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Research Papers

Subject-Specific Inverse Dynamics of the Head and Cervical Spine During in Vivo Dynamic Flexion-Extension

[+] Author and Article Information
William J. Anderst

e-mail: anderst@pitt.edu

James D. Kang

Department of Orthopaedic Surgery,
University of Pittsburgh,
Pittsburgh, PA 15203

1Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received October 5, 2012; final manuscript received January 7, 2013; accepted manuscript posted January 29, 2013; published online May 9, 2013. Assoc. Editor: Yener N. Yeni.

J Biomech Eng 135(6), 061007 (May 09, 2013) (8 pages) Paper No: BIO-12-1464; doi: 10.1115/1.4023524 History: Received October 05, 2012; Revised January 07, 2013; Accepted January 29, 2013

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.

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References

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. [CrossRef] [PubMed]
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.
Dunsker, S. B., Colley, D. P., and Mayfield, F. H., 1978, “Kinematics of the Cervical Spine,” Clin. Neurosurg., 25, pp. 174–183. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Hunter, L. Y., Braunstein, E. M., and Bailey, R. W., 1980, “Radiographic Changes Following Anterior Cervical Fusion,” Spine, 5(5), pp. 399–401. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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.
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. [CrossRef]
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]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [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]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
University of Iowa, downloaded 03/29/2012, https://mri.radiology.uiowa.edu/visible_human_datasets.html
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Winter, D. A., 2009, Biomechanics and Motor Control of Human Movement, 4th ed., Wiley, Hoboken, NJ.
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. [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
Zheng, L., Jahn, J., and Vasavada, A. N., 2012, “Sagittal Plane Kinematics of the Adult Hyoid Bone,” J. Biomech., 45(3), pp. 531–536. [CrossRef] [PubMed]
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.
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). [CrossRef]
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.
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. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

The biplane X-ray system. X-ray tubes (left) directed X-rays through the subject to image intensifiers (right). 2.5 ms X-ray pulses (70 kV, 160 mA) were generated by cardiac cine-angiography generators at a rate of 30 Hz and radiographic images were collected by high-speed cameras synchronized to the X-ray pulses.

Grahic Jump Location
Fig. 2

The skull and cervical spine model for a representative subject in an (a) extended orientation, (b) the neutral position, and (c) a flexed orientation. Reflective markers (green) determined skull and torso position, while vertebral positions were determined from model-based tracking of biplane radiographs. Muscle forces (red vectors) were generated by flexor muscles (yellow spheres identify insertions) when the head was in an extended orientation and by extensor muscles (magenta spheres identify insertions) when the head was in a flexed orientation. The orange vector represents the weight of head. The teal vector represents the total force applied by the head to C2. Anatomic coordinate systems were generated within each vertebra (only C7 is shown for clarity).

Grahic Jump Location
Fig. 3

The total force made by the skull on C2 while the head moved in flexion (blue diamonds) and extension (red squares). Data points indicate the average of all subjects (asymptomatic plus arthrodesis). Error bars indicate intersubject variability (the 95% confidence interval of the mean), however, within-subject comparisons were performed to identify differences between flexion and extension movement directions. P values comparing flexion versus extension, adjusted for multiple comparisons, are provided for each 10 deg increment of head flexion-extension. The horizontal axis indicates head flexion-extension angle relative to the neutral position.

Grahic Jump Location
Fig. 4

The perpendicular distance from the midpoint of the C2 superior facets to the line of action of the flexor muscles during the flexion (solid lines) and extension (dashed lines) motion. Data points indicate the average of all subjects (asymptomatic plus arthrodesis). Positive values indicate a flexion moment, negative values indicate an extension moment. Error bars indicate intersubject variability (the 95% confidence interval of the mean), however, within-subject comparisons were performed to identify differences between flexion and extension movement directions and to identify differences among 10 deg increments of head extension. Each flexion value was significantly greater than the corresponding extension value for longus capitus (LGC) (all p ≤ 0.003) and infrahyoid (all p ≤ 0.002) but only at 0 deg, 10 deg, and 20 deg of extension for the SCM moment arm (p ≤ 0.033). For the SCM and LGC, the average moment arm (flexion + extension movement direction) significantly decreased at each 10 deg increment of head extension from neutral to 40 deg of extension (all p ≤ 0.020 and all p ≤ 0.001, respectively). The infrahyoid moment arm significantly increased each 10 deg of head flexion-extension from neutral to 40 deg of extension (all p ≤ 0.001).

Grahic Jump Location
Fig. 5

The perpendicular distance from the midpoint of the C2 superior facets to the line of action of the extensor muscles during the flexion (solid lines) and extension (dashed lines) motion. Data points indicate the average of all subjects (asymptomatic plus arthrodesis). Negative values indicate an extension moment. Error bars indicate intersubject variability (the 95% confidence interval of the mean), however, within-subject comparisons were performed to identify differences between flexion and extension movement directions and to identify differences among 10 deg increments of head extension. Each extension value was significantly greater than the corresponding flexion value for the trapezius (Trap) (all p ≤ 0.001), semispinalis (SSP) (all p ≤ 0.001), and splenius capitis (SPL) (all p ≤ 0.002). Each extension value was significantly greater than the corresponding flexion value for the rectus capitis posterior major (RCP) from 10 deg to 40 deg of head flexion (all p ≤ 0.022). The Trap and SPL average moment arms (flexion + extension movement direction) were significantly different at each 10 deg increment of head flexion (all p ≤ 0.016 and all p ≤ 0.038, respectively), while the SSP average moment arm decreased significantly at each 10 deg increment of head flexion from neutral to 30 deg flexion (all p ≤ 0.015). The rectus capitis posterior major moment arm significantly decreased from 30 deg to 40 deg of head flexion (p = 0.019).

Grahic Jump Location
Fig. 6

Sensitivity of the model to changes in the sternocleidomastoid attachment site on the skull. The vertical axis is the percent change in force applied to C2, relative to the force determined using the original attachment site. The attachment site was repositioned 8, 4, 2, or 1 mm anterior (+) or posterior (−) to the original attachment site. Changing the SSP and infrahyoid attachment sites yielded changes in the C2 force curves that were smaller in magnitude but similar in pattern.

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