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Biomechanical and structural changes following the decellularization of bovine pericardial tissues for use as a tissue engineering scaffold

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Abstract

To achieve natural scaffolds for tissue engineering applications we decellularized bovine pericardial (BP) tissues according to two different protocols: a novel treatment based on Triton® X-100 (12 h, 4 °C) (BP1) and a trypsin/EDTA treatment (37 °C, 48 h) (BP2). Results were compared with commercially available acellular xenogeneic biomaterials, Veritas® and Collamed®. Biomechanical characteristics, high (Eh) and low (El) modulus of elasticity, of the fresh untreated tissue varied with the anatomical direction (apex to base (T) to transverse (L)) (mean ± SDEV): (41.63 ± 14.65–48.12 ± 10.19 MPa and 0.27 ± 0.05–0.30 ± 0.12 MPa respectively). BP1 had no mechanical effect (44.65 ± 19.73–52.67 ± 7.59 MPa and 0.37 ± 0.14–0.37 ± 0.11 MPa, respectively) but BP2 resulted in significant decrease in Eh and El (20.96 ± 8.17–36.82 ± 3.23 MPa and 0.20 ± 0.06–0.23 ± 0.06 MPa). Hysteresis ratio (h) varied (19–26 % of the loading energy) independently of anatomical direction. Glycosaminoglycans content was unaffected by BP1, while 22 % of chondroitin/dermatan sulphate and 60 % of hyaluronan were removed after BP2 treatment. Endothelial cell adhesion was achieved after 24 h and 3 days cell culture.

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References

  1. Steinhoff G, et al. Tissue engineering of pulmonary heart valves on allogenic acellular matrix conduits-in vivo restoration of valve tissue. Circulation. 2000;102:I50–5.

    Google Scholar 

  2. Stock UA, et al. Tissue engineered valved conduits in the pulmonary circulation. J Thorac Cardiovasc Surg. 2000;119:732–40.

    Article  CAS  Google Scholar 

  3. Sodian R, Hoerstrup SP, Sperling JS, Martin DP, Daebritz S, Mayer JE Jr, Vacanti JP. Evaluation of biodegradable, three-dimensional matrices for tissue engineering of heart valves. ASAIO J. 2000;46:107–10.

    Article  CAS  Google Scholar 

  4. Shinoka T. Tissue engineered heart valves: autologous cell seeding on biodegradable polymer scaffold. Artif Organs. 2002;26:402–6.

    Article  Google Scholar 

  5. Jockenhoevel S, et al. Fibrin gel—advantages of a new scaffold in cardiovascular tissue engineering. Eur J Cardiothorac Surg. 2001;19:424–30.

    Article  CAS  Google Scholar 

  6. Flanagan TC. In vivo remodeling and structural characterization of fibrin-based tissue-engineered heart valves in the adult sheep model. Tissue Eng A. 2009;15:2965–76.

    Article  CAS  Google Scholar 

  7. Ravi S, Chaikof EL. Biomaterials for vascular tissue engineering. Regen Med. 2010;5:107–20.

    Article  CAS  Google Scholar 

  8. Badylak SF. Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl Immunol. 2004;12:367–77.

    Article  CAS  Google Scholar 

  9. Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials. 2006;27:3675–83.

    CAS  Google Scholar 

  10. Limpert JN, Desai AR, Kumpf AL, Fallucco MA, Aridge DL. Repair of abdominal wall defects with bovine pericardium. Am J Surg. 2009;198:e60–5.

    Article  Google Scholar 

  11. Canda AE, Karaca A. Incisional hernia in action: the use of vacuum-assisted closure and porcine dermal collagen implant. Hernia. 2009;13:651–5.

    Article  CAS  Google Scholar 

  12. Badylak SF. The extracellular matrix as a biologic scaffold material. Biomaterials. 2007;28:3587–93.

    Article  CAS  Google Scholar 

  13. Mendoza-Novelo B, Avila EE, Cauich-Rodríguez JV, Jorge-Herrero E, Rojo FJ, Guinea GV, Mata-Mata JL. Decellularization of pericardial tissue and its impact on tensile viscoelasticity and glycosaminoglycan content. Acta Biomater. 2011;7:1241–8.

    Article  CAS  Google Scholar 

  14. Rieder E, et al. Tissue engineering of heart valves: decellularized porcine and human valve scaffolds differ importantly in residual potential to attract monocytic cells. Circulation. 2005;111:2792–7.

    Article  Google Scholar 

  15. Schmidt CE, Baier JM. Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials. 2000;21:2215–31.

    Article  CAS  Google Scholar 

  16. Doss M, Moid R, Wood JP, Miskovic A, Martens S, Moritz A. Pericardial patch augmentation for reconstruction of incompetent bicuspid aortic valves. Ann Thorac Surg. 2005;80:304–7.

    Article  Google Scholar 

  17. Mavrilas D, Sinouris EA, Vynios DH, Papageorgakopoulou N. Dynamic mechanical characteristics of intact and structurally modified bovine pericardial tissues. J Biomech. 2005;38:761–8.

    Article  CAS  Google Scholar 

  18. Iozzo RV, Murdoch AD. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB J. 1996;10:598–614.

    CAS  Google Scholar 

  19. Wilson GJ, Courtman DW, Klement P, Lee JM, Yeger H. Acellular matrix: a biomaterials approach for coronary artery bypass and heart valve replacement. Ann Thorac Surg. 1995;60:S353–8.

    Article  CAS  Google Scholar 

  20. Bader A, Schilling T, Teebken OE, Brandes G, Herden T, Steinhoff G, Haverich A. Tissue engineering of heart valves—human endothelial cell seeding of detergent acellularized porcine valves. Eur J Cardiothorac Surg. 1998;14:279–84.

    Article  CAS  Google Scholar 

  21. Bertipaglia B, et al. Cell characterization of porcine aortic valve and decellularized leaflets repopulated with aortic valve interstitial cells. Ann Thorac Surg. 2003;75:1274–82.

    Article  Google Scholar 

  22. Korossis SA, Booth C, Wilcox HE, Watterson KG, Kearney JN, Fisher J, Ingham E. Tissue engineering of cardiac valve prostheses II: biomechanical characterization of decellularized porcine aortic heart valves. J Heart Valve Dis. 2002;11:463–71.

    Google Scholar 

  23. Liao J, Joyce EM, Sacks MS. Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet. Biomaterials. 2008;29:1065–74.

    Article  CAS  Google Scholar 

  24. Cebotari S, et al. Construction of autologous human heart valves based on an acellular allograft matrix. Circulation. 2002;106:I63–8.

    Google Scholar 

  25. Patton JH Jr, Berry S, Kralovich KA. Use of human acellular dermal matrix in complex and contaminated abdominal wall reconstructions. Am J Surg. 2007;193:360–3.

    Article  Google Scholar 

  26. Catena F, Ansaloni L, Gazzotti F, Gagliardi S, Di Saverio S, D’Alessandro L, Pinna AD. Use of porcine dermal collagen graft for hernia repair in contaminated fields. Hernia. 2007;11:57–60.

    Article  CAS  Google Scholar 

  27. Kim H, Bruen K, Vargo D. Acellular dermal matrix in the management of high-risk abdominal wall defects. Am J Surg. 2006;192:705–9.

    Article  Google Scholar 

  28. Papadas TA. Alterations in the content and composition of glycosaminoglycans in human laryngeal carcinoma. Acta Otolaryngol. 2002;122:330–7.

    Article  CAS  Google Scholar 

  29. Reddy GK, Enwemeka CS. A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem. 1996;29:225–9.

    Article  CAS  Google Scholar 

  30. Fung YC. Elasticity of soft tissues in simple elongation. Am J Physiol. 1967;213:1532–44.

    CAS  Google Scholar 

  31. Anssari-Benam A, Bader DL, Screen HR. A combined experimental and modelling approach to aortic valve viscoelasticity in tensile deformation. J Mater Sci Mater Med. 2011;22:253–62.

    Article  CAS  Google Scholar 

  32. Shah SR, Vyavahare NR. The effect of glycosaminoglycan stabilization on tissue buckling in bioprosthetic heart valves. Biomaterials. 2008;29:1645–53.

    Article  CAS  Google Scholar 

  33. Sacks MS. Biaxial mechanical evaluation of planar biological materials. J Elast. 2000;61:199–246.

    Article  Google Scholar 

  34. Braga-Vilela AS, Pimentel ER, Marangoni S, Toyama MH, de Campos Vidal B. Extracellular matrix of porcine pericardium: biochemistry and collagen architecture. J Membr Biol. 2008;221:15–25.

    Article  CAS  Google Scholar 

  35. Simionescu D, Iozzo RV, Kefalides NA. Bovine pericardial proteoglycan: biochemical, immunochemical and ultrastructural studies. Matrix. 1989;9:301–10.

    Article  CAS  Google Scholar 

  36. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol. 1997;136:729–43.

    Article  CAS  Google Scholar 

  37. Winnemöller M, Schmidt G, Kresse H. Influence of decorin on fibroblast adhesion to fibronectin. Eur J Cell Biol. 1991;54:10–7.

    Google Scholar 

  38. Coleman PJ. Evidence for a role of hyaluronan in the spacing of fibrils within collagen bundles in rabbit synovium. Biochim Biophys Acta. 2002;1571:173–82.

    Article  CAS  Google Scholar 

  39. Bos KJ, Holmes DF, Meadows RS, Kadler KE, McLeod D, Bishop PN. Collagen fibril organisation in mammalian vitreous by freeze etch/rotary shadowing electron microscopy. Micron. 2001;32:301–6.

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partly supported by University of Patras research committee grand “K. Karatheodoris” #B711. We thank Synovis Surgical Innovations S.A., USA and Diophar S.A., GR for supplying Veritas® biomaterial for testing.

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Authors and Affiliations

  1. Laboratory of Biomechanics & Biomedical Engineering, Department of Mechanical Engineering & Aer/tics, University of Patras, 26500, Patras, Greece

    Eirini Pagoulatou, Despina Deligianni & Dimosthenis Mavrilas

  2. Laboratory of Biochemistry, Department of Chemistry, University of Patras, Rion, 26500, Patras, Greece

    Irene-Eva Triantaphyllidou & Demitrios H. Vynios

  3. Department of Anatomy-Histology-Embryology, University of Patras, Rion, 26500, Patras, Greece

    Dionysios J. Papachristou

  4. Department of Cardiothoracic Surgery, University of Patras, Rion, 26500, Patras, Greece

    Efstratios Koletsis

  5. Department of Pathology, University of Pittsburgh, Pittsburgh, PA, USA

    Dionysios J. Papachristou

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  1. Eirini Pagoulatou
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  2. Irene-Eva Triantaphyllidou
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  3. Demitrios H. Vynios
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  4. Dionysios J. Papachristou
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  6. Despina Deligianni
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  7. Dimosthenis Mavrilas
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Correspondence to Dimosthenis Mavrilas.

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Pagoulatou, E., Triantaphyllidou, IE., Vynios, D.H. et al. Biomechanical and structural changes following the decellularization of bovine pericardial tissues for use as a tissue engineering scaffold. J Mater Sci: Mater Med 23, 1387–1396 (2012). https://doi.org/10.1007/s10856-012-4620-8

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  • DOI: https://doi.org/10.1007/s10856-012-4620-8

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