Abstract
Tissues like the temporomandibular joint (TMJ) disc and the knee meniscus are often mistakenly viewed as a tantamount to hyaline cartilage, largely due to the absence of a comprehensive understanding of the distinguishing properties of cartilaginous tissues. Because of this confusion, fibrocartilaginous tissue engineering attempts may not be based on suitable experimental designs. Fibrocartilaginous tissues are markedly different than hyaline cartilage; however, the dearth of knowledge related to their cellular and biochemical composition, as well as their bio- mechanical characteristics, is stunning. Hyaline articular cartilage is exclusively composed of chondrocytes that produce primarily type II collagen, whereas the TMJ disc and the knee meniscus have a mixed cell population of fibroblasts and cells similar to chondrocytes, which predominantly secrete type I collagen. Additionally, fibrocartilaginous tissues have a low glycosaminoglycan content, a low compressive modulus, and a high tensile modulus when compared to hyaline cartilage. Therefore, it is crucial for fibrocartilaginous tissue engineering attempts to be tissue-specific, utilizing the knowledge of the distinct and unique properties of these tissues. At the same time, advances and insights related to the science and engineering aspect of hyaline cartilage regeneration must be carefully considered for the in vitro engineering of fibrocartilaginous tissues.
Similar content being viewed by others
References
1Adams, M. E., and H. Muir. The glycosaminoglycans of canine menisci. Biochem. J. 197:385-389, 1981.
2Akizuki, S., V. C. Mow, F. Muller, J. C. Pita, D. S. Howell, and D. H. Manicourt. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J. Orthop. Res. 4:379-392, 1986.
3Ali, A. M., and M. M. Sharawy. An immunohistochemical study of collagen types III, VI and IX in rabbit craniomandibular joint tissues following surgical induction of anterior disk displacement. J. Oral Pathol. Med. 25:78-85, 1996.
4Athanasiou, K. A., M. P. Rosenwasser, J. A. Buckwalter, T. I. Malinin, and V. C. Mow. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J. Orthop. Res. 9:330-340, 1991.
5Axelsson, S., A. Holmlund, and A. Hjerpe. Glycosaminoglycans in normal and osteoarthrotic human temporomandibular joint disks. Acta Odontol. Scand. 50:113-119, 1992.
6Beatty, M. W., M.J. Bruno, L.R. Iwasaki, and J. C. Nickel. Strain rate dependent orthotropic properties of pristine and impulsively loaded porcine temporomandibular joint disk. J. Biomed. Mater. Res. 57:25-34, 2001.
7Beek, M., M. P. Aarnts, J. H. Koolstra, A. J. Feilzer, and T. M. van Eijden. Dynamic properties of the human temporomandibular joint disc. J. Dent. Res. 80:876-880, 2001.
8Berkovitz, B. K., and J. Pacy. Age changes in the cells of the intra-articular disc of the temporomandibular joints of rats and marmosets. Arch. Oral Biol. 45:987-995, 2000.
9Berkovitz, B. K., and H. Robertshaw. Ultrastructural quantification of collagen in the articular disc of the temporomandibular joint of the rabbit. Arch. Oral Biol. 38:91-95, 1993.
10Buckwalter, J. A., and H. J. Mankin. Articular cartilage: Tissue design and chondrocyte-matrix interactions. Instr. Course Lect. 47:477-486, 1998.
11Carvalho, R. S., E. H. Yen, and D. M. Suga. Glycosaminoglycan synthesis in the rat articular disk in response to mechanical stress. Am. J. Orthod. Dentofacial Orthop. 107:401-410, 1995.
12Cheung, H. S. Distribution of type I, II, III, and V in the pepsin solubilized collagens in bovine menisci. Connect. Tissue Res. 16:343-356, 1987.
13Collier, S., and P. Ghosh. Effects of transforming growth factor beta on proteoglycan synthesis by cell and explant cultures derived from the knee joint meniscus. Osteoarthritis Cartilage. 3:127-138, 1995.
14Darling, E. M., and K. A. Athanasiou. Articular cartilage bioreactors and bioprocesses. Tissue Eng. 9:9-26, 2003.
15Detamore, M. S., and K. A. Athanasiou. Motivation, characterization and strategy for tissue engineering the temporomandibular joint disc. Tissue Eng. 9:1065-1087, 2003.
16Detamore, M. S., and K. A. Athanasiou. Structure and function of the temporomandibular joint disc: Implications for tissue engineering. J. Oral Maxillofac. Surg. 61:494-506, 2003.
17Detamore, M. S., and K. A. Athanasiou. Tensile properties of the porcine temporomandibular joint disc. J. Biomech. Eng. 125:558-565, 2003.
18Detamore, M. S., J. N. Hegde, R. R. Wagle, A. J. Almarza, D. Montufar-Solis, P. J. Duke, and K. A. Athanasiou. Cell type and distribution in the porcine temporomandibular joint disc. J. Den. Res. Manuscript submitted for publication.
19Dolwick, M. F. The temporomandibular joint: normal and abnormal anatomy. In: Internal Derangements of the Temporomandibular Joint, edited by C. A. Helms, R. W. Katzberg, and M. F. Dolwick. San Francisco: Radiology Research and Education Foundation, 1983, pp. 1-14.
20Eyre, D. R. Cartilage-specific collagens: Structural studies. In: Articular Cartilage and Osteoarthritis, edited by K. E. Kuettner. New York: Raven Press, 1992, pp. 119-131.
21Eyre, D. R. Collagen structure and function in articular cartilage: Metabolic changes in the development of osteoarthritis. In: Osteoarthritic Disorders: Workshop, Monterey, California, April 1994, edited by K. E. Kuettner, and V. M. Goldberg. Rosemont, IL: American Academy of Orthopaedic Surgeons, 1995, pp. 219-229.
22Eyre, D. R., and J. J. Wu. Collagen of fibrocartilage: A distinctive molecular phenotype in bovine meniscus. FEBS Lett. 158:265-270, 1983.
23Fithian, D. C., M. A. Kelly, and V. C. Mow. Material properties and structure–function relationships in the menisci. Clin. Orthop. 252:19-31, 1990.
24Fontenot, M. G. The viscoelasticity of human temporomandibular joint discs. Am. J. Phys. Anthropol. 66:168-169, 1985.
25Freed, L. E., A. P. Hollander, I. Martin, J. R. Barry, R. Langer, and G. Vunjak-Novakovic. Chondrogenesis in a cell–polymer–bioreactor system. Exp. Cell Res. 240:58-65, 1998.
26Gage, J. P., R. M. Shaw, and F. B. Moloney. Collagen type in dysfunctional temporomandibular joint disks. J. Prosthet. Dent. 74:517-520, 1995.
27Ghadially, F. N., J. M. Lalonde, and J. H. Wedge. Ultrastructure of normal and torn menisci of the human knee joint. J. Anat. 136(Pt. 4):773-791, 1983.
28Ghadially, F. N., I. Thomas, N. Yong, and J. M. Lalonde. Ultrastructure of rabbit semilunar cartilages. J. Anat. 125:499-517, 1978.
29Girdler, N. M. In vitro synthesis and characterization of a cartilaginous meniscus grown from isolated temporomandibular chondroprogenitor cells. Scand. J. Rheumatol. 27:446-453, 1998.
30Hasler, E. M., W. Herzog, J. Z. Wu, W. Muller, and U. Wyss. Articular cartilage biomechanics: Theoretical models, material properties, and biosynthetic response. Crit. Rev. Biomed. Eng. 27:415-488, 1999.
31Hellio Le Graverand, M. P., Y. Ou, T. Schield-Yee, L. Barclay, D. Hart, T. Natsume, and J. B. Rattner. The cells of the rabbit meniscus: Their arrangement, interrelationship, morphological variations and cytoarchitecture. J. Anat. 198:525-535, 2001.
32Herwig, J., E. Egner, and E. Buddecke. Chemical changes of human knee joint menisci in various stages of degeneration. Ann. Rheum. Dis. 43:635-640, 1984.
33Hu, J. C., and K. A. Athanasiou. Structure and function of articular cartilage. In: Handbook of Histology Methods for Bone and Cartilage, edited by Y. H. An and K. L. Martin. Totowa, NJ: Humana Press, 2003, pp. 73-95.
34Huang, C. Y., S. D. Matthews, R. G. Pollock, R. J. Pawluk, E. L. Flatow, L. U. Bigliani, and V. C. Mow. Regional and directional tensile properties of bovine glenohumeral cartilage. ASME Adv. Bioeng. 35:525-526, 1997.
35Ibarra, C., C. Jannetta, C. A. Vacanti, Y. Cao, T. H. Kim, J. Upton, and J. P. Vacanti. Tissue engineered meniscus: A potential new alternative to allogeneic meniscus transplantation. Transplant. Proc. 29:986-988, 1997.
36Ibarra, C., J. A. Koski, and R. F. Warren. Tissue engineering meniscus: Cells and matrix. Orthop. Clin. North Am. 31:411-418, 2000.
37Joshi, M. D., J. K. Suh, T. Marui, and S. L. Woo. Interspecies variation of compressive biomechanical properties of the meniscus. J. Biomed. Mater. Res. 29:823-828, 1995.
38Kempson, G. E. Mechanical properties of articular cartilage. In: The Joints and Synovial Fluid, edited by L. Sokoloff, New York: Academic Press, 1980, pp. 177-238.
39Kim, K. W., M. E. Wong, J. F. Helfrick, J. B. Thomas, and K. A. Athanasiou. Biomechanical characterization of the superior joint space of the porcine temporomandibular joint. Ann. Biomed. Eng. 31:924-930, 2003.
40Klompmaker, J., R. P. Veth, H. W. Jansen, H. K. Nielsen, J. H. de Groot, and A. J. Pennings. Meniscal replacement using a porous polymer prosthesis: A preliminary study in the dog. Biomaterials 17:1169-1175, 1996.
41Klompmaker, J., R. P. Veth, H. W. Jansen, H. K. Nielsen, J. H. de Groot, A. J. Pennings, and R. Kuijer. Meniscal repair by fibrocartilage in the dog: Characterization of the repair tissue and the role of vascularity. Biomaterials 17:1685-1691, 1996.
42Kopp, S. Topographical distribution of sulphated glycosaminoglycans in human temporomandibular joint disks. A histochemical study of an autopsy material. J. Oral Pathol. 5:265-276, 1976.
43Landesberg, R., E. Takeuchi, and J. E. Puzas. Cellular, biochemical and molecular characterization of the bovine temporomandibular joint disc. Arch. Oral Biol. 41:761-767, 1996.
44Leenslag, J. W., A. J. Pennings, R. P. H. Veth, H. K. L. Nielsen, and H. W. B. Jansen. A porous composite for reconstruction of meniscus lesions. In: Biological and Biomechanical Performance of Biomaterials: Proceedings of the Fifth European Conference on Biomaterials, Paris, France, September 4–6, 1985, edited by P. Christel, A. Meunier, and A. J. C. Lee, 1986 Amsterdam: Elsevier, 1986, p. 536.
45Maroudas, A. Different ways of expressing concentration of cartilage constituents with special reference to the tissue's organization and functional properties. In: Methods in Cartilage Research, edited by A. Maroudas and K. Kuettner, New York: Academic Press, 1990, pp. 211-212.
46Maroudas, A. Physicochemical properties of articular cartilage. In: Adult Articular Cartilage, edited by M. A. R. Freeman. Kent, England: Pitman Medical, 1979, pp. 215-290.
47Mauck, R. L., M. A. Soltz, C. C. Wang, D. D. Wong, P. H. Chao, W. B. Valhmu, C. T. Hung, and G. A. Ateshian. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J. Biomech. Eng. 122:252-260, 2000.
48McDevitt, C. A., and R. J. Webber. The ultrastructure and biochemistry of meniscal cartilage. Clin. Orthop. 252:8-18, 1990.
49Milam, S. B., R. J. Klebe, R. G. Triplett, and D. Herbert. Characterization of the extracellular matrix of the primate temporomandibular joint. J. Oral Maxillofac. Surg. 49:381-391, 1991.
50Mills, D. K., D. J. Fiandaca, and R. P. Scapino. Morphologic, microscopic, and immunohistochemical investigations into the function of the primate TMJ disc. J. Orofac. Pain 8:136-154, 1994.
51Minarelli, A. M., M. Del Santo Junior, and E. A. Liberti. The structure of the human temporomandibular joint disc: A scanning electron microscopy study. J. Orofac. Pain 11:95-100, 1997.
52Minarelli, A. M., and E. A. Liberti. A microscopic survey of the human temporomandibular joint disc. J. Oral Rehabil. 24:835-840, 1997.
53Miosge, N., K. Flachsbart, W. Goetz, W. Schultz, H. Kresse, and R. Herken. Light and electron microscopical immunohistochemical localization of the small proteoglycan core proteins decorin and biglycan in human knee joint cartilage. Histochem. J. 26:939-945, 1994.
54Mizoguchi, I., P. G. Scott, C. M. Dodd, F. Rahemtulla, Y. Sasano, M. Kuwabara, S. Satoh, S. Saitoh, Y. Hatakeyama, M. Kagayama, and H. Mitani. An immunohistochemical study of the localization of biglycan, decorin and large chondroitin-sulphate proteoglycan in adult rat temporomandibular joint disc. Arch. Oral Biol. 43:889-898, 1998.
55Mow, V. C., D. C. Fithian, and M. A. Kelly. Fundamentals of articular cartilage and meniscus biomechanics. In: Articular and Knee Function: Basic Science and Arthroscopy, edited by J. W. Erwing. New York: Raven Press, 1990, pp. 1-18.
56Mueller, S. M., S. Shortkroff, T. O. Schneider, H. A. Breinan, I. V. Yannas, and M. Spector. Meniscus cells seeded in type I and type II collagen-GAG matrices in vitro. Biomaterials 20:701-709, 1999.
57Muir, I. H. M. Biochemistry. In: Adult Articular Cartilage, edited by M. A. R. Freeman. Tunbridge Wells, England: Pitman Medical, 1979, pp. 145-214.
58Nakano, T., C. M. Dodd, and P. G. Scott. Glycosaminoglycans and proteoglycans from different zones of the porcine knee meniscus. J. Orthop. Res. 15:213-220, 1997.
59Nakano, T., and P. G. Scott. Changes in the chemical composition of the bovine temporomandibular joint disc with age. Arch. Oral Biol. 41:845-853, 1996.
60Nakano, T., and P. G. Scott. A quantitative chemical study of glycosaminoglycans in the articular disc of the bovine temporomandibular joint. Arch. Oral Biol. 34:749-757, 1989.
61Nakata, K., K. Shino, M. Hamada, T. Mae, T. Miyama, H. Shinjo, S. Horibe, K. Tada, T. Ochi, and H. Yoshikawa. Human meniscus cell: Characterization of the primary culture and use for tissue engineering. Clin. Orthop. 391(Suppl):S208-S218, 2001.
62Okazaki, J., A. Kamada, Y. Higuchi, T. Kanabayashi, T. Sakaki, and Y. Gonda. Age changes in the rat temporomandibular joint articular disc: A biochemical study on glycosaminoglycan content. J. Oral Rehabil. 23:536-540, 1996.
63Petersen, W., and B. Tillmann. Collagenous fibril texture of the human knee joint menisci. Anat. Embryol (Berl.) 197:317-324, 1998.
64Poole, A. R., T. Kojima, T. Yasuda, F. Mwale, M. Kobayashi, and S. Laverty. Composition and structure of articular cartilage: a template for tissue repair. Clin. Orthop. 391(Suppl):S26-S33, 2001.
65Poole, A. R., L. C. Rosenberg, A. Reiner, M. Ionescu, E. Bogoch, and P. J. Roughley. Contents and distributions of the proteoglycans decorin and biglycan in normal and osteoarthritic human articular cartilage. J. Orthop. Res. 14:681-689, 1996.
66Poole, A. R., C. Webber, I. Pidoux, H. Choi, and L. C. Rosenberg. Localization of a dermatan sulfate proteoglycan (DS-PGII) in cartilage and the presence of an immunologically related species in other tissues. J. Histochem. Cytochem. 34:619-625, 1986.
67Proctor, C. S., M. B. Schmidt, R. R. Whipple, M. A. Kelly, and V. C. Mow. Material properties of the normal medial bovine meniscus. J. Orthop. Res. 7:771-782, 1989.
68Puelacher, W. C., J. Wisser, C. A. Vacanti, N. F. Ferraro, D. Jaramillo, and J. P. Vacanti. Temporomandibular joint disc replacement made by tissue-engineered growth of cartilage. J. Oral Maxillofac. Surg. 52:1172-1177; Discussion, 1177–1178, 1994.
69Rees, L. A. The structure and function of the mandibular joint. Br. Dent. J. 96:125-133, 1954.
70Rodkey, W. G., J. R. Steadman, and S. T. Li. A clinical study of collagen meniscus implants to restore the injured meniscus. Clin. Orthop. 367(Suppl):S281-S292, 1999.
71Sandell, L. J. Molecular biology of collagens in normal and osteoarthritic cartilage. In: Osteoarthritic Disorders: Workshop, Monterey, California, April 1994, edited by K. E. Kuettner and V. M. Goldberg, Rosemont, IL: American Academy of Orthopaedic Surgeons, 1995, pp. 131-146.
72Scapino, R. P., P. B. Canham, H. M. Finlay, and D. K. Mills. The behaviour of collagen fibres in stress relaxation and stress distribution in the jaw-joint disc of rabbits. Arch. Oral Biol. 41:1039-1052, 1996.
73Scott, P. G., T. Nakano, and C. M. Dodd. Isolation and characterization of small proteoglycans from different zones of the porcine knee meniscus. Biochim. Biophys. Acta 1336:254-262, 1997.
74Scott, P. G., T. Nakano, and C. M. Dodd. Small proteoglycans from different regions of the fibrocartilaginous temporomandibular joint disc. Biochim. Biophys. Acta 1244:121-128, 1995.
75Shengyi, T., and Y. Xu. Biomechanical properties and collagen fiber orientation of TMJ discs in dogs: Part 1. Gross anatomy and collagen fiber orientation of the discs. J. Craniomandib. Disord. 5:28-34, 1991.
76Sindelar, B. J., S. P. Evanko, T. Alonzo, S. W. Herring, and T. Wight. Effects of intraoral splint wear on proteoglycans in the temporomandibular joint disc. Arch. Biochem. Biophys. 379:64-70, 2000.
77Smith, R. L., J. Lin, M. C. Trindade, J. Shida, G. Kajiyama, T. Vu, A. R. Hoffman, M. C. van der Meulen, S. B. Goodman, D. J. Schurman, and D. R. Carter. Time-dependent effects of intermittent hydrostatic pressure on articular chondrocyte type II collagen and aggrecan mRNA expression. J. Rehabil. Res. Dev. 37:153-161, 2000.
78Springer, I. N., B. Fleiner, S. Jepsen, and Y. Acil. Culture of cells gained from temporomandibular joint cartilage on non-absorbable scaffolds. Biomaterials 22:2569-2577, 2001.
79Stockwell, R. A. Biology of Cartilage Cells. Biological Structure and Function, Vol. 7. New York: Cambridge University Press, 1979, viii, 329pp.
80Stone, K. R., W. G. Rodkey, R. Webber, L. McKinney, and J. R. Steadman. Meniscal regeneration with copolymeric collagen scaffolds. In vitro and in vivo studies evaluated clinically, histologically, and biochemically. Am. J. Sports Med. 20:104-111, 1992.
81Sweigart, M. A., and K. A. Athanasiou. Toward tissue engineering of the knee meniscus. Tissue Eng. 7:111-129, 2001.
82Sweigart, M. A., A. C. AufderHeide, and K. A. Athanasiou. Fibrochondrocytes and their use in tissue engineering of the meniscus. In: Topics in Tissue Engineering, edited by N. Ashammakhi and P. Ferretti, E-book, 2003, pp. 1-19, http://www.tissue-engineering-oc.com.
83Tanaka, E., M. Tanaka, Y. Miyawaki, and K. Tanne. Viscoelastic properties of canine temporomandibular joint disc in compressive load-relaxation. Arch. Oral Biol. 44:1021-1026, 1999.
84Tanne, K., E. Tanaka, and M. Sakuda. The elastic modulus of the temporomandibular joint disc from adult dogs. J. Dent. Res. 70:1545-1548, 1991.
85Thomas, M., D. Grande, and R. H. Haug. Development of an in vitro temporomandibular joint cartilage analog. J. Oral Maxillofac. Surg. 49:854-856; Discussion, 857, 1991.
86Tissakht, M., and A. M. Ahmed. Tensile stress-strain characteristics of the human meniscal material. J. Biomech. 28:411-422, 1995.
87Venn, M., and A. Maroudas. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition. Ann. Rheum. Dis. 36:121-129, 1977.
88Verbruggen, G., R. Verdonk, E. M. Veys, P. Van Daele, P. De Smet, K. Van den Abbeele, B. Claus, and D. Baeten. Human meniscal proteoglycan metabolism in long-term tissue culture. Knee Surg. Sports Traumatol. Arthrosc. 4:57-63, 1996.
89Walsh, C. J., D. Goodman, A. I. Caplan, and V. M. Goldberg. Meniscus regeneration in a rabbit partial meniscectomy model. Tissue Eng. 5:327-337, 1999.
90Webber, R. J., M. G. Harris, and A. J. Hough, Jr. Cell culture of rabbit meniscal fibrochondrocytes: proliferative and synthetic response to growth factors and ascorbate. J. Orthop. Res. 3:36-42, 1985.
91Wong, M., P. Wuethrich, P. Eggli, and E. Hunziker. Zone-specific cell biosynthetic activity in mature bovine articular cartilage: A new method using confocal microscopic stereology and quantitative autoradiography. J. Orthop. Res. 14:424-432, 1996.
92Woo, S. L., W. H. Akeson, and G. F. Jemmott. Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. J. Biomech. 9:785-791, 1976.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Almarza, A.J., Athanasiou, K.A. Design Characteristics for the Tissue Engineering of Cartilaginous Tissues. Annals of Biomedical Engineering 32, 2–17 (2004). https://doi.org/10.1023/B:ABME.0000007786.37957.65
Issue Date:
DOI: https://doi.org/10.1023/B:ABME.0000007786.37957.65