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Neurological Research

A Journal of Progress in Neurosurgery, Neurology and Neurosciences

ISSN: 0161-6412 (Print) 1743-1328 (Online) Journal homepage: http://www.tandfonline.com/loi/yner20

Age-related variations in global spinal alignment


and sagittal balance in asymptomatic Japanese
adults

Kunio Yokoyama, Masahiro Kawanishi, Makoto Yamada, Hidekazu Tanaka,


Yutaka Ito, Shinji Kawabata & Toshihiko Kuroiwa

To cite this article: Kunio Yokoyama, Masahiro Kawanishi, Makoto Yamada, Hidekazu Tanaka,
Yutaka Ito, Shinji Kawabata & Toshihiko Kuroiwa (2017): Age-related variations in global spinal
alignment and sagittal balance in asymptomatic Japanese adults, Neurological Research

To link to this article: http://dx.doi.org/10.1080/01616412.2017.1296654

Published online: 01 Mar 2017.

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Download by: [Hacettepe University] Date: 12 April 2017, At: 23:10


Neurological Research, 2017
http://dx.doi.org/10.1080/01616412.2017.1296654

Age-related variations in global spinal alignment and sagittal balance in


asymptomatic Japanese adults
Kunio Yokoyamaa, Masahiro Kawanishia, Makoto Yamadaa, Hidekazu Tanakaa, Yutaka Itoa, Shinji Kawabatab
and Toshihiko Kuroiwab
a
Department of Neurosurgery, Takeda General Hospital, Kyoto, Japan; bDepartment of Neurosurgery and Department of Surgical Pathology,
Osaka Medical College, Osaka, Japan

ABSTRACT ARTICLE HISTORY


Objectives: The global spinal sagittal alignment varies widely among healthy individuals as it Received 24 October 2016
is affected by not only race, but also aging. We investigated age-related changes in the spinal Accepted 11 February 2017
alignment in asymptomatic Japanese individuals.
KEYWORDS
Methods: The subjects comprised 220 individuals without any spine-related neurological Global spinal alignment; age-
symptoms or treatment history thereof who visited our outpatient clinic. Lateral radiographs related variations; Japanese
of the whole spine were taken for all subjects in the standing position. Based on the images population
obtained, spino-pelvic parameters were calculated using Jackson’s method so as to analyze any
correlations with age.
Results: TIA, TK, and C2–C7A were found to markedly increase with age from late middle age
(P < 0.05). No correlation with aging was found for lumbosacral parameters or sagittal balance
(P > 0.05). However, there were 22 subjects (10%) with C7SVA > 50 mm, with those aged 70 years
or older accounting for half of this subpopulation. Sagittal balance tended to be retained even in
elderly subjects if lumbosacral lordosis was large enough to compensate for thoracic kyphosis.
A very strong correlation was found between the L1 slope and whole-spine sagittal balance
(P < 0.0001, r = −0.497).
Conclusions: Increases in cervicothoracic curvature occurring along with thoracic deformation
underlie age-related changes in the spine. In contrast, the lumbosacral spine compensates in
such a manner so as to maintain the sagittal balance. The whole-spine sagittal balance can
deteriorate if the compensatory changes in the lumbosacral spine are insufficient. The L1 slope
is a central parameter that defines the whole-spine sagittal balance.
Abbreviations: PI; pelvic incidence; SS; sacral slope; PT; pelvic tilt; LL; lumbar lordosis; C7SVA;
C7 sagittal vertical axis; SSA; spinosacral angle; TK; thoracic kyphosis; C2–C7SVA; C2–C7 sagittal
vertical axis; C2–C7A; C2–C7 Angle; TIA; thoracic inlet angle; NT; neck tilt.

Introduction 20 years, (2) absence of spinal pathology, and (3) no


history of hip, pelvic, or lower limb disorder. Individuals
When performing spinal surgery, it is important to
with a history of neck and back pain were excluded from
always keep the targeted whole-spine alignment in mind
this study.
[1–5]. Thus, we need to fully understand the whole-spine
Standing antero-posterior and lateral radiographs of
alignment in healthy individuals. However, whole-spine
the whole spine were taken for all individuals with their
alignment varies widely among healthy individuals due
arms in the fists-on-clavicles position and their knees
to racial and age-related variations [6–10]. The objec-
and hips fully extended. The following parameters were
tive of this study was to investigate age-related varia-
measured on the lateral whole-spine standing radio-
tions in whole-spine sagittal alignment in asymptomatic
graphs, as described by Jackson et al. [11] (Figures 1
Japanese individuals.
and 2): the distance between the C7 plumb line and the
posterior corner of the sacrum (C7-sagittal vertical axis,
Materials and methods C7SVA); the angle formed between the line drawn from
Under the approval of our institutional review board, the front side of T1 to the middle of the sacrum and
a cohort of 220 asymptomatic Japanese adults was the line passing through the sacral plateau (spinosacral
recruited between 1 January 2014 and 31 March 2015. angle, SSA); the angle between the inferior endplate of
The inclusion criteria are as follows: (1) age more than T12 and the superior endplate of S1 using the Cobb

CONTACT Kunio Yokoyama neu100@osaka-med.ac.jp


© 2017 Informa UK Limited, trading as Taylor & Francis Group
2  K. YOKOYAMA ET AL.

method (lumbar lordosis, LL); the angle formed by a line


drawn between the center of the femoral head and the
sacral endplate (pelvic incidence, PI); the angle formed
by a line drawn from the midpoint of the sacral end-
plate to the center of the bicoxofemoral axis and vertical
plumb line (pelvic tilt, PT); the angle formed by a line
drawn along the endplate of the sacrum and a horizontal
reference line (sacral slope, SS); the angle formed by a
line drawn along the superior endplate of the L1 and a
horizontal reference line (L1 slope); the angle between
the inferior endplate of C7 and the superior endplate of
T12 using the Cobb method (thoracic kyphosis, TK); the
angle formed by a line drawn along the superior endplate
of the T1 and a horizontal reference line (T1 slope); the
distance between the C2 plumb line and the posterior
corner of the C7 vertebra (C2–C7 sagittal vertical axis,
C2–C7 SVA); the angle formed by the vertical line of the
sternum tip and the line drawn in the center of the upper
end plate of the sternum connecting the center of the
T1 upper end plate (neck tilt, NT); the angle formed by
the sum of the T1 slope and the neck tilt (thoracic inlet
angle, TIA); and the angle between the posterior surface
of C2 and the posterior surface of C7 (C2–C7 angle,
C2–C7A). All parameters were measured two times by
one experienced radiologist by using imaging software
(Rapid Eye), and results were averaged. We analyzed the
correlation between aging and each obtained measure-
ment value.
Statistical analyses were performed using StatView,
Version 5.0 software (SAS Institute, Cary, NC).
Correlations between two variables were analyzed by
Figure 1. Radiographic measurements of total spinal and pelvic Pearson’s correlation coefficients. All data are presented
parameters PI: pelvic incidence; SS: sacral slope; PT: pelvic as mean ± SD, and differences were considered statisti-
tilt; LL: lumbar lordosis; C7SVA: C7 sagittal vertical axis; SSA: cally significant at a P < 0.05.
spinosacral angle; TK: thoracic kyphosis.

Figure 2. Radiographic measurements of cervical parameters C2–C7SVA: C2–C7 sagittal vertical axis; C2–C7A: C2–C7 angle; TIA:
thoracic inlet angle; NT: neck tilt.
NEUROLOGICAL RESEARCH  3

Table 1. Correlation between age and each spinal parameter. Results


Mean ± SD r p value The study cohort consisted of 220 subjects, 99 males, and
Age (years) 59.0 ± 17.4 – –
Gender (male/female) 99/121 – – 121 females with a mean age of 59.0 (range: 20–95 years).
Pelvic incidence (°) 53.4 ± 10.9 0.074 0.273 Table 1 presents the spinal parameters of 220 subjects.
Sacral slope (°) 35.7 ± 8.8 −0.19 0.779
Pelvic tilt (°) 17.2 ± 8.2 0.134 0.046
Age-related changes appeared most prominently in the
Lumbar lordosis (°) 49.8 ± 12.4 0.03 0.653 cervico-thoracic spine. The morphology of the thoracic
C7 sagittal vertical axis (cm) 1.33 ± 3.0 0.111 0.099 inlet changed markedly with age (thoracic inlet angle:
Spinosacral angle (°) 123.0 ± 8.7 −0.073 0.278
Thoracic kyphosis (°) 38.8 ± 10.4 0.215 0.001 P < 0.0001, r = 0.419; T1 slope: P = 0.008, r = 0.177; neck
T1 slope (°) 24.6 ± 7.5 0.177 0.008 tilt: P = 0.001, r = 0.259). Incidence of thoracic kyphosis
C2–C7 angle (°) 13.9 ± 14.2 0.272 <0.0001
C2–C7 SVA (cm) 2.02 ± 1.1 −0.025 0.720 and cervical lordosis was also increased with age (TK:
T1 inlet angle (°) 79.5 ± 10.6 0.419 <0.0001 P = 0.001, r = 0.215; C2–C7A: P < 0.0001, r = 0.272;
Neck tilt (°) 53.7 ± 10.2 0.259 0.001
L1 slope (°) 14.1 ± 7.0 0.077 0.254 Figure 3(A)). On the other hand, unexpectedly, there
was little correlation between the lumbosacral alignment
and age (PI: P = 0.273, r = 0.074; SS: P = 0.779, r = −0.19;

Figure 3. Relationships between the global sagittal parameters and age. (A) Cervico-thoracic parameters vs. age, (B) Sagittal balance
vs. age.

Figure 4. (A) Relationships between LL and C7SVA. (B) Relationships between C7SVA and the L1 slope.
4  K. YOKOYAMA ET AL.

Table 2. Correlation between radiographic parameters and were many individuals whose age-associated thoracic
sagittal balance. deformation was compensated for by lumbosacral lor-
C2–C7SVA C7SVA dosis, and whole-spine sagittal balance tended to be
r p-value r p-value successfully maintained in these subjects. Conversely,
Age (years) −0.025 0.720 0.111 0.053 sagittal balance tended to increase when lumbosacral
Gender (male/Female) – – – – lordosis was insufficient for the thoracic spine alignment
Pelvic incidence (°) −0.06 0.382 0.136 0.260
Sacral slope (°) −0.002 0.972 −0.037 0.209 even in young subjects.
Pelvic tilt (°) −0.063 0.361 0.218 0.003
Lumbar lordosis (°) −0.036 0.599 −0.308 0.002
C7 sagittal vertical axis 0.199 0.003 – – Discussion
(cm)
Spinosacral angle (°) −0.101 0.138 −0.386 0.001 Cervical lordosis and thoracic kyphosis begin to
Thoracic kyphosis (°) 0.214 0.002 −0.031 0.285
T1 slope (°) 0.351 <0.001 0.418 0.002 increase as early as around 50 years. As the first tho-
C2–C7 angle (°) −0.209 0.002 0.287 0.001 racic vertebra tilts forward and moves downward with
C2–C7 SVA (cm) – – 0.199 0.397
T1 inlet angle (°) 0.089 0.281 0.047 0.423 aging, the superior thoracic aperture is eventually
Neck tilt (°) −0.053 0.517 −0.249 0.041 leveled. Anatomically, the cervicothoracic transition
L1 slope (°) −0.061 0.373 −0.497 <0.0001
is where mobility changes rapidly and also the inflec-
tion point of the alignment. Therefore, it is thought to
be the site most exposed to stress from the head weight
[12]. Long-term exposure to these forces is thought
to result in deformation of the cervicothoracic spine
mainly in the first thoracic vertebra, as well as the
thorax. In the context of respiratory medicine, this
thoracic deformation is known to decrease the vol-
ume of the thoracic cavity, leading to decreases in total
lung capacity and breathing capacity [13,14]. Cervical
lordosis increases as the first thoracic vertebra tilts
forward, thereby maintaining the sagittal balance of
the cervical spine.
Unlike changes in cervicothoracic parameters,
changes in lumbosacral parameters did not exhibit
appreciable correlations with age. While lumbar lordosis
is generally thought to decrease with aging [7,8], many
elderly subjects in this study were found to have main-
tained lumbar lordosis. Lumbar lordosis is known to be
a critical determinant of sagittal balance, and the pres-
ent study found that sagittal balance was maintained in
many subjects whose lumbar lordosis was maintained. In
general, sagittal balance is considered poor when C7SVA
exceeds 50 mm [4], and decreased quality of life is often
observed in individuals with increased C7SVA. Although
our study population included asymptomatic individuals
only, 20 of 220 individuals had C7SVA exceeding 50 mm.
These individuals exhibited a reduced sacral slope and
Figure 5. Representative full lateral standing radiographs of increased pelvic tilt, which occurred to minimize the
a 78-year-old woman with positive sagittal balance (A) and a deterioration of sagittal balance. However, LL tended to
76-year-old woman with normal sagittal balance (B). be smaller in those with C7SVA > 50 mm. While lumbar
lordosis should have increased to maintain whole-spine
PT: P = 0.046, r = 0.134; LL: P = 0.653, r = 0.03). C2– sagittal balance, it had deteriorated in these subjects due
C7SVA and C7SVA did not exhibit any significant to lumbar degeneration, and thus insufficient compen-
correlations with age (C7SVA: P = 0.099, r = 0.111; C2– sation was observed (Figure 5). Therefore, it appears
C7SVA: P = 0.720, r = −0.025; Figure 3(B)). However, that lumbar alignment does not necessarily work in a
there were 22 subjects (10%) with C7SVA > 50 mm, 10 vector to improve the sagittal balance. It therefore seems
of whom were aged 70 years or older. Identified C7SVA- that the balance between the alignment of the lumbar
related factors included L1 slope, T1 slope, LL, C2–C7 and lower part of the spine and the alignment of the
angle, and pelvic tilt, among which L1 slope was the one thoracic and upper part of the spine is an important
factor correlated most strongly with C7SVA (P < 0.0001, compositional factor of whole-spine sagittal balance.
r = −0.497; Figure 4, Table 2). Even in the elderly, there This explains why the L1 slope, which is the inflection
NEUROLOGICAL RESEARCH  5

point of the thoracolumbar alignment, was the C7SVA [2] Booth KC, Bridwell KH, Lenke LG, et al. Complications
determinant with the highest level of correlation. Our and predictive factors for the successful treatment of
findings suggest that the L1 slope, which can be deter- flatback deformity (fixed sagittal imbalance). Spine.
1999;24:1712–1720.
mined with lateral radiographs in the standing position [3] Lafage V, Schwab F, Patel A, et al. Pelvic tilt and
without performing whole-spine radiography, is a useful truncal inclination: two key radiographic parameters
indicator for assessing whole-spine sagittal balance. in the setting of adults with spinal deformity. Spine.
There are several limitations in this study. First, while 2009;34:E599–606.
the study was focused on the relationship between [4] Schwab F, Ungar B, Blondel B, et al. Scoliosis research
society-Schwab adult spinal deformity classification: a
whole-spine alignment and aging, it is difficult to extract
validation study. Spine. 2012;37:1077–1082.
pure aging effects, since the spinal alignment is affected [5] Yokoyama K, Kawanishi M, Yamada M, et al. Spinopelvic
not only by age, but also by sex, height, and physique alignment and sagittal balance of asymptomatic
[15]. In addition, since the population in this study was adults with 6 lumbar vertebrae. Eur Spine J. 2016
composed entirely of Japanese subjects, the findings Nov;25(11):3583–3588.
are not necessarily applicable to individuals in Western [6] Gutman G, Labelle H, Barchi S, et al. Normal sagittal
parameters of global spinal balance in children and
countries. Finally, although it has been indicated that adolescents: a prospective study of 646 asymptomatic
knee posture should also be considered when assessing subjects. Eur Spine J. 2016;25:3650–3657.
sagittal balance [10,16], we did not investigate this in [7] Hasegawa K, Okamoto M, Hatsushikano S, et al.
the present study. This topic needs to be investigated in Normative values of spino-pelvic sagittal alignment,
the future. balance, age, and health-related quality of life in a
cohort of healthy adult subjects. Eur Spine J. 2016
Nov;25(11):3675–3686.
Conclusions [8] Yoshida G, Yasuda T, Togawa D, et al. Craniopelvic
alignment in elderly asymptomatic individuals: analysis of
Increases in cervicothoracic curvature accompanying 671 cranial centers of gravity. Spine. 2014;39:1121–1127.
thoracic deformation underlie the age-related changes [9] Oe S, Togawa D, Nakai K, et al. The influence of age and
in the spine. In response, the lumbosacral spine com- sex on cervical spinal alignment among volunteers aged
pensates so as to maintain the sagittal balance. The over 50. Spine. 2015;40:1487–1494.
[10] Iyer S, Lenke LG, Nemani VM, et al. Variations in sagittal
whole-spine sagittal balance may deteriorate if the com- alignment parameters based on age: a prospective
pensatory changes in the lumbosacral spine are insuffi- study of asymptomatic volunteers using full-body
cient, and the L1 slope is a central parameter that defines radiographs. Spine. 2016 Dec 1;41(23):1826–1836.
the whole-spine sagittal balance. [11] Jackson RP, McManus AC. Radiographic analysis
of sagittal plane alignment and balance in standing
volunteers and patients with low back pain matched
Contributors for age, sex, and size. A prospective controlled clinical
study. Spine. 1994;19:1611–1618.
KY, SK and TK conceived and designed the study, [12] Scheer JK, Tang JA, Smith JS, et al. Cervical spine
obtained funded and ethics approval, analysed the data, alignment, sagittal deformity, and clinical implications:
wrote the article in whole/part, and revised the article. a review. J Neurosurg Spine. 2013;19:141–159.
MK, YI, MY and HT collected and analysed the data. [13] Gayzik FS, Yu MM, Danelson KA, et al. Quantification of
age-related shape change of the human rib cage through
geometric morphometrics. J Biomech. 2008;41:1545–1554.
[14] Kent R, Lee SH, Darvish K, et al. Structural and
Disclosure statement material changes in the aging thorax and their role in
crash protection for older occupants. Stapp Car Crash
No potential conflict of interest was reported by the authors. J. 2005;49:231–249.
[15] Duval-Beaupère G, Robain G. Visualization on full spine
radiographs of the anatomical connections of the centres
References of the segmental body mass supported by each vertebra
[1] Berven SH, Deviren V, Smith JA, et al. Management of and measured in vivo. Int Orthop. 1987;11:261–269.
fixed sagittal plane deformity: outcome of combined [16] Barrey C, Roussouly P, Le Huec JC, et al. Compensatory
anterior and posterior surgery. Spine. 2003;28:1710– mechanisms contributing to keep the sagittal balance
1715. of the spine. Eur Spine J. 2013;22(Suppl 6):S834–S841.

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