Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
Contents lists available at ScienceDirect
Best Practice & Research Clinical Rheumatology journal homepage: www.elsevierhealth.com/berh
6
Novel imaging modalities in spondyloarthritis Lennart Jans, MD, PhD a, *, Jacob L. Jaremko, MD, PhD, FRCPC, Radiologist and Assistant Professor b, 1, Gurjit S. Kaeley, MBBS, MRCP, RhMSUS, Division Chief Associate Professor of Medicine, Rheumatology Fellowship Program Director, Director of Musculoskeletal Ultrasound c, 2 a
Department of Radiology, Faculty of Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Gent, Belgium b Dept. of Radiology and Diagnostic Imaging, Faculty of Medicine and Dentistry, University of Alberta Hospital, 2A2.41 WMC, 8440 e 112 St. NW, Edmonton T6G 2B7, AB, Canada c Division of Rheumatology, University of Florida College of Medicine, 653-1 West Eight Street, LRC 2nd Floor L-14, Jacksonville, FL 32209-6561, USA
a b s t r a c t Keywords: Spondyloarthritis Magnetic resonance imaging Ultrasound Sacroiliitis Diagnostic utility
Novel imaging techniques have emerged in the field of spondyloarthritis. This article will cover the role of, and the sensitivity and specificity of magnetic resonance imaging (MRI) and ultrasound in the diagnosis and monitoring of axial and peripheral SpA. It will discuss how the definition of a ‘positive MRI’ of the sacroiliac joints and spine is evolving. Differential diagnoses of inflammatory lesions of both the sacroiliac joints and the spine are addressed due to their importance in image interpretation. The article will also discuss the role of sonography in assessing peripheral entheses, joints, tendon sheaths, nails and soft tissues. The utility for clinical as well as an outcome measure will be discussed. We finally aim to give guidance on when and how to use these new modalities and on how to analyse and interpret the imaging findings in daily practice. © 2014 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ32 9 332 69 38. E-mail addresses: [email protected] (L. Jans), [email protected]fl.edu (G.S. Kaeley). 1 2
URL: http://www.ualberta.ca/~jjaremko/ Tel.: þ780 407 6907; fax: þ780 407 3853. Tel.: þ904 244 3702; fax: þ904 244 5650.
http://dx.doi.org/10.1016/j.berh.2014.10.006 1521-6942/© 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
2
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
Practice points - Imaging is important in early diagnosis of spondyloarthritis - MRI plays a key role in diagnosis and classification of patients with axial spondyloarthritis - Ultrasound shows arthritis, enthesitis and dactylitis in patients with peripheral spondyloarthritis Research agenda - A more stringent definition of a positive MRI’ may decrease false positive diagnosis of spondyloarthritis - Developing validated ultrasound arthritis, enthesitis and dactylitis scoring systems as outcome measures according to the OMERACT filter.
Introduction Seronegative axial spondyloarthritis (SpA) is a chronic inflammatory disease that affects the sacroiliac joints (SIJs) and the spine [1e5]. Peripheral manifestations of SpA include arthritis of synovial joints in the appendicular skeleton, enthesitis or dactylitis. On average, axial SpA remains undiagnosed for up to 7 years from the onset of clinical symptoms. There is an ongoing debate about the appropriate imaging approach in patients with suspected or confirmed SpA. As magnetic resonance imaging (MRI) of the SIJs enables the early diagnosis of axial SpA, its use in clinical practice has increased dramatically during the last decade [1]. Sonographic evaluation of non-axial manifestations of spondyloarthropathy may aid in diagnosis and may have a role as an outcome measure. In the following article, we will discuss utility of ultrasound in imaging the joints, entheses, soft tissues and digits of patients with spondyloarthropathy. MR imaging A thorough knowledge of normal imaging findings, typical features in SpA, and the differential diagnosis are crucial in image analysis and interpretation. This article presents recommendations for the use and interpretation of MRI and ultrasound in SpA based on expert opinion and on literature review. Why should we image? Axial SpA can be distinguished on the basis of patient history and typical clinical and laboratory findings. Patients with inflammatory back pain with an insidious onset of symptoms, 50% of all active lesions are located in the thoracic spine [14]. Should contrast medium be included in the MRI protocol?. Currently, it is under debate if the administration of contrast media increases the detection of osteitis, capsulitis, enthesitis and synovitis on MRI of the SIJs [15]. If BME is present, which is the main and mandatory feature in the diagnosis of axial SpA, STIR images only are sufficient. In the European Society of Skeletal Radiology (ESSR) arthritis subcommittee consensus paper, radiologists strongly state that contrast medium is of diagnostic importance for the differentiation of diagnoses other than sacroiliitis and should be applied in doubtful cases [6]. In children, the use of contrast medium is accepted by many for the detection of early subtle inflammatory changes in juvenile SpA [16]. MR image interpretation Sacroiliac joints. The SIJs are the most frequently involved site in SpA. The early lesions are tiny discontinuities of the subchondral bone plate along with subcortical BME, typically located at the inferior half of the joints and at the iliac surface, which is lined by fibrocartilage and less resistant to inflammatory damage. Active lesions are typically depicted on the STIR images. BME, one of the most important MRI features in SpA, is considered an active lesion, as well as capsulitis, enthesitis and synovitis. Structural changes are typically seen on the T1-weighted images and include fat deposition, erosions that sometimes result in a widened joint space with “string of pearls” appearance, sclerosis, “backfill” where the eroded joint reossifies [17] and finally ankylosis [6]. Spine. The spine is the second most frequent site of involvement in SpA. When vertebrae are involved, lesions generally present initially as erosions at the anterior aspect of the thoracolumbar vertebral bodies [18]. Later, the erosions are associated with sclerotic changes and syndesmophytes, which, in long-standing disease, tend to fuse. The distribution pattern of active and structural lesions includes corner inflammatory lesions, central inflammatory lesions and BME in the lateral and posterior spinal segments such as the pedicle, costotransverse and costovertebral joints is characteristic of SpA (Fig. 4) [15]. BME in these anatomical locations indicates active inflammation, whereas fatty infiltration or Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
5
Fig. 4. (aed) Active spinal SpA lesions in a 41-year-old male patient. Sagittal STIR MR images of the spine shows typical anterior and posterior corner inflammatory lesions in the thoracic spine as BME (arrows). Aseptic spondylodiscitis is seen as symmetric bone marrow edema of two adjacent vertebral bodies centred on the intervertebral disc space (arrowheads). BME of the head of rib is also present (long arrow). BME of the synchondrosis of the sternum is also depicted.
even ankylosis of the small joints indicate structural damage. Syndesmophytes, being thin strands of cortical bone, are generally best seen on radiographs, but, if prominent, they can at times be detected on MRI as well. Noninfectious spondylodiscitis is less common, and when present is characterized by BME and erosion at the vertebral end plates (Fig. 5). BME in the spinous process or at the ligament insertions on the spinous processes is also a feature of SpA [6]. Although spinal lesions typically develop later in the disease course than sacroiliitis, they may be the only active lesions in a symptomatic patient with longstanding disease, and therefore may determine prognosis and need for treatment, motivating routine whole-spine MRI in SpA monitoring at some centres [17]. Differential diagnosis Sacroiliitis. Diagnosing inflammatory sacroiliitis on MRI is not always straightforward and can be challenging. Several alternative diagnoses can be suggested based on a characteristic MRI appearance. Infectious sacroiliitis, osteitis condensans ilii, insufficiency fractures, osteoarthritis, diffuse idiopathic skeletal hyperostosis, anatomical variants and tumour may also result in BME of the SI joints [6,19]. Infection is most often unilateral and may demonstrate a joint effusion and periarticular soft tissue edema or collections. Osteitis condensans ilii generally presents as bilateral nearly symmetric iliac edema and later sclerosis, often triangular in shape and most often in women who have had one or more children, and is presumably related to mechanical strain during childbirth. The SI joint lines should remain smooth without erosions in this condition. Insufficiency fractures will present with linear edema and sclerosis in one or both sacral ala primarily paralleling the SI joints, rather than being centred within the SI joints themselves, which again should not show erosion. Osteoarthritis may have BME and irregularity of articular margins simulating sacroiliitis, but erosions are not a feature, and bony proliferation occurs at articular margins rather than centrally within the joint. Presence of a transitional lumbosacral junction or history of prior trauma may be associated with osteoarthritis [6,19]. Spinal inflammation. There is an overlap between degeneration and inflammation in the spine with regard to clinical symptoms and morphology on MRI. However, knowledge of certain morphological and clinical features facilitates the differentiation between the two entities. The changes seen in Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
6
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
Fig. 5. Active spinal inflammation in a 33-year-old male patient. Sagittal STIR MR image of the spine shows aseptic spondylodiscitis (arrows) as bone marrow edema of two adjacent vertebral bodies centred around the intervertebral disc space.
noninfectious spondylodiscitis are similar to active osteochondrosis. Analysis of the disc (usually not dehydrated in spondylitis), the location (degeneration typically at L4eS1, spondylodiscitis more often at levels higher in the thoracolumbar spine) and presence of other concomitant features such as corner inflammatory lesions may help differentiate these entities. Other differential diagnoses, such as infection, tumour, and stress reaction/fracture should be carefully excluded [6,19]. SpA without active inflammation. Both active and structural lesions of the SIJs and spine can be present in one patient at the same time. Moreover, in late-stage disease or under treatment, inflammatory lesions may turn into structural lesions such as fat deposition [20]. This underlines the importance of careful examination of the T1-weighted images for presence of structural lesions which can be easily missed on inspection of STIR images alone (Fig. 6). Definition of a ‘positive MRI’ for sacroiliitis in SpA It has been argued that the current ASAS definition of a ‘positive MRI’ of the SIJs and spine lacks specificity and may therefore result in false positive diagnosis of SpA. The definition includes BME as the only feature of active inflammation when it is present on at least two consecutive slices if only one lesion is seen, or, alternatively, at least two lesions on one slice should be present [9]. This definition has been fiercely debated among experts, as illustrated by the ESSR arthritis subcommittee consensus paper on imaging in SpA, stating that, in the absence of additional imaging features of SpA in the SIJs or spine, two tiny lesions
Contents lists available at ScienceDirect
Best Practice & Research Clinical Rheumatology journal homepage: www.elsevierhealth.com/berh
6
Novel imaging modalities in spondyloarthritis Lennart Jans, MD, PhD a, *, Jacob L. Jaremko, MD, PhD, FRCPC, Radiologist and Assistant Professor b, 1, Gurjit S. Kaeley, MBBS, MRCP, RhMSUS, Division Chief Associate Professor of Medicine, Rheumatology Fellowship Program Director, Director of Musculoskeletal Ultrasound c, 2 a
Department of Radiology, Faculty of Medicine, Ghent University Hospital, De Pintelaan 185, 9000 Gent, Belgium b Dept. of Radiology and Diagnostic Imaging, Faculty of Medicine and Dentistry, University of Alberta Hospital, 2A2.41 WMC, 8440 e 112 St. NW, Edmonton T6G 2B7, AB, Canada c Division of Rheumatology, University of Florida College of Medicine, 653-1 West Eight Street, LRC 2nd Floor L-14, Jacksonville, FL 32209-6561, USA
a b s t r a c t Keywords: Spondyloarthritis Magnetic resonance imaging Ultrasound Sacroiliitis Diagnostic utility
Novel imaging techniques have emerged in the field of spondyloarthritis. This article will cover the role of, and the sensitivity and specificity of magnetic resonance imaging (MRI) and ultrasound in the diagnosis and monitoring of axial and peripheral SpA. It will discuss how the definition of a ‘positive MRI’ of the sacroiliac joints and spine is evolving. Differential diagnoses of inflammatory lesions of both the sacroiliac joints and the spine are addressed due to their importance in image interpretation. The article will also discuss the role of sonography in assessing peripheral entheses, joints, tendon sheaths, nails and soft tissues. The utility for clinical as well as an outcome measure will be discussed. We finally aim to give guidance on when and how to use these new modalities and on how to analyse and interpret the imaging findings in daily practice. © 2014 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ32 9 332 69 38. E-mail addresses: [email protected] (L. Jans), [email protected]fl.edu (G.S. Kaeley). 1 2
URL: http://www.ualberta.ca/~jjaremko/ Tel.: þ780 407 6907; fax: þ780 407 3853. Tel.: þ904 244 3702; fax: þ904 244 5650.
http://dx.doi.org/10.1016/j.berh.2014.10.006 1521-6942/© 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
2
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
Practice points - Imaging is important in early diagnosis of spondyloarthritis - MRI plays a key role in diagnosis and classification of patients with axial spondyloarthritis - Ultrasound shows arthritis, enthesitis and dactylitis in patients with peripheral spondyloarthritis Research agenda - A more stringent definition of a positive MRI’ may decrease false positive diagnosis of spondyloarthritis - Developing validated ultrasound arthritis, enthesitis and dactylitis scoring systems as outcome measures according to the OMERACT filter.
Introduction Seronegative axial spondyloarthritis (SpA) is a chronic inflammatory disease that affects the sacroiliac joints (SIJs) and the spine [1e5]. Peripheral manifestations of SpA include arthritis of synovial joints in the appendicular skeleton, enthesitis or dactylitis. On average, axial SpA remains undiagnosed for up to 7 years from the onset of clinical symptoms. There is an ongoing debate about the appropriate imaging approach in patients with suspected or confirmed SpA. As magnetic resonance imaging (MRI) of the SIJs enables the early diagnosis of axial SpA, its use in clinical practice has increased dramatically during the last decade [1]. Sonographic evaluation of non-axial manifestations of spondyloarthropathy may aid in diagnosis and may have a role as an outcome measure. In the following article, we will discuss utility of ultrasound in imaging the joints, entheses, soft tissues and digits of patients with spondyloarthropathy. MR imaging A thorough knowledge of normal imaging findings, typical features in SpA, and the differential diagnosis are crucial in image analysis and interpretation. This article presents recommendations for the use and interpretation of MRI and ultrasound in SpA based on expert opinion and on literature review. Why should we image? Axial SpA can be distinguished on the basis of patient history and typical clinical and laboratory findings. Patients with inflammatory back pain with an insidious onset of symptoms, 50% of all active lesions are located in the thoracic spine [14]. Should contrast medium be included in the MRI protocol?. Currently, it is under debate if the administration of contrast media increases the detection of osteitis, capsulitis, enthesitis and synovitis on MRI of the SIJs [15]. If BME is present, which is the main and mandatory feature in the diagnosis of axial SpA, STIR images only are sufficient. In the European Society of Skeletal Radiology (ESSR) arthritis subcommittee consensus paper, radiologists strongly state that contrast medium is of diagnostic importance for the differentiation of diagnoses other than sacroiliitis and should be applied in doubtful cases [6]. In children, the use of contrast medium is accepted by many for the detection of early subtle inflammatory changes in juvenile SpA [16]. MR image interpretation Sacroiliac joints. The SIJs are the most frequently involved site in SpA. The early lesions are tiny discontinuities of the subchondral bone plate along with subcortical BME, typically located at the inferior half of the joints and at the iliac surface, which is lined by fibrocartilage and less resistant to inflammatory damage. Active lesions are typically depicted on the STIR images. BME, one of the most important MRI features in SpA, is considered an active lesion, as well as capsulitis, enthesitis and synovitis. Structural changes are typically seen on the T1-weighted images and include fat deposition, erosions that sometimes result in a widened joint space with “string of pearls” appearance, sclerosis, “backfill” where the eroded joint reossifies [17] and finally ankylosis [6]. Spine. The spine is the second most frequent site of involvement in SpA. When vertebrae are involved, lesions generally present initially as erosions at the anterior aspect of the thoracolumbar vertebral bodies [18]. Later, the erosions are associated with sclerotic changes and syndesmophytes, which, in long-standing disease, tend to fuse. The distribution pattern of active and structural lesions includes corner inflammatory lesions, central inflammatory lesions and BME in the lateral and posterior spinal segments such as the pedicle, costotransverse and costovertebral joints is characteristic of SpA (Fig. 4) [15]. BME in these anatomical locations indicates active inflammation, whereas fatty infiltration or Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
5
Fig. 4. (aed) Active spinal SpA lesions in a 41-year-old male patient. Sagittal STIR MR images of the spine shows typical anterior and posterior corner inflammatory lesions in the thoracic spine as BME (arrows). Aseptic spondylodiscitis is seen as symmetric bone marrow edema of two adjacent vertebral bodies centred on the intervertebral disc space (arrowheads). BME of the head of rib is also present (long arrow). BME of the synchondrosis of the sternum is also depicted.
even ankylosis of the small joints indicate structural damage. Syndesmophytes, being thin strands of cortical bone, are generally best seen on radiographs, but, if prominent, they can at times be detected on MRI as well. Noninfectious spondylodiscitis is less common, and when present is characterized by BME and erosion at the vertebral end plates (Fig. 5). BME in the spinous process or at the ligament insertions on the spinous processes is also a feature of SpA [6]. Although spinal lesions typically develop later in the disease course than sacroiliitis, they may be the only active lesions in a symptomatic patient with longstanding disease, and therefore may determine prognosis and need for treatment, motivating routine whole-spine MRI in SpA monitoring at some centres [17]. Differential diagnosis Sacroiliitis. Diagnosing inflammatory sacroiliitis on MRI is not always straightforward and can be challenging. Several alternative diagnoses can be suggested based on a characteristic MRI appearance. Infectious sacroiliitis, osteitis condensans ilii, insufficiency fractures, osteoarthritis, diffuse idiopathic skeletal hyperostosis, anatomical variants and tumour may also result in BME of the SI joints [6,19]. Infection is most often unilateral and may demonstrate a joint effusion and periarticular soft tissue edema or collections. Osteitis condensans ilii generally presents as bilateral nearly symmetric iliac edema and later sclerosis, often triangular in shape and most often in women who have had one or more children, and is presumably related to mechanical strain during childbirth. The SI joint lines should remain smooth without erosions in this condition. Insufficiency fractures will present with linear edema and sclerosis in one or both sacral ala primarily paralleling the SI joints, rather than being centred within the SI joints themselves, which again should not show erosion. Osteoarthritis may have BME and irregularity of articular margins simulating sacroiliitis, but erosions are not a feature, and bony proliferation occurs at articular margins rather than centrally within the joint. Presence of a transitional lumbosacral junction or history of prior trauma may be associated with osteoarthritis [6,19]. Spinal inflammation. There is an overlap between degeneration and inflammation in the spine with regard to clinical symptoms and morphology on MRI. However, knowledge of certain morphological and clinical features facilitates the differentiation between the two entities. The changes seen in Please cite this article in press as: Jans L, et al., Novel imaging modalities in spondyloarthritis, Best Practice & Research Clinical Rheumatology (2014), http://dx.doi.org/10.1016/j.berh.2014.10.006
6
L. Jans et al. / Best Practice & Research Clinical Rheumatology xxx (2014) 1e17
Fig. 5. Active spinal inflammation in a 33-year-old male patient. Sagittal STIR MR image of the spine shows aseptic spondylodiscitis (arrows) as bone marrow edema of two adjacent vertebral bodies centred around the intervertebral disc space.
noninfectious spondylodiscitis are similar to active osteochondrosis. Analysis of the disc (usually not dehydrated in spondylitis), the location (degeneration typically at L4eS1, spondylodiscitis more often at levels higher in the thoracolumbar spine) and presence of other concomitant features such as corner inflammatory lesions may help differentiate these entities. Other differential diagnoses, such as infection, tumour, and stress reaction/fracture should be carefully excluded [6,19]. SpA without active inflammation. Both active and structural lesions of the SIJs and spine can be present in one patient at the same time. Moreover, in late-stage disease or under treatment, inflammatory lesions may turn into structural lesions such as fat deposition [20]. This underlines the importance of careful examination of the T1-weighted images for presence of structural lesions which can be easily missed on inspection of STIR images alone (Fig. 6). Definition of a ‘positive MRI’ for sacroiliitis in SpA It has been argued that the current ASAS definition of a ‘positive MRI’ of the SIJs and spine lacks specificity and may therefore result in false positive diagnosis of SpA. The definition includes BME as the only feature of active inflammation when it is present on at least two consecutive slices if only one lesion is seen, or, alternatively, at least two lesions on one slice should be present [9]. This definition has been fiercely debated among experts, as illustrated by the ESSR arthritis subcommittee consensus paper on imaging in SpA, stating that, in the absence of additional imaging features of SpA in the SIJs or spine, two tiny lesions
