Professional Documents
Culture Documents
Basic Science
Abstract BACKGROUND CONTEXT: Intervertebral disc and facet joints are the two primary load-
bearing structures of the lumbar spine, and altered loading to these structures may be associated
with frontal plane spinal deviations.
PURPOSE: To determine the load on the lumbar facet joint and intervertebral disc under simu-
lated frontal plane pelvic obliquity combined loading, an in vitro biomechanical study was
conducted.
STUDY DESIGN/SETTING: An in vitro biomechanical study using a repeated-measures design
was used to compare L4–L5 facet joint and intervertebral disc loading across pure moment and
combined loading conditions.
METHODS: Eight fresh-frozen lumbosacral specimens were tested under five loading conditions:
flexion/extension, lateral bending, axial rotation using pure moment bending (610 Nm), and two
additional tests investigating frontal plane pelvic obliquity and axial rotation (sacrum tilted left
5 and at 10 followed by a 610-Nm rotation moment). Three-dimensional kinematics, facet load,
and intradiscal pressures were recorded from the L4–L5 functional spinal unit.
RESULTS: Sagittal and frontal plane loading resulted in significantly smaller facet joint forces
compared with conditions implementing a rotation moment (p!.05). The facet joint had the highest
peak load during the 10 combined loading condition (124.0630.2 N) and the lowest peak load in
flexion (26.8616.1 N). Intradiscal pressure was high in lateral flexion (495.66280.9 kPa) and
FDA device/drug status: Not applicable. Board of Directors: Pharmacokinesis (C); Scientific Advisory Board: Ne-
Author disclosures: JMP: Grant: American Society of Biomechanics Oncology ($0); Other Office: NeOncology ($0). KK: Nothing to disclose.
(B, Paid directly to institution/employer). JBW: Nothing to disclose. The disclosure key can be found on the Table of Contents and at www.
TPH: Stock Ownership: Orthopeutics, LP (51%), IntralinkSpine, Inc. TheSpineJournalOnline.com.
(35%), Ampac Biotechnology, Inc. (100%), Equinext, LLC (25%); Re- Institutional review board approval was not required as de-identified
search Support (Investigator Salary). WT: Nothing to disclose. NA: Royal- anatomic specimens are exempt according to US Code of Federal Regula-
ties: Medtronics (D), Globus (C), Nuvasive (C); Stock Ownership: Globus tions (45 CFR 46.101(b)).
(E); Private Investments: Medtronics (C); Consulting: Medtronics (B), * Corresponding author. Center for Orthopedic Research, Department
Trans 1 (B); Scientific Advisory Board: Globus (B), Trans 1 (B); Other Of- of Osteopathic Surgical Specialties, College of Osteopathic Medicine,
fice: Globus (B), Trans 1 (B). TCC: Stock Ownership: Pharmacokinesis, Michigan State University, West Fee Hall, 909 West Fee Road, East Lans-
NeOnc Technologies (options only); Consulting: Globus Medical (B); ing, MI 48824, USA. Tel.: (517) 975-3318; fax: (517) 975-3305.
E-mail address: popovi16@msu.edu (J.M. Popovich)
1529-9430/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.spinee.2013.04.011
1582 J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589
flexion (429.06212.9 kPa), whereas intradiscal pressures measured in rotation (253.26135.0 kPa)
and 5 and 10 combined loading conditions were low (255.56132.7 and 267.16127.1 kPa,
respectively).
CONCLUSIONS: Facet loading increased during simulated pelvic obliquity in frontal and trans-
verse planes, whereas intradiscal pressures were decreased compared with sagittal and frontal plane
motions alone. Altered spinopelvic alignment may increase the loads experienced by spinal tissue,
especially the facet joints. Ó 2013 Elsevier Inc. All rights reserved.
Keywords: Spinopelvic alignment; Pelvic obliquity; Facet joint; Disc pressure; Biomechanics
individually wrapped in isotonic saline-soaked gauze to length lumbar and lumbosacral specimens [41,49–51]. Two
allow for adequate hydration until mechanical testing was additional loading conditions were implemented to simulate
performed. frontal plane pelvic obliquity consisting of a 5 lateral bend
Each vertebral body was instrumented with an array of (tilted left such that the lumbar spine was in a right lateral
four infrared light-emitting diodes that were used to monitor bending position) of the sacrum (5 lateral bend and rotation
intervertebral kinematics (Optotrak 3020; Northern Digital, [LBþROT]) and a 10 lateral bend (tilted left) of the sacrum
Inc., Waterloo, Ontario, Canada). Three needle pressure sen- (10 LBþROT), both followed by 610 Nm axial rotation
sors (Model 6376; R.A. Denton, Inc., Rochester Hills, MI, moment. Therefore, a total of five different loading condi-
USA), each consisting of a 15-gauge needle embedded with tions were performed (Fig. 4).
three individual pressure sensors along the distal portion of Mechanical testing, motion analysis, and pressure sensor
the needle, were inserted to the L4 intervertebral disc (essen- systems were synchronized and captured data at 50 Hz.
tially providing a 33 matrix of pressure sensors) to measure Specimens were preconditioned using pure moment load-
intradiscal pressure (Fig. 1). The L4–L5 bilateral facet joint ing before testing. Because of the number of repeated me-
capsules were incised allowing for placement of a piezoresis- chanical tests, three loading cycles were implemented, and
tive force sensor (FlexiForce A-201; Tekscan, Inc., South the second complete loading cycle of each loading condi-
Boston, MA, USA). This force sensor was overlaid with tion was used for data analysis.
pressure-sensitive film (Prescale Measurement Film; Fuji-
film Corporation, Valhalla, NY, USA) and secured by adhe- Data reduction
sive tape (Kapton; Dupont, Wilmington, DE, USA).
Peak facet force represented the loading experienced by
Pressure-sensitive film was used as a qualitative indication
the lumbar facet joints during each loading condition. Mean
of sensor placement and was inspected after each testing con-
peak intradiscal pressure value (mean peak of all nine pres-
dition. A similar version of this sensor has been previously
sure sensors) was chosen to represent the overall loading
used to quantify lumbar facet joint forces [47,48]. Facet sen-
value for the intervertebral disc because the exact place-
sors were calibrated by applying loads to the sensing area of
ment (annulus or nucleus pulposus) of the sensors was
the sensor using a material testing device, and force values
not confirmed through dissection. There were no significant
(Newtons) were linearly interpolated (StrainSmart; Vishay
differences in mean peak intradiscal pressure between right
Micro-Measurements, Malvern, PA, USA). Despite place-
and left lateral bending and rotation conditions, and further-
ment of sensors in each joint, only force from the right facet
more, during frontal and transverse plane motions, primary
joint was recorded (Fig. 2).
loading on the facet joints occurs during ipsilateral lateral
Specimens were secured into a Bose Kinematic Spine
bending and contralateral rotations, respectively. As such,
Testing Device (Bose Corporation, Minnetonka, MN,
comparisons were made among flexion, extension, ipsilat-
USA) for mechanical testing (Fig. 3). The mechanical test-
eral lateral bending, contralateral axial rotation, and 5
ing protocol consisted of five cycles of dynamic pure
LBþROT and 10 LBþROT conditions.
moment loading (610 Nm) into flexion/extension, lateral
flexion, and axial rotation to precondition the spine, fol-
Data analysis
lowed by three loading cycles used to record data. The load-
ing rate was 1 /s until a 610-Nm load limit. This loading A one-way analysis of variance (ANOVA) with repeated
profile has been used or recommended when testing similar measures was performed to compare differences in peak
Fig. 1. An example of the approximate placement of the three needle pressure transducers in the intervertebral disc (Left) and a needle pressure transducer
position confirmed in the L4 disc under fluoroscopy (Right).
1584 J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589
Fig. 2. Force sensor overlaid with pressure-sensitive film and sealed with Kapton tape (Left) and insertion into the right L4–L5 facet joint (Right).
facet joint force and mean peak intradiscal pressure be- significant differences between any of these conditions. Ro-
tween loading conditions. Post hoc testing consisted of tation, 5 LB þ ROT, and 10 LB þ ROT had significantly
paired samples t tests to determine differences in facet lower intradiscal pressure than flexion (p5.002, .003, .01,
loads and intervertebral disc pressures among the different respectively) and lateral bending (p5.01, .01, .01, respec-
loading conditions. Statistical analyses were conducted us- tively). Similarly, rotation and 5 LBþROT had significantly
ing SPSS statistical software (version 15; SPSS, Inc., Chi- lower intradiscal pressure than extension (p5.03, .03, re-
cago, IL, USA), and statistical significance was set at spectively), whereas 10 LBþROT was not significant
p#.05. (p5.07). Mean peak intradiscal pressure for all six loading
conditions are presented in Fig. 6.
Results
Discussion
The ANOVA showed a significant difference in peak
facet joint force between loading conditions (p!.001). Our study investigated the effects of changing frontal
Lowest peak facet joint force was measured during flexion plane orientation of the sacrum (simulated pelvic obliquity)
(26.8616.1 N) and highest in the 10 LBþROT combined on resulting facet joint force and intervertebral disc pres-
loading condition (124.0630.2 N). Post hoc tests revealed sure. The results of this study demonstrate that the load
significant differences between the 10 LBþROT condition sharing of these tissues is dependent on the plane and direc-
and flexion (p!.001), extension (p!.001), lateral bending tion of loading. Facet joint force during combined loading
(p!.001), and rotation (p5.05). There was no significant was higher compared with loading in the three anatomic
difference between 10 LBþROT and 5 LBþROT condi- planes; however intradiscal pressures did not reveal the
tions (p5.12). The 5 LBþROT condition showed similar same patterns. These findings support the clinical notion
statistical results with the exception for when compared that pelvic obliquity may play a role in increasing loads
with rotation (p5.13). Rotation was also significantly on spinal tissues, particularly the facet joints.
greater than flexion (p5.001), extension (p!.001), and lat- Ipsilateral lateral bending and flexion produced similar
eral bending (p5.02). Peak facet joint forces for all six peak intradiscal pressures. Comparing our intradiscal pres-
loading conditions are presented in Fig. 5. sure data with other in vitro investigations yields similar
The ANOVA showed a significant difference in peak in- trends during loading in the anatomic planes [52–54]. Test-
tradiscal pressure between loading conditions (p5.003). ing conditions showed highest intradiscal pressures in lat-
High peak intradiscal pressures were measured during lat- eral bending, followed by flexion, and then axial rotation.
eral bending (495.66280.9 kPa) and flexion (429.06212.9 Steffen et al. [55] investigated the spatial intradiscal pres-
kPa), and there was no significant post hoc difference be- sure distribution of the L4 disc using three needle pressure
tween the two conditions (p5.18). Lowest peak intradiscal sensors that were similar to our experimental setup. They
pressures were measured during rotation (253.26135.0 found intradiscal pressure was highest in combined flexion
kPa), 5 LBþROT (255.56132.7 kPa), and 10 LBþROT and axial rotation and reported values of higher magnitude
(267.16127.1 kPa) conditions, in which there were no than presented in our study. Postexperiment location of
J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589 1585
Fig. 4. An illustration representing the different loading conditions. Flexion and extension are presented together in the sagittal plane testing condition, but
were separated during data analysis allowing for six comparisons.
1586 J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589
A limitation of this study was the combined loading con- readings, particularly from sensors in the annulus. Based
ditions only consisted of axial rotation during simulated on these previous studies, the nucleus pulposus would likely
frontal plane pelvic obliquity (5 LBþROT and 10 be best represented by the middle pressure sensor on the
LBþROT) in vitro. Although it would be interesting to de- needle that was inserted directly in the middle of the anterior
termine the effects of other combined motions (eg, flexion portion of the disc. These middle sensors yielded similar
and extension plus simulated frontal plane pelvic obliq- trends as the reported mean peak pressure values.
uity), the combination of the specimen length and con-
straints of the testing device would not allow for these
combined loading condition. Furthermore, it would have
Conclusions
been interesting to simulate multiple ‘‘real-life’’ situations,
which were not performed in this study. Simulating frontal plane postural deviations during bio-
A common limitation of in vitro testing is that the testing mechanical in vitro testing of the lumbosacral spine appears
is performed on cadaveric specimens devoid of functioning to affect facet joint and intervertebral disc loading behavior.
muscle tissue, and, therefore, the loads measured may not Incorporating these findings into the cumulative trauma
replicate in vivo loading. Whether the loads measured or paradigm may suggest a biomechanical role in spinal load-
differences between conditions are clinically relevant can- ing (particularly the facet joints) in individuals with frontal
not be answered with this study. However, because of the plane spine deviations. Further in vivo investigations are
repeated-measures design, the data presented in this study needed to determine whether a compounding or cumulative
do allow for comparisons across conditions. That is, regard- effect associated with facet loading is evident in patients
less of magnitude of loading, relative differences from one with frontal plane spinal deviations resulting from pelvic
condition to the other are analyzed and can be contributed obliquity. Managing the cause of such deviations may in
to the different conditions. We would hypothesize that the turn prevent the vicious cycle of injury from occurring
same pattern of loading would have occurred in vivo. and prevent further damage to spinal tissues.
Simulating the combined loading conditions that may be
experienced in the presence of pelvic obliquity and result-
ing spinal deviations does not allow for the calculation of
Acknowledgments
the actual segmental loads placed on every spinal level
tested. That is, although pure moment testing assumes that We would like to acknowledge the following entities for
the segmental load is uniform for each segment, the com- their support of this research: Foundation for Physical Ther-
bined effects of the specimen length, anatomic morphology, apy, International Society of Biomechanics, and American
and tissue variability would not allow for calculation of the Society of Biomechanics.
segmental loading during the combined loading conditions.
As mentioned, not all segments were the same length,
which may influence the results because of differences in References
the ligamentous support placed on the spine (eg, anterior [1] Adams MA, Hutton WC. The effect of posture on the role of the
and posterior longitudinal ligaments). This limitation is apophysial joints in resisting intervertebral compressive forces.
somewhat mitigated in that the effects on the results would J Bone Joint Surg Br 1980;62:358–62.
likely be relatively small in magnitude, and the repeated- [2] Lorenz M, Patwardhan A, Vanderby R Jr. Load-bearing characteris-
tics of lumbar facets in normal and surgically altered spinal seg-
measures design of the study compares the conditions ments. Spine 1983;8:122–30.
within each lumbosacral specimen. We would expect simi- [3] Yang KH, King AI. Mechanism of facet load transmission as a hy-
lar results within each specimen across the six loading con- pothesis for low-back pain. Spine 1984;9:557–65.
ditions if only segment length was varied. [4] Andersen JH, Haahr JP, Frost P. Risk factors for more severe re-
We used needle pressure sensors that were sensitive to gional musculoskeletal symptoms: a two-year prospective study of
a general working population. Arthritis Rheum 2007;56:1355–64.
the direction of load. The needle pressure sensors were in- [5] Bigos SJ, Spengler DM, Martin NA, et al. Back injuries in industry:
serted sensitive side up (facing the superior direction); a retrospective study. II. Injury factors. Spine 1986;11:246–51.
however, this may not have captured all loadings in the inter- [6] Heikkila JK, Koskenvuo M, Heliovaara M, et al. Genetic and envi-
vertebral disc. Mcnally and Adams [71] measured stress ronmental factors in sciatica. Evidence from a nationwide panel of
distribution across the lumbar intervertebral disc using a sin- 9365 adult twin pairs. Ann Med 1989;21:393–8.
[7] Marras WS, Lavender SA, Leurgans SE, et al. Biomechanical risk
gle pressure transducer mounted in a needle and navigated factors for occupationally related low back disorders. Ergonomics
across the disc, showing the annulus fibrosus and nucleus 1995;38:377–410.
pulposus function differently, especially in the presence of [8] Norman R, Wells R, Neumann P, et al. A comparison of peak vs cu-
disc degeneration [71,72]. Although we screened the speci- mulative physical work exposure risk factors for the reporting of
mens for disc height and other degenerative changes, we did low back pain in the automotive industry. Clin Biomech (Bristol,
Avon) 1998;13:561–73.
not investigate the disc tissue posttesting. Mean specimen [9] Punnett L, Wegman DH. Work-related musculoskeletal disorders:
age was 58.5 years; thus, age-related degenerative disc pro- the epidemiologic evidence and the debate. J Electromyogr Kinesiol
cesses could have taken place causing aberrant pressure 2004;14:13–23.
1588 J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589
[10] Le P, Solomonow M, Zhou BH, et al. Cyclic load magnitude is a risk [33] Pearcy MJ, Hindle RJ. Axial rotation of lumbar intervertebral joints
factor for a cumulative lower back disorder. J Occup Environ Med in forward flexion. Proc Inst Mech Eng H 1991;205:205–9.
2007;49:375–87. [34] Giles LG, Taylor JR. Lumbar spine structural changes associated
[11] Iatridis JC, Mente PL, Stokes IA, et al. Compression-induced with leg length inequality. Spine 1982;7:159–62.
changes in intervertebral disc properties in a rat tail model. Spine [35] Gurney B. Leg length discrepancy. Gait Posture 2002;15:195–206.
1999;24:996–1002. [36] Giles LG. Lumbosacral facetal ‘‘joint angles’’ associated with leg
[12] Lotz JC, Chin JR. Intervertebral disc cell death is dependent on the length inequality. Rheumatol Rehabil 1981;20:233–8.
magnitude and duration of spinal loading. Spine 2000;25:1477–83. [37] Giles LG, Taylor JR. The effect of postural scoliosis on lumbar
[13] Lotz JC, Colliou OK, Chin JR, et al. Compression-induced degener- apophyseal joints. Scand J Rheumatol 1984;13:209–20.
ation of the intervertebral disc: an in vivo mouse model and finite- [38] Buttermann GR, Beaubien BP. In vitro disc pressure profiles below
element study. Spine 1998;23:2493–506. scoliosis fusion constructs. Spine 2008;33:2134–42.
[14] Nakamura T, Iribe T, Asou Y, et al. Effects of compressive loading [39] Meir A, McNally DS, Fairbank JC, et al. The internal pressure and
on biomechanical properties of disc and peripheral tissue in a rat tail stress environment of the scoliotic intervertebral disc—a review.
model. Eur Spine J 2009;18:1595–603. Proc Inst Mech Eng H 2008;222:209–19.
[15] Ulrich JA, Liebenberg EC, Thuillier DU, Lotz JC. ISSLS prize win- [40] Meir AR, Fairbank JC, Jones DA, et al. High pressures and asym-
ner: repeated disc injury causes persistent inflammation. Spine metrical stresses in the scoliotic disc in the absence of muscle load-
2007;32:2812–9. ing. Scoliosis 2007;2:4.
[16] Videman T, Nurminen M, Troup JD. 1990 Volvo Award in clinical [41] Goel VK, Panjabi MM, Patwardhan AG, et al. Test protocols for
sciences. Lumbar spinal pathology in cadaveric material in relation evaluation of spinal implants. J Bone Joint Surg Am 2006;88(2
to history of back pain, occupation, and physical loading. Spine Suppl):103–9.
1990;15:728–40. [42] Goel VK, Wilder DG, Pope MH, Edwards WT. Biomechanical test-
[17] Brown KR, Pollintine P, Adams MA. Biomechanical implications of ing of the spine. Load-controlled versus displacement-controlled
degenerative joint disease in the apophyseal joints of human tho- analysis. Spine 1995;20:2354–7.
racic and lumbar vertebrae. Am J Phys Anthropol 2008;136:318–26. [43] Panjabi MM. Hybrid multidirectional test method to evaluate spinal
[18] Eubanks JD, Lee MJ, Cassinelli E, Ahn NU. Prevalence of lumbar adjacent-level effects. Clin Biomech (Bristol, Avon) 2007;22:
facet arthrosis and its relationship to age, sex, and race: an anatomic 257–65.
study of cadaveric specimens. Spine 2007;32:2058–62. [44] Wilke HJ, Wenger K, Claes L. Testing criteria for spinal implants:
[19] Tanno I, Murakami G, Oguma H, et al. Morphometry of the lumbar recommendations for the standardization of in vitro stability testing
zygapophyseal facet capsule and cartilage with special reference to of spinal implants. Eur Spine J 1998;7:148–54.
degenerative osteoarthritic changes: an anatomical study using fresh [45] Wilke HJ, Rohlmann A, Neller S, et al. Is it possible to simulate
cadavers of elderly Japanese and Korean subjects. J Orthop Sci physiologic loading conditions by applying pure moments? A com-
2004;9:468–77. parison of in vivo and in vitro load components in an internal fixator.
[20] Tischer T, Aktas T, Milz S, Putz RV. Detailed pathological changes Spine 2001;26:636–42.
of human lumbar facet joints L1-L5 in elderly individuals. Eur [46] Schmidt H, Heuer F, Claes L, Wilke HJ. The relation between
Spine J 2006;15:308–15. the instantaneous center of rotation and facet joint forces—a fi-
[21] Dunlop RB, Adams MA, Hutton WC. Disc space narrowing and the nite element analysis. Clin Biomech (Bristol, Avon) 2008;23:
lumbar facet joints. J Bone Joint Surg Br 1984;66:706–10. 270–8.
[22] Adams MA, McNally DS, Chinn H, Dolan P. Posture and the com- [47] Rousseau MA, Bradford DS, Hadi TM, et al. The instant axis of ro-
pressive strength of the lumbar spine. The clinical biomechanics tation influences facet forces at L5/S1 during flexion/extension and
award paper 1993. Clin Biomech 1994;9:5–14. lateral bending. Eur Spine J 2006;15:299–307.
[23] Adams MA, McMillan DW, Green TP, Dolan P. Sustained loading [48] Rousseau MA, Bradford DS, Bertagnoli R, et al. Disc arthroplasty
generates stress concentrations in lumbar intervertebral discs. Spine design influences intervertebral kinematics and facet forces. Spine
1996;21:434–8. J 2006;6:258–66.
[24] Schmidt H, Heuer F, Wilke HJ. Interaction between finite helical [49] Cholewicki J, Crisco JJ III, Oxland TR, et al. Effects of pos-
axes and facet joint forces under combined loading. Spine 2008; ture and structure on three-dimensional coupled rotations in
33:2741–8. the lumbar spine. A biomechanical analysis. Spine 1996;21:
[25] Schmidt H, Kettler A, Heuer F, et al. Intradiscal pressure, shear 2421–8.
strain, and fiber strain in the intervertebral disc under combined [50] Panjabi M, Yamamoto I, Oxland T, Crisco J. How does posture af-
loading. Spine 2007;32:748–55. fect coupling in the lumbar spine? Spine 1989;14:1002–11.
[26] Schmidt H, Kettler A, Rohlmann A, et al. The risk of disc prolapses [51] Yamamoto I, Panjabi MM, Crisco T, Oxland T. Three-dimensional
with complex loading in different degrees of disc degeneration—a fi- movements of the whole lumbar spine and lumbosacral joint. Spine
nite element analysis. Clin Biomech (Bristol, Avon) 2007;22: 1989;14:1256–60.
988–98. [52] Rao RD, Wang M, Singhal P, et al. Intradiscal pressure and kine-
[27] Nachemson A. Lumbar intradiscal pressure. Experimental studies matic behavior of lumbar spine after bilateral laminotomy and lam-
on post-mortem material. Acta Orthop Scand Suppl 1960;43:1–104. inectomy. Spine J 2002;2:320–6.
[28] Adams MA, Hutton WC. The mechanical function of the lumbar [53] Schmoelz W, Huber JF, Nydegger T, et al. Influence of a dynamic
apophyseal joints. Spine 1983;8:327–30. stabilisation system on load bearing of a bridged disc: an in vitro
[29] Adams MA, Hutton WC. The effect of posture on the lumbar spine. study of intradiscal pressure. Eur Spine J 2006;15:1276–85.
J Bone Joint Surg Br 1985;67:625–9. [54] Ingalhalikar AV, Reddy CG, Lim TH, et al. Effect of lumbar total
[30] Shirazi-Adl A, Drouin G. Load-bearing role of facets in a lumbar disc arthroplasty on the segmental motion and intradiscal pressure
segment under sagittal plane loadings. J Biomech 1987;20:601–13. at the adjacent level: an in vitro biomechanical study: presented at
[31] Dooris AP, Goel VK, Grosland NM, et al. Load-sharing between an- the 2008 Joint Spine Section Meeting Laboratory investigation.
terior and posterior elements in a lumbar motion segment implanted J Neurosurg Spine 2009;11:715–23.
with an artificial disc. Spine 2001;26:E122–9. [55] Steffen T, Baramki HG, Rubin R, et al. Lumbar intradiscal pressure
[32] Goel VK, Winterbottom JM, Weinstein JN, Kim YE. Load sharing measured in the anterior and posterolateral annular regions during
among spinal elements of a motion segment in extension and lateral asymmetrical loading. Clin Biomech (Bristol, Avon) 1998;13:
bending. J Biomech Eng 1987;109:291–7. 495–505.
J.M. Popovich et al. / The Spine Journal 13 (2013) 1581–1589 1589
[56] van Deursen DL, Snijders CJ, Kingma I, van Dieen JH. In vitro [64] Wiseman CM, Lindsey DP, Fredrick AD, Yerby SA. The effect of an
torsion-induced stress distribution changes in porcine intervertebral interspinous process implant on facet loading during extension.
discs. Spine 2001;26:2582–6. Spine 2005;30:903–7.
[57] van Deursen DL, Snijders CJ, van Dieen JH, et al. The effect of pas- [65] Niosi CA, Wilson DC, Zhu Q, et al. The effect of dynamic posterior
sive vertebral rotation on pressure in the nucleus pulposus. J Bio- stabilization on facet joint contact forces: an in vitro investigation.
mech 2001;34:405–8. Spine 2008;33:19–26.
[58] Yantzer BK, Freeman TB, Lee WE III, et al. Torsion-induced pres- [66] Zhu QA, Park YB, Sjovold SG, et al. Can extra-articular strains
sure distribution changes in human intervertebral discs: an in vitro be used to measure facet contact forces in the lumbar spine? an
study. Spine 2007;32:881–4. in-vitro biomechanical study. Proc Inst Mech Eng H 2008;222:
[59] Heuer F, Schmidt H, Wilke HJ. The relation between intervertebral 171–84.
disc bulging and annular fiber associated strains for simple and com- [67] Parent S, Labelle H, Skalli W, et al. Morphometric analysis of ana-
plex loading. J Biomech 2008;41:1086–94. tomic scoliotic specimens. Spine 2002;27:2305–11.
[60] Buttermann GR, Kahmann RD, Lewis JL, Bradford DS. An exper- [68] Ploumis A, Transfledt EE, Denis F. Degenerative lumbar scoliosis
imental method for measuring force on the spinal facet joint: de- associated with spinal stenosis. Spine J 2007;7:428–36.
scription and application of the method. J Biomech Eng 1991; [69] Pritchett JW, Bortel DT. Degenerative symptomatic lumbar scolio-
113:375–86. sis. Spine 1993;18:700–3.
[61] Hedman TP. A new transducer for facet force measurement in the [70] Shea KG, Ford T, Bloebaum RD, et al. A comparison of the micro-
lumbar spine: benchmark and in vitro test results. J Biomech architectural bone adaptations of the concave and convex thoracic
1992;25:69–80. spinal facets in idiopathic scoliosis. J Bone Joint Surg Am
[62] Schendel MJ, Wood KB, Buttermann GR, et al. Experimental mea- 2004;86-A:1000–6.
surement of ligament force, facet force, and segment motion in the [71] McNally DS, Adams MA. Internal intervertebral disc mechanics as
human lumbar spine. J Biomech 1993;26:427–38. revealed by stress profilometry. Spine 1992;17:66–73.
[63] Wilson DC, Niosi CA, Zhu QA, et al. Accuracy and repeatability of [72] Adams MA, McNally DS, Dolan P. ‘‘Stress’’ distributions inside in-
a new method for measuring facet loads in the lumbar spine. J Bio- tervertebral discs. The effects of age and degeneration. J Bone Joint
mech 2006;39:348–53. Surg Br 1996;78:965–72.