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Laminar tendon composites with enhanced mechanical properties

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Abstract

A strong isotropic material that is both biocompatible and biodegradable is desired for many biomedical applications, including rotator cuff repair, tendon and ligament repair, vascular grafting, among others. Recently, we developed a technique, called “bioskiving” to create novel 2D and 3D constructs from decellularized tendon, using a combination of mechanical sectioning, and layered stacking and rolling. The unidirectionally aligned collagen nanofibers (derived from sections of decellularized tendon) offer good mechanical properties to the constructs compared with those fabricated from reconstituted collagen. In this paper, we studied the effect that several variables have on the mechanical properties of structures fabricated from tendon slices, including crosslinking density and the orientation in which the fibers are stacked. We observed that following stacking and crosslinking, the strength of the constructs is significantly improved, with crosslinked sections having an ultimate tensile strength over 20 times greater than non-crosslinked samples, and a modulus nearly 50 times higher. The mechanism of the mechanical failure mode of the tendon constructs with or without crosslinking was also investigated. The strength and fiber organization, combined with the ability to introduce transversely isotropic mechanical properties makes the laminar tendon composites a biocompatible material that may find future use in a number of biomedical and tissue engineering applications.

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References

  1. Derwin KA, Badylak SF, Steinmann SP, Iannotti JP (2010) Extracellular matrix scaffold devices for rotator cuff repair. J Shoulder Elbow Surg 19:467–476

    Article  Google Scholar 

  2. Aurora A, McCarron J, Iannotti JP, Derwin K (2007) Commercially available extracellular matrix materials for rotator cuff repairs: state of the art and future trends. J Shoulder Elbow Surg 16:S171–S178

    Article  Google Scholar 

  3. Coons DA, Barber AF (2006) Tendon graft substitutes-rotator cuff patches. Sports Med Arthrosc 14:185–190

    Article  Google Scholar 

  4. Altman GH, Horan RL, Lu HH, Moreau J, Martin I, Richmond JC, Kaplan DL (2002) Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 23:4131–4141

    Article  Google Scholar 

  5. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen J, Lu H, Richmond J, Kaplan DL (2003) Silk-based biomaterials. Biomaterials 24:401–416

    Article  Google Scholar 

  6. Xu W, Zhou F, Ouyang C, Ye W, Yao M, Xu B (2010) Mechanical properties of small-diameter polyurethane vascular grafts reinforced by weft-knitted tubular fabric. J Biomed Mater Res A 92:1–8

    Article  Google Scholar 

  7. Dahl SLM, Rhim C, Song YC, Niklason LE (2007) Mechanical properties and compositions of tissue engineered and native arteries. Ann Biomed Eng 35:348–355

    Article  Google Scholar 

  8. Dai X, Xu Q (2011) Nanostructured substrate fabricated by sectioning tendon using a microtome for tissue engineering. Nanotechnology 22:494008

    Article  Google Scholar 

  9. Dai X, Schalek R, Xu Q (2011) Staining and Etching: a simple method to fabricate inorganic nanostructures from tissue slices. Adv Mater 24:370–374

    Article  Google Scholar 

  10. Alberti KA, Xu Q (2013) Slicing, stacking and rolling: fabrication of nanostructured collagen constructs from tendon sections. Adv Healthc Mater 2:817–821

    Article  Google Scholar 

  11. Alberti KA, Xu Q (2014) Bioinspired fabrication of nanostructures from tissue slices. In: Jabarri E (ed) Handbook of biomimetics and bioinspiration: biologically-driven engineering of materials, processes, devices and systems. World Scientific Publishing Company, Singapore

    Google Scholar 

  12. Ning LJ, Zhang Y, Chen XH, Luo JC, Li XQ, Yang ZM, Qin TW (2012) Preparation and characterization of decellularized tendon slices for tendon tissue engineering. J Biomed Mater Res A 100:1448–1456

    Article  Google Scholar 

  13. Cartmell JS, Dunn MG (2004) Development of cell-seeded patellar tendon allografts for anterior cruciate ligament reconstruction. Tissue Eng 10:1065–1075

    Article  Google Scholar 

  14. Alberti KA, Hopkins AM, Tang-Schomer MD, Kaplan DL, Xu Q (2014) The behavior of neuronal cells on tendon-derived collagen sheets as potential substrates for nerve regeneration. Biomaterials 35:3551–3557

    Article  Google Scholar 

  15. Qin TW, Chen Q, Sun YL, Steinmann SP, Amadio PC, An KN, Zhao C (2012) Mechanical characteristics of native tendon slices for tissue engineering scaffold. J Biomed Mater Res B Appl Biomater 100:752–758

    Article  Google Scholar 

  16. Cartmell J, Dunn M (2000) Effect of chemical treatments on tendon cellularity and mechanical properties. J Biomed Mater Res 49:134–140

    Article  Google Scholar 

  17. Jayakrishnan A, Jameela SR (1996) Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices. Biomaterials 17:471–484

    Article  Google Scholar 

  18. Dahl SLM, Kypson AP, Lawson JH, Blum JL, Strader JT, Li Y, Manson RJ, Tente WE, DiBernardo L, Hensley MT, Carter R, Williams TP, Prichard HL, Dey MS, Begelman KG, Niklason LE (2011) Readily available tissue-engineered vascular grafts. Sci Transl Med 3:68ra9

    Google Scholar 

  19. Kehoe S, Zhang XF, Boyd D (2011) FDA approved guidance conduits and wraps for peripheral nerve injury: a review of materials and efficacy. Injury 43:553–572

    Article  Google Scholar 

  20. Yamamoto N, Hayashi K, Kuriyama H, Ohno K, Yasuda K, Kaneda K (1992) Mechanical properties of the rabbit patellar tendon. J Biomech Eng 114:332–337

    Article  Google Scholar 

  21. Johnson GA, Tramaglini DM, Levine RE, Ohno K, Choi NY, Woo SL (1994) Tensile and viscoelastic properties of human patellar tendon. J Orthop Res 12:796–803

    Article  Google Scholar 

  22. Wren TA, Yerby SA, Beaupré GS, Carter DR (2001) Mechanical properties of the human achilles tendon. Clin Biomech (Bristol, Avon) 16:245–251

    Article  Google Scholar 

  23. Cheung DT, Perelman N, Ko EC, Nimni ME (1985) Mechanism of crosslinking of proteins by glutaraldehyde III. Reaction with collagen in tissues. Connect Tissue Res 13:109–115

    Article  Google Scholar 

  24. Ber S, Torun Köse G, Hasirci V (2005) Bone tissue engineering on patterned collagen films: an in vitro study. Biomaterials 26:1977–1986

    Article  Google Scholar 

  25. Barnes CP, Pemble CW, Brand DD, Simpson DG, Bowlin GL (2007) Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol. Tissue Eng 13:1593–1605

    Article  Google Scholar 

  26. Brown BN, Barnes CA, Kasick RT, Michel R, Gilbert TW, Beer-Stolz D, Castner DG, Ratner BD, Badylak SF (2010) Surface characterization of extracellular matrix scaffolds. Biomaterials 31:428–437

    Article  Google Scholar 

  27. Dahm M, Lyman WD, Schwell AB, Factor SM, Frater RW (1990) Immunogenicity of glutaraldehyde-tanned bovine pericardium. J Thorac Cardiovasc Surg 99:1082–1090

    Google Scholar 

  28. Liang HC, Chang Y, Hsu CK, Lee MH, Sung HW (2004) Effects of crosslinking degree of an acellular biological tissue on its tissue regeneration pattern. Biomaterials 25:3541–3552

    Article  Google Scholar 

  29. Vidal BDC, Mello MLS (2011) Collagen type I amide I band infrared spectroscopy. Micron 42:283–289

    Article  Google Scholar 

  30. Wang X, Zhang J, Wang Q (2008) Surface modification of GTA crosslinked collagen-based composite scaffolds with low temperature plasma technology. J Macromol Sci Part A 45:585–589

    Article  Google Scholar 

  31. Ocak B (2012) Complex coacervation of collagen hydrolysate extracted from leather solid wastes and chitosan for controlled release of lavender oil. J Environ Manage 100:22–28

    Article  Google Scholar 

  32. Legerlotz K, Riley GP, Screen HRC (2010) Specimen dimensions influence the measurement of material properties in tendon fascicles. J Biomech 43:2274–2280

    Article  Google Scholar 

  33. Buehler MJ (2010) Multiscale mechanics of biological and biologically inspired materials and structures. Acta Mech Solida Sinica 23:471–483

    Article  Google Scholar 

  34. Cox H (1952) The elasticity and strength of paper and other fibrous materials. Br J Appl Phys 3:72

    Article  Google Scholar 

  35. Drzal LT, Madhukar M (1993) Fibre-matrix adhesion and its relationship to composite mechanical properties. J Mater Sci 28:569–610

    Article  Google Scholar 

  36. Garett KW, Bailey JE (1977) Multiple transverse fracture in 90 cross-ply laminates of a glass fiber-reinforced polyester. J Mater Sci 12:157–168

    Article  Google Scholar 

  37. Aveston J, Kelly A (1973) Theory of multiple fracture of fibrous composites. J Mater Sci 8:352–362

    Article  Google Scholar 

  38. Amis AA, Basso O, Johnson DP (2001) The anatomy of the patellar tendon. Knee Surg Sports Traumatol Arthrosc 9:2–5

    Article  Google Scholar 

  39. Provenzano PP, Vanderby R (2006) Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25:71–84

    Article  Google Scholar 

  40. Vinson JR, Sierakowski RL (2006) The behavior of structures composed of composite materials. Springer, Dordrecht

    Google Scholar 

  41. Zimmermann EA, Gludovatz B, Schaible E, Dave NKN, Yang W, Meyers MA, Ritchie RO (2013) Mechanical adaptability of the Bouligand-type structure in natural dermal armour. Nat Commun 4:1–7

    Article  Google Scholar 

  42. Staab G (1999) Laminar composites. Butterworth-Heinemann, Oxford

    Google Scholar 

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Acknowledgements

QX acknowledges Pew Scholar for Biomedical Sciences program from Pew Charitable Trusts and NIH (1R03EB017402-01). KA acknowledges the IGERT fellowship from NSF and a Predoctoral Fellowship from the American Heart Association. This work utilized the facilities at the Harvard University Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Infrastructure Network (NNIN), which is supported by the National Science Foundation under NSF award no. ECS-0335765. We would also like to thank Todd Fritz for the photographs of the tendon sections in Fig. 1.

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The authors declare that there are no conflicts of interest.

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Correspondence to Qiaobing Xu.

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10853_2015_8842_MOESM1_ESM.tif

Supplementary Fig. 1 Tabulated data for: A) crosslinking in Fig. 3, B) pulling angle tests in Fig. 5, and C) stacking angle tests in Fig. 6. Native rat tendon has been shown to have a UTS of 64.1 ± 3.87 MPa and a modulus of 632 ± 51.3 MPa [16] (TIFF 549 kb)

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Alberti, K.A., Sun, JY., Illeperuma, W.R. et al. Laminar tendon composites with enhanced mechanical properties. J Mater Sci 50, 2616–2625 (2015). https://doi.org/10.1007/s10853-015-8842-2

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  • DOI: https://doi.org/10.1007/s10853-015-8842-2

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