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Systematic Review/Meta-Analysis|Articles in Press

A critical appraisal of clinical practice guidelines for diagnostic imaging in the spinal cord injury

  • Author Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Bin Guan
    Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China
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  • Author Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Guoyu Li
    Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China
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  • Author Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Ruiyuan Zheng
    Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China
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  • Yuxuan Fan
    Affiliations
    Department of Orthopaedics, Tianjin Medical University General Hospital, International Science and Technology Cooperation Base of Spinal Cord Injury, Tianjin Key Laboratory of Spine and Spinal Cord, Tianjin, 300052, P.R. China
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  • Liang Yao
    Affiliations
    Department of Health Research Methods, Evidence, and Impact, McMaster University, Canada
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  • Author Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Lingxiao Chen
    Correspondence
    Corresponding author. Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China. Faculty of Medicine and Health, The Back Pain Research Team, Sydney Musculoskeletal Health, The Kolling Institute, University of Sydney, Sydney, Australia. Tel.: (61) 0466965326; fax: (86) 053182169114.
    Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China

    Faculty of Medicine and Health, The Back Pain Research Team, Sydney Musculoskeletal Health, The Kolling Institute, University of Sydney, Sydney, Australia
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  • Author Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Shiqing Feng
    Correspondence
    Corresponding author. Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China. Tel.: (86) 13920286292; fax: (86) 0531-82169114.
    Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China

    Department of Orthopaedics, Tianjin Medical University General Hospital, International Science and Technology Cooperation Base of Spinal Cord Injury, Tianjin Key Laboratory of Spine and Spinal Cord, Tianjin, 300052, P.R. China
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  • Author Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Hengxing Zhou
    Correspondence
    Corresponding author. Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China. Tel.: (86) 13612051681; fax: (86) 0531-82169114.
    Footnotes
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
    Affiliations
    Department of Orthopaedics, Qilu Hospital of Shandong University, Shandong University Centre for Orthopaedics, Advanced Medical Research Institute, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, 250012, P.R. China

    Department of Orthopaedics, Tianjin Medical University General Hospital, International Science and Technology Cooperation Base of Spinal Cord Injury, Tianjin Key Laboratory of Spine and Spinal Cord, Tianjin, 300052, P.R. China
    Search for articles by this author
  • Author Footnotes
    ‡ Bin Guan, Guoyu Li, and Ruiyuan Zheng contributed equally to this work.
    † Hengxing Zhou, Shiqing Feng, and Lingxiao Chen were designated as co-corresponding authors.
Open AccessPublished:March 17, 2023DOI:https://doi.org/10.1016/j.spinee.2023.03.003

      Abstract

      BACKGROUND CONTEXT

      Spinal cord injury (SCI) is a serious health problem which carries a heavy economic burden. Imaging technologies play an important role in the diagnosis of SCI. Although several organizations have developed guidelines for diagnostic imaging of SCI, their quality has not yet been systematically assessed.

      PURPOSE

      We aim to conduct a systematic review to appraise SCI guidelines and summarize their recommendations for diagnostic imaging of SCI.

      STUDY DESIGN

      Systematic review.

      METHODS

      We searched Embase, Medline, Web of Science, Cochrane, some guideline-specific databases (eg, Scottish Intercollegiate Guidelines Network) and Google Scholar from January 2000 to January 2022. We included guidelines developed by nationally recognized organizations. If multiple versions could be obtained, we included the latest one. We appraised included guidelines using the Appraisal of Guidelines for Research and Evaluation, 2nd edition instrument which contains six domains (eg, scope and purpose). We also extracted recommendations and assessed their supporting evidence using levels of evidence (LOE). The evidence was categorized as A (the best quality), B, C, and D (the worst quality).

      RESULTS

      Seven guidelines (2008–2020) were included. They all received the lowest scores in the domain of applicability. All guidelines (7/7, 100%) recommended magnetic resonance imaging (MRI) in patients with SCI or SCI without radiographic abnormality (SCIWORA). A total of 12 recommendations involving patient age (eg, adult and child patients), timing of MRI (eg, as soon as possible and in the acute period), symptoms indicated for MRI (eg, a stiff spine and midline tenderness, suspected disc and posterior ligamentous complex injury, and neurological deficit), and types of MRI (eg, T2-weighted imaging and diffusion tensor imaging) were extracted. Among them, the LOE was C in nine (75%) recommendations and D in three (25%) recommendations.

      CONCLUSIONS

      Seven guidelines were included in the present systematic review, and all of them showed the worst applicability scores in the Appraisal of Guidelines for Research and Evaluation, 2nd edition instrument. They all weakly recommended MRI for patients with suspected SCI or SCIWORA based on a low LOE.

      Keywords

      Introduction

      In recent years, spinal cord injury (SCI), which carries a heavy economic burden, has become increasingly common [
      • Ahuja CS
      • Wilson JR
      • Nori S
      • Kotter MRN
      • Druschel C
      • Curt A
      • et al.
      Traumatic spinal cord injury.
      ,
      SCI facts and figures.
      ]. According to the Global Burden of Disease Study, there were 20.64 million (95% uncertainty interval: 18.93–23.61 million) prevalent cases of SCI recorded globally in 2019 [
      Global Burden of Disease Collaborative Network
      Global burden of disease study 2019 (GBD 2019) results.
      ]. According to the National Spinal Cord Injury Statistical Center, the average yearly expenses for patients with SCI ranged from $0.04 million to $1.08 million in the United States [
      SCI facts and figures.
      ].
      Diagnostic imaging plays important roles in the evaluation of patients with suspected SCI [
      • Shabani S
      • Meyer BP
      • Budde MD
      • Wang MC
      Diagnostic imaging in spinal cord injury.
      ]. Computed tomography (CT) is regarded as an initial imaging examination after spinal trauma for its clear radiographic image of the spinal column [
      • Eli I
      • Lerner DP
      • Ghogawala Z.
      Acute traumatic spinal cord injury.
      ]. Magnetic resonance imaging (MRI) is effective in detecting slight changes in soft tissues, supporting a better diagnosis of SCI and proper management [
      • Sharif S
      • Jazaib Ali MY
      Outcome prediction in spinal cord injury: myth or reality.
      ]. This makes it crucial in the evaluation of damage to neurological structures [
      • Kumar Y
      • Hayashi D.
      Role of magnetic resonance imaging in acute spinal trauma: a pictorial review.
      ].
      High-quality guidelines can promote efficient practices for health conditions [
      • Anderson DB
      • Luca K
      • Jensen RK
      • Eyles JP
      • Van Gelder JM
      • Friedly JL
      • et al.
      A critical appraisal of clinical practice guidelines for the treatment of lumbar spinal stenosis.
      ]. However, without information regarding the quality of existing guidelines, it is difficult for clinicians to choose high-quality guidelines [
      • Montero-Odasso MM
      • Kamkar N
      • Pieruccini-Faria F
      • Osman A
      • Sarquis-Adamson Y
      • Close J
      • et al.
      Evaluation of clinical practice guidelines on fall prevention and management for older adults: a systematic review.
      ]. Furthermore, a critical appraisal of relevant guidelines greatly benefits future work in this field, as more evidence is added by researchers [
      • Lee JL
      • Matthias MS
      • Menachemi N
      • Frankel RM
      • Weiner M.
      A critical appraisal of guidelines for electronic communication between patients and clinicians: the need to modernize current recommendations.
      ]. Although clinical practice guidelines for the diagnostic imaging of SCI have been published by some authoritative organizations, the consistency of the recommendations and the overall quality of the guidelines remain unclear. In 2021, Liang et al. [
      • Liang N
      • Wu S
      • Roberts S
      • Makaram N
      • Ngwayi JRM
      • Porter DE.
      Critical appraisal of paralyzed veterans of America Guidelines in spinal cord injury: an International Collaborative Study Using the Appraisal of Guidelines for Research and Evaluation II Instrument (AGREE II).
      ] appraised the guidelines for SCI published in the Paralyzed Veterans of America; however, not all available guidelines were included or focused on diagnostic imaging.
      Therefore, the purpose of this study is to critically appraise existing guidelines on diagnostic imaging of SCI, and to present recommendations based on an assessment of the supporting evidence.

      Methods

      Study design

      According to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [
      • Moher D
      • Liberati A
      • Tetzlaff J
      • Altman DG.
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      ], we conducted a systematic review and registered it on PROSPERO (CRD42022350091). The systematic review team consisted of two attendings, one epidemiologist, one guideline methodologist, two interns, and two medical students.

      Search strategy

      Guidelines developed in the past may not apply to current clinical practice. Based on the recommendations of a study published in Annals of Internal Medicine [
      • Erickson J
      • Sadeghirad B
      • Lytvyn L
      • Slavin J
      • Johnston BC.
      The scientific basis of guideline recommendations on sugar intake: a systematic review.
      ], the publication time of clinical practice guidelines was limited to January 2000 to January 2022. Using search strategies (Appendix 1) formulated by a professional librarian, we searched Embase, Medline, Cochrane, and Web of Science for clinical practice guidelines related to SCI. We also searched Google Scholar and some guideline-specific databases (eg, Scottish Intercollegiate Guidelines Network, Congress of Neurological Surgeons, National Institute for Health and Care Excellence, etc.) (Appendix 2) to supplement the results. We restricted the results to English-language.

      Selection of guidelines

      After the removal of duplicates, the titles and abstracts of the literature were reviewed independently by three reviewers to exclude documents which were not guidelines or were not related to SCI. Before reviewing full-text articles, we increased consistency by selecting 5% of the selected documents as a pilot test [
      • van Teijlingen E
      • Hundley V.
      The importance of pilot studies.
      ]. Differences were resolved through discussion. If differences persisted, senior scientists were available for consultation.
      Based on the recommendations of a study published in Annals of Internal Medicine [
      • Erickson J
      • Sadeghirad B
      • Lytvyn L
      • Slavin J
      • Johnston BC.
      The scientific basis of guideline recommendations on sugar intake: a systematic review.
      ], our inclusion criteria were as follows: (1) developed by nationally recognized committees, medical societies, or publicly funded institutions that formulated recommendations on SCI; (2) included specific methodological sections (for example, literature review, review of the evidence, and the methodology of the forming recommendations); and (3) was the latest version if several versions were available.

      Quality assessment of guidelines

      The included guidelines were appraised by three reviewers independently according to the Appraisal of Guidelines for Research and Evaluation, 2nd edition (AGREE II) instrument (www. agreetrust. org). The AGREE II instrument contains 23 items split into six different domains: scope and purpose (regarding aims, target population, and health problems of guidelines), stakeholder involvement (regarding appropriate stakeholders and intended users in the process of the guideline development), rigor of development (regarding the gathering of evidence and formulation or revisions of recommendations), clarity of presentation (regarding organizations and formats of guidelines and language), applicability (regarding potential barriers to, facilitators factors of, and possible resource impact of the practical application of guidelines), and editorial independence (regarding conflicts of interest in the process of formulating recommendations) [
      • Brouwers MC
      • Kho ME
      • Browman GP
      • Burgers JS
      • Cluzeau F
      • Feder G
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      ]. Further, the AGREE II instrument contains an overall rating item that indicates the general quality of appraised guidelines.
      We scored each item on a scale of 1 to 7 to indicate the degree of agreement between the criteria of AGREE II instrument and the content of the guidelines [
      • Brouwers MC
      • Kho ME
      • Browman GP
      • Burgers JS
      • Cluzeau F
      • Feder G
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      ]. One indicates strong disagreement, and 7 indicates strong agreement. We calculated the score for each domain as follows: (obtained score-minimum possible score)/(maximum possible score-minimum possible score) [
      • Brouwers MC
      • Kho ME
      • Browman GP
      • Burgers JS
      • Cluzeau F
      • Feder G
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      ]. We also calculated the overall rating score by averaging the scores of all 23 items [
      • Guan B
      • Fan Y
      • Zheng R
      • Fu R
      • Yao L
      • Wang W
      • et al.
      A critical appraisal of clinical practice guidelines on pharmacological treatments for spinal cord injury.
      ,
      • Zheng R
      • Guan B
      • Fan Y
      • Fu R
      • Yao L
      • Wang W
      • et al.
      A critical appraisal of clinical practice guidelines for management of four common complications after spinal cord injury.
      ]. Considering that the AGREE II instrument did not define a specific minimum threshold for the scores of each domain [
      • Brouwers MC
      • Kho ME
      • Browman GP
      • Burgers JS
      • Cluzeau F
      • Feder G
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      ], we set it to 50% in our study, referring to a prior study [
      • Anderson DB
      • Luca K
      • Jensen RK
      • Eyles JP
      • Van Gelder JM
      • Friedly JL
      • et al.
      A critical appraisal of clinical practice guidelines for the treatment of lumbar spinal stenosis.
      ]. If the scores of most domains (5–6 domains) were above 50%, the guideline would be evaluated as “recommended”; if the scores of some domains (1–4 domains) were above 50%, the guideline would be evaluated as “recommended with modifications”; if the scores of all domains were below 50%, the guideline would be evaluated as “not recommended” [
      • Simon A
      • Pratt M
      • Hutton B
      • Skidmore B
      • Fakhraei R
      • Rybak N
      • et al.
      Guidelines for the management of pregnant women with obesity: a systematic review.
      ].
      To enhance consistency among the three reviewers, we selected two guidelines from all included guidelines as a pilot before the formal appraisal [
      • van Teijlingen E
      • Hundley V.
      The importance of pilot studies.
      ]. The interquartile range (IQR) and the median score of each domain were calculated. We also calculated the interrater agreement by the intraclass correlation coefficient with a corresponding 95% confidence interval (CI) to measure the reliability of the results. A score of 0.01 to 0.20 indicates poor agreement; a score of 0.21 to 0.40 indicates fair agreement; a score of 0.41 to 0.60 indicates moderate agreement; a score of 0.61 to 0.80 indicates substantial agreement; a score of 0.81 to 1.00 indicates very good agreement [
      • Erickson J
      • Sadeghirad B
      • Lytvyn L
      • Slavin J
      • Johnston BC.
      The scientific basis of guideline recommendations on sugar intake: a systematic review.
      ]. Differences of three points or fewer in the item rating among raters were accepted [
      • Erickson J
      • Sadeghirad B
      • Lytvyn L
      • Slavin J
      • Johnston BC.
      The scientific basis of guideline recommendations on sugar intake: a systematic review.
      ]. Any discrepancy was discussed. If necessary, senior scientists were available for consultation. All calculations in our study were performed by IBM SPSS Statistics 25.0 and Microsoft Excel 2016.

      Recommendations on diagnostic imaging

      One reviewer extracted recommendations on diagnostic imaging of SCI with supporting evidence from guidelines which were evaluated as “recommended with modification” and “recommended.” Two reviewers checked the work. Any differences were resolved through discussion [
      • Khanji MY
      • Bicalho VV
      • van Waardhuizen CN
      • Ferket BS
      • Petersen SE
      • Hunink MG
      Cardiovascular risk assessment: a systematic review of guidelines.
      ].

      Appraisal of levels of evidence

      Given the lack of high-quality supporting evidence such as randomized controlled trials (RCTs), we evaluated the quality of supporting evidence of extracted recommendations by levels of evidence (LOE) based on a prior study whose quality of included supporting evidence was similar to ours [
      • Acuna SA
      • Huang JW
      • Scott AL
      • Micic S
      • Daly C
      • Brezden-Masley C
      • et al.
      Cancer screening recommendations for solid organ transplant recipients: a systematic review of clinical practice guidelines.
      ]. LOE was categorized as A, B, C or D. Grade A refers to individual RCTs and systematic reviews of RCTs; Grade B refers to systematic reviews of cohort/case-control studies, case-control studies, and cohort studies; Grade C refers to case report/series and poor-quality case-control studies or cohort studies; Grade D refers to troublingly inconsistent or inconclusive studies. Additionally, LOE will be assessed as D if one recommendation is an expert opinion formulated without explicit critical appraisal of evidence (Appendix 3).

      Results

      Selection of guidelines

      In total, 12,017 articles were available after the removal of duplicates. Seven guidelines from 2008 to 2020 were included after reviewing titles, abstracts, and full texts (Fig. 1). They were developed by AO Spine [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ], Paralyzed Veterans of America [
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providers.
      ], French Society of Anesthesia and Intensive Care Medicine [
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ], American Association of Neurological Surgeons and Congress of Neurological Surgeons Joint Guidelines Committee [
      • Rozzelle CJ
      • Aarabi B
      • Dhall SS
      • Gelb DE
      • Hurlbert RJ
      • Ryken TC
      • et al.
      Spinal cord injury without radiographic abnormality (SCIWORA).
      ], World Federation of Neurosurgical Societies Spine Committee [
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ,
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ], and Chinese Association of Spine and Spine Cord Injury [
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ]. Table 1 provides detailed information.
      Fig 1
      Fig. 1PRISMA flow chart showing the process in the systematic review.
      Table 1Characteristics of included guidelines
      GuidelineAuthorYearTarget populationDevelopment committees/agencies/associationsMethods used in recommendation developmentRecommendation on MRI
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome predictionFehlings et al.2017Spinal cord injuryAO SpineGRADE systemFor
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providersParalyzed Veterans of America2008Spinal cord injuryParalyzed Veterans of AmericaGuidance from Canadian Medical AssociationFor
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injuryRoquilly et al.2020Spinal cord injuryFrench Society of Anesthesia and Intensive Care MedicineGRADE systemFor
      Outcomes of spinal cord injury: WFNS Spine Committee RecommendationsParthiban et al.2020Cervical spinal cord injuryWFNS Spine CommitteeDelphi methodFor
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in ChinaZhang et al.2013Thoracolumbar spine cord injuryChinese Association of Spine and Spinal Cord InjuryDelphi methodFor
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee RecommendationsKonovalov et al.2020Pediatric cervical spinal cord injury/SCIWORAWFNS Spine CommitteeDelphi methodFor
      Spinal cord injury without radiographic abnormality (SCIWORA)Rozzelle et al.2013SCIWORAAANS/CNS Joint Guidelines CommitteeModified North American Spine Society criteriaFor
      AANS/CNS, American Association of Neurological Surgeons and Congress of Neurological Surgeons; GRADE, Grading of Recommendations Assessment, Development and Evaluation; MRI, magnetic resonance imaging; SCIWORA, Spinal Cord Injury Without Radiographic Abnormality; WFNS, World Federation of Neurosurgical Societies.
      The characteristics of all seven guidelines are outlined in Table 1. This includes their names, authors, edition years, target population, development committees/ agencies/ associations, methods used in recommendation development, recommendation on MRI respectively.

      Quality assessment of guidelines

      For all included guidelines, the scores for each domain were as follows: scope and purpose (range: 51.3%–86.7%, IQR: 56.9%–69.3%, median: 57.2%), stakeholder involvement (range: 17.9%–84.1%, IQR: 25.0%–53.9%, median: 34.3%), rigor of development (range: 41.3%–75.7%, IQR: 45.1%–61.8%, median: 55.1%), clarity of presentation (range: 77.8%–91.2%, IQR: 84.1%–88.0%, median: 87.0%), applicability (range: 5.8%–38.3%, IQR: 7.7%–15.7%, median: 9.7%), editorial independence (range: 22.2%–100%, IQR: 46.7%–84.4%, median: 50.0%), and overall rating (range: 3.5–5.4, IQR: 3.7–4.5, median: 3.7; Table 2, Fig. 2). The range of intraclass correlation coefficients was between 0.838 (95% CI: 0.707–0.921) and 0.975 (95% CI: 0.951–0.988), indicating that the consistency among the three raters was very good. Two guidelines [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ,
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ] scored over 50% in 5 to 6 domains and were evaluated as “recommended”; five guidelines [
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providers.
      ,
      • Rozzelle CJ
      • Aarabi B
      • Dhall SS
      • Gelb DE
      • Hurlbert RJ
      • Ryken TC
      • et al.
      Spinal cord injury without radiographic abnormality (SCIWORA).
      ,
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ,
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ,
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ] scored over 50% in 1 to 4 domains and were evaluated as “recommended with modification.” Therefore, we extracted recommendations from all included guidelines.
      Table 2Appraisal of guidelines through AGREE II instrument
      GuidelineIntraclass correlation coefficient (95% CI)Scope and purpose (%)Stakeholder involvement (%)Rigor of development (%)Clarity of presentation (%)Applicability (%)Editorial independence (%)Overall rating
      Fehlings et al. 20170.838 (0.707–0.921)86.784.168.391.238.3100.05.4
      Paralyzed Veterans of America 20080.890 (0.795–0.948)63.754.875.783.013.922.24.4
      Roquilly et al. 20200.900 (0.812–0.952)74.853.055.187.017.596.74.5
      Parthiban et al. 20200.939 (0.883–0.972)51.317.955.388.97.950.03.7
      Zhang et al. 20130.894 (0.802–0.950)56.734.343.277.87.572.23.7
      Konovalov et al. 20200.868 (0.756–0.937)57.218.046.985.25.843.33.5
      Curtis et al. 20130.975 (0.951–0.988)57.032.041.387.09.750.03.6
      95% CI, 95% confidence interval; AGREE II, Appraisal of Guidelines for Research and Evaluation, 2nd edition.
      The results of appraisals of all seven guidelines through the AGREE II instrument are outlined in Table 2. This includes six domains: scope and purpose, stakeholder involvement, rigor of development, clarity of presentation, applicability, and editorial independence, and overall rating with intraclass correlation coefficient companied with 95% CI.
      Fig 2
      Fig. 2Appraisal of guidelines through AGREE II instrument.

      Diagnostic imaging

      Twelve recommendations were extracted from the included guidelines. We described all included recommendations in detail in Appendix 4 and summarized them in Table 3. LOE was C in nine recommendations and D in three recommendations.
      Table 3Recommendations on MRI in the diagnosis of spinal cord injury from guidelines and LOE of recommendations
      Fehlings et al. 2017Paralyzed Veterans of America 2008Roquilly et al. 2020Parthiban et al. 2020Zhang et al. 2013Konovalov et al. 2020Rozzelle et al. 2013
      SCIPatient ageAdult++
      Children++
      Timing of MRIAs soon as possible++
      Acute period++
      Symptoms indicated for MRINeurological deficit+++
      Suspected disc and posterior ligamentous complex injury+
      A stiff spine and midline tenderness++
      Types of MRIT2WI++
      DTI++
      DTI sequences may be promising to predict outcome in both acute and chronic SCI patients. +, recommended for with LOE D; ++, recommended for with LOE C; +++, recommended for with LOE B; ++++, recommended for with LOE A. Grade A refers to individual RCTs and systematic reviews of RCTs; Grade B refers to systematic reviews of cohort/case-control studies, case-control studies, and cohort studies; Grade C refers to case report/series and poor-quality case-control studies or cohort studies; Grade D refers to troublingly inconsistent or inconclusive studies. LOE will also be assessed as D if one recommendation is an expert opinion formulated without explicit critical appraisal of evidence.
      SCIWORA+++
      DTI, diffusion tensor imaging; SCI, Spinal cord injury; SCIWORA, spinal cord injury without radiographic abnormality; T2WI, T2 weight imaging.
      low asterisk DTI sequences may be promising to predict outcome in both acute and chronic SCI patients. +, recommended for with LOE D; ++, recommended for with LOE C; +++, recommended for with LOE B; ++++, recommended for with LOE A. Grade A refers to individual RCTs and systematic reviews of RCTs; Grade B refers to systematic reviews of cohort/case-control studies, case-control studies, and cohort studies; Grade C refers to case report/series and poor-quality case-control studies or cohort studies; Grade D refers to troublingly inconsistent or inconclusive studies. LOE will also be assessed as D if one recommendation is an expert opinion formulated without explicit critical appraisal of evidence.

      Magnetic resonance imaging

      All guidelines (7/7, 100%) recommended MRI in the diagnosis of SCI or SCI without radiographic abnormality (SCIWORA). Specifically, two guidelines [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ,
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ], two guidelines [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ,
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ], three guidelines [
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providers.
      ,
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ,
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ], and one guideline [
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ] made recommendations on patient age, timing of MRI, symptoms indicated for MRI, and types of MRI, respectively.

      Patient age

      For patient age, one guideline [
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ] (1/2, 50%) recommended MRI for child patients (LOE: C), and one guideline [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ] (1/2, 50%) for adult patients (LOE: C).

      Timing of MRI

      Regarding the timing of MRI, one guideline [
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ] (1/2, 50%) recommended MRI as soon as possible once SCI was suspected (LOE: C), and one guideline [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ] (1/2, 50%) in the acute period (LOE: C).

      Symptoms indicated for MRI

      For the symptoms indicated for MRI, two guidelines [
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ,
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ] (2/3, 66.7%) recommended MRI for patients who had a neurological deficit (LOE: C [n=1] and D [n=1]), one guideline [
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providers.
      ] (1/3, 33.3%) for patients with a stiff spine and midline tenderness (LOE: C), and one guideline [
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ] (1/3, 33.3%) for patients with suspected disc and posterior ligamentous complex injury (LOE: D).

      Types of MRI

      Regarding the types of MRI, one guideline [
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ] (1/1, 100%) recommended that T2-weighted imaging (T2WI) was an acceptable method for the diagnosis of SCI (LOE: C) and diffusion tensor imaging (DTI) might be used to predict outcomes of patients with SCI (LOE: C).

      Discussion

      Seven guidelines regarding diagnostic imaging for patients with SCI were included in the systematic review. In the domains of clarity of presentation, scope and purpose, all included guidelines were above the minimum threshold. Over half of included guidelines were above the minimum threshold in the domains of rigor of development and editorial independence. In the domain of applicability, no guidelines reached the minimum threshold.
      The following accounted for the low scores of the domain of applicability of the included guidelines: (1) Advice and tools for the application of the recommendations were lacking; (2) potential facilitators of and barriers to the application of the recommendations were not discussed; and (3) potential cost implications of the application of the recommendations were not considered. In the future, guideline developers should describe potential factors that may promote or hinder the application of the recommendations, such as advice and tools for the application (eg, a quick reference guide), potential barriers to the application (eg, insufficient skills of practitioners), potential facilitators of the application (eg, sufficient imaging equipment for diagnosis), and potential cost implications of the application (eg, imaging acquisition costs), to improve the applicability of the guidelines [

      The Appraisal of guidelines for research and evaluation (AGREE) II instrument: introduction, user's manual and AGREE II instrument. 2017.

      ].
      Regarding patient age, one guideline [
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ] recommended MRI for child patients because it was a guideline for pediatric SCI. Another guideline [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ] recommended MRI for adult patients because the target population of most of the supporting evidence was adult patients. Notably, both recommendations were based on a low LOE. The other guidelines [
      Early acute management in adults with spinal cord injury: a clinical practice guideline for health-care providers.
      ,
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ,
      • Rozzelle CJ
      • Aarabi B
      • Dhall SS
      • Gelb DE
      • Hurlbert RJ
      • Ryken TC
      • et al.
      Spinal cord injury without radiographic abnormality (SCIWORA).
      ,
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ,
      • Zhang Z
      • Li F
      • Sun T
      An expert consensus on the evaluation and treatment of acute thoracolumbar spine and spinal cord injury in China.
      ] did not describe the patient age in the recommendations. To some extent, these data indicates that there is no high-level evidence to prove that there is an age limit for the use of MRI. One possible reason is that MRI is a safe imaging modality with the use of non-ionizing electromagnetic radiation. With proper management and care, MRI can be performed safely for patients of all ages [
      • Yousaf T
      • Dervenoulas G
      • Politis M.
      Advances in MRI Methodology.
      ,
      • Panych LP
      • Madore B.
      The physics of MRI safety.
      ].
      Regarding the timing of MRI, one guideline [
      • Roquilly A
      • Vigue B
      • Boutonnet M
      • Bouzat P
      • Buffenoir K
      • Cesareo E
      • et al.
      French recommendations for the management of patients with spinal cord injury or at risk of spinal cord injury.
      ] recommended that MRI should be performed as soon as possible once SCI was suspected but did not describe a specific time. Another guideline [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ] recommended MRI in the “acute period”, which was defined as “within a week of injury.” Both guidelines lacked high-quality evidence to prove their reliability, which made their recommendations weak. Although the quality of the supporting evidence was low, the consistency of recommendations was high. One possible reason is that MRI performed in the acute setting can play an important role in the evaluation of patients with suspected SCI for an earlier diagnosis and a timely treatment, which are beneficial to the prognosis of neurological function [
      • Ahuja CS
      • Wilson JR
      • Nori S
      • Kotter MRN
      • Druschel C
      • Curt A
      • et al.
      Traumatic spinal cord injury.
      ,
      • Shabani S
      • Meyer BP
      • Budde MD
      • Wang MC
      Diagnostic imaging in spinal cord injury.
      ]. Therefore, although the quality of the supporting evidence was low, the guidelines arrived at the consistent conclusions leading to the high consistency of the recommendations.
      One guideline [
      • Parthiban J
      • Zileli M
      • Sharif SY.
      Outcomes of spinal cord injury: WFNS Spine Committee Recommendations.
      ] recommended that T2WI was an acceptable method for the diagnosis of SCI and DTI might be used to predict outcomes of patients with SCI. In clinical practice, T2WI is the most important method for the detection of SCI [
      • Talbott JF
      • Huie JR
      • Ferguson AR
      • Bresnahan JC
      • Beattie MS
      Dhall SS. MR imaging for assessing injury severity and prognosis in acute traumatic spinal cord injury.
      ]. It can depict the pathology of most tissues well and have a high sensitivity to spinal cord edema and hemorrhage [
      • Kulkarni MV
      • McArdle CB
      • Kopanicky D
      • Miner M
      • Cotler HB
      • Lee KF
      • et al.
      Acute spinal cord injury: MR imaging at 1.5 T.
      ,
      • Bitar R
      • Leung G
      • Perng R
      • Tadros S
      • Moody AR
      • Sarrazin J
      • et al.
      MR pulse sequences: what every radiologist wants to know but is afraid to ask.
      ]. DTI is a useful imaging method for detecting the microstructure of spinal cord, which is based on diffusion of water molecules in biological tissues [
      • Kaushal M
      • Shabani S
      • Budde M
      • Kurpad S.
      Diffusion tensor imaging in acute spinal cord injury: a review of animal and human studies.
      ,
      • Clark CA
      • Werring DJ.
      Diffusion tensor imaging in spinal cord: methods and applications - a review.
      ]. It can evaluate the extent of spinal cord damage and monitor the effects of regeneration-inducing treatment [
      • Petersen JA
      • Wilm BJ
      • von Meyenburg J
      • Schubert M
      • Seifert B
      • Najafi Y
      • et al.
      Chronic cervical spinal cord injury: DTI correlates with clinical and electrophysiological measures.
      ]. However, the clinical utility of DTI is limited because susceptibility artifacts caused by cardiac and respiratory motions can affect its accuracy [
      • Shabani S
      • Meyer BP
      • Budde MD
      • Wang MC
      Diagnostic imaging in spinal cord injury.
      ]. The acquisition methods, data processing, and interpretation of DTI are also limiting factors [
      • Martin AR
      • Aleksanderek I
      • Cohen-Adad J
      • Tarmohamed Z
      • Tetreault L
      • Smith N
      • et al.
      Translating state-of-the-art spinal cord MRI techniques to clinical use: a systematic review of clinical studies utilizing DTI, MT, MWF, MRS, and fMRI.
      ]. Further, DTI metrics varies with age and signal quality [
      • Vedantam A
      • Jirjis MB
      • Schmit BD
      • Wang MC
      • Ulmer JL
      • Kurpad SN.
      Characterization and limitations of diffusion tensor imaging metrics in the cervical spinal cord in neurologically intact subjects.
      ]. These may be reasons why DTI was not widely recommended in the other included guidelines. The limited availability of relevant clinical studies with a long-term follow-up might also contribute to the weak recommendation for DTI.
      Two guidelines [
      • Rozzelle CJ
      • Aarabi B
      • Dhall SS
      • Gelb DE
      • Hurlbert RJ
      • Ryken TC
      • et al.
      Spinal cord injury without radiographic abnormality (SCIWORA).
      ,
      • Konovalov N
      • Peev N
      • Zileli M
      • Sharif S
      • Kaprovoy S
      • Timonin S.
      Pediatric cervical spine injuries and SCIWORA: WFNS Spine Committee Recommendations.
      ] recommended for MRI in the diagnosis of SCIWORA. SCIWORA is defined as the presence of clinical symptoms of traumatic myelopathy with no radiographic or computed tomographic features of spinal fracture or instability [
      • Szwedowski D
      • Walecki J.
      Spinal cord injury without radiographic abnormality (SCIWORA) - clinical and radiological aspects.
      ]. For this reason, MRI can be utilized to detect some characteristic pathomorphological changes in soft tissues of patients with SCIWORA, such as spinal cord hematomas and edema [
      • Atesok K
      • Tanaka N
      • O’Brien A
      • Robinson Y
      • Pang D
      • Deinlein D
      • et al.
      Posttraumatic spinal cord injury without radiographic abnormality.
      ].
      Referring to the suggestions of reviewers, this study did not include recommendations relevant to CT. CT is regarded as a first-line imaging modality after spinal trauma because it is sensitive to osseous abnormalities and can be performed rapidly [
      • Shabani S
      • Meyer BP
      • Budde MD
      • Wang MC
      Diagnostic imaging in spinal cord injury.
      ]. However, CT is less able to detect ongoing spinal cord edema and hemorrhage than MRI [
      • Fehlings MG
      • Martin AR
      • Tetreault LA
      • Aarabi B
      • Anderson P
      • Arnold PM
      • et al.
      A clinical practice guideline for the management of patients with acute spinal cord injury: recommendations on the role of baseline magnetic resonance imaging in clinical decision making and outcome prediction.
      ,
      • Ahuja CS
      • Schroeder GD
      • Vaccaro AR
      • Fehlings MG.
      Spinal cord injury-what are the controversies?.
      ].
      In the future, more high-quality evidence (eg, data from RCTs) is expected to formulate strong recommendations. However, considering the particularity of studies for diagnostic strategies, this could be difficult and challenging. With synthesis of existing evidence, clinical experience, and expert opinions, the Appropriate Use Criteria (AUC) methodology could be expected to be utilized by a rating panel to determine the appropriateness of MRI in various clinical scenarios [
      • Connolly SM
      • Baker DR
      • Coldiron BM
      • Fazio MJ
      • Storrs PA
      • Vidimos AT
      • et al.
      AAD/ACMS/ASDSA/ASMS 2012 appropriate use criteria for Mohs micrographic surgery: a report of the American Academy of Dermatology, American College of Mohs Surgery, American Society for Dermatologic Surgery Association, and the American Society for Mohs Surgery.
      ]. Additionally, more types of MRI for the diagnosis of SCI such as diffusion-weighted imaging and susceptibility-weighted imaging are expected to be studied and gradually introduced into future guidelines [
      • Thurnher MM
      • Bammer R.
      Diffusion-weighted MR imaging (DWI) in spinal cord ischemia.
      ,
      • Wang M
      • Dai Y
      • Han Y
      • Haacke EM
      • Dai J
      • Shi D.
      Susceptibility weighted imaging in detecting hemorrhage in acute cervical spinal cord injury.
      ].
      There were some strengths in our study. First, this study included seven available clinical practice guidelines on diagnostic imaging of SCI from 2008 to 2020 through a systematic search and critically appraised their qualities using the AGREE II instrument [
      • Brouwers MC
      • Kho ME
      • Browman GP
      • Burgers JS
      • Cluzeau F
      • Feder G
      • et al.
      AGREE II: advancing guideline development, reporting and evaluation in health care.
      ]. This strategy enabled an intuitive presentation of the qualities of existing available guidelines, which can help clinicians in selecting high-quality guidelines to facilitate consistent, efficient, and evidence-based practices in clinical conditions and provide guidance for future work for guideline developers. Second, to our knowledge, this study is the first time to summarize and analyze the recommendations on diagnostic imaging for SCI from existing available guidelines and evaluate the level of their supporting evidence by a unified evidence assessment system. The findings can help clinicians intuitively acquire similarities and differences of the recommendations in current existing guidelines and the quality of their supporting evidence.
      Our study also had some limitations. First, considering that the AGREE II instrument has not defined a specific minimum threshold for the scores of each domain and defined the method for evaluating the overall quality of appraised guidelines, the minimum threshold (50%) set for each domain and evaluation methods of the overall quality might be limitations. However, we evaluated the overall quality of the included guidelines based on two commonly used methods: 1) number of domains reaching the minimum threshold and 2) overall rating score. The results were similar, indicating that the set minimum threshold and evaluation methods did not significantly affect the appraisal results of the overall quality of the included guidelines and the subsequent extraction results of the recommendations. Second, the inclusion criterion that literature must be published in English may have caused several available guidelines to be omitted.
      In conclusion, seven guidelines were included in the present systematic review, and all of them showed the worst applicability scores in the AGREE II instrument. They all weakly recommended MRI for patients with suspected SCI or SCIWORA based on a low LOE.

      Declarations of Competing Interests

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

      Acknowledgments

      Dr Zhou was funded by Taishan Scholars Program of Shandong Province-Young Taishan Scholars (tsqn201909197). We thank Ping Yu from Library of Tianjin Medical University for developing the search strategies. We thank Runhan Fu from Shandong University and Wei Wang from Shandong University for their contributions to this study. This study received no funding.

      Appendix. Supplementary materials

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