Biomechanics of the Anulus Fibrosus and Nucleus Pulposus of the Human Lumbar Intervertebral Disc and the Effects of Degeneration

This dissertation provides an investigation and review of the material behavior of the anulus fibrosus and nucleus pulposus of the human lumbar intervertebral disc. The information, analyses, and conclusions of the studies presented reveal a new picture of the function and failure of the non-degenerate and degenerate intervertebral disc and provides a foundation which is necessary for accurate modeling of the disc.

A comprehensive series of studies on the mechanical behavior of the anulus fibrosus in tension is given. First, the tensile properties of single layer specimens of anulus are determined as a function of location within the disc to evaluate the behavior of the basic tensile structural unit of the highly organized anulus fibrosus. This is followed by a similar study on the tensile behavior of multiple layer samples which provides information regarding the interactions between each layer and anisotropy of the composite anulus. The effects of disc degeneration and aging on the tensile properties of the anulus fibrosus are also investigated to obtain a relationship between the morphological changes occuring in the anulus with degeneration and changes in its mechanical behavior.

The com pressive behaviors of the anulus fibrosus under large deform ations are also investigated. These material behaviors are described using a nonlinear biphasic mixture theory to evaluate the interactions between solid and fluid phases of the anulus. The effect of specimen orientation on these compressive material properties is also studied in order to evaluate the anisotropy of the anulus in confined compression. The results of this study are necessary for future modeling of the intervertebral disc with important implications for nutritional pathways.

The variety and polydispersity of the biomacromolecules comprising the nucleus pulposus gives rise to unique viscoelastic material behaviors. This dissertation investigates several forms for the relaxation spectrum in a viscoelastic model in order to obtain a model capable of describing the predominant viscoelastic behaviors of the non-degenerate and degenerate nucleus pulposus in shear. This study provides the first comprehensive series of tests on the loaddeformation behavior of the nucleus pulposus.

Year	Entry
1976	Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. April 29, 1976;260(5554):808-809.
1986	Mak AF. The apparent viscoelastic behavior of articular cartilage: the contributions from the intrinsic matrix viscoelasticity and interstitial fluid flows. J Biomech Eng. May 1986;108(2):123-130.
1993	Setton LA, Zhu W, Mow VC. The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. J Biomech. April–May 1993;26(4-5):581-592.
1993	Setton LA, Zhu W, Weidenbaum M, Ratcliffe A, Mow VC. Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J Orthop Res. March 1993;11(2):228-239.
1979	Nachemson AL, Schultz AB, Berkson MH. Mechanical properties of human lumbar spine motion segments: influences of age, sex, disc level, and degeneration. Spine. January–February 1979;4(1):1-8.
1995	Setton LA, Mow VC, Howell DS. Mechanical behavior of articular cartilage in shear is altered by transection of the anterior cruciate ligament. J Orthop Res. July 1995;13(4):473-482.
1991	Brinckmann P, Grootenboer H. Change of disc height, radial disc bulge, and intradiscal pressure from discectomy: an in vitro investigation on human lumbar discs. Spine. June 1991;16(6):641-646.
1978	Lin HS, Lui YK, Ray G, Nikravesh P. Systems identification for material properties of the intervertebral joint. J Biomech. 1978;11(1-2):1-14.
1982	Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res. 1982;9(4):247-248.
1952	Hirsch C, Schajowicz F. Studies on structural changes in the lumbar annulus fibrosus. Acta Orthop Scand. 1952;22(1-4):184-231.
1954	Hirsch C, Nachemson A. New observations on the mechanical behavior of lumbar discs. Acta Orthop Scand. 1954;23(4):254-283.
1980	Mow VC, Kuei SC, Lai WM, Armstrong CG. Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J Biomech Eng. February 1980;102(1):73-84.
1980	Mow VC, Lai WM. Recent developments in synovial joint biomechanics. SIAM Rev. 1980;22(3):275-317.
1976	Woo SL-Y, Akeson WH, Jemmott GF. Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. J Biomech. 1976;9(12):785-791.
1987	Nigul I, Nigul U. On algorithms of evaluation of Fung's relaxation function parameters. J Biomech. 1987;20(4):343-352.
1987	Pearce RH, Grimmer BJ, Adams ME. Degeneration and the chemical composition of the human lumbar intervertebral disc. J Orthop Res. 1987;5(2):198-205.
1990	O'Hara BP, Urban JP, Maroudas A. Influence of cyclic loading on the nutrition of articular cartilage. Ann Rheum Dis. July 1990;49(7):536-539.
1979	Urban JPG, Maroudas A. The measurement of fixed charged density in the intervertebral disc. Biochim Biophys Acta. August 6, 1979;586(1):166-178.
1984	Kelsey JL, Githens PB, White AA III, Holford TR, Walter SD, O'Connor T, Ostfeld AM, Weil U, Southwick WO, Calogero JA. An epidemiologic study of lifting and twisting on the job and risk for acute prolapsed lumbar intervertebral disc. J Orthop Res. 1984;2(1):61-66.
1993	Zhu W, Mow VC, Koob TJ, Eyre DR. Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments. J Orthop Res. November 1993;11(6):771-781.
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.
1945	Coventry MB, Ghormley RK, Kernohan JW. The intervertebral disc: its microscopic anatomy and pathology, I: anatomy, development, and physiology. J Bone Joint Surg. January 1945;27(1):105-112.
1985	Adams MA, Hutton WC. Gradual disc prolapse. Spine. July 1985;10(6):524-531.
1967	Galante JO. Tensile properties of the human lumbar annulus fibrosus. Acta Orthop Scand. 1967;(suppl 100):1-91.
1989	Proctor CS, Schmidt MB, Whipple RR, Kelly MA, Mow VC. Material properties of the normal medial bovine meniscus. J Orthop Res. November 1989;7(6):771-782.
1990	Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IK, Bishop PB. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine. May 1990;15(5):411-415.
1986	Holmes MH. Finite deformation of soft tissue: analysis of a mixture model in uni-axial compression. J Biomech Eng. November 1986;108(4):372-381.
1988	Miller JAA, Schmatz C, Schultz AB. Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine. February 1988;13(2):173-178.
1985	Holmes MH, Lai WM, Mow VC. Singular perturbation analysis of the nonlinear, flow-dependent compressive stress relaxation behavior of articular cartilage. J Biomech Eng. August 1985;107(3):206-218.
1976	Wu H-C, Yao R-F. Mechanical behavior of the human annulus fibrosus. J Biomech. 1976;9(1):1-7.
1994	Natarajan RN, Ke JH, Andersson GBJ. A model to study the disc degeneration process. Spine. February 1, 1994;19(3):259-265.
1983	Brinckmann P, Frobin W, Hierholzer E, Horst M. Deformation of the vertebral end-plate under axial loading of the spine. Spine. November–December 1983;8(8):851-856.
1982	Reuber M, Schultz A, Denis F, Spencer D. Bulging of lumbar intervertebral disks. J Biomech Eng. August 1982;104(3):187-192.
1990	Holmes MH, Mow VC. The nonlinear characteristics of soft gels and hydrated connective tissues in ultrafiltration. J Biomech. 1990;23(11):1145-1156.
1980	Bowen RM. Incompressible porous media models by use of the theory of mixtures. Int J Eng Sci. 1980;18(9):1129-1148.
1990	Schmidt MB, Mow VC, Chun LE, Eyre DR. Effects of proteoglycan extraction on the tensile behavior of articular cartilage. J Orthop Res. May 1990;8(3):353-363.
1990	Marchand F, Ahmed AM. Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine. May 1990;15(5):402-410.
1987	Keller TS, Spengler DM, Hansson TH. Mechanical behavior of the human lumbar spine, I: creep analysis during static compressive loading. J Orthop Res. 1987;5(4):467-478.
1976	Eyre DR, Muir H. Types I and II collagens in intervertebral disc: interchanging radial distributions in annulus fibrosus. Biochem J. July 1976;157(1):267-270.
1984	Dortmans LJMG, Sauren AAHJ, Rousseau EPM. Parameter estimation using the quasi-linear viscoelastic model proposed by Fung. J Biomech Eng. August 1984;106(3):198-203.
1988	Urban JPG, McMullin JF. Swelling pressure of the lumbar intervertebral discs influence of age, spinal level, composition, and degeneration. Spine. February 1988;13(2):179-187.
1987	Stokes IAF. Surface strain on human intervertebral discs. J Orthop Res. 1987;5(3):348-355.
1980	Hickey DS, Hukins DWL. Relation between the structure of the annulus fibrosus and the function and failure of the intervertebral disc. Spine. March–April 1980;5(2):106-116.
1985	Urban JPG, McMullin JF. Swelling pressure of the inervertebral disc: influence of proteoglycan and collagen contents. Biorheology. 1985;22(2):145-157.
1981	Urban JPG, Maroudas A. Swelling of the intervertebral disc in vitro. Connect Tissue Res. 1981;9(1):1-10.
1979	Andersson GBJ, Schultz AB. Effects of fluid injection on mechanical properties of intervertebral discs. J Biomech. 1979;12(6):453-458.
1979	Hakim NS, King AI. A three dimensional finite element dynamic response analysis of a vertebra with experimental verification. J Biomech. 1979;12(4):277-292.
1980	Woo SL-Y, Simon BR, Kuei SC, Akeson WH. Quasi-linear viscoelastic properties of normal articular cartilage. J Biomech Eng. May 1980;102(2):85-90.
1981	Woo SL-Y, Gomez MA, Akeson WH. The time and history-dependent viscoelastic properties of the canine medical collateral ligament. J Biomech Eng. November 1981;103(4):293-298.
1986	Shirazi-Adl A, Ahmed AM, Shrivastava S. A finite element study of a lumbar motion segment subjected to pure sagittal plane moments. J Biomech. 1986;19(4):331-350.
1984	Shirazi-Adl SA, Shrivastava SC, Ahmed A. Stress analysis of the lumbar disc-body unit in compression: a three-dimensional nonlinear finite element study. Spine. March 1984;9(2):120-134.
1991	Myers BS, McElhaney JH, Doherty BJ. The viscoelastic responses of the human cervical spine in torsion: experimental limitations of quasi-linear theory, and a method for reducing these effects. J Biomech. 1991;24(9):811-817.
1989	Shirazi-Adl A. On the fibre composite material models of disc annulus: comparison of predicted stresses. J Biomech. 1989;22(4):357-365.
1993	Fung YC. Biomechanics: Mechanical Properties of Living Tissues. 2nd ed. New York, NY: Springer-Verlag; 1993.
1990	Fithian DC, Kelly MA, Mow VC. Material properties and structure-function relationships in the menisci. Clin Orthop Relat Res. March 1990;252:19-31.
1994	Zhu W, Chern KY, Mow VC. Anisotropic viscoelastic shear properties of bovine meniscus. Clin Orthop Relat Res. September 1994;306:34-45.
1992	Cohen B. Anisotropic Hydrated Soft Tissues in Finite Deformation and the Biomechanics of the Growth Plate [PhD thesis]. Columbia University; 1992.
1988	Eyre DR, Dickson IR, Van Ness K. Collagen cross-linking in human bone and articular cartilage: age-related changes in the content of mature hydroxypyridinium residues. Biochem J. June 1988;252(2):495-500.
1968	Viidik A. A rheological model for uncalcified parallel-fibred collagenous tissue. J Biomech. January 1968;1(1):3-11.
1989	Roberts S, Menage J, Urban JPG. Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine. February 1989;14(2):166-174.
1986	Spilker RL, Jakobs DM, Schultz AB. Material constants for a finite element model of the intervertebral disk with a fiber composite annulus. J Biomech Eng. February 1986;108(1):1-11.
1981	Lyons G, Eisenstein SM, Sweet MBE. Biochemical changes in intervertebral disc degeneration. Biochim Biophys Acta. 1981;673:443-453.
1980	Lai WM, Mow VC. Drag-induced compression of articular cartilage during a permeation experiment. Biorheology. 1980;17(1-2):111-123.
1984	Mow VC, Mak AF, Lai WM, Rosenberg LC, Tang L-H. Viscoelastic properties of proteoglycan subunits and aggregates in varying solution concentrations. J Biomech. 1984;17(5):325-338.
1992	McNally DS, Adams MA. Internal intervertebral disc mechanics as revealed by stress profilometry. Spine. January 1992;17(1):66-73.
1967	Hirsch C, Galante J. Laboratory conditions for tensile tests in annulus fibrosus from human intervertebral discs. Acta Orthop Scand. 1967;38(2):148-162.
1995	Buckwalter JA. Aging and degeneration of the human intervertebral disc. Spine. June 1995;20(11):1307-1314.
1993	Kwan MK, Lin TH-C, Woo SL-Y. On the viscoelastic properties of the anteromedial bundle of the anterior cruciate ligament. J Biomech. April–May 1993;26(4-5):447-452.
1990	Kwan MK, Lai WM, Mow VC. A finite deformation theory for cartilage and other soft hydrated connective tissues, I: equilibrium results. J Biomech. 1990;23(2):145-155.
1984	Brickley-Parsons D, Glimcher MJ. Is the chemistry of collagen in intervertebral discs an expression of Wolff's Law? a study of the human lumbar spine. Spine. March 1984;9(2):148-163.
1978	White AA III, Panjabi MM. Clinical Biomechanics of the Spine. Philadelphia, PA: J.B. Lippincott Company; 1978.
1979	Parsons JR, Black J. Mechanical behavior of articular cartilage: quantitative changes with alteration of ionic environment. J Biomech. 1979;12(10):765-773.
1951	Virgin WJ. Experimental investigations into the physical properties of the intervertebral disc. J Bone Joint Surg. November 1951;33B(4):607-611.
1957	Brown T, Hansen RJ, Yorra AJ. Some mechanical tests on the lumbosacral spine with particular reference to the intervertebral discs: a preliminary report. J Bone Joint Surg. October 1957;39A(5):1135-1164.
1949	Friberg S, Hirsch C. Anatomical and clinical studies on lumbar disc degeneration. Acta Orthop Scand. 1949;19(2):222-242.
1990	Lai WM, Hou JS, Mow VC. A triphasic theory for the swelling properties of hydrated charged soft biological tissues. In: Mow VC, Ratcliffe A, Woo SL-Y, eds. Biomechanics of Diarthrodial Joints. Vol 1. New York, NY: Springer-Verlag; 1990:283-312.
1991	Lai WM, Hou JS, Mow VC. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng. August 1991;113(3):245-258.
1974	Belytschko T, Kulak RF, Schultz AB, Galante JO. Finite element stress analysis of an intervertebral disc. J Biomech. May 1974;7(3):277-285.
1986	Koeller W, Muehlhaus S, Meier W, Hartmann F. Biomechanical properties of human intervertebral discs subjected to axial dynamic compression: influence of age and degeneration. J Biomech. 1986;19(10):807-816.
1981	Maroudas A, Bannon C. Measurement of swelling pressure in cartilage and comparison with the osmotic pressure of constituent proteoglycans. Biorheology. 1981;18:619-632.
1989	Spirt AA, Mak AF, Wassell RP. Nonlinear viscoelastic properties of articular cartilage in shear. J Orthop Res. January 1989;7(1):43-49.
1976	Kempson GE, Tuke MA, Dingle JT, Barrett AJ, Horsefield PH. The effects of proteolytic enzymes on the mechanical properties of adult human articular cartilage. Biochim Biophys Acta. May 28, 1976;428(3):741-760.
1970	Farfan HF, Cossette JW, Robertson GH, Wells RV, Kraus H. The effects of torsion on the lumbar intervertebral joints: the role of torsion in the production of disc degeneration. J Bone Joint Surg. April 1970;52A(3):468-497.
1985	Simon BR, Wu JSS, Carlton MW, Evans JH, Kazarian LE. Structural models for human spinal motion segments based on a poroelastic view of the intervertebral disk. J Biomech Eng. November 1985;107(4):327-335.
1984	Simon BR, Coats RS, Woo SL-Y. Relaxation and creep quasilinear viscoelastic models for normal articular cartilage. J Biomech Eng. May 1984;106(2):159-164.
1985	Kwan MK-W. A Finite Deformation Theory for Nonlinearly Permeable Cartilage and Other Soft Hydrated Connective Tissues and Rheological Study of Cartilage Proteoglycans [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; December 1985.
1960	Nachemson A. Lumbar intradiscal pressure: experimental studies on post-mortem material. Acta Orthop Scand. 1960;31(suppl 43):1-104.
1964	Nachemson A, Morris JM. In vivo measurements of intradiscal pressure: discometry, a method for the determination of pressure in the lower lumbar discs. J Bone Joint Surg. July 1964;46A(5):1077-1092.
1980	Roth V, Mow VC. The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg. October 1980;62A(7):1102-1117.
1987	Ueno K, Liu YK. A three-dimenstional nonlinear finite element model of lumbar intervertebral joint in torsion. J Biomech Eng. August 1987;109(3):200-209.
1994	Best BA, Guilak F, Setton LA, Zhu W, Saed-Nejad F, Ratcliffe A, Weidenbaum M, Mow VC. Compressive mechanical properties of the human anulus fibrosus and their relationship to biochemical composition. Spine. January 15, 1994;19(2):212-221.
1990	Osti OL, Vernon-Roberts B, Fraser RD. Anulus tears and intervertebral disc degeneration: an experimental study using an animal model. Spine. August 1990;15(8):762-767.
1986	Akizuki S, Mow VC, Müller F, Pita JC, Howell DS, Manicourt DH. Tensile properties of human knee joint cartilage, I: influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res. 1986;4(4):379-392.
1981	Inoue H. Three-dimensional architecture of lumbar intervertebral discs. Spine. March–April 1981;6(2):139-146.
1994	Skaggs DL, Weidenbaum M, Iatridis JC, Ratcliffe A, Mow VC. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine. June 15, 1994;19(12):1310-1319.

Year

Entry

1976

Maroudas A. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. April 29, 1976;260(5554):808-809.

1986

Mak AF. The apparent viscoelastic behavior of articular cartilage: the contributions from the intrinsic matrix viscoelasticity and interstitial fluid flows. J Biomech Eng. May 1986;108(2):123-130.

1993

Setton LA, Zhu W, Mow VC. The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. J Biomech. April–May 1993;26(4-5):581-592.

1993

Setton LA, Zhu W, Weidenbaum M, Ratcliffe A, Mow VC. Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J Orthop Res. March 1993;11(2):228-239.

1979

Nachemson AL, Schultz AB, Berkson MH. Mechanical properties of human lumbar spine motion segments: influences of age, sex, disc level, and degeneration. Spine. January–February 1979;4(1):1-8.