Article Text
Abstract
Background: The Computed Tomography Syndesmophyte Score (CTSS) was developed as a reliable and sensitive tool to assess syndesmophytes in low-dose CT images of the entire spine in patients with axial spondyloarthritis (axSpA). The original paper provided sparce examples of the CTSS grades.
Objectives: Provide an atlas tailored to assist readers in understanding and employing the CTSS method.
Methods: In this paper, illustrations of the different grades and views of the CTSS are presented. CTSS is used to measure bone formation in the spine of patients with axial spondyloarthritis (axSpA), in the form of syndesmophytes. In both the sagittal and coronal planes, syndesmophytes can be graded from 0 to 3 over 23 vertebral units starting at C2 and ending at S1. The CTSS ranges from 0 (absence of axSpA-related syndesmophytes) to 552 (total ankylosis of the spine).
Results: The current atlas contains low-dose CT images of the spine without lesions (for reference) and all grades of syndesmophytes in different planes used in the CTSS. Examples are arranged per spinal segment (cervical, thoracic and lumbar).
Conclusions: These images can be used to assist any reader in the assessment of syndesmophytes on (low-dose) CT in patients with axSpA.
- Spondyloarthritis
- Spondylitis, Ankylosing
- Outcome Assessment, Health Care
Data availability statement
Data sharing not applicable as no datasets generated and/or analysed for this study. Not applicable.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
The CT Syndesmophyte Score (CTSS) was developed in 2017 as a reliable and sensitive tool to cross-sectionally (and longitudinally) assess the presence (and progression) of syndesmophytes in patients with axial spondyloarthritis (axSpA).
The original paper provided limited illustrative examples of the CTSS grades.
WHAT THIS STUDY ADDS
An atlas specifically tailored to assist readers in understanding and employing the CTSS method.
This atlas contains a large range of meticulously curated images, from normal to damaged spine (syndesmophytes) across different spinal segments and planes.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE, OR POLICY
These images serve as practical references to aid readers in effectively assessing syndesmophytes using (low-dose) CT scans in patients with axSpA.
This atlas sets the basis for precise and reliable CTSS assessment, thereby enhancing the external reproducibility and quality of research when employing this score.
Introduction
Axial spondyloarthritis (axSpA) is a chronic inflammatory rheumatic disease of the axial skeleton that leads to new bone formation of the spine in the form of syndesmophytes.1 These ectopic bone formation lesions embody the irreversible consequences of the disease and are associated with a significant burden. As such, syndesmophyte growth is associated with impairment of spinal mobility and functional disability.2 3
As an improvement over conventional radiography which has been the standard for imaging syndesmophytes in axSpA for many decades,4 5 low-dose CT facilitates the comprehensive assessment of syndesmophytes in the entire spine using acceptable levels of radiation exposure. A major advantage of this method is the assessment of the thoracic spine, which is challenging to evaluate on radiographs due to the superposition of structures, particularly the ribs.6
In 2017, low-dose CT scans from patients with axSpA from the Sensitive Imaging in Axial Spondyloartritis (SIAS) cohort were used to develop the CT Syndesmophyte Score (CTSS), which assesses syndesmophytes from C2 to S1.7 8 CTSS has shown to be a reliable and sensitive tool to cross-sectionally (and longitudinally) assess the presence (and progression) of syndesmophytes in patients with axSpA.7 8
Developments in CT detector technology,9 special filters10 11 and modern (AI-based) reconstructions algorithms,12 promise further reduction of ionising radiation for CT scans. Moreover, with a worldwide increased accessibility of low-dose CT, used in other diseases, namely for cancer screening,13 we may anticipate an upsurge of its usage in patients with axSpA, especially for research purposes.
Assessment of the entire spine using the CTSS method may pose challenges for inexperienced readers. The original paper by de Bruin et al described the score, but only limited examples were presented.7 Clear guidance on how to use the CTSS throughout the whole spine is crucial to guarantee its external reproducibility.
This paper discusses basic radiological concepts with relevance for any reader. An atlas is presented for the CTSS, with representative images for the normal spine along with reference images of different syndesmophyte grades. Examples are shown on different vertebral unit (VU) levels and in both sagittal and coronal planes. Any reader can use these reference images as examples to assist the assessment of syndesmophytes on (low-dose) CT in patients diagnosed with axSpA.
Scoring assessment
A schematic overview of the CTSS is shown in table 1 (adapted from de Koning et al).8 In the CTSS scoring method, 23 VUs are assessed starting with the lower half of C2 and ending at the upper half of S1. A VU consists of the lower half of a vertebra, the intervertebral disc space (IDS) and the upper half of the next vertebra (eg, VU1 encompasses the lower half of C2 and the upper half of C3).
Each VU is divided into quadrants and each image is scored in the sagittal and coronal planes (figure 1—adapted from de Bruin et al).7 The sagittal and coronal planes complement each other and must both be assessed from C2 to S1. By scrolling through coronal images, the reader assesses the left and right quadrants of the VU. In the sagittal plane, the reader assesses the anterior and posterior quadrants. These independent assessments should be performed in a standardised way. Ideally, a VU is assessed in both planes before moving to the next VU, evaluating the VUs from top to bottom of the spine.
Per VU, eight quadrants are assessed for the presence of syndesmophytes using a 0–3 grading score: ‘0’ if syndesmophytes are absent (figures 2 and 3), ‘1’ when syndesmophyte height is <50% of the IDS (figures 4 and 5), ‘2’ when syndesmophyte height reaches ≥50% of the IDS (figures 6 and 7) and ‘3’ if the syndesmophyte is bridging the IDS (figures 8 and 9). Of note, a score of ‘3’ is, by definition, assigned to both quadrants on opposite sides of the IDS, for example, upper and lower left quadrants (coronal view) or upper and lower anterior quadrants (sagittal view). The total range of the CTSS, including combined scores of coronal and sagittal quadrants, goes from 0 (absence of SpA-related syndesmophytes) to 552 (total ankylosis of the spine).7 Facet joint abnormalities are not included in the CTSS.
The judgement on whether abnormalities are present should be guided by the normal shape of each vertebra (representative examples are given in figures 2 and 3). Interpatient and intervertebra (within the same patient) normal anatomic variations of the vertebral shape may occur. Typical examples comprise the U-shaped vertebrae in the coronal plane of the cervical spine, where the normal sloped vertebral corners cannot be mistaken as syndesmophytes (images 1a to 1c of figure 2 and image 1c of figure 4). Moreover, in the sagittal plane of the lumbar spine, the endplate may exhibit a concave/convex shape, with the normal vertebral corners extending beyond the middle part of the vertebra. Once more, normal vertebral corners should not be confused with syndesmophytes (examples are marked with asterisks in figure 10).
Imaging acquisition
The examples used in the present atlas were obtained from coded low-dose CT images of patients with axSpA included in Leiden as part of the SPondyloArthritis Caught Early study and SIAS study.7 14 A few images were also obtained from patients with axSpA included in the AXspa International OutcoMe Assessment study, an ongoing study (in progress unpublished data). CTs were acquired in different machines from different vendors (online supplemental table 1). Helical CT scans were performed with the patient in supine position and arms up. The entire spine was assessed from the superior endplate of C2 to the inferior endplate of S5 using predefined settings (online supplemental table 1). Out of primary raw data or volume reconstructions, coronal and sagittal 1.5–3 mm images were generated with a sharp bone kernel by using iterative reconstructions (online supplemental table 2). The estimated radiation exposure for the total spine scan including the sacroiliac joints varied depending on the patients' body size and the scanner system but was invariably ≤4 mSv with an overall (estimated) effective dose of 2.1±1.2 mSv—further details given in the online supplemental table 1.
Supplemental material
Notifications and challenges
Each CT scan is a 3D reconstruction composed of 2D images. As only one slice of the scan can be viewed at a time, the identification of abnormalities requires repetitive scrolling through multiple slices. The reader should focus on one VU at a time, systematically assessing each VU individually preferably from top to bottom starting cervical (C2) and working their way down to S1. If a transitional vertebra (sixth lumbar vertebra) is present, any abnormalities in that vertebra can be noted separately as a free text comment.
The CTSS was developed to be used in patients with an established diagnosis of axSpA. Therefore, the diagnosis should be known before starting to score. This method focuses on syndesmophytes, and while applying the CTSS, some notifications and typical features are worth considering:
The syndesmophyte consists of a bony spur, in principle, originating from the vertebral corner (figures 4–11).
Syndesmophytes are classically vertically directed bony outgrowth lesions. These lesions contrast with horizontally directed extensions from the endplates, osteophytes/spondylophytes, which are seen in spondylosis and degenerative disc disease (DDD).15 A growth angle of ≥45° measured from the endplate is currently regarded as a surrogate to distinguish syndesmophytes from osteophytes.16 An easy approach is drawing a straight line parallel to and extending from the vertebral endplate; the syndesmophyte typically crosses this line upright to the opposite vertebra (figure 12). In the cervical spine, due to the concave or convex anatomy of the vertebral endplate (images 1a to 1c of figure 2), some adaptations of this method are necessary. First, the reader should compare one quadrant to the others within the same VU (eg, Q1 VU2 vs Q2 VU2, Q3 VU2 and Q4 VU2), followed by the comparison to a corresponding quadrant from another VU (eg, Q1 VU2 vs Q1 VU3), while considering the typical shape of the (cervical) vertebra and the natural variation among individual patients.
To be considered of grade 1 or higher, the syndesmophyte should cross the drawn straight line extending from the vertebral endplate (figure 4; third image can be scored as grade 1).
The IDS can be preserved in axSpA. However, IDS changes, such as IDS height loss or fissures, can also be observed as occurring in DDD, particularly with ageing.15 In the presence of such IDS alterations, the reader needs to be cautious with assessing syndesmophytes. In fact, exuberant bone formation due to degenerative changes might mimic syndesmophyte growth (figure 13).15 Also, in DDD, osteophytes can be difficult to differentiate from axSpA new bone formation, even if applying the ≥45° angle method explained in point 2 (figure 13). VUs with degenerative spondylophytes should be assigned a zero in the syndesmophyte grading. Occasionally, readers may find lesions compatible with syndesmophytes due to axSpA in vertebrae with reduced IDS height. In those circumstances, grades 1–3 should be attributed to syndesmophytes using the height of the IDS as it stands. Clinical information (eg, age, disease duration), if available, can assist in interpreting images avoiding misclassification of degeneration as axSpA.
Differentiation between primary ossified ligaments and bony outgrowths of the vertebral endplate might be challenging.15 However, the anatomy references, namely the site of attachment of the ligaments, can be of help (figure 14). Lesions clearly corresponding to ossified ligaments (eg, without a clear spur coming from the vertebral corner) must be excluded from the scoring according to the CTSS.
Readers should be aware of differential lesions since these lesions cannot be scored as part of the CTSS, a method specifically developed for axSpA-related syndesmophytes. Some examples include osteophytes, parasyndesmophytes or non-marginal syndesmophytes (originating from the lateral part of the vertebra), spondylosis or diffuse idiopathic skeletal hyperostosis (figures 12 and 13). Providing extensive information about these differential lesions is beyond the scope of this atlas. Main differences described for other imaging modalities, for example, conventional radiographs, also apply here and were previously reported.15
Subsequently, we describe other particularities and challenges readers may face when using the CTSS. One quadrant can display several grades in different slices. In figure 10, the upper corner syndesmophyte (white arrow) should be judged as grade 1 on the first two slices (A and B) but grade 2 on the following slice (C). The reader should report the highest grade; in the example, this is grade 2.
As mentioned above, syndesmophytes are assessed in both coronal and sagittal planes. By doing this, it is possible to assess a syndesmophyte in one plane while not visible, and therefore not assessed, in the other. Moreover, it is plausible that the grade given in a certain VU differs in sagittal and coronal planes (figure 11).
Depending on the CT manufacturer, radiation dose and reconstruction algorithms, some artefacts or poor imaging quality may be present.17–19 In these circumstances, the reader should avoid scoring a syndesmophyte if questionable or not clearly seen. figure 15 shows a paradigmatic example in which VUs can be difficult to assess because of streak artefacts.17 18 Modern algorithms with iterative AI-based reconstructions can reduce these artefacts.13 19 20 To accurately assess the CTSS, it is essential to guarantee equal imaging quality over the whole spine while ensuring low radiation exposure.20 Therefore, all measures for improving the image quality (eg, modern reconstruction techniques) and reducing the radiation exposure (eg, special filters) should be applied. The presence of artefacts or other concerns in using the CTSS scoring can be added as comment to the scoring sheet.
In summary, this atlas provides comprehensive guidance on how to use the CTSS when assessing syndesmophytes on (low-dose) CTs in patients with the diagnosis of axSpA. The reference images were carefully selected aiming at assisting the decisions of any reader (irrespective of experience) when scoring syndesmophytes according to the CTSS method.
Data availability statement
Data sharing not applicable as no datasets generated and/or analysed for this study. Not applicable.
Ethics statements
Patient consent for publication
Ethics approval
The SIAS study was approved by ethics committee at each centre (Leiden Medisch Ethische Toetsings Commissie - METC number: P10.021 and Herne Ethikkommission der Ruhr Universität Bochum number: 4366-12). The SPACE study protocol was approved by the medical ethical committee of the Leiden University Medical Center (reference number P08.105). The AXIOMA was approved by ethics committee at Zuyderland Medical Center (METCZ20200213) and by ethics committee of Hacettepe University (number 2021/27-31 [KA-20018]). All participants provided written informed consent before enrolment, and coded data were used. Participants gave informed consent to participate in the study before taking part.
Acknowledgments
We thank the AXIOMA center of Ankara (Hacettepe University Hospital, Ankara, Turkey) and their local PI (Levent Kiliç) for the permission to use images from this center in the atlas. We acknowledge Jan Heemskerk, clinical physicist at the department of Radiology and Nuclear Medicine of Leiden University Medical Center (Leiden, the Netherlands) for providing information on technical aspects.
References
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
Contributors Study conception and design: MLM, MdH, SR, DvdH and FAvG. Selection of images: MLM and MdH. Authentication of radiology concepts and imaging quality: MR, TD and KGH. Drafting the manuscript: MLM and MdH. All authors critically reviewed the manuscript for important intellectual contribution and approved the final version. Guarantors: MLM and MdH.
Funding MLM is supported by the Fundação para a Ciência e Tecnologia (FCT) grant SFRH/BD/143744/2019.
Competing interests MLM — none. SR: Research Grants — AbbVie, Galapagos, MSD, Novartis, Pfizer, UCB. Consultancy — AbbVie, Eli Lilly, Janssen, MSD, Novartis, Pfizer, Sanofi, UCB. DvdH: Consultancy — AbbVie, ArgenX, Bayer, BMS, Cyxone, Eisai, Galapagos, Gilead, Glaxo-Smith-Kline, Janssen, Lilly, Novartis, Pfizer, Takeda, UCB Pharma. Director of Imaging Rheumatology bv. MR: Consultancy — ASAS-group. TD: Grants/support — Canon Medical Systems and ASAS-group. Speaker’s bureau — Canon Medical Systems, Novartis, MSD, BioCad, UCB and Roche. Consultancy — Lilly. K-GAH: lecture honoraria — AbbVie, Lilly, MSD, Novartis, and Pfizer. Consultancy — AbbVie. Co-founder of BerlinFlame GmbH. FAvG: Research Grants — Novartis. Consultancy — MSD, AbbVie, Novartis and BMS. MdH: Consultancy and support for attending conferences — UCB.
Provenance and peer review Not commissioned; externally peer reviewed.
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