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Neuroradiology (2021) 63:305–316

https://doi.org/10.1007/s00234-020-02596-5

REVIEW

Systematic review of radiological cervical foraminal grading systems


James Meacock 1 & Moritz Schramm 1 & Senthil Selvanathan 1 & Stuart Currie 2 & Deborah Stocken 3 & David Jayne 4 &
Simon Thomson 1

Received: 8 August 2020 / Accepted: 27 October 2020 / Published online: 4 January 2021
# Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract
The study design of this paper is systematic review. The purpose of this review is to evaluate the existing radiological grading
systems that are used to assess cervical foraminal stenosis. The importance of imaging the cervical spine using CT or MRI in
evaluating cervical foraminal stenosis is widely accepted; however, there is no consensus for standardized methodology to assess
the compression of the cervical nerve roots. A systematic search of Ovid Medline databases, Embase 1947 to present, Cinahl,
Web of Science, Cochrane Library, ISRCTN and WHO international clinical trials was performed for reports of cervical
foraminal stenosis published before 01 February 2020. In collaboration with the University of Leeds, a search strategy was
developed. A total of 6952 articles were identified with 59 included. Most of the reports involved multiple imaging modalities
with standard axial and sagittal imaging used most. The grading themes that came from this systematic review show that the most
mature for cervical foraminal stenosis is described by (Kim et al. Korean J Radiol 16:1294, 2015) and (Park et al. Br J Radiol
86:20120515, 2013). Imaging of the cervical nerve root canals is mostly performed using MRI and is reported using subjective
terminology. The Park, Kim and Modified Kim systems for classifying the degree of stenosis of the nerve root canal have been
described. Clinical application of these scoring systems is limited by their reliance on nonstandard imaging (Park), limited
validation against clinical symptoms and surgical outcome data. Oblique fine cut images derived from three dimensional MRI
datasets may yield more consistency, better clinical correlation, enhanced surgical decision-making and outcomes.

Keywords Radiology . Neurosurgery . Grading . Radiculopathy . Systematic review and spine

Introduction which the cervical nerve roots pass. Nerve root compression
causes radiculopathy, the symptom of radiating arm pain is
The natural process of ageing leads to degenerative changes known as brachialgia and the syndrome may lead to signifi-
within the spine including disc prolapse, osteophyte forma- cant disability including loss of arm function. Brachialgia may
tion, facet joint hypertrophy and ligamental thickening. All occur at any age but patients commonly present over the age
these may lead to stenosis of the cervical foramina through of 40 [1, 2]. Seventy-five percent of cases may resolve with
conservative management [3] but those that do not frequently
require surgical intervention.
* James Meacock Imaging of cervical spine (through computed tomography
james.meacock@nhs.net (CT) and/or magnetic resonance imaging (MRI)) forms an
essential part of the patient management. It is used to confirm
1
Department of Neurosurgery, Leeds Teaching Hospital NHS Trust, the diagnosis, locate the level and region of nerve root com-
Leeds General Infirmary, Great George Street, Leeds LS1 3EX, UK pression and to plan for surgery. However, imaging is not
2
Department of Neuroradiology, Leeds Teaching Hospital NHS Trust, without its limitations. The type, length and location of the
Leeds General Infirmary, Great George Street, Leeds LS1 3EX, UK nerve root compression are highly variable, and the best way
3
Leeds Institute of Clinical Trials Research, University of Leeds, of radiologically assessing the degree and location of cervical
Clarendon Way, Leeds LS2 9NL, UK nerve root compression remains uncertain. The path the nerve
4
Department of Academic Surgery, St James University Hospital, root follows is not in a standard orthogonal plane, and the
Level 7 Clinical Sciences Bldg, Leeds LS9 7TF, England nerve root diameter is small (between two and three
millimetres) leading it to be poorly imaged using the routine
306 Neuroradiology (2021) 63:305–316

two millimetre slice T2-weighted axial and sagittal MRI se- reviewed the article titles and abstracts, then read the full text
quences of the cervical spine [4]. Moreover, in the clinical articles to confirm that they met the inclusion criteria.
setting, there exists no standard objective method of assess- Disagreements arising during each stage of report selection
ment to describe foraminal stenosis which leads to the use of were resolved by consensus. Data items extracted from the
subjective terms such as “minor”, “moderate” and “severe”. reports are shown in Table 2.
Providing potentially more benefit would be the existence of a
standardized approach to the assessment of foraminal stenosis
and nerve root compression that when applied to the imaging Results
provides information on the type of operation required and
that is predictive of patient prognosis and outcome. It will also Overview
provide a common framework for classifying cases.
The initial search identified 6952 articles. Removal of dupli-
cates left 3839. There were a further 3767 articles excluded
Objectives following title and abstract screening which did not meet the
selection criteria. From the remaining 72 full-text articles, a
The aim of this systematic review is to evaluate the methods further 13 articles were excluded as they did not meet the
currently described to image and classify cervical neural fo- inclusion criteria leaving a total of 59 articles included in the
raminal stenosis with specific emphasis on how well imaging systematic review (Fig. 1). The characteristics of the included
correlates with symptoms and predicts surgical outcome. reports that assessed cervical foraminal stenosis can be seen in
Table 3.
Reports were from the USA (40%), Europe (31%), South
Methods Korea (20%), Japan (6%), China (2%) and Canada (2%). In
total 44 of the reports examined both genders, 15 reports did
The PRISMA guidelines for reporting items, systematic re- not give a breakdown of what proportion of their population
views and metaanalyses [5] were followed. The search strate- was male or female. There were four cadaveric models with
gy was developed with University of Leeds health science two of these not providing data on gender. There was a wide
librarians with specific expertise in systematic review age range from 14 to 97 years.
development. The risk of bias for the study overall was medium as there
Inclusion criteria are cervical region of the spine; radiolog- were 59 reports in total included within this systematic review.
ical imaging was performed and quantification of the cervical There were 17 prospective reports, 39 retrospective reports
neuroforaminal stenosis was undertaken. Reports were ex- and three where it was not clear. All the reports outlined their
cluded based upon the following exclusion criteria: duplicate aims for what they wanted to achieve, and only 12 were not
publication, trauma; nonhuman models and written in a lan- clear with their inclusion or exclusion criteria for participants.
guage other than English. All full journal articles included their statistical analysis, and it
The literature search included Ovid Medline, Ovid Medline was only the conference articles that were not explicit in how
in progress and other nonindexed citations, Ovid Medline they derived their figures.
Epub Ahead of Print, Embase 1947 to present, Cinahl, Web There was only one report that assessed the C1 level of the
of Science, Cochrane Library, Clinical trials, ISRCTN registry cervical spine and one that went as far caudal as the T2 level.
and WHO international clinical trials registry platform. The The number of levels assessed varied by report, but most
search strategy was mapped to MESH headings and included commonly, four levels were graded followed by six levels.
terms and variants of the terms including but not limited to: Of all reports included, 20% did not indicate how many ob-
“Cervical vertebrae”, “Stenosis”, “Radiculopathy”, servers graded the scans, but when specified, 26% were grad-
“Grading”, “Park”, “Kim”, Imaging techniques including ed by two people, 14% were graded by a single person and
“MRI” and “CT”. Nonhuman reports were excluded (Table 14% by three people, followed by 7% with six people, 5%
1). Reports which were both qualitative and quantitative were with four people and 3% with seven people. There was a mix
included. PROSPERO was searched to ensure that there were of observers that assessed the scans including radiologists,
no other systematic reviews that were currently on-going for neurosurgeons and orthopaedic surgeons.
this research topic. The search protocol was peer reviewed Most of the reports involved multiple imaging modalities;
independently by two experts and searched for articles pub- 69% used MRI, 50% used CT and 14% used plain X-rays.
lished before 01 February 2020. Most used standard axial and sagittal imaging, 53% also used
Once the reports were extracted from the databases, they nonstandard oblique views along the length of the neural fo-
were loaded into a reference management system and ramina. Those reports that used MRI favoured 1.5 T over 3 T
deduplicated. Two authors (JM and MS) independently and only a single report utilized 0.2 T.
Neuroradiology (2021) 63:305–316 307

Table 1 Example search strategy


used in Ovid Medline 1 exp Cervical Vertebrae/
2 (Cervical or spinal or neck or foramen or foraminal).tw.
3 1 or 2
4 Constriction, Pathologic/
5 Spinal Stenosis/
6 stenosis.tw,kw.
7 or/4–6 [stenosis]
8 3 and 7
9 ((cervical or spinal or neck or foramen or foraminal
or neuroforaminal) adj3 (narrow* or constrict* or compress* or stenosis)).tw.
10 Radiculopathy/
11 (cervical adj3 radiculopath*).tw.
12 or/8–11
13 (grading or grade* or classification* or measure*).tw,kw.
14 “Severity of Illness Index”/
15 (Park or Kim or mKim).tw,kw.
16 classification.fs.
17 or/13–16 [grading systems]
18 exp Magnetic Resonance Imaging/
19 ((MR or NMR) adj2 tomograph*).tw.
20 ((magnetic resonance or MR or NMR or diffusion weighted) adj2 imag*).tw.
21 ((“T-2 weighted” or “T2 weighted”) adj2 imag*).tw.
22 ((MR or NMR) adj2 tomograph*).tw.
23 (MRI or CT or CAT).tw.
24 exp Tomography, X-Ray Computed/
25 (comput* adj3 tomograph*).tw.
26 or/18–25 [imaging techniques]
27 exp Animals/ not exp. Humans/
28 12 and 17 and 26
29 28 not 27

Measurements of the cervical neural foramina indicates that nerve compression occurs most frequently dur-
ing extension of the neck and foraminal width is smaller than
The neuroforamina were described as oval in shape having a height. Following extension reducing this dimension further
width: height ratio of approximately 2:3. This is generally may increase the likelihood of crossing a threshold leading to
continued throughout the cervical spine with the cross section- radiculopathy [52]. C4/5 undergoes the greatest percentage
al area of the foramina decreasing cranio-caudal [21]. The change, being the main pivot point, with a change in height
mean cervical foraminal diameter for healthy participants on of 26%, width of 35% and area of 31% between flexion and
MRI was shown to be 4.36 mm (± 1.21 mm) and on CT extension.
5.33 mm (± 1.39 mm). Those with stenosis (defined by expert Measurements in the axial plane of MRIs demonstrate that
opinion) were found to have a diameter on MRI of 2.21 mm (± the foraminal diameter is nearly 20% more stenosed than com-
0.64 mm) and on CT 2.86 mm (± 0.71 mm) measured using parative CT imaging [62]. Using oblique views allows appre-
electronic callipers. This showed a discrepancy of 18.2% for ciation of the true cross sectional area [19].
healthy individuals and 22.8% for those with stenosis [7].
Oblique CT of the neuroforamina obtained from cadavers de- CT and MRI modalities
termined that the cross-sectional area was a minimum of
33 mm2 up to a maximum of 55.5 mm2. Cadaveric reports correlating MR and CT have investigated
The cross-sectional area of the neural foramina can change global degeneration of the cervical spine with disc degenera-
with neck movement. Extension of the cervical spine was tion categorized as grades I to V. There was a statistically
reported to worsen symptoms by decreasing the area whilst significant correlation between worsening degeneration of
flexion improved symptoms by increasing the area. This the discs with neuroforaminal width, area and osteophyte
308 Neuroradiology (2021) 63:305–316

Table 2 Items extracted from articles in systematic review sagittal oblique scans but delivered poor interrater kappa cor-
i. Number of patients relation [53], as have 3D CT surface reconstruction [8]. Proton
ii. Gender of patient density zero echo time (ZTE) 3 T MRI was found to have
iii. The age of the patients, the age range and the mean age
contrast comparable to that of CT for assessment of
iv. Imaging technique used such as CT, MRI or other possible imaging
osteophytes [17], and it can visualize the bony anatomy of
modalities the cervical neuroforamina as easily as CT with comparable
a. Magnetic field of the MRI scanner interrater kappa correlations [18]. Diffusion tensor imaging
b. Contrast medium used (DTI) on 3 T MRI has been used to investigate the structural
v. Angle of viewing the neural foramina such as axial, coronal, sagittal or changes in the cervical nerve roots; however, this has not been
oblique imaging correlated with neurological outcomes [33].
vi. Study type
vi. Inclusion and exclusion criteria Grading systems
viii. C-spine Assessment
a. Number of levels The grading themes that came from this systematic review
b. The levels included show that the most mature grading for cervical foraminal ste-
ix. Investigators reviewing the imaging nosis is in the form of systems described by Kim et al. [46] and
a. Number involved Park et al. [25] which were used in 24% of the reports. Area
b. Experience analysis of the neural foramina was performed in 48%, and
x. Assessment method global analysis of cervical degenerative disease with a focus
a. Named system used on the neuroforamina was included in 41% of the reports.
b. Details of system used The report by Fu et al. [39] recruited 48 patients to develop
xi. Analysis of grading criteria a grading system to assess degenerative changes in the cervi-
a. Interrater agreement assessment cal spine. Each patient was assessed with an MRI scan, and
b. Intrarater agreement assessment there were seven domains including disc hydration, disc space
xii. Correlation with symptoms or surgical outcome data height, central stenosis, foraminal stenosis, end plate changes,
spondylolisthesis, anterolisthesis and cord signal change.
There was 75.7% inter and 81.6% intrarater correlation.
Patients were categorized into two morphological groups
spurs and increasing category of nerve compromise with de- based on the shape of the foraminal stenosis; ‘V-Shape’ where
creasing neuroforaminal width and area [26, 63]. the stenosis is narrow as the nerve enters the foramina but
When gross estimates of neuroforaminal stenosis in 25% widens as it exits and ‘Parallel-Shape’ where the stenosis
increments are used to compare CT with MRI the interrater was constant throughout the cervical foramina [10].
kappa correlation was shown to be comparable [6]. MRI can The Kim system was first published in 2011 by a Korean
identify radiological evidence of root compression where the team aiming to classify the compression of the nerves as they
nerve could be seen and was compressed by the surrounding passed through the neural foramina using T2-weighted axial
disc or osteophytes or where there was encroachment of the MR imaging. The Kim system defines three grades of com-
lateral recess or neuroforamina [13]. Herniation of the inter- pression that relate the neuroforaminal diameter to that of the
vertebral discs was measured using four grades of normal, uncompressed nerve as it exits the cervical neural foramina at
bulging, protruding or extruding. It was shown that there were the level of the anterior margin of the superior articular pro-
no discernible differences between the two different imaging cess. The grades for this system are as follows: grade 0: ab-
techniques for interpretation of disc pathology [30]. When sence of neural foraminal stenosis, grade 1: moderate stenosis
evaluating facet trophism and arthrosis, it was found that facet with the narrowest width of the neural foramen between 51
arthrosis was better identified on CT than MRI; however, facet and 100% of the width of the uncompressed nerve and grade
trophism was equally identified on both [16]. 2: severe stenosis with the narrowest width of the neural fora-
men less than 50% of the width of the uncompressed nerve. In
Assessment using nonstandard imaging their report, Kim et al. [46] studied 96 patients using seven
raters who reviewed the scans. There were two radiology
Axial and coronal fast spin echo multiplanar short tau inver- trainees and five musculoskeletal radiologists with between
sion recovery (FMPIR) sequences have showed increased sig- two and 17 years of experience which led to an overall
nal intensity in the nerve for several centimetres when com- interrater kappa correlation of between 0.50 and 0.58.
pared to unaffected nerves and was a possible way to identify Subsequently other teams have attempted to improve upon
a compressed nerve which was causing symptoms [9]. the Kim system by modifying it to include additional features.
Coronal oblique views have been attempted rather than Siller et al. [49] investigated in a group of 23 patients (11
Neuroradiology (2021) 63:305–316 309

Records identified through database Additional records identified through

Identification
searching other sources
(n = 6952) (n = 12)

Records after duplicates removed


(n = 3839)
Screening

Records screened Records excluded


(n = 3839) (n = 3767)

Full-text articles assessed for Full-text articles excluded,


Eligibility

eligibility with reasons


(n = 72) (n = 13)

Reports included in
qualitative synthesis
Included

(n = 59)

Fig. 1 Prisma diagram depicting the flow of information through the different phases of the systematic review

ACDF and 12 PCF) adding in two modifications to grade 1 foramina ratio of one did not correlate with clinical symptoms.
and grade 2 thus forming five grades in total to indicate wheth- Their grades were modified as follows: grade 0: neural foram-
er the compression was predominantly anterior. There was no inal width is ≥80% of the extra foraminal uncompressed nerve
mention of the number of raters, and no correlations were width, grade 1: neural foraminal width is <80% but >50% of the
reported. They clinically evaluated patients before and after extra foraminal uncompressed nerve width and grade 2: neural
surgery. There were 49 neuroforaminal stenoses (C4/5 being foraminal width is <50% of the extra foraminal uncompressed
the most affected at 32.7%) of which 39 were graded as grade nerve width. They had two musculoskeletal radiologists review
2a, nine as grade 1a, one as grade 2 therefore indicating a the scans with 11 and 13 years of experience. This report found
majority with anterior nerve root compression. A median im- that the interrater kappa correlation was overall 0.851 for the
provement of one MRC grade from three to four out of five standard Kim system and 0.948 for the modified Kim system.
was found, and there was also an improvement in Odom’s The overall correlation with clinical symptoms was shown to be
criteria from admission (69.6%) to final clinic (91.3%). This r = 0.484–0.562 (moderate) for the Kim system and r = 0.517–
information was not segregated by grade of compression. 0.782 (moderate to high) for the modified Kim system [23].
The report by Park et al. [23] looked to modify the Kim The path that the nerve root follows is not in a horizontal
system and published what they called the modified Kim plane in the cervical region [22]. Oblique imaging has been
System. This team from Korea used T2-weighted MR imaging used in plain radiographs since 1967 and in CT scans since
on a cohort of 159 patients. They considered that a nerve to 1982 [64, 65]. Park et al. [25] developed a scoring system
Table 3 Summary of study characteristics
310

Report Sample Report design Age range Sex Complexity of Observer C-spine Observers Extent of Imaging Angle Grading Symptom
size (mean) grading system (Cons/Jnr) levels (No) testing technique system correlation

M F MRI CT X-
ray

Douglas-Akinwande 18 Retrospective 28–60 (48) 11 7 Low C N/A 6 Medium 1.5 T Y N Oblique Other
et al. [6]
Grams et al. [7] 17 Retrospective 35–78 (63) 9 8 Low C N/A 3 Low 3T Y N Standard Other
Schell et al. [8] 25 Retrospective 41–75 8 17 Low C C5-C7 (4) 3 Low N Y N Oblique Other
(56.6)
Dailey [9] 4 N/A 38–54 3 1 High N/A C5-C7 (3) 1 Low 1.5 T N N Standard Other
(46.75)
Gu et al. [10] 36 Prospective N (55.5) 31 5 Low N/A C3-T1 (5) N/A Low N Y N Standard Other
Brenke et al. [11] 79 N/A 42–64.6 40 39 Medium N/A N/A N/A Low N Y N Oblique Area Y
(53.3)
Roberts et al. [12] 19 Retrospective 54–81 12 7 Low C N/A (2) 7 Low N Y N Oblique Other
(62.7)
Lin et al. [13] 68 Retrospective 22–76 (48) 37 31 Low C C2-T1 (7) 1 Medium 1.5 T N N Standard Other
Oh et al. [14] 60 Retrospective 25–59 35 25 Low N/A C3-C7 (4) 2 Medium Y Y Y Standard Other Y
cohort (42.7)
Maulucci et al. [15] 7 N/A 48–67 N N Medium J C3-C6 (3) 2 Low N Y N Standard Area
(57.5)
Xu et al. [16] 54 Retrospective 40–74 36 18 Low N/A C2-C6 (4) 3 Medium 1.5 T Y N Standard Other
cohort (52.6)
Sneag et al. [17] 19 N/A N (58.4) 7 12 Low J C2-T1 (6) N/A Low 3T Y N Oblique Other
Argentieri et al. [18] 34 N/A N (57.5) 17 17 Low C C2-T1 (6) 2 Low 3T Y N Oblique Other
Tabaraee et al. [19] 72 Retrospective N (N) N N Medium N/A C2-T1 (6) N/A Medium N Y N Oblique Area
Su et al. [20] 18 N/A N (52.2) 7 11 Medium N/A C3-C7 (5) N/A Low N Y Y Standard Other
Lentell et al. [21] 20 Prospective 22–25 10 10 Medium J C2-T1 (6) N/A Low 1.5 T N Y Oblique Area
(23.7)
Park [22] 289 Retrospective N (50) 155 134 Medium N/A N/A 6 High Y N N Oblique Park Y
Park et al. [23] 356 Retrospective 17–80 (47) 159 197 Medium J C4-C7 (3) 2 High 1.5 T N N Standard mKim Y
Park et al. [24] 166 Retrospective 25–81 (46) 98 68 Medium J C4-C7 (3) 2 High 1.5 T N N Oblique Park Y
Park et al. [25] 50 Retrospective 19–97 (49) 37 13 Medium N/A C4-C7 (3) 2 Low 1.5 T N N Oblique Park
Sohn et al. [26] 7 Prospective 44–85 4 3 Medium J C1-T1 (7) 3 Medium 1.5 T Y N Oblique Area
(65.3)
Mao et al. [27] 10 Retrospective N (40.3) 6 4 Medium J C3-C7 (4) 1 Medium 3T N N Oblique Area
Case-control
Takasaki et al. [28] 23 Retrospective 19–34 12 11 Medium C C4-T1 (4) 2 Low 0.2 T N N Oblique Area
(24.52)
Usa et al. [29] 11 Retrospective 19–26 N N Medium C C2-T1 (6) 1 Low 3T N N Standard Area
(21.1)
Lee et al. [4] 289 Retrospective 20–79 (50) 155 134 Medium C C4-C7 (3) 6 High 1.5 T N N Oblique Park Y
Neuroradiology (2021) 63:305–316
Table 3 (continued)

Report Sample Report design Age range Sex Complexity of Observer C-spine Observers Extent of Imaging Angle Grading Symptom
size (mean) grading system (Cons/Jnr) levels (No) testing technique system correlation

M F MRI CT X-
ray

Yi et al. [30] 51 N/A 17–83 31 20 Medium C C2-C7 (5) 3 Medium 1.5 T Y N Standard Other
(49.3)
Walraevens et al. 20 Retrospective N (N) N N Medium N/A N/A 4 Low N Y Y Standard Other
Neuroradiology (2021) 63:305–316

[31]
Liu et al. [32] 15 Retrospective 23–49 (35) 10 5 Medium J C2-C7 (5) 3 Low 3T N N Oblique Area
Liang et al. [33] 30 Prospective 25–62 (49) 14 16 High C C5-T1 (4) 1 Low 3T N N Standard Other
Lee et al. [34] 188 Prospective 14–81 (41) 80 108 Medium J C4-C7 (3) 2 High 1.5 T N N Oblique Park Y
Kim
mKim
Siemionow et al. [35] 43 Retrospective N (57.3) 15 28 Medium C C3-C7 (4) 2 Medium N Y N Oblique Area
Jenis et al. [36] 6 Prospective N (71.6) N N Medium C C5-C7 (2) N/A Low N Y N Oblique Area
Kintzelé et al. [37] 74 N/A 34–79 (55) 44 30 Medium J C3-T1 (5) 2 Medium 3T N N Standard Park
Weber et al. [38] 74 Retrospective N (N) N N Medium C N/A N/A Medium 3T N N Oblique Park
Fu et al. [39] 48 Retrospective 15–91 23 25 Low C C2-T1 (6) 6 Medium Y N N Standard Other
(50.9)
Cosar et al. [40] 13 N/A 35–58 5 8 High N/A C4-C7 (3) N/A Low Y N N Standard Area
(48.6)
Dostal et al. [41] 34 Retrospective N (N) N N Medium C N/A N/A Low N Y N Standard Area
Miyazaki et al. [42] 50 Retrospective 19–69 (44) 22 28 Medium N/A C2-T1 (6) 4 Medium 0.6 T N N Standard Other
Park et al. [43] 26 Retrospective 50–86 16 10 Medium J C2-T1 (6) 2 Medium 1.5 T N N Oblique Other
(60.8)
Janusz and 35 Prospective N (N) N N Medium N/A N/A N/A Low N Y N Standard Area
Siemionow [44]
Lee et al. [45] 50 Retrospective N (N) N N Medium C C3-C7 (4) 2 Medium Y N N Oblique Other
Lee et al. [45] 50 Retrospective N (N) N N Medium J C3-C7 (4) 2 Medium Y N N Oblique Other
cross sectional
Kim et al. [46] 96 N/A 61–86 50 46 Medium C N/A 7 Medium 3T N N Standard Kim
(68.4)
Ko et al. [47] 438 N/A 20–84 243 195 Medium N/A C4-C7 (3) 3 High N Y N Standard Other
(54.3)
Nakamura and 104 N/A N (55.2) 88 16 Medium N/A C4-T1 (4) 1 Medium Y Y N Oblique Area Y
Taguchi [48]
Siller et al. [49] 23 Retrospective 36–78 19 4 Medium C C2-T1 (6) N/A Medium Y N N Standard mKim Y
cross sectional (59.9)
Kitagawa et al. [50] 7 Retrospective 25–42 (31) 7 0 Medium C C3-C7 (4) 1 Low N Y N Oblique Area
Mizouchi et al. [51] 42 Retrospective N (N) N N Medium N/A C4-T2 (5) 1 Medium N Y N Standard Area Y
Chang et al. [52] 5 Prospective 27–31 (N) 3 2 Medium J C3-C7 (5) 1 Low N Y Y Standard Area
Freund et al. [53] 25 Retrospective N (N) N N Low J N/A 4 Low Y N Y Oblique Other
311
312 Neuroradiology (2021) 63:305–316

based on oblique MR imaging. Building on the work pub-

correlation
Symptom lished by Wildermuth et al. [66] using MR imaging and
Roberts et al. [12] using CT imaging in the lumbar spine

Y
Park used existing MRI scans reformatted to show oblique
Grading

views of the neural foramina. This oblique sagittal grading


system

Other
Standard Area

Oblique Area

Area
Area
Area

Area
Oblique Park
Kim
system based on T2 weighted imaging involves the quantifi-
cation of the obliteration of perineural fat. The four grades for

Standard
Standard
Standard
Oblique

Oblique
this system were grade 0, no neural foraminal stenosis, grade
Angle

1, mild foraminal stenosis and no morphological changes.


Less than 50% perineural fat obliteration around the nerve
ray
MRI CT X-

N
N
N

N
N
N
N
N root circumference, grade 2, moderate foraminal stenosis
technique

and no morphological changes. Greater than 50% perineural


N
N
Y

N
Y
Y
Y
N
Observers Extent of Imaging

1.5 T
1.5 T

fat obliteration around the nerve root circumference and grade


3T

Y
N

N
N
N
3, severe foraminal stenosis showing morphological changes
or nerve root collapse. The Park system showed overall cor-
Medium
Medium
testing

relation with clinical symptoms in a cohort of 166 patients of


High
Low
Low

Low
Low
Low

between r = 0.630 and r = 0.653 [24] and when repeated in a


larger cohort of 289 patients clinical manifestations were
found to be between r = 0.570 and r = 0.715 [4, 67].
N/A
N/A

N/A

N/A
N/A

Park et al. [68] used a similar grading system based on the


2
2
3

one above but with greater simplicity to include normal, foram-


levels (No)

C3-C7 (4)
C2-C7 (5)

C3-C7 (4)
C3-C7 (4)

C2-T1 (6)
C3-T1 (5)
C2-T1 (6)

inal stenosis or indeterminate if the rater was not sure. The report
C-spine

defined foraminal stenosis as simply obliteration of the perineu-


N/A

ral fat, but unlike Park et al. [25], they did not quantify the extent
of obliteration. They had interrater kappa correlations of 0.557
(Cons/Jnr)
Observer

for axial alone, 0.412 for sagittal alone, 0.606 for axial and
N/A

sagittal views (the highest for this report) and 0.556 for oblique
C

C
C
C

J
J

sagittal views when two spinal surgeons graded the scans.


A conference article by Lee et al. [45] reviewed 50 patients
grading system
Complexity of

and, although not referenced, appeared to try and adapt and


combine the Kim and Park systems using assessment of mor-
Medium

Medium

Medium

Medium
Medium
Medium

Medium

phology on the axial images alone and extent of nerve root


Low

compression from both axial and oblique sagittal imaging.


The grades were as follows: morphology on T2 axial scans
17

31

18
N

N
F

2
4

(A: no stenosis, B: focal type with compression <50% of


Age range Sex

23

33
M

N
4
6
3
9

foraminal length and C: diffuse type with compression


21–67 (56)
35–75 (N)
28–71 (N)
27–31 (N)

>50% of foraminal length), extent of compression on T2 axial


(50.8)

(48.1)
(mean)

scans (grade 0: no compression, grade 1: nerve root compres-


22–81

24–70
N (N)

N (N)

sion is <50% of extraforaminal diameter and grade 2: nerve


root compression is >50% of extraforaminal diameter) with
the third criteria being extent of compression on T2 oblique
Sample Report design

Retrospective
Retrospective

Retrospective
Prospective

Prospective

Prospective

sagittal scans (grade 0: no compression, grade 1: max com-


pression does not pass the midline or interpedicular space and
N/A

N/A

grade 2: compression passes midline or severe deformation of


nerve). The morphology part of the system demonstrated an
interrater kappa correlation of 0.67–0.88, and the extent of
size

110
40

64

11
24

13

compression was 0.55–0.80 for the axial and 0.69–0.86 on


1

5
Table 3 (continued)

the oblique sagittal imaging. Ko et al. [47] used the axial


grading scheme from Lee et al. [45] but applied it to CT scans
Smith et al. [61]
Yeni et al. [58]
Yeni et al. [59]
Yeni et al. [60]
Kim et al. [55]

Ray et al. [56]

rather than MRI. They had a cohort of 438 patients and three
He et al. [57]
Anderst [54]

orthopaedic surgeons (one junior and two senior) graded the


Report

scans with interrater kappa correlation reported as 0.84 for


morphology and 0.86 for the extent of compression.
Neuroradiology (2021) 63:305–316 313

The pure Park system has been assessed in eight reports making decisions relating to surgical decompression of the
and the system was used by a minimum of two raters up to a nerve [10]. It is difficult to fully decompress the nerve when
maximum of six. In the report by Lee et al. [4] reviewing 289 the stenosis runs throughout the neuroforamina as in the par-
patients by six raters, they demonstrated the lowest interrater allel-shaped stenosis rather than predominantly focused prox-
kappa correlation of 0.80, but it has been shown to be as high imally. It has also been demonstrated that this middle zone is
as 0.94 by Kintzele et al. [37] albeit in a smaller patient cohort significant in the development of radiculopathy [26]. It is un-
of 74 patients with two raters. clear whether anterior or posterior surgical decompression is
In the report by Lee et al. [34], who reviewed a patient superior for different types of stenosis.
cohort of 188 to compare all three common grading systems, The current clinical method for grading foraminal stenosis
Park, Kim and modified Kim, there were two musculoskeletal is often subjective and reported by radiologists as mild, mod-
radiologists with experience of 10 and 15 years that reviewed erate or severe. It has been shown that around 10% of cases are
the images. Interrater kappa correlation was highest for the reported as abnormal in asymptomatic patients and a similar
Park system at 0.913 (0.856–0.970) followed by the modified number reported as normal in symptomatic patients [70].
Kim system 0.823 (0.745–0.902) and then the standard Kim The Kim system showed excellent interrater correlation
system 0.769 (0.688–0.851). It was shown that 51 patients had and used only axial imaging. The Park system reports higher
neurological manifestations. The correlation coefficient for interrater correlation but relies on oblique imaging which is
the Park system was r = 0.737 and r = 0.741 (higher than that not always available. In the report by Lee et al. [34], it was
in Park et al. [24]), Kim was r = 0.658 and r = 0.768 and the shown that there were discrepancies between the Park, Kim
modified Kim was r = 0.714 and r = 0.764. and modified Kim systems where the Park system indicated
that the neuroforaminal stenosis was grade 3 but the Kim and
modified Kim systems determined stenosis to be grade 1,
Discussion patients were shown to have neurological symptoms more in
keeping with an increased severity of stenosis.
MRI is the imaging modality of choice for assessing soft tissue The Kim and Park grading systems have been shown to
detail including degenerative changes and nerve roots. It is correlate with symptoms but have not been used in prospec-
inferior to CT in its ability to outline bone and osteophytic tive trials to assess surgical outcomes or in randomized trials
features, and it can overestimate the osseous contribution to to guide the surgical approach.
foraminal stenosis [8]. This limitation is however lessening A standardized, reproducible and accurate method for im-
due to new developments such as ZTE-MRI [31]. aging and reporting on foraminal stenosis could improve di-
The cervical nerve roots exit obliquely to standard axial and agnosis and inform surgical decision-making especially with
sagittal imaging. Oblique imaging has been performed as early regard to whether to perform surgery from the front or the
as 1967 using plain film x-rays and 1982 using CT. Oblique back of the neck. There is a clear need to improve the imaging
imaging has been shown to decrease interobserver variability and reporting of cervical foraminal stenosis.
when assessing cervical foraminal stenosis. Oblique sequences
can add complexity to the MRI protocol [25] but if a volumetric
three dimensional MRI is performed the scan time is not signif-
icantly different. Each sequence takes around three minutes, Conclusions
whereas volumetric data can be obtained in around the same
time if reformatting time is excluded. The time to reformat is Imaging of the cervical nerve root canals is mostly performed
falling rapidly with the increasing processing power of modern- using MRI and is reported using subjective terminology. The
day computing technology. This can then be used to generate Park, Kim and Modified Kim systems for classifying the de-
the traditional axial and sagittal images as well as oblique views gree of stenosis of the nerve root canal have been described.
with very little difference in image fidelity [34]. During flexion The clinical application of these scoring systems is limited by
and extension the calibre of the neuroforamina changes signif- their reliance on nonstandard imaging (Park), limited valida-
icantly [4]. Extension of the neck can decrease the tion against clinical symptoms and very limited validation
neuroforamina by more than 10% [26]. The standard recumbent against surgical outcome. Oblique fine cut images derived
position of a patient with neutral neck position used for most from three dimensional MRI datasets may yield more consis-
MRI scans may therefore underestimate the degree of foraminal tency, better clinical correlation, enhanced surgical decision-
stenosis; however, this motion is difficult to facilitate with pa- making and outcomes.
tients restricted by a necessary neck coil.
The normal neuroforamina has been described as having Authors’ contributions On behalf of all authors, I declare that we have
the narrowest width on entry, and it then widens towards the participated sufficiently in the writing of the paper to take public respon-
exit [69]. The shape of stenosis may be important when sibility for all the information submitted within this manuscript. All
314 Neuroradiology (2021) 63:305–316

authors have reviewed the final version of the manuscript and approve it to two-dimensional modalities. Glob Spine J 7:266–271. https://
for publication. doi.org/10.1177/2192568217699190
9. Dailey AT, Tsuruda JS, Goodkin R et al (1996) Magnetic resonance
Funding This study was partly funded by the Leeds General Infirmary neurography for cervical radiculopathy: a preliminary report.
Neurosurgery Research Fund. Dr. Meacock is supported by a Royal Neurosurgery 38(3):488–492. https://doi.org/10.1097/00006123-
College of Surgeons Research Fellowship and a National Institute of 199603000-00013
Health Research grant. 10. Gu BS, Park JH, Seong HY, Jung SK, Roh SW (2017) Feasibility
of posterior cervical foraminotomy in cervical foraminal stenosis:
prediction of surgical outcomes by the foraminal shape on preop-
Compliance with ethical standards erative computed tomography. SPINE 42:E267–E271. https://doi.
org/10.1097/BRS.0000000000001785
Conflict of interest The authors declare that they have no conflict of 11. Brenke C, Dostal M, Carolus A, Weiß C, Radü EW, Schmieder K
interest. et al (2014) Clinical relevance of neuroforaminal patency after an-
terior cervical discectomy and fusion. Acta Neurochir 156:1197–
Ethical approval All procedures performed in the studies involving hu- 1203. https://doi.org/10.1007/s00701-014-2090-0
man participants were in accordance with the ethical standards of the 12. Roberts CC, Troy McDaniel N, Krupinski EA, Erly WK (2003)
institutional and/or national research committee and with the 1964 Oblique reformation in cervical spine computed tomography: a
Helsinki Declaration and its later amendments or comparable ethical new look at an old friend. Spine 28:167–170. https://doi.org/10.
standards. 1097/00007632-200301150-00013
13. Lin C-H, Tsai Y-H, Chang C-H et al (2013) The comparison of
Informed consent Informed consent was obtained from all individual multiple F-wave variable studies and magnetic resonance imaging
participants included in the study. examinations in the assessment of cervical radiculopathy. Am J
Phys Med Rehabil 92:737–745. https://doi.org/10.1097/PHM.
0b013e31827d6546
14. Oh CH, Kim DY, Ji GY, Kim YJ, Yoon SH, Hyun D et al (2014)
Cervical arthroplasty for moderate to severe disc degeneration: clin-
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