Mechanical properties of the porcine pericardium extracellular matrix cross-linked with glutaraldehyde and tannic acid

• Autorzy: Dąbrowska Karolina Zofia , Turek Artur , Grzejda Rafał , Kobielarz Magdalena

Identyfikatory

DOI

10.37190/ABB-02119-2022-01

• Języki publikacji: EN

Abstrakty

EN

The aim of this study was to determine the influence of factors such as temperature and glutaraldehyde (GA) concentration on the mechanical properties of porcine pericardia, in order to propose the recommended optimal conditions of a cross-linking process. It was also to verify whether tannic acid (TA), a natural cross-linking agent that stabilizes collagenous tissues by a different mechanism than GA, may positively influence the strength of pericardium. Methods: The samples were incubated at various temperatures (4, 22, and 37 °C) and GA concentration solutions (0.6, 1.5 and 3%) for 7 days. Three series were selected and additionally cross-linked with 0.3% TA for another 7 days. Mechanical properties of cross-linked pericardium samples, i.e., ultimate tensile strength (UTS) and elastic modulus (E) were measured in uniaxial tensile testing. The hyperelastic model for incompressible materials – isotropic by Ogden [24] and anisotropic by Fung [7] were utilized to describe the mechanical behaviour of treated pericardium. Results: The temperature has an influence on cross-linking effects; the lowest values of UTS were reported for specimens cross-linked at 22 °C, while the mechanical properties of series treated at 4 °C or 37 °C were comparable. At a particular temperature of incubation, the GA concentrations have not affected the mechanical properties of tissues. The dependence between mechanical parameters and agent concentration was only observed for specimens treated with GA at 37 °C. Conclusions: The conditions of the cross-linking process affect the mechanical properties of the porcine pericardium. Room temperature (22 °C) and the concentration of 1.5% GA occurred to be ineffective. The mechanical properties of GA-treated pericardium were improved by an additional TA cross-linking.

Słowa kluczowe

EN

porcine pericardium; collagen; glutaraldehyde; tannic acid; mechanical properties; uniaxial tensile testing

• Wydawca: Oficyna Wydawnicza Politechniki Wrocławskiej
• Czasopismo: Acta of Bioengineering and Biomechanics
• Rocznik: 2022
• Tom: Vol. 24, no. 3
• Strony: 21--31
• Opis fizyczny: Bibliogr. 40 poz., rys., tab., wykr.

Twórcy

autor

Dąbrowska Karolina Zofia

• Faculty of Mechanical Engineering, Wrocław University of Science and Technology, Wrocław, Poland.

autor

Turek Artur

• Department of Biopharmacy, Faculty of Pharmaceutical Sciences in Sosnowiec, Medical University of Silesia, Katowice, Poland.

autor

Grzejda Rafał

• Department of Mechanics, Faculty of Mechanical Engineering and Mechatronics, West Pomeranian University of Technology in Szczecin, Szczecin, Poland.

autor

Kobielarz Magdalena

• Department of Mechanics, Materials and Biomedical Engineering, Faculty of Mechanical Engineering, Wrocław University of Science and Technology, Wrocław, Poland.

Bibliografia

• [1] AGUIARI P., FIORESE M., IOP L., GEROSA G., BAGNO A., Mechanical testing of pericardium for manufacturing prosthetic heart valves, Interact. Cardiovasc. Thorac. Surg., 2016, 22 (1), 72–84, DOI: 10.1093/icvts/ivv282.
• [2] ARBEITER D., GRABOW N., WESSARGES Y., STERNBERG K., SCHMITZ K.P., Suitability of porcine pericardial tissue for heart valve engineering: Biomechanical properties, Biomed. Tech. (Berl.), 2012, 57 (Suppl. 1), 882–883, DOI: 10.1515/bmt-2012-4332.
• [3] BALDWIN A., BOOTH B.W., Biomedical applications of tannic acid, J. Biomater. Appl., 2022, 36 (8), 1503–1523, DOI: 10.1177/08853282211058099.
• [4] BONDARENKO N.A., SUROVTSEVA M.A., LYKOV P., KIM I.I., ZHURAVLEVA I.Y., POVESCHENKO V., Cytotoxicity of xenogeneic pericardium preserved by epoxy cross-linking agents, Sovrem. Tehnol. v Med., 2021, 13 (4), 27–33, DOI: 10.17691/stm2021.13.4.03.
• [5] BRAGA-VILELA A.S., PIMENTEL E.R., MARANGONI S., TOYAMA M.H., CAMPOS VIDAL B. DE, Extracellular matrix of porcine pericardium: Biochemistry and collagen architecture, J. Membr. Biol., 2008, 221 (1), 15–25, DOI: 10.1007/s00232-007-9081-5.
• [6] CABALLERO A., SULEJMANI F., MARTIN C., PHAM T., SUN W., Evaluation of transcatheter heart valve biomaterials: Biomechanical characterization of bovine and porcine pericardium, J. Mech. Behav. Biomed. Mater., 2017, 75, 486–494, DOI: 10.1016/j.jmbbm.2017.08.013.
• [7] CHUONG C.J., FUNG Y.C., Three-Dimensional Stress Distribution in Arteries, J. Biomech. Eng., 1983, 105 (3), 268–274, DOI: 10.1115/1.3138417.
• [8] COHN D., YOUNES H., MILGARTER E., URETZKY G., Mechanical behaviour of isolated pericardium: species, isotropy, strain rate and collagenase effect on pericardial tissue, Clin. Mater., 1987, 2 (2), 115–124, DOI: 10.1016/0267-6605(87)90030-8.
• [9] COURTMAN D.W., PEREIRA C.A., KASHEF V., DONNA M., LEE J.M., WILSON G.J., Development of a pericardial acellular matrix biomaterial: Biochemical and mechanical effects of cell extraction, J. Biomed. Mater. Res., 1994, 28 (6), 655–666, DOI: 10.1002/jbm.820280602.
• [10] CWALINA B., TUREK A., JASTRZĘBSKA M., FLUDER A., KOSTKA P., Stress changes in pericardium tissue during its modification with tannic acid, Inż. Biomat., 2002, 5 (23–25), 67–70.
• [11] CWALINA B., TUREK A., NOŻYŃSKI J., JASTRZĘBSKA M., NAWRAT Z., Structural changes in pericardium tissue modified with tannic acid, Int. J. Artif. Organs, 2005, 28 (6), 648–653, DOI: 10.1177/039139880502800614.
• [12] DEBELLE L., ALIX A.J.P., The structures of elastins and their function, Biochimie, 1999, 81 (10), 981–994, DOI: 10.1016/S0300-9084(99)00221-7.
• [13] FERRANS V., HILBERT S., JONES M., Biomaterials. Replacement Cardiac Valves, 1991.
• [14] GRABENWÖGER M., SIDER J., FITZAL F., ZELENKA C., WINDBERGER U., GRIMM M., I WSP., Impact of glutaraldehyde on calcification of pericardial bioprosthetic heart valve material, Ann. Thorac Surg., 62 (3), 772–777, 1996.
• [15] ISENBURG J.C., SIMIONESCU D.T., VYAVAHARE N.R., Tannic acid treatment enhances biostability and reduces calcification of glutaraldehyde fixed aortic wall, Biomaterials, 2005, 26 (11), 1237–1245, DOI: 10.1016/j.biomaterials.2004.04.034.
• [16] ISENBURG J.C., SIMIONESCU D.T., VYAVAHARE N.R., Elastin stabilization in cardiovascular implants: Improved resistance to enzymatic degradation by treatment with tannic acid, Biomaterials, 2004, 25 (16), 3293–3302, DOI: 10.1016/j.biomaterials.2003.10.001.
• [17] JASTRZĘBSKA M., MRÓZ I., BARWIŃSKI B., ZALEWSKA-REJDAK J., TUREK A., CWALINA B., Supramolecular structure of human aortic valve and pericardial xenograft material: Atomic force microscopy study, J. Mater Sci.: Mater Med., 2008, 19 (1), 249–256, DOI: 10.1007/s10856-006-0049-2.
• [18] JASTRZĘBSKA M., WRZALIK R., KOCOT A., ZALEWSKA-REJDAK J., CWALINA B., Hydration of glutaraldehyde-fixed pericardium tissue: Raman spectroscopic study, J. Raman Spectrosc., 2003, 34 (6), 424–431, DOI: 10.1002/jrs.1016.
• [19] JASTRZĘBSKA M., ZALEWSKA-REJDAK J., WRZALIK R., KOCOT A., MRÓZ I., BARWIŃSKI B. et al., Tannic acid-stabilized pericardium tissue: IR spectroscopy, atomic force microscopy, and dielectric spectroscopy investigations, J. Biomed. Mater Res. A, 2006, 78A (1), 148–156, DOI: 10.1002/jbm.a.30717.
• [20] KOBIELARZ M., Effect of collagen fibres and elastic lamellae content on the mechanical behaviour of abdominal aortic aneurysms, Acta Bioeng. Biomech., 2020, 22 (3), 9–21, DOI: 10.37190/ABB-01580-2020-02.
• [21] LEIKINA E., MERTTS M. V., KUZNETSOVA N., LEIKIN S., Type I collagen is thermally unstable at body temperature, Proc. Natl. Acad. Sci. USA, 2002, 99 (3), 1314–1318, DOI: 10.1073/pnas.032307099.
• [22] MEYER M., Processing of collagen based biomaterials and the resulting materials properties, Biomed. Eng. Online, 2019, 18, 24, DOI: 10.1186/s12938-019-0647-0.
• [23] NAIMARK W.A., LEE J.M., LIMEBACK H., CHEUNG D.T., Correlation of structure and viscoelastic properties in the pericardia of four mammalian species, Am. J. Physiol. – Heart Circ. Physiol., 1992, 263 (4), H1095–H1106, DOI: 10.1152/ajpheart.1992.263.4.h1095.
• [24] OGDEN R.W., Large deformation isotropic elasticity – on the correlation of theory and experiment for incompressible rubMechanical properties of the porcine pericardium extracellular matrix cross-linked with glutaraldehyde and tannic acid 31 berlike solids, Proc. R. Soc. A Math. Phys. Eng. Sci., 1972, 326 (1567), 565–584, DOI: 10.1098/rspa.1972.0026.
• [25] OLDE DAMINK L.H.H., DIJKSTRA P.J., VAN LUYN M.J.A., VAN WACHEM P.B., NIEUWENHUIS P., FEIJEN J., Glutaraldehyde as a cross-linking agent for collagen-based biomaterials, J. Mater. Sci. Mater Med., 1995, 6 (8), 460–472, DOI: 10.1007/BF00123371.
• [26] ROSENTHAL J.T., SHAW B.W., HARDESTY R.L., Principles of multiple organ procurement from cadaver donors, Ann. Surg., 1983, 198 (5), 617–621, DOI: 10.1097/00000658-198311000-00010.
• [27] SCHOEN F.J., LEVY R.J., Calcification of tissue heart valve substitutes: Progress toward understanding and prevention, Ann. Thorac. Surg., 2005, 79 (3), 1072–1080, DOI: 10.1016/j.athoracsur.2004.06.033.
• [28] SHABETAI R., The pericardium, Kluwer Academic Publishers, 2003.
• [29] SHAH S.R., VYAVAHARE N.R., The effect of glycosaminoglycan stabilization on tissue buckling in bioprosthetic heart valves, Biomaterials, 2008, 29 (11), 1645–1653, DOI: 10.1016/j.biomaterials.2007.12.009.
• [30] SIMIONESCU D., SIMIONESCU A., DEAC R., Mapping of glutaraldehyde-treated bovine pericardium and tissue selection for bioprosthetic heart valves, J. Biomed. Mater. Res., 1993, 27 (6), 697–704, DOI: 10.1002/jbm.820270602.
• [31] SINGHAL P., LUK A., BUTANY J., Bioprosthetic Heart Valves: Impact of implantation on biomaterials, Int. Sch. Res. Not., 2013, 2013. 728791, DOI: 10.5402/2013/728791.
• [32] SIONKOWSKA A., KACZMAREK B., LEWANDOWSKA K., Modification of collagen and chitosan mixtures by the addition of tannic acid, J. Mol. Liq., 2014, 199, 318–323, DOI: 10.1016/j.molliq.2014.09.028.
• [33] TUREK A., CWALINA B., KOBIELARZ M., Radioisotopic investigation of crosslinking density in bovine pericardium used as a biomaterial, Nukleonika, 2013, 58 (4), 511–517.
• [34] UMASHANKAR P.R., MOHANAN P.V., KUMARI T.V., Glutaraldehyde treatment elicits toxic response compared to decellularization in bovine pericardium, Toxicol. Int., 2012, 19 (1), 51–58, DOI: 10.4103/0971-6580.94513.
• [35] VELMURUGAN P., SINGAM E.R.A., JONNALAGADDA R.R., SUBRAMANIAN V., Investigation on interaction of tannic acid with type i collagen and its effect on thermal, enzymatic, and conformational stability for tissue engineering applications, Biopolymers, 2014, 101 (5), 471–483, DOI: 10.1002/bip.22405.
• [36] WALRAFEN G.E., CHU Y.C., Nature of collagen-water hydration forces: A problem in water structure, Chem. Phys., 2000, 258 (2–3), 427–446, DOI: 10.1016/S0301-0104(00)00072-0.
• [37] WANG D., JIANG H., LI J., ZHOU J.Y., HU S.S., Mitigated calcification of glutaraldehyde-fixed bovine pericardium by Tannic acid in rats, Chin. Med. J., 2008, 121 (17), 1675–1679, DOI: 10.1097/00029330-200809010-00017.
• [38] ZILLA P., WEISSENSTEIN C., HUMAN P., DOWER T., VON OPPELL U.O., High glutaraldehyde concentrations mitigate bioprosthetic root calcification in the sheep model, Ann. Thorac. Surg., 2000, 70 (6), 2091–2095, DOI: 10.1016/S0003-4975(00)02011-7.
• [39] ZILLA P., ZHANG Y., HUMAN P., KOEN W., VON OPPELL U., Improved ultrastructural preservation of bioprosthetic tissue, J. Heart Valve Dis., 1997, 6 (5), 492–501.
• [40] ZOUHAIR S., SASSO E.D., TULADHAR S.R., FIDALGO C., VEDOVELLI L., FILIPPI A., A comprehensive comparison of bovine and porcine decellularized pericardia: New insights for surgical applications, Biomolecules, 2020, 10 (3), 371, DOI: 10.3390/biom10030371.