A Systematic Review of Semiquantitative and Qualitative Radiologic Criteria for the Diagnosis of Lumbar Spinal Stenosis

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1 Musculoskeletal Imaging Original Research Andreisek et al. Radiologic Criteria for the Diagnosis of LSS Musculoskeletal Imaging Original Research Gustav Andreisek 1 Mario Imhof 2 Maria Wertli 2 Sebastian Winklhofer 1 Christian W. A. Pfirrmann 3 Juerg Hodler 1 Johann Steurer 2 For the Lumbar Spinal Stenosis Outcome Study Working Group Zurich Andreisek G, Imhof M, Wertli M, et al. Keywords: lumbar spinal stenosis, MRI, spine DOI: /AJR Received October 9, 2012; accepted after revision February 28, G. Andreisek was a coworker in a study that resulted in U.S. patent application 12/947,256; has received grants from the Swiss National Science Foundation, Holcim, and Siemens Healthcare; has given talks at a congress sponsored by Mepha Pharma AG, Switzerland, and talks at symposia and CME courses organized and sponsored by Guerbet; and is co or sub principal investigator in several clinical trials at the University of Zurich with sponsors including Millennium Pharmaceuticals, Eli Lilly and Company, GlaxoSmithKline, Cytheris SA, Roche, BioChemics, Novartis, Bristol-Myers Squibb, Topotarget, and Merck Sharp & Dohme. The department where G. Andreisek works receives grants from Siemens Healthcare, Bayer HealthCare, Cordis, and Guerbet. The institute where S. Winklhofer and J. Hodler work receives grants from Siemens Healthcare, Bayer HealthCare, and Guerbet. 1 Department of Radiology, University Hospital Zurich, Ramistrasse 100, 8091 Zurich, Switzerland. Address correspondence to G. Andreisek (gustav@andreisek.de). 2 Horten Centre for Patient Oriented Research and Knowledge Transfer, University of Zurich, Zurich, Switzerland. 3 Department of Radiology, Orthopedic University Hospital Balgrist, Zurich, Switzerland. WEB This is a web exclusive article. AJR 2013; 201:W735 W X/13/2015 W735 American Roentgen Ray Society A Systematic Review of Semiquantitative and Qualitative Radiologic Criteria for the Diagnosis of Lumbar Spinal Stenosis OBJECTIVE. The objective of our study was to perform a systematic review of the semiquantitative and qualitative radiologic criteria that are used for the diagnosis of lumbar spinal stenosis (LSS). MATERIALS AND METHODS. A four-step systematic literature search including the MEDLINE database was performed by an experienced librarian to reveal all semiquantitative or qualitative radiologic criteria used for the diagnosis of LSS. The precise definitions of all criteria, normal or abnormal values (if applicable), and intra- and interrater reliability were noted by two independent readers. Descriptive statistics were used. RESULTS. A total of 14 semiquantitative or qualitative radiologic parameters were identified and distinguished according to relevant anatomic spaces into criteria for central canal stenosis, lateral (recess) stenosis, and foraminal stenosis. Great variability in terms of the exact definitions of the criteria was found. For 10 of the 14 criteria, the intra- and interrater reliability data were found with kappa values ranging from 0.01 to 1.0. CONCLUSION. Our systematic literature review identified 14 different semiquantitative or qualitative radiologic criteria that are used for the diagnosis of LSS; however, these criteria show remarkable variability in terms of their exact individual definitions and intraand interrater reliability. L umbar spinal stenosis (LSS) is the most common cause for lumbar spinal surgery in patients older than 65 years [1]. The diagnosis is typically based on symptoms, clinical examination findings, and radiologic findings [2]. Although there is agreement that MRI is the best imaging modality because of its outstanding soft-tissue contrast, CT, CT myelography, and even radiography are frequently used in the evaluation of LSS [3]. Remarkable variability is seen in the literature with regard to the radiologic criteria used for the diagnosis [4]. Various quantitative measures, such as the anteroposterior diameter of the spinal canal or the cross-sectional area of the spinal canal, are frequently applied to LSS even though most of those measures are limited by little evidence for their usefulness in the literature and even though many different threshold values exist for them [5, 6]. Recent data derived from a systematic Delphi survey [7] have shown that the number of quantitative measures and the lack of their standardized use translate into confusion in the clinical routine given that even specialized radiologists apply different measures differently [8]. In the same survey [7], investigators observed that many radiologists also use semiquantitative or only qualitative criteria to describe LSS. Some radiologists may even use very vague and subjective descriptions such as minor, medium, or major LSS. To overcome this individual subjectivity of radiologists and to reach some level of standardization, several different classifications systems have been described in the past years [9 11]. Besides these studies describing the principles, use, and advantages of individual classification systems, there is, to our knowledge, no systematic review of the literature on the semiquantitative and qualitative radiologic criteria for the diagnosis of LSS. Thus, the purpose of our study was to perform a systematic review of the semiquantitative and qualitative radiologic criteria used for the diagnosis of LSS. Materials and Methods For this literature review study, no ethics board approval or consent of any individual was necessary. AJR:201, November 2013 W735

2 Andreisek et al. Literature Searches Literature searches were performed by an experienced librarian with special training and skills in literature searches. To minimize the number of missed studies, the librarian used a four-step approach to identify the relevant studies on semiquantitative and qualitative radiologic criteria for the diagnosis of LSS. The first step included identification of all references that were identified in our recent research projects on LSS [5]. Second, all criteria from the Delphi survey a study in which experts in lumbar spinal imaging were asked to list all the radiologic criteria they use for the diagnosis of LSS in clinical routine were included. Third, a standardized literature search of MEDLINE (U.S. National Library of Medicine) was performed using the following terms: facet joint, facet joints arthrosis, grading system, intervertebral disk displacement, ligamentum flavum thickness, lumbar epidural lipomatosis, lumbar foraminal stenosis, lumbar facet joint grading, lumbar spinal stenosis, lumbar vertebrae, magnetic resonance imaging, nerve root impingement, nomenclature, osteoarthritis, and redundant nerve roots. As a last step, the reference lists of all articles that were derived in steps 1 3 were screened for additional relevant articles on semiquantitative and qualitative radiologic criteria for LSS. After completion of the four-step literature search, MEDLINE was then searched for studies reporting on the reliability of the identified radiologic criteria. Therefore, free text for every semiquantitative or qualitative radiologic criterion and the Medical Subject Heading (MeSH) term reproducibility of results were used. Only articles published in English or German were included in this systematic review. We excluded studies that reported solely on the classification of disk or endplate abnormalities and on noncompressive myelopathies or abnormalities of the cauda equina because those studies primarily refer to different diseases and do not focus on the diagnosis of LSS. Data Extraction and Statistical Analysis Two reviewers independently screened all studies for semiquantitative or qualitative radiologic criteria; precise definitions of the criteria; and normal and abnormal values, if applicable. All criteria, definitions, and normal or abnormal values were noted. In addition, data reflecting the reproducibility of results such as the intra- and interreader reliability of each semiquantitative or qualitative radiologic criterion were noted. Only descriptive statistics are presented. Statistical analysis was not performed. Fig. 1 Three-dimensional surface-rendered CT images illustrate anatomic spaces. In upper part, dorsal view of lumbar vertebra L4 and its pedicles is provided. In lower part, same vertebra is shown from top. Dashed lines connect both figure parts and outline location of anatomic spaces. Extraforaminal (E) space is lateral to neuroforamen. Foraminal space (F) is bordered by cephalad and caudal pedicles, facet joints dorsally, and vertebral body and disks ventrally. Lateral recess (L) is bordered laterally by pedicle, dorsally by superior articular facet, and ventrally by vertebral body and disks. Central portion (C) of spinal canal is bordered laterally by lateral recess, dorsally by vertebral arch, and ventrally by vertebral body and disks. A Fig. 2 MRI of lumbar spinal stenosis (LSS) and of healthy spine. A, Sagittal T2-weighted MR image of symptomatic 76-year-old woman with LSS (arrows) at levels L3 L4 and L4 L5. B, Sagittal T2-weighted MR image of healthy 38-year-old male volunteer without any signs of LSS. B W736 AJR:201, November 2013

3 Radiologic Criteria for the Diagnosis of LSS Results Literature Searches All articles identified in recent research projects on LSS revealed four semiquantitative or qualitative radiologic parameters for LSS (step 1) [5]. A total of 21 experts responded to the Delphi survey [7]. They mentioned seven semiquantitative or qualitative radiologic parameters that were then included in this systematic review (step 2). The review of the articles identified in an extensive search of MEDLINE revealed another three semiquantitative or qualitative radiologic criteria (step 3). Screening the reference lists of all published studies that were derived in steps 1 3 did not reveal additional criteria. Overall, a total of 14 semiquantitative or qualitative radiologic parameters were identified (Appendix 1). The criteria can be characterized according to the relevant anatomic spaces into criteria for central spinal canal stenosis, lateral (recess) stenosis, and foraminal stenosis (Figs. 1 3 and Tables 1 3). The criteria for central stenosis include a description of spinal canal compression in relation to its normal size [12]; subjective (eyeballing) evaluation of the central spinal canal [13]; evaluation of the obliteration of the anterior CSF space and degree of separation of the cauda equina on axial T2-weighted images [10]; evaluation of the relation of fluid to nerve roots in the central spinal canal on axial T2-weighted MR images [11]; assessment for the nerve root sedimentation sign [14]; assessment of the thickness of the ligamentum flavum (anteroposterior); presence of enlarged, elongated, and tortuous nerve roots [15 17]; and absence or reduction of posterior epidural A Fig. 3 Axial T2-weighted MR images show lumbar spinal stenoses at different locations in different patients. A, 54-year-old man with central spinal canal stenosis (arrow). B, 67-year-old woman with neuroforaminal stenosis (arrow). C, 64-year-old man with unilateral stenosis of right lateral recess (arrow). fat and excessive deposition of epidural fat in the central spinal canal [18 20]. The criteria for lateral stenosis include evaluation of compression of the subarticular zone, which is equal to the lateral recess, in relation to its normal size [12]; a description of the usually cone-shaped portion of the bony spinal canal that extends laterally from the origin of the nerve root to the medial end of the neural foramen [21]; and grading of nerve root compression in the lateral recess [22]. Different grading systems have been reported for the following parameter: compression of the subarticular zone. The criteria for foraminal stenosis include evaluation of the amount of perineural epidural fat around the nerve root [23]; the presence of perineural intraforaminal fat around the nerve root in the neuroforamen in combination with nerve root compression [21]; facet joint degeneration with joint space narrowing, subchondral sclerosis, osteophytes, cyst formation, and joint deformation [24]; compression of the foraminal zone [12]; grading of nerve root impingement by the foramen [12]; grading of nerve root impingement [25]; assessment of the relationship of the nerve root with adjacent disks [26]; classification based on epidural compression of the lumbar nerve root [27]; and quantitative and qualitative assessments of the size and shape of the foramen [13, 28]. Intra- and Interrater Reliability Data on the intra- and interrater reliability have been published for most of the parameters (Table 4). No data could be identified for the following parameters: hypertrophy of the ligamentum flavum, redundant nerve roots of B the cauda equina, reduction of posterior epidural fat, and nerve root compression in the lateral recess. All of the values for intrarater reliability and interrater reliability with a few exceptions are in the moderate (κ = ) to high (κ > 0.61) range [29]. The variability is most prominent for hypertrophic facet joint degeneration with kappa values ranging from 0.16 to 0.89 for intrarater reliability and from 0.01 to 0.89 for interrater reliability. Discussion Although imaging has been used for many years for the diagnosis of LSS and MRI has practically become the standard imaging modality, there are, surprisingly, no universally accepted radiologic criteria for any of the different imaging modalities. Quantitative criteria can be differentiated from semiquantitative and qualitative radiologic criteria because the latter are inherently based on the subjectivity of the evaluation of the interpreter. Recent studies have listed commonly used quantitative criteria [5]. However, radiologists and clinicians use semiquantitative and qualitative radiologic criteria for the diagnosis of LSS more often than quantitative criteria. As shown in the recent literature [7, 30 32], different criteria often are used or applied differently by using different definitions of the same criterion; using custom-made modifications of those criteria; or simply using the criteria incorrectly because of a lack of knowledge, preciseness, or thoroughness. Overall, this variability reduces comparability of radiologic reports and hampers communication among radiologists as well as between radiologists and clinicians [4]. In research situations, this variability may lead to misinterpretation of findings C AJR:201, November 2013 W737

4 Andreisek et al. TABLE 1: Semiquantitative or Qualitative Radiologic Criteria for the Diagnosis of Lumbar Spinal Stenosis: Central Spinal Canal Stenosis Parameter Definition of Parameter Classification Criteria for Classification Compression of central spinal canal Compression in relation to normal size of central spinal canal [12] Subjective (eyeballing) evaluation of central spinal canal [13, 28] No stenosis Mild stenosis Compression of < 1/3 of its normal size Moderate stenosis Compression of 1/3 2/3 of its normal size Severe stenosis Compression of > 2/3 of its normal size Grade 1 Normal central (spinal) canal; normal is defined subjectively depending on size of person Grade 2 Slight reduction of central (spinal) canal; grade 2 is also normal but with smaller overall canal dimensions Grade 3 Mild reduction of central (spinal) canal; overall dimensions are borderline a Grade 4 Moderate reduction of central (spinal) canal; size and shape are abnormal Grade 5 Severe reduction of central (spinal) canal; there is circumferential constriction at intersvertebral paces b Obliteration of anterior CSF space Nerve root sedimentation sign Hypertrophy of ligamentum flavum Obliteration of anterior CSF space and degree of separation of cauda equina on axial T2- weighted images [10] Relation of fluid to nerve roots in central spinal canal on axial T2-weighted MR images [11] Sedimentation of lumbar nerve roots to dorsal part of dural sac on supine MRI scans [14] Thickness (anteroposterior) of ligamentum flavum c Grade 0 No stenosis and anterior CSF space is not obliterated Grade 1 Mild stenosis: Anterior CSF space is mildly obliterated but all nerves in cauda equina can be clearly separated from each other Grade 2 Moderate stenosis: Anterior CSF space is moderately obliterated and some nerves in cauda equina are aggregated, making it impossible to visually separate them Grade 3 Severe stenosis: Anterior CSF space is obliterated so severely as to show marked compression of dural sac and none of the nerves in the cauda equina can be visually separated from one another, appearing instead as one bundle Grade A Minor stenosis: CSF is clearly visible inside dural sac, but its distribution is inhomogeneous A1 Rootlets lie dorsally and occupy less than half of dural sac area A2 Rootlets lie dorsally in contact with dura but in horseshoe configuration A3 Rootlets lie dorsally and occupy more than half of dural sac area A4 Rootlets lie centrally and occupy majority of dural sac area Grade B Moderate stenosis: Rootlets occupy whole dural sac but individual rootlets can still be seen; some CSF is still present giving a grainy appearance to sac Grade C Severe stenosis: No rootlets can be recognized and dural sac shows homogeneous gray signal intensity with no CSF signal visible; there is posterior epidural fat present Grade D Extreme stenosis: In addition to no rootlets being recognizable, there is no posterior epidural fat Sign is either positive (nerve roots sediment) or negative (Table 1 continues on next page) W738 AJR:201, November 2013

5 Radiologic Criteria for the Diagnosis of LSS TABLE 1: Semiquantitative or Qualitative Radiologic Criteria for the Diagnosis of Lumbar Spinal Stenosis: Central Spinal Canal Stenosis (continued) Parameter Definition of Parameter Classification Criteria for Classification Redundant nerve roots of cauda equina Reduction of posterior epidural fat Enlarged, elongated, and tortuous nerve roots [15 17] No grading system found Absence or reduction of posterior epidural fat Normal amount of posterior epidural fat Epidural lipomatosis Excessive deposition of epidural fat in central spinal canal [18 20] Small amount of posterior epidural fat Very small amount of posterior epidural fat Classification according to Borré et al. [18] Up to 50% absent d Up to 75% absent d Grading system based on ratio of dural sac diameter to diameter of epidural fat and on ratio of diameter of epidural fat to diameter of spinal canal e Grade 0 Normal amount of epidural fat: dural sac epidural fat ratio 1.5 and epidural fat spinal canal ratio 40% Grade 1 Mild epidural fat overgrowth: dural sac epidural fat ratio = and epidural fat spinal canal ratio = 41 50% Grade 2 Moderate epidural fat overgrowth: dural sac epidural fat ratio = and epidural fat spinal canal ratio = 51 74% Grade 3 Severe epidural fat overgrowth: dural sac epidural fat ratio 0.33 and epidural fat spinal canal ratio 75% Y sign according to Kuhn et al. [19] In axial images, thecal sac is compressed by epidural fat into a Y shape Classification according to Ishikawa et al. [21] for sagittal images Grade 1 Epidural fat observed within border between anterosuperior edges of upper and lower neighboring neural arches Grade 2 Fat observed over border at middle but not at edges of neural arches on both sides Grade 3 Fat observed over border at edges of neural arches on at least one side Classification according to Ishikawa et al. [20] for axial images Fat accumulation at each intervertebral disk level from L1 to L5 was classified as absent, concave, flat, convex, or exhibiting the Y shape described by Kuhn et al. [19] a Examples: an otherwise normal canal with large disk herniation within the canal, prominent ligamentum flavum, generous articular facets, granulation, or scar tissue from prior operative procedures. b Examples: severe disk herniation, degenerative changes of the facet joints, and spondylolisthesis. c In one study, normal is up to 5 mm [37]; in another study, mean thickness was 4.4 mm in patients with spinal stenosis and 2.4 mm in a control group [38]. d Measurements are obtained on axial cuts parallel to superior endplates and through middle of intervertebral disk. e Measurements are obtained at axial plane parallel and tangent to superior endplate of S1 vertebral body. AJR:201, November 2013 W739

6 Andreisek et al. TABLE 2: Semiquantitative or Qualitative Radiologic Criteria for the Diagnosis of Lumbar Spinal Stenosis: Lateral Spinal Stenosis Parameter Definition of Parameter Classification Criteria for Classification Compression of subarticular zone (i.e., lateral No stenosis recess) in relation to its normal size [12] a Mild stenosis Compromise of < 1/3 of its normal size Moderate stenosis Compromise of 1/3 2/3 of its normal size Severe stenosis Compromise of > 2/3 of its normal size Cone-shaped portion of bony spinal canal that Grade 1 Normal lateral recess; in axial view, neural canal is triangular extends laterally from thecal origin of nerve without lateral compression in area of exiting nerve root and root to medial end of neural foramen [21] pedicles are of normal length; on sagittal view, space between lamina and vertebral body should be at least 5 mm Grade 2 Also a normal variant; canal is trefoil in shape and conical recess is well formed, but there is no compression of exiting nerve; distance between buckled lamina and posterior edge of vertebral body is at least 5 mm Grade 3 Bony recess is slightly narrower than 5 mm; this narrowing is usually caused by expansion into canal of laminae and articular process Grade 4 Moderate recess stenosis: Recess is objectively narrow; this narrowing in combination with enlargement of facets, ligamentum flavum hypertrophy, and short pedicles produces spinal stenosis Grade 5 Severe recess stenosis: Exiting nerve is objectively compressed and may be impossible to identify within recess; foraminal component of nerve may be swollen b Nerve root compression in lateral recess [22] Grade 0 No lateral recess narrowing or root compression Compression of subarticular zone Nerve root compression in lateral recess and severely limits the value of some studies, especially longitudinal observations and outcome studies. In clinical routine, this variability may have negative effects on the diagnosis and therapy of patients with LSS, which may have some medicolegal implications as well. In our study, we have thus reviewed systematically the semiquantitative and qualitative radiologic criteria described in the literature and what has been reported about their reliability in terms of inter- and intrareader agreement. We found criteria for central spinal canal stenosis, lateral (recess) stenosis, and foraminal stenosis. Many radiologists and clinicians will be familiar with at least some of the individual criteria for example, compression of the central spinal canal (Table 1); however, as shown by our study, two different characterizations and definitions exist for this criterion in the literature [12, 13, 28]: One is Grade 1 Grade 2 Grade 3 based on a semiquantitative evaluation of the diameter of the spinal canal by the reader who must determine if there is a mild, moderate, or severe stenosis depending on if one third of the spinal canal, two thirds of the spinal canal, or the complete spinal canal is narrowed, respectively. Besides this semiquantitative characterization and definition of compression of the central spinal canal, a five-grade system exists with a purely subjective evaluation of the spinal canal (Table 1). Adding to the confusion is the fact that the same terms for grading LSS (i.e., mild, moderate, and severe) are used to grade this criterion (compression of the central spinal canal) even though the two underlying definitions found in the literature are completely different [13, 28]. As an example of the variability in radiologic criteria for lateral spinal (recess) stenosis, there are two criteria that describe Evidence of lateral recess narrowing but no objective evidence of root compression More significant lateral recess narrowing (angular or trefoil) with nerve root judged to be flattened or widened but with preservation of CSF around root in recess Severe nerve root compression within lateral recess with obliteration of CSF from recess a Lurie et al. [12] define the subarticular zone as per Fardon et al. [39] as extending from the medial edge of the articular facet to the edge of the neuroforamen. b It is quite common that recess stenosis is associated with central and foraminal stenosis. compression of the subarticular zone [12, 21]. Whereas the first is a relatively simple 3-point grading system (one third or less, one third to two thirds, or more than two thirds) based on the amount of compression of the recess, the second is very complicated and is based on a mixture of semiquantitative and qualitative measures. In addition, the latter grading system is further complicated because it mixes descriptions of normal variants (grades 1 and 2) and of pathologic conditions, with higher grades correlating with increasing severity of compression. This classification also lacks clear definitions; for example, grade 4 is defined as a moderate recess stenosis in which the recess is objectively narrow. However, narrow is not specifically defined and readers might interpret narrow differently. Finally, the term objectively in this context is misleading be- W740 AJR:201, November 2013

7 Radiologic Criteria for the Diagnosis of LSS TABLE 3: Qualitative Parameters for the Diagnosis of Lumbar Spinal Stenosis: Foraminal Spinal Stenosis Parameter Definition of Parameter Classification Criteria for Classification Perineural intraforaminal fat Hypertrophic facet joint degeneration Amount of perineural epidural fat around the nerve root [23] Presence of perineural intraforaminal fat around nerve root in neuroforamen in combination with nerve root compression [21] Degeneration with joint space narrowing, subchondral sclerosis, osteophytes, cyst formation, and joint deformation [24] Grade 1 Normal segments; normal dorsolateral border of intervertebral disk and normal form of foraminal epidural fat; oval or inverted pear shape according to Stephens et al. [40] Grade 2 Slight foraminal stenosis and deformity of epidural fat and remaining fat still completely surrounds exiting nerve root Grade 3 Marked foraminal stenosis and epidural fat only partially surrounds nerve root Grade 4 Advanced stenosis with complete obliteration of foraminal epidural fat Grade 0 Absence of foraminal stenosis Grade 1 Mild foraminal stenosis: perineural fat obliteration surrounding nerve root in two opposing directions (vertical or transverse); it involves contact with superior and inferior portions of nerve root or anterior and posterior portions of nerve root; no evidence of morphologic change in nerve root is present Grade 2 Moderate foraminal stenosis: perineural fat obliteration surrounding nerve root in four directions without morphologic change in both vertical and transverse directions Grade 3 Severe foraminal stenosis: nerve root collapse or morphologic change Classification according to Pathria et al. [33] a Grade 0 No degeneration: normal Grade 1 Mild degeneration: narrowing of facet joint Grade 2 Moderate degeneration: narrowing plus sclerosis or hypertrophy Grade 3 Severe degeneration: narrowing, sclerosis, and osteophytes Classification according to Pathria et al. [33] b Grade 0 No degeneration: normal facet joint space (width: mean ± SD, 2 ± 4 mm) Grade 1 Mild degenerative disease: narrowing of facet joint space (< 2 mm), small osteophytes, mild hypertrophy of articular process, or a combination of these findings Grade 2 Moderate degenerative disease: narrowing of facet joint space, moderate osteophytes, moderate hypertrophy of articular process, mild subarticular bone erosions, or a combination of these findings Grade 3 Severe degenerative disease: narrowing of facet joint space, large osteophytes, severe hypertrophy of articular process, severe subarticular bone erosions, subchondral cysts, or a combination of these findings Classification according to Coste et al. [36] Grade 1 Association of articular space narrowing and subchondral osteosclerosis Grade 2 Association of articular space narrowing, subchondral osteosclerosis, and osteophytes (Table 3 continues on next page) AJR:201, November 2013 W741

8 Andreisek et al. TABLE 3: Qualitative Parameters for the Diagnosis of Lumbar Spinal Stenosis: Foraminal Spinal Stenosis (continued) Parameter Definition of Parameter Classification Criteria for Classification Compression of foraminal zone Foraminal nerve root impingement Compression of foraminal zone [12] No stenosis Grade of nerve root impingement by foramen [12] Nerve root impingement classified depending on direction from where nerve root impingement happens [25] Relationship of nerve root with adjacent disks [26] Classification according to Rothman and Glenn [28] Grade 1 Normal facets: Facet joint space measures approximately 1 3 mm and is smooth and well corticated Grade 2 Normal to slightly enlarged facets: Frequently osteoarthritic spurs project slightly into canal; amount of degenerative change is usually mild Grade 3 Mildly pathologic facets: Mild but definite indentation by articular process or by spurs arising from them is present; neural foramina may be narrowed; degenerative change is usually mild with minimal bony facet hypertrophy and canal compression; there may be additional canal encroachment caused by swelling or fibrous enlargement of joint capsule and ligamentum flavum Grade 4 Moderate facet hypertrophy: Joint surfaces may be partially smooth but are usually disorganized, pitted, sclerotic, and eroded; osteoarthritic spurs usually arise from both superior and inferior facets; joint capsules are often enlarged and occasionally calcified; hypertrophy of laminae Grade 5 Severe facet hypertrophy: There is gross erosion, pitting, and irregularity of facet joint; hypertrophic spur formation may be located at anterior aspect of facet joint; hypertrophic bone may become very thick and dense; facets are associated with marked thickening and irregularity of laminae; subluxation of facets, causing degenerative spondylolisthesis, can occur Mild stenosis Compromise of < 1/3 of its normal size Moderate stenosis Compromise of 1/3 2/3 of its normal size Severe stenosis Compromise of > 2/3 of its normal size None Touching Displacing Compressing Modified according to Kunogi and Hasue [43] Anteroposterior nerve root entrapment caused by a tip of the superior articular process or ligamentum flavum Cephalocaudal nerve root entrapment resulting from compression of nerve by border of pedicle, osteophytic ridge, or bulging annulus Circumferential nerve root entrapment: not specified No contact Contact without deviation of nerve root Contact with deviation of nerve root Nerve root compression (Table 3 continues on next page) W742 AJR:201, November 2013

9 Radiologic Criteria for the Diagnosis of LSS TABLE 3: Qualitative Parameters for the Diagnosis of Lumbar Spinal Stenosis: Foraminal Spinal Stenosis (continued) Parameter Definition of Parameter Classification Criteria for Classification Grade 0 Normal, no compromise of nerve root: There is no evident contact of disk material with nerve root, and epidural fat layer between nerve root and disk material is preserved Classification based on epidural compression of lumbar nerve root [27] Grade 1 Contact: There is visible contact of disk material with nerve root and normal epidural fat layer between the two is not evident; nerve root has a normal position and there is no dorsal deviation Grade 2 Deviation: Nerve root is displaced dorsally by disk material Grade 3 Compression: Nerve root is compressed between disk material and wall of spinal canal; it may appear flattened or be indistinguishable from disk material Grade 1 Normal: Foramina must be at least 1 cm high and 5 mm wide; there must be smooth bony walls; perineural fat surrounding nerve root should be clearly seen; presence or absence of abnormalities is not considered Size and shape of foramen Size of foramen is assessed both quantitatively and qualitatively; bony configuration of foramen is included [13, 28] Grade 2 Slightly narrow but normal foramina: Foramina are reduced in height to just under 10 mm but should be at least 5 mm wide; when present, osteophytes are always minimal in size and facets are normally aligned in sagittal view Grade 3 Narrow foramen of questionable clinical significance: Foramina are reduced in size more than are grade 2 foramina; some perineural fat can still be seen around nerve on sagittal views Grade 4 Moderately abnormal foramina: Foramina just fit a normal-size nerve and there is no reserve space; prominent osteophytes arising from facet joints or vertebral endplates may severely compress nerve Grade 5 Severe foraminal stenosis: Diameter incapable of containing a normal nerve root even at rest; there is severe osteophyte formation with bony indentation on nerve and facet joint degeneration a Adapted by Abbas et al. [41] and Fujiwara et al. [42]. b Modified by Weishaupt et al. [34] and Stieber et al. [35]. cause this classification system is mainly a subjective grading system. Another example for many different characterizations and definitions existing for the same abnormality is hypertrophic facet joint degeneration. Underlying somatic (or anatomic) abnormalities for LSS in patients with facet joint degeneration may include osteophyte formation, bone remodeling with bony hypertrophy, thickening of ligamentous structures such as the joint capsule and ligamentum flavum, joint space narrowing with subsequent loss of height and foraminal stenosis, and spondylolisthesis. The current grading systems for facet joint degeneration mainly focus on the description of those anatomic abnormalities, but their association with LSS is rarely included in these grading systems [33 36]. Great variability is seen with regard to the intra- and interrater reliability of the individual radiologic criteria. Most reported kappa values have a broad range even for criteria that have been evaluated in many studies; for example, the intra- and interrater agreement ranged from almost complete disagreement to almost perfect agreement for the criterion hypertrophic facet joint degeneration (Table 4). Overall, most criteria were reported to have at least a moderate intra- and interrater reliability. How these reliability data translate into the clinical routine remains unclear because most data were acquired under research conditions; a true clinical setting was chosen to evaluate agreement between readers in only a few studies. Overall many different semiquantitative and qualitative radiologic criteria for the diagnosis of LSS exist. The descriptions of the criteria in the literature vary in preciseness and the use of these criteria in clinical routine and under research conditions also varies. Introducing more or new radiologic criteria to quantify stenosis might not solve these problems but will likely enhance them. Thus, as a consequence for daily practice and all clinically oriented research studies, future studies on LSS should draw attention to the use of the existing, most commonly used radiologic criteria until a universally accepted consensus about how to diagnose LSS on radiologic examinations is established. For the latter, joint work of radiologists and clinicians of each subspecialty is required to create guidelines for imaging and radiologic criteria. Ideally, this work might be achieved on an international level with consensus work by international societies, but it can also be done on a national level to define nationally accepted radiologic criteria. The advantage of national guidelines might be consideration of nomenclature differences with regard to different languages. After a final consensus has been achieved, there, however, will still remain some common and major clinical issues regarding LSS such as persistent uncertainty regarding the relationship between abnormalities observed at imaging and clinical symptoms [4]. It is fairly well known that the severity and characteristics of symptoms in patients with identical LSS at imaging may vary signif- AJR:201, November 2013 W743

10 Andreisek et al. TABLE 4: Kappa Values for Intra- and Interrater Reliability of Criteria Used for the Diagnosis of Lumbar Spinal Stenosis κ [Reference No.] Critieria Intrarater Reliability Interrater Reliability Central stenosis Compression of central spinal canal 0.82 [13] [12, 13, 28] Reduced or absent fluid around cauda equina [10, 11] [10, 11] Nerve root sedimentation sign 1.0 [14] 0.93 [14] Hypertrophy of ligamentum flavum No data No data Redundant nerve roots of cauda equina No data No data Reduction of posterior epidural fat No data No data Epidural lipomatosis (for Borré et al. [18] classification) [18] [18] Lateral stenosis Compression of subarticular zone [12] 0.49 [12] Nerve root compression in lateral recess No data No data Foraminal stenosis Perineural intraforaminal fat [10, 23, 40] [10, 23, 40] Hypertrophic facet joint degeneration [24, 26, 28, 33 38] [24, 26, 28, 33 35, 37, 38] [36] Compression of foraminal zone [12] 0.58 [12] Foraminal nerve root impingement [12, 23, 26, 27] [12, 23, 26, 27] Size and shape of foramen No data 0.47 [13] icantly. This characteristic of LSS seems to be the major challenge for future clinical research in the field of LSS. To our knowledge, several large prospective multicenter trials that will address at least some of these issues are currently ongoing in different countries and the aims of these studies include correlation of imaging and clinical symptoms and outcome. Our study has potential limitations. Although a four-step approach was used for searching publications, only MEDLINE was thoroughly searched in this study using the terms mentioned earlier. However, references from two of our recent research projects [5, 7] were included, and for those prior projects, thorough searches of MEDLINE, EMBASE (Elsevier), and the Cochrane Library (Cochrane Collaboration) were performed. Nevertheless, some studies, such as studies in which different descriptions of LSS were used, could have been missed. Another limitation is the fact that only studies published in English and German were included. This inclusion criterion was applied because none of the authors has sufficient knowledge of other foreign languages to allow analysis. Nevertheless, our study included input from 21 international radiologic experts from different countries including France in this field who reported seven semiquantitative and qualitative radiologic criteria [7], all of which were included in our list. Therefore, we are confident that we did not miss relevant parameters or criteria. In conclusion, our systematic literature review identified 14 different semiquantitative and qualitative radiologic criteria that are used for the diagnosis of LSS; however, we found that there is remarkable variability in terms of the exact individual definitions and the intraand interrater reliability of these criteria. References 1. Deyo RA, Gray DT, Kreuter W, Mirza S, Martin BI. United States trends in lumbar fusion surgery for degenerative conditions. Spine 2005; 30: ; discussion, Katz JN, Harris MB. Clinical practice: lumbar spinal stenosis. N Engl J Med 2008; 358: Morita M, Miyauchi A, Okuda S, Oda T, Iwasaki M. Comparison between MRI and myelography in lumbar spinal canal stenosis for the decision of levels of decompression surgery. J Spinal Disord Tech 2011; 24: Andreisek G, Hodler J, Steurer J. Uncertainties in the diagnosis of lumbar spinal stenosis. Radiology 2011; 261: Steurer J, Roner S, Gnannt R, Hodler J; LumbSten Research Collaboration. Quantitative radiologic criteria for the diagnosis of lumbar spinal stenosis: a systematic literature review. BMC Musculoskelet Disord 2011; 12: Dora C, Walchli B, Elfering A, Gal I, Weishaupt D, Boos N. The significance of spinal canal dimensions in discriminating symptomatic from asymptomatic disc herniations. Eur Spine J 2002; 11: Mamisch N, Brumann M, Hodler J, Held U, Brunner F, Steurer J; Lumbar Spinal Stenosis Outcome Study Working Group Zurich. Radiologic criteria for the diagnosis of spinal stenosis: results of a Delphi survey. Radiology 2012; 264: Friedly JL, Jarvik JG. Agreeing (or not) on how to describe spinal stenosis: expanding a narrow mindset. Radiology 2012; 264: Arana E, Royuela A, Kovacs FM, et al. Lumbar spine: agreement in the interpretation of 1.5-T MR images by using the Nordic Modic Consensus Group classification form. Radiology 2010; 254: Lee GY, Lee JW, Choi HS, Oh KJ, Kang HS. A new grading system of lumbar central canal stenosis on MRI: an easy and reliable method. Skeletal Radiol 2011; 40: Schizas C, Theumann N, Burn A, et al. Qualitative grading of severity of lumbar spinal stenosis based on the morphology of the dural sac on magnetic resonance images. Spine 2010; 35: Lurie JD, Tosteson AN, Tosteson TD, et al. Reliability of readings of magnetic resonance imaging features of lumbar spinal stenosis. Spine (Phila Pa 1976) 2008; 33: Rankine JJ, Hutchinson CE, Hughes DG. MRI of lumbar spondylosis: a comparison of sagittal T2 W744 AJR:201, November 2013

11 Radiologic Criteria for the Diagnosis of LSS weighted and three sequence examinations. Br J Radiol 1997; 70: Barz T, Melloh M, Staub LP, et al. Nerve root sedimentation sign: evaluation of a new radiological sign in lumbar spinal stenosis. Spine (Phila Pa 1976) 2010; 35: Min JH, Jang JS, Lee SH. Clinical significance of redundant nerve roots of the cauda equina in lumbar spinal stenosis. Clin Neurol Neurosurg 2008; 110: Suzuki K, Takatsu T, Inoue H, Teramoto T, Ishida Y, Ohmori K. Redundant nerve roots of the cauda equina caused by lumbar spinal canal stenosis. Spine (Phila Pa 1976) 1992; 17: Hakan T, Celikoğlu E, Aydoseli A, Demir K. The redundant nerve root syndrome of the cauda equina. Turk Neurosurg 2008; 18: Borré DG, Borré GE, Aude F, Palmieri GN. Lumbosacral epidural lipomatosis: MRI grading. Eur Radiol 2003; 13: Kuhn MJ, Youssef HT, Swan TL, Swenson LC. Lumbar epidural lipomatosis: the Y sign of thecal sac compression. Comput Med Imaging Graph 1994; 18: Ishikawa Y, Shimada Y, Miyakoshi N, et al. Decompression of idiopathic lumbar epidural lipomatosis: diagnostic magnetic resonance imaging evaluation and review of the literature. J Neurosurg Spine 2006; 4: Lee S, Lee JW, Yeom JS, et al. A practical MRI grading system for lumbar foraminal stenosis. AJR 2010; 194: Bartynski WS, Lin L. Lumbar root compression in the lateral recess: MR imaging, conventional myelography, and CT myelography: comparison with surgical confirmation. AJNR 2003; 24: Wildermuth S, Zanetti M, Duewell S, et al. Lumbar spine: quantitative and qualitative assessment of positional (upright flexion and extension) MR imaging and myelography. Radiology 1998; 207: Bohndorf K, Imhof H, Fischer W. Radiologic diagnosis for bones and joints (in German). Stuttgart, Germany: Thieme, Aota Y, Niwa T, Yoshikawa K, Fujiwara A, Asada T, Saito T. Magnetic resonance imaging and magnetic resonance myelography in the presurgical diagnosis of lumbar foraminal stenosis. Spine 2007; 32: Weishaupt D, Zanetti M, Hodler J, Boos N. MR imaging of the lumbar spine: prevalence of intervertebral disk extrusion and sequestration, nerve root compression, end plate abnormalities, and osteoarthritis of the facet joints in asymptomatic volunteers. Radiology 1998; 209: Pfirrmann CWA, Dora C, Schmid MR, Zanetti M, Hodler J, Boos N. MR image based grading of lumbar nerve root compromise due to disk herniation: reliability study with surgical correlation. Radiology 2004; 230: Rothman SLG, Glenn WV Jr. Multiplanar CT of the spine. Baltimore, MD: University Park Press, Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: Mariconda M, Fava R, Gatto A, Longo C, Milano C. Unilateral laminectomy for bilateral decompression of lumbar spinal stenosis: a prospective comparative study with conservatively treated patients. J Spinal Disord Tech 2002; 15: Koc Z, Ozcakir S, Sivrioglu K, Gurbet A, Kucukoglu S. Effectiveness of physical therapy and epidural steroid injections in lumbar spinal stenosis. Spine 2009; 34: Genevay S, Atlas SJ, Katz JN. Variation in eligibility criteria from studies of radiculopathy due to a herniated disc and of neurogenic claudication due to lumbar spinal stenosis: a structured literature review. Spine 2010; 35: Pathria M, Sartoris DJ, Resnick D. Osteoarthritis of the facet joints: accuracy of oblique radiographic assessment. Radiology 1987; 164: Weishaupt D, Zanetti M, Boos N, Hodler J. MR imaging and CT in osteoarthritis of the lumbar facet joints. Skeletal Radiol 1999; 28: Stieber J, Quirno M, Cunningham M, Errico TJ, Bendo JA. The reliability of computed tomography and magnetic resonance imaging grading of lumbar facet arthropathy in total disc replacement patients. Spine 2009; 34:E833 E Coste J, Judet O, Barre O, Siaud JR, Cohen de Lara A, Paolaggi JB. Inter- and intraobserver variability in the interpretation of computed tomography of the lumbar spine. J Clin Epidemiol 1994; 47: Grenier N, Kressel HY, Schiebler ML, Grossman RI, Dalinka MK. Normal and degenerative posterior spinal structures: MR imaging. Radiology 1987; 165: Park JB, Chang H, Lee JK. Quantitative analysis of transforming growth factor beta 1 in ligamentum flavum of lumbar spinal stenosis and disc herniation. Spine (Phila Pa 1976) 2001; 26:E492 E Fardon DF, Milette PC; Combined Task Forces of the North American Spine Society, American Society of Spine Radiology, and American Society of Neuroradiology. Nomenclature and classification of lumbar disc pathology: recommendations of the combined task forces of the North American Spine Society, American Society of Spine Radiology, and American Society of Neuroradiology. Spine 2001; 26:E93 E Stephens MM, Evans JH, O Brien JP. Lumbar intervertebral foramens: an in vitro study of their shape in relation to intervertebral disc pathology. Spine (Phila Pa 1976) 1991; 16: Abbas J, Hamoud K, Peleg S, et al. Facet joints arthrosis in normal and stenotic lumbar spines. Spine (Phila Pa 1976) 2011; 36:E1541 E Fujiwara A, Tamai K, Yamato M, et al. The relationship between facet joint osteoarthritis and disc degeneration of the lumbar spine: an MRI study. Eur Spine J 1999; 8: Kunogi J, Hasue M. Diagnosis and operative treatment of intraforaminal and extraforaminal nerve root compression. Spine (Phila Pa 1976) 1991; 16: (Appendix follows on next page) AJR:201, November 2013 W745

12 Andreisek et al. APPENDIX 1: Semiquantitative or Qualitative Radiologic Criteria for Lumbar Spinal Stenosis Central stenosis Compression of the central spinal canal Obliteration of anterior CSF space a Nerve root sedimentation sign Hypertrophy of the ligamentum flavum a Redundant nerve roots of the cauda equina a Reduction of posterior epidural fat Epidural lipomatosis a Lateral stenosis Compression of the subarticular zone Nerve root compression in the lateral recess Foraminal stenosis Perineural intraforaminal fat a Hypertrophic facet joint degeneration a Compression of the foraminal zone Foraminal nerve root impingement Size and shape of the foramen a From the recently published Delphi survey [7]. W746 AJR:201, November 2013

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