The Clinical Correlation of a New Practical MRI Method for Grading Cervical Neural Foraminal Stenosis Based on Oblique Sagittal Images

Musculoskeletal Imaging Original Research Park et al. MRI for Grading Cervical Foraminal Stenosis Musculoskeletal Imaging Original Research Hee Jin Park 1,2 Sam Soo Kim 2 Chul Hee Han 1 So Yeon Lee 1 Eun Chul Chung 1 Mi Sung Kim 1 Heon Ju Kwon 1 Park HJ, Kim SS, Han CH, et al. Keywords: cervical foraminal stenosis, MRI, neural foramen, spine DOI:10.2214/AJR.13.11647 Received July 27, 2013; accepted after revision November 15, 2013. 1 Department of Radiology, Sungkyunkwan University School of Medicine, Kangbuk Samsung Hospital, Seoul, Korea. 2 Department of Radiology, Kangwon National University School of Medicine, 1 Kangwondaehak-gil, Chuncheon 200-722, Korea. Address correspondence to S. S. Kim (samskim@kangwon.ac.kr). AJR 2014; 203:412 417 0361 803X/14/2032 412 American Roentgen Ray Society The Clinical Correlation of a New Practical MRI Method for Grading Cervical Neural Foraminal Stenosis Based on Oblique Sagittal Images OBJECTIVE. The purpose of this study was to determine whether each grade in a new system suggested by Park et al. (Park system) to assess cervical neural foraminal stenosis validly correlates with the associated clinical findings and to evaluate the interobserver agreement in grading between two MRI readers. MATERIALS AND METHODS. We evaluated 166 patients (98 men and 68 women; mean age, 46 years) at our institution who underwent oblique sagittal MRI of the cervical spine. Using the new Park grading system, two radiologists evaluated the MRI findings for the presence and grade of cervical neural foraminal stenosis at the most narrow point. A neurosurgeon assessed the associated clinical manifestations. A positive neurologic manifestation of the cervical neural foraminal stenosis was defined as more than one positive neurologic clinical manifestation combined with more than one positive neurologic sign. Interobserver agreements between the two radiologists were analyzed using kappa statistics. Correlation coefficients (R) to assess the relationship between the grade and neurologic manifestations were calculated with nonparametric correlation analysis (Spearman correlation). The relationship between the assigned grade and the clinical manifestations was analyzed several ways: vertebrae level (C4 5, C5 6, or C6 7) and by age group (< 46 years and 46 years). RESULTS. Among patients who were evaluated by each reader to be grade 0, only 19 (17%) and 20 patients (18%) showed positive neurologic manifestations, respectively, with most patients showing negative neurologic manifestations. Among the patients who were grade 2 and 3, one reader found all patients and the second reader found all but one patient (100% and 93%, respectively) to have positive neurologic manifestations. According to the correlation coefficients, each Park grade was moderately correlated with the associated neurologic manifestations, such that higher grades were associated with more severe clinical manifestations. If we consider grade 2 or 3 MRI findings positive for identifying positive neurologic manifestations, the sensitivities and specificities were 39.7% and 99.0% (reader 1) and 39.7% and 99.0% (reader 2), respectively. CONCLUSION. The Park system, based on oblique sagittal MRI sections, provides a reliable and reproducible assessment of the severity of cervical neural foraminal stenosis. According to the Park system, grades 2 and 3 are associated with positive neurologic manifestations, and the Park system successfully predicts positive neurologic manifestations at these grades. C ervical neural foraminal stenosis results in radiculopathy and is often caused by degenerative osteophytes or laterally herniated disks [1]. The MRI diagnosis of the cervical neural foraminal stenosis is important because a correct diagnosis can predict prognosis and determine appropriate treatment methods [2]. However, to our knowledge, there have been no widely used diagnostic criteria or grading systems for cervical neural foraminal stenosis in contrast with established systems for characterizing lumbar neural foraminal stenosis. One of the limitations in the ability to characterize cervical neural foraminal stenosis is that, unlike the lumbar neural foramen, the cervical neural foramen is oriented at a 45 oblique angle so that routine sagittal images do not offer clear views [3]. Because of the limitations of these routine sagittal images specifically, the inability to correctly reflect the anatomic relationship between the nerve root and the neural foramen previous studies on grading of cervical neural foraminal stenosis were not highly reproducible [4]. Recently, Park et al. 412 AJR:203, August 2014

MRI for Grading Cervical Foraminal Stenosis [2] reported a new MRI grading system for cervical neural foraminal stenosis. They classified cervical neural foraminal stenosis into four grades according to MRI findings on 45 T2- weighted oblique sagittal images (Fig. 1): grade 0, no cervical neural foraminal stenosis; grade 1, presence of perineural fat obliteration of less than 50% of the nerve root circumference; grade 2, nearly complete perineural fat obliteration (more than 50% of the nerve root circumference without morphologic change of the root itself); and grade 3, nerve root collapse and deformity. Park et al. showed that this new grading system can provide a reliable assessment of cervical neural foraminal stenosis, and they showed the grading system was reproducible. Park et al. recommended this new grading system as an easy way to objectively evaluate cervical neural foraminal stenosis. Therefore, we sought to explore this new system by evaluating the agreement between MRI readers and by determining whether the grades in this new system validly correlate with the clinical findings. A C D Fig. 1 Schematic illustrations of Park system for grading cervical neural foraminal stenosis. Drawings by Park HJ. Adapted with permission from [2]. A D, Drawings show grade 0 (A), oblique sagittal plane of cervical neural foramen showing no significant stenosis and no perineural fat obliteration; grade 1 (B), mild perineural fat obliteration (50% or less of circumference of corresponding nerve root obliterated); grade 2 (C), moderate perineural fat obliteration (more than 50% of circumference of corresponding nerve root is obliterated) and morphologic change of nerve root is not seen; and grade 3 (D), in addition to severe perineural fat obliteration, collapsed nerve root and morphologic change are present. B Materials and Methods Case Selection Our institutional review board approved this study and waived the requirement for informed consent because of its retrospective nature. Our study population included 98 consecutive men (59%; age range, 29 72 years) and 68 consecutive women (41%; age range, 25 81 years) who visited our institution because of neck pain, radiating pain in the upper extremities, and weakness of the hand or finger and underwent MRI of the cervical spine between December 2010 and May 2012. Patients ranged in age from 25 to 81 years with a mean age (± SD) of 46 ± 13 years. Seventy-eight patients were younger than 46 years (47%), and 88 patients were 46 years old or older (53%). Exclusion criteria included tumor (three cases), acute trauma (n = 16), surgical history (n = 5), and central disk herniation (n = 23). Patients with symptoms at different cord levels or on the opposite side of the stenosis were also excluded (n = 1). The same neurosurgeon assessed the clinical manifestations and performed the neurologic examinations. The neurosurgeon had fellowship training in spine surgery and had 20 years of experience. We considered neurologic clinical manifestations to be positive if the patients showed paresthesia, extremity weakness, numbness, and funicular or radicular pain [5]. The neurologic signs we measured included positive Lhermitte sign, Spurling sign, decreased response of deep tendon reflex, and positive denervation sign on electromyography [5]. Electromyography was performed in four cases, but all other neurologic examinations were performed in all patients. More than one positive neurologic clinical manifestation combined with more than one positive neurologic sign was considered to be a positive neurologic manifestation of corresponding cervical neural foraminal stenosis [6]. Symptoms in the lower extremities, symptoms on the opposite side of the stenosis, or symptoms on a different vertebral level than the stenosis were not considered positive neurologic manifestations. MRI Parameters MRI examinations were performed using the same protocol for each patient on a 1.5-T magnet (Intera, Philips Healthcare) using a SYN head coil (Philips Healthcare) and fast spin-echo imaging. T2-weighted images were obtained in the axial and sagittal planes with the patient in the supine position. The MRI parameters were as follows: axial T2-weighted turbo spin-echo (TR/TE, 2500/100; FOV, 17 cm; matrix, 315 250; slice thickness, 3 mm; signal average, 1; interslice gap, 0.3 mm); sagittal T2-weighted spin-echo (TR/TE, 2500/100; FOV, 24 cm; matrix, 360 280; slice thickness, 4 mm; signal average, 3; interslice gap, 0 mm); axial T1-weighted spin-echo (TR/TE, 700/10; FOV, 17 cm; matrix, 315 250; slice thickness, 3 mm; signal average, 1; interslice gap, 0.3 mm); and sagittal T1-weighted spin-echo (TR/TE, 500/10; FOV, 24 cm; matrix, 360 280; slice thickness, 4 mm; signal average, 3; interslice gap, 0 mm). Oblique sagittal images were acquired by identifying the medial edge of the neural foramen, and seven images were obtained progressing laterally through the foramen at a projection angle of 45 bilaterally. The angled projections were obtained with the following parameters: TR range/te, 1400 2500/100; FOV, 24 cm; matrix, 360 280; slice thickness, 3 mm; interslice gap 0 mm; and signal average, 3. The images included the medial margin of each pedicle, isthmus of the foramen, and lateral edge of the foramen [7]. The mean scanning time was 3.25 minutes. Image Analysis The MRI results were interpreted independently by two fellowship-trained, musculoskeletal radiologists with 8 and 13 years of experience. The radiologists were blinded to the clinical AJR:203, August 2014 413

Park et al. TABLE 1: Distribution of Foraminal Stenosis by Vertebral Level Park Grade Vertebral Level information and radiologic reports. A total of 166 foramina of 166 patients and corresponding nerve roots from C4 5 to C6 7 were qualitatively analyzed. Both radiologists assessed the presence and grade of cervical neural foraminal stenosis at the narrowest point according to the new grading system suggested by Park et al. [2] (Park system). Statistical Analysis We used chi-square tests to analyze the prevalence of each grade according to the cervical level. Interobserver agreements between the two radiologists were analyzed using kappa statistics. The agreement between readers was analyzed according to each cervical level, and the agreement was also measured after breaking down the patients into two age groups. The strength of the interobserver agreement was characterized as follows: poor (< 0.1), slight (0.1 to 0.2), fair (0.2 to 0.4), moderate (0.4 to 0.6), substantial (0.6 to 0.8), and almost perfect (0.8 to 1) [8]. Correlation coefficients (R) to assess the relationship between the grade and neurologic manifestations were calculated by nonparametric correlation analysis (Spearman correlation). We analyzed the relationship between grade and neurologic manifestations at each vertebral level (C4 5, C5 6, and C6 7). We also broke down the patients into two age groups (< 46 years and 46 years) to explore the relationship between grade and neurologic manifestations. A weak correlation between grade and neurologic 0 1 2 3 Reader 1 Reader 2 Reader 1 Reader 2 Reader 1 Reader 2 Reader 1 Reader 2 Reader 1 Reader 2 C4 5 36 (32) 35 (31) 4 (15) 6 (21) 2 (13) 1 (7) 0 (0) 0 (0) 42 42 C5 6 40 (35) 41 (36) 16 (59) 13 (47) 9 (60) 11 (79) 7 (64) 7 (64) 72 72 C6 7 37 (33) 37 (33) 7 (26) 9 (32) 4 (27) 2 (14) 4 (36) 4 (36) 52 52 Overall 113 (100) 113 (100) 27 (100) 28 (100) 15 (100) 14 (100) 11 (100) 11 (100) 166 166 p 0.891 0.781 0.013 0.267 0.074 0.002 0.549 0.549 Note Data in parentheses are percentages. Fig. 2 Chart shows prevalence of each Park system grade. Black bars indicate grades of reader 1 and gray bars indicate grades of reader 2. Patients (No.) 130 110 manifestations was defined as correlation coefficients between 0.1 and 0.3, a moderate correlation was between 0.3 and 0.7, a relatively high correlation was between 0.7 and 0.9, and above 0.9 was considered a very high correlation [9]. With clinical manifestation used as the standard of reference, the sensitivity and specificity of grades 2 and 3 stenosis were calculated with a 95% CI. Statistical analyses were performed using PASW software, version 18.0 (IBM), and p values of < 0.05 were considered to be statistically significant. Results Schematic illustrations of cervical neural foraminal stenosis according to the Park system are shown in Figure 1. The 90 70 50 30 10 Grade 0 Grade 1 Grade 2 Grade 3 distribution of cervical neural foraminal stenosis by vertebral level is shown in Table 1 and Figure 2; grade 0 was the most common (113, 68%) score, and grade 3 was least common (11, 7%). The frequency of each grade was evenly distributed according to the cervical level, which is consistent with the results of the previous study by Park et al. [2]. We found positive neurologic manifestations in 63 patients and negative neurologic manifestations in 103 patients through a search of the electronic medical report system (Figs. 3 6). Among patients who were evaluated grade 0 by each reader, 19 patients (17%) and 20 patients (18%), respectively, showed positive TABLE 2: Prevalence of Grade Assignments Organized by Radiologist and Associated Neurologic Manifestations by Grade Radiologist Parameter Park Grade 0 1 2 3 1 Prevalence 113 (68) 27 (16) 15 (9) 11 (7) 166 (100) Positive neurologic manifestations 19 (30) 19 (30) 14 (22) 11 (18) 63 (100) 2 Prevalence 113 (68) 28 (17) 14 (8) 11 (7) 166 (100) Positive neurologic manifestations 20 (32) 19 (30) 13 (21) 11 (18) 63 (100) Note Data in parentheses are percentages. 414 AJR:203, August 2014

MRI for Grading Cervical Foraminal Stenosis neurologic manifestations. Among 27 patients with grade 1 by reader 1, eight patients (30%) had negative neurologic manifestations, and among 28 patients with grade 1 by reader 2, eight patients (29%) had negative neurologic manifestations. Among patients who were grades 2 and 3, one reader found that all patients had positive neurologic manifestations and the other reader found all but one patient to have positive neurologic manifestations (100% and 93%, respectively). In other words, of all patients with grade 2 or 3 cervical neural foraminal stenosis, one of the readers found just one patient to be free from neurologic manifestations (Table 2). The overall interobserver agreement was almost perfect (k = 0.879) (Table 3), and the agreements at each vertebral level were almost perfect (k = 0.824 0.875). When the relationship between grade and clinical manifestations was broken down by age, no statistically significant relationships were observed. A moderate correlation between grade and neurologic manifestations was found (R = 0.565 and R = 0.675) (Table 4), but there was no statistical significance between R at each level. In the younger age group (< 46 years), the R of reader 1 was 0.617 and the R of reader 2 was 0.586. In the older age group ( 46 years), the R of reader 1 was 0.698 and the R of reader 2 was 0.678 (Table 5). Although the R values of the older age groups were higher than the younger age group, they were Fig. 3 Example of Park grade 1 in 44-year-old woman with left shoulder pain. Oblique sagittal T2- weighted turbo spin-echo image (TR/TE, 2000/100) shows mild (less than 50% of circumference of nerve root obliterated) perineural fat obliteration in cervical neural foramen at C5 6 on left side (arrow). Patient showed positive neurologic manifestations. TABLE 3: Relationship Between Radiologists Value Vertebral Level not significantly different (p > 0.05). If we consider grade 2 or 3 MRI findings positive for identifying positive neurologic manifestations, the sensitivities and specificities were 39.7% and 99.0% (reader 1) and 39.7% and 99.0% (reader 2), respectively. Fig. 4 Example of Park grade 2 in 81-year-old woman with radiating pain in right upper extremity. Oblique sagittal T2-weighted turbo spin-echo image (TR/TE, 2000/100) shows moderate (greater than 50% of circumference of nerve root is obliterated) perineural fat obliteration in cervical neural foramen at C5 6 on right (arrows). Patient showed positive neurologic manifestations. Age (y) C4 5 C5 6 C6 7 < 46 46 κ 0.824 0.887 0.875 0.845 0.898 0.879 p < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 Note Strength of the interobserver agreement (κ) was characterized as follows: poor (< 0.1), slight (0.1 to 0.2), fair (0.2 to 0.4), moderate (0.4 to 0.6), substantial (0.6 to 0.8), and almost perfect (0.8 to 1). TABLE 4: Correlation Coefficients (R) of Assigned MRI Grade and Observed Neurologic Manifestations by Vertebral Level Observer Vertebral Level C4 5 C5 6 C6 7 Reader 1 0.675 (< 0.001) 0.651 (< 0.001) 0.574 (< 0.001) Reader 2 0.603 (< 0.001) 0.636 (< 0.001) 0.565 (< 0.001) Note Data in parentheses are p values. TABLE 5: Correlation Coefficients (R) of Assigned MRI Grade and Observed Neurologic Manifestations Organized by Age Group Observer Age Group (y) < 46 46 Reader 1 0.653 (< 0.001) 0.617 (< 0.001) 0.698 (< 0.001) 0.365 Reader 2 0.630 (< 0.001) 0.586 (< 0.001) 0.678 (< 0.001) 0.331 Note Data in parentheses are p values. a p values for comparison between age groups < 46 and 46 years are shown. Discussion The evaluation of cervical neural foraminal stenosis using MRI must be accurate, easy, and consistently reproducible between different observers. A labor-intensive precise quantitative analysis is not practical in a clin- Fig. 5 Example of Park grade 3 in 53-year-old man with tingling sensation in left upper extremity. Oblique sagittal T2-weighted turbo spin-echo image (TR/TE, 1460/100) shows collapsed nerve root and surrounding bony structures at C5 6 (arrows) on left side. Patient showed positive neurologic manifestations. p a AJR:203, August 2014 415

Park et al. ical setting, but a semiquantitative measurement does help eliminate some of the factors that lead to variability caused by internal subjective standards [10]. The Park system offers a remedy by providing a reliable and reproducible assessment of the severity of cervical neural foraminal stenosis, and this new grading system is an easy method with which to accomplish an objective evaluation [2]. In this study, the interobserver agreements between readers at each vertebral level were similar to the initially reported values by Park et al. [2], which ranged from 0.824 to 0.887. Park et al. also reported that the prevalence of grade 3 findings at the C5 6 level is significantly higher than at other levels, which may be due to the C5 6 level having the largest range of vertebral motion. In addition, the most severe deformities of the neural foramen are found at the C5 6 level. In our study, grade 3 scores tended to occur more often at the C5 6 level than at other levels (64% of grade 3 scores were at the C5 6 level), but this was not a statistically significant effect. The difference in our results from the Park et al. report might be due to differences in study population size. Park et al. evaluated only 50 patients, whereas we evaluated 166 patients. In addition to analyzing the Park system by vertebral level, we assessed the correlation of the Park system to clinical manifestations and neurologic signs. The overall R values of both readers showed moderate correlation (0.630 and 0.653) between grade and clinical manifestations and neurologic signs. In the study of the correlation between grading and lumbar neural foraminal stenosis, Park et al. [5] reported an overall R of 0.75. Similar R values, regardless of different anatomic locations, may result from the fact that both grading systems are composed of similar morphologic analysis methods. As in our study, Park et al. evaluated the severity of the stenosis according to the amount of perineural fat obliteration [11]. In addition to our analysis at each vertebral level, we also grouped the study population into two categories by age: those above the mean study age and those below the mean age. The older age group showed higher R values, or stronger relationships between the assigned grade and the associated clinical manifestations, than the younger age group. Despite this trend, the two age groups were not statistically different in the relationship between their Park system grades and the associated clinical manifestations (p > 0.05) (Table 5). When considering whether the Park system grade is a sufficient tool with which to predict clinical manifestations, we had interesting results. In patients graded 0, we found 17 18% to have positive neurologic manifestations, with the remaining 82 83% having negative neurologic manifestations. In patients graded 2 or 3, we found 93 100% to have positive neurologic manifestations (0 7% had negative neurologic manifestations) (Fig. 2 and Table 2). Therefore, we conclude that patients with MRI findings that indicate grades 2 and 3 will most likely have positive neurologic manifestations, allowing clinicians to use a grade 2 or 3 MRI finding to predict what is seen clinically. In general, patients do not present for MRI without some clinical manifestation already present. In those cases in which there is a confusing clinical presentation, this grading system would facilitate pinpointing the single or multiple levels truly accounting for the symptoms. Although most of the patients with grade 0 cervical neural foraminal stenosis were free of neurologic manifestations, we cannot ignore that nearly 20% of them did have positive neurologic manifestations. Thus, unlike grade 2 or 3, which are strongly associated with clinical manifestations, grade 0 is not strictly free of clinical manifestations. Therefore, using grade 0 MRI findings as a predictor of clinical findings is unreliable. Our findings conflict with what was seen by Park et al. [6], who found that a central cervical spinal stenosis grade of 0 does appropriately predict negative neurologic manifestations. Park et al. reported that only 2 6% of positive neurologic manifestations were found in grade 0 patients. The clinical significance of grade 1 is also controversial. About 30% of grade 1 patients showed negative neurologic manifestations, and these values do not support the probability of positive neurologic manifestations or negative neurologic manifestations. Therefore, we conclude that the Park system can accurately predict positive neurologic manifestations in the cases of grades 2 and 3, but whether this system can accurately predict negative neurologic manifestations in the case of grade 0 is not certain and will require more exploration. One limitation of our study is that it is not a quantitative study regarding our measures of clinical manifestations. We made the assumption that each clinical sign and each clinical manifestation carries the same weight to create positive neurologic manifestations [6]. Fig. 6 Example of Park grade 1 in 55-year-old woman with neck pain. Oblique sagittal T2-weighted turbo spin-echo image (TR/TE, 1640/100) shows mild (less than 50% of circumference of nerve root) perineural fat obliteration in cervical neural foramen at C5 6 on left side (arrow). Patient showed no neurologic manifestations. The clinical manifestations were classified as either positive or negative, which could be an oversimplification. Moreover, using clinical manifestations and neurologic examination is an imperfect diagnostic method. The second limitation is a single posture (neutral position) of the patients during image acquisition. The diameter of the neural foramen can be changed as the spine moves into extension or flexion [5]. The third limitation is that this study was performed at a single medical center, which may limit its reproducibility because physicians or surgeons at other institutes may classify clinical manifestations differently depending on their protocols. In conclusion, the Park system of cervical neural foraminal stenosis based on oblique sagittal MRI provides a reliable and reproducible diagnosis of the severity of cervical neural foraminal stenosis, and this new grading system is a simple method with which to gather an objective evaluation. In addition to its ease of use, the Park system grade correlates with clinical findings. Patients assigned grades 2 and 3 were consistently found to have positive neurologic manifestations. However, patients with grade 0 tended to have negative neurologic manifestations, and we found the overall relationship between grade 0 and its clinical manifestations to be less reliable. References 1. Yousem DM, Atlas SW, Goldberg HI, Grossman RI. Degenerative narrowing of the cervical spine neural foramina: evaluation with high-resolution 416 AJR:203, August 2014

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