Dynamic cervical spine loading can produce facet capsule injury. Despite a large proportion of neck pain being attributable to the C2/C3 facet capsule, potential mechanisms are not understood. This study replicated low-speed frontal and rear-end traffic collisions in occiput-C3 human cadaveric cervical spine specimens and used kinematic and full-field strain analyses to assess injury. Specimens were loaded quasi-statically in flexion and extension before and after dynamic rotation of C3 at 100 deg/s. Global kinematics in the sagittal plane were tracked at 1 kHz, and C2/C3 facet capsule full-field strains were measured. Dynamic loading did not alter the kinematics from those during quasi-static (QS) loading, but maximum principal strain (MPS) and shear strain (SS) were significantly higher (p = 0.028) in dynamic flexion than for the same quasi-static conditions. The full-field strain analysis demonstrated that capsule strain was inhomogeneous, and that the peak MPS generally occurred in the anterior aspect and along the line of the C2/C3 facet joint. The strain magnitude in dynamic flexion continued to rise after the rotation of C3 had stopped, with a peak MPS of 12.52 ± 4.59% and a maximum SS of 5.34 ± 1.60%. The peak MPS in loading representative of rear-end collisions approached magnitudes previously shown to induce pain in vivo, whereas strain analysis using linear approaches across the facet joint was lower and may underestimate injury risk compared to full-field analysis. The time at which peak MPS occurred suggests that the deceleration following a collision is critical in relation to the production of injurious strains within the facet capsule.

References

1.
Siegmund
,
G. P.
,
Winkelstein
,
B. A.
,
Ivancic
,
P. C.
,
Svensson
,
M. Y.
, and
Vasavada
,
A.
,
2009
, “
The Anatomy and Biomechanics of Acute and Chronic Whiplash Injury
,”
Traffic Inj. Prev.
,
10
(
2
), pp.
101
112
.
2.
Jaumard
,
N. V.
,
Welch
,
W. C.
, and
Winkelstein
,
B. A.
,
2011
, “
Spinal Facet Joint Biomechanics and Mechanotransduction in Normal, Injury and Degenerative Conditions
,”
ASME J. Biomech. Eng.
,
133
(
7
), p.
071010
.
3.
Lord
,
S. M.
,
Barnsley
,
L.
,
Wallis
,
B. J.
, and
Bogduk
,
N.
,
1996
, “
Chronic Cervical Zygapophysial Joint Pain After Whiplash. A Placebo-Controlled Prevalence Study
,”
Spine
,
21
(
15
), pp.
1737
1744
; discussion 1744–1735.
4.
Quinlan
,
K. P.
,
Annest
,
J. L.
,
Myers
,
B.
,
Ryan
,
G.
, and
Hill
,
H.
,
2004
, “
Neck Strains and Sprains Among Motor Vehicle Occupants—United States, 2000
,”
Accid. Anal. Prev.
,
36
(
1
), pp.
21
27
.
5.
Zuby
,
D. S.
, and
Lund
,
A. K.
,
2010
, “
Preventing Minor Neck Injuries in Rear Crashes—Forty Years of Progress
,”
J. Occup. Environ. Med.
,
52
(
4
), pp.
428
433
.
6.
White
,
K.
,
Hudgins
,
T. H.
, and
Alleva
,
J. T.
,
2009
, “
Cervical Facet Mediated Pain
,”
Disease
,
55
(
12
), pp.
729
736
.
7.
Schofferman
,
J.
,
Bogduk
,
N.
, and
Slosar
,
P.
,
2007
, “
Chronic Whiplash and Whiplash-Associated Disorders: An Evidence-Based Approach
,”
J. Am. Acad. Orthop. Surg.
,
15
(
10
), pp.
596
606
.
8.
Radanov
,
B. P.
,
Sturzenegger
,
M.
, and
Di Stefano
,
G.
,
1995
, “
Long-Term Outcome After Whiplash Injury. A 2-Year Follow-Up Considering Features of Injury Mechanism and Somatic, Radiologic, and Psychosocial Findings
,”
Medicine
,
74
(
5
), pp.
281
297
.
9.
Gellhorn
,
A. C.
,
2011
, “
Cervical Facet-Mediated Pain
,”
Phys. Med. Rehab. Clin. N. Am.
,
22
(
3
), pp.
447
458
.
10.
Manchikanti
,
L.
,
Singh
,
V.
,
Rivera
,
J.
, and
Pampati
,
V.
,
2002
, “
Prevalence of Cervical Facet Joint Pain in Chronic Neck Pain
,”
Pain Physician
,
5
(
3
), pp.
243
249
.
11.
Berglund
,
A.
,
Alfredsson
,
L.
,
Cassidy
,
J. D.
,
Jensen
,
I.
, and
Nygren
,
Å.
,
2000
, “
The Association Between Exposure to a Rear-End Collision and Future Neck or Shoulder Pain: A Cohort Study
,”
J. Clin. Epidemiol.
,
53
(
11
), pp.
1089
1094
.
12.
Bogduk
,
N.
, and
Marsland
,
A.
,
1988
, “
The Cervical Zygapophysial Joints as a Source of Neck Pain
,”
Spine
,
13
(
6
), pp.
610
617
.
13.
Fukui
,
S.
,
Ohseto
,
K.
,
Shiotani
,
M.
,
Ohno
,
K.
,
Karasawa
,
H.
,
Naganuma
,
Y.
, and
Yuda
,
Y.
,
1996
, “
Referred Pain Distribution of the Cervical Zygapophyseal Joints and Cervical Dorsal Rami
,”
Pain
,
68
(
1
), pp.
79
83
.
14.
Barnsley
,
L.
,
Lord
,
S. M.
,
Wallis
,
B. J.
, and
Bogduk
,
N.
,
1995
, “
The Prevalence of Chronic Cervical Zygapophysial Joint Pain After Whiplash
,”
Spine
,
20
(
1
), pp.
20
25
; discussion 26.
15.
Chen
,
H. B.
,
Yang
,
K. H.
, and
Wang
,
Z. G.
,
2009
, “
Biomechanics of Whiplash Injury
,”
Chin. J. Traumatol.
,
12
(
5
), pp.
305
314
.
16.
Winkelstein
,
B. A.
,
2011
, “
How Can Animal Models Inform on the Transition to Chronic Symptoms in Whiplash?
,”
Spine
,
36
(
Suppl. 25
), pp.
S218
S225
.
17.
Chen
,
C.
,
Lu
,
Y.
,
Cavanaugh
,
J. M.
,
Kallakuri
,
S.
, and
Patwardhan
,
A.
,
2005
, “
Recording of Neural Activity From Goat Cervical Facet Joint Capsule Using Custom-Designed Miniature Electrodes
,”
Spine
,
30
(
12
), pp.
1367
1372
.
18.
Inami
,
S.
,
Shiga
,
T.
,
Tsujino
,
A.
,
Yabuki
,
T.
,
Okado
,
N.
, and
Ochiai
,
N.
,
2001
, “
Immunohistochemical Demonstration of Nerve Fibers in the Synovial Fold of the Human Cervical Facet Joint
,”
J. Orthop. Res.
,
19
(
4
), pp.
593
596
.
19.
McLain
,
R. F.
,
1994
, “
Mechanoreceptor Endings in Human Cervical Facet Joints
,”
Spine
,
19
(
5
), pp.
495
501
.
20.
Kras
,
J. V.
,
Tanaka
,
K.
,
Gilliland
,
T. M.
, and
Winkelstein
,
B. A.
,
2013
, “
An Anatomical and Immunohistochemical Characterization of Afferents Innervating the C6-C7 Facet Joint After Painful Joint Loading in the Rat
,”
Spine
,
38
(
6
), pp.
E325
E331
.
21.
Kras
,
J. V.
,
Weisshaar
,
C. L.
,
Pall
,
P. S.
, and
Winkelstein
,
B. A.
,
2015
, “
Pain From Intra-Articular NGF or Joint Injury in the Rat Requires Contributions From Peptidergic Joint Afferents
,”
Neurosci. Lett.
,
604
, pp.
193
198
.
22.
Cavanaugh
,
J. M.
,
Lu
,
Y.
,
Chen
,
C.
, and
Kallakuri
,
S.
,
2006
, “
Pain Generation in Lumbar and Cervical Facet Joints
,”
J. Bone Joint Surg. Am.
,
88
(
Suppl. 2
), pp.
63
67
.
23.
Kallakuri
,
S.
,
Singh
,
A.
,
Lu
,
Y.
,
Chen
,
C.
,
Patwardhan
,
A.
, and
Cavanaugh
,
J. M.
,
2008
, “
Tensile Stretching of Cervical Facet Joint Capsule and Related Axonal Changes
,”
Eur. Spine J.
,
17
(
4
), pp.
556
563
.
24.
Crosby
,
N. D.
,
Gilliland
,
T. M.
, and
Winkelstein
,
B. A.
,
2014
, “
Early Afferent Activity From the Facet Joint After Painful Trauma to Its Capsule Potentiates Neuronal Excitability and Glutamate Signaling in the Spinal Cord
,”
Pain
,
155
(
9
), pp.
1878
1887
.
25.
Pearson
,
A. M.
,
Ivancic
,
P. C.
,
Ito
,
S.
, and
Panjabi
,
M. M.
,
2004
, “
Facet Joint Kinematics and Injury Mechanisms During Simulated Whiplash
,”
Spine
,
29
(
4
), pp.
390
397
.
26.
Tominaga
,
Y.
,
Ndu
,
A. B.
,
Coe
,
M. P.
,
Valenson
,
A. J.
,
Ivancic
,
P. C.
,
Ito
,
S.
,
Rubin
,
W.
, and
Panjabi
,
M. M.
,
2006
, “
Neck Ligament Strength is Decreased Following Whiplash Trauma
,”
BMC Musculoskeletal Disord.
,
7
, p.
103
.
27.
Winkelstein
,
B. A.
,
McLendon
,
R. E.
,
Barbir
,
A.
, and
Myers
,
B. S.
,
2001
, “
An Anatomical Investigation of the Human Cervical Facet Capsule, Quantifying Muscle Insertion Area
,”
J. Anat.
,
198
(
Pt. 4
), pp.
455
461
.
28.
Cusick
,
J. F.
,
Pintar
,
F. A.
, and
Yoganandan
,
N.
,
2001
, “
Whiplash Syndrome: Kinematic Factors Influencing Pain Patterns
,”
Spine
,
26
(
11
), pp.
1252
1258
.
29.
Ivancic
,
P. C.
,
Panjabi
,
M. M.
,
Ito
,
S.
,
Cripton
,
P. A.
, and
Wang
,
J. L.
,
2005
, “
Biofidelic Whole Cervical Spine Model With Muscle Force Replication for Whiplash Simulation
,”
Eur. Spine J.
,
14
(
4
), pp.
346
355
.
30.
Dehner
,
C.
,
Elbel
,
M.
,
Schick
,
S.
,
Walz
,
F.
,
Hell
,
W.
, and
Kramer
,
M.
,
2007
, “
Risk of Injury of the Cervical Spine in Sled Tests in Female Volunteers
,”
Clin. Biomech.
,
22
(
6
), pp.
615
622
.
31.
Panjabi
,
M. M.
,
Cholewicki
,
J.
,
Nibu
,
K.
,
Grauer
,
J.
, and
Vahldiek
,
M.
,
1998
, “
Capsular Ligament Stretches During In Vitro Whiplash Simulations
,”
J. Spinal Disord.
,
11
(
3
), pp.
227
232
.
32.
Winkelstein
,
B. A.
,
Nightingale
,
R. W.
,
Richardson
,
W. J.
, and
Myers
,
B. S.
,
2000
, “
The Cervical Facet Capsule and Its Role in Whiplash Injury: A Biomechanical Investigation
,”
Spine
,
25
(
10
), pp.
1238
1246
.
33.
Anderst
,
W. J.
,
Donaldson
,
W. F.
, 3rd
,
Lee
,
J. Y.
, and
Kang
,
J. D.
,
2014
, “
In Vivo Cervical Facet Joint Capsule Deformation During Flexion–Extension
,”
Spine
,
39
(
8
), pp.
E514
E520
.
34.
Kras
,
J. V.
,
Dong
,
L.
, and
Winkelstein
,
B. A.
,
2014
, “
Increased Interleukin-1alpha and Prostaglandin E2 Expression in the Spinal Cord at 1 Day After Painful Facet Joint Injury: Evidence of Early Spinal Inflammation
,”
Spine
,
39
(
3
), pp.
207
212
.
35.
Dong
,
L.
,
Quindlen
,
J. C.
,
Lipschutz
,
D. E.
, and
Winkelstein
,
B. A.
,
2012
, “
Whiplash-Like Facet Joint Loading Initiates Glutamatergic Responses in the DRG and Spinal Cord Associated With Behavioral Hypersensitivity
,”
Brain Res.
,
1461
, pp.
51
63
.
36.
Bogduk
,
N.
, and
Yoganandan
,
N.
,
2001
, “
Biomechanics of the Cervical Spine—Part 3: Minor Injuries
,”
Clin. Biomech.
,
16
(
4
), pp.
267
275
.
37.
Luan
,
F.
,
Yang
,
K. H.
,
Deng
,
B.
,
Begeman
,
P. C.
,
Tashman
,
S.
, and
King
,
A. I.
,
2000
, “
Qualitative Analysis of Neck Kinematics During Low-Speed Rear-End Impact
,”
Clin. Biomech.
,
15
(
9
), pp.
649
657
.
38.
Yoganandan
,
N.
,
Pintar
,
F. A.
, and
Cusick
,
J. F.
,
2002
, “
Biomechanical Analyses of Whiplash Injuries Using an Experimental Model
,”
Accid. Anal. Prev.
,
34
(
5
), pp.
663
671
.
39.
Ivancic
,
P. C.
,
Panjabi
,
M. M.
, and
Ito
,
S.
,
2006
, “
Cervical Spine Loads and Intervertebral Motions During Whiplash
,”
Traffic Inj. Prev.
,
7
(
4
), pp.
389
399
.
40.
Siegmund
,
G. P.
,
Myers
,
B. S.
,
Davis
,
M. B.
,
Bohnet
,
H. F.
, and
Winkelstein
,
B. A.
,
2001
, “
Mechanical Evidence of Cervical Facet Capsule Injury During Whiplash: A Cadaveric Study Using Combined Shear, Compression, and Extension Loading
,”
Spine
,
26
(
19
), pp.
2095
2101
.
41.
Winkelstein
,
B. A.
,
Nightingale
,
R. W.
,
Richardson
,
W. J.
, and
Myers
,
B. S.
,
1999
, “
Cervical Facet Joint Mechanics: Its Application to Whiplash Injury
,”
Stapp Car Crash J.
,
43
, pp.
243
252
.
42.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2008
, “
Altered Collagen Fiber Kinematics Define the Onset of Localized Ligament Damage During Loading
,”
J. Appl. Physiol.
,
105
(
6
), pp.
1881
1888
.
43.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2011
, “
Detection of Altered Collagen Fiber Alignment in the Cervical Facet Capsule After Whiplash-Like Joint Retraction
,”
Ann. Biomed. Eng.
,
39
(
8
), pp.
2163
2173
.
44.
Lu
,
Y.
,
Chen
,
C.
,
Kallakuri
,
S.
,
Patwardhan
,
A.
, and
Cavanaugh
,
J. M.
,
2005
, “
Neural Response of Cervical Facet Joint Capsule to Stretch: A Study of Whiplash Pain Mechanism
,”
Stapp Car Crash J.
,
49
, pp.
49
65
.
45.
Yoganandan
,
N.
,
Pintar
,
F. A.
, and
Klienberger
,
M.
,
1998
, “
Cervical Spine Vertebral and Facet Joint Kinematics Under Whiplash
,”
ASME J. Biomech. Eng.
,
120
(
2
), pp.
305
307
.
46.
Panjabi
,
M. M.
,
Cholewicki
,
J.
,
Nibu
,
K.
,
Babat
,
L. B.
, and
Dvorak
,
J.
,
1998
, “
Simulation of Whiplash Trauma Using Whole Cervical Spine Specimens
,”
Spine
,
23
(
1
), pp.
17
24
.
47.
Descarreaux
,
M.
,
Blouin
,
J. S.
, and
Teasdale
,
N.
,
2003
, “
A Non-Invasive Technique for Measurement of Cervical Vertebral Angle: Report of a Preliminary Study
,”
Eur. Spine J.
,
12
(
3
), pp.
314
319
.
48.
Yoganandan
,
N.
,
Pintar
,
F. A.
,
Zhang
,
J.
, and
Baisden
,
J. L.
,
2009
, “
Physical Properties of the Human Head: Mass, Center of Gravity and Moment of Inertia
,”
J. Biomech.
,
42
(
9
), pp.
1177
1192
.
49.
Deng
,
B.
,
Begeman
,
P. C.
,
Yang
,
K. H.
,
Tashman
,
S.
, and
King
,
A. I.
,
2000
, “
Kinematics of Human Cadaver Cervical Spine During Low Speed Rear-End Impacts
,”
Stapp Car Crash J.
,
44
, pp.
171
188
.
50.
Bogduk
,
N.
, and
Mercer
,
S.
,
2000
, “
Biomechanics of the Cervical Spine—I: Normal Kinematics
,”
Clin. Biomech.
,
15
(
9
), pp.
633
648
.
51.
Anderst
,
W. J.
,
2015
, “
Bootstrap Prediction Bands for Cervical Spine Intervertebral Kinematics During In Vivo Three-Dimensional Head Movements
,”
J. Biomech.
,
48
(
7
), pp.
1270
1276
.
52.
Bostrom
,
O.
,
Fredriksson
,
R.
,
Haland
,
Y.
,
Jakobsson
,
L.
,
Krafft
,
M.
,
Lovsund
,
P.
,
Muser
,
M. H.
, and
Svensson
,
M. Y.
,
2000
, “
Comparison of Car Seats in Low Speed Rear-End Impacts Using the BioRID Dummy and the New Neck Injury Criterion (NIC)
,”
Accid. Anal. Prev.
,
32
(
2
), pp.
321
328
.
53.
Dehner
,
C.
,
Schick
,
S.
,
Kraus
,
M.
,
Hell
,
W.
, and
Kramer
,
M.
,
2013
, “
Muscle Activity Influence on the Kinematics of the Cervical Spine in Rear-End Sled Tests in Female Volunteers
,”
Traffic Inj. Prev.
,
14
(
4
), pp.
369
377
.
54.
Grauer
,
J. N.
,
Panjabi
,
M. M.
,
Cholewicki
,
J.
,
Nibu
,
K.
, and
Dvorak
,
J.
,
1997
, “
Whiplash Produces an S-Shaped Curvature of the Neck With Hyperextension at Lower Levels
,”
Spine
,
22
(
21
), pp.
2489
2494
.
55.
Stemper
,
B. D.
,
Yoganandan
,
N.
,
Gennarelli
,
T. A.
, and
Pintar
,
F. A.
,
2005
, “
Localized Cervical Facet Joint Kinematics Under Physiological and Whiplash Loading
,”
J. Neurosurg
,
3
(
6
), pp.
471
476
.
56.
Ghole
,
S. A.
,
Ivancic
,
P. C.
,
Tominaga
,
Y.
,
Gimenez
,
S. E.
, and
Panjabi
,
M. M.
,
2004
, “
Incremental and Single Trauma Produce Equivalent Subfailure Soft Tissue Injury of the Cervical Spine
,”
Clin. Biomech.
,
19
(
8
), pp.
784
789
.
57.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2009
, “
Vector Correlation Technique for Pixel-Wise Detection of Collagen Fiber Realignment During Injurious Tensile Loading
,”
J. Biomed. Opt.
,
14
(
5
), p.
054010
.
58.
Zhang
,
S.
,
Cao
,
X.
,
Stablow
,
A. M.
,
Shenoy
,
V. B.
, and
Winkelstein
,
B. A.
,
2016
, “
Tissue Strain Reorganizes Collagen With a Switch-Like Response That Regulates Neuronal ERK Phosphorylation In Vitro: Implications for Ligamentous Injury and Mechanotransduction
,”
ASME J. Biomech. Eng.
,
138
(
2
), p.
021013
.
59.
Lu
,
Y.
,
Chen
,
C.
,
Kallakuri
,
S.
,
Patwardhan
,
A.
, and
Cavanaugh
,
J. M.
,
2005
, “
Neurophysiological and Biomechanical Characterization of Goat Cervical Facet Joint Capsules
,”
J. Orthop. Res.
,
23
(
4
), pp.
779
787
.
60.
Lu
,
Y.
,
Chen
,
C.
,
Kallakuri
,
S.
,
Patwardhan
,
A.
, and
Cavanaugh
,
J. M.
,
2005
, “
Development of an In Vivo Method to Investigate Biomechanical and Neurophysiological Properties of Spine Facet Joint Capsules
,”
Eur. Spine J.
,
14
(
6
), pp.
565
572
.
61.
Avramov
,
A. I.
,
Cavanaugh
,
J. M.
,
Ozaktay
,
C. A.
,
Getchell
,
T. V.
, and
King
,
A. I.
,
1992
, “
The Effects of Controlled Mechanical Loading on Group-II, III, and IV Afferent Units From the Lumbar Facet Joint and Surrounding Tissue. An In Vitro Study
,”
J. Bone Joint Surg.
,
74
(
10
), pp.
1464
1471
.
62.
Lee
,
D. J.
, and
Winkelstein
,
B. A.
,
2012
, “
The Failure Response of the Human Cervical Facet Capsular Ligament During Facet Joint Retraction
,”
J. Biomech.
,
45
(
14
), pp.
2325
2329
.
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