The Spine Journal 17 (2017) 12721284

Clinical Study

Kinematic evaluation of cervical sagittal balance and thoracic inlet

alignment in degenerative cervical spondylolisthesis using kinematic
magnetic resonance imaging
Permsak Paholpak, MDa,b, Alexander Nazareth, BSa, Patrick C. Hsieh, MDc,
Zorica Buser, PhDa,*, Jeffrey C. Wang, MDa
a
Department of Orthopaedic Surgery, Keck School of Medicine, University of Southern California, 2011 Zonal Ave, HMR710, Los Angeles, CA 90033, USA
b
Department of Orthopaedics, Faculty of Medicine, Khon Kaen University, 123 Mittraparp Highway, Muang District, Khon Kaen 40002, Thailand
c
Department of Neurological Surgery, Keck School of Medicine, University of Southern California, 1520 San Pablo St Suite 3800, Los Angeles,
CA 90033, USA
Received 8 August 2016; revised 19 January 2017; accepted 24 April 2017

Abstract BACKGROUND CONTEXT: T1 slope is a novel thoracic parameter used to assess cervical spine
sagittal balance. Thoracic index (TI) parameters including T1 slope and cervical sagittal alignment
parameters may play an important role in degenerative cervical spondylolisthesis (DCS). Current
literature regarding the relationship between TI and cervical sagittal alignment parameters in pa-
tients with DCS is limited.
PURPOSE: (1) To evaluate the T1 slope, cervical sagittal alignment, and thoracic inlet parameter
in patients with DCS using kinematic magnetic resonance imaging (kMRI), and (2) to find a cor-
relation between the T1 slope, TI, and other cervical sagittal parameters in patients with DCS.
DESIGN/SETTING: Retrospective kMRI study, Level III.
PATIENT SAMPLE: Fifty-two patients with DCS from 1,128 patients from a cervical kMRI database.
OUTCOME MEASURES: T1 slope, C2C7 angle, sagittal vertical axis C2C7 (SVA C2C7), cranial
tilt, cervical tilt, neck tilt, and thoracic inlet angle (TIA).
METHODS: Cervical spine kMRIs of 52 patients with DCS (mean age 51.7standard deviation)
were analyzed in neutral, flexion, and extension positions. Patients with DCS were divided into two
groups: anterolisthesis (N=33) and retrolisthesis (N=19). Each listhesis group was subclassified into
grade 1 (slip 23 mm) and grade 2 (slip>3 mm).
RESULTS: Grade 2 retrolisthesis had the largest T1 slope followed by grade 1 retrolisthesis, grade
2 anterolisthesis, and grade 1 anterolisthesis. Significant differences were found between the
anterolisthesis and the retrolisthesis groups in the neutral position (p=.025). The flexion position had
the largest T1 slope and showed a significant difference with anterolisthesis in the neutral position
(p=.041). Sagittal vertical axis C2C7 showed strong correlation with cranial tilt in all DCS groups
and all positions.

FDA device/drug status: Not applicable.
Author disclosures: PP: Nothing to disclose. AN: Nothing to disclose.
PCH: Consulting: DePuy Synthes (D), Medtronic (E), outside the submit-
ted work. ZB: Consulting: Xenco Medical (B), AO Spine (B). JCW: Royalties:
Aesculap (B), Biomet (G), Amedica (C), SeaSpine (D), Synthes (C); Stock
Ownership: Fziomed (2500 shares, 1%, <1%); Private Investments:
Promethean Spine (1 shares, 1%, <1% of entity, unknown amount of shares),
Paradigm Spine (1 shares, 1%, <1% of entity, unknown amount of shares),
Benevenue (1 shares, 1%, <1% of entity, unknown amount of shares), NexGen
(1 shares, 1%, <1% of entity, unknown amount of shares), Vertiflex (1 shares,
1%, <1% of entity, unknown amount of shares), ElectroCore (1 shares, 1%,
<1% of entity, unknown amount of shares), Surgitech (1 shares, 1%, <1%
of entity, unknown amount of shares), Expanding Orthopaedics (33000 shares,
1%, 33,000 options, <1% of entity), Osprey (10 shares, 1%, 10 options, <1%
of entity), Bone Biologics (51255 shares, 1%, 51,255 options, <1% of entity),
CurativeBiosciences (1875 shares, 1%, 1875 options, <1% of entity),
PearlDiver (25000 shares, 1%, 25,000 options, <1% of entity); Board of Di-
rectors: North American Spine Society (nonfinancial), North American Spine
Foundation (nonfinancial), Cervical Spine Research Society (nonfinancial,
reimbursement for travel for board meetings), AO Spine (E), AO Founda-
tion (E); Fellowship Support: AO Foundation (E, Paid directly to institution/
employer), outside the submitted work.
The disclosure key can be found on the Table of Contents and at
www.TheSpineJournalOnline.com.
* Corresponding author. Department of Orthopaedic Surgery, Keck
School of Medicine, University of Southern California, Elaine Stevely
Hoffman Medical Research Center, HMR 710, 2011 Zonal Ave, Los Angeles,
CA 90033, USA. Tel: +1 323-442-0206.
E-mail address: zbuser@usc.edu (Z. Buser)

http://dx.doi.org/10.1016/j.spinee.2017.04.026
1529-9430/ 2017 Elsevier Inc. All rights reserved.
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284
CONCLUSIONS: In our study, T1 slope was larger in grade 2 DCS, and the retrolisthesis group
had larger T1 slope than the anterolisthesis group. Presence of larger T1 slope was significantly cor-
related with larger cervical lordosis curvature. Furthermore, cranial tilt was strongly correlated with
SVA C2C7. 2017 Elsevier Inc. All rights reserved.
Keywords: Cervical sagittal parameters; Cervical spine; Degenerative cervical spondylolisthesis; kMRI; Spondylolisthesis;
T1 slope; Thoracic index parameters
Introduction
Degenerative cervical spondylolisthesis (DCS) is one of
the most common indications of cervical spine surgery, par-
ticularly in patients older than 50 years of age [14]. The
prevalence of DCS has been reported in the literature, with
wide variation from 3.9% to 20% [1,5,6], which may reflect
the lack of well-defined diagnostic criteria.
Previous studies have defined DCS as a translation of the
vertebra for more than 2 mm in the anterior (anterolisthesis)
or the posterior (retrolisthesis) direction [510]. Park et al.
found that in patients with DCS, both anterolisthesis and
retrolisthesis were stable in disease progression between 2
and almost 8 years after the initial diagnosis [1]. Preopera-
tive retrolisthesis showed higher incidence of postoperative
instability and reoccurrence of retrolisthesis compared with
baseline anterolisthesis [1,11]. Xu et al. [12] reported that ap-
proximately 92% of patients with C4C5 DCS who underwent
anterior fusion had retrolisthesis.
Current literature regarding the etiology and predispos-
ing factors for DCS is limited, although these have been
well studied in lumbar spondylolisthesis [13]. Deburge et al.
[3] suggested that DCS more commonly occurs in the cer-
vical spine mid-region because of relative hypermobility in
conjunction with degenerative change of facets and laxity
of surrounding ligaments. Liu et al. proposed that disc and
facet joint degeneration occurred simultaneously, and that
both may be initiating causes in altering spine mechanics,
resulting in DCS [14]. Xu et al. found facet tropism and T1
slope to be preoperative risk factors for the development of
DCS [12]. T1 slope is a novel thoracic parameter that re-
flects cervical spine sagittal balance and may have similar
importance to pelvic incidence in the lumbosacral spine
[8,1517]. Previous studies have reported a correlation between
the T1 slope and C2C7 Cobb angle [15,16,18], sagittal
vertical axis (SVA) [15], and poor clinical outcome after
laminoplasty [19]. Jun et al. demonstrated that the DCS
anterolisthesis group had significantly higher T1 slope than
a control group [8]. To the best of our knowledge, there are
no published kinematic magnetic resonance imaging (kMRI)
studies on the relationship between thoracic index (TI)
and cervical sagittal alignment parameters in patients with
DCS.
The aims of this study were to (1) evaluate T1 slope, cer-
vical sagittal alignment, and thoracic inlet parameter in patients
with DCS using kMRI, and (2) find correlation between T1
slope, TI, and other cervical sagittal parameters in patients
with DCS.
1273
Materials and methods
Study design
This is a retrospective cross-sectional study.
Selection of patients and grouping
Institutional review board approval was obtained before
initiation of the study. We retrospectively reviewed 1,128 pa-
tients with neck pain who were referred by their physicians
to private radiology centers to obtain kMRI of the cervical
spine between November 2010 and February 2016. Exclu-
sion criteria included diagnosis of congenital anomaly, spinal
deformity, inflammatory diseases, infection, tumor, or pre-
vious cervical spine surgery.
Degenerative cervical spondylolisthesis was defined as an-
terior (anterolisthesis group) or posterior (retrolisthesis group)
based on the direction of slippage with more than 2 mm of
the cephalad vertebra on the caudad vertebra [610]. Degen-
erative cervical spondylolisthesis was divided into grade 1
(slip 23 mm) and grade 2 (slip>3 mm) [5].
Kinematic magnetic resonance imaging
Kinematic magnetic resonance imaging of the cervical spine
was performed using a 0.6 Tesla MRI scanner (Upright Multi-
Position, Fonar Corp, New York, NY, USA). The MR unit uses
a vertical orientation of two opposing magnetic doughnuts, al-
lowing patients to be scanned in the weight-bearing position.
The image protocol included T1- and T2-weighted sagittal fast
spin echo images that were obtained using a flexible surface
coil with the patient seated in upright weight-bearing neutral
(0), flexion (40), and extension (20) positions. The imaging
protocol for T1-weighted sagittal spin echo images included
repetition time 671 ms, echo time 17 ms, thickness 4.0 mm,
field of view 30 cm, matrix 256224, number of excitations
2, and for the T2-wighted fast spin echo images protocol con-
sisted of repetition time 3,000 ms, echo time 140 ms, thickness
4.0 mm, field of view 30 cm, matrix 256224, number of ex-
citations 2. Images were viewed using the eRAD PACS system
(version 7.2.38.0, Greenville, SC, USA).
Thoracic index parameters
T1 slope was measured as the angle between a horizon-
tal line and the T1 upper end plate. Neck tilt (NT) was defined
as the angle formed by a vertical line passing through the upper
border of the sternum and a second line drawn from the
1274 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284

A B

C D

Fig. 1. Cervical sagittal parameters and thoracic inlet parameters measurement on kinematic magnetic resonance imaging (kMRI) image. (A) C2C7 angle
and T1 slope. (B) Sagittal vertical axis C2C7 (SVA C2C7) and T1 slope. (C) Cervical tilt and cranial tilt. (D) Thoracic inlet angle (TIA) and neck tilt
angle.

sternum tip through the center of the T1 upper end plate. Tho-
racic inlet angle (TIA) was defined as the angle formed by
a perpendicular line off the T1 upper end plate and another
line connecting the center of the T1 upper end plate and the
upper point of the sternum (Fig. 1). Thoracic inlet angle was
calculated as the sum of T1 slope and NT [8,15].
Cervical spine sagittal alignment parameters
The C2C7 angle, cervical lordotic curvature measure-
ment, was defined as the angle between the tangent lines
of the lower end plates of C2 and C7 (Fig. 1A). The posi-
tive value was defined as kyphotic alignment, whereas the
negative value indicates lordotic alignment.
Sagittal vertical axis C2C7, which assessed the orienta-
tion of C2 in relation to C7 in the horizontal plane, is the
horizontal distance between the center of C2 and the posterior
edge of the C7 upper end plate (Fig. 1B). The center of C2
was determined as the point of intersection of crossing di-
agonals within the C2 vertebral body on the central sagittal
kMRI picture (Fig. 1B, C) [15,20]. A positive value indi-
cated that the center of C2 was anterior to the posterior edge
of the C7 upper end plate, whereas a negative value indi-
cated that the center of C2 was posterior.
Orientation parameters including cervical tilt and cranial
tilt were measured [15]. Cervical tilt was defined as the angle
formed between a perpendicular line off the center of the T1
upper end plate and another line extending from the center
of the T1 upper end plate to the center of C2. A positive value
indicated that the line extending from the center of the T1
upper end plate to the center of C2 is anterior to the perpen-
dicular line off the center of the T1 upper end plate, whereas
a negative value indicated that the line was posterior. The cranial
tilt was defined as the angle formed between the line from
the center of the T1 upper end plate through the C2 center
and a vertical line off the center of the T1 upper end plate
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284 1275

(Fig. 1C). A positive value indicated that the line extending
from the center of the T1 upper end plate to the center of C2
was anterior to the vertical line off the center of the T1 upper
end plate, whereas a negative value indicated that the line was
posterior.
Statistical analysis
The sample size of 54 in each DCS group was calcu-
lated by using the effect size of 0.549 and the power of 0.8.
The effect size was calculated by using the mean and stan-
dard deviation of T1 slope from the anterolisthesis (21.548.18)
and the retrolisthesis (26.469.68) groups in neutral posi-
tion. Unfortunately, from 1,128 patients with cervical kMRI,
only 52 had DCS.
Differences between TI and cervical spine parameters in
flexion, neutral, and extension were analyzed using Wilcoxon
signed rank test. Mann-Whitney U test was performed to
analyze differences in TI and cervical spine parameters
between the two listhesis groups. Wilcoxon signed rank test
was used to analyze between grades within each listhesis
group. Pearson correlation coefficient was used to test the cor-
relation between TI and cervical sagittal parameters.
Interobserver agreement between the two examiners and
intraobserver agreement by one reader were analyzed using
kappa statistics. One examiner has 6 years of experience in
spine surgery. The other examiner has 1 year of experience
in spine radiographic measurement. All statistical analyses
were performed in SPSS Statistics (Version 23.0, IBM,
Chicago, IL, USA). Statistical significance was set at p<.05.
Results
Out of 1,128 reviewed patients, a total of 52 patients with
DCS (mean age: 51.78.64, 54% female) met the eligibility
criteria. Thirty-three patients (mean age: 50.158.92, 60.6%
female) were classified into the anterolisthesis group, with 16
patients having grade 1 and 17 patients having grade 2 ante-
rior DCS. Nineteen patients (mean age: 54.427.6, 57.9% male)
were classified in the retrolisthesis group: 14 patients were grade
1, and 5 patients were grade 2. The CONsolidated Standards
of Reporting Trials diagram is shown in Fig. 2. The affected
levels in the anterolisthesis group were C4C5 (40%), C5C6
(13.5%), and C3C4 (9.6%), whereas in the retrolisthesis group
they included C5C6 (15.4%), C4C5 (9.6%), C3C4 (7.7%),
and C6C7 (3.8%). Eight patients had more than one level
of DCS; these patients were classified using the spinal level,
which showed the greatest magnitude of translation. Table 1

Fig. 2. CONsolidated Standards of Reporting Trials (CONSORT) diagram. DCS, degenerative cervical spondylolisthesis; kMRI, kinematic magnetic reso-
nance imaging.

Table 1
Demographic data of patients with cervical degenerative spondylolisthesis (DCS)

Patients Age Gender Cervical level

DCS (N) MeanSD Male Female C3C4 C4C5 C5C6 C6C7
Overall 52 51.718.64 24 28 9 26 15 2
Anterolisthesis 33 50.158.92 13 20 5 21 7 0
Grade 1 16 50.137.3 8 8 3 10 3 0
Grade 2 17 50.1710.45 5 12 2 11 4 0
Retrolisthesis 19 54.427.6 11 8 4 5 8 2
Grade 1 14 55.648.1 5 6 2 5 6 1
Grade 2 5 515.14 3 2 2 0 2 1
SD, standard deviation.
1276 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284

representsthe patients demographic data and DCS level dis- intra- and interobserver agreement values (kappa values) of all
tribution. For the NT and TIA parameters, two patients (one parameters.
grade 1 anterolisthesis and one grade 1 retrolisthesis) were ex- Significant differences in kinematic parameters were found
cluded because of the low image quality. Table 2 shows the between the anterolisthesis and the retrolisthesis groups in
all three positions (Table 3, Fig. 3, Left, Middle, Right). The
retrolisthesis group had significantly more cervical lordosis
Table 2 in the neutral position only (p=.004). The anterolisthesis group
Intra- and interobserver reliability values (kappa values) of all parameters
had significantly higher SVA C2C7 in both neutral and ex-
Parameter Intraobserver Interobserver tension positions (p=.02). The retrolisthesis group had
C2C7 angle 0.893 0.861 significantly higher T1 slope in the neutral position only (p=.03).
SVA C2C7 0.991 0.884 The retrolisthesis group had significantly more negative cer-
T1 slope 0.93 0.857
Neck tilt 0.927 0.88
vical tilt in all three positions (neutral: p<.001, flexion: p=.01,
TIA 0.902 0.873 extension: p=.03). Cranial tilt angle was significantly lower
Cervical tilt 0.931 0.861 in the retrolisthesis group in the neutral (p=.03) and exten-
Cranial tilt 0.898 0.874 sion (p=.04) positions. There were no significant differences
SVA, sagittal vertical axis; TIA, thoracic index angle. between grade 1 and grade 2 DCS in the anterolisthesis

Table 3
Difference between the anterolisthesis and the retrolisthesis groups
Difference between
anterolisthesis
All cases (N=52) Anterolisthesis (N=33) Retrolisthesis (N=19) and retrolisthesis
MeanSD MeanSD MeanSD p-value
C2C7 angle
Neutral 5.2910.88 1.789.23 11.3811.05 .004*
Flexion 13.7712.33 14.8013.85 11.999.18 .482
Extension 23.2211.46 21.1112.07 26.879.56 .079
SVA C2C7
Neutral 26.3410.38 28.9910.25 21.729.1 .015*
Flexion 45.2511.74 47.2710.83 41.7512.71 .157
Extension 11.4512.18 14.1612.30 6.7610.72 .015*
T1 slope
Neutral 23.348.99 21.548.18 26.469.68 .025*
Flexion 26.2111.47 25.2411.93 27.8810.73 .582
Extension 23.548.75 22.38.77 25.678.52 .414
Neck tilt (N=50) (N=32) (N=18)
Neutral 47.6210.27 46.6510.23 49.3510.41 .233
Flexion 48.9810.77 48.5611.7 49.749.18 .701
Extension 48.619.55 48.239.44 49.299.98 .578
TIA (N=50) (N=32) (N=18)
Neutral 72.1912.07 69.239.9 77.4613.99 .37
Flexion 76.5711.52 75.310.3 78.8313.45 .396
Extension 72.211.5 70.410.26 75.4113.13 .091
Cervical tilt
Neutral 7.68.14 3.685.86 14.407.06 <.000*
Flexion 3.898.75 6.527.37 0.699.25 .010*
Extension 15.6313.36 14.29.07 18.1018.68 .032*
Cranial tilt
Neutral 15.78.63 17.88.32 12.068.13 .025*
Flexion 30.0610.88 31.7110.7 27.1910.87 .220
Extension 6.088.94 8.19.53 2.576.68 .036*
SVA, sagittal vertical axis; TIA, thoracic index angle; SD, standard deviation.
* Statistically significant difference.

A positive value means kyphosis; negative value means lordosis.

A positive value means the center of C2 is anterior to the posterior edge of the C7 upper end plate; a negative value means the center of C2 is posterior
to the posterior edge of the C7 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the perpendicular line off the
center of the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the
perpendicular line off the center of the T1 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the vertical line off the center of
the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the vertical line
off the center of the T1 upper end plate.
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284 1277

Fig. 3. The figure shows the difference in cervical sagittal parameters and thoracic index parameters between anterolisthesis and retrolisthesis in three po-
sitions. (Left) In neutral position. (Middle) In flexion position. (Right) In extension position. *Statistically significant difference at p-value of less than .05.
SVA C2C7, sagittal vertical axis C2C7; SD, standard deviation.
1278 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284

Table 4
Comparison of all parameters between grades of slip in each spondylolisthesis group
Anterolisthesis (N=33) Retrolisthesis (N=19)
Grade 1 (N=16) Grade 2 (N=17) Grade 1 (N=14) Grade 2 (N=5)
Standard Standard Standard Standard
Mean deviation Mean deviation p-Value Mean deviation Mean deviation p-Value
C2C7 angle Neutral 2.16 9.44 1.42 9.31 .877 12.11 11.30 9.34 11.28 .345
Flexion 15.94 16.56 13.72 11.13 .959 12.30 8.00 11.14 13.06 .686
Extension 20.58 12.90 21.61 11.60 .836 27.74 9.30 24.46 10.97 .345
SVA C2C7 Neutral 25.96 11.02 31.85 8.86 .063 20.09 9.23 26.30 7.74 .5
Flexion 45.21 10.57 49.21 11.02 .234 41.33 13.72 42.94 10.62 .5
Extension 12.84 13.09 15.41 11.77 .642 3.31 8.12 16.42 12.01 .013
T1 slope* Neutral 20.18 8.25 22.83 8.14 .334 25.61 7.85 28.82 14.56 .893
Flexion 24.04 11.47 26.37 12.60 .460 27.06 9.88 30.20 13.86 .5
Extension 21.16 9.37 23.37 8.32 .820 25.81 9.88 25.28 3.01 .5
Neck tilt* Neutral 50.45 10.76 43.29 8.71 .1 49.04 12.13 50.16 4.27 .686
Flexion 52.49 12.54 45.09 10.02 .132 48.45 9.55 53.12 8.04 .5
Extension 50.77 9.72 45.99 8.87 .427 49.06 10.93 49.90 8.00 .893
TIA Neutral 71.07 10.09 67.61 9.73 .478 76.55 14.45 79.82 14.02 .345
Flexion 77.13 7.89 73.68 12.04 .394 77.04 13.32 83.48 14.13 .893
Extension 72.03 11.72 68.96 8.88 .460 74.71 14.58 77.24 9.46 .345
Cervical tilt Neutral 4.67 5.86 2.76 5.89 .642 14.77 7.08 13.36 7.74 .345
Flexion 5.71 7.70 7.28 7.19 .642 .03 9.59 2.70 8.91 .893
Extension 14.69 9.59 13.74 8.82 .877 25.29 8.62 2.02 25.34 .08
Cranial tilt Neutral 15.39 8.25 20.07 7.95 .134 10.84 7.84 15.46 8.85 .686
Flexion 29.75 9.53 33.55 11.68 .326 27.09 11.07 27.50 11.53 .893
Extension 6.47 9.66 9.63 9.43 .6 .52 6.06 8.30 5.08 .04
SVA, sagittal vertical axis; TIA, thoracic index angle.
* Number of samples: anterolisthesis=32, Gr 1 anterolisthesis=15, retrolisthesis=18, Gr 1 retrolisthesis=13.

Statistically significant difference; Wilcoxon signed rank test.

A positive value means kyphosis; a negative value means lordosis.

A positive value means the center of C2 is anterior to the posterior edge of the C7 upper end plate; a negative value means the center of C2 is posterior
to the posterior edge of the C7 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the perpendicular line off the
center of the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the
perpendicular line off the center of the T1 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the vertical line off the center of
the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the vertical line
off the center of the T1 upper end plate.

group across all positions (Table 4). For the retrolisthesis group,
grade 2 showed significantly higher SVA C2C7 (p=.018),
cervical tilt (p=.016), and cranial tilt (p=.018) than did grade
1 in the extension position only.
Significant differences were found when comparing the
anterolisthesis and the retrolisthesis groups within each spon-
dylolisthesis grade (Table 5). In grade 1 DCS, the retrolisthesis
group had a significantly lower C2C7 angle (p=.02) and cer-
vical tilt (p=.001) in the neutral position. Degenerative cervical
spondylolisthesis grade 1 retrolisthesis also had lower cer-
vical tilt (p=.005) and SVA C2C7 (p=.04) than the grade 1
anterolisthesis in extension. For grade 2, the retrolisthesis group
had significantly higher TIA (p=.046) and lower cervical tilt
(p=.014) in the neutral position. Grade 2 retrolisthesis also
had lower cervical tilt than grade 2 anterolisthesis in the flexion
position (p=.046).
T1 slope was significantly higher in the retrolisthesis group
than in the anterolisthesis group, and in grade 2 than in grade
1 (Table 6). For C2C7 angle, the retrolisthesis group, com-
pared with the anterolisthesis group, had more lordosis and
showed more lordosis in grade 1 than in grade 2 in the neutral
position, but in flexion position, grade 2 had more lordosis
than grade 1. In the extension, retrolisthesis grade 2 had less
lordosis than grade 1, but anterolisthesis grade 2 still had more
lordosis than grade 1, but the difference between them is small
(Fig. 4). The T1 slope showed a statistically significant dif-
ference between the neutral and the flexion position in the
anterolisthesis group (Fig. 5).
In the neutral position, overall DCS, T1 had a statistical-
ly significant correlation with C2C7 angle, SVA C2C7,
NT, TIA, cervical tilt, and cranial tilt (Table 7). For the
anterolisthesis group, T1 slope showed a statistically signif-
icant correlation with C2C7 angle, SVA C2C7, NT, cervical
tilt, and cranial tilt. In the retrolisthesis group, the T1 slope
showed a significant correlation with C2C7 angle, SVA
C2C7, TIA, cervical tilt, and cranial tilt. In the flexion po-
sition, for overall DCS, the T1 slope showed a significant
correlation with SVA C2C7, NT, TIA, cervical tilt, and cranial
tilt. For anterolisthesis, the T1 slope showed a significant re-
lation with SVA C2C7, TIA, NT, cervical tilt, and cranial
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284 1279

Table 5
Comparison of all parameters in the same grade of slip between the anterolisthesis group and the retrolisthesis group
Grade 1 spondylolisthesis Grade 2 spondylolisthesis
Anterolisthesis (N=16) Retrolisthesis (N=14) Anterolisthesis (N=17) Retrolisthesis (N=5)
Standard Standard Standard Standard
Mean deviation Mean deviation p-Value Mean deviation Mean deviation p-Value
C2C7 angle Neutral 2.16 9.44 12.11 11.30 .017 1.42 9.31 9.34 11.28 .183
Flexion 15.94 16.56 12.30 8.00 .950 13.72 11.13 11.14 13.06 .273
Extension 20.58 12.90 27.74 9.30 .114 21.61 11.60 24.46 10.97 .505
SVA C2C7 Neutral 25.96 11.02 20.09 9.23 .145 31.85 8.86 26.30 7.74 .183
Flexion 45.21 10.57 41.33 13.72 .724 49.21 11.02 42.94 10.62 .170
Extension 12.84 13.09 3.31 8.12 .046 15.41 11.77 16.42 12.01 .724
T1 slope* Neutral 20.18 8.25 25.61 7.85 .036 22.83 8.14 28.82 14.56 .224
Flexion 24.04 11.47 27.06 9.88 .547 26.37 12.60 30.20 13.86 .784
Extension 21.16 9.37 25.81 9.88 .371 23.37 8.32 25.28 3.01 .754
Neck tilt* Neutral 50.45 10.76 49.04 12.13 .908 43.29 8.71 50.16 4.27 .078
Flexion 52.49 12.54 48.45 9.55 .475 45.09 10.02 53.12 8.04 .147
Extension 50.77 9.72 49.06 10.93 .908 45.99 8.87 49.90 8.00 .411
TIA Neutral 71.07 10.09 76.55 14.45 .311 67.61 9.73 79.82 14.02 .046
Flexion 77.13 7.89 77.04 13.32 1.000 73.68 12.04 83.48 14.13 .183
Extension 72.03 11.72 74.71 14.58 .322 68.96 8.88 77.24 9.46 .127
Cervical tilt Neutral 4.67 5.86 14.77 7.08 .001 2.76 5.89 13.36 7.74 .014
Flexion 5.71 7.70 .03 9.59 .151 7.28 7.19 2.70 8.91 .046
Extension 14.69 9.59 25.29 8.62 .005 13.74 8.82 2.02 25.34 .225
Cranial tilt Neutral 15.39 8.25 10.84 7.84 .119 20.07 7.95 15.46 8.85 .290
Flexion 29.75 9.53 27.09 11.07 .632 33.55 11.68 27.50 11.53 .389
Extension 6.47 9.66 .52 6.06 .096 9.63 9.43 8.30 5.08 .938
SVA, sagittal vertical axis; TIA, thoracic index angle.
* Number of samples: anterolisthesis=32, Gr 1 anterolisthesis=15, retrolisthesis=18, and Gr 1 retrolisthesis=13.

Statistically significant difference.

A positive value means kyphosis; a negative value means lordosis.

A positive value means the center of C2 is anterior to the posterior edge of the C7 upper end plate; a negative value means the center of C2 is posterior
to the posterior edge of the C7 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the perpendicular line off the
center of the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the
perpendicular line off the center of the T1 upper end plate.

A positive value means the line extending from the center of the T1 upper end plate to the center of C2 is anterior to the vertical line off the center of
the T1 upper end plate; a negative value means the line extending from the center of the T1 upper end plate to the center of C2 is posterior to the vertical line
off the center of the T1 upper end plate.

tilt. For retrolisthesis, the T1 slope showed a significant re-
lationship with SVA C2C7, TIA, and cranial tilt. In the
extension position, for overall DCS, T1 slope showed a sig-
nificant relationship with C2C7 angle, cervical tilt, cranial
tilt, and TIA. For anterolisthesis, the T1 slope showed a sig-
nificant correlation with C2C7 angle, SVA C2C7, cervical
tilt, cranial tilt, and TIA. For retrolisthesis, T1 slope showed
a significant correlation with TIA only.
Discussion
The prevalence of DCS has been reported in the literature
to vary from 4% to 29% [15]. Similarly, in our study, the
prevalence of DCS was 4.6% (2.9% anterolisthesis, 1.7%
retrolisthesis). The most common affected levels were C4C5
in the anterolisthesis group, and C5C6 in the retrolisthesis
group.
Previous kMRI studies evaluated T1 slope only in the neutral
position [8,16,17,19]. Jun et al. suggested that large T1 slope
may be one of the predisposing factors in the onset of
anterolisthesis DCS by increasing TIA and, therefore, in-
creasing the C2C7 lordosis [8]. T1 slope is used to determine
the sagittal balance of the cervical spine and has been pre-
viously correlated with C2C7 angle and SVAC2C7 [8,15,20].
Patients with a high T1 slope may rely on the posterior para-
spinal neck muscles to maintain horizontal gaze and mini-
mize the energy expenditure from head positioning. Regarding
the posterior neck muscle compensation, several studies hy-
pothesized that the posterior neck muscle compensation was
one important preventive mechanism from postoperative
cervical kyphosis progression, especially in patients with high
T1 slope [15,16]. Weakness of the posterior neck muscle in-
creased the chance of postoperative kyphosis progression and
even influenced head deformity [15,19,21,22]. Weng et al. pos-
tulated that in patients with higher T1 slope, the posterior neck
muscle played an important role in maintaining cervical lor-
dosis to maintain horizontal gaze and minimize energy
expenditure from head position [15].
The T1 slope results and its correlation with C2C7
angle and SVA C2C7 may be hypothetically explained by
1280 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284

Fig. 4. The figure demonstrates the difference between grading of DCS in three positions. (Left) In neutral position. (Middle) In flexion position. (Right) In
extension position. *Statistically significant difference at p-value of less than .05. DCS, degenerative cervical spondylolisthesis; SVA C2C7, sagittal vertical
axis C2C7.
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284 1281

Table 6
Comparison of mean of all parameters regarding position on kMRI image
p-Value
Parameters Anterolisthesis (N=33) Gr 1 (N=16) Gr2 (N=17) Retrolisthesis (N=19) Gr 1 (N=14) Gr 2 (N=5)
T1 slope Neutral-Flexion .021 .173 .058 .904 .730 .893
Neutral-Extension .943 .205 .435 .334 .433 .686
Flexion-Extension .064 .679 .051 .560 .730 .686
C2C7 angle Neutral-Flexion <.001 <.001 <.001 <.001 .001 .043
Neutral-Extension <.001 <.001 <.001 <.001 .001 .043
Flexion-Extension <.001 <.001 <.001 <.001 .001 .043
TIA* Neutral-Flexion <.001 .004 .006 .396 .807 .225
Neutral-Extension .150 .094 .435 .139 .124 .5
Flexion-Extension .003 .036 .037 .081 .235 .225
Neck tilt* Neutral-Flexion .051 .069 .298 .647 .972 .345
Neutral-Extension .1 .570 .130 .349 .208 1
Flexion-Extension .674 .147 .507 .647 .972 .345
SVA C2C7 Neutral-Flexion <.001 <.001 <.001 <.001 .001 .053
Neutral-Extension <.001 .001 .001 .001 .001 .225
Flexion-Extension <.001 <.001 <.001 <.001 .001 .043
Cervical tilt Neutral-Flexion <.001 <.001 .001 <.001 .001 .5
Neutral-Extension <.001 .002 <.001 .027 .001 .686
Flexion-Extension <.001 <.001 <.001 .009 .001 .138
Cranial tilt Neutral-Flexion <.001 .001 .001 <.001 .001 .127
Neutral-Extension <.001 <.002 .003 .002 .002 .225
Flexion-Extension <.001 <.001 .001 <.001 .001 .043
SVA, sagittal vertical axis; TIA, thoracic index angle; kMRI, kinematic magnetic resonance imaging.
* Number of samples: anterolisthesis=32, Gr 1 anterolisthesis=15, retrolisthesis=18, Gr 1 retrolisthesis=13.

Statistically significant difference; Wilcoxon signed rank test.

Fig. 5. The figure shows the difference of T1 slope in each group of DCS in three positions. *Statistically significant difference at p-value of less than .05.
DCS, degenerative cervical spondylolisthesis; Ant, anterolisthesis; Retro, retrolisthesis; Gr 1, grade 1 spondylolisthesis; Gr 2, grade 2 spondylolisthesis.

the compensatory mechanism of posterior neck muscles.
In flexion, posterior neck muscles might be stretched
and weaker than in the neutral and extension positions
[19,21,22]. Therefore, they might be unable to provide the
adequate compensatory action to maintain the T1 slope and
SVA C2C7, potentially leading to an increased risk of
developing anterior cervical sagittal imbalance in patients
with DCS. In grade 2 DCS, the posterior neck muscles
might have compensated high T1 slope by reducing cervical
lordosis, which might have prevented further slippage espe-
cially in the retrolisthesis group. Cervical lordosis in grade
2 DCS groups was greater than in grade 1 DCS groups, and
correlated with T1 slope, although there was no statistical
significance.
The SVA C2C7 is used to define the sagittal cervical
balance, and previous studies have found SVA C2C7 values
of 15.611.2 mm in healthy patients [20,23]. Ames et al.
[20] found that the SVA C2C7 results were correlated with
 1282
Table 7
Pearson correlation and p-value of the parameters of all cervical degenerative spondylolisthesis group in neutral position (N=52)
T1 slope TIA Neck tilt SVA C2C7 Cervical tilt Cranial tilt
All Ant Ret All Ant Ret All Ant Ret All Ant Ret All Ant Ret All Ant Ret

P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284

C2C7 angle N .524 .359* .610 .351* .151 .33 .093 .176 .167 .237 .118 .09 .709 .516 .761 .116 .002 .065
F .163 .152 .0161 .277 .176 .498* .044 .093 .504* .262 .129 .538* .486 .400* .734 .217 .104 .466*
E .469 .482 .364 .331* .31 .271 .124 .142 .157 .523 .435* .622 .433 .773 .124 .372 .293 .419
T1 slope N .525 .307 .672 .296* .475 .149 .420 .584 .543* .503 .354* .567* .577 .751 .698
F .519 .426* .660 .454 .584 .162 .538 .643 .493* .455 .482 .416 .696 .794 .633
E .584 .532 .630 .214 .296 .11 .207 .363* .104 .401 .430* .398 .374 .511 .341
TIA N .620 .646 .600 .257 .473 .33 .325* .125 .512* .264 .385* .454
F .456 .437* .520* .21 .517 .08 .469 .146 .809 .197 .390* .008
E .573 .598 .552* .073 .222 .022 .225 .208 .211 .177 .293 .207
Neck tilt N .135 .05 .216 .066 .307 .015 .268 .26 .21
F .286* .142 .580* .014 .344 .562* .477 .406* .650
E .015 .089 .176 .06 .141 .013 .06 .139 .18
SVA C2C7 N .527 .480 .353 .941 .925 .953
F .424 .25 .522* .916 .904 .932
E .463 .659 .316 .957 .962 .943
Cervical tilt N .416 .351* .194
F .323* .15 .44
E .408 .556 .306
SVA, sagittal vertical axis; TIA, thoracic index angle.
Bold numbers annotate significant correlations.
Neck tilt and TIA, N=50.
*
Correlation is significant at the .05 level (two-tailed).

Correlation is significant at the .01 level (two-tailed).
 P. Pahpolak et al. / The Spine Journal 17 (2017) 12721284
neck disability, general health score, and myelopathy sever-
ity. In our study, all DCS groups had SVA C2C7 higher
values in neutral and flexion positions, and grade 2 had
higher values than grade 1 than previously reported. Similar
to previous studies, SVA C2C7 was correlated with T1
slope in the anterolisthesis group in all positions, and in the
retrolisthesis group in neutral and flexion positions [15,20].
SVA C2C7 showed very strong correlation with cranial tilt
in all groups of DCS and in all positions. The posterior
neck muscle compensatory mechanism could potentially
explain our SVA C2C7 results especially in grade 1 DCS.
The cervical tilt showed correlation with T1 slope and
C2C7 angle in nearly all groups and positions of DCS.
The cervical tilt angle also reflected cervical lordosis; the
more negative angle, the more cervical lordosis. Retrolisthesis
had more negative cervical angle than anterolisthesis in all
positions except in grade 2 retrolisthesis in the extension
position. Grade 2 DCS had less negative angle than grade 1
DCS, except retrolisthesis in flexion. We hypothesize that
the explanation of these findings might be similar to the
previous parameter, with the compensatory muscle mecha-
nism being present in the neutral and extension positions
but not in the flexion position. The cranial tilt showed strong
relation with SVA C2C7 in all positions and groups of
DCS. This correlation may suggest that the takeoff point of
the cervical spine from the thoracic spine may have an
important role in cervical sagittal alignment in patients with
DCS [15]. The T1 slope value is equal to the difference
between the cranial tilt and the cervical tilt value [15]. T1
slope and TIA correlation in our study were similar to the
previous studies, which showed that a large TIA led to an
increased T1 slope [8,1518] .
Based on our data, we hypothesize that T1 slope, C2C7
angle, and SVA C2C7 might have a significant effect on the
direction of slip in DCS. The retrolisthesis group had higher
T1 slope, more C2C7 lordosis curvature, and less SVA than
the anterolisthesis group. As for the retrolisthesis, larger T1
slope and larger lordosis curvature might be the cause or sequel
of the posterior translation. A longitudinal study is needed
to evaluate this association.
Because kMRI is not readily available worldwide, most
spine surgeons evaluate cervical sagittal and TI parameters
using dynamic plain radiograph and neutral MRI modali-
ties. Results of our study suggest that T1 slope, C2C7 angle,
SVA C2C7, cervical tilt, and cranial tilt are significantly dif-
ferent between the two listhesis groups. Although our study
does not have capabilities to define the exact correlation
between the higher T1 slope and larger cervical lordosis with
DCS, we did find the correlation between higher grade of
listhesis and higher T1 slope. Our results, together with the
study from Jun et al., suggest that the large T1 slope might
not only be one of the predisposing factors in the onset of
DCS but also affect the severity and direction of slippage.
Therefore, we would suggest that the restoration or preser-
vation of cervical lordosis curvature and SVA C2C7 should
be taken into account when performing laminoplasty in
1283
patients with DCS. However, in patients undergoing com-
bined laminectomy and fusion procedures, SVA C2C7 but
not cervical lordosis has been shown to affect postoperative
outcome [20,24]. Cranial tilt can be readily measured because
it does not require calibration and therefore should be con-
sidered as an alternative to assessing cervical sagittal balance.
Furthermore, in patients with high T1 slope DCS, an addi-
tional translation at the adjacent levels might be present after
surgery, leading to slip progression [19,21]. The postopera-
tive posterior neck muscle strengthening exercises and
avoidance of excessive neck flexion may help prevent further
slip progression in patients with non-fusion DCS.
It is possible that small sample sizes and unbalanced cohort
participant numbers because of the retrospective nature of this
study may have limited its power to detect the true differ-
ences between the groups. Another limitation is that there was
no control group for comparison with DCS. Future studies
aimed at examining the correlation between DCS and disc
degeneration, posterior neck muscle fatty degeneration, and
facet tropism are warranted; these were not examined in this
study.
Conclusions
This is the first study to evaluate cervical sagittal and tho-
racic inlet parameters in DCS using kMRI. The retrolisthesis
group had larger T1 slope and more cervical lordosis than
the anterolisthesis group. Higher grade of listhesis corre-
lated with larger T1 slope. The cranial tilt can be used as one
effective parameter in cervical sagittal alignment evaluation
and may be favorable owing to its simple measurement.
Because of the small sample sizes, our results may not be
indicative of all DCS. Furthermore, a well-controlled cohort
study or a larger case-control study is needed to overcome
the limitations of this study.
Acknowledgment
The study was supported by departmental funds. Authors
would like to thank AiM Radiology Medical Group, espe-
cially Yusuf A. Khan, Sameer U. Khan, and Aziza Qadir, MD,
for their help obtaining and uploading kMRI images into the
database.
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