Abstract
Various methods have been tried to treat the main meniscus problem, meniscal tears, for which we believe tissue engineering could be a viable solution. In this study, a three dimensional, collagen-based meniscus substitute was prepared by tissue engineering using human fibrochondrocytes and a collagen based-scaffold. This construct was made with 3 different collagen-based foams interspaced with two electrospun nano/microfibrous mats. The top layer was made of collagen type I–chondroitin sulfate–hyaluronic acid (Coll–CS–HA), and the middle and the bottom layers were made of only collagen type I with different porosities and thus with different mechanical properties. The mats of aligned fibers were a blend of collagen type I and poly(l-lactic acid-co-glycolic acid) (PLGA). After seeding with human fibrochondrocytes, cell attachment, proliferation, and production of extracellular matrix and glucoseaminoglycan were studied. Cell seeding had a positive effect on the compressive properties of foams and the 3D construct. The 3D construct with all its 5 layers had better mechanical properties than the individual foams.
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References
Newman AP, Anderson DR, Daniel AU, Dales MC. Mechanics of the healed meniscus in a canine model. Am J Sports Med. 1989;17:164–75.
Proctor CS, Schmidt MB, Whipple RR, Kelly MA, Mow VC. Material properties of the normal medial bovine meniscus. J Orthop Res. 1989;7:771–2.
Fithian DC, Kelly MA, Mow VC. Material properties and structure–function relationships in the menisci. Clin Orthop Relat Res. 1990;252:19–31.
Zhu W, Chern KY, Mow VC. Anisotropic viscoelastic shear properties of bovine meniscus. Clin Orthop Relat Res. 1994;306:34–45.
Lee J, Fu F. The meniscus: basic science and clinical applications. Oper Tech Orthop. 2000;10:162–8.
Makris EA, Hadidi P, Athanasiou KA. The knee meniscus: structure–function, pathophysiology, current repair techniques, and prospects for regeneration. Biomaterials. 2011;32:7411–31.
Mandal BB, Park S-H, Gil ES, Kaplan DL. Multilayered silk scaffolds for meniscus tissue engineering. Biomaterials. 2011;32:639–51.
Tan G-K, Dinnes DLM, Myers PT, Cooper-White JJ. Effects of biomimetic surfaces and oxygen tension on redifferentiation of passaged human fibrochondrocytes in 2D and 3D cultures. Biomaterials. 2012;32:5600–14.
Kon E, Filardo G, Tschon M, Fini M, Giavaresi G, Reggiani LM, Chiari C, Nehrer S, Martin I, Salter DM, Ambrosio L, Marcacci M. Tissue engineering for total meniscus substitution: animal study in sheep model—results at 12 months. Tissue Eng. 2012;18(15):1–10.
Fairbank TJ. Knee joint changes after meniscectomy. J Bone Joint Surg Br. 1948;30B:664–70.
Rath E, Richmond JC. The menisci: basic science and advances in treatment. Br J Sports Med. 2000;34:252–7.
Englund M, Roos EM, Lohmander LS. Impact of type of meniscal tear on radiographic and symptomatic knee osteoarthritis: a sixteen-year follow up of meniscectomy with matched controls. Arthritis Rheum. 2003;48:2178–87.
Bertiaume MJ, Raynauld JP, Martel-Pelletier J, Labonte F, Beadoin G, Bloch DA, Choquette D, Haraoui B, Altman R, Hochberg M, Meyer J, Cline G, Pelletier J. Meniscal tear and extrusion are strongly associated with progression of symptomatic knee osteoarthritis as assessed by quantitative magnetic resonance imaging. Ann Rheum Dis. 2005;64:556–63.
Rodkey WG, DeHaven KE, Montgomery WH III, Baker CL, Beck CL, Hornel SE, Steadman JR, Cole BJ, Briggs KK. Comparison of the collagen meniscus implant with partial meniscectomy. A prospective randomized trial. J Bone Joint Surg Am. 2008;90(7):1413–26.
Mouzopoulos G, Siebold R. Partial meniscus substitution with tissue engineered scaffold: an overview. Clin Sports Med. 2012;31:167–81.
Cui X, Hasegawa A, Lotz M, D’Lima D. Structured three-dimensional co-culture of mesenchymal stem cells with meniscus cells promotes meniscal phenotypes without hypertrophy. Biotechnol Bioeng. 2012;109(9):2369–80.
Sweigart MA, Athanasiou KA. Toward tissue engineering of the knee meniscus. Tissue Eng. 2001;7:111–29.
Buma P, Ramrattan NN, van Tienen TG, Veth Rene PH. Tissue engineering of the meniscus. Biomaterials. 2004;25:1523–32.
McDermott ID. Mini-symposium: soft tissue knee problems: (ii) meniscal tears. Curr Orthop. 2006;20:85–93.
Hoben GM, Athanasiou KA. Meniscus repair with fibrocartilage engineering. Sports Med Arthrosc. 2006;14:129–37.
Angele P, Johnstone B, Kujat R, Zellner J, Nerlich M, Goldberg V, Yoo J. Stem cell based tissue engineering for meniscus repair. J Biomed Res A. 2007;85:445–55.
Schoenfeld AJ, Landis WJ, Kay DB. Tissue-engineered meniscal constructs. Am J Orthop. 2007;36:614–20.
van der Bracht H, Verdonk R, Verbruggen G, Elewaut D, Verdonk P. Cell-based meniscus tissue engineering. In: Ashammakhi N, Reis RL, Chiellini E, editors. Topics in tissue engineering, vol 3, chap 2; 2007 (e-book).
Drengk A, Stürmer KM, Frosch K-H. Current concepts in meniscus tissue engineering. Curr Rheum Rev. 2008;4:196–201.
Toyonaga T, Uezaki N, Chikama H. Substitute meniscus of Teflon-net for the knee joint of dogs. Clin Orthop. 1983;179:291–7.
Veth RP, Jansen HW, Leenslag JW, Pennings AJ, Hartel RM, Nielsen HK. Experimental meniscal lesions reconstructed with a carbon fiber–polyurethane–poly(l-lactide) graft. Clin Orthop. 1986;202:286–93.
Leenslag JW, Pennings AJ, Veth RPH, Nielsen HKL, Jansen HWB. A porous composite for reconstruction of meniscus lesions. In: Christel P, Meunier A, Lee AJC, editors. Biological and biomechanical performance of biomaterials. Amsterdam: Elsevier Science Publishers; 1986. p. 147.
Webber RJ. In vitro culture of meniscal tissue. Clin Orthop. 1990;252:114–20.
Ibarra C, Koski JA, Warren RF. Tissue engineering meniscus: cells and matrix. Orthop Clin North Am. 2000;31:411–8.
Kobayashi M, Toguchida J, Oka M. Development of an artificial meniscus using polyvinyl alcohol hydrogel for early return to, and continuance of, athletic life in sportspersons with severe meniscus injury, I: mechanical evaluation. Knee. 2003;10:47–51.
Kang S-W, Son S-M, Lee J-S, Lee ES, Lee K-Y, Park S-G, Park J-H, Kim B-S. Regeneration of whole meniscus using meniscal cells and polymeric scaffolds in a rabbit total meniscectomy model. J Biomed Mater Res A. 2006;77A:659–71.
Cook JL, Tomlinson JL, Kreeger JM, Cook CR. Induction of meniscal regeneration in dogs using a novel biomaterial. Am J Sports Med. 1999;27:658–65.
Gastel JA, Muirhead WR, Lifrak JT, Fadale PD, Hulstyn MJ, Labrador DP. Meniscal tissue regeneration using a collagenous biomaterial derived from porcine small intestine submucosa. Arthroscopy. 2001;17:151–9.
Walsh CJ, Goodman D, Caplan AI, Goldberg VM. Meniscus regeneration in a rabbit partial meniscectomy model. Tissue Eng. 1999;5:327–37.
Bruns J, Kahrs J, Kampen J, Behrens P, Plitz W. Autologous perichondral tissue for meniscal replacement. J Bone Joint Surg Br. 1998;80:918–23.
Stone KR. Meniscus replacement. Clin Sports Med. 1996;15:557–71.
Stone KR, Steadman JR, Rodkey WG, Li ST. Regeneration of meniscal cartilage with use of a collagen scaffold. Analysis of preliminary data. J Bone Joint Surg Am. 1997;79:1770–7.
Linke R, Ulmer M, Imhoff A. Replacement of the meniscus with a collagen implant (CMI). Oper Orthop Traumatol. 2006;18(5–6):453–62.
de Groot J. Actifit, polyurethane meniscus implant: basic science. In: Beaufils P, Verdonk R, editors. The meniscus. Heidelberg: Springer; 2010. p. 383–7.
Halili Ndreu A, Hasirci N, Hasirci V. A mechanically functional collagen-based construct designed as a meniscus substitute. J Biomater Tissue Eng. 2013;3:178–84.
Mossman T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63.
Kinikoglu B, Rodríguez-Cabello JC, Damour O, Hasirci V. The influence of elastin-like recombinant polymer on the self-renewing potential of a 3D tissue equivalent derived from human lamina propria fibroblasts and oral epithelial cells. Biomaterials. 2011;32(25):5756–64.
Harley BA, Leung JH, Silva ECCM, Gibson LJ. Mechanical characterization of collagen–glucosaminoglycan scaffolds. Acta Biomater. 2007;3:463–74.
Hellio Le Graverand M-P, Ou Y, Schield-Yee T, Barclay L, Hart D, Natsume T, Rattner JB. The cells of the rabbit meniscus: their arrangement, interrelationship, morphological variations and cytoarchitecture. J Anat. 2001;198:525–35.
Athanasiou KA, Sanchez-Adams J. Engineering the knee meniscus. In: Synthesis lectures on tissue engineering. San Rafael: Morgan and Claypool Publishers; 2009 (e-book).
Wildey GM, McDevitt CA. Matrix protein mRNA levels in canine meniscus cells in vitro. Arch Biochem Biophys. 1998;353(1):10–5.
Verdonk PCM, Forsyth RG, Wang J, Almqsvist KF, Verdonk R. Characterisation of human knee meniscus cell phenotype. Osteoarthritis Cartilage. 2005;13:548–60.
Suzuki Y, Takeuchi N, Sagelashi Y, Yamaguchi T, Itoh H, Iwata H. Effects of hyaluronic acid on meniscal injury in rabbits. Arch Orthop Trauma Surg. 1998;117:303–6.
Kon E, Chiari C, Marcacci M, Delcogliano M, Salter DM, Martin I, Ambrosio L, Fini M, Tschon M, Tognana E, Plasenzotti R, Nehrer S. Tissue engineering for total meniscal substitution: animal study in sheep model. Tissue Eng A. 2008;14(6):1067–80.
Keogh MB, O’Brien FJ, Daly JS. Substrate stiffness and contractile behavior modulate the functional maturation of osteoblasts on Coll–GAG scaffold. Acta Biomater. 2010;6:4305–13.
Webber RJ, Zitaglio T, Hough AJ. In vitro cell proliferation and proteoglycan synthesis of rabbit meniscal fibrochondrocytes as a function of age and sex. Arthritis Rheum. 1986;29(8):1010–6.
Basalo IM, Mauck RL, Kelly TA, Nicoll SB, Chen FH, Hung CT, Ateshian GA. Cartilage interstitial fluid load support in unconfined compression following enzymatic digestion. J Biomech Eng. 2004;126:779–86.
Wilson CG, Vanderploeg EJ, Zuo F, Sandy JD, Levenston ME. Aggrecanolysis and in vitro matrix degradation in the immature bovine meniscus: mechanisms and functional implications. Arthritis Res Ther. 2009;11(6):R173.
Nerurkar NL, Han W, Mauck RL, Elliott DL. Homologous structure-function relationships between native fibrocartilage and tissue engineered from MSC-seeded nanofibrous scaffolds. Biomaterials. 2011;32:461–8.
Zorlutuna P, Elsheikh A, Hasirci V. Nanopatterning of collagen scaffolds improve the mechanical properties of tissue engineered vascular grafts. Biomacromolecules. 2009;10:814–21.
Le-P Yan, Oliviera JM, Oliviera AL, Caridade SG, Mano JF, Reis RL. Macro/microporous silk fibroin scaffolds with potential for articular cartilage and meniscus tissue engineering applications. Acta Biomater. 2012;8:289–301.
Acknowledgments
Ministry of Industry and Commerce of Turkey (SanTez project No. 00356.STZ.2009-1), and TUBITAK (Program: 2215) who supported this study and Dr. A. Ndreu Halili are gratefully acknowledged. We would also like to thank Dr. A. Kiziltay for her contribution through mechanical testing and acknowledge Kocaeli University KÖGEM (Center for Stem Cell and Gene Therapies Research and Practice) for performing flow cytometry analysis.
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Halili, A.N., Hasirci, N. & Hasirci, V. A multilayer tissue engineered meniscus substitute. J Mater Sci: Mater Med 25, 1195–1209 (2014). https://doi.org/10.1007/s10856-014-5145-0
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DOI: https://doi.org/10.1007/s10856-014-5145-0