Tissue Engineering Human Small-Caliber Autologous Vessels Using a Xenogenous Decellularized Connective Tissue Matrix Approach: Preclinical Comparative Biomechanical Studies
Corresponding Author
Jörg Heine
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Department of Oral, Craniomaxillofacial, and Facial Plastic Surgery, University Hospital Schleswig-Holstein Campus Kiel, Kiel
Dr. Jörg Heine, Department of Oral, Craniomaxillofacial, and Facial Plastic Surgery, University Hospital Schleswig-Holstein Campus Kiel, Arnold-Heller Str. 16, 24105 Kiel, Germany. E-mail: [email protected]Search for more papers by this authorAndreas Schmiedl
Department of Functional and Applied Anatomy, Hannover Medical School, Hannover
Search for more papers by this authorSerghei Cebotari
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Search for more papers by this authorMatthias Karck
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Department of Cardiac Surgery, University Hospital Heidelberg, Heidelberg
Search for more papers by this authorHeike Mertsching
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Fraunhofer IGB Stuttgart, Stuttgart, Germany
Search for more papers by this authorAxel Haverich
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Search for more papers by this authorKlaus Kallenbach
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Department of Cardiac Surgery, University Hospital Heidelberg, Heidelberg
Search for more papers by this authorCorresponding Author
Jörg Heine
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Department of Oral, Craniomaxillofacial, and Facial Plastic Surgery, University Hospital Schleswig-Holstein Campus Kiel, Kiel
Dr. Jörg Heine, Department of Oral, Craniomaxillofacial, and Facial Plastic Surgery, University Hospital Schleswig-Holstein Campus Kiel, Arnold-Heller Str. 16, 24105 Kiel, Germany. E-mail: [email protected]Search for more papers by this authorAndreas Schmiedl
Department of Functional and Applied Anatomy, Hannover Medical School, Hannover
Search for more papers by this authorSerghei Cebotari
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Search for more papers by this authorMatthias Karck
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Department of Cardiac Surgery, University Hospital Heidelberg, Heidelberg
Search for more papers by this authorHeike Mertsching
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Fraunhofer IGB Stuttgart, Stuttgart, Germany
Search for more papers by this authorAxel Haverich
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Search for more papers by this authorKlaus Kallenbach
Department of Cardiovascular and Thoracic Surgery, Hannover Medical School
Leibniz Research Laboratory for Biotechnology and Artificial Organs (LEBAO)
Department of Cardiac Surgery, University Hospital Heidelberg, Heidelberg
Search for more papers by this authorAbstract
Suggesting that bioartificial vascular scaffolds cannot but tissue-engineered vessels can withstand biomechanical stress, we developed in vitro methods for preclinical biological material testings. The aim of the study was to evaluate the influence of revitalization of xenogenous scaffolds on biomechanical stability of tissue-engineered vessels. For measurement of radial distensibility, a salt-solution inflation method was used. The longitudinal tensile strength test (DIN 50145) was applied on bone-shaped specimen: tensile/tear strength (SigmaB/R), elongation at maximum yield stress/rupture (DeltaB/R), and modulus of elasticity were determined of native (NAs; n = 6), decellularized (DAs; n = 6), and decellularized carotid arteries reseeded with human vascular smooth muscle cells and human vascular endothelial cells (RAs; n = 7). Radial distensibility of DAs was significantly lower (113%) than for NAs (135%) (P < 0.001) or RAs (127%) (P = 0.018). At levels of 120 mm Hg and more, decellularized matrices burst (120, 160 [n = 2] and 200 mm Hg). Although RAs withstood levels up to 300 mm Hg, ANOVA revealed a significant difference from NA (P = 0.018). Compared with native vessels (NAs), SigmaB/R values were lower in DAs (44%; 57%) (P = 0.014 and P = 0.002, respectively) and were significantly higher in RAs (71%; 83%) (both P < 0.001). Similarly, DeltaB/R values were much higher in DAs compared with NAs (94%; 88%) (P < 0.001) and RAs (87%; 103%) (P < 0.001), but equivalent in NAs and RAs. Modulus of elasticity (2.6/1.1/3.7 to 16.6 N/mm2) of NAs, DAs, RAs was comparable (P = 0.088). Using newly developed in vitro methods for small-caliber vascular graft testing, this study proved that revitalization of decellularized connective tissue scaffolds led to vascular graft stability able to withstand biomechanical stress mimicking the human circulation. This tissue engineering approach provides a sufficiently stable autologized graft.
REFERENCES
- 1 Tiwari A, Salacinski HJ, Hamilton G, Seifalian AM. Tissue engineering of vascular bypass grafts: role of endothelial cell extraction. Eur J Vasc Endovasc Surg 2001; 21: 193–201.
- 2 Nakayama Y, Ishibashi-Ueda H, Takamizawa K. In vivo tissue-engineered small-caliber arterial graft prosthesis consisting of autologous tissue (biotube). Cell Transplant 2004; 13: 439–49.
- 3 Niklason LE, Gao J, Abbott WM, et al. Functional arteries grown in vitro. Science 1999; 284: 489–93.
- 4 McFetridge PS, Daniel JW, Bodamyali T, Horrocks M, Chaudhuri JB. Preparation of porcine carotid arteries for vascular tissue engineering applications. J Biomed Mater Res A 2004; 70: 224–34.
- 5 L'Heureux N, Paquet S, Germain L, Labbe R, Auger FA. A completely biological tissue-engineered human blood vessel. FASEB J 1998; 12: 47–56.
- 6 Wang XN, Chen CZ, Yang M, Gu YJ. Implantation of decellularized small-caliber vascular xenografts with and without surface heparin treatment. Artif Organs 2007; 31: 99–104.
- 7 Cai WW, Gu YJ, Wang XN, Chen CZ. Heparin coating of small-caliber decellularized xenografts reduces macrophage infiltration and intimal hyperplasia. Artif Organs 2009; 33: 448–55.
- 8 Wilson GJ, Yeger H, Klement P, Lee JM, Courtman DW. Acellular matrix allograft small caliber vascular protheses. ASAIO Trans 1990; 36: M340–3.
- 9 Bader A, Schilling T, Teebken OE, et al. Tissue engineering of heart valves—human endothelial cell seeding of detergent acellularized porcine valves. Eur J Cardiothorac Surg 1998; 14: 279–84.
- 10 Liu SQ. Biomechanical basis of vascular tissue engineering. Crit Rev Biomed Eng 1999; 27: 75–148.
- 11 Schmitz-Rixen T, Hamilton G. Compliance—a critical parameter in maintenance of arterial reconstruction? In: RM Greenhalgh, L Hollier, eds. The Maintenance of Arterial Reconstruction. London & Philadelphia, PA: W.B. Saunders, 1991; 37–49.
- 12 Watkins MT, Sharefkin JB, Zajtchuk R, et al. Adult human saphenous vein endothelial cells: assessment of their reproductive capacity for use in endothelial seeding of vascular prostheses. J Surg Res 1984; 36: 588–96.
- 13 Millon LE, Guhados G, Wan W. Anisotropic polyvinyl alcohol-bacterial cellulose nanocomposite for biomedical applications. J Biomed Mater Res B Appl Biomater 2008; 86B: 444–52.
- 14 Loose DA, Borchard F. Kriterien zur Prüfung einer kombinierten Gefäßprothese: Ergebnisse experimenteller, klinischer und morphologischer Untersuchungen. Stuttgart: Thieme, 1980; 4.
- 15 Murase Y, Narita Y, Kagami H, et al. Evaluation of compliance and stiffness of decellularized tissues as scaffolds for tissue-engineered small caliber vascular grafts using intravascular ultrasound. ASAIO J 2006; 52: 450–5.
- 16 Kallenbach K, Sorrentino S, Mertsching H, et al. Novel small animal model for accelerated investigation of tissue engineered aortic valved conduits. Tissue Eng C Methods 2010; 16: 41–50.
- 17 Bader A, Steinhoff G, Strobl K, et al. Engineering of human vascular aortic tissue based on a xenogenic starter matrix. Transplantation 2000; 70: 7–14.
- 18 Sarkar S, Schmidt-Rixen T, Hamilton G, Seifalian AM. Achieving the ideal properties for vascular bypass grafts using tissue engineered approach: a review. Med Biol Eng Comput 2007; 45: 327–36.
- 19 Nasseri BA, Pomerantseva I, Kaazempur-Mofrad MR, et al. Dynamic rotational seeding and cell culture system for vascular tube formation. Tissue Eng 2003; 9: 291–9.
- 20 Tiwari A, Salacinski HJ, Seifalian AM, Hamilton G. New prostheses for use in bypass grafts with special emphasis on polyurethanes. Cardiovasc Surg 2002; 10: 191–7.
- 21
Greenwald SE,
Berry CL.
Improving vascular grafts: the importance of mechanical and haemodynamic properties.
J Pathol
2000; 190: 292–9.
10.1002/(SICI)1096-9896(200002)190:3<292::AID-PATH528>3.0.CO;2-S CAS PubMed Web of Science® Google Scholar
- 22 Beyer F, Doebis C, Busch A, et al. Decline of surface MHC I by adenoviral gene transfer of anti-MHC I intrabodies in human endothelial cells—new perspectives for the generation of universal donor cells for tissue transpantation. J Gene Med 2004; 6: 616–23.
- 23 Arrigoni C, Camozzi D, Remuzzi A. Vascular tissue engineering. Cell Transplant 2006; 15: S119–25.
- 24 Thoumine O, Nerem RM, Girarad PR. Oscillatory shear stress and hydrostatic pressure modulate cell-matrix attachment proteins in cultured endothelial cells. In Vitro Cell Dev Biol Anim 1995; 31: 45–54.
- 25 Hoerstrup SP, Sodian R, Daebritz S, et al. Functional living trileaflet heart valves grown in vitro. Circulation 2000; 102: III44–9.
- 26 Hoerstrup SP, Zünd G, Sodian R, Schnell AM, Grünenfelder J, Turina MI. Tissue engineering of small caliber vascular grafts. Eur J Cardiothorac Surg 2001; 20: 164–9.
- 27 Hamann H, Cyba-Altunbay S, Reuchlin G. Sicherheitsaspekte und Qualitätskontrolle in der Implantation von Gefäßprothesen. In: K Balzer, K Brachmann, eds. Sicherheitsaspekte und Qualitätskontrolle in der Gefäßchirurgie. Die Lebensqualität des Gefäßpatienten [ . . . ] Januar 1998. Darmstadt: Steinkopff, 1994; 53.
- 28
Gupta BS,
Kasyanov VA.
Biomechanics of human common carotid artery and design of novel hybrid textile compliant vascular grafts.
J Biomed Mater Res
1997; 34: 341–9.
10.1002/(SICI)1097-4636(19970305)34:3<341::AID-JBM9>3.0.CO;2-K CAS PubMed Web of Science® Google Scholar
- 29 L'Heureux N, Germain L, Labbe R, Auger FA. In vitro construction of a human blood vessel from cultured vascular cells: a morphologic study. J Vasc Surg 1993; 17: 499–509.
- 30 Cebotari S, Mertsching H, Kallenbach K, et al. Construction of autologous human heart valves based on an acellular allograft matrix. Circulation 2002; 106: I63–8.
- 31 Kallenbach K, Leyh RG, Lefik E, et al. Guided tissue regeneration: porcine matrix does not transmit PERV. Biomaterials 2004; 25: 3613–20.
- 32 Kumar TR, Krishnan LK. Fibrin-mediated endothelial cell adhesion to vascular biomaterials resists shear stress due to flow. J Mater Sci Mater Med 2002; 13: 751–5.
- 33 Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 2005; 11: 1–18.
- 34 Ludwig NS, Yoder C, McConney M, Vargo TG, Kader KN. Directed type IV collagen self-assembly on hydroxylated PTFE. J Biomed Mater Res A 2006; 78: 615–9.
- 35 Shadwick RE. Mechanical design in arteries. J Exp Biol 1999; 202: 3305–13.
- 36 Cox MA, Gawlitta D, Driessen NJ, Oomens CW, Baaijens FP. The non-linear mechanical properties of soft engineered biological tissues determined by finite spherical indentation. Comput Methods Biomech Biomed Engin 2008; 11: 585–92.
- 37 Oie T, Murayama Y, Fukuda T, et al. Local elasticity imaging of vascular tissues using a tactile mapping system. Artif Organs 2009; 12: 40–6.
- 38 Slaughter MS, Pagani FD, Rogers JG, et al.; HeartMate II Clinical Investigators. Clinical management of continuous-flow left ventricular assist devices in advanced heart failure. J Heart Lung Transplant 2010; 29(4 Suppl): S1–39.
- 39 Nasseri BA, Alexi-Meskishvili V, Nordmeyer S, et al. Predictors for the use of left ventricular assist devices in infants with anomalous left coronary artery from the pulmonary artery. Ann Thorac Surg 2010; 90: 580–7.
- 40 Back MR, Maynard M, Winkler A, Bandyk DF. Expected flow parameters within hemodialysis access and selection for remedial intervention of nonmaturing conduits. Vasc Endovascular Surg 2008; 42: 150–8.
- 41 Chang CY, O'Rourke DK, Cass SP. Update on skull base surgery. Otolaryngol Clin North Am 1996; 29: 467–501.
- 42 Johnson MH, Chiang VL, Ross DA. Interventional neuroradiology adjuncts and alternatives in patients with head and neck vascular lesions. Neurosurg Clin N Am 2005; 16: 547–60.
- 43 Sanna M, Piazza P, Ditrapani G, Agarwal M. Management of the internal carotid artery in tumors of the lateral skull base: preoperative permanent balloon occlusion without reconstruction. Otol Neurotol 2004; 25: 998–1005.
- 44 Rodríguez-Vegas JM, Trillo Bohajar E, Ruiz Alonso E, Casado Pérez C. Refining the anterolateral thigh free flap to prevent orocervical fistula in head and neck reconstruction. Plast Reconstr Surg 2004; 114: 174–7.
- 45 Liu H, McKenna LA, Dean MF. An N-terminal peptide from link protein can stimulate biosynthesis of collagen by human articular cartilage. Arch Biochem Biophys 2000; 378: 116–22.
- 46 Lichtenberg A, Tudorache I, Cebotari S, et al. Preclinical testing of tissue-engineered heart-valves reendothelialized under stimulated physiological conditions. Circulation 2006; 114: I559–65.
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