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Research Papers

Upper Cervical Spine Loading Simulating a Dynamic Low-Speed Collision Significantly Increases the Risk of Pain Compared to Quasi-Static Loading With Equivalent Neck Kinematics

[+] Author and Article Information
Timothy P. Holsgrove

Department of Bioengineering,
School of Engineering and Applied Science,
University of Pennsylvania,
210 South 33rd Street,
Room 240 Skirkanich Hall,
Philadelphia, PA 19104
e-mail: thols@seas.upenn.edu

Nicolas V. Jaumard

Department of Neurosurgery,
Pennsylvania Hospital,
University of Pennsylvania,
Washington Square West Building,
235 South 8th Street,
Philadelphia, PA 19106
e-mail: njaumard@gmail.com

Nina Zhu

Department of Bioengineering,
School of Engineering and Applied Science,
University of Pennsylvania,
210 South 33rd Street,
Room 240 Skirkanich Hall,
Philadelphia, PA 19104
e-mail: nzhu@seas.upenn.edu

Nicholas S. Stiansen

Department of Bioengineering,
School of Engineering and Applied Science,
University of Pennsylvania,
210 South 33rd Street,
Room 240 Skirkanich Hall,
Philadelphia, PA 19104
e-mail: nsti@seas.upenn.edu

William C. Welch

Department of Neurosurgery,
Pennsylvania Hospital,
University of Pennsylvania,
Washington Square West Building,
235 South 8th Street,
Philadelphia, PA 19106
e-mail: william.welch@uphs.upenn.edu

Beth A. Winkelstein

Department of Bioengineering,
School of Engineering
and Applied Science,
University of Pennsylvania,
210 South 33rd Street,
Room 240 Skirkanich Hall,
Philadelphia, PA 19104;
Department of Neurosurgery,
Pennsylvania Hospital,
University of Pennsylvania,
Washington Square West Building,
235 South 8th Street,
Philadelphia, PA 19106
e-mail: winkelst@seas.upenn.edu

1Corresponding author.

Manuscript received February 10, 2016; final manuscript received September 8, 2016; published online November 3, 2016. Assoc. Editor: Brian D. Stemper.

J Biomech Eng 138(12), 121006 (Nov 03, 2016) (10 pages) Paper No: BIO-16-1053; doi: 10.1115/1.4034707 History: Received February 10, 2016; Revised September 08, 2016

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.

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References

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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
White, K. , Hudgins, T. H. , and Alleva, J. T. , 2009, “ Cervical Facet Mediated Pain,” Disease, 55(12), pp. 729–736.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Gellhorn, A. C. , 2011, “ Cervical Facet-Mediated Pain,” Phys. Med. Rehab. Clin. N. Am., 22(3), pp. 447–458. [CrossRef]
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. [PubMed]
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. [CrossRef] [PubMed]
Bogduk, N. , and Marsland, A. , 1988, “ The Cervical Zygapophysial Joints as a Source of Neck Pain,” Spine, 13(6), pp. 610–617. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Chen, H. B. , Yang, K. H. , and Wang, Z. G. , 2009, “ Biomechanics of Whiplash Injury,” Chin. J. Traumatol., 12(5), pp. 305–314. [PubMed]
Winkelstein, B. A. , 2011, “ How Can Animal Models Inform on the Transition to Chronic Symptoms in Whiplash?,” Spine, 36(Suppl. 25), pp. S218–S225. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
McLain, R. F. , 1994, “ Mechanoreceptor Endings in Human Cervical Facet Joints,” Spine, 19(5), pp. 495–501. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
Cusick, J. F. , Pintar, F. A. , and Yoganandan, N. , 2001, “ Whiplash Syndrome: Kinematic Factors Influencing Pain Patterns,” Spine, 26(11), pp. 1252–1258. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Bogduk, N. , and Yoganandan, N. , 2001, “ Biomechanics of the Cervical Spine—Part 3: Minor Injuries,” Clin. Biomech., 16(4), pp. 267–275. [CrossRef]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
Bogduk, N. , and Mercer, S. , 2000, “ Biomechanics of the Cervical Spine—I: Normal Kinematics,” Clin. Biomech., 15(9), pp. 633–648. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]

Figures

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Fig. 1

Global view (a) of the occiput (Occ)-to-C3 specimen, with tracking markers at each level. The Occ was fixed to a phantom head. The C3 vertebra was rigidly fixed to the cradle, which was actuated for dynamic tests, with all other levels unconstrained in the sagittal and axial planes. The C2/C3 facet capsule was imaged (b) with two cameras, from which 2D facet kinematics were measured (c), and 3D reconstructions were used to measure the maximum principal strain (MPS) (d) and shear strain.

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Fig. 2

Mean (±95% confidence intervals (CI)) quasi-static kinematics (flexion positive) at the Occ/C1 (a), C1/C2 (b), and C2/C3 (c) levels with respect to the global ROM predynamic (Pre-D) and postdynamic (Post-D) loadings

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Fig. 3

Mean (±95% CI) rotation angle (flexion positive) at Occ/C1 (a), C1/C2 (b), and C2/C3 (c) levels during dynamic flexion, and dynamic extension (d)–(f) applied at 100 deg/s to the C3 level from 20 to 81 ms

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Fig. 4

Mean (±95% CI) peak MPS ((a) and (b)) and peak SS ((c) and (d)) of the C2/C3 facet capsule during dynamic actuation of the C3 applied at 100 deg/s from 20 to 8 ms in flexion ((a) and (c)) and extension ((b) and (d))

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Fig. 5

Mean (±95% CI) peak MPS (a) and mean MPS (b) on the C2/C3 facet capsule during flexion and extension at 100 deg/s compared to quasi-static loading. An asterisk (*) denotes a significant difference (p < 0.05).

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Fig. 6

Representative full-field strain for specimen 1 ((a) and (b)) and specimen 4 ((c) and (d)). The peak MPS during dynamic flexion ((a) and (c)) and the MPS at equivalent C2/C3 rotation during quasi-static testing ((b) and (d)) are shown. The variable MPS across the facet capsule was determined; the arrows show the MPS direction within each element.

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Fig. 7

Mean rotation angle (flexion positive) during dynamic actuation applied at 100 deg/s to the C3 level from 20 to 81 ms in either flexion (a) or extension (b). The visual representations above the plots show the shape of the spine at 0, 40, 81, 120, and 150 ms.

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