Eur Spine J DOI 10.1007/s00586-015-4049-0
ORIGINAL ARTICLE
Does lumbar spinal stenosis increase the risk of spondylotic cervical spinal cord compression? Blanka Adamova1,2 • Josef Bednarik1,2 • Tereza Andrasinova1 • Ivana Kovalova1,2 • Roman Kopacik1,2 • Michal Jabornik1 • Milos Kerkovsky2,3 • Barbora Jakubcova3 • Jiri Jarkovsky4
Received: 16 December 2014 / Revised: 21 April 2015 / Accepted: 23 May 2015 Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The aim of this prospective cross-sectional observational comparative study was to determine the prevalence of spondylotic cervical cord compression (SCCC) and symptomatic cervical spondylotic myelopathy (CSM) in patients with symptomatic lumbar spinal stenosis (LSS) in comparison with a general population sample and to seek to identify predictors for the development of CSM. Methods A group of 78 patients with LSS (48 men, median age 66 years) was compared with a randomly selected age- and sex-matched group of 78 volunteers (38 men, median age 66 years). We evaluated magnetic resonance imaging findings from the cervical spine and neurological examination. Results The presence of SCCC was demonstrated in 84.6 % of patients with LSS, but also in 57.7 % of a sample of volunteers randomly recruited from the general population. Clinically symptomatic CSM was found in 16.7 % of LSS patients in comparison with 1.3 % of volunteers (p = 0.001). Multivariable logistic regression proposed the Oswestry Disability Index of 43 % or more as the only independent predictor of symptomatic CSM in LSS patients (OR 9.41, p = 0.008). & Blanka Adamova [email protected] 1
Department of Neurology, University Hospital and Masaryk University Brno, Jihlavska 20, 625 00 Brno, Czech Republic
2
CEITEC-Central European Institute of Technology, Masaryk University, Brno, Czech Republic
3
Department of Radiology, University Hospital and Masaryk University Brno, Jihlavska 20, 625 00 Brno, Czech Republic
4
Institute of Biostatistics and Analyses, Masaryk University, Kamenice 3, 625 00 Brno, Czech Republic
Conclusions The presence of symptomatic LSS increases the risk of SCCC; the prevalence of SCCC is higher in patients with symptomatic LSS in comparison with the general population, with an evident predominance of more serious types of MRI-detected compression and a clinically symptomatic form (CSM). Symptomatic CSM is more likely in LSS patients with higher disability as assessed by the Oswestry Disability Index. Keywords Lumbar spinal stenosis Cervical stenosis Cervical cord compression Cervical myelopathy Tandem stenosis Abbreviations ASCCC Asymptomatic spondylotic cervical cord compression CSM Cervical spondylotic myelopathy CSR Cervical spondylotic radiculopathy LSS Lumbar spinal stenosis MRI Magnetic resonance imaging ODI Oswestry Disability Index OR Odds ratio ROC Receiver operating characteristic SCCC Spondylotic cervical cord compression
Introduction Spondylosis frequently affects not just one segment of the spine; it is generally more widespread. The most commonly affected regions are the lumbar and cervical spine [1]. Concurrent cervical and lumbar stenosis is usually recorded as ‘‘tandem stenosis’’. Dagi et al. [2] noted that tandem stenosis is characterized by the triad of neurogenic claudication, progressive gait disturbance and findings of
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Eur Spine J
mixed myelopathy and polyradiculopathy in both the upper and lower extremities. Tandem stenosis should therefore be borne in mind for patients with gait disturbance, weakness of the lower extremities and upper and lower motor neuron lesions of the lower extremities and the cervical and lumbar segments of spine should be investigated, preferably by means of magnetic resonance imaging (MRI). Determination of the more clinically symptomatic segment may well have an influence on choice of optimal therapy. There are no exact epidemiological data on the prevalence of tandem stenosis and that information which exists varies widely. The prevalence of tandem stenosis in a cadaveric study of the general population performed by Lee et al. [3] ranged from 0.9 to 5.4 %; it was calculated at 2.05 % by Bajwa et al. [4]. The association of degenerative changes and congenital stenosis of the cervical and lumbar spine implies that stenosis in one part of the spine positively predicts development of stenosis in the other [3–5]. Clinically symptomatic tandem stenosis has been diagnosed in 3.4 % of patients undergoing surgery for spinal stenosis [6], while other authors describe the prevalence of symptomatic tandem stenosis at around 5 % in patients with spinal stenosis [1]. Lee et al. [7] reported moderate or severe asymptomatic cervical cord compression in 24 % of lumbar stenosis patients. The aim of this prospective study was to determine the prevalence of MRI-detected spondylotic cervical cord compression (SCCC) that could be either asymptomatic or could manifest itself as symptomatic CSM in a cohort of patients with symptomatic LSS in comparison with a randomly selected age- and sex-matched population sample. In addition, predictors for the development of CSM in LSS patients were also sought.
•
• •
Presence of central LSS (an osteoligamentous narrowing of the lumbar spinal canal) at one level at least, established by MRI. The presence of central stenosis on MRI of the lumbar spine was considered in morphological terms as encroachment on the thecal sac with compression of nervous structures. The MRI scans were assessed by an experienced neuroradiologist. Absence of isolated herniated nucleus pulposus and isolated lateral or foraminal stenosis. Correlation between clinical and radiological findings.
In total, 78 patients (48 men, 30 women) with LSS were included into the analysis. An MRI of the cervical spine was performed unless patients had a history of surgically addressed CSM (4 patients). All the LSS patients were specifically examined for clinical symptoms/signs of CSM and/or CSR. The presence of clinically manifested cervical myelopathy known before the entry into the study was also investigated. Also established was the number of stenotic levels in the lumbar spine (by MRI), the presence/absence of neurogenic claudication, and the Oswestry Disability Index. Control group
Patients with clinically symptomatic LSS examined in our Department of Neurology within a period of 4 months (October 2013–January 2014) were included in this study.
For recruitment of volunteers, we used three-level method of intentional sampling by trained recruiter. First step included random choice of residence within South Moravian region (with equivalent representation of towns and villages). The choice of household was then done using random walk method [8]. The choice of volunteer within the approached family was done with respect to equivalent representation of gender, type of occupation (physically demanding vs. sedentary) and representation of decades above the age of forty. The primary data included 89 volunteers. Preliminary analysis, however, revealed that the volunteer/LSS patient sample structure was unbalanced in terms of sex. Propensity score matching based on logistic regression with age and sex as covariates was therefore employed to obtain a fully balanced dataset prior to further analyses, reducing the numbers of volunteers to 78 (38 men, 40 women) (see Fig. 1 for subject recruitment). MRIs of the cervical spine were performed (see below). Volunteers with radiological spondylotic cervical cord compression revealed on MRI were examined by a neurologist to assess clinical symptoms/signs of CSM and/or CSR.
Inclusion criteria
MRI of cervical and lumbar spine
•
All examinations were performed on a 1.5-T MR scanner. The protocol of cervical spine MRI involved conventional sequences for the evaluation of the spine and spinal cord
Materials and methods The study was reviewed and approved by the local medical research ethics committee. Informed and signed consent was given in writing by all subjects. Patients with lumbar spinal stenosis
Clinically symptomatic LSS (neurogenic claudication and/or radicular pain, e.g., low back pain radiating below the knee to one or both lower limbs).
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Eur Spine J
and 5th–95th percentile range. The statistical significance of differences between groups was expressed in terms of Fisher’s exact test or maximum likelihood Chi-square test for categorical variables, while the non-parametric Mann–Whitney U test was employed for continuous variables. The diagnostic power of potential predictors of clinically symptomatic spondylotic cervical myelopathy in LSS was assessed by means of ROC curves and described using AUC (area under the curve) and its statistical significance; optimal cut-offs were identified using a combination of their sensitivity and specificity. Univariable and multivariable logistic regression were applied to assess association of the predictive factors examined and the risk endpoint (i.e., binary coded to the presence of clinically symptomatic CSM). Odds ratios at 95 % confidence limits were calculated and tested using Wald’s test. The final multivariable model consisted of statistically significant variables in univariable analysis combined with age and sex forced into the model. Analysis was computed by SPSS 22 (IBM Corporation, 2013); a = 0.05 was adopted as the level of statistical significance in all analyses. Fig. 1 Study flowchart, including subject recruitment
morphology, including T1, T2 and STIR (short-tau inversion recovery) images in the sagittal plane and axial T2weighted gradient-echo scans coherently covering five segments of cervical spine from C2/C3 to C6/C7 levels. The clinical status of patients/volunteers was blinded for a neuroradiologist who evaluated cervical spine MRIs. For classification of cervical cord compression, we used a modification of the grading system proposed by Shimomura et al. [9], Teresi et al. [10] and Yu et al. [11]. Spondylotic cervical cord compression was classified as impingement, i.e., focal concave defect of the spinal cord contour with at least partially preserved subarachnoid space (type I); flat spinal cord compression with either partial obliteration of subarachnoid space (type IIa); or with diminished subarachnoid space (type IIb). On the T2 gradient-echo axial scans the lowest sagittal spinal canal diameter and the level at which it occurred were recorded. Any abnormal T2 hyperintensity of the spinal cord was also noted. The protocol of lumbar spine MRI comprised T1, T2 and STIR sequences in the sagittal plane and axial T2weighted scans covering the intervertebral segments with spinal canal stenosis. Statistical approaches Standard robust summary statistics were used to describe primary data: relative and absolute frequencies, median
Results Prevalence of ASCCC and CSM The prevalence of ASCCC, CSM and CSR was assessed and compared in LSS patients and the control group of volunteers. The basic characteristics (age, sex) of LSS patients and controls appear in Tables 1 and 2. Table 1 is compiled from all volunteers (primary data), while Table 2 derives from the matched data of volunteers (see above). The balance of volunteers in terms of sex had no significant effect on radiological and clinical data relevant to SCCC. Data from the matched group of volunteers were used for further analysis. SCCC was disclosed by MRI in 66 patients (84.6 %) with LSS and in 45 (57.7 %) volunteers. The difference is highly statistically significant (p \ 0.001). The lowest sagittal cervical spinal canal diameter was lower (median 8.4 mm) in LSS patients than in volunteers (median 9.8 mm, p \ 0.001). The lowest sagittal spinal canal diameter was found in both groups at C5/6 level (52.6 % of volunteers, 44.9 % of LSS patients). Abnormal T2 hyperintensity of the cervical cord occurred more frequently in LSS patients (13.5 % vs. 3.8 %, p = 0.043). The frequency of single compression types appears in Fig. 2; LSS patients had more serious types of compression (p = 0.006). Figure 3a–d shows the results for tandem stenosis on MRI (SCCC in LSS patients).
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Eur Spine J Table 1 Comparison of LSS patients and volunteer control group—primary data Parameter
Volunteers (N = 89)
Agea
65.0 (42.0–77.0)
66.0 (53.0–82.0)
0.594
Sex, maleb
38 (42.7 %)
48 (61.5 %)
0.015
50 (56.2 %)
66 (84.6 %)
ORIGINAL ARTICLE
Does lumbar spinal stenosis increase the risk of spondylotic cervical spinal cord compression? Blanka Adamova1,2 • Josef Bednarik1,2 • Tereza Andrasinova1 • Ivana Kovalova1,2 • Roman Kopacik1,2 • Michal Jabornik1 • Milos Kerkovsky2,3 • Barbora Jakubcova3 • Jiri Jarkovsky4
Received: 16 December 2014 / Revised: 21 April 2015 / Accepted: 23 May 2015 Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The aim of this prospective cross-sectional observational comparative study was to determine the prevalence of spondylotic cervical cord compression (SCCC) and symptomatic cervical spondylotic myelopathy (CSM) in patients with symptomatic lumbar spinal stenosis (LSS) in comparison with a general population sample and to seek to identify predictors for the development of CSM. Methods A group of 78 patients with LSS (48 men, median age 66 years) was compared with a randomly selected age- and sex-matched group of 78 volunteers (38 men, median age 66 years). We evaluated magnetic resonance imaging findings from the cervical spine and neurological examination. Results The presence of SCCC was demonstrated in 84.6 % of patients with LSS, but also in 57.7 % of a sample of volunteers randomly recruited from the general population. Clinically symptomatic CSM was found in 16.7 % of LSS patients in comparison with 1.3 % of volunteers (p = 0.001). Multivariable logistic regression proposed the Oswestry Disability Index of 43 % or more as the only independent predictor of symptomatic CSM in LSS patients (OR 9.41, p = 0.008). & Blanka Adamova [email protected] 1
Department of Neurology, University Hospital and Masaryk University Brno, Jihlavska 20, 625 00 Brno, Czech Republic
2
CEITEC-Central European Institute of Technology, Masaryk University, Brno, Czech Republic
3
Department of Radiology, University Hospital and Masaryk University Brno, Jihlavska 20, 625 00 Brno, Czech Republic
4
Institute of Biostatistics and Analyses, Masaryk University, Kamenice 3, 625 00 Brno, Czech Republic
Conclusions The presence of symptomatic LSS increases the risk of SCCC; the prevalence of SCCC is higher in patients with symptomatic LSS in comparison with the general population, with an evident predominance of more serious types of MRI-detected compression and a clinically symptomatic form (CSM). Symptomatic CSM is more likely in LSS patients with higher disability as assessed by the Oswestry Disability Index. Keywords Lumbar spinal stenosis Cervical stenosis Cervical cord compression Cervical myelopathy Tandem stenosis Abbreviations ASCCC Asymptomatic spondylotic cervical cord compression CSM Cervical spondylotic myelopathy CSR Cervical spondylotic radiculopathy LSS Lumbar spinal stenosis MRI Magnetic resonance imaging ODI Oswestry Disability Index OR Odds ratio ROC Receiver operating characteristic SCCC Spondylotic cervical cord compression
Introduction Spondylosis frequently affects not just one segment of the spine; it is generally more widespread. The most commonly affected regions are the lumbar and cervical spine [1]. Concurrent cervical and lumbar stenosis is usually recorded as ‘‘tandem stenosis’’. Dagi et al. [2] noted that tandem stenosis is characterized by the triad of neurogenic claudication, progressive gait disturbance and findings of
123
Eur Spine J
mixed myelopathy and polyradiculopathy in both the upper and lower extremities. Tandem stenosis should therefore be borne in mind for patients with gait disturbance, weakness of the lower extremities and upper and lower motor neuron lesions of the lower extremities and the cervical and lumbar segments of spine should be investigated, preferably by means of magnetic resonance imaging (MRI). Determination of the more clinically symptomatic segment may well have an influence on choice of optimal therapy. There are no exact epidemiological data on the prevalence of tandem stenosis and that information which exists varies widely. The prevalence of tandem stenosis in a cadaveric study of the general population performed by Lee et al. [3] ranged from 0.9 to 5.4 %; it was calculated at 2.05 % by Bajwa et al. [4]. The association of degenerative changes and congenital stenosis of the cervical and lumbar spine implies that stenosis in one part of the spine positively predicts development of stenosis in the other [3–5]. Clinically symptomatic tandem stenosis has been diagnosed in 3.4 % of patients undergoing surgery for spinal stenosis [6], while other authors describe the prevalence of symptomatic tandem stenosis at around 5 % in patients with spinal stenosis [1]. Lee et al. [7] reported moderate or severe asymptomatic cervical cord compression in 24 % of lumbar stenosis patients. The aim of this prospective study was to determine the prevalence of MRI-detected spondylotic cervical cord compression (SCCC) that could be either asymptomatic or could manifest itself as symptomatic CSM in a cohort of patients with symptomatic LSS in comparison with a randomly selected age- and sex-matched population sample. In addition, predictors for the development of CSM in LSS patients were also sought.
•
• •
Presence of central LSS (an osteoligamentous narrowing of the lumbar spinal canal) at one level at least, established by MRI. The presence of central stenosis on MRI of the lumbar spine was considered in morphological terms as encroachment on the thecal sac with compression of nervous structures. The MRI scans were assessed by an experienced neuroradiologist. Absence of isolated herniated nucleus pulposus and isolated lateral or foraminal stenosis. Correlation between clinical and radiological findings.
In total, 78 patients (48 men, 30 women) with LSS were included into the analysis. An MRI of the cervical spine was performed unless patients had a history of surgically addressed CSM (4 patients). All the LSS patients were specifically examined for clinical symptoms/signs of CSM and/or CSR. The presence of clinically manifested cervical myelopathy known before the entry into the study was also investigated. Also established was the number of stenotic levels in the lumbar spine (by MRI), the presence/absence of neurogenic claudication, and the Oswestry Disability Index. Control group
Patients with clinically symptomatic LSS examined in our Department of Neurology within a period of 4 months (October 2013–January 2014) were included in this study.
For recruitment of volunteers, we used three-level method of intentional sampling by trained recruiter. First step included random choice of residence within South Moravian region (with equivalent representation of towns and villages). The choice of household was then done using random walk method [8]. The choice of volunteer within the approached family was done with respect to equivalent representation of gender, type of occupation (physically demanding vs. sedentary) and representation of decades above the age of forty. The primary data included 89 volunteers. Preliminary analysis, however, revealed that the volunteer/LSS patient sample structure was unbalanced in terms of sex. Propensity score matching based on logistic regression with age and sex as covariates was therefore employed to obtain a fully balanced dataset prior to further analyses, reducing the numbers of volunteers to 78 (38 men, 40 women) (see Fig. 1 for subject recruitment). MRIs of the cervical spine were performed (see below). Volunteers with radiological spondylotic cervical cord compression revealed on MRI were examined by a neurologist to assess clinical symptoms/signs of CSM and/or CSR.
Inclusion criteria
MRI of cervical and lumbar spine
•
All examinations were performed on a 1.5-T MR scanner. The protocol of cervical spine MRI involved conventional sequences for the evaluation of the spine and spinal cord
Materials and methods The study was reviewed and approved by the local medical research ethics committee. Informed and signed consent was given in writing by all subjects. Patients with lumbar spinal stenosis
Clinically symptomatic LSS (neurogenic claudication and/or radicular pain, e.g., low back pain radiating below the knee to one or both lower limbs).
123
Eur Spine J
and 5th–95th percentile range. The statistical significance of differences between groups was expressed in terms of Fisher’s exact test or maximum likelihood Chi-square test for categorical variables, while the non-parametric Mann–Whitney U test was employed for continuous variables. The diagnostic power of potential predictors of clinically symptomatic spondylotic cervical myelopathy in LSS was assessed by means of ROC curves and described using AUC (area under the curve) and its statistical significance; optimal cut-offs were identified using a combination of their sensitivity and specificity. Univariable and multivariable logistic regression were applied to assess association of the predictive factors examined and the risk endpoint (i.e., binary coded to the presence of clinically symptomatic CSM). Odds ratios at 95 % confidence limits were calculated and tested using Wald’s test. The final multivariable model consisted of statistically significant variables in univariable analysis combined with age and sex forced into the model. Analysis was computed by SPSS 22 (IBM Corporation, 2013); a = 0.05 was adopted as the level of statistical significance in all analyses. Fig. 1 Study flowchart, including subject recruitment
morphology, including T1, T2 and STIR (short-tau inversion recovery) images in the sagittal plane and axial T2weighted gradient-echo scans coherently covering five segments of cervical spine from C2/C3 to C6/C7 levels. The clinical status of patients/volunteers was blinded for a neuroradiologist who evaluated cervical spine MRIs. For classification of cervical cord compression, we used a modification of the grading system proposed by Shimomura et al. [9], Teresi et al. [10] and Yu et al. [11]. Spondylotic cervical cord compression was classified as impingement, i.e., focal concave defect of the spinal cord contour with at least partially preserved subarachnoid space (type I); flat spinal cord compression with either partial obliteration of subarachnoid space (type IIa); or with diminished subarachnoid space (type IIb). On the T2 gradient-echo axial scans the lowest sagittal spinal canal diameter and the level at which it occurred were recorded. Any abnormal T2 hyperintensity of the spinal cord was also noted. The protocol of lumbar spine MRI comprised T1, T2 and STIR sequences in the sagittal plane and axial T2weighted scans covering the intervertebral segments with spinal canal stenosis. Statistical approaches Standard robust summary statistics were used to describe primary data: relative and absolute frequencies, median
Results Prevalence of ASCCC and CSM The prevalence of ASCCC, CSM and CSR was assessed and compared in LSS patients and the control group of volunteers. The basic characteristics (age, sex) of LSS patients and controls appear in Tables 1 and 2. Table 1 is compiled from all volunteers (primary data), while Table 2 derives from the matched data of volunteers (see above). The balance of volunteers in terms of sex had no significant effect on radiological and clinical data relevant to SCCC. Data from the matched group of volunteers were used for further analysis. SCCC was disclosed by MRI in 66 patients (84.6 %) with LSS and in 45 (57.7 %) volunteers. The difference is highly statistically significant (p \ 0.001). The lowest sagittal cervical spinal canal diameter was lower (median 8.4 mm) in LSS patients than in volunteers (median 9.8 mm, p \ 0.001). The lowest sagittal spinal canal diameter was found in both groups at C5/6 level (52.6 % of volunteers, 44.9 % of LSS patients). Abnormal T2 hyperintensity of the cervical cord occurred more frequently in LSS patients (13.5 % vs. 3.8 %, p = 0.043). The frequency of single compression types appears in Fig. 2; LSS patients had more serious types of compression (p = 0.006). Figure 3a–d shows the results for tandem stenosis on MRI (SCCC in LSS patients).
123
Eur Spine J Table 1 Comparison of LSS patients and volunteer control group—primary data Parameter
Volunteers (N = 89)
Agea
65.0 (42.0–77.0)
66.0 (53.0–82.0)
0.594
Sex, maleb
38 (42.7 %)
48 (61.5 %)
0.015
50 (56.2 %)
66 (84.6 %)
