Abstract
The superficial tangential zone (STZ) plays a significant role in normal articular cartilage’s ability to support loads and retain fluids. To date, tissue engineering efforts have not replicated normal STZ function in cartilage repairs. This finite element study examined the STZ’s role in normal and repaired articular surfaces under different contact conditions. Contact area and pressure distributions were allowed to change with time, tension-compression nonlinearity modeled collagen behavior in the STZ, and nonlinear geometry was incorporated to accommodate finite deformation. Responses to loading via impermeable and permeable rigid surfaces were compared to loading via normal cartilage, a more physiologic condition, anticipating the two rigid loading surfaces would bracket that of normal. For models loaded by normal cartilage, an STZ placed over the inferior repair region reduced the short-term axial compression of the articular surface by 15%, when compared to a repair without an STZ. Covering the repair with a normal STZ shifted the flow patterns and strain levels back toward that of normal cartilage. Additionally, reductions in von Mises stress (21%) and an increase in fluid pressure (13%) occurred in repair tissue under the STZ. This continues to show that STZ properties of sufficient quality are likely critical for the survival of transplanted constructs in vivo. However, response to loading via normal cartilage did not always fall within ranges predicted by the rigid surfaces. Use of more physiologic contact models is recommended for more accurate investigations into properties critical to the success of repair tissues.
Similar content being viewed by others
References
Almeida E, Spilker R (1997) Mixed and penalty finite element models for the nonlinear behavior of biphasic soft tissues in finite deformation: part I—alternate formulations. Comput Methods Biomech Biomed Eng 1(1): 25–46
Almeida E, Spilker R (1998) Mixed and penalty finite element models for the nonlinear behavior of biphasic soft tissues in finite deformation: part II—nonlinear examples. Comput Methods Biomech Biomed Eng 1(2): 151–170
Ateshian GA (2007) Artificial cartilage: weaving in three dimensions. Nat Mater 6(2): 89–90
Ateshian GA, Rajan V, Chahine NO, Canal CE, Hung CT (2009) Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J Biomech Eng 131: 061003-1-10
Bartlett W, Gooding C, Carrington R, Skinner J, Briggs T, Bentley G (2005) Autologous chondrocyte implantation at the knee using a bilayer collagen membrane with bone graft. J Bone Joint Surg Br 87(3): 330–332
Below S, Arnoczky S, Dodds J, Kooima C, Walter N (2002) The splitline pattern of the distal femur: a consideration in the orientation of autologous cartilage grafts. Arthroscopy 18(6): 613–617
Butler D, Goldstein S, Guilak F (2000) Functional tissue engineering: the role of biomechanics. J Biomech Eng 122(6): 570–575
Chen A, Bae W, Schinagl R, Sah R (2001) Depth- and strain- dependent mechanical and electromechanical properties of full-thickness bovine articular cartilage in confined compression. J Biomech 34(1): 1–12
Cherubino P, Grassi F, Bulgheroni P, Ronga M (2003) Autologous chondrocyte implantation using a bilayer collagen membrane: a preliminary report. J Orthop Surg 11(1): 10–15
Chiang H, Jiang CC (2009) Repair of articular cartilage defects: review and perspectives. J Formos Med Assoc 108(2): 87–101
Cohen B, Gardner T, Ateshian G (1993) The influence of transverse isotropy on cartilage indentation behavior: a study of the human humeral head. Trans 39th Ann Mtg Ortho Res Soc
DiSilvestro MR, Suh JK (2001) A cross-validation of the biphasic poroviscoelastic model of articular cartilage in unconfined compression, indentation, and confined compression. J Biomech 34(4): 519–525
Donzelli P, Spilker R, Ateshian G, Mow V (1999) Contact analysis of biphasic transversely isotropic cartilage layers and correlations with tissue failure. J Biomech 32: 1037–1047
Frank CB, Shrive NG, Boorman RS, Lo IK, Hart DA (2004) New perspectives on bioengineering of joint tissues: joint adaptation creates a moving target for engineering replacement tissues. Ann Biomed Eng 32(3): 458–465 Review
Garcia J, Altiero N, Haut R (2000) Estimation of in situ elastic properties of biphasic cartilage based on a transversely isotropic hypo-elastic model. J Biomech Eng 122(1): 1–8
Gardner T, Xin L, Mow V (2003) Validation of articular cartilage tensile moduli from transversely isotropic biphasic indentation FEM analysis. Trans ASME 2003 Summer Bioeng Conf
Getgood A, Brooks R, Fortier L, Rushton N (2009) Articular cartilage tissue engineering: today’s research, tomorrow’s practice?. J Bone Joint Surg Br 91(5): 565–576 Review
Glaser C, Putz R (2002) Functional anatomy of articular cartilage under compressive loading Quantitative aspects of global, local and zonal reactions of the collagenous network with respect to the surface integrity. Osteoarthr Cartil 10(2): 83–99
Guilak F (2004) Biomechanical factors in tissue engineering of articular cartilage. In: Goldberg V, Caplan A (eds) Orthopedic tissue engineering: basic science and practices. Marcel Dekker Publishers, New York
Ho ST, Hutmacher DW, Ekaputra AK, Hitendra D, Hui JH (2010) The evaluation of a biphasic osteochondral implant coupled with an electrospun membrane in a large animal model. Tissue Eng Part A 16: 1123–1141
Holmes M, Lai W, Mow V (1985) Singular perturbation analysis of the nonlinear, flow-dependent compressive stress relaxation behavior of articular cartilage. J Biomech Eng 107(3): 206–218
Huang CY, Soltz MA, Kopacz M, Mow VC, Ateshian GA (2003) Experimental verification of the roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in the biphasic response of cartilage. J Biomech Eng 125(1): 84– 93
Hung C, Mauck R,Wang C, Lima E, Ateshian G (2004) A paradigm for functional tissue engineering of articular cartilage via applied physiologic deformational loading. Ann Biomed Eng 32(1):35–49. Erratum in: Ann Biomed Eng 2004 32(3):510
Huang C, Stankiewicz A, Ateshian G, Mow V (2005) Anisotropy, inhomogeneity, and tension-compression nonlinearity of human glenohumeral cartilage in finite deformation. J Biomech 38: 799–809
Ionescu LC, Garcia GH, Zachry TL, Lee GC, Sennett BJ, Mauck RL (2010) In vitro meniscus integration potential is inversely correlated with tissue maturation state. Trans ASME 2010 Summer Bioeng Conf
Iwasa J, Engebretsen L, Shima Y, Ochi M (2009) Clinical application of scaffolds for cartilage tissue engineering. Knee Surg Sports Traumatol Arthrosc 17(6): 561–577 Epub 20 Nov 2008. Review
Jeffery A, Blunn G, Archer C, Bentley G (1991) Three-dimensional collagen architecture in bovine articular cartilage. J Bone Joint Surg Br 73(5): 795–801
Jurvelin JS, Arokoski JP, Hunziker EB, Helminen HJ (2000) Topographical variation of the elastic properties of articular cartilage in the canine knee. J Biomech 33: 669–675
Klein TJ, Maida J, Sah RL, Hutmacher DW (2009a) Tissue engineering of articular cartilage with biomimetic zones. Tissue Eng Part B 15(2): 143–157
Klein TJ, Rizzi SC, Reichert JC, Georgi N, Malda J, Schuurman W, Crawford RW, Hutmacher DW (2009b) Strategies for zonal cartilage repair using hydrogels. Macromol Biosci 9(11): 1049–1058
Korhonen R, Wong M, Arokoski J, Lindgren R, Helminen H, Hunziker E, Jurvelin J (2002) Importance of the superficial tissue layer for the indentation stiffness of articular cartilage. Med Eng Phys 24(2): 99–108
Krishnan R, Park S, Eckstein F, Ateshian G (2003) Inhomogeneous cartilage properties enhance superficial interstitial fluid support and frictional properties, but do not provide a homogeneous state of stress. J Biomech Eng 125: 569–577
Krishnan R, Kopacz M, Ateshian G (2004) Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication. J Orthop Res 22(3): 565–570
Lai W, Mow V (1980) Drag-induced compression of articular cartilage during a permeation experiment. Biorheology 17(1–2): 111–123
Li L, Buschmann M, Shirazi-Adl A (2000) A fibril reinforced nonhomogeneous poroelastic model for articular cartilage: inhomogeneous response in unconfined compression. J Biomech 33: 1533–1541
Li L, Buschmann M, Shirazi-Adl A (2003) Strain-rate dependent stiffness of articular cartilage in unconfined compression. J Biomech Eng 125(2):161–168. Erratum in: J Biomech Eng 2003 125(4):566
Martin I, Obradovic B, Treppo S, Grodzinsky A, Langer R, Freed L, Vunjak-Novakovic G (2000) Modulation of the mechanical properties of tissue engineered cartilage. Biorheology 37(1–2): 141–147
McNickle AG, Provencher MT, Cole BJ (2008) Overview of existing cartilage repair technology. Sports Med Arthrosc 16(4): 196–201 Review
Mizrahi J, Maroudas A, Lanir Y, Ziv I, Webber T (1986) The “instantaneous” deformation of cartilage: effects of collagen fiber orientation and osmotic stress. Biorheology 23(4): 311–330
Moutos FT, Freed LE, Guilak F (2007) A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 6(2): 162–167 Epub 21 Jan 2007
Moutos FT, Guilak F (2008) Composite scaffolds for cartilage tissue engineering. Biorheology 45(3–4): 501–512
Mow V, Lai W, Holmes M (1982) Advanced theoretical and experimental techniques in cartilage research. In: Huiskes R, VanCampen D, DeWijn J (eds) Biomechanics: principle and applications, vol I. Martinus Nijhoff Publishers, The Hague
Mow V, Good P, Gardner T (2000) A new method to determine the tensile properties of articular cartilage using the indentation test. Trans 46th Ann Mtg Ortho Res Soc
Muir H, Bullough P, Maroudas A (1970) The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg Br 52(3): 554–563
Ng KW, Ateshian GA, Hung CT (2009) Zonal chondrocytes seeded in a layered agarose hydrogel create engineered cartilage with depth-dependent cellular and mechanical inhomogeneity. Tissue Eng Part A 15(00): 1–10
Nho SJ, Pensak MJ, Seigerman DA, Cole BJ (2010) Rehabilitation after autologous chondrocyte implantation in athletes. Clin Sports Med 29: 267–282
Olsen S, Oloyede A, Adam C (2004) A finite element formulation and program to study transient swelling and load-carriage in healthy and degenerate articular cartilage. Comput Methods Biomech Biomed Eng 7(2): 111–120
Owen JR, Wayne JS (2006a) Influence of a superficial tangential zone over repairing cartilage defects: implications for tissue engineering. Biomech Model Mechanobiol 5(2–3): 102–110
Owen JR, Wayne JS (2006b) Impact of the superficial tangential zone in cartilage on tissue engineering efforts. Trans 52nd Ann Mtg Ortho Res Soc
Owen JR, Wayne JS (2006c) Influence of the superficial tangential zone cartilage under contact loading: implications for tissue engineering efforts. Trans ASME 2006 Summer Bioeng Conf
Owen JR, Wayne JS (2008) Influence of the superficial tangential zone for cartilage modeled in finite deformation and with tension/compression nonlinearity. Trans ASME 2008 Summer Bioeng Conf
Revell CM, Athanasiou KA (2009) Success rates and immunologic responses of autogenic, allogenic, and xenogenic treatments to repair articular cartilage defects. Tissue Eng Part B 15(1): 1–15
Roth V, Mow V (1980) The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg Am 62(7): 1102–1117
Ronga M, Federico G, Paolo B (2004) Arthroscopic autologous chondrocyte implantation for the treatment of a chondral defect in the tibial plateau of the knee. Arthroscopy 20(1): 79–84
Setton L, Zhu W, Mow V (1993) The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. J Biomech 26(4/5): 581–592
Smith C, Goldberg V, Mansour J (2001) Analysis of the mechanical environment in a repairing osteochondral defect. Trans 47thAnn Mtg Ortho Res Soc
Soltz M, Ateshian G (2000) A conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. J Biomech Eng 122(6): 576–586
Toolan B, Frenkel S, Pachence J, Yalowitz L, Alexander H (1996) Effects of growth-factor-enhanced culture on a chondrocyte-collagen implant for cartilage repair. J Biomed Mater Res 31(2): 273–280
Torzilli P (1993) Effects of temperature, concentration and articular surface removal on transient solute diffusion in articular cartilage. Med Biol Eng Comp 31(Suppl): S93–S98
Torzilli P, Dethmers D, Rose D, Schryuer H (1983) Movement of interstitial water through loaded articular cartilage. J Biomech 16(3): 169–179
van der Voet A (1997) A comparison of finite element codes for the solution of biphasic poroelastic problems. Proc Inst Mech Eng H 211: 209–211
Vinatier C, Mrugala D, Jorgensen C, Guicheux J, Noël D (2009) Cartilage engineering: a crucial combination of cells, biomaterials and biofactors. Trends Biotechnol. 27(5): 307–314 Epub 28 Mar 2009. Review
Wayne J (1995) Load partitioning influences the mechanical response of articular cartilage. Ann Biomed Eng 23: 40–47
Wayne J, Woo S, Kwan M (1991) Finite element analyses of repaired articular surfaces. J Eng Med Proc InstMech Eng(H) 205(3): 155–162
Wilson W, van Rietbergen B, van Donkelaar CC, Huiskes R (2003) Pathways of load-induced cartilage damage causing cartilage degeneration in the knee after meniscectomy. J Biomech 36: 845–851
Wilson W, van Donkelaar C, van Rietbergen B, Ito K, Huiskes R (2004) Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study. J Biomech 37(3):357–366. Erratum in: J Biomech (2005) 38:2138–2140
Wilson W, Driessen NJ, van Donkelaar CC, Ito K (2006) Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. Osteoarthr Cartil 14: 1196–1202
Xu J, Zaporojan V, Peretti G, Roses R, Morse K, Roy A, Mesa J, Randolph M, Bonassar L, Yaremchuk M (2004) Injectable tissue-engineered cartilage with different chondrocyte sources. Plast Reconstr Surg 113(5): 1361–1371
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Owen, J.R., Wayne, J.S. Contact models of repaired articular surfaces: influence of loading conditions and the superficial tangential zone. Biomech Model Mechanobiol 10, 461–471 (2011). https://doi.org/10.1007/s10237-010-0247-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-010-0247-1