The effects of degeneration and surgery on cervical spine mechanics are commonly evaluated through in vitro testing and finite element models derived from these tests. The objectives of the current study were to estimate the load applied to the C2 vertebra during in vivo functional flexion-extension and to evaluate the effects of anterior cervical arthrodesis on spine kinetics. Spine and head kinematics from 16 subjects (six arthrodesis patients and ten asymptomatic controls) were determined during functional flexion-extension using dynamic stereo X-ray and conventional reflective markers. Subject-specific inverse dynamics models, including three flexor muscles and four extensor muscles attached to the skull, estimated the force applied to C2. Total force applied to C2 was not significantly different between arthrodesis and control groups at any 10 deg increment of head flexion-extension (all p values ≥ 0.937). Forces applied to C2 were smallest in the neutral position, increased slowly with flexion, and increased rapidly with extension. Muscle moment arms changed significantly during flexion-extension, and were dependent upon the direction of head motion. The results suggest that in vitro protocols and finite element models that apply constant loads to C2 do not accurately represent in vivo cervical spine kinetics.

References

References
1.
Patil
,
P. G.
,
Turner
,
D. A.
, and
Pietrobon
,
R.
,
2005
, “
National Trends in Surgical Procedures for Degenerative Cervical Spine Disease: 1990–2000
,”
Neurosurgery
,
57
(
4
), pp.
753
758
.10.1227/01.NEU.0000175729.79119.1d
2.
Fielding
,
J. W.
,
1964
, “
Normal and Selected Abnormal Motion of the Cervical Spine From the Second Cervical Vertebra to the Seventh Cervical Vertebra Based on Cineroentgenography
,”
J. Bone Joint Surg.
,
46
, pp.
1779
1781
.
3.
Dunsker
,
S. B.
,
Colley
,
D. P.
, and
Mayfield
,
F. H.
,
1978
, “
Kinematics of the Cervical Spine
,”
Clin. Neurosurg.
,
25
, pp.
174
183
.
4.
Baba
,
H.
,
Furusawa
,
N.
,
Imura
,
S.
,
Kawahara
,
N.
,
Tsuchiya
,
H.
, and
Tomita
,
K.
,
1993
, “
Late Radiographic Findings After Anterior Cervical Fusion for Spondylotic Myeloradiculopathy
,”
Spine
,
18
(
15
), pp.
2167
2173
.10.1097/00007632-199311000-00004
5.
Matsunaga
,
S.
,
Kabayama
,
S.
,
Yamamoto
,
T.
,
Yone
,
K.
,
Sakou
,
T.
, and
Nakanishi
,
K.
,
1999
, “
Strain on Intervertebral Discs After Anterior Cervical Decompression and Fusion
,”
Spine
,
24
(
7
), pp.
670
675
.10.1097/00007632-199904010-00011
6.
Schwab
,
J. S.
,
Diangelo
,
D. J.
, and
Foley
,
K. T.
,
2006
, “
Motion Compensation Associated With Single-Level Cervical Fusion: Where Does the Lost Motion Go?
,”
Spine
,
31
(
21
), pp.
2439
2448
.10.1097/01.brs.0000239125.54761.23
7.
Hunter
,
L. Y.
,
Braunstein
,
E. M.
, and
Bailey
,
R. W.
,
1980
, “
Radiographic Changes Following Anterior Cervical Fusion
,”
Spine
,
5
(
5
), pp.
399
401
.10.1097/00007632-198009000-00002
8.
Gore
,
D. R.
, and
Sepic
,
S. B.
,
1998
, “
Anterior Discectomy and Fusion for Painful Cervical Disc Disease. A Report of 50 Patients With an Average Follow-Up of 21 Years
,”
Spine
,
23
(
19
), pp.
2047
2051
.10.1097/00007632-199810010-00002
9.
Hilibrand
,
A. S.
,
Carlson
,
G. D.
,
Palumbo
,
M. A.
,
Jones
,
P. K.
, and
Bohlman
,
H. H.
,
1999
, “
Radiculopathy and Myelopathy at Segments Adjacent to the Site of a Previous Anterior Cervical Arthrodesis
,”
J. Bone Joint Surg.
,
81
(
4
), pp.
519
528
.
10.
Goffin
,
J.
,
Geusens
,
E.
,
Vantomme
,
N.
,
Quintens
,
E.
,
Waerzeggers
,
Y.
,
Depreitere
,
B.
,
Van Calenbergh
,
F.
, and
van Loon
,
J.
,
2004
, “
Long-Term Follow-Up After Interbody Fusion of the Cervical Spine
,”
J. Spinal Disord. Tech.
,
17
(
2
), pp.
79
85
.10.1097/00024720-200404000-00001
11.
Ishihara
,
H.
,
Kanamori
,
M.
,
Kawaguchi
,
Y.
,
Nakamura
,
H.
, and
Kimura
,
T.
,
2004
, “
Adjacent Segment Disease After Anterior Cervical Interbody Fusion
,”
Spine J.
,
4
(
6
), pp.
624
628
.10.1016/j.spinee.2004.04.011
12.
Kulkarni
,
V.
,
Rajshekhar
,
V.
, and
Raghuram
,
L.
,
2004
, “
Accelerated Spondylotic Changes Adjacent to the Fused Segment Following Central Cervical Corpectomy: Magnetic Resonance Imaging Study Evidence
,”
J. Neurosurg.
,
100
(
1 Suppl. Spine
), pp.
2
6
.10.3171/jns.2004.100.1.0002
13.
Bohlman
,
H. H.
,
Emery
,
S. E.
,
Goodfellow
,
D. B.
, and
Jones
,
P. K.
,
1993
, “
Robinson Anterior Cervical Discectomy and Arthrodesis for Cervical Radiculopathy. Long-Term Follow-Up of One Hundred and Twenty-Two Patients
,”
J. Bone Joint Surg.
,
75
(
9
), pp.
1298
1307
.
14.
Gore
,
D. R.
, and
Sepic
,
S. B.
,
1984
, “
Anterior Cervical Fusion for Degenerated or Protruded Discs. A Review of One Hundred Forty-Six Patients
,”
Spine
,
9
(
7
), pp.
667
671
.10.1097/00007632-198410000-00002
15.
Watters
,
W. C.
, 3rd
, and
Levinthal
,
R.
,
1994
, “
Anterior Cervical Discectomy With and Without Fusion. Results, Complications, and Long-Term Follow-Up
,”
Spine
,
19
(
20
), pp.
2343
2347
.
16.
Hilibrand
,
A. S.
,
Yoo
,
J. U.
,
Carlson
,
G. D.
, and
Bohlman
,
H. H.
,
1997
, “
The Success of Anterior Cervical Arthrodesis Adjacent to a Previous Fusion
,”
Spine
,
22
(
14
), pp.
1574
1579
.10.1097/00007632-199707150-00009
17.
Sasso
,
R. C.
,
Anderson
,
P. A.
,
Riew
,
K. D.
, and
Heller
,
J. G.
,
2011
, “
Results of Cervical Arthroplasty Compared With Anterior Discectomy and Fusion: Four-Year Clinical Outcomes in a Prospective, Randomized Controlled Trial
,”
J. Bone Joint Surg.
,
93
(
18
), pp.
1684
1692
.10.2106/JBJS.J.00476
18.
Jawahar
,
A.
,
Cavanaugh
,
D. A.
,
Kerr
,
E. J.
, 3rd
,
Birdsong
,
E. M.
, and
Nunley
,
P. D.
,
2010
, “
Total Disc Arthroplasty Does Not Affect the Incidence of Adjacent Segment Degeneration in Cervical Spine: Results of 93 Patients in Three Prospective Randomized Clinical Trials
,”
Spine J.
,
10
(
12
), pp.
1043
1048
.10.1016/j.spinee.2010.08.014
19.
McAfee
,
P. C.
,
Reah
,
C.
,
Gilder
,
K.
,
Eisermann
,
L.
, and
Cunningham
,
B.
,
2011
, “
A Meta-Analysis of Comparative Outcomes Following Cervical Arthroplasty or Anterior Cervical Fusion: Results From Four Prospective Multi-Center Randomized Clinical Trials and Up to 1226 Patients
,”
Spine
, May 15,
37
(
11
), pp.
943
952
.
20.
Kelly
,
M. P.
,
Mok
,
J. M.
,
Frisch
,
R. F.
, and
Tay
,
B. K.
,
2011
, “
Adjacent Segment Motion After Anterior Cervical Discectomy and Fusion Versus Prodisc-c Cervical Total Disk Arthroplasty: Analysis From a Randomized, Controlled Trial
,”
Spine
,
36
(
15
), pp.
1171
1179
.10.1097/BRS.0b013e3181ec5c7d
21.
DiAngelo
,
D. J.
,
Roberston
,
J. T.
,
Metcalf
,
N. H.
,
McVay
,
B. J.
, and
Davis
,
R. C.
,
2003
, “
Biomechanical Testing of an Artificial Cervical Joint and an Anterior Cervical Plate
,”
J. Spinal Disord. Tech.
,
16
(
4
), pp.
314
323
.10.1097/00024720-200308000-00002
22.
Brodke
,
D. S.
,
Klimo
,
P.
, Jr.
,
Bachus
,
K. N.
,
Braun
,
J. T.
, and
Dailey
,
A. T.
,
2006
, “
Anterior Cervical Fixation: Analysis of Load-Sharing and Stability With Use of Static and Dynamic Plates
,”
J. Bone Joint Surg.
,
88
(
7
), pp.
1566
1573
.10.2106/JBJS.E.00305
23.
Davies
,
M. A.
,
Bryant
,
S. C.
,
Larsen
,
S. P.
,
Murrey
,
D. B.
,
Nussman
,
D. S.
,
Laxer
,
E. B.
, and
Darden
,
B. V.
,
2006
, “
Comparison of Cervical Disk Implants and Cervical Disk Fusion Treatments in Human Cadaveric Models
,”
J. Biomech. Eng.
,
128
(
4
), pp.
481
486
.10.1115/1.2205373
24.
Dmitriev
,
A. E.
,
Cunningham
,
B. W.
,
Hu
,
N.
,
Sell
,
G.
,
Vigna
,
F.
, and
McAfee
,
P. C.
,
2005
, “
Adjacent Level Intradiscal Pressure and Segmental Kinematics Following a Cervical Total Disc Arthroplasty: An In Vitro Human Cadaveric Model
,”
Spine
,
30
(
10
), pp.
1165
1172
.10.1097/01.brs.0000162441.23824.95
25.
Eck
,
J. C.
,
Humphreys
,
S. C.
,
Lim
,
T. H.
,
Jeong
,
S. T.
,
Kim
,
J. G.
,
Hodges
,
S. D.
, and
An
,
H. S.
,
2002
, “
Biomechanical Study on the Effect of Cervical Spine Fusion on Adjacent-Level Intradiscal Pressure and Segmental Motion
,”
Spine
,
27
(
22
), pp.
2431
2434
.10.1097/00007632-200211150-00003
26.
Brolin
,
K.
, and
Halldin
,
P.
,
2004
, “
Development of a Finite Element Model of the Upper Cervical Spine and a Parameter Study of Ligament Characteristics
,”
Spine
,
29
(
4
), pp.
376
385
.10.1097/01.BRS.0000090820.99182.2D
27.
del Palomar
,
A. P.
,
Calvo
,
B.
, and
Doblare
,
M.
,
2008
, “
An Accurate Finite Element Model of the Cervical Spine Under Quasi-Static Loading
,”
J. Biomech.
,
41
(
3
), pp.
523
531
.10.1016/j.jbiomech.2007.10.012
28.
Kallemeyn
,
N.
,
Gandhi
,
A.
,
Kode
,
S.
,
Shivanna
,
K.
,
Smucker
,
J.
, and
Grosland
,
N.
,
2010
, “
Validation of a C2-C7 Cervical Spine Finite Element Model Using Specimen-Specific Flexibility Data
,”
Med. Eng. Phys.
,
32
(
5
), pp.
482
489
.10.1016/j.medengphy.2010.03.001
29.
Maiman
,
D. J.
,
Kumaresan
,
S.
,
Yoganandan
,
N.
, and
Pintar
,
F. A.
,
1999
, “
Biomechanical Effect of Anterior Cervical Spine Fusion on Adjacent Segments
,”
Biomed. Mater. Eng.
,
9
(
1
), pp.
27
38
.
30.
Womack
,
W.
,
Leahy
,
P. D.
,
Patel
,
V. V.
, and
Puttlitz
,
C. M.
,
2011
, “
Finite Element Modeling of Kinematic and Load Transmission Alterations Due to Cervical Intervertebral Disc Replacement
,”
Spine
, Aug 1,
36
(
17
), pp.
E1126
1133
.
31.
Panjabi
,
M. M.
,
Cholewicki
,
J.
,
Nibu
,
K.
,
Grauer
,
J.
,
Babat
,
L. B.
, and
Dvorak
,
J.
,
1998
, “
Critical Load of the Human Cervical Spine: An In Vitro Experimental Study
,”
Clin. Biomechan.
,
13
(
1
), pp.
11
17
.10.1016/S0268-0033(97)00057-0
32.
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
.10.1016/j.jbiomech.2009.03.029
33.
Panjabi
,
M. M.
,
Crisco
,
J. J.
,
Vasavada
,
A.
,
Oda
,
T.
,
Cholewicki
,
J.
,
Nibu
,
K.
, and
Shin
,
E.
,
2001
, “
Mechanical Properties of the Human Cervical Spine As Shown by Three-Dimensional Load-Displacement Curves
,”
Spine
,
26
(
24
), pp.
2692
2700
.10.1097/00007632-200112150-00012
34.
DiAngelo
,
D. J.
, and
Foley
,
K. T.
,
2004
, “
An Improved Biomechanical Testing Protocol for Evaluating Spinal Arthroplasty and Motion Preservation Devices in a Multilevel Human Cadaveric Cervical Model
,”
Neurosurg. Focus
,
17
(
3
), p.
E4
.
35.
Patwardhan
,
A. G.
,
Havey
,
R. M.
,
Ghanayem
,
A. J.
,
Diener
,
H.
,
Meade
,
K. P.
,
Dunlap
,
B.
, and
Hodges
,
S. D.
,
2000
, “
Load-Carrying Capacity of the Human Cervical Spine in Compression is Increased Under a Follower Load
,”
Spine
,
25
(
12
), pp.
1548
1554
.10.1097/00007632-200006150-00015
36.
Patwardhan
,
A. G.
,
Havey
,
R. M.
,
Meade
,
K. P.
,
Lee
,
B.
, and
Dunlap
,
B.
,
1999
, “
A Follower Load Increases the Load-Carrying Capacity of the Lumbar Spine in Compression
,”
Spine
,
24
(
10
), pp.
1003
1009
.10.1097/00007632-199905150-00014
37.
Seacrist
,
T.
,
Arbogast
,
K. B.
,
Maltese
,
M. R.
,
Garcia-Espana
,
J. F.
,
Lopez-Valdes
,
F. J.
,
Kent
,
R. W.
,
Tanji
,
H.
,
Higuchi
,
K.
, and
Balasubramanian
,
S.
,
2012
, “
Kinetics of the Cervical Spine n Pediatric and Adult Volunteers During Low Speed Frontal Impacts
,”
J. Biomech.
,
45
(
1
), pp.
99
106
.10.1016/j.jbiomech.2011.09.016
38.
Pintar
,
F. A.
,
Yoganandan
,
N.
, and
Baisden
,
J.
,
2005
, “
Characterizing Occipital Condyle Loads Under High-Speed Head Rotation
,”
Stapp Car Crash J.
,
49
, pp.
33
47
.
39.
Pintar
,
F. A.
,
Yoganandan
,
N.
, and
Maiman
,
D. J.
,
2010
, “
Lower Cervical Spine Loading in Frontal Sled Tests Using Inverse Dynamics: Potential Applications for Lower Neck Injury Criteria
,”
Stapp Car Crash J.
,
54
, pp.
133
166
.
40.
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
.10.1080/15389580600789127
41.
Moroney
,
S. P.
,
Schultz
,
A. B.
, and
Miller
,
J. A.
,
1988
, “
Analysis and Measurement of Neck Loads
,”
J. Orthop. Res.
,
6
(
5
), pp.
713
720
.10.1002/jor.1100060514
42.
Siegmund
,
G. P.
,
Blouin
,
J. S.
,
Brault
,
J. R.
,
Hedenstierna
,
S.
, and
Inglis
,
J. T.
,
2007
, “
Electromyography of Superficial and Deep Neck Muscles During Isometric, Voluntary, and Reflex Contractions
,”
J. Biomech. Eng.
,
129
(
1
), pp.
66
77
.10.1115/1.2401185
43.
Thorhauer
,
E.
,
Miyawaki
,
M.
,
Illingworth
,
K.
,
Holmes
,
A.
, and
Anderst
,
W.
,
2010
, “
Accuracy of Bone and Cartilage Models Obtained From CT and MRI
,”
American Society of Biomechanics
,
Providence, RI
.
44.
University of Iowa, downloaded
03/29/2012, https://mri.radiology.uiowa.edu/visible_human_datasets.html
45.
Anderst
,
W. J.
,
Baillargeon
,
E.
,
Donaldson
,
W. F.
, 3rd
,
Lee
,
J. Y.
, and
Kang
,
J. D.
,
2011
, “
Validation of a Noninvasive Technique to Precisely Measure In Vivo Three-Dimensional Cervical Spine Movement
,”
Spine
,
36
(
6
), pp.
E393
E400
.10.1097/BRS.0b013e31820b7e2f
46.
Bey
,
M. J.
,
Zauel
,
R.
,
Brock
,
S. K.
, and
Tashman
,
S.
,
2006
, “
Validation of a New Model-Based Tracking Technique for Measuring Three-Dimensional, In Vivo Glenohumeral Joint Kinematics
,”
J. Biomech. Eng.
,
128
(
4
), pp.
604
609
.10.1115/1.2206199
47.
Martin
,
D. E.
,
Greco
,
N. J.
,
Klatt
,
B. A.
,
Wright
,
V. J.
,
Anderst
,
W. J.
, and
Tashman
,
S.
,
2011
, “
Model-Based Tracking of the Hip: Implications for Novel Analyses of Hip Pathology
,”
J. Arthroplasty
,
26
(
1
), pp.
88
97
.10.1016/j.arth.2009.12.004
48.
Anderst
,
W.
,
Zauel
,
R.
,
Bishop
,
J.
,
Demps
,
E.
, and
Tashman
,
S.
,
2009
, “
Validation of Three-Dimensional Model-Based Tibio-Femoral Tracking During Running
,”
Med. Eng. Phys.
,
31
(
1
), pp.
10
16
.10.1016/j.medengphy.2008.03.003
49.
Winter
,
D. A.
,
2009
,
Biomechanics and Motor Control of Human Movement
,
4th ed.
,
Wiley
,
Hoboken, NJ
.
50.
Chancey
,
V. C.
,
Nightingale
,
R. W.
,
Van Ee
,
C. A.
,
Knaub
,
K. E.
, and
Myers
,
B. S.
,
2003
, “
Improved Estimation of Human Neck Tensile Tolerance: Reducing the Range of Reported Tolerance Using Anthropometrically Correct Muscles and Optimized Physiologic Initial Conditions
,”
Stapp Car Crash J.
,
47
, pp.
135
153
.
51.
Ackland
,
D. C.
,
Merritt
,
J. S.
, and
Pandy
,
M. G.
,
2011
, “
Moment Arms of the Human Neck Muscles in Flexion, Bending and Rotation
,”
J. Biomech.
,
44
(
3
), pp.
475
486
.10.1016/j.jbiomech.2010.09.036
52.
Oi
,
N.
,
Pandy
,
M. G.
,
Myers
,
B. S.
,
Nightingale
,
R. W.
, and
Chancey
,
V. C.
,
2004
, “
Variation of Neck Muscle Strength Along the Human Cervical Spine
,”
Stapp Car Crash J.
,
48
, pp.
397
417
.
53.
Andrade
,
A. V.
,
Gomes
,
P. F.
, and
Teixeira-Salmela
,
L. F.
,
2007
, “
Cervical Spine Alignment and Hyoid Bone Positioning With Temporomandibular Disorders
,”
J. Oral Rehabil.
,
34
(
10
), pp.
767
772
.10.1111/j.1365-2842.2006.01698.x
54.
Zheng
,
L.
,
Jahn
,
J.
, and
Vasavada
,
A. N.
,
2012
, “
Sagittal Plane Kinematics of the Adult Hyoid Bone
,”
J. Biomech.
,
45
(
3
), pp.
531
536
.10.1016/j.jbiomech.2011.11.040
55.
Benjamini
,
Y.
, and
Hochberg
,
Y.
,
1995
, “
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
,”
J. R. Stat. Soc. Ser. B
,
57
(
1
), pp.
289
300
.
56.
Anderst
,
W. J.
,
Donaldson
,
W. F.
,
Lee
,
J. Y.
, and
Kang
,
J. D.
,
2013
, “
Cervical Spine Intervertebral Kinematics With Respect to the Head are Different During Flexion and Extension Motions
,”
J Biomech.
, (in press).10.1016/j.jbiomech.2013.03.004
57.
Hattori
,
S.
,
Oda
,
H.
, and
Kawai
,
U.
,
1981
, “
Cervical Intradiscal Pressure in Movements and Traction of the Cervical Spine
,”
Z. Orthop.
,
119
, pp.
568
569
.
58.
Vasavada
,
A. N.
,
Li
,
S.
, and
Delp
,
S. L.
,
1998
, “
Influence of Muscle Morphometry and Moment Arms on the Moment-Generating Capacity of Human Neck Muscles
,”
Spine
,
23
(
4
), pp.
412
422
.10.1097/00007632-199802150-00002
You do not currently have access to this content.