Journal of Biomechanics 48 (2015) 2060–2066

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Journal of Biomechanics
journal homepage: www.elsevier.com/locate/jbiomech
www.JBiomech.com

Mechanical analysis of the human cadaveric thoracic spine

with intact rib cage
Erin M. Mannen a, John T. Anderson b,1, Paul M. Arnold c,2, Elizabeth A. Friis d,n
a
University of Kansas, Mechanical Engineering, 1530 W 15th Street, Learned Hall Room 3138, Lawrence, KS 66045, USA
b
Children's Mercy Hospital and Clinics of Kansas City, Orthopaedic Surgery, 2401 Gillham Road, Kansas City MO 64108, USA
c
University of Kansas Medical Center, Department of Neurosurgery, 3901 Rainbow Bvld., MS 3021, Kansas City, KS 66160, USA
d
University of Kansas, Mechanical Engineering, 1530 W 15th Street, Learned Hall Room 3138, Lawrence, KS 66045, USA

art ic l e i nf o a b s t r a c t

Article history: The goal of this study was to characterize the overall in-plane and basic coupled motion of a cadaveric
Accepted 22 March 2015 human thoracic spine with intact true ribs. Researchers are becoming increasingly interested in the
thoracic spine due to both the high prevalence of injury and pain in the region and also innovative
Keywords: surgical techniques that utilize the rib cage. Computational models can be useful tools to predict loading
Thoracic spine patterns and understand effects of surgical procedures or medical devices, but they are often limited by
Rib cage insufficient cadaveric input data. In this study, pure moments to 75 N m were applied in flexion–
Human cadaver extension, lateral bending, and axial rotation to seven human cadaveric thoracic spine specimens (T1–
Biomechanics T12) with intact true ribs to determine symmetry of in-plane motion, differences in neutral and elastic
Range of motion
zone motion and stiffness, and significance of out-of-plane rotations and translations. Results showed
that lateral bending and axial rotation exhibited symmetric motion, neutral and elastic zone motion and
stiffness values were significantly different for all modes of bending (po 0.05), and out-of-plane rota-
tions and translations were greater than zero for most rotations and translations. Overall in-plane
rotations were 7.773.4° in flexion, 9.6 73.7° in extension, 23.3 7 8.4° in lateral bending, and 26.3 712.2°
in axial rotation. Results of this study could provide inputs or validation comparisons for computational
models. Future studies should characterize coupled motion patterns and local and regional level bio-
mechanics of cadaveric human thoracic spines with intact true ribs.
& 2015 Elsevier Ltd. All rights reserved.

1. Introduction intact rib cage. In addition, computational models often depend on

biomechanical data as inputs, so the lack of data on the intact rib cage
Research on the thoracic spine and the thoracolumbar regions is limits the progress to develop a computational model that accurately
attracting interest due to both the potential to utilize the rib cage to represents a spine with intact rib cage. The goal of this study was to
explore fusion alternatives and also to study causes and treatment characterize the overall in-plane motion and stiffness and basic cou-
options of problems occurring in these areas. Some medical device pled motion patterns of a human cadaveric thoracic spine with intact
developers are designing systems that attach directly to the rib cage as true ribs.
a way to treat patients with thoracic insufficiency syndrome or sco- Computational modeling may help inform medical device
liosis (Campbell, 2013). Other researchers are interested in under- design or surgical procedure planning, but the few thoracic models
standing the loading mechanics of the spine and rib cage that may that exist may not be appropriately informed by mechanical
lead to pain and vertebral fractures in the thoracic spine (Andersen cadaveric testing because research on a full thoracic spine is sparse
et al., 2007; Delmas et al., 2005; Melton et al., 1993). However, there is (Andriacchi et al., 1974; Bruno et al., 2012; Closkey et al., 1992; Iyer
little understanding of the mechanics of the thoracic spine with an et al., 2010). Vertebral fracturing, scoliosis, and back pain in the
thoracic spine might be better understood if the computational
n
Corresponding author. Tel.: þ 1 785 864 2104. models to predict loading patterns were more robust. This study
E-mail addresses: erinmannen@gmail.com (E.M. Mannen), sought to provide a thorough understanding of the overall bio-
jtanderson@cmh.edu (J.T. Anderson), parnold@kumc.edu (P.M. Arnold), mechanical motion of the human thoracic spine with intact rib
lfriis@ku.edu (E.A. Friis).
1
Tel.: þ1 816 234 3693. cage for the purpose of providing reliable inputs and validation
2
Tel.: þ1 913 588 7587. comparison values for computational models and medical device

http://dx.doi.org/10.1016/j.jbiomech.2015.03.021
0021-9290/& 2015 Elsevier Ltd. All rights reserved.
 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066 2061

design that could be used to understand and advance thoracic

spine treatments.
The thoracic spine, due to the rib cage, presents added chal-
lenges in mechanical testing when compared to the lumbar or
cervical spine. While methods for mechanical testing in the lum-
bar and cervical regions are well-developed and frequently con-
ducted, testing of the thoracic spine is much less common and
standardized. Some researchers have analyzed functional spine
units or short segments of the thoracic spine (Oda et al., 2002;
Panjabi et al., 1976; Sangiorgio et al., 2013). Others have studied
segments of the thoracic spine without the rib cage intact, dis-
secting the ribs a few centimeters lateral to the costovertebral
joints (Ilharreborde et al., 2010; Sangiorgio et al., 2013). However,
one study suggests that the rib cage provides 30 to 40 percent of
the stability in the thoracic region (Watkins et al., 2005). It is
therefore critical to understand the overall biomechanics of the
full thoracic region with an intact rib cage. There are only three
studies that have examined full thoracic spine biomechanics (T1–
T12) of a human cadaveric spine with an intact rib cage (Healy
et al., 2014; Horton et al., 2005; Watkins et al., 2005); one study
looked at T2–T10 (Feiertag et al., 1995). None of this work has
provided biomechanical information of the intact specimen other
than in-plane range-of-motion (ROM) data. There remains a sig-
nificant gap in the understanding of overall motion, stiffness, and
basic coupled motion of a human cadaveric thoracic specimen
with an intact rib cage.
This research effort aimed to understand the motion of a human
cadaveric thoracic spine with an intact rib cage. The following
hypotheses were tested for overall motion: (i) in-plane motion will
be symmetric for right and left lateral bending, and right and left
axial rotation, (ii) neutral and elastic zones, and neutral and elastic
zone stiffness values will be significantly different in all modes of
bending, and (iii) significant out-of-plane rotations and translations
in all planes will occur in all modes of bending.

2. Methods
Fig. 1. Photo of a T1–T12 human cadaveric specimen with true ribs, depicted here
from the left in the lateral bending testing mode. T1 and T12 were potted, and T12
2.1. Experimental design was fixed rigidly to the base of the spine test machine. An optical motion-capture
pin was inserted into the superior potting (T1). Specimens were loaded to þ 5 N m
Seven human fresh-frozen cadaver thoracic specimens (T1–T12) were dissected in flexion–extension, lateral bending, and axial rotation.
to include only vertebrae, true ribs (T1–T10), sternum, intervertebral disks, and
stabilizing ligaments. Age at the time of death was 71 77 years. All specimens were
x-rayed to determine existence of fractures, severe abnormalities or osteophytes, or
USA). Each specimen was aligned and mounted in a novel spine testing machine
previous surgeries that would cause exclusion. All specimens were considered
(Applied Test Systems, Butler, PA, USA) which allowed for the continuous application
acceptable to be included in the study (n¼ 7). Table 1 provides a detailed
of a pure moment to a specified load limit with control over the rate of displacement
description of the specimen group.
(Mannen et al., 2015). The inferior end (T12) was rigidly mounted to the machine, and
Specimens were kept hydrated and thawed to room temperature before testing.
the superior end (T1) was unconstrained and free to move in all directions.
Screws were inserted into the T1 and T12 vertebrae, and each end was potted parallel
An optical motion-capture research pin with three non-collinear markers
to the vertebral end plate using auto-body filler potting (Bondo, 3M, St. Paul, MN,
(Optotrak, Northern Digital Inc., Waterloo, ON, Canada) was inserted into the
posterior edge of the superior potting (considered T1). Error in the motion-capture
diodes was reported as 7 0.1 mm in translational motion which was calculated to
Table 1 be 7 0.06° for the experimental setup (Northern Digital, Inc., 2010). The local
Details on cadaveric specimens used in the study. All specimens were white males. coordinate system at T1 was defined as the centroid of the potting, representing
the centroid of the T1 vertebrae. Fig. 1 shows the experimental setup.
Specimen Age Height (in.) Weight Cause of death Pure moments were applied to a load limit of 75 N m at a displacement rate of
number (years) (lbs) 1 °/s in three modes of bending [flexion–extension, lateral bending, and axial
rotation] applied in a random order. Each specimen was tested for five cycles; the
1 82 71 200 End stage debility third cycle was used for data analysis. Saline solution was sprayed on the specimen
2 59 70 198 Atherosclerotic cardio- throughout testing to preserve mechanical integrity. Load was recorded from the
vascular disease test machine, and angular and translational displacements were calculated from
3 76 72 220 Undetermined the displacement data from the optical motion-capture pin at T1.
4 69 70 160 Undetermined
5 66 70 300 End stage debility
2.2. Data and statistics
6 70 73 220 Urinary bladder cancer
7 73 70 170 Hypertension
Matlab (MathWorks, Natick, MA, USA) was used to analyze the data and per-
form statistics. Euler decomposition techniques in which the first Euler rotation
Mean (7 St 71 (7) 70 (1) 209 (46) corresponded with the mode of bending were used to determine both in-plane and
Dev) out-of-plane rotations (Crawford et al., 1996). Fig. 2 shows the following in-plane
Range 59–82 70–73 160–300 rotation and stiffness parameters that were found for each mode of bending
2062 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066

Fig. 2. Schematic of the displacement vs. load curve of a typical testing cycle.
Overall range-of-motion, neutral zone range-of-motion, elastic zone range-of-
motion, neutral zone stiffness, and elastic zone stiffness are depicted.

(flexion, extension, right lateral bending, left lateral bending, right axial rotation,
and left axial rotation), reported in degrees or degrees/N m (Wilke et al., 1998):

 Neutral zone: angulation difference at zero load of complete flexion–extension,

lateral bending, and axial rotation cycles,
 Neutral zone stiffness: slope of the load vs. angular displacement curve at
0 N m,
 Elastic zone: angular displacement from the end of neutral zone to the point of
maximum loading ( 7 5 N m),
 Elastic zone stiffness: slope of the load vs. angular displacement curve at the
point of maximum loading ( 7 5 N m),
 Range-of-motion: angular displacement from 0 N m to maximum load
( 75 N m).

Mean overall in-plane range-of-motion, elastic zone, neutral zone stiffness, and
elastic zone stiffness were calculated for flexion, extension, right/left lateral
bending, and right/left axial rotation, individually. Mean neutral zone was calcu-
lated for the entire cycles of flexion–extension, lateral bending, and axial rotation. Fig. 3. Typical overall in-plane angular displacement vs. load cycle in (A) flexion
Mean out-of-plane rotation range-of-motions were reported as percentages of (þ )/extension(  ), (B) right( þ)/left(  ) lateral bending, and (C) right( þ)/left(–)
the in-plane rotation range-of-motion for each mode of bending, normalized for axial rotation for T1. Specimens were loaded to 75 N m for 5 cycles.
each specimen. Mean flexion–extension ratios, lateral bending ratios, and axial
rotation ratios were found for every mode of bending. Each ratio was defined as the
range-of-motion in any given direction (flexion–extension, lateral bending, or axial
rotation) divided by the in-plane range-of-motion specific to that mode of bending.
For example, the flexion–extension ratio for the lateral bending mode of bending
was defined as the out-of-plane range-of-motion in flexion–extension divided by
the in-plane range-of-motion in lateral bending, reported as a percentage.
Mean translational displacements of T1 were defined as deviations from the
neutral position at 75 N m for right–left lateral, anterior–posterior, and superior–
inferior translations. The mean translational deviations in every direction right–left
lateral, anterior–posterior, and superior–inferior) for each mode of testing (flexion–
extension, lateral bending, and axial rotation) were reported for overall motion.
To test the stated hypotheses, Student's t-tests at a p o 0.05 significance level
were used to compare (i) in-plane range-of-motion, elastic zone, neutral zone
stiffness, and elastic zone stiffness to determine symmetry between right/left lat-
eral bending and right/left axial rotation, (ii) neutral zone to elastic zone, and
neutral zone stiffness to elastic zone stiffness in all modes of bending, and (iii) all
out-of-plane rotations and translations to zero motion in all modes of bending.

3. Results

3.1. In-plane

Typical in-plane angular displacement vs. load cycles for flexion– Fig. 4. Mean overall in-plane range-of-motion values of T1 with respect to T12 for
extension, lateral bending, and axial rotation are depicted in Fig. 3. flexion, extension, flexion–extension, lateral bending, and axial rotation. Standard
deviation bars and maximum and minimum values (х) are depicted. Values were
No significant difference was found between right/left lateral bend-
significantly different for flexion and extension, flexion–extension and lateral
ing or right/left axial rotation for range-of-motion, elastic zone, bending, and flexion–extension and axial rotation (p o 0.05).
neutral zone stiffness, or elastic zone stiffness, so all lateral bending
and axial rotation values were reported for the total cycles. stiffness values are depicted in Fig. 6. Mean overall, neutral zone
Overall in-plane range-of-motion values for all modes of and elastic zone in-plane range-of-motion values, and neutral and
bending are depicted in Fig. 4. Neutral zone and elastic zone values elastic zone stiffness values for all modes of bending are reported
are depicted in Fig. 5. Mean neutral zone stiffness and elastic zone in Table 2.
 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066 2063

4. Discussion

4.1. In-plane: overall range-of-motion

As seen in Fig. 4, the mean in-plane range-of-motion was lar-

gest in axial rotation followed by lateral bending, though no sig-
nificant difference was found between the two. The lowest range-
of-motion occurred in flexion–extension, with extension exhibit-
ing a significantly larger range-of-motion than flexion. The stan-
dard deviations ranged from 36% to 46% of the mean range-of-
motion values. Null hypothesis (i) that overall in-plane motion will
be symmetric for right/left lateral bending and right/left axial
rotation failed to be rejected for range-of-motion values, indicating
symmetry in range-of-motion.
These results were comparable to previously published litera-
ture. Table 3 is a summary of the in-plane range-of-motion data
from the present study alongside the results of four previous
studies known to the authors that analyzed intact human cada-
veric full (T1–T12) or nearly-full (T2–T10) thoracic segments with
intact rib cages (Feiertag et al., 1995; Healy et al., 2014; Horton
et al., 2005; Watkins et al., 2005)
Healy et al. sought to understand the changes in range-of-
motion of the thoracic region after a series of decompression
Fig. 5. Mean and standard deviations of the overall neutral zone and elastic zone
surgical techniques utilizing a custom-made automated robotic
angular displacements for each mode of bending: flexion, extension, flexion– test system. As a part of the study, the in-plane range-of-motion
extension, lateral bending, and axial rotation. Neutral zone values were sig- values were reported for flexion–extension, lateral bending, and
nificantly different in flexion–extension and lateral bending (po 0.05). Elastic zone
axial rotation. When compared to the present study, results agree
values were significantly different in flexion and extension, flexion and lateral
bending, and flexion and axial rotation (p o 0.05). Neutral zone and elastic zone that flexion–extension was the stiffest of all modes of bending,
values were significantly different in lateral bending and axial rotation (p o0.05). while lateral bending and axial rotation showed larger and com-
parable range-of-motion values. However, Healy et al. reported
larger range-of-motion values for all modes of bending. This could
be contributed to the much lower average age of the specimens
used by Healy et al. when compared to the present research.
Watkins et al. used an adapted automated test machine for the
purpose of understanding the contribution of the rib cage and
sternum to thoracic stability in flexion–extension, lateral bending,
and axial rotation. Specimens were tested in three conditions:
intact, fractured sternum, and rib cage removed. Intact range-of-
motion results in axial rotation are comparable and similar to the
present study, as the load limit was 7 5 N m in axial rotation. In
flexion–extension and lateral bending modes, the load limits were
only 72 N m. The range-of-motion in flexion–extension and lat-
eral bending of the present study at 72 N m were found to be
6.2 73.1° and 8.5 73.6°, respectively, comparing closely to the
measures of 7.9° and 10.4°, respectively, as reported by Watkins
et al. The two other studies used manual loading techniques to
examine the role of various anatomical elements or the effect of
Fig. 6. Mean and standard deviations of the overall neutral zone stiffness and the sequence of surgical releases in flexion–extension and lateral
elastic zone stiffness for each mode of bending: flexion, extension, lateral bending,
bending range-of-motion of the thoracic region. Because these
and axial rotation. Neutral zone stiffness and elastic zone stiffness were sig-
nificantly different for extension and lateral bending (p o0.05). Neutral zone studies were conducted on manual machines, it is more difficult to
stiffness values were significantly different for flexion and lateral bending, exten- directly compare range-of-motion results with the present study.
sion and lateral bending, and extension and axial rotation (p o0.05). Feiertag et al. included only T2–T10, so lower range-of-motion
values are to be expected when compared with studies conducted
on the full thoracic segment of T1–T12. Assuming that the T2–T10
3.2. Out-of-plane segment (9 vertebrae) constitutes 75% of the T1–T12 segment (12
vertebrae), it is interesting to note that flexion–extension range-
Out-of-plane rotation data are depicted in Fig. 7. All rotation of-motion reported is 72% of flexion–extension range-of-motion in
ratios for all modes of bending are reported in Table 2. the present study, and lateral bending range-of-motion reported is
57% of lateral bending range-of-motion in the present study. While
3.3. Translations several considerations (e.g., vertebral level, true vs. floating rib
levels, load limits, and vertebral height) were not taken into
Mean translations of T1 in anterior–posterior, right–left, and account when making these basic observations, they highlight the
superior–inferior directions for all modes of bending are reported in need to understand motion at local and regional levels as well as
Table 2. overall motion in the thoracic spine.
2064 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066

Table 2
Mean ( 7 standard deviation) values of in-plane and out-of-plane range-of-motion, stiffness, and translation for all modes of bending. This intact specimen data set will be
useful in validation of thoracic spine computational models and device testing.

Flexion Extension Flexion–extension Lateral bending Axial rotation

In-plane
Overall ROM (deg) 7.7 (3.4) 9.6 (3.7) 17.3 (7.0) 23.3 (8.4) 26.3 (12.2)
Neutral zone ROM (deg) – – 2.3 (1.0) 4.5 (3.2) 3.0 (1.6)
Elastic zone ROM (deg) 6.6 (3.1) 8.4 (3.3) – 9.4 (3.2) 11.6 (5.5)
Neutral zone stiffnes (N m/deg) 0.40 (0.22) 0.44 (0.30) – 0.23 (0.13) 0.26 (0.16)
Elastic zone stiffness (N m/deg) 2.12 (1.22) 1.22 (0.82) – 1.48 (0.95) 1.47 (1.43)

Out-of-plane rotation ratios

Flexion–extension (%) – – – 24.0 (15.3) 25.5 (17.7)
Lateral bending (%) – – 14.0 (9.2) – 12.1 (10.5)
Axial rotation (%) – – 18.2 (26.0) 12.4 (8.6) –

Translations
Anterior–posterior (mm) – – 12.6 (11.1) 3.9 (2.6) 6.7 (5.1)
Right–left (mm) – – 2.9 (1.9) 30.4 (23.5) 8.6 (9.1)
Superior–inferior (mm) – – 3.4 (4.3) 4.2 (3.6) 1.6 (1.4)

4.3. In-plane: neutral zone stiffness and elastic zone stiffness

Stiffness data has been reported for the cervical and lumbar
regions (Panjabi, 1992), but to the authors' knowledge, no neutral
zone stiffness or elastic zone stiffness data for human cadaveric
thoracic spines with rib cages is reported in previously published
literature. Neutral zone stiffness and elastic zone stiffness values
were symmetric for right/left lateral bending, and right/left axial
rotation, thus failing to reject null hypothesis (i). As shown in
Fig. 6, neutral zone stiffness values in the thoracic spine were
found to be significantly lower than elastic zone stiffness values in
extension and lateral bending; trends for this same behavior were
Fig. 7. Mean and standard deviations of the ratios of angular motions of T1 with
respect to T12 in all rotations for all modes of bending [flexion–extension, lateral
also observed for flexion and axial rotation (p ¼0.08, p ¼0.06). This
bending, and axial rotation]. For example, the flexion–extension-ratio represents stiffness data along with range-of-motion, neutral zone, and
the motion in the flexion–extension plane divided by the in-plane motion of the elastic zone data can provide researchers with a baseline under-
applied mode of bending. Thus, the flexion–extension-ratio is 100% in the flexion– standing of the shape of the in-plane displacement vs. loading
extension mode of bending. For each mode of bending, no significant difference
curve of the thoracic spine with rib cage.
was found between the two out-of-plane range-of-motions. Significance was found
between the in-plane range-of-motion and both corresponding out-of-plane range-
of-motions for each mode of bending (p o 0.05). All out-of-plane rotations in all 4.4. Out-of-plane motion
modes of bending were found to be significantly different than zero motion
(po 0.05) except flexion–extension motion in the axial rotation mode of bending
To the authors' knowledge, no out-of-plane motion data for
(p¼ 0.19).
human cadaveric thoracic spines with rib cages is reported in pre-
viously published literature. As presented in Fig. 7, out-of-plane
rotations were observed in all modes of bending except flexion–
4.2. In-plane: neutral zone and elastic zone
extension motion in axial rotation. In axial rotation, the standard
deviation of the flexion–extension ratio was over 100% of the mean
To the authors' knowledge, no neutral zone or elastic zone data
value which may be attributed to a large out-of-plane rotation of 65%
for human cadaveric thoracic spines with rib cages is reported in
for the flexion–extension ratio in specimen two. As seen in Table 1,
previously published literature. Elastic zone values were sym- specimen two was the youngest of all cadaveric specimens and
metric for right/left lateral bending, and right/left axial rotation, exhibited the largest range-of-motion in axial rotation. The large out-
thus failing to reject null hypothesis (i). As expected, sigmoidal of-plane rotation brings into question the correlation between age
behavior which has been previously reported in the lumbar and and thoracic motion and coupling mechanics; future work should
cervical regions of the spine was also found in the full thoracic focus on age-related differences.
region (see Fig. 3). Neutral zone values were significantly lower Coupled motion has been studied in the thoracic spine on animal
than elastic zone values for all modes of bending (see Fig. 5), thus models, living humans, and human functional spine units (Fujimori
failing to reject null hypothesis (ii). et al., 2012; Fujimori et al., 2013; Panjabi et al., 1976; Sizer et al.,
Researchers have reported that neutral zone values of cadaveric 2007; Takeuchi et al., 1999; Willems et al., 1996). Results of these
canine thoracic sections range from 0.6° to 5.9° for all modes of studies generally agree that (1) lateral bending and axial rotation
tend to exhibit coupling, (2) coupling patterns may not be consistent
bending (Oda et al., 1996; Takeuchi et al., 1999), while neutral zone
throughout the entire thoracic spine, (3) a large variation in coupling
results from the present study range from 2.3° to 4.5°, within the
mechanics between specimens is present even within the same
range reported for the canine studies. Further testing should be
study, and (4) there is a poor correlation between computational
done to better understand neutral zone and elastic zone regions of modeling and experimental results. The limitations of these studies
the human thoracic spine. make comparison of data difficult.
 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066 2065

Table 3
Summary of overall (T1–T12) mean ( 7 standard deviation) in-plane range-of-motion (ROM) data from published literature from tests done on human cadaveric specimens
with intact ribs. Note that Feiertag et al. performed tests on T2–T10 segments, and Horton et al. and Feiertag et al. used manual loading systems while all others used
automated test machines.

Author, year Age (years) Load limits Range-of-motion (deg)

Flexion/ Lateral Axial rotation Range-of-motion Flexion/extension Lateral Axial rotation
extension bending measure bending

Present study, 2015 71 (7) 5Nm 5Nm 5Nm Overall 17.3 (7.0) 23.3 (8.4) 26.3 (12.2)
59–82 Overall range 8.0–25.8 11.2–35.7 13.3–44.6
Neutral zone 2.3 (1.0) 4.5 (3.2) 3.0 (1.6)
Elastic zone F 6.6 (3.1), E 8.4 9.4 (3.2) 11.6 (5.5)
(3.3)

Healy et al. (2014) 59 (9.5) 5Nm 5Nm 5Nm Overall 26.9 (10.0) 42.1 (19.0) 43.7 (16.9)

Watkins et al. 72a 2Nm 2Nm 5 N mb Overall 7.93a 10.36a 23.03a

(2005)
55–91 Overall range 2.64–15.64 1.92–26.81 6.17–51.44

Horton et al. 73.6a 25 N – – Overall 30.2 (9.0) – –

(2005) 65–82

Feiertag et al. – 89 N 89 N – Overall 12.6 (5.6) 14.5 (5.5) –

(1995)

(–) Value not reported.

a
Standard deviation not reported.
b
50 N axial preload applied.

In the present study, it was observed that the coupling patterns thoracic spine so that cadaveric work could be more reliable when
may not remain constant throughout the loading and unloading applied to living people. In addition, the average age of the speci-
cycles; this data will be reported in subsequent manuscripts. While mens in this study was 71 years, so results should be used with
the results of the present study give researchers a basic under- caution when applying to a younger demographic.
standing of coupled motion in the full human thoracic spine, there is This study did not model specific musculature or intra-abdominal
much work to be done to understand the shape of the coupled pressure, though some researchers are representing these elements
motion patterns. A thorough understanding of the patterns of cou- in computational models (Bruno et al., 2012; Iyer et al., 2010). Both
pled motion in the cadaveric thoracic spine, both on the entire factors may contribute to increased stability in the thoracic spine and
thoracic column and on local and regional levels, is necessary to fully decreased compressive forces (Hodges et al., 2001; Stokes et al.,
characterize the biomechanics in the human thoracic spines with rib 2010), but more research should be done to better understand the
cages. effects of these parameters.
No follower or compressive loads were used in this study. Geo-
4.5. Translations metric limitations would have prevented the application of a fol-
lower load if the methods utilized in the cervical or lumbar regions
To the authors' knowledge, no translational motion data for were used (Patwardhan et al., 2000), as the anterior portions of the
human cadaveric thoracic spines with rib cages is reported in vertebral column were obstructed by the rib cage. To the authors'
previously published literature. As expected, in flexion–extension knowledge, only one study with an intact rib cage has used com-
and lateral bending, the largest translations of T1 were exhibited pressive loads, and only in axial rotation (Watkins et al., 2005). One
in anterior–posterior and right–left planes, respectively. Likewise, study suggests that a follower load in the thoracic spine without a rib
in axial rotation, the largest and most comparable translations cage may mimic physiological loading (Stanley et al., 2004), though
were seen in the anterior–posterior and right–left planes, though more work needs to be done to determine both a method of appli-
no significant difference was found between any planes. cation and the significance of follower or compressive loads in a
The importance of allowing unconstrained motion on the thoracic specimens with rib cages. While a compressive preload has
superior end was supported by measured translations compared been shown to increase bending stiffness in lumbar functional spine
to zero motion that occurred in all directions in all modes of units (Patwardhan et al. 2003), the effect of preloads or follower
bending (statistically significant except for trend of superior– loads in the thoracic spines with rib cages.
inferior motion in flexion–extension at p ¼0.08). More in-depth
analysis including local and regional vertebral translations should 4.7. Future work
be studied.
There is much work to be done in mechanical characterization
4.6. Limitations of the thoracic spine. Although some researchers have analyzed
overall range-of-motion, the lack of a standardized testing method
A major limitation of working with cadaveric tissue is the com- in the thoracic spine renders it difficult to compare results of
parison and application of the results to living humans. It would be different studies. The spine testing community would benefit from
interesting to better understand the relationship between in vitro defining the preferred testing method for human cadaveric thor-
human motion and in vivo cadaveric human motion analysis in the acic spine specimens with an intact rib cage.
2066 E.M. Mannen et al. / Journal of Biomechanics 48 (2015) 2060–2066

In addition, while overall behavior is a critical first step in char- in trunk lateral bending: in vivo three-dimensional analysis. Spine J. 14,
acterizing thoracic spinal motion, local and regional level analyses 1991–1999.
Healy, A.T., Lubelski, D., Mageswaran, P., Bhowmick, D.A., Bartsch, A.J., Benzel, E.C.,
are necessary to better understand the biomechanics of the spine Mroz, T.E., 2014. Biomechanical analysis of the upper thoracic spine after
and rib cage. This information will give researchers more accurate decompressive procedures. Spine J. 14, 1010–1016.
inputs to improve upon computational models. Finally, by fully Hodges, P.W., Cresswell, A.G., Daggfeldt, K., Thorstensson, A., 2001. In vivo mea-
surement of the effect of intra-abdominal pressure on the human spine. J.
understanding the biomechanics of the thoracic spine, researchers Biomech. 34, 347–353.
could study the overall and local level effects of thoracic instru- Horton, W.C., Kraiwattanapong, C., Akamaru, T., Minamide, A., Park, J.S., Park, M.S.,
mentation and surgical procedures in the thoracic region on both Hutton, W.C., 2005. The role of the sternum, costosternal articulations, inter-
vertebral disc, and facets in thoracic sagittal plane biomechanics: a comparison
cadaveric and computational models. of three different sequences of surgical release. Spine 30, 2014–2023.
The results of this study add to the understanding of human Ilharreborde, B., Zhao, K., Boumediene, E., Gay, R., Berglund, L., An, K.N., 2010. A
thoracic biomechanics. Further work should be done to more fully dynamic method for in vitro multisegment spine testing. Orthop. Traumatol.
Surg. Res. 96, 456–461.
characterize the coupling motion patterns and local and regional
Iyer, S., Christiansen, B.A., Roberts, B.J., Valentine, M.J., Manoharan, R.K., Bouxsein,
level biomechanics of human cadaveric spines with intact rib cages. M.L., 2010. A biomechanical model for estimating loads on thoracic and lumbar
vertebrae. Clin. Biomech. 25, 853–858.
Mannen, E.M., Ranu, S.S., Villanueva, A.M., Friis, E.A., 2015. Validation of a novel
spine test machine. J. Med. Devices, 9.
Conflict of interest Melton 3rd, L.J., Lane, A.W., Cooper, C., Eastell, R., O’Fallon, W.M., Riggs, B.L., 1993.
Prevalence and incidence of vertebral deformities. Osteoporos. Int. 3, 113–119.
The authors have no financial or personal relationships that Northern Digital, Inc., 2010. Optotrak Certus Brochure. Waterloo, Canada.
Oda, I., Abumi, K., Cunningham, B.W., Kaneda, K., McAfee, P.C., 2002. An in vitro
would inappropriately influence the results of this study. human cadaveric study investigating the biomechanical properties of the
thoracic spine. Spine 27, E64–E70.
Oda, I., Abumi, K., Lu, D., Shono, Y., Kaneda, K., 1996. Biomechanical role of the
posterior elements, costovertebral joints, and rib cage in the stability of the
Acknowledgments thoracic spine. Spine 21, 1423–1429.
Panjabi, M.M., 1992. The stabilizing system of the spine. Part II. Neutral zone and
The authors thank Nikki Galvis and Emily Shipman for their instability hypothesis. J. Spinal Disord. 5, 390–396 (discussion 397).
Panjabi, M.M., Brand Jr., R.A., White 3rd, A.A., 1976. Mechanical properties of the
help during testing. The donation of specimens by Oread Medical, human thoracic spine as shown by three-dimensional load–displacement
LLC is greatly appreciated. curves. J. Bone Jt. Surg. 58, 642–652.
Patwardhan, A.G., Havey, R.M., Ghanayem, A.J., Diener, H., Meade, K.P., Dunlap, B.,
Hodges, S.D., 2000. Load-carrying capacity of the human cervical spine in
compression is increased under a follower load. Spine 25, 1548–1554.
References Patwardhan, A.G., Havey, R.M., Carandang, G., Simonds, J., Voronov, L.I., Ghanayem,
A.J., Meade, K.P., Gavin, T.M., Paxinos, O., 2003. Effect of compressive follower
preload on the flexion–extension response of the human lumbar spine. J.
Andersen, J.H., Haahr, J.P., Frost, P., 2007. Risk factors for more severe regional
Orthop. Res. 21, 540–546.
musculoskeletal symptoms: a two-year prospective study of a general working
Sangiorgio, S.N., Borkowski, S.L., Bowen, R.E., Scaduto, A.A., Frost, N.L., Ebramzadeh,
population. Arthritis Rheumatol. 56, 1355–1364.
E., 2013. Quantification of increase in three-dimensional spine flexibility fol-
Andriacchi, T., Schultz, A., Belytschko, T., Galante, J., 1974. A model for studies of
lowing sequential Ponte osteotomies in a cadaveric model. Spine Deform. 1,
mechanical interactions between the human spine and rib cage. J. Biomech. 7,
171–178.
497–507.
Sizer Jr., P.S., Brismee, J.M., Cook, C., 2007. Coupling behavior of the thoracic spine: a
Bruno, A.G., Anderson, D.E., D’Agostino, J., Bouxsein, M.L., 2012. The effect of
systematic review of the literature. J. Manip. Physiol. Ther. 30, 390–399.
thoracic kyphosis and sagittal plane alignment on vertebral compressive
Stanley, S.K., Ghanayem, A.J., Voronov, L.I., Havey, R.M., Paxinos, O., Carandang, G.,
loading. J. Bone Miner. Res. 27, 2144–2151.
Zindrick, M.R., Patwardhan, A.G., 2004. Flexion–extension response of the
Campbell Jr., R.M., 2013. VEPTR: past experience and the future of VEPTR principles.
thoracolumbar spine under compressive follower preload. Spine 29, E510–E514.
Eur. Spine J. 22 (Suppl. 2), S106–S117.
Stokes, I.A., Gardner-Morse, M.G., Henry, S.M., 2010. Intra-abdominal pressure and
Closkey, R.F., Schultz, A.B., Luchies, C.W., 1992. A model for studies of the
abdominal wall muscular function: spinal unloading mechanism. Clin. Bio-
deformable rib cage. J. Biomech. 25, 529–539.
mech. 25, 859–866.
Crawford, N.R., Yamaguchi, G.T., Dickman, C.A., 1996. Methods for determining
Takeuchi, T., Abumi, K., Shono, Y., Oda, I., Kaneda, K., 1999. Biomechanical role of the
spinal flexion/extension, lateral bending, and axial rotation from marker
intervertebral disc and costovertebral joint in stability of the thoracic spine: a
coordinate data: analysis and refinement. Hum. Mov. Sci. 15, 55–78.
canine model study. Spine 24, 1414–1420.
Delmas, P.D., van de Langerijt, L., Watts, N.B., Eastell, R., Genant, H., Grauer, A.,
Watkins 4th, R, Watkins 3rd, R., Williams, L., Ahlbrand, S., Garcia, R., Karamanian, A.,
Cahall, D.L., 2005. Underdiagnosis of vertebral fractures is a worldwide pro-
Sharp, L., Vo, C., Hedman, T., 2005. Stability provided by the sternum and rib
blem: the IMPACT study. J. Bone Miner. Res. 20, 557–563.
cage in the thoracic spine. Spine 30, 1283–1286.
Feiertag, M.A., Horton, W.C., Norman, J.T., Proctor, F.C., Hutton, W.C., 1995. The effect
Wilke, H.J., Wenger, K., Claes, L., 1998. Testing criteria for spinal implants: recom-
of different surgical releases on thoracic spinal motion. A cadaveric study. Spine
mendations for the standardization of in vitro stability testing of spinal
20, 1604–1611.
implants. Eur. Spine J. 7, 148–154.
Fujimori, T., Iwasaki, M., Nagamoto, Y., Ishii, T., Kashii, M., Murase, T., Sugiura, T.,
Willems, J.M., Jull, G.A., J, K.F., 1996. An in vivo study of the primary and coupled
Matsuo, Y., Sugamoto, K., Yoshikawa, H., 2012. Kinematics of the thoracic spine
rotations of the thoracic spine. Clin. Biomech. 11, 311–316.
in trunk rotation in vivo 3-dimensional analysis. Spine 37, E1318–E1328.
Fujimori, T., Iwasaki, M., Nagamoto, Y., Matsuo, Y., Ishii, T., Sugiura, T., Kashii, M.,
Murase, T., Sugamoto, K., Yoshikawa, H., 2013. Kinematics of the thoracic spine