Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus

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Skaggs, D. L.¹; Weidenbaum, M.¹; Iatridis, J. C.¹; Ratcliffe, A.¹; Mow, V. C.¹

Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus

Spine. June 1994;19(12):1310-1319

©1994 J. B. Lippincott Company

Affiliations

¹Orthopaedic Research Laboratory, Department of Orthopaedic Surgery, Columbia-Presbyterian Medical Center, New York, New York
Abstract and keywords

Study Design: The structure-function relationship of anulus fibrosus of nondegenerate lumba intervertebral discs was investigated.

Objectives: The tensile properties and biochemical composition of single lamella specimens from human anulus librosus and their variations with anatomic region were determined.

Summery of Background Data: Regional differences in composition and ultrastructure suggest differences in tensile properties.

Methods: Single lamella specimens were isolated from the anulus, equilibrated in 0.15 ± NaCl and tested in uniaxial tension using a slow strain-rate protocol. Adjacent specimens were used to determine biochemical composition (Including nycration, collagen, proteonlycan, and hydroxypyridinium crosslink density). Tensile properties, biochemical composition, and anatomic location were compared.

Results: Significant radial and circumferential variations in tensile properties of anulus were detected, with the anterior being, stiffer than the posterolateral regions, and the outer being stiffer than the inner regions.

Conclusions: The regional differences in tensile properties may result predominantly from structural rather than compositional variations and may contribute to the clinical frequency of anulus failure in the postarolateral region.

Keywords: anulus fibrosus; mechanical properties; collagen; proteoglycan; disc degeneration
Links

DOI: 10.1097/00007632-199406000-00002

PubMed: 8066509

WoS: A1994NR65500002
History

Accepted: 1993-12-06

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Year	Entry
2004	Haug E, Choi H-Y, Robin S, Beaugonin M. Human models for crash and impact simulation. In: Ayache N, ed. Computational Models for the Human Body. Amsterdam, The Netherlands: Elsevier B.V; 2004:231-452. Ciarlet PG, ed. Handbook of Numerical Analysis; vol 12.
2010	DeWit JA, Cronin DS. Cervical spine segment finite element model validation and verification at traumatic loading levels for injury prediction. In: Proceedings of the 2010 International IRCOBI Conference on the Biomechanics of Impact. September 15-17, 2010; Hannover, Germany.59-70.
2004	Bass EC, Ashford FA, Segal MR, Lotz JC. Biaxial testing of human annulus fibrosus and its implications for a constitutive formulation. Ann Biomed Eng. September 2004;32(9):1231-1242.
2005	Holzapfel GA, Schulze-Bauer CAJ, Feigl G, Regitnig P. Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech Model Mechanobiol. March 2005;3(3):125-140.
1998	Iatridis JC, Setton LA, Foster RJ, Rawlins BA, Weidenbaum M, Mow VC. Degeneration affects the anisotropic and nonlinear behaviors of human anulus fibrosus in compression. J Biomech. June 1998;31(6):535-544.
2005	Iatridis JC, MacLean JJ, Ryan DA. Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading. J Biomech. March 2005;38(3):557-565.
2009	Panzer MB, Cronin DS. C4–C5 segment finite element model development, validation, and load-sharing investigation. J Biomech. March 11, 2009;42(4):480-490.
2000	Elliott DM, Setton LA. A linear material model for fiber-induced anisotropy of the anulus fibrosus. J Biomech Eng. April 2000;122(2):173-179.
2003	Baer AE, Laursen TA, Guilak F, Setton LA. The micromechanical environment of intervertebral disc cells determined by a finite deformation, anisotropic, and biphasic finite element model. J Biomech Eng. February 2003;125(1):1-11.
2017	Barker JB, Cronin DS, Nightingale RW. Lower cervical spine motion segment computational model validation: kinematic and kinetic response for quasi-static and dynamic loading. J Biomech Eng. June 2017;139(6):061009.
2012	DeWit JA, Cronin DS. Cervical spine segment finite element model for traumatic injury prediction. J Mech Behav Biomed Mater. June 2012;10:138-150.
1997	Fujita Y, Duncan NA, Lotz JC. Radial tensile properties of the lumbar annulus fibrosus are site and degeneration dependent. J Orthop Res. November 1997;15(6):814-819.
1999	Iatridis JC, Kumar S, Foster RJ, Weidenbaum M, Mow VC. Shear mechanical properties of human lumbar annulus fibrosus. J Orthop Res. September 1999;17(5):732-737.
2007	Nerurkar NL, Elliott DM, Mauck RL. Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res. August 2007;25(8):1018-1028.
1995	Acaroglu ER, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M. Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine. December 15, 1995;20(24):2690-2701.
1996	Ebara S, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M. Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine. March 15, 1996;21(4):452-461.
1996	Iatridis JC, Weidenbaum M, Setton LA, Mow VC. Is the nucleus pulposus a solid or a fluid? mechanical behaviors of the nucleus pulposus of the human intervertebral disc. Spine. May 15, 1996;21(15):1174-1184.
1998	Lotz JC, Colliou OK, Chin JR, Duncan NA, Liebenberg E. Compression-induced degeneration of the intervertebral disc: an in vivo mouse model and finite-element study. Spine. December 1, 1998;23(23):2493-2506.
2012	Strange DGT. Mechanics of Biomimetic Materials for Tissue Engineering of the Intervertebral Disc [PhD thesis]. Cambridge, UK: University of Cambridge; December 2012.
2018	Fischenich KM. Development of a Novel Block Copolymer Hydrogel for Meniscal Replacement [PhD thesis]. Colorado State University; 2018.
1996	Iatridis JC. Biomechanics of the Anulus Fibrosus and Nucleus Pulposus of the Human Lumbar Intervertebral Disc and the Effects of Degeneration [PhD thesis]. Columbia University; 1996.
2020	Sloan SR Jr. Tissue-Engineered Annulus Fibrosus Repair and Nucleus Pulposus Augmentation in Pre-Clinical Models of Intervertebral Disc Degeneration [PhD thesis]. Ithaca, NY: Cornell University; May 2020.
2012	Isaacs JL. Micromechanics of the Annulus Fibrosus: Role of Biomolecules in Mechanical Function [PhD thesis]. Drexel University; May 2012.
1999	Elliott DM. The Fiber-Induced Anisotropic Material Behaviors of the Anulus Fibrosus of the Intervertebral Disc in Tension [PhD thesis]. Duke University; 1999.
2001	Baer AE. The Micromechanical Environment of Intervertebral Disc Cells [PhD thesis]. Duke University; 2001.
2008	Cao L. Micromechanics of the Pericellular Matrix and Cells in the Intervertebral Disc: Three-Dimensional Finite Element Modeling Based on in Situ Morphology [PhD thesis]. Duke University; 2008.
2015	Hwang PY. Cadherin-Mediated Cell-Cell Interactions Regulates Phenotype and Morphology of Nucleus Pulposus Cells of the Intervertebral Disc [PhD thesis]. Duke University; 2015.
2007	Connelly JT. Regulatory Mechanisms in the Chondrogenesis of Mesenchymal Progenitors: The Roles of Cyclic Tensile Loading and Cell-Matrix Interactions [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2007.
2017	Christou A. Modelling Spinal Injury Due to High-Rate Axial Loading [PhD thesis]. Imperial College London; June 2017.
2016	Gao X. Modeling the Biomechanics and Mechanobiology of Intervertebral Discs [PhD thesis]. University of Miami; August 2016.
2018	Long RG. Repair of Herniated Intervertebral Discs: Designing and Translating Annulus Fibrosus Sealants [PhD thesis]. Icahn School of Medicine at Mount Sinai; 2018.
2019	Torre OM. Intervertebral Disc Regeneration in Neonatal Mice [PhD thesis]. Icahn School of Medicine at Mount Sinai; 2019.
2005	Shin G. Viscoelastic Responses of the Lumbar Spine During Prolonged Stooping [PhD thesis]. North Carolina State University; 2005.
1999	Bass EC. Biaxial Nonlinear Elastic Response of the Human Lumbar Annulus Fibrosus and Its Role in the Determination of a Physiologically Relevant Constitutive Relation [PhD thesis]. Berkeley, CA: Berkeley, University of California; 1999.
2002	Wagner DR. A Mechanistic Strain Energy Function and Experimental Results for the Human Annulus Fibrosus [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2002.
2008	Schultz DS. Structure-Function Relationships in Soft Tissue Mechanics: Examining How the Micro-Scale Architecture of Biochemical Constituents Effects Health [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2008.
2019	Bezci SE. Time-Dependent Characterization of Fluid Flow Into the Intervertebral Disc [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2019.
2019	Yang B. Simulating Intervertebral Disc Mechanics Using Finite Element Method [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2019.
1998	Colliou OK. Role of Mechanical Loading in Intervertebral Disc Degeneration [PhD thesis]. San Francisco, University of California; 1998.
2002	Walsh AJL. Tissue Remodeling in the Intervertebral Disc: Response to Dynamic Loading and Growth Factors [PhD thesis]. San Francisco, University of California; 2002.
2017	Ouyang A. Effects of Design Factors and Microenvironment on Mesenchymal Stem Cells and Nucleus Pulposus Cells for Intervertebral Disc Tissue Engineering [PhD thesis]. San Francisco, University of California; 2017.
2020	Horne D. Development of Novel Energy-Based Musculoskeletal Therapies [PhD thesis]. San Francisco, University of California; 2020.
2011	Morschauser MA. Development of Collagen Thin Films for Intervertebral Disc Cell Culture & Examination of Cell Phenotypes and Interactions [PhD thesis]. University of Maryland; 2011.
2004	Lin C-Y. A New Spine Interbody Fusion System: Integrating Topology Optimized Biodegradable Interbody Fusion Cages With Cell-Based and Ex Vivo Gene Therapy [PhD thesis]. University of Michigan; 2004.
2005	Guerin HAL. A Nonlinear Anisotropic Continuum Model of Human Annulus Fibrosus Mechanical Behavior [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2005.
2009	O'Connell GD. Degeneration Affects the Structural and Tissue Mechanics of the Intervertebral Disc [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2009.
2010	Nerurkar NL. Integrating Theoretical and Experimental Methods for Multi-Scale Tissue Engineering of the Annulus Fibrosus of the Intervertebral Dis [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2010.
2014	Yoder JH. Intervertebral Disc Structure and Mechanical Function Under Physiological Loading Quantified Non-Invasively Utilizing MRI and Image Registration [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2014.
2016	Peloquin JM. Tensile Mechanics of the Knee Meniscus in the Context of Cracks: Failure and Fracture Mechanisms, Strain Concentrations, and the Effect of Specimen Shape [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2016.
2006	Panzer MB. Numerical Modelling of the Human Cervical Spine in Frontal Impact [Master's thesis]. University of Waterloo; 2006.
2009	Gregory DE. The Influence of the Tensile Material Properties of Single Annulus Fibrosus Lamellae and the Interlamellar Matrix Strength on Disc Herniation and Progression [PhD thesis]. University of Waterloo; 2009.
2010	Langohr GDG. Cervical Total Level Arthroplasty System With PEEK All-Polymer Articulations [Master's thesis]. University of Waterloo; 2010.
2013	Noguchi M. Examining Changes in Intradiscal Pressure During Intervertebral Disc Herniation [Master's thesis]. University of Waterloo; 2013.
2014	Gooyers CE. Exploring Interactions Between Force, Repetition and Posture on Low Back Joint Loading and Intervertebral Disc Injury [PhD thesis]. University of Waterloo; 2014.
2014	Karakolis T. Prolonged Sitting, Standing, and the Sit-Stand Paradigm for Office Workers: An Investigation Into Lumbar Spine Intervertebral Joint Load Distribution [PhD thesis]. University of Waterloo; 2014.
2018	Gruevski KM. The Aging Spine: The Effect of Cyclic Loading, Simulated Degeneration and Prolonged Sitting on Joint Stiffness Across Age [PhD thesis]. University of Waterloo; 2018.
2018	Khor F. Computational Modeling of Hard Tissue Response and Fracture in the Lower Cervical Spine Under Compression Including Age Effects [Master's thesis]. University of Waterloo; 2018.
2020	Fabre MAC. Development of Elderly Posture Male and Female Finite Element Neck Models and Assessment of Tissue-Level Response Under Impact Loading [Master's thesis]. University of Waterloo; 2020.
2020	Shen D. Investigation of Whiplash Associated Disorders Using Finite Element Neck Models With Active Musculature in Frontal, Rear and Lateral Impact [Master's thesis]. University of Waterloo; 2020.
1996	Kim Y. A Finite-Element Study of Intervertebral Cages and Spinal Bone Remodeling [PhD thesis]. University of Wisconsin – Madison; 1996.
1997	Rapoff AJ. Tensile Fatigue of Intervertebral Disc Annulus and a Probabilistic Rule of Mixtures for Elastic Moduli [PhD thesis]. University of Wisconsin – Madison; August 1997.