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Research Papers

Failure Properties and Damage of Cervical Spine Ligaments, Experiments and Modeling

[+] Author and Article Information
Ana Trajkovski

Faculty of Mechanical Engineering,
University of Ljubljana,
Aškerčeva cesta 6,
Ljubljana 1000, Slovenia
e-mail: ana.trajkovski@fs.uni-lj.si

Senad Omerović

Faculty of Mechanical Engineering,
University of Ljubljana,
Aškerčeva cesta 6,
Ljubljana 1000, Slovenia
e-mail: senad.omerovic@fs.uni-lj.si

Marija Hribernik

Medical Faculty,
University of Ljubljana,
Vrazov trg 2,
Ljubljana 1000, Slovenia
e-mail: marjana.hribernik@mf.uni-lj.si

Ivan Prebil

Faculty of Mechanical Engineering,
University of Ljubljana,
Aškerčeva cesta 6,
Ljubljana 1000, Slovenia
e-mail: ivan.prebil@fs.uni-lj.si

Contributed by the Bioengineering Division of ASME for publication in the Journal of Biomechanical Engineering. Manuscript received March 25, 2013; final manuscript received December 30, 2013; accepted manuscript posted January 6, 2014; published online February 13, 2014. Assoc. Editor: Brian D. Stemper.

J Biomech Eng 136(3), 031002 (Feb 13, 2014) (9 pages) Paper No: BIO-13-1156; doi: 10.1115/1.4026424 History: Received March 25, 2013; Revised December 30, 2013; Accepted January 06, 2014

Cervical spine ligaments have an important role in providing spinal cord stability and restricting excessive movements. Therefore, it is of great importance to study the mechanical properties and model the response of these ligaments. The aim of this study is to characterize the aging effects on the failure properties and model the damage of three cervical spine ligaments: the anterior and the posterior longitudinal ligament and the ligamentum flavum. A total of 46 samples of human cadaveric ligaments removed within 24–48 h after death have been tested. Uniaxial tension tests along the fiber direction were performed in physiological conditions. The results showed that aging decreased the failure properties of all three ligaments (failure load, failure elongation). Furthermore, the reported nonlinear response of cervical ligaments has been modeled with a combination of the previously reported hyperelastic and damage model. The model predicted a nonlinear response and damage region. The model fittings are in agreement with the experimental data and the quality of agreement is represented with the values of the coefficient of determination close to 1.

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References

Troyer, K. L. and Puttlitz, C. M., 2011, “Human Cervical Spine Ligaments Exhibit Fully Nonlinear Viscoelastic Behavior,” Acta Biomater., 7(2), pp. 700–709. [CrossRef] [PubMed]
Bass, C. R., Planchak, C. J., Salzar, R. S., Lucas, S. R., Rafaels, K. A., Shender, B. S., and Paskoff, G., 2007, “The Temperature-Dependent Viscoelasticity of Porcine Lumbar Spine Ligaments,” Spine, 32(16), pp. E436–E442. [CrossRef] [PubMed]
Yoganandan, N., Kumaresan, S., and Pintar, F. A., 2001, “Biomechanics of the Cervical Spine—Part 2: Cervical Spine Soft Tissue Responses and Biomechanical Modeling,” Clin. Biomech. (Bristol, Avon), 16(1), pp. 1–27. [CrossRef] [PubMed]
Quapp, K. M. and Weiss, J. A., 1998, “Material Characterization of Human Medial Collateral Ligament,” ASME J. Biomech. Eng., 120(6), pp. 757–763. [CrossRef]
White, A. A. and Panjabi, M. M., 1990, “Clinical Biomechanics of the Spine,” J.B. Lippincott Philadelphia.
Ivancic, P. C., Pearson, A. M., Panjabi, M. M., and Ito, S., 2004, “Injury of the Anterior Longitudinal Ligament During Whiplash Simulation,” Eur. Spine J., 13(1), pp. 61–68. [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]
Panjabi, M. M., Cholewicki, J., Nibu, K., Grauer, J. N., Babat, L. B., and Dvorak, J., 1998, “Mechanism of Whiplash Injury,” Clin. Biomech. (Bristol, Avon), 13(4-5), pp. 239–249. [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 Musculoskelet. Disord., 7, p. 103. [CrossRef] [PubMed]
Panjabi, M. M., Pearson, A. M., Ito, S., Ivancic, P. C., Gimenez, S. E., and Tominaga, Y., 2004, “Cervical Spine Ligament Injury During Simulated Frontal Impact,” Spine, 29(21), pp. 2395–2403. [CrossRef] [PubMed]
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]
Pearson, A. M., Panjabi, M. M., Ivancic, P. C., Ito, S., Cunningham, B. W., Rubin, W., and Gimenez, S. E., 2005, “Frontal Impact Causes Ligamentous Cervical Spine Injury,” Spine, 30(16), pp. 1852–1858. [CrossRef] [PubMed]
Cusick, J. F. and Yoganandan, N., 2002, “Biomechanics of the Cervical Spine 4: Major Injuries,” Clin. Biomech., 17(1), pp. 1–20. [CrossRef]
Ito, S., Ivancic, P. C., Panjabi, M. M., and Cunningham, B. W., 2004, “Soft Tissue Injury Threshold During Simulated Whiplash: A Biomechanical Investigation,” Spine, 29(9), pp. 979–987. [CrossRef] [PubMed]
Cappon, H.v.R. M., Wismans, J., Hell, W., Lang, D., and Svensson, M., 2003, “Whiplash Injuries, Not Only a Problem in Rear-End Impact,” 18th International Technical Conference on the Enhanced Safety of Vehicles.
Omerovic, S., Stojanović, A., Krašna, S., and Prebil, I., 2012, “Finite Element Model of Human Head, Neck and Torso for Adult and 3 y.o. Child,” J. Biomech., 45(1), p. S205. [CrossRef]
Curatolo, M., Bogduk, N., Ivancic, P. C., McLean, S. A., Siegmund, G. P., and Winkelstein, B. A., 2011, “The Role of Tissue Damage in Whiplash-Associated Disorders: Discussion Paper 1,” Spine, 36(25), pp. S309–S315. [CrossRef] [PubMed]
Chazal, J., Tanguy, A., Bourges, M., Gaurel, G., Escande, G., Guillot, M., and Vanneuville, G., 1985, “Biomechanical Properties of Spinal Ligaments and a Histological Study of the Supraspinal Ligament in Traction,” J. Biomech., 18(3), pp. 167–176. [CrossRef] [PubMed]
Myklebust, J. B., Pintar, F., Yoganandan, N., Cusick, J. F., Maiman, D., Myers, T. J., and Sances, A., Jr., 1988, “Tensile Strength of Spinal Ligaments,” Spine, 13(5), pp. 526–531. [CrossRef] [PubMed]
Yoganandan, N., Kumaresan, S., and Pintar, F. A., 2000, “Geometric and Mechanical Properties of Human Cervical Spine Ligaments,” ASME J. Biomech. Eng., 122(6), pp. 623–629. [CrossRef]
Butler, J., Pintar, F., Yoganandan, N., Myklebust, J., Reinartz, J., and Sances, A., Jr., 1988, “Static and Dynamic Comparison of Human Cervical Spinal Ligaments,” Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 672, pp. 679–680.
Yoganandan, N., Pintar, F., Butler, J., Reinartz, J., Sances, A., Jr., and Larson, S. J., 1989, “Dynamic Response of Human Cervical Spine Ligaments,” Spine, 14(10), pp. 1102–1110. [CrossRef] [PubMed]
Przybylski, G. J., Carlin, G. J., Patel, P. R., and Woo, S. L., 1996, “Human Anterior and Posterior Cervical Longitudinal Ligaments Possess Similar Tensile Properties,” J. Orthop. Res., 14(6), pp. 1005–1008. [CrossRef] [PubMed]
Ivancic, P. C., Coe, M. P., Ndu, A. B., Tominaga, Y., Carlson, E. J., Rubin, W., Dipl-Ing, F. H., and Panjabi, M. M., 2007, “Dynamic Mechanical Properties of Intact Human Cervical Spine Ligaments,” Spine J., 7(6), pp. 659–665. [CrossRef] [PubMed]
Shim, V. P. W., Liu, J. F., and Lee, V. S., 2006, “A Technique for Dynamic Tensile Testing of Human Cervical Spine Ligaments,” Exp. Mech., 46(1), pp. 77–89. [CrossRef]
Bass, C. R., Lucas, S. R., Salzar, R. S., Oyen, M. L., Planchak, C., Shender, B. S., and Paskoff, G., 2007, “Failure Properties of Cervical Spinal Ligaments Under Fast Strain Rate Deformations,” Spine, 32(1), pp. E7–E13. [CrossRef] [PubMed]
Lucas, S. R., Bass, C. R., Salzar, R. S., Oyen, M. L., Planchak, C., Ziemba, A., Shender, B. S., and Paskoff, G., 2008, “Viscoelastic Properties of the Cervical Spinal Ligaments Under Fast Strain-Rate Deformations,” Acta Biomater., 4(1), pp. 117–125. [CrossRef] [PubMed]
Mattucci, S. F. E., Moulton, J. A., Chandrashekar, N., and Cronin, D. S., 2012, “Strain Rate Dependent Properties of Younger Human Cervical Spine Ligaments,” J. Mech. Behav. Biomed. Mater., 10, pp. 216–226. [CrossRef] [PubMed]
Neumann, P., Ekstrom, L. A., Keller, T. S., Perry, L., and Hansson, T. H., 1994, “Aging, Vertebral Density, and Disc Degeneration Alter the Tensile Stress-Strain Characteristics of the Human Anterior Longitudinal Ligament,” J. Orthop. Res., 12(1), pp. 103–112. [CrossRef] [PubMed]
Nachemson, A. L. and Evans, J. H., 1968, “Some Mechanical Properties of the Third Human Lumbar Interlaminar Ligament (Ligamentum Flavum),” J. Biomech., 1(3), pp. 211–220. [CrossRef] [PubMed]
Moon, D. K., Woo, S. L., Takakura, Y., Gabriel, M. T., and Abramowitch, S. D., 2006, “The Effects of Refreezing on the Viscoelastic and Tensile Properties of Ligaments,” J. Biomech., 39(6), pp. 1153–1157. [CrossRef] [PubMed]
Cheng, S., Clarke, E. C., and Bilston, L. E., 2009, “The Effects of Preconditioning Strain on Measured Tissue Properties,” J. Biomech., 42(9), pp. 1360–1362. [CrossRef] [PubMed]
Quinn, K. P. and Winkelstein, B. A., 2011, “Preconditioning is Correlated With Altered Collagen Fiber Alignment in Ligament,” ASME J. Biomech. Eng., 133(6), p. 064506. [CrossRef]
Natali, A., Pavan, P., Carniel, E., Dario, P., and Izzo, I., 2008, “Characterization of Soft Tissue Mechanics With Aging,” IEEE Eng. Med. Biol. Mag., 27(4), pp. 15–22. [CrossRef] [PubMed]
Holzapfel, G. A. and Simo, J. C., 1996, “A New Viscoelastic Constitutive Model for Continuous Media at Finite Thermomechanical Changes,” Int. J. Solids Struct., 33(20–22), pp. 3019–3034. [CrossRef]
Natali, A. N., Pavan, P. G., Carniel, E. L., Lucisano, M. E., and Taglialavoro, G., 2005, “Anisotropic Elasto-Damage Constitutive Model for the Biomechanical Analysis of Tendons,” Med. Eng. Phys., 27(3), pp. 209–214. [CrossRef] [PubMed]
Weiss, J., Gardiner, J., Ellis, B., Lujan, T., and Phatak, N., 2005, “Three-Dimensional Finite Element Modeling of Ligaments: Technical Aspects,” Med. Eng. Phys., 27(10), pp. 845–861. [CrossRef] [PubMed]
Weiss, J. A. and Gardiner, J. C., 2001, “Computational Modeling of Ligament Mechanics,” Crit. Rev. Biomed. Eng., 29(3), pp. 303–371. [CrossRef] [PubMed]
Guo, Z. and De Vita, R., 2009, “Probabilistic Constitutive Law for Damage in Ligaments,” Med. Eng. Phys., 31(9), pp. 1104–1109. [CrossRef] [PubMed]
Calvo, B., Peña, E., Martinez, M. A., and Doblaré, M., 2007, “An Uncoupled Directional Damage Model for Fibred Biological Soft Tissues. Formulation and Computational Aspects,” Int. J. Numer. Methods Eng., 69(10), pp. 2036–2057. [CrossRef]
Pena, E., 2011, “Damage Functions of the Internal Variables for Soft Biological Fibred Tissues,” Mech. Res. Commun., 38(8), pp. 610–615. [CrossRef]
Calvo, B., Peña, E., Martins, P., Mascarenhas, T., Doblaré, M., Natal Jorge, R. M., and Ferreira, A., 2009, “On Modelling Damage Process in Vaginal Tissue,” J. Biomech., 42(5), pp. 642–651. [CrossRef] [PubMed]
Peña, E., Calvo, B., Martínez, M. A., and Doblaré, M., 2008, “On Finite-Strain Damage of Viscoelastic-Fibred Materials. Application to Soft Biological Tissues,” Int. J. Numer. Methods Eng, 74(7), pp. 1198–1218. [CrossRef]
Yong-Hing, K., Reilly, J., and Kirkaldy-Willis, W. H., 1976, “The Ligamentum Flavum,” Spine, 1(4), pp. 226–234. [CrossRef]
Provenzano, P. P., Heisey, D., Hayashi, K., Lakes, R., and Vanderby, R., Jr., 2002, “Subfailure Damage in Ligament: A Structural and Cellular Evaluation,” J. Appl. Physiol., 92(1), pp. 362–371. [PubMed]
Putz, R., 1992, “The Detailed Functional Anatomy of the Ligaments of the Vertebral Column,” Ann. Anat., 174(1), pp. 40–47. [CrossRef] [PubMed]
Stojanović, A., Omerović, S., Krašna, S. and Prebil, I., 2012, “Mechanical Properties of Human Cervical Spine Ligaments: Age Related Changes,” J. Biomech., 45(1), p. S611. [CrossRef]
Holzapfel, G. A., 2005, “Similarities Between Soft Biological Tissues and Rubberlike Materials,” Proceedings of the 4th European Conference on Constitutive Models for Rubber (ECCMR 2005), pp. 607–617.
Hayashi, K., Yabuki, T., Kurokawa, T., Seki, H., Hogaki, M., and Minoura, S., 1977, “The Anterior and the Posterior Longitudinal Ligaments of the Lower Cervical Spine,” J. Anat., 124(3), pp. 633–636. [PubMed]
Holzapfel, G. A., 2000, “Nonlinear Solid Mechanics: A Continuum Approach for Engineering,” Wiley, Chichester, New York.
Weiss, J. A., 1991, “A Constitutive Model and Finite Element Representation for Transversely Isotropic Soft Tissues,” Ph.D. thesis, The University of Utah, Salt Lake City, UT.
Ogden, R. W., 1997, “Non-Linear Elastic Deformations,” Dover Publications, Mineola, N.Y.
Galle, B., Ouyang, H., Shi, R., and Nauman, E., 2010, “A Transversely Isotropic Constitutive Model of Excised Guinea Pig Spinal Cord White Matter,” J. Biomech., 43(14), pp. 2839–2843. [CrossRef] [PubMed]
Weiss, J. A., Gardiner, J. C., and Bonifasi-Lista, C., 2002, “Ligament Material Behavior is Nonlinear, Viscoelastic and Rate-Independent Under Shear Loading,” J. Biomech., 35(7), pp. 943–950. [CrossRef] [PubMed]
Simo, J. C., 1987, “On a Fully Three-Dimensional Finite-Strain Viscoelastic Damage Model: Formulation and Computational Aspects,” Comput. Methods Appl. Mech. Eng., 60(2), pp. 153–173. [CrossRef]
Calvo, B., Ramírez, A., Alonso, A., Grasa, J., Soteras, F., Osta, R., and Muñoz, M. J., 2010, “Passive Nonlinear Elastic Behaviour of Skeletal Muscle: Experimental Results and Model Formulation,” J. Biomech., 43(2), pp. 318–325. [CrossRef] [PubMed]
Nakagawa, H., Mikawa, Y., and Watanabe, R., 1994, “Elastin in the Human Posterior Longitudinal Ligament and Spinal Dura. A Histologic and Biochemical Study,” Spine, 19(19), pp. 2164–2169. [CrossRef] [PubMed]
Yahia, L. H., Garzon, S., Strykowski, H., and Rivard, C. H., 1990, “Ultrastructure of the Human Interspinous Ligament and Ligamentum Flavum. A Preliminary Study,” Spine, 15(4), pp. 262–268. [CrossRef] [PubMed]
Panjabi, M. M. and Courtney, T. W., 2001, “High-Speed Subfailure Stretch of Rabbit Anterior Cruciate Ligament: Changes in Elastic, Failure and Viscoelastic Characteristics,” Clin. Biomech., 16(4), pp. 334–340. [CrossRef]
Cowin, S. C. and Doty, S. B., 2007, Tissue Mechanics, Springer, New York.
Arnoux, P. J., Chabrand, P., Jean, M., and Bonnoit, J., 2002, “A Visco-Hyperelastic Model With Damage for the Knee Ligaments Under Dynamic Constraints,” Comput. Methods Biomech. Biomed. Eng., 5(2), pp. 167–174. [CrossRef]
Peña, E., 2011, “A Rate Dependent Directional Damage Model for Fibred Materials: Application to Soft Biological Tissues,” Comput. Mech., 48(4), pp. 407–420. [CrossRef]
Martins, P., Pena, E., Jorge, R. M., Santos, A., Santos, L., Mascarenhas, T., and Calvo, B., 2012, “Mechanical Characterization and Constitutive Modelling of the Damage Process in Rectus Sheath,” J. Mech. Behav. Biomed. Mater., 8, pp. 111–122. [CrossRef] [PubMed]
Standring, S., 2008, Gray's Anatomy: The Anatomical Basis of Clinical Practice, Churchill Livingstone Elsevier, New York.
Quinn, K. P. and Winkelstein, B. A., 2007, “Cervical Facet Capsular Ligament Yield Defines the Threshold for Injury and Persistent Joint-Mediated Neck Pain,” J. Biomech., 40(10), pp. 2299–2306. [CrossRef] [PubMed]
Gardiner, J. C. and Weiss, J. A., 2003, “Subject-Specific Finite Element Analysis of the Human Medial Collateral Ligament During Valgus Knee Loading,” J. Orthop. Res., 21(6), pp. 1098–1106. [CrossRef] [PubMed]
Heuer, F., Wolfram, U., Schmidt, H., and Wilke, H. J., 2008, “A Method to Obtain Surface Strains of Soft Tissues Using a Laser Scanning Device,” J. Biomech., 41(11), pp. 2402–2410. [CrossRef] [PubMed]
Tong, J., Cohnert, T., Regitnig, P., and Holzapfel, G. A., 2011, “Effects of Age on the Elastic Properties of the Intraluminal Thrombus and the Thrombus-Covered Wall in Abdominal Aortic Aneurysms: Biaxial Extension Behaviour and Material Modelling,” Eur. J. Vasc. Endovasc. Surg., 42(2), pp. 207–219. [CrossRef] [PubMed]

Figures

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Fig. 1

(a) PLL column, and (b) bone-ligament-bone units

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Fig. 2

Potted bone-ligament-bone units

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Fig. 3

Better fixture of the PLL

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Fig. 4

(a) Test rig, and (b) fixed sample in chamber of the test rig

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Fig. 5

Scheme of ligament length definition

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Fig. 6

Ligament load-displacement curves

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Fig. 7

Age related changes of (a) ultimate load, (b) ultimate displacement, (c) stiffness, (d) ultimate stress, (e) ultimate strain, and (f) modulus for ALL, PLL, and LF

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Fig. 8

Fitted experimental data for several samples

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