Relative risk factors of nerve root sedimentation sign (SedSign) in patients with severe central lumbar spinal stenosis (LSS) Relative risk factors of nerve root sedimentation sign (SedSign) in patients with severe central...
Yu, Haiming; Han, Yunfeng; Zhang, Rui; Sun, Chu; Wang, Mingda; Yue, Bo; Chou, Kaiping; Li, Bin; Zhang, Nan
ALL LIFE 2023, VOL. 16, NO. 1, 2172460 https://doi.org/10.1080/26895293.2023.2172460 COMPUTATIONAL LIFE SCIENCES, BIOINFORMATICS AND SYSTEM BIOLOGY Relative risk factors of nerve root sedimentation sign (SedSign) in patients with severe central lumbar spinal stenosis (LSS) a b a a a a a a Haiming Yu , Yunfeng Han ,Rui Zhang ,Chu Sun , Mingda Wang ,BoYue , Kaiping Chou ,Bin Li and Nan a,c Zhang a b Second Aﬃliated Hospital of Qiqihar Medical College, Qiqihar, People’s Republic of China; Department of statistics, Qiqihar Medical College, Qiqihar, People’s Republic of China; Aﬃliated Xinhua Hospital of Dalian University, Dalian, People’s Republic of China ABSTRACT ARTICLE HISTORY Received 24 November 2021 The incidence of nerve root sedimentation sign (SedSign) was evaluated to explore potential patho- Accepted 7 January 2023 genesis in patients with severe lumbar spinal stenosis (LSS). In a total of 209 patients with severe LSS, 290 intervertebral levels were narrow, among which 248 showed a positive SedSign, giving a preva- KEYWORDS lence of 85.52%. Those levels with a positive SedSign were further analyzed relative to those with a Lumbar spinal stenosis (LSS); negative SedSign. There was no significant difference between the two groups for the cross-sectional nerve root sedimentation area (CSA) or the posteroanterior diameter (PAD). In contrast, there was a significant difference sign (Sedsign); diﬀerence between the groups for the grade of degenerative facet joint (DFJ) (p < 0.05), the thickness of cross-sectional area diﬀerence (CSAD); thickness ligamentum flavum (TLF) (p < 0.01), and the cross-sectional area difference (CSAD) (p < 0.01). In of ligamentum ﬂavum (TLF); addition, receiver operating characteristic (ROC) curves were used to identify associated factors. The grade of degenerative facet area under the ROC curve for PAD was 0.608 (p < 0.05), for DFJ was 0.634 (p < 0.05), for TLF was 0.74 joint (DFJ) (p < 0.01), and for CSAD was 0.911 (p < 0.01). In summary, a positive SedSign has notable advan- tages in assisting with the diagnosis of severe LSS. Compression of the dural sac from the rear may be the main risk factors of a positive SedSign. Introduction To improve the ability to diagnose LSS, Barz et al. (2010) introduced a new radiological index, the nerve Lumbar spinal stenosis (LSS) is represented by the root sedimentation sign (SedSign). The SedSign is a reduction of the lumbar spinal canal capacity, com- phenomenonvisibleinaxialMRIscans:whenapatient pression of the dural sac, and entrapment of nerve is in the supine position, an MRI scan shows that the roots, which collectively induce a series of clinical dys- lumbar nerveroots sediment,asaresultofgravity,to functionsinthe patient(Atlasetal. 2000; Verbiest 2001). Although patient history, clinical examination, thedorsalpartofthe duralsac in patients with no sus- electrophysiological analyses, and confirmatory imag- picion of LSS. In contrast, in patients with severe LSS, ing findings such as cross-sectional area (CSA) of the such sedimentation is almost always absent, this phe- dural sac (Schizas et al. 2010;Hiyamaetal. 2019)and nomenon being referred to as a positive sedimentation posteroanterior diameter (PAD) of the spinal canal sign. According to the report from Barz et al., the Sed- Sign is 94% sensitive and 100% specific for LSS, when (Haig et al. 2007) can be used to diagnose LSS, there are used in conjunction with the criteria of walking dis- currently no universally accepted diagnostic criteria tance ≤ 200 m and CSA of the dural sac ≤ 80 mm to for LSS (Fritz et al. 1997;Atlas et al. 2005; Kapural et al. define probable LSS cases (Barz et al. 2010). Another 2007). Because diagnosis of LSS is difficult when clin- research also showed that the sensitivity of the SedSign ical symptoms such as pain and functional limitations was 60–96% in postoperative spines (Tomkins-Lane often occur only during activity but disappear at rest, et al. 2013). All these studies suggest that a posi- imaging findings do not always correlate with clinical tive SedSign is a sensitive MRI parameter of patients symptoms (Alyas et al. 2008; Arabmotlagh et al. 2019). CONTACT Nan ZHANG firstname.lastname@example.org Second Aﬃliated Hospital of Qiqihar Medical College, No37, Zhonghua West Road, Jianhua District, Qiqihar, Heilongjiang Province 161000, People’s Republic of China Aﬃliated Xinhua Hospital of Dalian University, Dalian, Liaoning 116000, People’s Republic of China © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 H. YU ET AL. with LSS, especially patients with severe morphologi- axial T2-weighted images (thickness, 4 mm; 20% gap calspinalstenosis. size). All patients were imaged while in the standard A SedSign measurement is simple, intuitive, and supine position,withbothlegsstraight. Thescan- easy to obtain, and is considered a good indicator for ning range covered L1/2 to L5/S1, and the three scans the use of diagnosing severe LSS in clinical practice described above were acquired for each intervertebral (Macedo et al. 2013;Zhang et al. 2015). However, the level. We used a complete digital image storage area mechanism responsible for a positive SedSign is still measurement system (Accurad V4.0 software) to pro- not clear. What risk factors are related specifically to cess the obtained data. All MRI parameters for each the phenomenon of a positive SedSign? We hypothe- image scan were separately assessed by three radiolo- sized that a positive SedSign is associated with a change gistswho areexperienced independentinvestigators. in the dural sac at the level of intervertebral stenosis of Themeanvalue of thethree calculations wasusedas patients with LSS. To test our hypothesis, we investi- the measurement for further analysis. gated the incidence of a positive SedSign and corre- For each patient, the PAD of the spinal canal was lations with MRI parameters in patients with severe measured in the three MRI scans of narrow levels as LSS. the distance between the midpoint of the posterior margin of the disc and the midpoint of the posterior wall of the spinal canal (Figure 1a). The minimum Materials and methods PAD was used for further investigation as it is indica- tive of the narrowing of the spinal canal in the sagittal Participants plane. Thethickness of theligamentumflavum (TLF) This study was a retrospective review, which was wasmeasuredonaxial T2-weightedMRimagesat approved by the ethics committee of Qiqihar Medical the level of the facet joint as shown in Figure 1(b). College (reference number 201822). The MR images of The maximum TLF was determined as an indicator patients with severe LSS were obtained from our hospi- of dural sac posterior compression. In addition, the tal for individuals admitted for inpatient or outpatient lumbar facet joints were graded on both the left and treatment between January 2017 and June 2019, all of right side at levels L1/2, L2/3, L3/4, and L4/5, and then whom were consistent with LSS diagnostic criteria and the average value was used to determine the degenera- were assessed for eligibility based on the following cri- tive facet joint (DFJ) grade. Four grades of DFJ were teria: (1) a CSA of the dural sac of ≤ 80 mm for at least defined using criteria similar to those published by one level in an axial MRI scan; (2) typical intermittent Kalichman et al. (2008)and Weishauptetal. (1999); claudication, with or without lower back pain or leg these criteria are shown in Table 1. pain; and (3) walking distance ≤ 500 m. The exclusion criteria were as follows: (1) presence of lower extremity Definition of the maximum cross-sectional area arterial occlusive syndrome, lumbar tumor, multiple difference (CSAD) nerve injury, spinal trauma, or limited mobility caused by osteoarthritis; (2) presence of coronary thrombo- The CSA of the dural sac was measured based on sis or a previous stent surgery; (3) LSS at level L5/S1 the area bounded by the edge of the epidural sac was excluded because the S1 and S2 nerve roots leave (Figure 1a) in each narrow intervertebral level of the the dural sac in a ventral position, inhibiting sedimen- three MRI scans to determine the minimum CSA, tation to the dorsal part of the dural sac according to which represents the absolute compression of the dural Barz et al. (2010). sac. To describe thechangeinthe duralsac,weintro- duced the maximum cross-sectional area difference (CSAD) of the dural sac, which was calculated by MRI data acquisition subtractingthe minimumCSA measured across the A total of 627 patients who had undergone MRI exam- three scans at each level where stenosis had occurred ination of the lumbar spine were included in this from the maximum CSA; the difference represents the study. MRI scans were made with a magnetic reso- CSAD value for that particular level. A higher CSAD nanceinstrument(HITACHIechelon1.5 T,Japan)and value indicates a greater change in the dural sac at the consistedofsagittalT1- andT2-weighted images and level of narrowing. Conversely, a lower CSAD value ALL LIFE 3 Figure 1. Measurement of the cross-sectional area (CSA) of the dural sac and the posteroanterior diameter (PAD) of the spinal canal. b: Measurement of the thickness of the ligamentum ﬂavum (TLF) and the space of the facet joint (FJ) which can used to evaluate DFJ. Table 1. Criteria for grading degeneration of the facet joint. a disagreement between the raters, a consensus was reached between both investigators, who were assisted Grade Criteria by another experienced independent investigator as a 0 Normal facet joint space (2 − 4 mm wide) 1 Narrowing of the joint space (< 2 mm) and/or small third opinion. All imaged levels for each individual osteophytes and/or mild hypertrophy of the articular process were classified as having a positive or negative SedSign. 2 Narrowing of the joint space (< 1 mm) and/or moderate osteophytes and/or moderate hypertrophy of the articular process and/or mild subarticular bone erosions 3 Severe narrowing of the joint space and/or large osteophytes Statistical analysis and/or severe hypertrophy of the articular process and/or severe subarticular bone erosions and/or subchondral cysts Data are shown as the mean ± standard deviation. and/or vacuum phenomenon in the joints The t-test was applied for comparisons between the positive SedSign group and the negative group. The indicates a more gradual narrowing of the dural sac receiver operating characteristic (ROC) curve was under pressure. used to assess correlations between morbidity of pos- itive SedSign and parameters such as the minimum CSA, minimum PAD, maximum TLF, grade of DFJ, Determining the nerve root SedSign and maximum CSAD. SPSS18.0 software was used for all statistical analyses, and p < 0.05 was considered as Patients were rated by the other three investigators as statistically significant. SedSignpositiveornegativebasedontheirMRimages. In brief, a vertical line was drawn along the midpoint of the posteroanterior diameter of the spinal canal, and Results a horizontal line was drawn that divided the dural sac into an upperand lowerpartineachaxial T2-weighted According to the inclusion/exclusion criteria, 209 image. AnegativeSedSign wasdefinedashavingall patients were included in the current study, and their caudae equinae located in the lower part of the dural general information was shown in Table 2.There sac with the exception of the two ventral nerve roots were 84 males and 125 females, aged 57.3 ± 14.9 that exit caudal to the level at which the observations and 62.68 ± 11.06 years, respectively. There was no were made (Figure 2a). A positive SedSign was defined significant difference in Oswestry Disability Index as an absence of cauda equina sedimentation because (ODI) and walking distance between male and female of the tight canal, a result of the distortion of the dural patients, but a significant difference in BMI was found. sac, with the majority of nerve roots located in the Among these patients, 290 intervertebral levels were upper part of the sac (Figure 2b). Where there was identified as having severe LSS, which included 248 4 H. YU ET AL. Figure 2. A negative SedSign was deﬁned as having all caudae equinae located in the lower part of the horizontal red dashed line with the exception of the two ventral nerve roots that exit caudal to the level at which the image was taken. b: A positive SedSign was deﬁned as an absence of cauda equina sedimentation, and a ‘squashing’ of the dural sac, with the majority of nerve roots located above the horizontal red dashed line. The horizontal dashed line passes through the midpoint of the posteroanterior diameter of the spinal canal (the red solid line). Table 2. The general information of 209 patients with severe LSS. Claudication Cases Age BMI ODI distance Male 84 65.3 ± 12.32 27.83 ± 2.05∗ 65.36 ± 15.29 220 ± 164.2 Female 125 63.74 ± 13.66 24.68 ± 1.96 63.95 ± 13.26 239.7 ± 198.1 ∗p < 0.05. Table 3. Distribution of a positive SedSign across 290 levels of difference in the maximum TLF and the grade of DFJ, LSS. and the maximum CSAD (p < 0.05). SedSign SedSign To evaluate any correlations between a positive Sed- Distribution Levels of LSS (positive) (negative) Morbidity Sign and the above parameters, we further studied L1/2 level 2 2 0 100% the sensitivity between the prevalence of a positive L2/3 level 12 12 0 100% L3/4 level 87 76 11 87.36% SedSign and these parameters with the ROC curve L4/5 level 189 158 31 83.60% method (Figure 4). Our results suggested that there Total 290 248 42 85.52% is no obvious correlation between the prevalence of a positive SedSign and minimum CSA (p > 0.05). How- ever, the prevalence was moderately correlated with intervertebral levels with a positive SedSign and 42 lev- minimum PAD and DFJ (p < 0.05). Finally, significant els with a negative SedSign. The occurrence of positive and negative SedSign measurements at different inter- correlation was observed between the prevalence of a vertebral levels for the 290 levels with severe LSS is positive SedSign and the maximum TLF and CSAD shown in Table 3.The prevalence of apositiveSedSign (p < 0.01). was 85.52% for all levels. We then compared several parameters, including Discussion minimum PAD and CSA, DFJ, maximum TLF and CSAD, between the levels with a positive SedSign Here we conducted a retrospective study to evaluate (n = 248) and those with a negative SedSign (n = 42), the lumbar MR images of 209 patients with severe LSS, and the results are shown in Figure 3. Between the including 84 male and 125 female patients. We found positiveandnegativeSedSigngroups,therewasnosig- no significant difference in average age and ODI, and nificant difference with respect to the minimum PAD in particular, no significant difference could be found and CSA (p > 0.05). However, there was a significant in walking distance, between male and female with ALL LIFE 5 Figure 3. The MRI parameters were evaluated between the positive SedSign group and the negative SedSign group. a: The minimum CSA. b: The minimum PAD. c: The maximum TLF. d: The grade of DFJ. e: The maximum CSAD. ∗p < 0.05 and ∗∗p < 0.01. severe LSS. However, we found a significant difference 85.52% in this study. Our results suggested a positive in BMI between the two, which may be due to gender SedSign was most common in the lower lumbar spine, differences between male and female. In total, 290 lum- which is consistent with the segments that show a high bar sections were diagnosed as severe LSS based on our incidence of LSS (Binder et al. 2002;Wuand Cruz inclusion criteria, and 248 intervertebral discs were 2020). Thus, our results suggested that a positive Sed- assigned to the positive SedSign group. There were Sign should be used as an image parameter for the only 2 sections at the L1/2 level and 12 at the L2/3 level diagnosis of and screening for LSS in clinical practice. diagnosed as severe LSS, all of which were assessed as Although the SedSign has been reported to have having positive SedSign (100%). Meanwhile, the inci- high diagnostic sensitivity, specificity, and efficacy, and dence of a positive SedSign was 76 in 87 L3/4 levels good clinical application value for the diagnosis of LSS (87.36%) and 158 in 189 L4/5 levels (83.6%). There- (Barz et al. 2010;Macedoetal. 2013;Tomkins-Lane fore, the overall incidence of a positive SedSign was et al. 2013;Zhang et al. 2015), the pathogenesis and 6 H. YU ET AL. considered that the CSA could be insufficient as a diag- nostic tool (Staub et al. 2011;Piechotaetal. 2019). Lohman et al. (2006) confirmed that the degree of LSS andtheCSAoftheduralsachadnosignificantcorrela- tion with the severity of clinical symptoms. Our results also showed that the minimum CSA was not signif- icantly different between the positive SedSign group and the negative SedSign group; at the same time, the ROC curve also showed that there was no significant correlation between the prevalence of a positive Sed- Sign and the minimum CSA. Thus, it is also believed that the CSA of the dural sac and PAD of the spinal canal cannot fully explain the involvement of nerves in LSS due to the great individual differences. Figure 4. Correlation between the prevalence of a positive Sed- To further investigate the possible pathogenesis that Sign and grade of DF, maximum TLF and CSAD, minimum CSA leads to a positive SedSign, we conducted a novel radi- and PAD. The area under the ROC curve (AUC) for the grade of ological parameter, the maximum CSAD of the dural DFJ was 0.634 (a line, 95% CI: 0.576 − 0.69, p < 0.05). The AUC sac, to describe the narrowing change of the dural sac. for maximum CSAD was 0.913 (b line, 95% CI: 0.875 − 0.943, p < 0.01). The AUC for maximum TLF were 0.793 (c line, 95% CI: In the present study, we observed the sagittal and axial 0.742 − 0.839, p < 0.01). The AUC for minimum CSA was 0.543 (d MR images of the patients with severe LSS who were line, 95% CI: 0.484 − 0.601, p > 0.05). The AUC for minimum PAD determined as having a positive SedSign at the L4/5 was 0.608 (e line, 95% CI: 0.55 − 0.665, p < 0.05). level (Figure 5). The dural sac was pushed ventrally or toward the center of the spinal canal by posterior compression in the region where the most severe nar- correlated risk factors of positive SedSign were still rowing occurred (Figure 5c), and the CSA was at its unclear. As well known, the PAD of spinal canal, as minimuminthisscanimage.However,the duralsac a linear indicator of the spinal canal, is measured as at the adjacent sites was less compressed, as shown the distance from the midpoint of the anterior wall in Figure 5(b), and the corresponding CSA was more to the midpoint of the posterior wall, and was used normal. The maximum CSAD of the dural sac was to assess the degree of spinal stenosis in the sagit- large, which indicated an acute change in the dural sac tal plane (Sheldom et al. 1976). In the present study, between the narrowest section and the normal section. we found that there was no significant difference in Asaresult, thenerve rootswerepulledtowardthe the PAD between the positive and negative SedSign center of the spinal canal and a positive SedSign was groups, although the ROC curve for the PAD showed observed on theMRimage.Incontrast,when themax- a mid-correlation between a positive SedSign and the imum CSAD was small, there was only minor variation PAD. We considered that the main reason may be the in the dural sac between the level at which narrow- physiologically invalid cavity filled with adipose tis- ing occurred and normal levels, resulting in minimal sue existing between the posterior of the dural sac and displacement of the nerve roots and the absence of a the posterior wall of the spinal canal, which may affect positive SedSign in the MR image at the levels adjacent the PAD of the spinal canal to reefl ct the degree of to the stenosis. Meanwhile, significant differences also spinal canal stenosis eeff ctively. In addition, the CSA were observed in the maximum CSAD between the of the dural sac, as the spinal canal area parameter, was positive group and the negative group, and the ROC superior to vertebral canal diameter line parameters curve result also showed that there was the highest cor- in diagnosing LSS (Hamanishi et al. 1994). Due to the relation between the maximum CSAD and incidence characteristics of the spinal canal morphology, some rate of positive SedSign. All these results suggested that degenerative changes occur in the non-midline part of thepositiveSedSign is more closelyrelated to achange the spinal canal, often inducing lateral recess stenosis in the dural sac caused by posterior compression at the andfinallyleadtoreduction in spinal canalvolume level of stenosis, which may be the main reason for the (Hamanishi et al. 1994). However, some researchers appearance of sedimentation syndrome. ALL LIFE 7 Figure 5. The relationship between a positive SedSign and a change in the CSA of the dural sac at the level of stenosis. a: A sagittal T2- weighted image of L4/5 shows compression of the dural sac because of substantial narrowing in the third MRI scan. b: The ﬁrst transverse layer of level L4/5, at which point the dural sac was lightly compressed, and there was minimal tendency of the neve roots or cauda equina to move ventrally or toward the center of the spinal canal. A suggestion of a positive SedSign was observed, although not deﬁnitively. c: The second transverse layer of level L4/5 OR MR image, at which point the narrowing of the dural sac was increased, the nerve roots were shifted substantially, and a positive SedSign was present. d: The third transverse layer of level L4/5 showed the greatest stenosis. Because of the narrowing of the canal, the nerves were ‘‘squashed’’ and therefore present on both sides of the equator, such that a positive SedSign was apparent. To verify the hypothesis, two posterolateral param- cord (Karavelioglu et al. 2016). They have been con- eters, thickness of ligamentum flavum (TLF) and firmedtohaveimportant rolesinthe development degeneration of facet joint (DFJ), were further assessed of LSS (Fukuyama et al. 1995; Sakamaki et al. 2009; as to their correlation with the positive SedSign. The Zhang et al. 2010). TLF and DFJ can induce a decrease ligamentum flavum and facet joint are the main struc- in the central tube volume by compression from the tures that make up the posterior and lateral spinal behind the dural sac, which is the cause of LSS (Wess- canal walls, and have a protective eeff ct on the spinal berg and Frennered 2017;Anetal. 2018;Nakashima 8 H. YU ET AL. et al. 2019). Therefore, we analyzed the TLF and DFJ with other criteria. The prevalence of a positive Sed- between the two groups and found a significant dif- Sign showed a higher correlation with changes in the ference for each of these parameters between the posi- compression of the dural sac relative to other imag- tive and negative groups. In addition, The ROC curve ing parameters. Compression from the posterior spinal result also showed that a positive SedSign was signifi- canal, such as thickening of the ligamentum flavum cantly correlated with the grade of DFJ and the TLF. All and facet joint degeneration, may be the main cause these demonstrated that a positive SedSign was highly of a positive SedSign. related to risk factors from the posterior spinal canal. This wouldalsoexplain whythere is adieff rentpreva- Author contributions statement lence of a positive SedSign between cases of severe LSS andmoderate/mildLSS. Thechangeofcompressed Conception and design of the research: Nan ZHANG dural sac was less in patients with mild-to-moderate and Yunfeng HAN; acquisition of data: Haiming YU, LSS, and for whom the MR images rarely show a posi- Rui ZHANG, Chu SUN, and Bo YUE; analysis and tive SedSign. However, when the dural sac (nerve roots interpretation of data: Haiming YU, Rui ZHANG, Chu or the cauda equina) was obviously squeezed from the SUN, Bo YUE, Mingda WANG, Kaiping CHOU, and posterior side and moved sharply toward the center of Bin LI; statistical analysis: Yunfeng HAN; drafting the spinal canal or ventrally at the level where stenosis the manuscript: Haiming YU; revision of manuscript occurred, the adjacent unaec ff ted O nerve roots (or the for important intellectual content: Nan ZHANG. All cauda equina) were also pulled to shift to the center of authors read and approved the final manuscript. the spinal canal or ventrally, and a positive SedSign was observed in MR images. Barz et al. (2014)reportedthat Disclosure statement a positive SedSign was more common when the epidu- No potential conflict of interest was reported by the author(s). ral pressure was increased in LSS patients, which also indirectly supports our results. Of course, as LSS develops from complex patho- Funding physiological changes, there are many factors that can This work was financially supported by the Doctoral Research decrease the volume of the spinal canal, such as lum- Funding of Qiqihar Medical College (QMSI201901) and bar kyphosis (Jung et al. 2018;Parketal. 2018), loss Clinical Research Project of Heilongjiang Health Commission (2019-026). of physiological lordosis (Celestre 2018), giant central lumbar disc herniation (Ammar et al. 2018;Tulloch and Papadopoulos 2018), and lateral recess stenosis Data availability statement (Raja et al. 2020), and can result in typical clinical Thedatathatsupport thefindings of this studyare availablein symptoms of LSS. Not all LSS cases will show a positive https://data.mendeley.com/datasets/w5p4n7rhwy/1. SedSign, which suggests that there are limitations of SedSign determination in clinical practice. In addition, References in the current study, we focused only on the distri- bution of SedSign in patients with severe LSS. The Alyas F, Connell D, Saifuddin A. 2008. Upright positional MRI of the lumbar spine. Clin Radiol. 63:1035–1048. validity of this theory on a wider scale is not currently Ammar A, Zarnegar R, Yassari R1, Kinon M. Large central lum- known. Further study is needed to determine the dis- bar disc herniation causing acute cauda equina syndrome tribution of a positive SedSign among patients with with loss of evoked potentials during prone positioning for mild-to-moderate LSS. surgery. Surg Neurol Int. 2018; 9:66. AnSJ,MunJU,KangKN,KimYU. 2018. 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