Research Papers

Peak Stress in the Annulus Fibrosus Under Cyclic Biaxial Tensile Loading

[+] Author and Article Information
Chad E. Gooyers

Giffin Koerth Forensic Engineering and Science,
40 University Avenue, Suite 800,
Toronto, ON M5J 1T1, Canada
e-mail: cgooyers@giffinkoerth.com

Jack P. Callaghan

Canada Research Chair in Spine Biomechanics
and Injury Prevention,
Department of Kinesiology,
Faculty of Applied Health Sciences,
University of Waterloo,
Waterloo, ON N2L 3G1, Canada
e-mail: jack.callaghan@uwaterloo.ca

1Corresponding author.

Manuscript received July 20, 2015; final manuscript received March 8, 2016; published online March 29, 2016. Assoc. Editor: James C. Iatridis.

J Biomech Eng 138(5), 051006 (Mar 29, 2016) (7 pages) Paper No: BIO-15-1365; doi: 10.1115/1.4032996 History: Received July 20, 2015; Revised March 08, 2016

Numerous in vitro studies have examined the initiation and propagation of fatigue injury pathways in the annulus fibrosus (AF) using isolated motion segments; however, the cycle-varying changes to the AF under cyclic biaxial tensile loading conditions have yet to be examined. Therefore, the primary objective of this study was to characterize the cycle-varying changes in peak tensile stress in multilayer AF tissue samples within a range of physiologically relevant loading conditions at subacute magnitudes of tissue stretch up to 100 loading cycles. A secondary aim was to examine whether the stress-relaxation response would be different across loading axes (axial and circumferential) and whether this response would vary across regions of the intervertebral disk (IVD) (anterior and posterior–lateral). The results from the study demonstrate that several significant interactions emerged between independent factors that were examined in the study. Specifically, a three-way interaction between the radial location, magnitude of peak tissue stretch, and cycle rate (p = 0.0053) emerged. Significant two-way interactions between the magnitude of tissue stretch and cycle number (p < 0.0001) and the magnitude of tissue stretch and loading axis (p < 0.0001) were also observed. These findings are discussed in the context of known mechanisms for structural damage, which have been linked to fatigue loading in the IVD (e.g., cleft formation, radial tearing, increased neutral zone, disk bulging, and loss of intradiscal pressure).

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Bruehlmann, S. B. , Rattner, J. B. , Matyas, J. R. , and Duncan, N. A. , 2002, “ Regional Variations in the Cellular Matrix of the Annulus Fibrosus of the Intervertebral Disc,” J. Anat., 201(2), pp. 159–171. [CrossRef] [PubMed]
Marchand, F. , and Ahmed, A. M. , 1990, “ Investigation of the Laminate Structure of the Lumbar Disc Annulus,” Spine, 15(5), pp. 402–410. [CrossRef] [PubMed]
Inoue, H. , 1981, “ Three-Dimensional Architecture of Lumbar Intervertebral Discs,” Spine, 6(2), pp. 139–146. [CrossRef] [PubMed]
McNally, D. S. , and Adams, M. A. , 1992, “ Internal Intervertebral Disc Mechanics as Revealed by Stress Profilometry,” Spine, 17(1), pp. 66–73. [CrossRef] [PubMed]
Green, T. P. , Adams, M. A. , and Dolan, P. , 1993, “ Tensile Properties of the Annulus Fibrosus—II. Ultimate Tensile Strength and Fatigue Life,” Eur. Spine J., 2(4), pp. 209–214. [CrossRef] [PubMed]
Iatridis, J. C. , and Gwynn, I. , 2004, “ Mechanisms for Mechanical Damage in the Intervertebral Disc Annulus Fibrosus,” J. Biomech., 37(8), pp. 1165–1175. [CrossRef] [PubMed]
Bayliss, M. T. , Johnstone, B. , and O'Brien, J. P. , 1988, “ Proteoglycan Synthesis in the Human Intervertebral Disc. Variation With Age, Region and Pathology,” Spine, 13(9), pp. 972–981. [CrossRef] [PubMed]
Ishihara, H. , McNally, D. S. , Urban, J. P. G. , and Hall, A. C. , 1996, “ Effects of Hydrostatic Pressure on Matrix Synthesis in Difference Regions of the Intervertebral Disk,” J. Appl. Physiol., 80(3), pp. 839–846. [PubMed]
Adams, M. A. , and Hutton, W. C. , 1982, “ Prolapsed Intervertebral Disc,” Spine, 7(3), pp. 184–191. [CrossRef] [PubMed]
Callaghan, J. P. , and McGill, S. M. , 2001, “ Intervertebral Disc Herniation: Studies on a Porcine Model Exposed to Highly Repetitive Flexion/Extension Motion With Compressive Force,” Clin. Biomech., 16(1), pp. 28–37. [CrossRef]
Simunic, D. I. , Robertson, P. A. , and Broom, N. D. , 2004, “ Mechanically Induced Disruption of Healthy Bovine Intervertebral Disc,” Spine, 29(9), pp. 972–978. [CrossRef] [PubMed]
Aultman, C. D. , Scannell, J. , and McGill, S. M. , 2005, “ The Direction of Progressive Herniation in Porcine Spine Motion Segments is Influenced by the Orientation of the Bending Axis,” Clin. Biomech., 20(2), pp. 126–129. [CrossRef]
Tampier, C. , Drake, J. D. M. , Callaghan, J. P. , and McGill, S. M. , 2007, “ Progressive Disc Herniation: An Investigation of the Mechanism Using Radiologic, Histochemical, and Microscopic Dissection Techniques on a Porcine Mode,” Spine, 32(25), pp. 2869–2874. [CrossRef] [PubMed]
Parkinson, R. J. , and Callaghan, J. P. , 2009, “ The Role of Dynamic Flexion in Spine Injury Is Altered by Increasing Dynamic Load Magnitude,” Clin. Biomech., 24(2), pp. 148–154. [CrossRef]
Yates, J. P. , Giangregorio, L. , and McGill, S. M. , 2010, “ The Influence of Intervertebral Disc Shape on the Pathway of Posterior/Posterolateral Partial Herniation,” Spine, 35(7), pp. 734–739. [CrossRef] [PubMed]
Gooyers, C. E. , McMillan, E. M. , Noguchi, M. , Quadrilatero, J. , and Callaghan, J. P. , 2015, “ Characterizing the Combined Effects of Force, Repetition and Posture on Injury Pathways and Micro-Structural Damage in Isolated Functional Spinal Units From Sub-Acute-Failure Magnitude of Cyclic Compressive Loading,” Clin. Biomech., 30(9), pp. 953–959. [CrossRef]
Skaggs, D. L. , Weidenbaum, M. , Iatridis, J. C. , and Ratcliffe, A. , 1994, “ Regional Variation in Tensile Properties and Biochemical Composition of the Human Lumbar Annulus Fibrosus,” Spine, 19(12), pp. 1310–1319. [CrossRef] [PubMed]
Iatridis, J. C. , MacLean, J. J. , and Ryan, D. A. , 2005, “ Mechanical Damage to the Intervertebral Disc Annulus Fibrosus Subjected to Tensile Loading,” J. Biomech., 38(3), pp. 557–565. [CrossRef] [PubMed]
Stokes, I. A. , 1987, “ Surface Strain on Human Intervertebral Discs,” J. Orthop. Res., 5(3), pp. 348–355. [CrossRef] [PubMed]
Bass, E. C. , Ashford, F. A. , Segal, M. R. , and Lotz, J. C. , 2004, “ Biaxial Testing of Human Annulus Fibrosus and Its Implications for a Constitutive Formulation,” Ann. Biomed. Eng., 32(9), pp. 1231–1242. [CrossRef] [PubMed]
Bruehlmann, S. B. , Hulme, P. A. , and Duncan, N. A. , 2004, “ In Situ Intercellular Mechanics of the Bovine Outer Annulus Fibrosus Subjected to Biaxial Strains,” J. Biomech., 37(2), pp. 223–231. [CrossRef] [PubMed]
Gregory, D. E. , and Callaghan, J. P. , 2011, “ A Comparison of Uniaxial and Biaxial Mechanical Properties of the Annulus Fibrosus: A Porcine Model,” ASME J. Biomech. Eng., 133(2), p. 024503. [CrossRef]
Hollingsworth, N. T. , and Wagner, D. R. , 2012, “ The Stress and Strain States of the Posterior Annulus Under Flexion,” Spine, 37(18), pp. E1134–E1139. [CrossRef] [PubMed]
O'Connell, G. D. , Sen, S. , and Elliott, D. M. , 2012, “ Human Annulus Fibrosus Material Properties From Biaxial Testing and Constitutive Modeling Are Altered With Degeneration,” Biomech. Model. Mechanobiol., 11(3–4), pp. 493–503. [CrossRef] [PubMed]
Galante, J. O. , 1967, “ Tensile Properties of the Human Lumbar Annulus Fibrosus,” Acta Orthop. Scand., 38(Suppl 100), pp. 1–91. [CrossRef] [PubMed]
Eilaghi, A. , Flanagan, J. G. , Brodland, W. G. , and Ethier, C. R. , 2009, “ Strain Uniformity in Biaxial Specimens is Highly Sensitive to Attachment Details,” ASME J. Biomech. Eng., 131(9), p. 091003. [CrossRef]
Heuer, F. , Schmidt, H. , and Wilke, H.-J. , 2008, “ Stepwise Reduction of Functional Spinal Structures Increased Disc Bulge and Surface Strains,” J. Biomech., 41(9), pp. 1953–1960. [CrossRef] [PubMed]
Waters, T. R. , Putz-Anderson, V. , Garg, A. , and Fine, L. J. , 1993, “ Revised NIOSH Equation for the Design and Evaluation of Manual Lifting Tasks,” Ergonomics, 36(7), pp. 749–776. [CrossRef] [PubMed]
Cohen, J. , 1988, Statistical Power Analysis for the Behavioral Sciences—Revised Edition, Academic Press, New York.
Gregory, D. E. , and Callaghan, J. P. , 2011, “ A Comparison of Uniaxial and Biaxial Mechanical Properties of the Annulus Fibrosus: A Porcine Model,” ASME J. Biomech., 133(2), p. 024503. [CrossRef]
Elliott, D. M. , and Setton, L. A. , 2001, “ Anisotropic and Inhomogeneous Tensile Behaviour of the Human Annulus Fibrosus: Experimental Measurement and Material Model Predictions,” ASME J. Biomech. Eng., 123(3), pp. 256–263. [CrossRef]
Zak, M. , and Pezowicz, C. , 2013, “ Spinal Sections and Regional Variations in the Mechanical Properties of the Annulus Fibrosus Subjected to Tensile Loading,” Acta Bioeng. Biomech., 15(1), pp. 51–59. [PubMed]
Cassidy, J. J. , Hiltner, A. , and Baer, E. , 1989, “ Hierarchical Structure of the Intervertebral Disc,” Connect. Tissue Res., 23(1), pp. 75–88. [CrossRef] [PubMed]
Rajsekaran, S. , Bajaj, N. , Tubaki, V. , Kanna, R. M. , and Shetty, A. P. , 2013, “ ISSLS Prize Winner: The Anatomy of Failure in Lumbar Disc Herniation: An In Vivo, Multimodal, Prospective Study of 181 Subjects,” Spine, 38(17), pp. 1491–1500. [CrossRef] [PubMed]
Wade, K. R. , Robertson, P. A. , Thambyah, A. , and Broom, N. D. , 2014, “ How Healthy Discs Herniate,” Spine, 39(13), pp. 1018–1028. [CrossRef] [PubMed]
Adams, M. A. , Dolan, P. , Hutton, W. C. , and Porter, R. W. , 1990, “ Diurnal Changes in Spinal Mechanics and Their Clinical Significance,” J. Bone Jt. Surg. Br., 72(2), pp. 266–270.
Gruevski, K. M. , Gooyers, C. E. , Karakolis, T. , and Callaghan, J. P. , 2015, “ The Effect of Local Hydration Environment on the Mechanical Properties of Isolated Porcine Annular Samples,” ASME J. Biomech. Eng. (submitted).
Hirsch, C. , and Galante, J. , 1967, “ Laboratory Conditions for Tensile Tests in Annulus Fibrosus From Human Intervertebral Discs,” Acta Orthop. Scand., 38(2), pp. 148–162. [CrossRef] [PubMed]
Gregory, D. E. , and Callaghan, J. P. , 2010, “ An Examination of the Influence of Strain Rate on Sub-Failure Mechanical Properties of the Annulus Fibrosus,” ASME J. Biomech. Eng., 132(9), p. 091010. [CrossRef]
Marras, W. S. , Lavendar, S. A. , Ferguson, S. A. , Splittstoesser, R. E. , Yang, G. , and Schabo, P. , 2010, “ Instrumentation for Measuring Dynamic Spinal Load Moment Exposures in the Workplace,” J. Electromyogr. Kinesiol., 20(1), pp. 1–9. [CrossRef] [PubMed]
Oxland, T. R. , Panjabi, M. M. , Southern, E. P. , and Duranceau, J. S. , 1991, “ An Anatomic Basis for Spinal Instability: A Porcine Trauma Model,” J. Orthop. Res., 9(3), pp. 452–462. [CrossRef] [PubMed]
Yingling, V. R. , Callaghan, J. P. , and McGill, S. M. , 1999, “ The Porcine Cervical Spine as a Model for the Human Lumbar Spine: An Anatomical, Geometric and Functional Comparison,” J. Spinal Disorders, 12(5), pp. 415–423. [CrossRef]


Grahic Jump Location
Fig. 6

Average peak unnormalized tensile stress in AF tissue samples excised from the posterior–lateral region of the IVD, across experimental conditions. Note: y-axis scale doubles when moving left to right between subplots.

Grahic Jump Location
Fig. 5

Average peak unnormalized tensile stress in AF tissue samples excised from the anterior region of the IVD, across experimental conditions. Note: y-axis scale doubles when moving left to right between subplots.

Grahic Jump Location
Fig. 4

Profile plot of average (+ standard deviation) unnormalized peak stress data across the magnitude of peak stress and loading axis. Average data collapsed across anterior and posterior regions of the IVD and cycle number are presented.

Grahic Jump Location
Fig. 3

Profile plot of average (+ standard deviation) unnormalized peak stress data across the magnitude of peak stress and loading cycle number

Grahic Jump Location
Fig. 2

Profile plot of average (+ standard deviation) unnormalized peak stress data across the magnitude of peak stretch and cycle rate for (a) anterior and (b) posterior–lateral regions. Average data across cycle number 1, 10, and 100 is presented.

Grahic Jump Location
Fig. 1

Representative cycle-varying changes of stress stretch-ratio loading curves for (a) circumferential and (b) axial loading axes (c34, anterior sample, 10 cycles per minute stretch at 12–20%)



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