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Accepted Manuscript

Radiological analysis on kinematical characteristics of Modic changes based on


lumbar disc degeneration grade

Fan Zhang, Hongli Wang, Haocheng Xu, Minghao Shao, M.D, Feizhou Lu, M.D,
Jianyuan Jiang, Xiaosheng Ma, M.D, Xinlei Xia, M.D

PII: S1878-8750(18)30580-1
DOI: 10.1016/j.wneu.2018.03.098
Reference: WNEU 7710

To appear in: World Neurosurgery

Received Date: 8 October 2017


Revised Date: 13 March 2018
Accepted Date: 14 March 2018

Please cite this article as: Zhang F, Wang H, Xu H, Shao M, Lu F, Jiang J, Ma X, Xia X, Radiological
analysis on kinematical characteristics of Modic changes based on lumbar disc degeneration grade,
World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.03.098.

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Introduction
Modic changes (MCs) were firstly reported by Modic et al in the lumbar spine and were
believed to be bone marrow or endplate changes visible on MRI of patients with degenerative
disc disease [1,2]. Generally, there are 3 different types of MCs with different typically
changed MRI signals named as MC I, II and III, sometimes, authors also consider normal

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endplate as Modic Type 0 or Grade 0[2, 3]. During the recent few decades, low back pain was
widely agreed to be associated with MCs [4-8], however, the potential mechanisms remained
unclear. In fact, though most of the authors suggested that low back pain caused by MCs were

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attributed to endplate inflammation or infection [9-14], several researchers proposed that there
was a close relationship between MCs and segmental instability [15, 16]. However, motion

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characteristics of MCs in the lumbar spine was rarely reported and previous results only
showed that MC I might be a unstable phase requiring spinal fusion while MC II might indicate

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translational instability[5,15-18]; Furthermore, considering that segmental motion was
determined both by the intervertebral disc and the endplate, and MCs had a close relationship
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with DD[5,19-21], it is necessary to take DD into consideration in analyzing motion
characteristics for the segments with MCs; Finally, due to the unequal effects of endplate and
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intervertebral disc on segmental motion[21], spine surgeon may have difficulty in determining
segmental motion clinically for the segments with both advanced DD(such as grade E,
indicating greatly reduced segmental motion) and early endplate degeneration(such as MC I,
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indicating segmental hyper-motion). As a result, the purpose of this study is not only to
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comprehensively evaluate the motion differences between different types of MCs, but also to
analyze the kinematical characteristics of MCs based on different DD grades.
Material and Methods
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Patient Population
Informed consent was obtained from all individual participants included in the study, and
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this study was approved by the Ethical Committee of Huashan Hospital of Fudan University.
. 894 consecutive patients(495 men and 399 women) with slight(Visual Analogue Scale, 0
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VAS 3) or tolerable low back pain (3 VAS 6) were reviewed The exclusion criteria
were severe low back pain (VAS 7), trauma, infection, rheumatoid arthritis, spinal tumors,
and history of lumbar spine surgery. A total of 4470 segments from L1/2 to L5/S1 were
retrospectively evaluated for all the patients in this study and those with MCs were selected and
evaluated for statistical comparisons.
Image assessment

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All images were recorded by computer-based measurements and all calculations were
performed with Centricity Web 2.1(GE Healthcare, USA). Midsagittal T2-weighted MR
images were selected for the assessment of the grade of DD, and both T1 and T2-weighted MR
images were used for defining different types of MCs. Briefly, DD was classified into 5 grades
from A to E according to the system proposed by Pfirrmann et al (Table 1) [22]. Grade A

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indicated normal whereas grade E indicated the most advanced DD. MCs were classified into
Type 0, I, II and III. MC 0 indicated normal endplate. Modic Type I had a hypointense signal
on T1-weighted sequences and a hyperintense signal on T2-weighted sequences. Modic Type

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II had a hyperintense signal on T1-weighted sequences and hyper- or isointense signal on
T2-weighted sequences. Type III MCs had a hypointense signal on T1- and T2-weighted

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sequence [1, 2]. All of the MR images were reviewed by two blinded radiologists and κ value
was used to describe the intra- and interobserver reliability of the ratings for MCs(κ=0.945 and

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0.896 ) and the grading for DD(κ=0.901and 0.825).
Segmental angular motion was measured by using X-ray images in flexion and extension
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positions. Both angular and translational motions were recorded. Briefly, vertebral bodies were
marked at 4 points (anterior-inferior, anterior-superior, posterior-superior, and
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posterior-inferior) from L1 to S1. The lowest lumbar vertebra was defined as L5. Total angular
motion was calculated as the absolute value of the difference between the angle between
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adjacent vertebral bodies in flexion and in extension in degrees (Fig. 1a, b). Total translational
motion was also calculated as the absolute value of the difference between flexion and
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extension in millimeters (Fig. 2 d, e). The calculations of all patients were conducted and
recorded by an experienced spine specialist twice within a 12-week interval between
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measurements. The final values of angular and translational motion were the mean of the 2
measurements. κ values of intraobserver reliability in angular and translational motion were
0.912 and 0.821 respectively. For the analysis of interclass error, another examiner performed
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the measurements in 100 segments and the κ value of interobserver reliability in angular and
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translational motion was 0.824 and 0.801 respectively.


Statistical Analysis
Kruskal-Wallis test (with Dunn-Bonferroni test for post hoc comparisons) was applied for
the comparisons in angular and translational motion between MC 0, I, II and III. Data were
presented as x ± S.D and Quartiles were presented as P50[P25, P75]. SPSS (version 19, IBM
Corp. USA) and SAS (version 9.4, NORTH CAROLINA. USA) were used for statistical
analysis. A p value less than 0.05 was considered statistically significant and the statistical
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power was presented as “1-β”.


Results
Prevalence of MCs
MCs were observed in 260 (29.08%) of 894 patients. 308 segments had MCs: Type I in 57
segments, Type II in 217 segments, and Type III in 34 segments. Most of the MCs were found

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at L5/S1 (137), followed by L4/5(97), L3/4(44), L2/3(19) and L1/2(11).
There was no MC in segments with normal discs (DD grade A), and MC III was not observed
in segments with DD grade B either. Also, there are several groups with relatively small

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numbers which are B-MC I (13 segments), C-MC I (7 segments), D-MC I (9 segments), B-MC
II (9 segments), C-MC III (5 segments), D-MC III (12 segments) and E-MC III (17

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segments).(Table 2)
Angular motions of different types of MCs

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Results of angular motion were presented in Table 2, 3 and Fig. 2a. In the group of DD grade
B, there was no statistical difference between MC 0, I and II(P=0.053); In the group of DD
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grade C, MC III had the lowest angular motion though the statistical power were relative
weak(P=0.02), in addition, no statistical difference were found between MC 0, I and II; In the
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group of DD grade D, the angular motion of MC II was significantly higher than that of MC 0,
and MC III still presented the lowest angular motion(P 0.001), in addition, there was no
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difference between MC I and II; In the group of DD grade E, significantly larger angular
motions were found in the segments with MC I as was compared to that of MC II (P
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0.001)though the statistical power was relatively weak, and in this group, MC III still
presented the lowest angular motion.
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Translational motions of different types of MCs


Results of translational motion were presented in Table 2, 3 and Fig. 2b. In the group of DD
grade B, there was no statistical difference in translational motion between MC 0, I and
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II(P=0.21); In the group of DD grade C, MC III had a significantly reduced segmental


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translational motion (P=0.03), and there was no difference in segmental angular motion
between MC 0, I and II; In the group of DD grade D, MC II presented a larger segmental
translational motion than MC 0 with a robust statistical power (P 0.001) but without any
statistical difference when was compared to MC I, in addition, MC III still indicated the
lowest translational motion; There was no difference between MC 0, I, II and III in
translational motion between the segments with DD grade E (P=0.1).
Discussion
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As segmental instability is a potential reason of low back pain in patients with MCs, a
thorough understanding of the kinematical characteristics of MCs is necessary for improving
doctor-patient communication and optimizing treatment selection, however, previous studies
didn’t take the effect of DD on segmental motion into consideration in analyzing motion
characteristics of MCs [5]. As a matter of fact, there is a close relationship between DD and

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MC, and MCs are more likely to present in the segments with advanced DD grades [2, 3, 5,
19, 23, 24], which could explain the fact that why certain MC types were not found at
segments with DD grade A and B in the current study; more importantly, segmental motion

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was determined both by the disc and the endplate, and quite a many authors have proven that
segmental motion could be significantly changed with DD progressing[25, 26], as a result, it is

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important to consider the effects of DD on segmental motion in analyzing kinematical
characteristics of MCs, especially in the segments with advanced DD grades.

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MC I may indicate increased angular motion in DD grade E
Our results indicated that MC-I might increase angular motion in DD grade E. Actually, this
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conclusion was still debatable due to the weak statistical power, however, we could still
consider MC-I as a signal of increased segmental angular motion because many authors had
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proven that MC I might indicate the early phase of endplate degeneration and could cause
segmental instability[3, 15, 17, 18].
It is interesting that statistically increased angular motion was only found in the group of DD
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grade E. Actually, angular motion would significantly be reduced only when DD progressed
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to grade E, indicating that the disc could not maintain normal segmental angular motion [25,
26], and at this time, segmental angular motion might be more likely to be determined by the
endplate, not to mention that the effect of endplate degeneration on segmental angular motion
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are believed to be inherently greater than that of DD [21, 27]; In addition, increased angular
motion is always followed with decreased translational motion and vice versa [5, 25, 26], as a
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result, our result was also supported by the fact that translational motion was relatively small
in the segment with MC I and DD grade E(Fig. 2b). Generally, MC I may increase segmental
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angular motion especially in the segments that were previously believed to be stable, but
more studies need to be done in the future.
MC II may indicate increased translational motion in DD grade D
Translational motions of the segments with MC II were observed to be significantly
increased in the segments with DD grade D with a robust statistical power in our study. This
result was actually agreed with the previously reported conclusion [5], furthermore, higher DD
grades would cause more translational motion especially in the segments with DD grade C and
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D [21, 25, 26], therefore, with DD and endplate degeneration progressing, translational
instability would become more and more obvious. As a result, our result showed that MC II
might be a sign of segmental translational instability especially in the segments with DD grade
D.
MC III indicates a final stable phase and there was no difference in angular and

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translational motion between MC I and II
According to our study, kinematical characteristics of MC III could be easily concluded. As
was showed in Table 1, 2 and Fig.2, MC III showed significantly decreased segmental motions

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both in angle and translation almost in all DD groups, indicating a final stable phase as was
reported previously [1-3].

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We also found that there was no statistical difference in angular and translational motion
between MC I and II in all DD grades except grade E. In fact, the natural course of MC still

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remained unclear, and mixed MC types (especially I/II) were increasingly reported indicating
that MC I and II might belong to the same degenerative phase causing low back pain and they
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were difficult to be clearly separated [28, 29].
This study has several limitations. First, the Pfirmann grading system suffers from
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shortcomings in that it doesn't take age into consideration and has difficulty in assessing disc
pathology in elderly patients; Second, segmental motion is also affected by the level of the
lumbar spine, as a result, the effects of MCs may present different motion characteristics at
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each lumbar level; Third, some groups were of small sample size and consequently resulted
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in weak statistical powers; Finally, it will be better if motion characteristics of MCs could be
correlated to clinical symptoms.
Conclusions
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In conclusion, DD should be taken into consideration in analyzing motion characteristics of


the segments with MCs. MC I and II may increase angular or translational motion in
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segments with advanced DD grades, which were previously believed to be stable. MC III may
indicate a final stable phase and there is no obvious difference in segmental motion between
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MC I and II.

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Acknowledgements:
This study is supported by: National Natural Science Foundation of China (No. 81472036)
(Feizhou Lu received the funding).
Fan Zhang, Hongli Wang, Haocheng Xu contributed equally to this work.
The datasets analyzed during the current study are available from the corresponding author

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on reasonable request.

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27. Li Y, Lord E, Cohen Y, Ruangchainikom M, Wang B, Lv G, Wang JC. Effects of sagittal


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Figure Captions
Fig.1. Examples of angular (a, b) and translational (d, e) motion from flexion to extension. c
and f showed the MRI images of the same case, indicating MC II and DD grade E of L5/S1.

Fig.2. Statistical results of the segmental motions. * indicates that segmental motion of

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MC-III (both angular and translational motion) is statistically lower than any other groups; **
indicates that segmental motion of MC-II (both angular and translational motion) is
statistically different from that of MC-0; *** indicates that the angular motion of MC-I is

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statistically higher than that of MC-II

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Table 1. DD grading system proposed by Pfirrmann et al


Distinction of Signal Height of
Grade Structure
Nucleus and Anulus Intensity Intervertebral Disc
Hyperintense,
Homogeneous, isointense to

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A (I) Clear Normal
bright white cerebrospinal
fluid

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Hyperintense,
Inhomogeneous
isointense to
B (II) with or without Clear Normal

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cerebrospinal
horizontal bands
fluid
C Inhomogeneous, Normal to slightly

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Unclear Intermediate
(III) gray decreased

D Inhomogeneous,
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Lost
Intermediate
to
Normal to
moderately
(IV) gray to black
hypointense decreased
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Inhomogeneous, Collapsed disc
E (V) Lost Hypointense
black space
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Table 2. Number, angular motion and translational motion of the segments with Disc
degeneration and Modic changes x ± S.D
Modic 0 Modic I Modic II Modic III
96 (seg.) / / /
A 4.93±1.75° / / /

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0.63±0.52mm / / /
359(seg.) 13(seg.) 9(seg.) /

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B 5.66±1.41° 5.01±1.69° 4.99±2.97° /
1.38±0.83mm 1.55±0.30mm 1.49±0.34mm /

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301(seg.) 7(seg.) 35(seg.) 5(seg.)
C 5.77±2.52° 5.40±3.84° 6.18±4.02° 1.54±0.75°
1.35±0.80mm 1.61±1.35mm 1.62±1.06mm 0.39±0.25mm

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198(seg.) 9(seg.) 112(seg.) 12(seg.)
D 4.6±1.35°
1.02±0.72mm
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4.47±3.20°
1.48±0.98mm
4.23±2.02°
2.14±0.76mm
1.06±0.59°
0.43±0.39mm
38(seg.) 28(seg.) 61(seg.) 17(seg.)
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E 2.63±1.10° 6.37±3.08° 4.42±2.38° 1.46±1.19°
0.62±0.38mm 0.46±0.43mm 0.67±0.63mm 0.38±0.37mm
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Seg. = Segments
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Table 3: Statistical results of the comparisons in segmental motions between different


types of Modic Changes
Translational
Groups Angular Motion XA.2 XT.2 pA. pT. 1-βA. 1-βT.
Motion
A-MC 0 4.59[4.24, 4.99] 0.54[0.13, 0.99] / / / / / /

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B-MC 0 5.64[4.99, 6.5] 1.33[0.85, 1.77] 5.86 3.14 0.053 0.21 0.64 0.82
B-MC I 5.45[4.74, 6.09] 1.64[1.20, 1.73]

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B-MC II 4.29[3.68, 5.81] 0.85[1.33, 1.77]
C-MC 0 6.03[5.07, 7.27] 1.29[0.70, 1.85] 9.68 9.29 0.02 0.03 0.19 0.38

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C-MC I 5.07[0.83 ,9.97] 1.49[0.24, 2.95]
C-MC II 6.11[3.29, 9.56] 1.48[0.93, 1.94]
C-MC

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1.64[0.78, 2.26] 0.28[0.15 ,0.66]
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D-MC 0
D-MC I
4.67[4.21, 5.33]
4.48[1.87, 6.68]
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0.93[0.50, 1.47]
1.24[0.67, 2.54]
41.62 141.33 0.00 0.00 0.65 0.84

D-MC II 4.09[3.10, 5.10] 2.08[1.67, 2.49]


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D-MC
1.25[0.41, 1.43] 0.31[0.10, 0.75]
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E-MC 0 2.50[2.07, 3.25] 0.60[0.34, 0.89] 31.95 6.30 0.00 0.10 0.34 0.60
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E-MC I 7.92[3.45, 8.89] 0.39[0.08, 0.80]


E-MC II 4.31[2.38, 6.32] 0.47[0.15, 1.00]
E-MC
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0.85[0.60, 2.22] 0.20[0.13, 0.66]


III
MC=Modic Change
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A.=Angular Motion
T.=Translational Motion
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1. Kinematical characteristics of MCs should be analyzed based on disc degeneration grade.

2. MC I may increase angular motion in segments with DD grade E and MC II indicates

more translational motion in segments with DD grade D.

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3. MC III indicates a final stable phase of segmental motion.

4. There is no difference in segmental motion between MC I and II.

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Abbreviations:

MC: Modic Change

DD: Disc Degeneration

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