Eur Spine J DOI 10.1007/s00586-015-3925-y
ORIGINAL ARTICLE
CT morphometry of adult thoracic intervertebral discs Justin G. R. Fletcher1 • Mark D. Stringer1 • Christopher A. Briggs2 Tilman M. Davies3 • Stephanie J. Woodley1
•
Received: 14 January 2015 / Revised: 30 March 2015 / Accepted: 1 April 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose Despite being commonly affected by degenerative disorders, there are few data on normal thoracic intervertebral disc dimensions. A morphometric analysis of adult thoracic intervertebral discs was, therefore, undertaken. Methods Archival computed tomography scans of 128 recently deceased individuals (70 males, 58 females, 20–79 years) with no known spinal pathology were analysed to determine thoracic disc morphometry and variations with disc level, sex and age. Reliability was assessed by intraclass correlation coefficients (ICCs). Results Anterior and posterior intervertebral disc heights and axial dimensions were significantly greater in men (anterior disc height 4.0 ± 1.4 vs 3.6 ± 1.3 mm; posterior disc height 3.6 ± 0.90 vs 3.4 ± 0.93 mm; p \ 0.01). Disc heights and axial dimensions at T4-5 were similar or smaller than at T2-3, but thereafter increased caudally (mean anterior disc height T4-5 and T10-11, 2.7 ± 0.7 and 5.4 ± 1.2 mm, respectively, in men; 2.6 ± 0.8 and 5.1 ± 1.3 mm, respectively, in women; p \ 0.05). Except at T2-3, anterior disc height decreased with advancing age and anteroposterior and transverse disc dimensions
Electronic supplementary material The online version of this article (doi:10.1007/s00586-015-3925-y) contains supplementary material, which is available to authorized users. & Stephanie J. Woodley
[email protected] 1
Department of Anatomy, University of Otago, Dunedin, New Zealand
2
Department of Anatomy and Cell Biology, University of Melbourne, Melbourne, Australia
3
Department of Mathematics and Statistics, University of Otago, Dunedin, New Zealand
increased; posterior and middle disc heights and indices of disc shape showed no consistent statistically significant changes. Most parameters showed substantial to almost perfect agreement for intra- and inter-rater reliability. Conclusions Thoracic disc morphometry varies significantly and consistently with disc level, sex and age. This study provides unique reference data on adult thoracic intervertebral disc morphometry, which may be useful when interpreting pathological changes and for future biomechanical and functional studies. Keywords Intervertebral disc Thoracic spine Computed tomography Morphometry Age
Introduction The thoracic spine is unique, particularly in regard to articulation with the rib cage and its physiological kyphosis. These features contribute to markedly different biomechanical properties compared to other spinal regions, such as reduced mobility [1, 2] and increased compressive load bearing capacity [3]. This suggests the likelihood of substantial differences in intervertebral disc morphology. However, despite documented changes associated with kyphosis [4, 5], scoliosis [6] and degeneration [7], relatively little is known about the normal morphology and morphometry of thoracic discs. Intervertebral disc morphology and/or morphometry varies with activity, age and sex. For example, disc height varies diurnally according to erect or supine posture [8] and is affected by body weight [9]. Advancing age is associated with changes in the cervical [10], lumbar [11, 12] and thoracic spines [4, 5], the latter directly affecting the degree of thoracic kyphosis [13]. Age-related changes in the molecular composition of thoracic intervertebral discs have
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also been described [14, 15]. Reported sex differences include the biomechanical properties of thoracic spinal segments [16] and morphometric differences between intervertebral discs in the cervical [10, 17] and lumbar spines [11, 12]. However, no previous study has systematically investigated age-related changes or sex differences in thoracic intervertebral disc morphometry. Several studies have examined variation in thoracic intervertebral disc height with disc level [18–21] and concluded that disc heights decrease caudally to a minimum at T4-5 before increasing to reach a maximum height at T1011. Regional variation in thoracic disc height was investigated most recently by Kunkel et al. [21], with measurements taken both directly and from radiographs of isolated, embalmed thoracic spinal segments. However, due to the relatively small sample size of just 30 cadavers, associations with age or sex could not be explored. Understanding normal thoracic disc morphometry is important when interpreting the pathological changes associated with kyphosis, scoliosis and disc degeneration. The aim of this study was to investigate the morphometry of adult thoracic intervertebral discs in individuals with no known spinal disease and to analyse potential variations in disc dimensions with sex, disc level and age.
Methods Subjects Computed tomography (CT) scans from deceased adults who had undergone autopsy at the Victorian Institute of Forensic Medicine (VIFM), Australia, between June and November 2012, were analysed retrospectively. Approval was obtained from the VIFM Ethics Committee (EC 9/2012) and the Multi-Region Ethics Committee, New Zealand (MEC/12/EXP/048) before commencing the study. Individuals received at VIFM within 24 h of death who had not died as a result of a motor vehicle accident were selected sequentially by date to produce six age cohorts (20–29 years, 30–39 years, etc. up to 70–79 years), each consisting of 12 males and 12 females. Potential scans were then subjected to the following exclusion criteria: evidence of scoliosis, previous spinal surgery or vertebral fracture, imaging in a non-anatomical position or a poor quality scan. Fifty-three individuals were excluded at this stage and replaced by new subjects. During subsequent CT scan analysis additional exclusion criteria were applied, including the presence of multiple disc abnormalities or six lumbar vertebrae. Subjects with only a single abnormal disc were retained but the affected disc was omitted from the analysis. Subjects excluded during this phase of the study could not be replaced (Online Resource 1).
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CT scanning and morphometric analysis CT scans were performed using a Toshiba Aquilion 16 multi-detector scanner (Toshiba Corp. Tokyo, Japan) with the deceased positioned supine. Helical slices (0.5 mm) were acquired using 120 kVp and 300 mA exposure factors, and raw data reconstructed into 2 mm slices with a 0.2-mm overlap (viewed using Aquarius Workstation, TeraRecon Inc. San Mateo, CA, USA). Analysis was undertaken using OsiriX 4.0 (OsiriX Imaging Software, 2012), with the CT images opened as three-dimensional multi-planar reconstructions. Vertebral levels were identified by reference to the first rib and T1 vertebral body (sagittal plane). An axial slice was selected through the middle of the disc of interest, parallel to the endplates of the vertebrae above and below. Mid-sagittal planes were then defined by the centre of the tip of the vertebral spinous process and the most anterior aspect of the vertebral body [22]. Alternate thoracic discs from T2-3 caudally were analysed in mid-sagittal and coronal sections (Fig. 1). Three disc heights (anterior, middle and posterior) and two axial disc dimensions (anteroposterior and transverse) were measured. Indices of disc wedging [21] and convexity (modified from Twomey and Taylor [11]) were calculated (Fig. 1). To assess intra-observer repeatability, 32 (25 %) subjects were randomly selected for blind re-measurement after an interval of at least 6 weeks. Assessment of interrater reproducibility was achieved by randomly selecting 23 (18 %) subjects for repeat measurement by an independent observer. Statistical analyses Means and standard deviations of each parameter were calculated for males and females in each age cohort at each selected intervertebral disc level. Unpaired t tests were performed to assess for statistically significant differences between data sets in groups of interest. Four of the disc parameters (anterior disc height [ADH], posterior disc height [PDH], anteroposterior disc dimension [APDD] and transverse disc dimension [TDD]) were modelled via linear mixed models to assess the independent influences of sex, disc level and age. Fitting of such a model required complete data sets, meaning 104 subjects were included (58 males, 46 females; mean age 47 years) as data were missing for one disc level in 24 subjects. Three predictors: sex, disc level and age were included, and a stochastic error term was included to account for any within-subject response correlation. All possible interaction terms between the predictors were considered and a conventional ‘topdown’ model selection criterion at a level of 5 % was applied. Coefficient estimation was performed via restricted
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Fig. 1 Morphological parameters measured on alternate thoracic discs
maximum likelihood (REML) methods [23] within the statistical programming environment R [24], using the contributed package nlme [25]. Single two-way mixed intraclass correlation coefficients (ICCs) were calculated using IBM SPSS (version 20, IBM Corp., New York, USA) to establish the intra- and interreliability of each of the measured parameters using the criteria of Landis and Koch [26].
Results Demographic data Thoracic spines from a total of 128 deceased adults (70 males, 58 females; aged 20–79 years at death) were analysed (Online Resource 1). Mean height and weight were 1.73 ± 0.07 m and 83.9 ± 16.4 kg for men and 1.61 ± 0.06 m and 68.9 ± 19.2 kg for women, respectively (see Table 1, Online Resource 2, for anthropometric data for each age cohort). There was a statistically significant decrease in stature between 20- to 29 and 70- to 79 year-olds in men (1.76 ± 0.05 vs 1.69 ± 0.06 m; p = 0.006) and women (1.64 ± 0.07 vs 1.58 ± 0.05 m; p = 0.04) while mean weight was relatively constant.
Morphometric data Sex With the exception of MDH and wedge index (WI), all disc dimensions were significantly greater in men than women. As MDH values were similar in both sexes, the disc convexity index (DCI) was greater in women (p \ 0.001; Table 1). Linear mixed models fitted to ADH, APDD and TDD data showed that the mean values of these parameters were statistically significantly greater in men than in women, independent of age and disc level, by 3 mm (p = 0.015), 2.2 mm (p \ 0.001) and 3.3 mm (p \ 0.001), respectively. There was no statistically significant difference between the PDH of males and females after controlling for age and disc level. Disc level Mean disc heights at T4-5 were similar or smaller than at T2-3, but thereafter increased caudally (Tables 2, 3; Fig. 2). Anterior disc height (Table 2) and MDH (Fig. 2; Table 2, Online Resource 2) decreased from T2-3 to minimum values at T4-5 in both men and women and then increased caudally to maximum values at T10-11.
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Eur Spine J Table 1 Mean values of all morphometric parameters for all disc levels combined (n = 128)
Morphometric parameters
Mean ± SD Female
Difference (%)
p (2-tailed)
Male
ADH (mm)
4.0 ± 1.4
3.6 ± 1.3
9
0.003
PDH (mm)
3.6 ± 0.9
3.4 ± 0.9
6
0.010
MDH (mm)
4.8 ± 1.1
4.9 ± 1.2
-2
0.325
APDD (mm)
27.2 ± 5.2
23.8 ± 4.4
14
\0.001
TDD (mm)
\0.001
31.6 ± 6.0
27.7 ± 5.2
14
WI
1.1 ± 0.5
1.1 ± 0.4
5
0.100
DCI
1.3 ± 0.3
1.4 ± 0.3
-9
\0.001
ADH anterior disc height, APDD anteroposterior disc dimension, DCI disc convexity index, MDH middle disc height, PDH posterior disc height, SD standard deviation, TDD transverse disc dimension, WI wedge index
Table 2 Mean anterior disc height by disc level and age in males and females (n = 128)
Age cohort (years)
Anterior disc height (mm) Mean ± SD T2-3
T4-5
T6-7
T8-9
T10-11
2.7 ± 0.6
3.0 ± 0.8
4.0 ± 0.8
5.0 ± 0.9
5.8 ± 1.1
Male 20–29 30–39
2.6 ± 0.4
2.6 ± 0.6
3.5 ± 0.9
4.5 ± 0.8
5.1 ± 0.8
40–49
2.8 ± 0.8
2.8 ± 0.6
3.8 ± 0.7
4.9 ± 1.2
5.7 ± 0.8
50–59
2.9 ± 0.6
2.6 ± 0.7
4.1 ± 1.1
5.3 ± 1.0
6.4 ± 1.9
60–69 70–79
3.2 ± 1.0 3.3 ± 0.9
2.6 ± 0.7 2.4 ± 0.6
4.0 ± 0.5 3.9 ± 0.8
5.0 ± 1.4 4.6 ± 0.4
5.4 ± 1.1 4.7 ± 1.0
Mean
2.9 ± 0.8
2.7 ± 0.7
3.9 ± 0.8
4.9 ± 1.0
5.4 ± 1.2
20–29
2.8 ± 0.8
2.9 ± 0.9
3.8 ± 0.7
4.5 ± 1.3
5.7 ± 1.1
30–39
2.8 ± 0.9
2.6 ± 1.0
3.5 ± 0.9
4.3 ± 0.8
5.3 ± 0.9
40–49
2.8 ± 0.8
2.7 ± 0.7
3.7 ± 0.8
4.1 ± 0.6
5.1 ± 1.8
50–59
2.4 ± 0.6
2.7 ± 0.4
3.2 ± 0.7
4.2 ± 0.4
4.7 ± 1.3
Female
60–69
2.1 ± 0.3
2.7 ± 0.8
3.3 ± 0.8
3.6 ± 1.0
4.5 ± 1.1
70–79
3.0 ± 0.5
2.1 ± 0.6
3.2 ± 0.8
4.7 ± 0.9
5.6 ± 0.9
Mean
2.7 ± 0.7
2.6 ± 0.8
3.4 ± 0.8
4.2 ± 0.9
5.1 ± 1.3
All differences between adjacent disc levels were statistically significant (p \ 0.05) with the exception of ADH between T2-3 and T4-5. Posterior disc height decreased from T2-3 to T4-5 in men, but was similar at these two levels in females, before increasing caudally to a maximum at T8-9 and T10-11, respectively (Table 3). Statistically significant differences in PDH were only evident between T2-3 and T4-5 and T4-5 and T6-7 (p \ 0.001) in men and T4-5 and T6-7 (p \ 0.001) in women. A relatively linear increase down the thoracic spine was apparent for APDD (Table 4), while the mean TDD of discs at T2-3 and T4-5 were similar and thereafter increased caudally to a maximum at T10-11 in both sexes (Table 5). Differences between adjacent disc levels for both these parameters were significant except for the TDD
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between T2-3 and T4-5 (p = 0.240 in males and p = 0.876 in females). With the exception of a decrease in ADH (p = 0.253), PDH (p = 0.011) and TDD (p = 0.303) between T2-3 and T4-5, linear mixed models fitted to each of the four disc parameters confirmed a statistically significant caudal increase in disc height or dimensions independent of age and sex. Wedge index (Fig. 3) increased down the thoracic spine. In the upper thoracic spine (T2-3 and T4-5), WI values were less than 1 indicating that ADH was less than PDH. The T6-7 disc showed little wedging with a mean value close to 1. In the lower thoracic spine, T8-9 to T10-11, ADH exceeded PDH as shown by wedge indices greater than 1. Consequently, the discs were opposing the thoracic
Eur Spine J Table 3 Posterior disc height by disc level and age in males and females (n = 128)
Age cohort (years)
Posterior disc height (mm) Mean ± SD T2-3
T4-5
T6-7
T8-9
T10-11
Male 20–29
3.3 ± 0.8
3.8 ± 0.7
4.1 ± 0.7
4.5 ± 1.0
3.5 ± 0.9
30–39
3.2 ± 0.7
3.0 ± 0.7
3.2 ± 0.9
3.4 ± 1.0
3.7 ± 0.8
40–49
3.5 ± 0.7
3.3 ± 0.8
3.8 ± 0.7
4.1 ± 0.7
3.9 ± 0.8
50–59
3.7 ± 0.8
2.5 ± 0.5
3.8 ± 1.4
3.8 ± 0.8
4.0 ± 1.6
60–69
3.4 ± 0.6
2.7 ± 0.7
3.7 ± 0.9
4.1 ± 0.8
3.5 ± 1.0
70–79 Mean
3.7 ± 0.7 3.5 ± 0.7
3.0 ± 0.6 3.1 ± 0.8
4.2 ± 0.7 3.8 ± 0.9
3.8 ± 0.8 3.9 ± 0.9
3.8 ± 0.7 3.7 ± 0.9
20–29
3.0 ± 0.7
2.9 ± 0.9
3.9 ± 0.4
4.1 ± 0.8
3.8 ± 1.1
30–39
3.3 ± 1.0
3.1 ± 1.0
3.4 ± 0.9
3.8 ± 0.8
4.0 ± 0.8
40–49
3.3 ± 0.6
3.1 ± 1.0
3.7 ± 0.7
3.8 ± 0.8
4.1 ± 0.7
Female
50–59
2.8 ± 0.6
2.8 ± 0.6
3.0 ± 0.8
3.5 ± 0.8
3.8 ± 1.4
60–69
2.4 ± 0.7
2.7 ± 0.6
3.5 ± 0.9
2.9 ± 1.1
3.3 ± 0.7
70–79
3.5 ± 0.5
2.8 ± 0.3
3.7 ± 1.4
4.1 ± 0.7
4.1 ± 0.9
Mean
3.0 ± 0.8
2.9 ± 0.8
3.5 ± 0.9
3.7 ± 0.9
3.8 ± 1.0
(p = 0.003), and in women between T4-5 and T6-7 (p = 0.002). Age
Fig. 2 Middle disc height of subjects of all ages combined by disc level
kyphosis at these levels. The difference between WI of adjacent discs was not statistically significant in the upper thoracic spine, but significant differences were evident in the middle and lower thoracic spine (from T4-5 to T10-11 in males, and T6-7 to T10-11 in females; p \ 0.008). Disc convexity index (Fig. 4) was greater than 1 across all disc levels indicating that all discs were biconvex. This parameter decreased caudally from a maximum at T2-3 and T4-5 to a minimum at T8-9. The difference in DCI between adjacent discs was statistically significant in men between T4-5 and T6-7 (p \ 0.001) and between T8-9 and T10-11
In both sexes anterior and posterior disc heights in 60- to 69-year-olds (mean range anterior 2.1–5.4 mm, posterior 2.4–3.7 mm) were less than or similar to values in 20- to 29-year-olds (mean range anterior 2.7–5.8, posterior 2.9–4.5 mm) at most disc levels. However, disc heights in 70- to 79-year-olds (mean range anterior 2.1–5.6 mm, posterior 2.8–4.2 mm) were often greater than in 60- to 69-year-olds. MDH in men was greater in 50- to 59- year olds (mean range 3.6–6.4 mm) than in 20- to 29-year-olds (mean range 4.2–5.8 mm) across all disc levels except T4-5, while in females it decreased across age cohorts (except at T4-5) to minimum values in 60- to 69-year-olds (mean range 4.1–5.3 mm). Anteroposterior and transverse disc dimensions showed increases with age across all disc levels and sexes (Tables 4, 5). Mean WI changed little across age cohorts in both men and women. Similarly, DCI changed little with age, although discs did increase in convexity from 20–29 to 30–39 year olds in both sexes, with a statistically significant difference for the T6-7 intervertebral disc in males (p = 0.003). Linear mixed models confirmed a statistically significant decrease in ADH (Fig. 5) and increase in APDD and TDD with advancing age, independent of sex and disc level. Conversely, the model fitted to PDH indicated that there was no statistically significant decrease in PDH with advancing age.
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Eur Spine J Table 4 Anteroposterior disc dimension by disc level and age in males and females (n = 128)
Age cohort (years)
Anteroposterior disc dimension (mm) Mean ± SD T2-3
T4-5
T6-7
T8-9
T10-11
Male 20–29
19.9 ± 2.6
23.1 ± 2.6
27.2 ± 2.8
29.6 ± 3.1
31.0 ± 2.9
30–39
19.0 ± 1.5
22.4 ± 2.0
26.2 ± 2.0
29.5 ± 2.9
31.4 ± 2.6
40–49
19.5 ± 1.0
24.4 ± 1.7
27.3 ± 2.0
31.3 ± 2.7
32.0 ± 2.7
50–59
22.2 ± 2.2
24.4 ± 0.9
29.0 ± 2.7
32.7 ± 1.8
33.6 ± 3.1
60–69
20.4 ± 2.0
24.5 ± 1.7
28.6 ± 2.3
32.2 ± 3.0
32.9 ± 2.3
70–79 Mean
20.3 ± 2.1 20.1 ± 2.1
25.3 ± 2.6 24.0 ± 2.2
28.3 ± 2.3 27.7 ± 2.5
32.3 ± 3.2 31.2 ± 3.0
33.1 ± 3.9 32.3 ± 3.0
20–29
17.1 ± 1.8
20.8 ± 1.6
24.4 ± 2.2
26.8 ± 2.5
27.3 ± 2.1
30–39
17.6 ± 1.6
20.6 ± 2.0
23.3 ± 1.7
26.3 ± 1.6
28.5 ± 2.4
40–49
17.8 ± 1.7
21.0 ± 1.4
24.6 ± 1.4
27.0 ± 2.1
27.9 ± 3.1
Female
Table 5 Transverse disc dimension by disc level and age in males and females (n = 128)
50–59
18.3 ± 1.6
22.1 ± 2.3
25.5 ± 2.2
27.5 ± 2.8
28.8 ± 2.4
60–69
18.4 ± 1.9
22.0 ± 2.0
25.5 ± 2.1
27.7 ± 2.1
29.2 ± 2.4
70–79
17.0 ± 1.4
20.8 ± 1.4
24.5 ± 2.2
27.8 ± 2.3
28.0 ± 3.7
Mean
17.7 ± 1.7
21.1 ± 1.8
24.6 ± 2.1
27.1 ± 2.2
28.3 ± 2.6
T6-7
T8-9
T10-11
Age cohort (years)
Transverse disc dimension (mm) Mean ± SD T2-3
T4-5
Male 20–29
25.7 ± 2.5
25.2 ± 2.3
30.0 ± 2.0
33.6 ± 1.8
38.6 ± 2.6
30–39
25.3 ± 2.4
24.6 ± 2.0
28.0 ± 2.3
32.3 ± 2.5
37.3 ± 2.6
40–49
26.5 ± 2.7
25.9 ± 2.4
30.3 ± 2.9
34.6 ± 3.3
38.6 ± 3.7
50–59
26.5 ± 1.3
27.4 ± 0.9
32.0 ± 2.0
36.9 ± 2.1
42.3 ± 3.0
60–69
26.8 ± 2.4
27.0 ± 2.6
30.7 ± 3.3
36.0 ± 3.1
40.8 ± 3.3
70–79 Mean
28.1 ± 1.5 26.5 ± 2.3
26.5 ± 2.2 26.0 ± 2.3
31.2 ± 3.0 30.3 ± 2.9
37.0 ± 3.2 35.0 ± 3.2
41.7 ± 3.6 39.8 ± 3.5
22.2 ± 1.8
22.7 ± 1.6
26.2 ± 2.2
30.1 ± 2.5
34.1 ± 2.1
Female 20–29 30–39
22.6 ± 1.6
22.1 ± 2.0
24.8 ± 1.7
28.9 ± 1.6
34.5 ± 2.4
40–49
24.2 ± 1.7
23.1 ± 1.4
26.0 ± 1.4
30.8 ± 2.1
34.8 ± 3.1
50–59
23.1 ± 1.6
23.3 ± 2.3
26.1 ± 2.2
30.8 ± 2.8
35.6 ± 2.4
60–69
23.5 ± 1.9
24.3 ± 2.0
28.0 ± 2.1
31.8 ± 2.1
36.1 ± 2.4
70–79
23.8 ± 1.4
23.9 ± 1.4
26.6 ± 2.2
32.2 ± 2.2
35.4 ± 3.7
Mean
23.1 ± 1.6
23.2 ± 2.1
26.2 ± 2.5
30.6 ± 3.0
35.0 ± 3.0
Reliability
Discussion
All ICCs for both intra- and inter-rater reliability showed substantial or almost perfect agreement (0.62–0.99) except the inter-rater reproducibility of ADH (0.54) and PDH (0.50), which showed moderate agreement (Table 3, Online Resource 2).
All disc dimensions were greater in men than women except MDH (and thus DCI). Greater disc dimensions in men are probably largely due to a scaling effect, as mean differences in disc and vertebral body heights (6–9 %) between males and females were proportionally similar to
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Fig. 3 Wedge index of subjects of all ages combined by disc level
Fig. 4 Disc convexity index of subjects of all ages combined by disc level
their mean difference in stature (7 %). Several previous studies of intervertebral discs from other spinal regions have found larger disc dimensions in men [10–12]. Previous investigations have also recorded a craniocaudal increase in disc height, except at T4-5, which was either similar in height or shorter than the disc at T2-3 [18, 19, 21]. Greater disc height in more caudal discs was expected since the lower thoracic spine has a greater range of flexion/extension than the upper thoracic spine [1]. This may also explain the increased disc height at T2-3, which is situated near the more mobile cervical spine. To the best of our knowledge, no study has previously investigated anteroposterior or transverse dimensions of thoracic intervertebral discs. The finding that these parameters increase caudally is not surprising as more caudal
discs support a greater compressive load and a greater axial cross-sectional area reduces compressive stress. A similar craniocaudal increase has been found in lumbar discs [11, 22]. The cranial and caudal thoracic discs were more wedgeshaped than the relatively uniform disc at T6-7; discs above this level had a posterior height greater than the anterior, and discs below this level were wedged in the opposite direction. These findings differ somewhat from those of Kunkel et al. [21] who observed similar trends below T6-7 and at T2-3 and T4-5, but noted that the T1-2 and T3-4 discs were taller anteriorly than posteriorly, which eliminates any clear sequence in disc WI in the upper thoracic spine. T1-2 and T3-4 discs were not measured in the present study. No previous study has investigated changes in thoracic intervertebral disc height with age. However, Hurxthal [18] reported that total disc height across the thoracolumbar spine (T6-7 to L4-5) was greater in 47- to 75-year-olds than 25- to 30-year-olds. The reduction in ADH with advancing age found in this study has several important implications: not only does it suggest a reduced range of flexion/extension in older individuals, as in the cervical spine [10], but also that greater compressive loads are transmitted via articular facet joints [27] as well as concomitant postural changes [4, 5]. Numerous factors probably contribute to the age-related reduction in ADH. The thoracic kyphosis that occurs with advancing age [13] causes greater compressive loads on the anterior aspect of a thoracic intervertebral disc [28]. The region of a disc in the concavity of a spinal curvature contains reduced levels of water and proteoglycan [6], both of which are key determinants of disc height. General agerelated changes to the disc include reduced levels of nuclear proteoglycan, water and disc pressure [29] and decreased disc nutrition [30]. Disc metabolism becomes impaired, proteoglycan content falls and matrix metalloproteases increase [31], ultimately leading to matrix degeneration and reduced disc height. This study has several limitations. Data were acquired from recently deceased individuals rather than living subjects. Lack of access to health records meant that inclusion criteria for ‘normal’ spines relied on cause of death and CT findings. Alternate thoracic discs were analysed because of time constraints. Using CT to measure intervertebral disc parameters, disc margins could only be defined using the bony margins of adjacent vertebrae; although magnetic resonance imaging allows direct measurement of disc parameters and offers a means of quantitatively assessing disc degeneration [32], measurements of disc height may in fact be less precise than using radiographs [33]. Despite these limitations, the analysis of multiple disc dimensions, a relatively large sample size and the use of thin slice CT scans rather than lateral radiographs resulted in the most
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Fig. 5 Linear mixed models in male subjects fitted to the following: a anterior disc height; b posterior disc height; c anteroposterior disc dimension; d transverse disc dimension
comprehensive study of thoracic intervertebral disc morphometry to date. In conclusion, our findings indicate that adult thoracic intervertebral disc morphometry varies considerably with sex, disc level, and age. Most disc dimensions are greater in men than women. There is a craniocaudal increase in disc height and anteroposterior and transverse disc dimensions, except at T4-5, which tends to be similar or smaller in size than the T2-3 disc. Anterior disc height decreases while anteroposterior and transverse disc dimensions increase with advancing age. The morphometric data derived in this study should provide reliable reference data on adult thoracic intervertebral discs, which may be useful when interpreting
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pathological changes and conducting biomechanical and functional studies of the thoracic spine. Acknowledgments The authors would like to thank the staff of the Victorian Institute of Forensic Medicine (VIFM), particularly Trish O’Brien; Dr. Alice Guidera for assisting with the inter-rater reliability analyses; and Mr. Robbie McPhee for helping produce Fig. 1. No external funding was received to undertake this study. Conflict of interest
None.
Ethical standard Research ethics: Approval was received from the Victorian Institute of Forensic Medicine Ethics Committee (EC 9/2012) and the Multi-Region Ethics Committee, New Zealand (MEC/12/EXP/048).
Eur Spine J
References 1. White AA, Panjabi MM (1990) Clinical biomechanics of the spine. Lippincott, Philadelphia 2. Brasiliense LB, Lazaro BC, Reyes PM, Dogan S, Theodore N, Crawford NR (2011) Biomechanical contribution of the rib cage to thoracic stability. Spine 36:E1686–E1693 3. Andriacchi T, Schultz A, Belytschko T, Galante J (1974) A model for studies of mechanical interactions between the human spine and rib cage. J Biomech 7:497–507 4. Manns RA, Haddaway MJ, McCall IW, Cassar Pullicino V, Davie MW (1996) The relative contribution of disc and vertebral morphometry to the angle of kyphosis in asymptomatic subjects. Clin Radiol 51:258–262 5. Goh S, Price RI, Leedman PJ, Singer KP (1999) The relative influence of vertebral body and intervertebral disc shape on thoracic kyphosis. Clin Biomech 14:439–448 6. Roberts S, Menage J, Eisenstein SM (1993) The cartilage endplate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 11:747–757 7. Matsumoto M, Okada E, Ichihara D, Watanabe K, Chiba K, Toyama Y, Fujiwara H, Momoshima S, Nishiwaki Y, Hashimoto T, Takahata T (2010) Age-related changes of thoracic and cervical intervertebral discs in asymptomatic subjects. Spine 35:1359–1364 8. Botsford DJ, Esses SI, Ogilvie-Harris DJ (1994) In vivo diurnal variation in intervertebral disc volume and morphology. Spine 19:935–940 9. Lidar Z, Behrbalk E, Regev GJ, Salame K, Keynan O, Schweiger C, Appelbaum L, Levy Y, Keidar A (2012) Intervertebral disc height changes after weight reduction in morbidly obese patients and its effect on quality of life and radicular and low back pain. Spine 37:1947–1952 10. Yukawa Y, Kato F, Suda K, Yamagata M, Ueta T (2012) Agerelated changes in osseous anatomy, alignment, and range of motion of the cervical spine. Part i: radiographic data from over 1200 asymptomatic subjects. Eur Spine J 21:1492–1498 11. Twomey L, Taylor J (1985) Age changes in lumbar intervertebral discs. Acta Orthop Scand 56:496–499 12. Frobin W, Brinckmann P, Biggemann M, Tillotson M, Burton K (1997) Precision measurement of disc height, vertebral height and sagittal plane displacement from lateral radiographic views of the lumbar spine. Clin Biomech 12(Suppl 1):S1–S63 13. Fon GT, Pitt MJ, Thies AC Jr (1980) Thoracic kyphosis: range in normal subjects. AJR 134:979–983 14. Scott JE, Bosworth TR, Cribb AM, Taylor JR (1994) The chemical morphology of age-related changes in human intervertebral disc glycosaminoglycans from cervical, thoracic and lumbar nucleus pulposus and annulus fibrosus. J Anat 184:73–82 15. Tan CI, Kent GN, Randall AG, Edmondston SJ, Singer KP (2003) Age-related changes in collagen, pyridinoline, and deoxypyridinoline in normal human thoracic intervertebral discs. J Gerontol A Biol Sci Med Sci 58:B387–B393 16. Stemper BD, Board D, Yoganandan N, Wolfla CE (2010) Biomechanical properties of human thoracic spine disc segments. J Craniovertebr Junction Spine 1:18–22
17. Frobin W, Leivseth G, Biggemann M, Brinckmann P (2002) Vertebral height, disc height, posteroanterior displacement and dens-atlas gap in the cervical spine: precision measurement protocol and normal data. Clin Biomech 17:423–431 18. Hurxthal LM (1968) Measurement of anterior vertebral compressions and biconcave vertebrae. Am J Roentgenol Radium Ther Nucl Med 103:635–644 19. Pooni JS, Hukins DW, Harris PF, Hilton RC, Davies KE (1986) Comparison of the structure of human intervertebral discs in the cervical, thoracic and lumbar regions of the spine. Surg Radiol Anat 8:175–182 20. Giles LGF, Singer KP (2000) Clinical anatomy and management of thoracic spine pain. Butterworth-Heinemann, Oxford 21. Kunkel ME, Herkommer A, Reinehr M, Bockers TM, Wilke HJ (2011) Morphometric analysis of the relationships between intervertebral disc and vertebral body heights: an anatomical and radiographic study of the human thoracic spine. J Anat 219:375–387 22. van der Houwen EB, Baron P, Veldhuizen AG, Burgerhof JG, van Ooijen PM, Verkerke GJ (2010) Geometry of the intervertebral volume and vertebral endplates of the human spine. Ann Biomed Eng 38:33–40 23. Faraway JJ (2006) Extending the linear model with R: generalised linear mixed effects and non parametric regression models. Chapman & Hall, Florida 24. R Core Team (2012) R: a language and environment for statistical computing 25. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1–104 26. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174 27. Adams MA, Pollintine P, Tobias JH, Wakley GK, Dolan P (2006) Intervertebral disc degeneration can predispose to anterior vertebral fractures in the thoracolumbar spine. J Bone Miner Res 21:1409–1416 28. Singer KP, Jones TJ, Breidahl PD (1990) A comparison of radiographic and computer-assisted measurements of thoracic and thoracolumbar sagittal curvature. Skeletal Radiol 19:21–26 29. Adams MA, McNally DS, Dolan P (1996) Stress distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br 78:965–972 30. Urban JP, Smith S, Fairbank JC (2004) Nutrition of the intervertebral disc. Spine 29:2700–2709 31. Handa T, Ishihara H, Ohshima H, Osada R, Tsuji H, Obata K (1997) Effects of hydrostatic pressure on matrix synthesis and matrix metalloproteinase production in the human lumbar intervertebral disc. Spine 22:1085–1091 32. Zhang Z, Chan Q, Anthony MP, Samartzis D, Cheung KM, Khong PL, Kim M (2012) Age-related diffusion patterns in human lumbar intervertebral discs: a pilot study in asymptomatic subjects. Magn Reson Imaging 30:181–188 33. Frobin W, Brinckmann P, Kramer M, Hartwig E (2001) Height of lumbar discs measured from radiographs compared with degeneration and height classified from MR images. Eur Radiol 11:263–269
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