imaging in rheumatoid arthritis finger joints. Annals of the rheumatic diseases, 65: , SZKUDLAREK M., KLARLUND M., NARVESTAD E., COURT-PAYEN M., STRANDBERG C., JENSEN K.E., et al.: Ultrasonography of the metacarpophalangeal and proximal interphalangeal joints in rheumatoid arthritis: A comparison with magnetic resonance imaging, conventional radiography and clinical examination. Arthritis research & therapy, 8: R52, MAGARELLI N., GUGLIELMI G., Di MATTEO L., TARTARO A., MATTEI P.A. and BONOMO L.: Diagnostic utility of an echo-contrast agent in patients with synovitis using power doppler ultrasound: A preliminary study with comparison to contrast-enhanced MRI. European Radiology, 11: , 2001.

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