Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography

Journal of Clinical Neuroscience xxx (xxxx) xxx

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Clinical study

Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography Mitsunori Ozaki a,⇑, Kazuya Nishioka b, Mari Kitayama a, Takumi Kawaguchi a, Naoyuki Nakao a a b

Department of Neurological Surgery, Wakayama Medical University, 811-1 Kimiidera, Wakayama 641-0012, Japan Kyoto Kihara Hospital, 25 Tohji Higashimonzencho, Minami-ku, Kyoto 601-8428, Japan

a r t i c l e

i n f o

Article history: Received 1 April 2019 Accepted 4 October 2019 Available online xxxx Keywords: Cervical canal stenosis Foraminal canal Computed tomography Radiculopathy Posterior decompression

a b s t r a c t Cervical foraminal canal stenosis is a common disease, but any relationships between the measurement values of cervical foraminal canals and clinical symptoms have yet to be explored. We aim to determine a numerical cutoff point of cervical foraminal bony canal size that does not lead to radiculopathy so as to establish criteria for the surgical indication. We reconstructed angled sagittal slices along a nerve root on computed tomography (CT) on a workstation from pre-operative CT data and measured 1152 cervical foraminal canals (144 patients) from Cervical (C) 4/5 to C7/Thoracic (Th) 1. We evaluated the relationship between the size of foraminal canals and clinical manifestations. Receiver operating characteristic (ROC) analysis was used to calculate cutoff points of each foraminal canal size with positive neurologic manifestations. Of the 144 patients’ 1152 nerve roots, 286 nerve roots (24.8%) were diagnosed as radiculopathy by neurological examinations. The mean measured value of all foraminal canals on angled sagittal CT imagery was 3.39 ± 1.37 mm. The cutoff point of foraminal canal sizes without radiculopathy was 2.7 mm (sensitivity 0.680, specificity 0.591) overall. A cutoff point ascertained by quantitative evaluation of cervical foraminal canal size is useful for making diagnosis of cervical foraminal canal bony stenosis. Ó 2019 Elsevier Ltd. All rights reserved.

1. Introduction A cervical spinal nerve exits the spinal cord and is obliquely oriented toward the neural foramen. Spondylosis of the facet joint and/or herniation of the intervertebral disc often cause nerve root compression which may induce cervical radiculopathy. This common disease is often accompanied by pain and/or sensorimotor deficit [1]. Computed tomography (CT) or Magnetic Resonance Image (MRI) is useful for evaluation of foraminal canal stenosis. Posterior laminoforaminotomy is recommended as an excellent surgical treatment option for symptomatic cervical radiculopathy [2]. Although some qualitative grading systems for correlation between foraminal canal stenosis and clinical manifestations have been reported [3–5], the size of cervical foraminal canals has not been considered. It is unknown if there is any asymptomatic limitation in the size of foraminal canals [6]. With the advent of modern workstations, it has become easier to reconstruct CT or MRI data, and arbitrary thin slice images are

⇑ Corresponding author. E-mail address: [email protected] (M. Ozaki).

readily available at any time [7]. The current study aims to use angled sagittal CT imagery to calculate the cutoff point of the foraminal canal size that causes symptomatic radiculopathy. A numerical cutoff point would contribute to the understanding of the underlying pathophysiology of cervical radiculopathy caused by foraminal canal bony stenosis. Criteria for surgical indication may be established. 2. Patients and methods 2.1. Case selection We retrospectively reviewed the medical records of 224 consecutive patients who underwent cervical posterior decompression between the period of April 2011 and December 2016, within a five-year-and-nine-month period (69 months). None underwent anterior approach. Exclusion criteria were: (1) foraminal canal stenosis caused not by bony structures, but by soft tissues such as intervertebral disc hernia or ligaments; all patients were diagnosed by pre-surgical MRI, (2) presence of cervical instability, (3) history of surgery on the cervical spine and (4) history of any neurological diseases. Our study was ultimately comprised of 144 patients (mean age: 67.2, range: 35–87, male: female = 102:42).

https://doi.org/10.1016/j.jocn.2019.10.009 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: M. Ozaki, K. Nishioka, M. Kitayama et al., Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.009

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M. Ozaki et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

2.2. CT parameters and quantitative measurements for cervical foraminal canal stenosis

A

All patients underwent cervical helical CT (0.625 mm thickness; GE healthcare, Chicago, USA) as routine pre-operative evaluation. The CT imaging data were reconstructed at window width 2000 and window level 350 on Aquarius iNtuition Client Viewer (TeraRecon, California, USA) under the following protocol: (1) To obtain axial images, a conventional sagittal image was sliced parallel to each vertebral disc (Fig. 1A (a, b)) (2) Foraminal canals were identified from axial images and we acquired angled sagittal images along each foraminal canal that was parallel to a nerve root. (Fig. 1A (b, c)) (3) The narrowest minor axis of foraminal canal, orthogonally to a nerve root, was measured in the consecutive angled sagittal images (Fig. 1B). We regarded this narrowest minor axis as the foraminal canal size. Fig. 2 is an indicated case. In a conventional axial image (Fig. 2A), it is difficult to distinguish the difference between right and left foraminal canal sizes. By this method, however, whether the foraminal canal size at left side is narrower than on the right side can be indicated with a measured value (Fig. 2B). A single spinal neurosurgeon with 25 years of experience reconstructed all imaging data and measured all foraminal canal sizes retrospectively without clinical or surgical information. He measured the foraminal canal sizes on Aquarius iNtuition Client Viewer (TeraRecon, California, USA), which enabled measurement of the length at second decimal place in millimeters.

B

*

medial

lateral to right 2.9mm

* medial

lateral to left 1.5mm

Fig. 2. An example of measurement of the narrowest foramina canal. A: A conventional axial image at C5/6. It is difficult to distinguish the difference between the foraminal canal sizes at right and left sides. B: Consecutive angled sagittal images. It is possible to indicate the narrowest foraminal canal. Each asterisk shows the narrowest foraminal canal slice at right and left sides. Each double-headed arrow shows the measured foraminal canals. The measured values of the foraminal canal are 2.9 mm and 1.5 mm respectively.

2.4. Statistical analysis 2.3. Clinical correlation Neurological examinations were performed by the abovementioned single spinal neurosurgeon without imaging information. He diagnosed radiculopathy with upper extremity weakness, paresthesia, numbness and radicular pain corresponding to each segmental level [1]. More than one positive neurologic sign was considered to be a positive neurologic manifestation of each foraminal canal stenosis [8].

A (a)

(b)

Receiver operating characteristic (ROC) analysis was used to calculate cutoff points of each foraminal canal size with positive neurologic manifestations. The cutoff points of foraminal canal size without radiculopathy were rounded off to two decimal places. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for ‘R’ (The R Foundation for Statistical Computing, Vienna, Austria). More precisely, it is a modified version of Rcommander, designed to add statistical functions frequently used in biostatistics [9].

(c) 3. Results

C5 C6

B C5 C6

medial

* lateral to right

Fig. 1. Reconstruction of CT imaging data. A: (a) Conventional sagittal image. White line is parallel to the vertebral disc. (b) Axial images parallel to the vertebral disc. White line is parallel to the foraminal canal. (c) Angled sagittal image along the foraminal canal in a parallel position to a nerve root. B: Consecutive angled sagittal images. Asterisk shows the narrowest foraminal canal slice from the medial side to the lateral side. Double-headed arrow shows the measured foraminal canal.

Of the 144 patients’ 1152 nerve roots, 286 nerve roots (24.8%) were diagnosed as radiculopathy by neurological examinations. The number of C5/6 (C6) radiculopathy was the largest at both right and left sides. All data from each segmental level are shown in Table 1. The mean measured value of all foraminal canals on angled sagittal CT imagery was 3.39 mm ± 1.37 mm. All mean measured values at each segmental level from C4/5 to C7/Th1 are shown in Table 2. ROC analysis indicated the cutoff point of foraminal canal sizes without radiculopathy is 2.7 mm (sensitivity 0.680, specificity 0.591) overall. The area under the curve (AUC) value

Table 1 The segmental levels in 144 patients of cervical radiculopathy. Segmental level

Right

Left

Total

C5 C6 C7 C8 Total

21 (14.6%) 86 (59.7%) 26 (18.1%) 15 (10.4%) 148 (25.7%)

31 (21.5%) 61 (42.4%) 30 (20.8%) 16 (11.1%) 138 (24.0%)

52 (18.1%) 147 (51.0%) 56 (19.4%) 31 (10.8%) 286 (24.8%)

Please cite this article as: M. Ozaki, K. Nishioka, M. Kitayama et al., Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.009

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M. Ozaki et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx Table 2 Measured values of foraminal canals. Segmental level

Right (cm)

Left (cm)

Total (cm)

C5 C6 C7 C8 Total

3.12 ± 1.14 2.83 ± 1.23 3.13 ± 1.24 4.34 ± 1.46 3.36 ± 1.40

3.34 ± 1.24 3.02 ± 1.18 3.09 ± 1.18 4.21 ± 1.41 3.42 ± 1.34

3.23 ± 1.20 2.93 ± 1.21 3.11 ± 1.21 4.28 ± 1.44 3.39 ± 1.37

Values are mean ± SD.

Table 3 Cutoff point of each foraminal canal size without positive neurologic manifestations and their area under the curve (AUC) value. Right

Left

Segmental level

Cutoff point (mm)

AUC

Cutoff point (mm)

AUC

C5 C6 C7 C8 All

2.8 2.3 2.8 2.4 2.3

0.74 0.63 0.60 0.61 0.68

2.7 3.0 2.5 2.4 3.1

0.72 0.53 0.58 0.61 0.64

was 0.66 (Fig. 3). The cutoff points and AUC values in each segmental level are shown in Table 3.

4. Discussion Evaluation of cervical foraminal canal bony stenosis using angled sagittal slices along a nerve root on CT produces useful clinical information for cervical radiculopathy. In this study, the cutoff point of foraminal canal sizes without radiculopathy was 2.7 mm. The AUC value, showing the accuracy of the analysis was 0.66. These cutoff points will contribute to faster/more accurate diagnosis of cervical radiculopathy. Cervical radiculopathy is a common clinical entity caused by compression of a cervical nerve root. As well as patient history and physical examinations, imaging modalities play an important role in its diagnosis and localization [1]. Plain X-rays give useful information about the overall alignment and instability of the spine. CT is the most sensitive examination of the bony structures of the spine. MRI has the greatest ability to show soft tissue, such as hernia or ligaments. Thinner slice data is, however, available on CT imaging compared to MRI. CT images are more suitable for reconstruction on workstations. Moreover, radiculopathy due to osteophytes reportedly responds very well to laminoforaminotomy [10]. Therefore, in the current study, we highlighted cervical foraminal bony stenosis and adopted CT imaging as a preoperative evaluation.

1.0

Sensitivity

0.8

0.6

2.700 (0.680, 0.591)

0.4

0.2

Area Under the Curve(AUC): 0.66

0.0 1.0

0.8

0.6

0.4

0.2

0.0

Specificity Fig. 3. Receiver operating characteristic analysis for a cutoff point of each foraminal canal size without positive neurologic manifestation. Sensitivity is 0.680 and specificity is 0.591. Area under the curve value is 0.66.

To evaluate the cervical foraminal canal stenosis in detail, the reformatting of standard axial CT or MRI images in angled sagittal slices along a nerve root has been attempted. Sensitivity, specificity and accuracy of angled sagittal images are often reported to be higher than those of conventional axial images in making diagnosis of foraminal canal stenosis [7,8,11–15]. Angled sagittal images also supposedly have better inter-observer agreement than conventional images and should be considered in the routine evaluation of neural foraminal canal stenosis [3,4,13,14,16]. Grading systems for MRI have been recently proposed. Kim et al. (2015) reported an MRI grading system for cervical foraminal canal stenosis based on axial images for the first time. They compared the narrowest width of the neural foramen with that of the extraforaminal nerve root [3]. Park et al. (2015) suggested a modification of Kim’s system based on T2 axial images on MRI: Grade 0: narrowest neural foramen >80% of extraforaminal root Grade 1: <80%, but >50% Grade 2: <50% of extraforaminal root [5] A grading system based on oblique sagittal images has also been proposed [4]. These grading systems provide reliable assessments and good reproducibility [3,4]. Relationships between these grading systems and positive neurologic manifestations have been suggested [5,8,16]. To the best of our knowledge, however, no studies based on measurement data of cervical foraminal stenosis have been reported. Lee et al. (2017) proposed that a diameter of the C4/5 foramen of <2 mm was significantly related to C5 palsy after expansive open-door laminoplasty in binary logistic regression test [17]. The present report is the first to propose criteria based on measured values on CT images to examine the relationship between foraminal canal sizes and clinical manifestation in cervical foraminal canal bony stenosis. The cutoff point of foraminal canal sizes without radiculopathy was 2.7 mm overall, which would contribute to faster/more accurate diagnosis of cervical foraminal canal bony stenosis. Limitations of the present study are those intrinsic to a retrospective design. Surgical indication was not based on the cutoff point calculated in this study, so surgical outcomes were not analyzed. A prospective study including an evaluation of the results of the surgeries is needed to investigate the cutoff point of foraminal canal sizes without radiculopathy. A single experienced spinal surgeon reconstructed all imaging data and measured all foraminal canal sizes retrospectively. Although he replicated all image data without clinical information, it is difficult to consider the results of this study as perfectly reproducible without measurement errors or intra-observer agreement. The cutoff point calculated in this study also had relatively low sensitivity and specificity. We think, however, this study is valuable because it shows the approximate data as quantitative value for the first time. We cannot deny the possibility of mistaking cervical segmental symptoms and radiculopathy. Although neurologic signs such as Spurling’s sign, deep tendon reflexes, or electromyograms are applied to diagnose the responsible lesion [5], it is difficult to clearly preoperatively distinguish radiculopathy from segmental symptoms. Indeed, Choi

Please cite this article as: M. Ozaki, K. Nishioka, M. Kitayama et al., Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.009

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et al. (2017) reported that approximately 50% of their cervical myelopathy patients had accompanying radiculopathy [18]. In conclusion, the present study demonstrates a cutoff point of foraminal canal sizes without radiculopathy based on angled sagittal CT imagery. Quantitative evaluation for cervical foraminal canal bony stenosis could contribute to diagnosis of cervical foraminal canal stenosis. Compliance with ethical standards Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Ethical approval This study was approved by the Wakayama Medical University Ethical Review Board. Informed consent Formal consent is not required for this type of study. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We acknowledge proofreading and editing by Benjamin Phillis at the Clinical Study Support Center at Wakayama Medical University. References [1] Caridi JM, Pumberger M, Hughes AP. Cervical radiculopathy: a review. HSS J 2011;7(3):265–72. https://doi.org/10.1007/s11420-011-9218-z. [2] Kato S, Ganau M, Fehlings MG. Surgical decision-making in degenerative cervical myelopathy – anterior versus posterior approach. J Clin Neurosci 2018;58:7–12. https://doi.org/10.1016/j.jocn.2018.08.046. [3] Kim S, Lee JW, Chai JW, Yoo HJ, Kang Y, Seo J, et al. A new MRI grading system for cervical foraminal stenosis based on axial T2-weighted images. Korean J Radiol 2015;16(6):1294–302. https://doi.org/10.3348/kjr.2015.16.6.1294.

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Please cite this article as: M. Ozaki, K. Nishioka, M. Kitayama et al., Quantitative evaluation for cervical foraminal bony stenosis based on angled sagittal slices along a nerve root on computed tomography, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.10.009