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Musculoskeletal Imaging Original Research

Joe et al.
MRI of Lumbar Endplate Herniation

Musculoskeletal Imaging
Original Research
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Herniation of Cartilaginous
Endplates in the Lumbar Spine:
MRI Findings
Eugene Joe1,2 OBJECTIVE. The purpose of this study was to determine reliable MRI findings suggest-
Joon Woo Lee1 ing disk herniation with cartilage endplate herniation in the lumbar spine.
Kun Woo Park 3 MATERIALS AND METHODS. The records of 73 patients who underwent lumbar spi-
Jin Sup Yeom 3 nal MRI and lumbar microdiskectomy between March 2005 and January 2009 were searched
Eugene Lee1 to find those with the diagnosis of disk herniation with cartilage endplate herniation con-
firmed during surgery. The following morphologic features were assessed: posterior corners
Guen Young Lee1
(posterior marginal nodes, dorsal corner defects, Modic changes, and posterior osteophytes),
Heung Sik Kang1 mid endplates (endplate irregularities, Modic changes), and heterogeneous low signal inten-
Joe E, Lee JW, Park KW, et al. sity of extruded material. The chi-square test and multiple logistic regression analysis with
age, body mass index, and sex as covariates were used for the analysis. The ROC curve was
obtained with scores of the statistically significant MRI findings.
RESULTS. Posterior marginal nodes, posterior osteophytes, Modic changes in posterior
corners, mid endplate irregularities, Modic changes in mid endplates, and heterogeneous low
signal intensity of extruded material were significantly more frequent in patients with disk
herniation with cartilage endplate herniation (0.000 < p < 0.009). The AUC for diagnosing
disk herniation with cartilage endplate herniation with our scoring system of the six MRI
findings (06) was 0.888.
CONCLUSION. The presence of disk herniation with cartilage endplate herniation
could be ascertained with the following MRI findings: posterior marginal nodes, posterior
osteophytes, mid endplate irregularities, heterogeneous low signal intensity of extruded ma-
terial, and Modic changes in posterior corners and mid endplates.

L
umbar disk herniation is a condi- factor in controlling diffusion of the disk
Keywords: cartilage endplate, disk herniation, lumbar tion in which a tear of the annu- proper (nucleus pulposus and annulus fibro-
MRI, lumbar spine, MRI lus fibrosus allows the nucleus sus), the only source of nutrition to the nucle-
pulposus to bulge and exert me- us pulposus [5]. Endplate damage, which can
DOI:10.2214/AJR.14.13319
chanical compression on the nerve root. It is start as site-specific focal breaks, can result
Received June 15, 2014; accepted after revision considered one of the key causes of back in a cascade of events resulting in degenera-
September 22, 2014. pain. An intervertebral disk has three major tion. In such a case, a CEP becomes sclerotic
structural components: nucleus pulposus, and loses contact with blood vessels, provid-
1
Department of Radiology, Seoul National University annulus fibrosus, and cartilaginous endplate ing less nutrition to the disk and the CEP it-
Bundang Hospital, 300 Gumidong, Bundag-Gu,
(CEP). Many reports have appeared on the self. As a result, the proteoglycan content de-
Seongnam, Gyeongi-do 463-707, Republic of Korea.
Address correspondence to J. W. Lee anatomy, mechanics, and chemistry of the creases within the disk; the result is loss of
(joonwoo2@gmail.com). nucleus and annulus, but little is known water and osmotic pressure in the disk [6, 7].
about the MRI characteristics of CEPs and The association between the severity of end-
2
Department of Radiology, Gachon University Gil Medical CEP herniation because their average thick- plate damage and disk degeneration has been
Center, Incheon, Republic of Korea.
ness of the CEP is only 0.6 mm, making it documented, and CEP loss is also associat-
3
Department of Orthopedics, Seoul National University difficult to recognize at routine MRI exami- ed with disk calcification and rupture (e.g.,
Bundang Hospital, Seongnam, Republic of Korea. nations [13] (Fig. 1). Schmorl nodes, a protrusion of a disk into the
A CEP consists of a thin layer of hyaline adjacent vertebral body) [5, 8, 9].
AJR 2015; 204:10751081 cartilage between a disk and a vertebral body. Willburger et al. [10] found that a great-
0361803X/15/20451075
Functionally, a CEP is considered a gateway er proportion of the CEP in a herniated disk
for nutrient transport from blood vessels into correlated with increased pain intensity val-
American Roentgen Ray Society its central disk [4]. It is the most important ue. Brock et al. [11] reported that multiple

AJR:204, May 2015 1075


Joe et al.

jection period in days were also gathered by retro-


spective chart review.

MR Image Acquisition
At our institution, MRI was performed with ei-
ther a 1.5-T (Gyroscan, Philips Healthcare) or a 3-T
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(Intera Achieva, Philips Healthcare) system with


a Sense spine coil for the 3-T system or a Syner-
gy spine coil (both Philips Healthcare) for the 1.5-
T system. The patients were placed in the supine
position with a cushion under both knees. Sagittal
and axial T1-weighted spin-echo images (TR/TE,
500/15) and sagittal and axial T2-weighted fast
spin-echo images (TR/TE, 3600/120) were ob-
tained. The parameters were as follows: slice thick-
ness, 4 mm; slice gap, 0.4 mm; FOV, 32 cm for sag-
Fig. 1Diagram shows disk herniation without (left) and with (right) with cartilage endplate herniation. ittal images and 16 cm for axial images; matrix,
512 512; flip angle, 90; and number of signals
and recurrent sequestered fragments almost in the admission records of the patients electronic acquired, 3. The imported MR images obtained at
always consist of endplate material. Carreon medical charts: age, sex, body mass index (BMI), various hospitals before the referral to our hospital
et al. [12] observed differences in the absorp- symptom duration in days, sensory changes scored were obtained with various MRI systems and vari-
tion of herniated CEPs and annulus fibro- 0100, motor grade scored 05, straight leg raising ous protocols. All images were deidentified before
sus after cervical spinal trauma and report- (SLR) test result, visual analog scale (VAS) score analysis and were randomly numbered.
ed that CEPs exhibited less absorption and for leg pain and back pain, and the Oswestry Dis-
seemed to be the same size. These findings ability Index (ODI) score. Data were gathered by Analysis of MR Images
may reflect metabolic alterations that occur a radiologist after retrospective chart review. The The MR images were assessed by a radiologist
in the course of disk degeneration and ex- number of previous epidural injections and the in- with 10 years of experience as a staff spinal radi-
plain the importance of having a method of
assessing CEPs and CEP herniation. TABLE 1: Demographic Data on 73 Patients With Disk Herniation With or
Some MRI studies have been conduct- Without Cartilage Endplate (CEP) Herniation
ed on CEPs and the relation between CEP
Disk Herniation Without Disk Herniation With
herniation and recurrent disk herniation [5, Characteristic CEP Herniation CEP Herniation pa
1315]. Schmid et al. [15] reported that CEP
herniations are common and that changes in Age (y) 45.58 (10.93) 50.82 (15.28) 0.180
marrow signal intensity of the vertebral end- 60 33 (55) 27 (45) 0.037b
plate on MR images are indicative of carti- > 60 3 (23) 10 (77)
laginous material in the extruded disk herni-
Male-to-female ratio 10:26 18:19 0.067b
ation material. To our knowledge, however,
a reliable method of identifying CEP hernia- Body mass index 24.07 (3.01) 24.27 (3.84) 0.658
tion has not been described. Symptom duration (d) 63.67 (52.44) 74.27 (81.99) 0.675
The main aim of our study was to find a Sensory score (0100) 80.56 (20.56) 72.70 (28.05) 0.312
method of diagnosing disk herniation with
Motor score (05) 4.60 (0.59) 4.63 (0.45) 0.941
CEP herniation and differentiating it from
disk herniation without CEP herniation. Straight leg raising test 48.19 (19.90) 55.68 (22.30) 0.113
result ()

Materials and Methods Visual analog scale


score for pain
Patients
This study was approved by our institutional re- Leg 7.62 (1.63) 8.08 (1.16) 0.221
view board; informed consent was not required be- Back 4.29 (3.28) 4.86 (3.31) 0.477
cause of the retrospective nature of the study. Sev- Oswestry Disability 61.63 (21.83) 62.85 (22.22) 0.825
enty-three patients (45 women, 28 men; mean age, Index score
48 years; range, 2782 years) who underwent mi-
No. of previous 0.97 (1.42) 1.27 (1.56) 0.485
crodiskectomy for lumbar disk herniation between injections
March 2005 and January 2009 and had information
Injection period (d) 58.63 (76.78) 36.24 (42.38) 0.614
in the surgical record about whether CEP herniation
was present were included. All patients underwent NoteExcept for age group and male-to-female ratio, which are numbers of patients with percentages in
parenthesis, data are mean with SD in parentheses.
preoperative lumbar spinal MRI. Before the op- aMann-Whitney test for equality of means unless otherwise indicated.

erations, the following clinical data were assessed bChi-square test with Bonferroni correction.

1076 AJR:204, May 2015


MRI of Lumbar Endplate Herniation

ologist and by an orthopedist, and the two achieved orly as an intraosseous hernia with focal avulsion Modic change was also defined as a change in sub-
consensus. They focused on the spinal level that [1620]. The readers classified an intraosseous her- chondral bone marrow signal intensity in a vertebral
was operated on after MRI was performed. Both niated disk at the posterior corner of a vertebral end- endplate that included the midportion of the end-
observers were blinded to the surgical results, radi- plate with a bony avulsion, particularly on a sagit- plate [22, 23]. Heterogeneous low signal intensity
ologic reports, and clinical information except for tal MR image, as a lumbar posterior marginal node. of extruded material was recorded when the signal
operation level. The examinations were reviewed A dorsal vertebral corner defect was defined, as de- intensity of a herniated disk was heterogeneous and
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at random to avoid bias. After the first session of scribed by previous researchers [15, 21], as a loss had an area of low signal intensity compared with
MRI review, the two readers determined which and rounding off of the posterior corner of a verte- the signal intensity of the mother disk.
items would be assessed on spinal MR images. bra on a sagittal MR image. The presence of a Mod- The assessed MRI findings were further classi-
These items included lumbar posterior marginal ic change in the posterior corner was defined as a fied into three categories: morphologic features of
nodes, dorsal vertebral corner defects, the presence change in subchondral bone marrow signal intensity the posterior corners (lumbar posterior marginal
of Modic changes in the posterior corners, poste- in the vertebral endplate that included the posterior nodes, dorsal corner defects, Modic changes, and
rior osteophytes, irregularities in the midportion of corner of a vertebral body [22, 23]. A posterior os- posterior osteophytes), mid endplates (endplate ir-
an endplate, the presence of Modic changes in the teophyte was considered present when a bony pro- regularities, Modic changes), and extruded material
midportion of an endplate, and heterogeneous low jection was seen at the posterior corner of a verte- (Figs. 24).
signal intensity of extruded material. bral body [24, 25]. A mid endplate irregularity was
A lumbar posterior marginal node has been de- considered present when the linearity and integrity Data and Statistical Analyses
fined as a posterior premarginal intraspongeous her- of the middle portion of an endplate was lost on a Patients were assigned to one of two groups:
niated disk displacing the marginal border posteri- sagittal MR image. The presence of a mid endplate disk herniation with CEP herniation or disk her-
niation without CEP herniation. To determine
the differences between the two groups, a chi-
square test was used to compare categoric vari-
ables (sex, grouped clinical data, MRI findings).
Differences between the quantitative variables
(age, height, weight, BMI, symptom duration,
motor power, sensory change, angle at SLR test,
VAS score, ODI score) of the two groups were
analyzed with the Mann-Whitney test. Statisti-
cally significant variables were also analyzed by
multiple logistic regression to check for the in-
fluence of age, BMI, and sex as covariates. Lin-
ear by linear association was used for the trend
assessment of the MRI scoring system to deter-
A B mine the presence of disk herniation with CEP
herniation. ROC analysis was also performed to
Fig. 267-year-old woman with disk herniation with cartilage endplate herniation. differentiate disk herniation with and disk herni-
A, Sagittal T2-weighted MR image (TR/TE, 3057/100) shows changes in posterior corner: lumbar posterior
marginal node (white arrow), posterior osteophyte (black arrow), and Modic changes (changes in subchondral ation without CEP herniation. The optimal cutoff
bone marrow signal intensity in endplate) (arrowhead). point was defined as the value at which the sum
B, Sagittal T2-weighted MR image (TR/TE, 3057/100) shows mid endplate Modic changes (white arrows) and of the sensitivity and specificity was maximized.
endplate irregularity (black arrow) of vertebral body.
SPSS software (version 17, IBM SPSS) was used
for all calculations. The level of statistical signif-
icance was set at 0.05.

Results
Demographic Data
The demographic data are summarized
in Table 1. Thirty-seven patients (18 men,
19 women; mean age, 51 years; range, 27
82 years) were found at surgery to have disk
herniation with CEP herniation. Disk hernia-
tion with CEP herniation was more common
in patients older than 60 years (10/13, 77%)
than in those younger than 60 years (27/60,
45%) (p = 0.037). There was no significant
Fig. 340-year-old man with disk herniation with Fig. 4 45-year-old man with disk herniation with difference in terms of mean symptom dura-
cartilage endplate herniation. Sagittal T2-weighted cartilage endplate herniation. Sagittal T2-weighted tion, sensory change, motor weakness, SLR
MR image (TR/TE, 3300/115) shows changes of MR image (TR/TE, 3708/120) shows dorsal vertebral
extruded material: heterogeneous low signal corner defect (arrow). test result, VAS score, ODI score, or number
intensity of extruded disk (arrows). of previous epidural injections.

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Joe et al.

TABLE 2: Comparison of MRI Results Among 73 Patients With Disk MRI Findings
Herniation With or Without Cartilage Endplate (CEP) Herniation The MRI findings are summarized in Ta-
ble 2. Lumbar posterior marginal nodes were
Disk Herniation Disk Herniation
Without CEP With CEP significantly more frequent in patients with
Characteristic Herniation Herniation pa pb (23/37, 62%) than in those without (6/36,
17%) CEP herniation (p < 0.001). Posteri-
Lumbar posterior marginal nodes < 0.001 < 0.001
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or osteophytes were also significantly more


Absent 30 14 frequent in patients with disk herniation with
Present 6 23 (16/37, 43%) than in those without (3/36, 8%)
Posterior osteophytes 0.001 0.001 CEP herniation (p = 0.001). Modic changes
in the posterior corners were more common
Absent 33 21
in patients with (26/37, 70%) than in those
Present 3 16 without (14/36, 39%) CEP herniation (p =
Modic changes < 0.001 0.001 0.009). Mid endplate Modic changes (21/37,
Absent 20 6 57%) and mid endplate irregularities (24/37,
65%) were significantly more frequent in pa-
Present 16 31
tients with CEP herniation than in those with-
Modic changes in posterior corners 0.007 0.009 out CEP herniation (6/36, 17%; 8/36, 22%)
Absent 22 11 (p = 0.001; p = 0.001). Heterogeneous low
Present 14 26 signal intensity of herniated disks was sig-
nificantly more frequent in patients with disk
Modic changes in mid endplate < 0.001 0.003
herniation with CEP herniation (19/37, 51%)
Absent 30 16 than in those without CEP herniation (5/36,
Present 6 21 14%) (p = 0.001). The dorsal corner defects,
Mid endplate irregularities < 0.001 0.001 disk levels, volume of disk herniation, pres-
ence of disk migration, and disk degenera-
Absent 28 13
tion in patients with disk herniation with and
Present 8 24 those without CEP herniation were not sig-
Heterogeneous signal intensity of 0.001 0.001 nificantly different (Figs. 5 and 6).
extruded disks MRI scoring was conducted to diagnose
Absent 31 18 disk herniation with CEP herniation accord-
Present 5 19 ing to the six statistically significant MRI
findings (lumbar posterior marginal nodes,
Dorsal vertebral corner defects 0.172 0.263
presence of Modic changes in posterior cor-
Absent 13 8 ners, posterior osteophytes, mid endplate ir-
Present 23 29
TABLE 3: Scores of Six Statistically
Disk level 0.121 0.761 Significant MRI Findings
L2-3 1 0 in Patients With Disk
L3-4 3 1
Herniation With or
Without Cartilage Endplate
L4-5 14 24 (CEP) Herniation
L5-S1 18 12
Disk
Volume of disk herniation 0.436 0.443 Herniation Disk
Without Herniation
Mild 15 11
CEP With CEP
Moderate 18 24 Score Herniation Herniation Total
Severe 3 2 0 12 1 13
Disk migration 0.935 0.476 1 12 1 13
Absent 12 12 2 8 9 17
Present 24 25 3 2 6 8
Disk degeneration (Pfirrmann type) 0.208 0.988 4 2 11 13
C 24 19 5 0 6 6
D 12 6 6 0 3 3
E 0 2 Total 36 37 73
NoteData are numbers of patients. NoteSignificant positive trend was found for MRI
aChi-square test.
score and CEP herniation (p < 0.001) (linear by linear
bMultiple logistic regression analysis with age, body mass index, and sex as covariates.
association).

1078 AJR:204, May 2015


MRI of Lumbar Endplate Herniation

regularities, presence of Modic changes in


mid endplates, and heterogeneous low signal
intensity of extruded material) (Fig. 7). The
presence of each finding was given 1 point,
so scores ranged from 0 to 6. A statistically
significant positive trend was found between
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the MRI score and disk herniation with CEP


herniation (p < 0.001). No patient with disk
herniation without CEP herniation had a
score of 5 or 6 (Table 3 and Fig. 8). The ROC
curve of this scoring system was also gener-
ated. The AUC for diagnosing disk hernia-
tion with CEP herniation using the scoring
system was 0.888. When the MRI scoring
Fig. 537-year-old man with disk herniation without Fig. 667-year-old woman with disk herniation with
criterion for disk herniation with CEP herni- cartilage endplate herniation. Sagittal T2-weighted MR cartilage endplate herniation. Sagittal T2-weighted
ation was set at 2.5, the sensitivity and speci- image (TR/TE, 3100/100) shows only dorsal vertebral MR image (TR/TE, 3057/100) shows mid endplate
ficity were 70% and 90% (Fig. 9). corner defect at superior corner of S1 endplate. irregularity, Modic changes (change in subchondral
bone marrow signal intensity in endplate) in mid
endplate and posterior corner, posterior osteophyte,
Discussion be considered if patients with radiculopathy small lumbar posterior marginal node, and
The results of this study suggest that the have MRI findings suggestive of disk hernia- heterogeneous signal intensity of extruded material.
following six MRI findings are useful for the tion with CEP herniation.
diagnosis of disk herniation with CEP herni- There have been several reports on the tis- microsurgical removal of herniated material,
ation and for differentiating it from disk her- sue composition of herniated material [11, 27 25 patients had hyaline cartilaginous materi-
niation without CEP herniation: lumbar pos- 29]. Schmid et al. [15] compared preoperative al in their extrusions. Similarly, in our study,
terior marginal nodes, Modic changes in the MRI findings and the tissue composition of among 73 patients who had herniated mate-
posterior corners, posterior osteophytes, mid herniated disks. They reported that among 51 rial microsurgically removed, 37 patients had
endplate irregularities, Modic changes in the patients with herniated disks who underwent cartilaginous material in their extruded disks.
mid endplates, and heterogeneous low signal
intensity of extruded material. According to
results of previous studies [12, 26], herniated
disks with CEP herniation are less absorp- 12
tive than herniated disks without CEP herni-
ation. Consequently, patients with disk her-
niation with CEP herniation are more likely
10
to have recurrent episodes of radiculopa-
thy and to need surgical treatment [11, 26].
Therefore, we suggest that early operation
8
No. of Patients

Fig. 7Diagram shows six MRI findings suggesting 0


disk herniation with cartilage endplate herniation: 0 1 2 3 4 5 6
posterior marginal nodes, posterior osteophytes, mid
endplate irregularities, heterogeneous low signal MRI Score
intensity of extruded material, and Modic changes
(changes in subchondral bone marrow signal Fig. 8Histogram shows number of patients who had disk herniation with (gray) and without (black) cartilage
intensity in endplate) in posterior corners and mid endplate (CEP) herniation according to scoring system with six statistically significant MRI findings (06). No
endplates. patient with score of 5 or 6 had CEP herniation.

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Joe et al.

bral corner defects, but contrary to our ex- Conclusion


1.0 pectation, they were not significantly corre- The presence of CEP herniation can be as-
lated with CEP herniations. Dorsal vertebral certained with the following MRI findings:
0.8 corner defects were easily seen in the corner lumbar posterior marginal nodes, posterior
of disk herniations simply as herniated disk osteophytes, mid endplate irregularities, het-
material covering the posterior corner of the erogeneous low signal intensity of extruded
0.6
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Sensitivity

vertebral body on MR images, so they may material, and Modic changes in the posterior
not be related to endplate degeneration. corners and midportion of the endplates.
0.4 In our study, disk herniation with CEP
herniation was more commonly found in References
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0.2
concordant with those in previous histopath- structural properties of the cartilage end-plate and
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1 Specificity
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Fig. 9Graph shows ROC curve determined with
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scoring system using six statistically significant MRI
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MRI of Lumbar Endplate Herniation

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