Article Text
Abstract
Background A range of sacroiliac joint (SIJ) MRI protocols are used in clinical practice but not all were specifically designed for diagnostic ascertainment. This can be confusing and no standard diagnostic SIJ MRI protocol is currently accepted worldwide.
Objective To develop a standardised MRI image acquisition protocol (IAP) for diagnostic ascertainment of sacroiliitis.
Methods 13 radiologist members of Assessment of SpondyloArthritis International Society (ASAS) and the SpondyloArthritis Research and Treatment Network (SPARTAN) plus two rheumatologists participated in a consensus exercise. A draft IAP was circulated with background information and online examples. Feedback on all issues was tabulated and recirculated. The remaining points of contention were resolved and the revised IAP was presented to the entire ASAS membership.
Results A minimum four-sequence IAP is recommended for diagnostic ascertainment of sacroiliitis and its differential diagnoses meeting the following requirements. Three semicoronal sequences, parallel to the dorsal cortex of the S2 vertebral body, should include sequences sensitive for detection of (1) changes in fat signal and structural damage with T1-weighting; (2) active inflammation, being T2-weighted with fat suppression; (3) bone erosion optimally depicting the bone–cartilage interface of the articular surface and (4) a semiaxial sequence sensitive for detection of inflammation. The IAP was approved at the 2022 ASAS annual meeting with 91% of the membership in favour.
Conclusion A standardised IAP for SIJ MRI for diagnostic ascertainment of sacroiliitis is recommended and should be composed of at least four sequences that include imaging in two planes and optimally visualise inflammation, structural damage and the bone–cartilage interface.
- Magnetic Resonance Imaging
- Axial Spondyloarthritis
- Arthritis
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Introduction
For several decades, MRI has been used to investigate the early diagnosis of inflammatory sacroiliitis.1 2 However, worldwide agreement has been lacking regarding the essential components of a diagnostic MRI protocol for suspected arthropathy of the sacroiliac joint (SIJ). The Assessment of SpondyloArthritis International Society (ASAS) published a ‘Definition of active sacroiliitis on MRI for classification of axial spondyloarthritis (axSpA)’ in 2009 and updated the definition in 2016.3 This definition relies on two MRI sequences to make this determination—semicoronal T1 spin echo and short tau inversion recovery (STIR). Although the ASAS definition does not preclude more MRI sequences being performed since its publication, a single-plane, two-sequence approach to the MRI acquisition protocol has sometimes been inadvertently used for diagnostic purposes when a more comprehensive protocol may be preferable for routine clinical practice.
In 2015, the Arthritis Subcommittee of the European Society of Skeletal Radiology published its recommendations for an SIJ MRI ‘image acquisition protocol’ (IAP) for diagnostic purposes that required four MRI sequences.4 In 2019, a review of the topic was published by the British Society of Spondyloarthritis making seven recommendations for the ‘acquisition and interpretation of MRI of the spine and SIJ in the diagnosis of axSpA in the UK’.5 However, this publication did not specifically focus on the SIJ MRI acquisition protocol and recommendation #2 stated only that ‘T1-weighted and fat-suppressed, fluid-sensitive sequences are recommended’ with no details provided.
In 2020, an informal survey of 24 academic radiology departments (12 Europe, 12 North America) confirmed that 24/24 sites performed a minimum of 3 MRI sequences, with 19 performing 4–8 sequences because all centres considered the 2-sequence SIJ MRI protocol to be inadequate for diagnostic purposes. Our objective was to develop the minimum requirements for a standardised IAP for diagnostic MRI evaluation of the SIJ for axSpA that could be applied worldwide on all MRI platforms.
Methods
13 radiologist members of ASAS and the SpondyloArthritis Research and Treatment Network (SPARTAN), including two members of Young-ASAS specialising in paediatric radiology, along with one European and one North American rheumatologist with extensive MRI experience in SpA clinical practice and research, were invited to participate in a consensus exercise. A draft IAP was circulated to all participants along with background information and justification for the draft proposal. Examples of the proposed IAP performed on new, 10 and 22 years’ old MRI scanners were made available online for participants to review (https://www.carearthritis.com/service/mri-spa-imaging-acquisition-protocols/). The principles applied to the development of the protocol were as follows:
The proposed protocol should:
Adhere to basic principles of multiplanar cross-sectional imaging.
Be possible to perform on all MRI platforms in routine clinical use regardless of the age of the scanner.
Be practical to perform on all MRI platforms within a reasonable acquisition time.
Consider the complexity and variability of SIJ anatomy and adjacent ligamentous and vascular structures.
Be capable of detecting all common and most uncommon MRI findings that may be found in sacroiliitis and its differential diagnoses.6
Common in SpA—bone marrow oedema (BME), erosion, fat lesion, sclerosis, ankylosis, inflammation/fluid in the joint space
Less common in SpA—capsulitis, enthesitis, inflammation in an erosion cavity, backfill, bone budding.
Not usually a feature of SpA—osteophyte, extra-articular bone bridge, intra-articular gas, subchondral cyst.
Consider the inevitability of MRI artefacts and, where possible, allow crucial observations to be made even in the presence of significant artefact.
Consider future MRI developments being not overly prescriptive.
Be based on available evidence but not constrained by the lack of published evidence when expert opinion is strongly in favour of a specific approach.
Initially, the four-sequence IAP that was recommended for SIJ MRI as part of the Classification of Axial Spondyloarthritis Inception Cohort Study study was circulated for discussion. This protocol specifies which sequences should be acquired with advice regarding the acquisition parameters. Feedback on all issues was received by email, tabulated and recirculated. Participants were unanimously in favour of several components of the protocol including imaging in at least two planes and consistent orientation of the semicoronal sequences. It was also agreed that recommendations regarding lumbar spine or whole spine imaging were beyond the scope of this exercise. Other matters under discussion included whether to (a) include imaging of the whole pelvis, (b) recommend a different protocol for children and (c) allow elimination of the T1-weighted sequence in favour of T2-weighted Dixon imaging.
Two months later, a videoconference meeting took place and most remaining points of contention were resolved. Next the revised draft of the IAP was presented at the ASAS annual meeting to the entire membership on 14 January 2022, discussed and voted on.
Results
A four-sequence IAP, three semicoronal and one semiaxial, was recommended as a minimum standard for diagnostic ascertainment of sacroiliitis and its differential diagnoses (table 1).
The requirements for the four-sequence protocol are as follows:
(A) Consistent orientation of the sequences necessitates that they be performed orthogonal to a consistently present and clearly identifiable part of the sacrum. It is recommended that semicoronal sequences be performed parallel to the dorsal cortex of the S2 vertebral body (figure 1). This recommendation was adopted because it was unanimously agreed that consistent orientation of the semicoronal sequences is essential. SIJ anatomy is highly variable and the interpretation of the variable anatomy is facilitated by consistent orientation of the images. The dorsal cortex of the S2 vertebra was the selected reference line because it is (1) the most consistently available straight line on a sagittal image of the sacrum, (2) not affected by variation in lumbosacral transitional vertebrae, (3) clearly visible on all types of MRI sequence and (4) unaffected by SIJ arthropathy or lumbosacral spondylosis.
(B) Four sequences are required—three-semicoronal sequences and one-semiaxial sequence (figure 2) and should be composed of (1) a semicoronal sequence sensitive for the detection of fat signal changes due to structural damage in bone and bone marrow with T1-weighted imaging recommended. A ‘fat-bright’ sequence with low or absent water signal is considered essential to accurately detect fat lesions in bone marrow and fat metaplasia in an erosion cavity (also called ‘backfill’). Bright water signal would interfere with these observations, and therefore, the sequence must either have low water signal through T1-weighting and/or absent water signal achieved by deconvolution of signal by the Dixon method producing ‘fat-only’ images. (2) A semicoronal sequence sensitive for the detection of active inflammation, being T2-weighted with suppression of fat signal. It is essential that fat signal in bone marrow is markedly reduced or eliminated to allow accurate detection of the increased water signal that occurs when bone marrow is actively inflamed, otherwise known as BME. It is also essential that signal from erythropoietic marrow be reduced as much as possible through proper T2-weighting. Proton density (PD) and intermediate-weighted (IW) sequences are not suitable for detection of BME in the SIJ or spine (discussed further below). (3) A semicoronal sequence that is designed to optimally depict the bone-cartilage interface of the articular surface and to be sensitive for detection of bone erosion. Although all sequences may sometimes demonstrate articular surface erosion, visualisation of an erosion is affected by multiple factors that include its size and surrounding tissue reaction. This may include sclerosis (low signal on all pulse sequences), BME (bright on T2FS, low on T1), fat lesion (bright on T1, low on T2FS) plus the internal signal of the erosion, which may vary according to the degree of activity and/or tissue repair. As a consequence of all these variables, it was recommended that the sequence should have thin slices to reduce partial volume averaging. This will improve sensitivity for small erosion defects even if the thin slice sequence has slightly lower in-plane resolution compared with the standard 3–4 mm thick spin echo sequences. It should be T1-weighted with fat signal suppression to permit more consistent contrast between the bone surface and the erosion cavity/articular surface/joint space. (4) A semiaxial sequence, perpendicular to the semicoronal sequences, sensitive for detection of active inflammation/BME. At least one additional sequence in a second plane was considered an absolute requirement because the detection of BME is pivotal in early axSpA diagnosis. The identification of the size, shape and distribution of the BME lesion is important for distinguishing BME due to axSpA from BME due to biomechanical or degenerative causes. The availability of a second sequence in the semiaxial plane allows the observer to more confidently see the exact anatomical distribution of a lesion and also to exclude false positive findings on one T2-weighted sequence due to phase encoding artefacts that commonly mimic BME but are rarely replicated on a second sequence perpendicular to the first. Therefore, it is recommended that the minimum requirement should include a semiaxial sequence that is T2-weighted with fat suppression sensitive for BME detection.
The IAP was approved at the 2022 ASAS annual meeting by a vote of the entire membership with 91% in favour.
Discussion
13 radiologists from Europe and North America and two ASAS/SPARTAN rheumatologists participated in a consensus exercise regarding the development of a standardised IAP for MRI of the SIJ. A four-sequence protocol was recommended and approved by ASAS in 2022.
The first component of the protocol is a requirement that the orientation of the sequences should be orthogonal to the sacrum. The anatomy of the SIJ is highly variable with anatomical variants seen in 40%–80% of subjects.7 8 This creates challenges for image interpretation and so the articular surfaces of the SIJ need to be imaged in two planes that are perpendicular to the main orientation of the joints and perpendicular to each other. This is currently the case for MRI of all other joints and the SIJ should not be treated differently. Because of the variability of sacroiliac anatomy and the lumbosacral junction, the dorsal surface of the S2 vertebral body is the only consistent straight line available from which the MRI technologist can consistently plan the orientation of the sequences (figure 1). In addition, this part of the sacrum is not affected by SpA.
A range of lesions may be seen in the SIJ related to inflammatory and degenerative disorders. The complexity of the findings in difficult cases necessitates a comprehensive protocol that will be of diagnostic quality in nearly all cases including adults and children. Imaging in more than one plane is a basic principle of cross-sectional radiology because recognition of the patterns of anatomy and pathology is easier when more than one plane is available. For example, MRI positivity for sacroiliitis according to ASAS criteria decreases in healthy populations by 33%–56% when BME in the SIJ is assessed in two perpendicular planes instead of only the semicoronal plane.9
Sensitive detection of active inflammation is an essential part of the protocol. The required BME-sensitive sequence should be properly T2-weighted. Some prior publications have confirmed that T2-weighted images are superior to PD weighted or IW images for the detection of BME in the SIJ10 11 and this concurs with the authors’ experience. This is not surprising as sacral bone marrow is composed of a combination of fatty and erythropoietic marrow at most ages. When sequences are fat suppressed, the erythropoietic marrow may appear relatively bright on a dark background but this problem can be ameliorated by proper T2-weighting. The effect of T2-weighting is to reduce signal from bound water (such as in cartilage, muscle or erythropoietic marrow) but signal remains strong in free water (such as in cerebrospinal fluid or BME). Technically, this means the time to echo must be long enough—approximately 80+ms for spin echo sequences and 50+ms for STIR. The water component of T2-weighted Dixon imaging appears to be equally effective for BME detection compared with STIR or T2 with fat saturation.12 The key requirements of the recommended protocol are strong T2-weighting plus the suppression or elimination of bone marrow fat signal. All authors agreed there is sufficient evidence to confirm that contrast-enhanced sequences are not usually necessary in adults or children and should be reserved for unusual circumstances.13–17 Contrast enhancement would require additional cost and inconvenience with limited additional benefit. In addition, synovitis, that may be better seen with contrast enhancement, and contrast enhancement of inflammatory tissue in the joint space rarely occurs without associated BME in adults.17
In children, the clinical situation is slightly different. Interpretation of paediatric SIJ MRI is more difficult because of greater variation in the normal appearances at sites of growth and the differential diagnosis for pain in the SIJ region is different in children. Also, SIJ MRI scans are often supervised in children when a decision regarding contrast enhancement can be made with the aid of real-time expert interpretation. For these reasons, the group chose not to make a specific recommendation regarding a paediatric SIJ MRI protocol.
A T1-weighted spin echo sequence is considered essential for accurate depiction of anatomy, visualisation of certain specific lesions and for the diagnostic assessment of the SIJ for all patients and not just spondyloarthritis cases. T1-weighted spin echo sequences are ‘fat-sensitive’ and fat lesions and backfill in subchondral bone, which are important SpA-related lesions, are best seen on T1-weighted spin echo. The Dixon technique allows any sequence acquisition to be broken down into separate fat-only and water-only images. For example, using the Dixon method, a T2-weighted spin echo sequence can be reconstructed to produce water-only images that appear identical to a T2-weighted sequence with fat saturation, plus fat-only images in which bone marrow fat is bright and the water signal is removed. While there is some evidence that T2-weighted Dixon sequences may be able to provide accurate depiction of structural damage changes in SpA, the literature is limited and contradictory. Özgen showed that a T2-weighted multipoint Dixon sequence can demonstrate the BME, sclerosis and fat lesions of sacroiliitis with better contrast-to-noise than conventional sequences. However, the publication did not assess detection of erosion or diagnostic accuracy.18 Athira et al suggest that T2 Dixon sequences are superior or comparable to conventional MR sequences, whereas Chien et al concluded that the presence of subchondral oedema in active sacroiliitis decreased the diagnostic accuracy of SIJ erosion detection on T2W Dixon MRI.19 20 All of these studies were quite limited by their inclusion of only a small number of subjects and only addressing the MRI findings of axSpA. There is no literature available at this time that compares the accuracy of T2-Dixon imaging to conventional sequences for a range of SIJ conditions in broader populations of patients with low back pain. Consequently, an alternative to including a T1-weighted spin echo cannot be recommended at this time.
In the early years, SIJ MRI focused more on the detection of active inflammation that could not be detected by other means. However, BME frequently occurs in other conditions, especially degeneration of the SIJ, and detection of subtle erosion is just as important as BME detection for early diagnosis.21 It has been shown that structural damage changes can develop early in sacroiliitis and that they occur as frequently as active inflammatory lesions at the time of diagnosis.22 In addition, there has been a tendency towards overreliance on the importance of BME for diagnosis by some local radiologists compared with central MRI readers.22 Whereas in fact, the findings with the highest diagnostic value are actually the structural damage changes, in isolation or in combination with BME23 and it is often only the coexistence of subtle erosion with BME that facilitates discrimination between sacroiliitis and its differential diagnoses. Erosion detection has historically relied on the T1-weighted spin echo sequence but erosions in early disease may be small and are not easy to detect on 3–4 mm thick slices. Furthermore, the subchondral bone plate is extremely thin and is often poorly defined on thick slices so that ‘loss of subchondral cortex’ may be simulated on thick slices in a joint with such frequent anatomical variation, and the majority of children demonstrate absence or blurring of the subchondral cortex on T1-weighted spin echo MRI.24
Using CT as the gold standard, the reported sensitivity and specificity of T1-weighted spin echo in erosion detection are 61%–79% and 93%–95%, respectively.25 26 In recent years, numerous publications have confirmed the superiority of thin slice sequences for the detection of SIJ erosion compared with T1-weighted spin echo with sensitivity in the range of 82%–96% and specificity 93%–97%.25–30 In addition, reader reliability for erosion detection significantly improves using a thin slice 3D sequence (kappa 0.71) compared with standard thickness 2D T1-weighted spin echo (kappa 0.56).26 It may not matter which 3D gradient echo sequence is employed and the key factors that lead to this superiority include (a) thin slices with good in-plane resolution resulting in a small voxel size and less partial volume averaging that makes small erosions easier to see and (b) gradient echo imaging is superior to spin echo for depicting defects in bone. On gradient echo, healthy bone appears darker due to signal loss related to the presence of calcium in the bone which then makes an erosion cavity appear brighter by comparison because the calcified bone has been destroyed by the erosion (figure 3). This has been known for decades and thicker-slice gradient echo sequences have been used to image the SIJ for over 25 years.31 Multiple thin slice 3D sequences based on a gradient echo technique have been shown to be superior to T1-weighted spin echo, even if the thicker spin echo sequence has superior in-plane resolution. These include (in alphabetical order): balanced steady-state free precession, Liver Acquisition with Volume Acceleration, sometimes called Black Bone, susceptibility weighted image, ultrashort echo time, volumetric interpolated breath-hold examination, ZTE (zero echo time) to mention but a few,25–30 with some examples provided in figure 3. Very little data are available to directly compare these sequences with each other and it is also unclear for several of these sequences if erosion detection is better with or without fat suppression although the majority of publications recommend that the 3D gradient echo sequence be performed with T1-weighting and fat suppression. Also, more recently, it has been shown that a ‘BoneMRI’ reconstruction algorithm can create synthetic CT-like images from a 3D gradient echo MRI sequence that appear similar to CT images.32 Regardless of exactly which sequence is used, radiologists should recognise the benefit of acquiring a dedicated erosion-sensitive sequence, rather than relying only on STIR and T1-weighted sequences for interpretation. They should include this sequence in their standard SIJ MRI protocol and if only a 2D sequence is available, then a T1-weighted sequence with fat suppression is recommended for erosion detection. Rheumatologists should also encourage this practice by requesting the inclusion of an erosion-sensitive sequence when SIJ MRI is being performed on their patients.
It is suggested that the semiaxial sequence may be performed with a larger field of view and more slices so as to include the pubic symphysis, hip joints and most of the pelvic entheses thereby including one sequence in the protocol which can assess overall pelvic morphology and sites of potential inflammation in the pelvis outside the SIJ.33 If only one sequence is performed in the semi-axial plane, a T2-weighted spin echo Dixon sequence with all four components reconstructed (in-phase, out-of-phase, water-only and fat-only) may be particularly suitable as it may allow adequate evaluation of most components of sacroiliitis and sacroiliac anatomy.
It should be noted that this protocol has not been designed for screening purposes. It is intended as a diagnostic protocol and not only for axSpA but also for the differential diagnoses of sacroiliitis such as normal variation, joint degeneration, osteitis condensans ilii and other stress/strain reactions and would also detect septic arthritis and focal bone lesions. The recommendations do not include any discussion regarding whether all or part of the spine should or should not be scanned which depends on the population and local factors including cost, availability and the referring physician’s plans for management if the MRI is positive or negative for axSpA. This protocol is designed for adults and all clinical circumstances in which the SIJ are being scanned for possible axSpA regardless of who the requesting healthcare provider may be. Although not specifically designed for use in the paediatric population, the principles and recommended sequences should also be applicable to SIJ MRI in children. However, a comprehensive paediatric protocol needs to be developed that addresses issues which may be specific to that population.
Conclusion
A standardised IAP for MRI of the SIJ for diagnostic evaluation of sacroiliitis due to axSpA is recommended and should be composed of at least four sequences that incorporate imaging of the joints in two planes orthogonal to the sacrum and include an inflammation-sensitive, a fat-sensitive and an erosion-sensitive sequence that will optimally visualise active inflammation, structural damage lesions and the bone-cartilage interface. The protocol can be applied to any MRI scanner and radiologists should follow the principles that underlie the consensus recommendation in the design of their local SIJ MRI protocol.
Ethics statements
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Acknowledgments
The MRI examples illustrated in figures 1–3 are all provided, with permission, by the North American cohort of the Classification of Axial Spondyloarthritis Inception Cohort Study (CLASSIC) study. This work has been presented in abstract form at two international meetings:EULAR 2022 Congress, Copenhagen, Denmark, 1 June 2022–4 June 2022. Development of international consensus on a standardised image acquisition protocol for diagnostic evaluation of the sacroiliac joints by MRI–an ASAS-SPARTAN collaboration (abstract). R Lambert, X Baraliakos, S Bernard, J Carrino, T Diekhoff, I Eshed et al. Ann Rheum Dis 2022, 81 suppl 1:802—Abstract #3365American College of Rheumatology—ACR Convergence 2022, Philadelphia, Pennsylvania, USA, November 10 November 2022–14 November 2022. Development of International Consensus on a Standardised Image Acquisition Protocol for Diagnostic Evaluation of the Sacroiliac Joints by MRI—an ASAS-SPARTAN Collaboration [abstract]. Lambert R, Baraliakos X, Bernard S, Carrino J, Diekhoff T, Eshed I, Hermann K, Herregods N, Jaremko J, Jans L, Jurik A, O'Neill J, Reijnierse M, Tuite M, Maksymowych W. Arthritis Rheumatol. 2022; 74 (suppl 9). Abstract #1258
References
Footnotes
Handling editor Josef S Smolen
Contributors All authors meet all four ICMJE criteria for authorship, and all who meet the four criteria are identified as authors. There are no other contributors to the work. No one who fulfils the criteria has been excluded as an author. RGWL: submitting and corresponding author. Responsible for planning, conducting and reporting the work. Guarantor. XB: coauthor involved in conducting and reporting the work. SAB: coauthor involved in conducting and reporting the work. JAC: coauthor involved in conducting and reporting the work TD: coauthor involved in conducting and reporting the work. IE: coauthor involved in conducting and reporting the work. KGH: coauthor involved in conducting and reporting the work. NH: coauthor involved in conducting and reporting the work. JJ: coauthor involved in conducting and reporting the work. LJ: coauthor involved in conducting and reporting the work. AGJ: coauthor involved in conducting and reporting the work. JMDO’N: coauthor involved in conducting and reporting the work. MR: coauthor involved in conducting and reporting the work. MJT: coauthor involved in conducting and reporting the work. WPM: coauthor involved in conducting and reporting the work.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests RGWL: consulting fees from CARE Arthritis and Image Analysis Group. XB: contract with Novartis; Consulting fees from Amgen, Bristol-Myers Squibb, Chugai, Eli Lilly, Galapagos, Janssen, Merck Sharp & Dohme, Novartis, Pfizer, Roche, Sandoz, Sanofi, and UCB; Payment or honoraria from Amgen, Bristol-Myers Squibb, Chugai, Eli Lilly, Galapagos, Janssen, Merck Sharp & Dohme, Novartis, Pfizer, Roche, Sandoz, Sanofi, and UCB; Meeting support from Eli Lilly, Janssen, Novartis, Pfizer and UCB; Participation on a Data Safety Monitoring Board or Advisory Board: Amgen, Bristol-Myers Squibb, Eli Lilly, Galapagos, Janssen, Merck Sharp & Dohme, Novartis, Pfizer, Roche, Sandoz, Sanofi and UCB; Leadership role: Editorial Board Member of Annals of Rheumatic Diseases, ASAS President, EULAR President Elect. SAB: Royalties from Elsevier. JAC: Consulting fees from AstraZeneca and Covera Health; Participation on a Data Safety Monitoring Board or Advisory Board: Carestream, Image Analysis Group, Image Biopsy Lab; Leadership role: RSNA, ACR, IAOAI. TD: Grants or contracts from Berlin Institute of Health (BIH); Payment or honoraria from Berlinflame, Canon Medical Systems, Janssen, MSD, Novartis, UCB. IE: Payment or honoraria from Lilly, Novartis. KGH: Payment or honoraria from MSD, AbbVie Novartis; Cofounder of BerlinFlame. NH: None declared. JJ: Stock in Exo. LJ: None declared. AGJ: None declared. JMDO'N:– None declared. MR: ISS Seed Grant; Consultant for ASAS. MJT: Consulting fees from GE HealthCare; Meeting support from International Skeletal Society; Leadership role—President-elect International Skeletal Society. WPM: Grants or contracts from Abbvie, BMS, Eli-Lilly, Pfizer, UCB; Consulting fees from Abbvie, Celgene, BMS, Eli-Lilly, Galapagos, Pfizer, UCB; Payment or honoraria from Abbvie, Janssen, Pfizer, Novartis; Leadership role—SPARTAN Board of Directors; Chief Medical Officer, CARE Arthritis.
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