Biomechanical evaluation of suture-holding properties of native and tissue-engineered articular cartilage

Biomechanics and Modeling in Mechanobiology - Tập 14 - Trang 73-81 - 2014
G. D. DuRaine1, B. Arzi1,2, J. K. Lee1, C. A. Lee3, D. J. Responte1, J. C. Hu1, K. A. Athanasiou1,3
1Department of Biomedical Engineering, College of Engineering, University of California Davis, Davis, USA
2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California Davis, Davis, USA
3Department of Orthopaedic Surgery, School of Medicine, University of California Davis Medical Center, Sacramento, USA

Tóm tắt

The purpose of this study was to determine suture-holding properties of tissue-engineered neocartilage relative to native articular cartilage. To this end, suture pull-out strength was quantified for native articular cartilage and for neocartilages possessing various mechanical properties. Suture-holding properties were examined in vitro and in vivo. Neocartilage from bovine chondrocytes was engineered using two sets of exogenous stimuli, resulting in neotissue of different biochemical compositions. Compressive and tensile properties and glycosaminoglycan, collagen, and pyridinoline cross-link contents were assayed (study 1). Suture pull-out strength was compared between neocartilage constructs, and bovine and leporine native cartilage. Uniaxial pull-out test until failure was performed after passing 6-0 Vicryl through each tissue (study 2). Subsequently, neocartilage was implanted into a rabbit model to examine short-term suture-holding ability in vivo (study 3). Neocartilage glycosaminoglycan and collagen content per wet weight reached $$4.55 \pm 1.62\,\%$$ and $$4.21 \pm 0.77\,\%$$ , respectively. Tensile properties for neocartilage constructs reached $$2.6 \pm 0.77$$  MPa for Young’s modulus and $$1.39 \pm 0.63$$  MPa for ultimate tensile strength. Neocartilage reached $$\sim $$ 33 % of suture pull-out strength of native articular cartilage. Neocartilage cross-link content reached 50 % of native values, and suture pull-out strength correlated positively with cross-link content $$(R^{2}=0.74)$$ . Neocartilage sutured into rabbit osteochondral defects was successfully maintained for 3 weeks. This study shows that pyridinoline cross-links in neocartilage may be vital in controlling suture pull-out strength. Neocartilage produced in vitro with one-third of native tissue pull-out strength appears sufficient for construct suturing and retention in vivo.

Tài liệu tham khảo

Asanbaeva A, Masuda K, Thonar EJ, Klisch SM, Sah RL (2008) Cartilage growth and remodeling: modulation of balance between proteoglycan and collagen network in vitro with beta-aminopropionitrile. Osteoarthr Cartil 16(1):1–11. doi:10.1016/j.joca.2007.05.019 Athanasiou KA, Rosenwasser MP, Buckwalter JA, Malinin TI, Mow VC (1991) Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J Orthop Res 9(3):330–340. doi:10.1002/jor.1100090304 Athanasiou KA, Agarwal A, Dzida FJ (1994) Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. J Orthop Res 12(3):340–349. doi:10.1002/jor.1100120306 Aufderheide AC, Athanasiou KA (2007) Assessment of a bovine co-culture, scaffold-free method for growing meniscus-shaped constructs. Tissue Eng 13(9):2195–2205. doi:10.1089/ten.2006.0291 Elder BD, Athanasiou KA (2008) Synergistic and additive effects of hydrostatic pressure and growth factors on tissue formation. PLoS One 3(6):e2341. doi:10.1371/journal.pone.0002341 Elder BD, Athanasiou KA (2009a) Effects of temporal hydrostatic pressure on tissue-engineered bovine articular cartilage constructs. Tissue Eng Part A 15(5):1151–1158. doi:10.1089/ten.tea.2008.0200 Elder BD, Athanasiou KA (2009b) Hydrostatic pressure in articular cartilage tissue engineering: from chondrocytes to tissue regeneration. Tissue Eng Part B Rev 15(1):43–53. doi:10.1089/ten.teb.2008.0435 Elder BD, Athanasiou KA (2009c) Systematic assessment of growth factor treatment on biochemical and biomechanical properties of engineered articular cartilage constructs. Osteoarthr Cartil 17(1):114–123. doi:10.1016/j.joca.2008.05.006 Eleswarapu SV, Responte DJ, Athanasiou KA (2011) Tensile properties, collagen content, and crosslinks in connective tissues of the immature knee joint. PLoS One 6(10):e26178. doi:10.1371/journal.pone.0026178 Eyre DR, Dickson IR, Van Ness K (1988) Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J 252(2):495–500 Farhadi J, Fulco I, Miot S, Wirz D, Haug M, Dickinson SC, Hollander AP, Daniels AU, Pierer G, Heberer M, Martin I (2006) Precultivation of engineered human nasal cartilage enhances the mechanical properties relevant for use in facial reconstructive surgery. Ann Surg 244(6):978–985. doi:10.1097/01.sla.0000247057.16710.be discussion 985 Fry P, Harkness ML, Harkness RD, Nightingale M (1962) Mechanical properties of tissues of lathyritic animals. J Physiol 164:77–89 Hu JC, Athanasiou KA (2006) A self-assembling process in articular cartilage tissue engineering. Tissue Eng 12(4):969–979 Huey DJ, Athanasiou KA (2011a) Maturational growth of self-assembled, functional menisci as a result of TGF-beta1 and enzymatic chondroitinase-ABC stimulation. Biomaterials 32(8):2052–2058. doi:10.1016/j.biomaterials.2010.11.041 Huey DJ, Athanasiou KA (2011b) Tension-compression loading with chemical stimulation results in additive increases to functional properties of anatomic meniscal constructs. PLoS One 6(11):e27857. doi:10.1371/journal.pone.0027857 Hunziker EB, Stahli A (2008) Surgical suturing of articular cartilage induces osteoarthritis-like changes. Osteoarthr Cartil 16(9):1067–1073. doi:10.1016/j.joca.2008.01.009 Mow VC, Gibbs MC, Lai WM, Zhu WB, Athanasiou KA (1989) Biphasic indentation of articular cartilage-II. A numerical algorithm and an experimental study. J Biomech 22(8–9):853–861 Murphy MK, DuRaine GD,Reddi A, Hu JC, Athanasiou KA (2013) Inducing articular cartilage phenotype in costochondral cells. Arthritis Res Ther 15(6): R214. doi:10.1186/ar4409 Mustarde JC (1978) Correction of prominent ears using buried mattress sutures. Clin Plast Surg 5(3):459–464 Natoli RM, Responte DJ, Lu BY, Athanasiou KA (2009a) Effects of multiple chondroitinase ABC applications on tissue engineered articular cartilage. J Orthop Res 27(7):949–956. doi:10.1002/jor.20821 Natoli RM, Revell CM, Athanasiou KA (2009b) Chondroitinase ABC treatment results in greater tensile properties of self-assembled tissue-engineered articular cartilage. Tissue Eng Part A 15(10):3119–3128. doi:10.1089/ten.TEA.2008.0478 Responte DJ, Natoli RM, Athanasiou KA (2007) Collagens of articular cartilage: structure, function, and importance in tissue engineering. Crit Rev Biomed Eng 35(5):363–411 Strehin I, Nahas Z, Arora K, Nguyen T, Elisseeff J (2010) A versatile pH sensitive chondroitin sulfate-PEG tissue adhesive and hydrogel. Biomaterials 31(10):2788–2797. doi:10.1016/j.biomaterials.2009.12.033 Toriumi DM, Tardy ME (1995) Cartilage suturing techniques for correction of nasal tip deformities. Oper Tech Otolaryngol Head Neck Surg 6(4):265–273 Trowbridge EA, Lawford PV, Crofts CE (1989) Pericardial heterografts: a comparative study of suture pull-out and tissue strength. J Biomed Eng 11(4):311–314 Williamson AK, Chen AC, Masuda K, Thonar EJ, Sah RL (2003a) Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J Orthop Res 21(5):872–880. doi:10.1016/S0736-0266(03)00030-5 Williamson AK, Masuda K, Thonar EJ, Sah RL (2003b) Growth of immature articular cartilage in vitro: correlated variation in tensile biomechanical and collagen network properties. Tissue Eng 9(4):625–634. doi:10.1089/107632703768247322 Woessner JF Jr (1961) The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93:440–447