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Morphological Post-implantation Features of Aortic Conduits After Long-term wet Storage

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Abstract

Purpose

Improved methods for obtaining connective tissue structures in cardiac surgery are actively developed over the world. An important aspect of this research pertains to long-term wet storage of cardiovascular biomaterial that optimally preserves the initial morphological characteristics.

Methods

Native and decellularized porcine aortas were stored for 50 days in several biocidal solutions (complex alcohol solution, a mixture of ethanol and glycerol, a mixture of antibiotics), and subsequently implanted in animals and studied histologically. The aortic specimens were implanted subcutaneously into 15 adult WAG rats. The samples were retrieved after 3 months and evaluated for calcium content using a quantitative spectroanalytical procedure. Aortic specimens were also orthotopically implanted into the vascular bed of 3 minipigs, harvested after 6 months, and histologically evaluated.

Results

Atomic absorption spectroscopy showed that decellularized materials accumulated 4.8–9.2 times less calcium, depending on the storage solution used. Morphological and morphometrical analysis of orthotopically implanted aortic fragments in minipigs showed better preservation of decellularized material that had been stored in a complex alcohol solution and mixture of antibiotics.

Conclusion

Functional and histological evidence was obtained demonstrating long-term storage without freezing of o aortic specimens without alteration of their biophysical properties and structure. The developed technique will be used in the future for the fabrication of vascular prostheses and heart valves.

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References

  1. Lisy, M., Kalender, G., Schenke-Layland, K., Brockbank, K. G., Biermann, A., & Stock, U. A. (2017). Allograft Heart Valves: current aspects and future applications. Biopreservation and Biobanking, 15(2), 148–157. https://doi.org/10.1089/bio.2016.0070.

    Article  CAS  PubMed  Google Scholar 

  2. Fioretta, E. S., von Boehmer, L., Motta, S. E., Lintas, V., Hoerstrup, S. P., & Emmert, M. Y. (2019). Cardiovascular tissue engineering: From basic science to clinical application. Experimental Gerontology, 117, 1–12. https://doi.org/10.1016/j.exger.2018.03.022

    Article  CAS  PubMed  Google Scholar 

  3. VeDepo, M. C., Detamore, M. S., Hopkins, R. A., & Converse, G. L. (2017). Recellularization of decellularized heart valves: Progress toward the tissue-engineered heart valve. Journal of Tissue Engineering, 8, 2041731417726327. https://doi.org/10.1177/2041731417726327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zhuravleva, I. Y., Nichay, N. R., Kulyabin, Y. Y., Timchenko, T. P., Korobeinikov, A. A., Polienko, Y. F., Shatskaya, S. S., Kuznetsova, E. V., Voitov, A. V., Bogachev-Prokophiev, A. V., & Karaskov, A. M. (2018). In search of the best xenogeneic material for a paediatric conduit: an experimental study. Interactive Cardiovascular And Thoracic Surgery, 26, 738–744. https://doi.org/10.1093/icvts/ivx445.

    Article  PubMed  Google Scholar 

  5. Lee, J., Chan, M. C., James, C., & Lantis, J. C. (2020). Cryopreserved allograft use in vascular surgery. Surgical Technology International, 37, 237–243.

    PubMed  Google Scholar 

  6. Britikov, D. V., Lauk-Dubitski, S., Serov, R., & Hugaev, G. (2019). Morphological evaluation of a new technique for cryopreservation of valvular and vascular allografts. Annals of Surgery, 24(1), 16–23. https://doi.org/10.24022/1560-9502-2019-24-1-16-23(In Russ.).

    Article  Google Scholar 

  7. Wollmann, L. C., Suss, P. H., Kraft, L., Ribeiro, V. S., Noronha, L., da Costa, F. D. A., & Tuon, F. F. (2020). Histological and biomechanical characteristics of human decellularized allograft heart valves after eighteen months of storage in saline solution. Biopreservation and Biobanking, 18, 90–101. https://doi.org/10.1089/bio.2019.0106.

    Article  CAS  PubMed  Google Scholar 

  8. Kraft, L., Ribeiro, V. S. T., & de Nazareno Wollmann, L. C. F. (2020). Determination of antibiotics and detergent residues in decellularized tissue-engineered heart valves using LC–MS/MS. Cell and Tissue Banking, 21, 573–584. https://doi.org/10.1007/s10561-020-09856-x.

    Article  CAS  PubMed  Google Scholar 

  9. VeDepo, M. C., Buse, E. E., Quinn, R. W., Williams, T. D., Detamore, M. S., Hopkins, R. A., & Converse, G. L. (2017). Species-specific effects of aortic valve decellularization. Acta Biomaterialia, 50, 249–258. https://doi.org/10.1016/j.actbio.2017.01.008.

    Article  PubMed  Google Scholar 

  10. Keane, T. J., Londono, R., Turner, N. J., & Badylak, S. F. (2012). Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials, 33, 1771–1781. https://doi.org/10.1016/j.biomaterials.2011.10.054.

    Article  CAS  PubMed  Google Scholar 

  11. Vasiliyeva, M. B., Kuznetsova, E. V., Rusakova, Y. L., Chepeleva, Е. V., Dokuchaeva, A. A., Bukreeva, L. N., & Sergeevichev, D. S. (2020). Effects of biocidal solutions and wet tissue treatment on the biological properties of porcine aortic wall. Complex Issues of Cardiovasc Diseases, 9, 63–73. https://doi.org/10.17802/2306-1278-2020-9-1-63-73(In Russ.).

    Article  Google Scholar 

  12. Lichtenberg, A., Tudorache, I., Cebotari, S., Ringes-Lichtenberg, S., & Sturz, G. (2006). In vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. Biomaterials, 27, 4221–4229. https://doi.org/10.1016/j.biomaterials.200603.047.

    Article  CAS  PubMed  Google Scholar 

  13. Krasilnikova, A., Sergeevichev, D., Fomenko, V., Korobeynikov, A., Vasiliyeva, M., Yunoshev, A., Karaskov, A., & Pokushalov, E. (2018). Globular chitosan treatment of bovine jugular veins: evidence of anticalcification efficacy in the subcutane-ous rat model. Cardiovascular Pathology, 32, 1–7. https://doi.org/10.1016/j.carpath.2017.08.003.

    Article  CAS  PubMed  Google Scholar 

  14. Zhuravleva, I. Y. (2016). Biocidal composition for aseptic storage of prosthetic material from animal tissue. Patent for invention RU 2580621C1. Bull, 10, 1–10.

    Google Scholar 

  15. Shavandi, A., Bekhit, A. E. A., Saeedi, P., Izadifar, Z., Bekhit, A. A., & Khademhosseini, A. (2018). Polyphenol uses in biomaterials engineering. Biomaterials, 167, 91–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Theodoridis, K., Müller, J., Ramm, R., Findeisen, K., Andrée, B., Korossis, S., Haverich, A., & Hilfiker, A. (2016). Effects of combined cryopreservation and decellularization on the biomechanical, structural and biochemical properties of porcine pulmonary heart valves. Acta Biomaterialia, 43, 71–77. https://doi.org/10.1016/j.actbio.2016.07.013.

    Article  CAS  PubMed  Google Scholar 

  17. Collatusso, C., Roderjan, J. G., de Noronha, L., Klosowski, A., Suss, P. H., Guarita-Souza, L. C., & Costa, F. D. A. D. (2019). Decellularization as a method to reduce calcification in bovine pericardium bioprosthetic valves. Interactive Cardiovascular and Thoracic Surgery, 29, 302–311. https://doi.org/10.1093/icvts/ivz041.

    Article  PubMed  Google Scholar 

  18. Huyan, Y., Chang, Y., & Song, J. (2021). Application of homograft valved conduit in cardiac surgery. Frontiers in Cardiovascular Medicine, 8, 740871. https://doi.org/10.3389/fcvm.2021.740871.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dréno, B., Zuberbier, T., Gelmetti, C., Gontijo, G., & Marinovich, M. (2019). Safety review of phenoxyethanol when used as a preservative in cosmetics. Journal of the European Academy of Dermatology and Venereology, 33, 15–24. https://doi.org/10.1111/jdv.15944.

    Article  PubMed  Google Scholar 

  20. Yeo, S. Y., Hamzan, M. I., Sulaiman, W., & Halim, W. A., A.S (2021). The cost-effectiveness of maintaining an inhouse glycerol-preserved skin bank. Burns : Journal Of The International Society for Burn Injuries, 48, 390–395. https://doi.org/10.1016/j.burns.2021.05.001.

    Article  PubMed  Google Scholar 

  21. Ziza, V., Canaud, L., Gandet, T., Molinari, N., Alonso, W., Chastan, R., Branchereau, P., & Picard, E. (2015). Outcomes of cold-stored venous allograft for below-knee bypasses in patients with critical limb ischemia. Journal of Vascular Surgery, 62, 974–983. https://doi.org/10.1016/j.jvs.2015.04.437.

    Article  PubMed  Google Scholar 

  22. Badria, A. F., Koutsoukos, P. G., & Mavrilas, D. (2020). Decellularized tissue-engineered heart valves calcification: what do animal and clinical studies tell us? Journal of Materials Science: Materials in Medicine, 31, 132. https://doi.org/10.1007/s10856-020-06462-x.

    Article  CAS  PubMed  Google Scholar 

  23. Gallyamov, M. O., Chaschin, I. S., Khokhlova, M. A., Grigorev, T. E., Bakuleva, N. P., & Lyutova, I. G. (2014). Collagen tissue treated with chitosan solutions in carbonic acid for improved biological prosthetic heart valves. Materials Science & Engineering C Materials for Biological Applications, 37, 127–140. https://doi.org/10.1016/j.msec.2014.01.017.

    Article  CAS  Google Scholar 

  24. Khorramirouz, R., Go, J. L., Noble, C., Jana, S., Maxson, E., Lerman, A., & Young, M. D. (2018). A novel surgical technique for a rat subcutaneous implantation of a tissue engineered scaffold. Acta Histochemica, 120(3), 282–291. https://doi.org/10.1016/j.acthis.2018.02.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Cramer, M., Chang, J., Li, H., Serrero, A., El-Kurdi, M., Cox, M., Schoen, F. J., & Badylak, S. F. (2022). Tissue response, macrophage phenotype, and intrinsic calcification induced by cardiovascular biomaterials: can clinical regenerative potential be predicted in a rat subcutaneous implant model? Journal of Biomedical Materials Research Part A, 110, 245–256. https://doi.org/10.1002/jbm.a.37280.

    Article  CAS  PubMed  Google Scholar 

  26. Simionescu, D. T. (2004). Prevention of calcification in bioprosthetic heart valves: Challenges and perspectives. Expert Opinion on Biological Therapy, 4(12), 1971–1985. https://doi.org/10.1517/14712598.4.12.1971.

    Article  CAS  PubMed  Google Scholar 

  27. McGregor, C. G. A., Carpentier, A., Lila, N., Logan, J. S., & Byrne, G. W. (2011). Cardiac xenotransplantation technology provides mate-rials for improved bioprosthetic heart valves. The Journal of Thoracic and Cardiovascular Surgery, 141, 269–275. https://doi.org/10.1016/j.jtcvs.2010.08.064.

    Article  CAS  PubMed  Google Scholar 

  28. Kluin, J., et al. (2017). In situ heart valve tissue engineering using a bioresorbable elastomeric implant – from material design to 12 months follow-up in sheep. Biomaterials, 125, 101–117. https://doi.org/10.1016/j.biomaterials.2017.02.007.

    Article  CAS  PubMed  Google Scholar 

  29. Meuris, B., Ozaki, S., Herijgers, P., Verbeken, E., & Flameng, W. (2003). Bioprosthetic tissue calcification: influence of blood contact and arterial pressure. An experimental study in rats and sheep. Journal of Heart Valve Diseases, 12(3), 392–399.

    Google Scholar 

  30. Connolly, J. M., Bakay, M. A., Alferiev, I. S., Gorman, R. C., & Gorman, J. H. (2011). Triglycidylamine cross-linking combined with ethanol inhibits bioprosthetic heart valve calcification. The Annals of Thoracic Surgery, 92(3), 858–865. https://doi.org/10.1016/j.athoracsur.2011.04.104.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Magsumov, T., Ziyinga, L., & Sedov, I. (2020). Comparative study of the protein denaturing ability of different organic cosolvents. International Journal of Biological Macromolecules, 160, 880–888. https://doi.org/10.1016/j.ijbiomac.2020.05.260.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was carried out within the state assignment of Ministry of Health of Russian Federation (theme # 121031300224-1).

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Authors and Affiliations

  1. NMRC named after academician E.N. Meshalkin of the Ministry of Health of the Russian Federation, 15 Rechkunovskaya st, Novosibirsk, Russia, 630055

    David Sergeevichev, Elena Kuznetsova, Maksim Zhulkov, Yanina Rusakova, Elena Chepeleva & Irina Zhuravleva

  2. Zelman Institute for the Medicine and Psychology, Novosibirsk State University, 1, Pirogov st, Novosibirsk, Russia, 630090

    Maria Vasiliyeva

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  1. David Sergeevichev
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by DS, MV and EK. MZ, YR. and EC. conducted animal experiments. DS analysed data and wrote the manuscript. IZ helped material preparation and analysis with constructive discussions All authors read and approved the final manuscript.

Corresponding author

Correspondence to David Sergeevichev.

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Conflict of interest

The authors declare no competing interests regarding this manuscript.

Ethical Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the local ethical committee of NMRC named after academician E.N. Meshalkin of the Ministry of Health of the Russian Federation (approval date 26 Dec 2014, protocol 45).

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Sergeevichev, D., Vasiliyeva, M., Kuznetsova, E. et al. Morphological Post-implantation Features of Aortic Conduits After Long-term wet Storage. J. Med. Biol. Eng. 43, 185–194 (2023). https://doi.org/10.1007/s40846-023-00784-1

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  • DOI: https://doi.org/10.1007/s40846-023-00784-1

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