Rheumatology Advance Access published March 22, 2014
RHEUMATOLOGY
Concise report
53, 273
doi:10.1093/rheumatology/keu034
Synovial inflammation assessed by ultrasonography correlates with MRI-proven osteitis in patients with rheumatoid arthritis
Objective. The aim of this study was to explore whether assessment of synovial inflammation by ultrasonography correlates with MRI-proven osteitis in patients with RA. Methods. Thirty RA patients who fulfilled 2010 RA classification criteria and were naive to DMARDs, including biologics and glucocorticoids, were consecutively enrolled in this study. Grey scale (GS) and power Doppler (PD) images of articular synovitis and bone erosion in both wrist and MCP joints were evaluated by the method proposed by the European League Against Rheumatism. MRI-proven osteitis of the identical sites was also evaluated within 3 days using the RA MRI scoring system (RAMRIS). The CochranArmitage test and Spearman’s correlation coefficient were used to investigate the correlation of each US finding with MRI-proven osteitis. Results. MRI-proven osteitis was found in 8.3% of MCP joints and 48.3% of wrist joints. Its prevalence was increased in the joints where the GS or PD grade of articular synovitis was 2 or 3. In addition, MRIproven osteitis was found preferentially in the joints positive for bone erosion on US. A clear correlation was demonstrated between the GS or PD grade of articular synovitis or the presence of US bone erosion and RAMRIS osteitis score in both MCP joints and wrist joints. Conclusion. Our data indicate that joint injury assessed by US correlates with MRI-proven osteitis in patients with RA. Key words: rheumatoid arthritis, ultrasonography, magnetic resonance imaging, synovitis, osteitis.
Introduction Ultrasonography is a useful imaging modality in patients suffering from arthritis conditions that can be used to reveal articular synovitis, tenosynovitis and bone erosion [13]. In RA, apparent bone erosion is the characteristic 1 Department of Public Health and 2Department of Immunology and Rheumatology, Nagasaki University Graduate School of Biomedical Sciences, 3Center for Health & Community Medicine, Nagasaki University, 4Department of Health Sciences and 5Department of Radiological Sciences, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki and 6Department of Internal Medicine, Sasebo City General Hospital, Sasebo, Japan.
Submitted 9 August 2013; revised version accepted 28 January 2014. Correspondence to: Shin-ya Kawashiri, Department of Public Health, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan. E-mail: [email protected]
feature, resulting from osteoclastic bone resorption derived from a combination of synovitis and osteitis [4]. Our recent report suggests that US-proven moderate to severe synovitis is indicative of subsequent bone damage, although US is not able to directly detect bone inflammation [3]. Via MRI, synovitis, osteitis and bone erosion have been identified [57]. Our previous research has shown that osteitis is the most specific MRI feature to predict the development of RA among patients with early undifferentiated arthritis [7]. These observations have been followed by immunohistochemical analysis of bone specimens, in which postoperative samples positive for pre-operative MRI-proven osteitis were found to contain increased numbers of osteoclasts and receptor activator nuclear factor kB (NF-kB) ligand expression [8].
! The Author 2014. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected]
1
CLINICAL SCIENCE
Abstract
Downloaded from http://rheumatology.oxfordjournals.org/ at Serials Section Norris Medical Library on April 2, 2014
Shin-ya Kawashiri1,2, Takahisa Suzuki2, Yoshikazu Nakashima2, Yoshiro Horai2, Akitomo Okada2, Ayako Nishino2, Naoki Iwamoto2, Kunihiro Ichinose2, Kazuhiko Arima1, Mami Tamai3, Hideki Nakamura2, Tomoki Origuchi4, Masataka Uetani5, Kiyoshi Aoyagi1, Katsumi Eguchi6 and Atsushi Kawakami2
Shin-ya Kawashiri et al.
Considering that US-proven moderate to severe synovitis and MRI-proven osteitis are landmarks of RA, these are suspected to both be present, although reports that show the presence of both synovitis and osteitis have not been found in the literature. In the present study we focused on the wrist and MCP joints, which are most affected by RA, and tried to identify the correlations between US findings and MRI features.
Patients and methods Patients
Clinical and laboratory assessment A diagnosis of RA was made by Japan College of Rheumatology (JCR)certified rheumatologists (H.N. and A.K.) using clinical histories, physical findings, blood tests including RF (Dade Behring, Marburg, Germany; cut-off value 14 IU/ml), ACPA (DIASTAT anti-CCP, Axis-Shield, Dundee, UK; cut-off value 4.5 U/ml), CRP (Eiken Chemical, Tokyo, Japan) and ESR, hands and feet plain radiography and the 2010 RA classification criteria [9].
US assessment Each patient underwent a US assessment on the same day as the clinical evaluation by a JCR-certified rheumatologist (S.K.) who was blinded to the clinical and MRI findings (S.K. is also an instructor of US certified by JCR). Images from all the examinations were stored and the US scoring reliability was examined in randomly selected patients at the end of the study. The obtained images were also evaluated by the other experienced US examiner (T.S.) and the two examiners discussed and reached a consensus score. A systematic multiplanar grey scale (GS) and power Doppler (PD) examination of the second to fifth MCP joints (proximal and distal) and wrist joints was performed with the same scanner (Toshiba AplioXG) using a multifrequency linear transducer (12 MHz). These same sites are examined in the osteitis RA MRI scoring system (RAMRIS) developed by the OMERACT Magnetic Resonance Imaging Group [10]. The US score included the following 10 joints per person: bilateral wrists and the second to fifth MCP joints. We scanned a total of 300 joints (60 wrists and 240 MCP joints) in 30 RA patients. All joint regions were sonographically examined in a standardized manner according to the European League Against Rheumatism (EULAR) [11] and JCR guidelines on a semi-quantitative scale as described [12, 13]. Settings for PD (velocity range
2
MRI assessment Plain MRIs of the wrist and finger joints were acquired using a 1.5 T system (Sigma, GE Medical Systems, Milwaukee, WI, USA) with an extremity coil, as we recently described [7, 14], within 3 days of the US evaluation. The images were evaluated for osteitis by an OMERACTRAMRIS technique (evaluated by M.U., who is an experienced musculoskeletal radiologist and blinded to the clinical status and US findings) at the standard sites of the second to fifth MCP joints (proximal and distal) and wrist joints (first to fifth base of the metacarpal, trapezium, trapezoid, capitate, hamate, scaphoid, lunate, triquetrum, pisiform, distal radius and distal ulna) [10]. Osteitis is defined by a lesion within the trabecular bone with ill-defined margins and signal characteristics consistent with increased water content: high signal intensity on weighted fat-saturated and short tau inversion recovery images and low signal intensity on T1-weighted images [10].
Statistical analyses The presence of an association between a variable containing two variables, such as US-proven synovitis (GS and PD grade) or US-proven bone erosion and MRIproven osteitis, was analysed by the CochranArmitage test and Spearman’s correlation coefficient. The overall significance level for statistical analysis was 5% (twosided). P-values
RHEUMATOLOGY
Concise report
53, 273
doi:10.1093/rheumatology/keu034
Synovial inflammation assessed by ultrasonography correlates with MRI-proven osteitis in patients with rheumatoid arthritis
Objective. The aim of this study was to explore whether assessment of synovial inflammation by ultrasonography correlates with MRI-proven osteitis in patients with RA. Methods. Thirty RA patients who fulfilled 2010 RA classification criteria and were naive to DMARDs, including biologics and glucocorticoids, were consecutively enrolled in this study. Grey scale (GS) and power Doppler (PD) images of articular synovitis and bone erosion in both wrist and MCP joints were evaluated by the method proposed by the European League Against Rheumatism. MRI-proven osteitis of the identical sites was also evaluated within 3 days using the RA MRI scoring system (RAMRIS). The CochranArmitage test and Spearman’s correlation coefficient were used to investigate the correlation of each US finding with MRI-proven osteitis. Results. MRI-proven osteitis was found in 8.3% of MCP joints and 48.3% of wrist joints. Its prevalence was increased in the joints where the GS or PD grade of articular synovitis was 2 or 3. In addition, MRIproven osteitis was found preferentially in the joints positive for bone erosion on US. A clear correlation was demonstrated between the GS or PD grade of articular synovitis or the presence of US bone erosion and RAMRIS osteitis score in both MCP joints and wrist joints. Conclusion. Our data indicate that joint injury assessed by US correlates with MRI-proven osteitis in patients with RA. Key words: rheumatoid arthritis, ultrasonography, magnetic resonance imaging, synovitis, osteitis.
Introduction Ultrasonography is a useful imaging modality in patients suffering from arthritis conditions that can be used to reveal articular synovitis, tenosynovitis and bone erosion [13]. In RA, apparent bone erosion is the characteristic 1 Department of Public Health and 2Department of Immunology and Rheumatology, Nagasaki University Graduate School of Biomedical Sciences, 3Center for Health & Community Medicine, Nagasaki University, 4Department of Health Sciences and 5Department of Radiological Sciences, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki and 6Department of Internal Medicine, Sasebo City General Hospital, Sasebo, Japan.
Submitted 9 August 2013; revised version accepted 28 January 2014. Correspondence to: Shin-ya Kawashiri, Department of Public Health, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan. E-mail: [email protected]
feature, resulting from osteoclastic bone resorption derived from a combination of synovitis and osteitis [4]. Our recent report suggests that US-proven moderate to severe synovitis is indicative of subsequent bone damage, although US is not able to directly detect bone inflammation [3]. Via MRI, synovitis, osteitis and bone erosion have been identified [57]. Our previous research has shown that osteitis is the most specific MRI feature to predict the development of RA among patients with early undifferentiated arthritis [7]. These observations have been followed by immunohistochemical analysis of bone specimens, in which postoperative samples positive for pre-operative MRI-proven osteitis were found to contain increased numbers of osteoclasts and receptor activator nuclear factor kB (NF-kB) ligand expression [8].
! The Author 2014. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected]
1
CLINICAL SCIENCE
Abstract
Downloaded from http://rheumatology.oxfordjournals.org/ at Serials Section Norris Medical Library on April 2, 2014
Shin-ya Kawashiri1,2, Takahisa Suzuki2, Yoshikazu Nakashima2, Yoshiro Horai2, Akitomo Okada2, Ayako Nishino2, Naoki Iwamoto2, Kunihiro Ichinose2, Kazuhiko Arima1, Mami Tamai3, Hideki Nakamura2, Tomoki Origuchi4, Masataka Uetani5, Kiyoshi Aoyagi1, Katsumi Eguchi6 and Atsushi Kawakami2
Shin-ya Kawashiri et al.
Considering that US-proven moderate to severe synovitis and MRI-proven osteitis are landmarks of RA, these are suspected to both be present, although reports that show the presence of both synovitis and osteitis have not been found in the literature. In the present study we focused on the wrist and MCP joints, which are most affected by RA, and tried to identify the correlations between US findings and MRI features.
Patients and methods Patients
Clinical and laboratory assessment A diagnosis of RA was made by Japan College of Rheumatology (JCR)certified rheumatologists (H.N. and A.K.) using clinical histories, physical findings, blood tests including RF (Dade Behring, Marburg, Germany; cut-off value 14 IU/ml), ACPA (DIASTAT anti-CCP, Axis-Shield, Dundee, UK; cut-off value 4.5 U/ml), CRP (Eiken Chemical, Tokyo, Japan) and ESR, hands and feet plain radiography and the 2010 RA classification criteria [9].
US assessment Each patient underwent a US assessment on the same day as the clinical evaluation by a JCR-certified rheumatologist (S.K.) who was blinded to the clinical and MRI findings (S.K. is also an instructor of US certified by JCR). Images from all the examinations were stored and the US scoring reliability was examined in randomly selected patients at the end of the study. The obtained images were also evaluated by the other experienced US examiner (T.S.) and the two examiners discussed and reached a consensus score. A systematic multiplanar grey scale (GS) and power Doppler (PD) examination of the second to fifth MCP joints (proximal and distal) and wrist joints was performed with the same scanner (Toshiba AplioXG) using a multifrequency linear transducer (12 MHz). These same sites are examined in the osteitis RA MRI scoring system (RAMRIS) developed by the OMERACT Magnetic Resonance Imaging Group [10]. The US score included the following 10 joints per person: bilateral wrists and the second to fifth MCP joints. We scanned a total of 300 joints (60 wrists and 240 MCP joints) in 30 RA patients. All joint regions were sonographically examined in a standardized manner according to the European League Against Rheumatism (EULAR) [11] and JCR guidelines on a semi-quantitative scale as described [12, 13]. Settings for PD (velocity range
2
MRI assessment Plain MRIs of the wrist and finger joints were acquired using a 1.5 T system (Sigma, GE Medical Systems, Milwaukee, WI, USA) with an extremity coil, as we recently described [7, 14], within 3 days of the US evaluation. The images were evaluated for osteitis by an OMERACTRAMRIS technique (evaluated by M.U., who is an experienced musculoskeletal radiologist and blinded to the clinical status and US findings) at the standard sites of the second to fifth MCP joints (proximal and distal) and wrist joints (first to fifth base of the metacarpal, trapezium, trapezoid, capitate, hamate, scaphoid, lunate, triquetrum, pisiform, distal radius and distal ulna) [10]. Osteitis is defined by a lesion within the trabecular bone with ill-defined margins and signal characteristics consistent with increased water content: high signal intensity on weighted fat-saturated and short tau inversion recovery images and low signal intensity on T1-weighted images [10].
Statistical analyses The presence of an association between a variable containing two variables, such as US-proven synovitis (GS and PD grade) or US-proven bone erosion and MRIproven osteitis, was analysed by the CochranArmitage test and Spearman’s correlation coefficient. The overall significance level for statistical analysis was 5% (twosided). P-values
