A current challenge concerns developing new bioresorbable stents that combine optimal mechanical properties and biodegradation rates with limited thrombogenicity. In this context, twinning-induced plasticity (TWIP) steels are good material candidates. In this work, the hemocompatibility of a new TWIP steel was studied in vitro via hemolysis and platelet activation assessments. Cobalt chromium (CoCr) L605 alloy, pure iron (Fe), and magnesium (Mg) WE43 alloy were similarly studied for comparison. No hemolysis was induced by TWIP steel, pure Fe, or L605 alloy. Moreover, L605 alloy did not affect CD62P exposure, αIIbβ3 activation at the platelet surface, or phosphorylation of protein kinase C (PKC) substrates upon thrombin stimulation. In contrast, TWIP steel and pure Fe significantly decreased platelet response to the agonist. Given that similar inhibitory effects were obtained when using a conditioned medium previously incubated with TWIP steel, we postulated TWIP steel corrosion to be likely to release components counteracting platelet activation. We showed that the main ion form present in the conditioned medium is Fe3+. In conclusion, TWIP steel resorbable scaffold displays anti-thrombogenic properties in vitro, which suggests that it could be a promising platform for next-generation stent technologies.
References
[1]
Libby, P., Ridker, P.M. and Hansson, G.K. (2011) Progress and Challenges in Translating the Biology of Atherosclerosis. Nature, 473, 317-325.
https://doi.org/10.1038/nature10146
[2]
Corban, M.T., Lerman, L.O. and Lerman, A. (2019) Endothelial Dysfunction. Arteriosclerosis, Thrombosis, and Vascular Biology, 39, 1272-1274.
https://doi.org/10.1161/ATVBAHA.119.312836
[3]
Maddox, T.M., Stanislawski, M.A., Grunwald, G.K., Bradley, S.M., Ho, P.M., Tsai, T.T., Patel, M.R., Sandhu, A., Valle, J., Magid, D.J., Leon, B., Bhatt, D.L., Fihn, S.D. and Rumsfeld, J.S. (2014) Nonobstructive Coronary Artery Disease and Risk of Myocardial Infarction. JAMA, 312, 1754-1763.
https://doi.org/10.1001/jama.2014.14681
[4]
Du, F. and Zhou, J. (2018) Vascular Intervention: From Angioplasty to Bioresorbable Vascular Scaffold. Advances in Experimental Medicine and Biology, 1097, 181-189. https://doi.org/10.1007/978-3-319-96445-4_9
[5]
Iqbal, J., Gunn, J. and Serruys, P.W. (2013) Coronary Stents: Historical Development, Current Status and Future Directions. British Medical Bulletin, 106, 193-211.
https://doi.org/10.1093/bmb/ldt009
[6]
Borhani, S., Hassanajili, S., Ahmadi Tafti, S.H. and Rabbani, S. (2018) Cardiovascular Stents: Overview, Evolution, and Next Generation. Progress in Biomaterials, 7, 175-205. https://doi.org/10.1007/s40204-018-0097-y
[7]
Weber, M., Steinle, H., Golombek, S., Hann, L., Schlensak, C., Wendel, H.P. and Avci-Adali, M. (2018) Blood-Contacting Biomaterials: In Vitro Evaluation of the Hemocompatibility. Frontiers in Bioengineering and Biotechnology, 6, 99.
https://doi.org/10.3389/fbioe.2018.00099
[8]
Yen, J.H., Chen, S.F., Chern, M.K. and Lu, P.C. (2014) The Effect of Turbulent Viscous Shear Stress on Red Blood Cell Hemolysis. Journal of Artificial Organs, 17, 178-185. https://doi.org/10.1007/s10047-014-0755-3
[9]
Merle, N.S., Grunenwald, A., Figueres, M.L., Chauvet, S., Daugan, M., Knockaert, S., Robe-Rybkine, T., Noe, R., May, O., Frimat, M., Brinkman, N., Gentinetta, T., Miescher, S., Houillier, P., Legros, V., Gonnet, F., Blanc-Brude, O.P., Rabant, M., Daniel, R., Dimitrov, J.D. and Roumenina, L.T. (2018) Characterization of Renal Injury and Inflammation in an Experimental Model of Intravascular Hemolysis. Frontiers in Immunology, 9, 179. https://doi.org/10.3389/fimmu.2018.00179
[10]
Rossaint, J., Margraf, A. and Zarbock, A. (2018) Role of Platelets in Leukocyte Recruitment and Resolution of Inflammation. Frontiers in Immunology, 9, 2712.
https://doi.org/10.3389/fimmu.2018.02712
[11]
Etulain, J. and Schattner, M. (2014) Glycobiology of Platelet-Endothelial Cell Interactions. Glycobiology, 24, 1252-1259. https://doi.org/10.1093/glycob/cwu056
[12]
Diamond, S.L. (2016) Systems Analysis of Thrombus Formation. Circulation Research, 118, 1348-1362. https://doi.org/10.1161/CIRCRESAHA.115.306824
[13]
Jaffer, I.H., Fredenburgh, J.C., Hirsh, J. and Weitz, J.I. (2015) Medical Device-Induced Thrombosis: What Causes It and How Can We Prevent It? Journal of Thrombosis and Haemostasis, 13, S72-S81. https://doi.org/10.1111/jth.12961
[14]
Swieringa, F., Spronk, H.M.H., Heemskerk, J.W.M. and van der Meijden, P.E.J. (2018) Integrating Platelet and Coagulation Activation in Fibrin Clot Formation. Research and Practice in Thrombosis and Haemostasis, 2, 450-460.
https://doi.org/10.1002/rth2.12107
[15]
Dziewierz, A. and Dudek, D. (2018) Current Perspectives on the Role of Bioresorbable Scaffolds in the Management of Coronary Artery Disease. Kardiologia Polska, 76, 1043-1054. https://doi.org/10.5603/KP.a2018.0130
[16]
Dave, B. (2016) Bioresorbable Scaffolds: Current Evidences in the Treatment of Coronary Artery Disease. Journal of Clinical and Diagnostic Research, 10, OE01-OE07.
https://doi.org/10.7860/JCDR/2016/21915.8429
[17]
Moravej, M. and Mantovani, D. (2011) Biodegradable Metals for Cardiovascular Stent Application: Interests and New Opportunities. International Journal of Molecular Sciences, 12, 4250-4270. https://doi.org/10.3390/ijms12074250
[18]
Walker, E.K., Nauman, E.A., Allain, J.P. and Stanciu, L.A. (2015) An in Vitro Model for Preclinical Testing of Thrombogenicity of Resorbable Metallic Stents. Journal of Biomedical Materials Research Part A, 103, 2118-2125.
https://doi.org/10.1002/jbm.a.35348
[19]
Liu, B. and Zheng, Y.F. (2011) Effects of Alloying Elements (Mn, Co, Al, W, Sn, B, C and S) on Biodegradability and in Vitro Biocompatibility of Pure Iron. Acta Biomaterialia, 7, 1407-1420. https://doi.org/10.1016/j.actbio.2010.11.001
[20]
Liu, Y., Wu, Y., Bian, D., Gao, S., Leeflang, S., Guo, H., Zheng, Y. and Zhou, J. (2017) Study on the Mg-Li-Zn Ternary Alloy System with Improved Mechanical Properties, Good Degradation Performance and Different Responses to Cells. Acta Biomaterialia, 62, 418-433. https://doi.org/10.1016/j.actbio.2017.08.021
[21]
Yahata, C. and Mochizuki, A. (2017) Platelet Compatibility of Magnesium Alloys. Materials Science & Engineering C—Materials for Biological Applications, 78, 1119-1124. https://doi.org/10.1016/j.msec.2017.04.153
[22]
Feyerabend, F., Wendel, H.P., Mihailova, B., Heidrich, S., Agha, N.A., Bismayer, U. and Willumeit-Romer, R. (2015) Blood Compatibility of Magnesium and Its Alloys. Acta Biomaterialia, 25, 384-394. https://doi.org/10.1016/j.actbio.2015.07.029
[23]
Peuster, M., Hesse, C., Schloo, T., Fink, C., Beerbaum, P. and von Schnakenburg, C. (2006) Long-Term Biocompatibility of a Corrodible Peripheral Iron Stent in the Porcine Descending Aorta. Biomaterials, 27, 4955-4962.
https://doi.org/10.1016/j.biomaterials.2006.05.029
[24]
Peuster, M., Wohlsein, P., Brugmann, M., Ehlerding, M., Seidler, K., Fink, C., Brauer, H., Fischer, A. and Hausdorf, G. (2001) A Novel Approach to Temporary Stenting: Degradable Cardiovascular Stents Produced from Corrodible Metal-Results 6-18 Months after Implantation into New Zealand White Rabbits. Heart, 86, 563-569. https://doi.org/10.1136/heart.86.5.563
[25]
Waksman, R., Pakala, R., Baffour, R., Seabron, R., Hellinga, D. and Tio, F.O. (2008) Short-Term Effects of Biocorrodible Iron Stents in Porcine Coronary Arteries. Journal of Interventional Cardiology, 21, 15-20.
https://doi.org/10.1111/j.1540-8183.2007.00319.x
[26]
Haude, M., Erbel, R., Erne, P., Verheye, S., Degen, H., Vermeersch, P., Weissman, N., Prati, F., Bruining, N., Waksman, R. and Koolen, J. (2016) Safety and Performance of the Drug-Eluting Absorbable Metal Scaffold (DREAMS) in Patients with De Novo Coronary Lesions: 3-Year Results of the Prospective, Multicentre, First-in-Man BIOSOLVE-I Trial. EuroIntervention, 12, e160-e166.
https://doi.org/10.4244/EIJ-D-15-00371
[27]
Sakamoto, A., Jinnouchi, H., Torii, S., Virmani, R. and Finn, A.V. (2018) Understanding the Impact of Stent and Scaffold Material and Strut Design on Coronary Artery Thrombosis from the Basic and Clinical Points of View. Bioengineering (Basel), 5, 71. https://doi.org/10.3390/bioengineering5030071
[28]
Sezer, N., Evis, Z., Kayhan, S.M., Tahmasebifar, A. and Koç, M. (2018) Review of Magnesium-Based Biomaterials and Their Applications. Journal of Magnesium and Alloys, 6, 23-43. https://doi.org/10.1016/j.jma.2018.02.003
[29]
Idrissi, H., Renard, K., Ryelandt, L., Schryvers, D. and Jacques, P.J. (2010) On the Mechanism of Twin Formation in Fe-Mn-C TWIP Steels. Acta Materialia, 58, 2464-2476. https://doi.org/10.1016/j.actamat.2009.12.032
[30]
Renard, K. and Jacques, P.J. (2012) On the Relationship between Work Hardening and Twinning Rate in TWIP Steels. Materials Science and Engineering A, 542, 8-14.
https://doi.org/10.1016/j.msea.2012.01.123
[31]
De Cooman, B.C., Estrin, Y. and Kim, S.K. (2018) Twinning-Induced Plasticity (TWIP) Steels. Acta Materialia, 142, 283-362.
https://doi.org/10.1016/j.actamat.2017.06.046
[32]
Goodhead, L.K. and MacMillan, F.M. (2017) Measuring Osmosis and Hemolysis of Red Blood Cells. Advances in Physiology Education, 41, 298-305.
https://doi.org/10.1152/advan.00083.2016
[33]
ASTM F. F756-08 (2013) Standard Practice for Assessment of Hemolytic Properties of Materials, ASTM Book of Standards. ASTM International, West Conshohocken.
[34]
Cheng, J., Liu, B., Wu, Y.H. and Zheng, Y.F. (2013) Comparative in Vitro Study on Pure Metals (Fe, Mn, Mg, Zn and W) as Biodegradable Metals. Journal of Materials Science & Technology, 29, 619-627. https://doi.org/10.1016/j.jmst.2013.03.019
[35]
Huang, T., Cheng, Y. and Zheng, Y. (2016) In Vitro Studies on Silver Implanted Pure Iron by Metal Vapor Vacuum Arc Technique. Colloids and Surfaces B: Biointerfaces, 142, 20-29. https://doi.org/10.1016/j.colsurfb.2016.01.065
[36]
Li, M., Cheng, Y., Zheng, Y.F., Zhang, X., Xi, T.F. and Wei, S.C. (2012) Surface Characteristics and Corrosion Behaviour of WE43 Magnesium Alloy Coated by SiC Film. Applied Surface Science, 258, 3074-3081.
https://doi.org/10.1016/j.apsusc.2011.11.040
[37]
Wei, Z., Tian, P., Liu, X. and Zhou, B. (2014) Hemocompatibility and Selective Cell Fate of Polydopamine-Assisted Heparinized PEO/PLLA Composite Coating on Biodegradable AZ31 Alloy. Colloids and Surfaces B: Biointerfaces, 121, 451-460.
https://doi.org/10.1016/j.colsurfb.2014.06.036
[38]
Zhou, W.R., Zheng, Y.F., Leeflang, M.A. and Zhou, J. (2013) Mechanical Property, Biocorrosion and in Vitro Biocompatibility Evaluations of Mg-Li-(Al)-(RE) Alloys for Future Cardiovascular Stent Application. Acta Biomaterialia, 9, 8488-8498.
https://doi.org/10.1016/j.actbio.2013.01.032
[39]
Mao, L., Yuan, G., Niu, J., Zong, Y. and Ding, W. (2013) In Vitro Degradation Behavior and Biocompatibility of Mg-Nd-Zn-Zr Alloy by Hydrofluoric Acid Treatment. Materials Science & Engineering C-Materials for Biological Applications, 33, 242-250. https://doi.org/10.1016/j.msec.2012.08.036
[40]
Gu, X., Zheng, Y., Cheng, Y., Zhong, S. and Xi, T. (2009) In Vitro Corrosion and Biocompatibility of Binary Magnesium Alloys. Biomaterials, 30, 484-498.
https://doi.org/10.1016/j.biomaterials.2008.10.021
[41]
Huang, T., Cheng, J., Bian, D. and Zheng, Y. (2016) Fe-Au and Fe-Ag Composites as Candidates for Biodegradable Stent Materials. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 104, 225-240.
https://doi.org/10.1002/jbm.b.33389
[42]
ISO 10993 (2002) Biological Evaluation of Medical Devices—Part 4: Selection of Tests for Interactions with Blood. International Organization for Standardization, Genève.
[43]
Moore, S.F., Hunter, R.W. and Hers, I. (2014) Protein Kinase C and P2Y12 Take Center Stage in Thrombin-Mediated Activation of Mammalian Target of Rapamycin Complex 1 in Human Platelets. Journal of Thrombosis and Haemostasis, 12, 748-760. https://doi.org/10.1111/jth.12552
[44]
Huang, T., Cheng, J. and Zheng, Y.F. (2014) In Vitro Degradation and Biocompatibility of Fe-Pd and Fe-Pt Composites Fabricated by Spark Plasma Sintering. Materials Science & Engineering C-Materials for Biological Applications, 35, 43-53.
https://doi.org/10.1016/j.msec.2013.10.023
[45]
Hermawan, H., Purnama, A., Dube, D., Couet, J. and Mantovani, D. (2010) Fe-Mn Alloys for Metallic Biodegradable Stents: Degradation and Cell Viability Studies. Acta Biomaterialia, 6, 1852-1860. https://doi.org/10.1016/j.actbio.2009.11.025
[46]
Nemmar, A., Beegam, S., Yuvaraju, P., Yasin, J., Tariq, S., Attoub, S. and Ali, B.H. (2016) Ultrasmall Superparamagnetic Iron Oxide Nanoparticles Acutely Promote Thrombosis and Cardiac Oxidative Stress and DNA Damage in Mice. Particle and Fibre Toxicology, 13, 22. https://doi.org/10.1186/s12989-016-0132-x
[47]
Rooyakkers, T.M., Stroes, E.S., Kooistra, M.P., van Faassen, E.E., Hider, R.C., Rabelink, T.J. and Marx, J.J. (2002) Ferric Saccharate Induces Oxygen Radical Stress and Endothelial Dysfunction in Vivo. European Journal of Clinical Investigation, 32, 9-16. https://doi.org/10.1046/j.1365-2362.2002.0320s1009.x
[48]
Eckly, A., Hechler, B., Freund, M., Zerr, M., Cazenave, J.P., Lanza, F., Mangin, P.H. and Gachet, C. (2011) Mechanisms Underlying FeCl3-Induced Arterial Thrombosis. Journal of Thrombosis and Haemostasis, 9, 779-789.
https://doi.org/10.1111/j.1538-7836.2011.04218.x
[49]
Ciciliano, J.C., Sakurai, Y., Myers, D.R., Fay, M.E., Hechler, B., Meeks, S., Li, R., Dixon, J.B., Lyon, L.A., Gachet, C. and Lam, W.A. (2015) Resolving the Multifaceted Mechanisms of the Ferric Chloride Thrombosis Model Using an Interdisciplinary Microfluidic Approach. Blood, 126, 817-824.
https://doi.org/10.1182/blood-2015-02-628594
[50]
Schoenwaelder, S.M. and Jackson, S.P. (2015) Ferric Chloride Thrombosis Model: Unraveling the Vascular Effects of a Highly Corrosive Oxidant. Blood, 126, 2652-2653.
https://doi.org/10.1182/blood-2015-09-668384
[51]
Barr, J.D., Chauhan, A.K., Schaeffer, G.V., Hansen, J.K. and Motto, D.G. (2013) Red Blood Cells Mediate the Onset of Thrombosis in the Ferric Chloride Murine Model. Blood, 121, 3733-3741. https://doi.org/10.1182/blood-2012-11-468983
[52]
Miron, V.R., Bauermann, L., Morsch, A.L., Zanin, R.F., Correa, M., da Silva, A.C., Mazzanti, C., Morsch, V.M., Lunkes, G.I. and Schetinger, M.R. (2007) Enhanced NTPDase and 5’-Nucleotidase Activities in Diabetes Mellitus and Iron-Overload Model. Molecular and Cellular Biochemistry, 298, 101-107.
https://doi.org/10.1007/s11010-006-9357-6
