Features of polyurethane and xenopericardial patch remodeling using a large animal model as an example

Objective: to compare the remodeling features of polyurethane (PU) and bovine pericardium (BP) patches that have been implanted in a sheep carotid artery for 6 months. Materials and methods. Synthetic matrices were fabricated from a 12% PU solution in chloroform by electrospinning on a Nanon-01A machine (MECC, Japan). Biological matrices made from commercially produced PU (Kem-Periplas Neo, CJSC Neocor, Russia) were used for comparison. The matrices were implanted as vascular patches into sheep carotid arteries (n = 3). Implantation period was 6 months. Via ultrasound scan, the patency of arteries bearing the implanted vascular prostheses was evaluated. After removal, the matrix samples were studied by histological examination, scanning electron microscopy and confocal microscopy. Prior to this, they had been stained with specific fluorescently labeled antibodies. The GraphPad Prism 8 application was used to process statistical data. Results. The sheep carotid artery wall was completely patent, with no aneurysmal dilatations, significant stenoses, and hematomas six months after the PU and BP matrices were implanted. The PU matrix was distinguished by a less pronounced connective-tissue capsule and no neointima hyperplasia; the thickness of the remodeled PU wall was 731.2 (711.5; 751.3) μm. At the same time, there was BP neointimal hyperplasia with a thickness of 627 (538; 817) μm and a remodeled wall thickness of 1723 (1693; 1772) μm. In comparison to BP, the PU matrix exhibited greater endothelialization and structural integrity. Conclusion. An in vivo study on sheep demonstrated the potential of PU matrix, a novel and effective material for vascular reconstruction, to maintain harmonious remodeling, bioinertness and structural integrity when in contact with blood. Due to its excellent elastic qualities and durability, PU is interesting both as a monocomponent and as a component of a composite material that can be used to create products for the needs of cardiovascular surgery.

1. Virani SS, Alonso A, Benjamin EJ, Bittencourt MS, Callaway CW, Carson AP et al. Heart Disease and Stroke Statistics-2020 Update: A Report From the American Heart Association. Circulation. 2020; 141 (9): e139– e596. doi: 10.1161/CIR.0000000000000757.

2. Feigin VL, Brainin M, Norrving B, Martins S, Sacco RL, Hacke W et al. World Stroke Organization (WSO): Global Stroke Fact Sheet 2022. Int J Stroke. 2022; 17 (1): 18–29. doi: 10.1177/17474930211065917.

3. Pashneh-Tala S., MacNeil S., Claeyssens F. The TissueEngineered Vascular Graft-Past, Present, and Future. Tissue Eng Part B Rev. 2016; 22 (1): 68–100. doi: 10.1089/ten.teb.2015.0100.

4. Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP et al. Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association. Circulation. 2019; 139 (10): 56–528. doi: 10.1161/CIR.0000000000000659.

5. Roth GA, Mensah GA, Johnson CO, Addolorato G, Ammirati E, Baddour LM et al. Global Burden of Cardiovascular Diseases and Risk Factors, 1990–2019: Update From the GBD 2019 Study. J Am Coll Cardiol. 2020; 76 (25): 2982–3021. doi: 10.1016/j.jacc.2020.11.010.

6. Yarikov AV, Balyabin AV, Yashin КS, Mukhin AS. Surgical Treatment Modalities of Carotid Artery Stenosis (Review). Modern Technologies in Medicine. 2015; 7 (4): 189–200. doi: 10.17691/stm2015.7.4.25.

7. Muto A, Nishibe T, Dardik H, Dardik A. Patches for carotid artery endarterectomy: current materials and prospects. J Vasc Surg. 2009; 50 (1): 206–213. doi: 10.1016/j.jvs.2009.01.062.

8. Chernyavskiy AM, Larionov PM, Stolyarov MS, Starodubtsev VB. Structural transformation of xenopericardium after implantation into the carotid artery (prospective study). Pathology of blood circulation and cardiac surgery. 2007; 4: 37–40.

9. Kudryavtseva Yu.A. Bioprosthetic heart valves. From idea to clinical use. Complex Issues of Cardiovascular Diseases. 2015; (4): 6–16. (In Russ.). doi: 10.17802/2306-1278-2015-4-6-16.

10. Rezvova MA, Ovcharenko EA, Glushkova TV, Kudryavtseva YuA, Barbarash LS. Evaluation of calcification resistance of xenopericardium treated with polyhydroxy compounds. Russian Journal of Transplantology and Artificial Organs. 2021; 23 (1): 75–83. doi: 10.15825/1995-1191-2021-1-75-83.

11. Weber SS, Annenberg AJ, Wright CB, Braverman TS, Mesh CL. Early pseudoaneurysm degeneration in biologic extracellular matrix patch for carotid repair. J Vasc Surg. 2014; 59 (4): 1116–1118. doi: 10.1016/j.jvs.2013.05.012.

12. Fokin AA, Kuvatov AV. Remote results of carotid artery reconstructions using a patch. Journal of Experimental and Clinical Surgery. 2013; 6 (2): 239–243.

13. Ren S, Li X, Wen J, Zhang W, Liu P. Systematic review of randomized controlled trials of different types of patch materials during carotid endarterectomy. PLoS One. 2013; 8 (1): e55050. doi: 10.1371/journal.pone.0055050.

14. Alawy M, Tawfick W, ElKassaby M, Shalaby A, Zaki M, Hynes N, Sultan S. Late Dacron Patch Inflammatory Reaction after Carotid Endarterectomy. Eur J Vasc Endovasc Surg. 2017; 54 (4): 423–429. doi: 10.1016/j.ejvs.2017.06.015.

15. Xu JH, Altaf N, Tosenovsky P, Mwipatayi BP. Management challenges of late presentation Dacron patch infection after carotid endarterectomy. BMJ Case Rep. 2017; 2017: bcr2017221541. doi: 10.1136/bcr-2017-221541.

16. Rerkasem K, Rothwell PM. Systematic review of randomized controlled trials of patch angioplasty versus primary closure and different types of patch materials during carotid endarterectomy. Asian J Surg. 2011; 34 (1): 32–40. doi: 10.1016/S1015-9584(11)60016-X.

17. Kucinska-Lipka J, Gubanska I, Janik H, Sienkiewicz M. Fabrication of polyurethane and polyurethane based composite fibres by the electrospinning technique for soft tissue engineering of cardiovascular system. Mater Sci Eng C Mater Biol Appl. 2015; 46: 166–176. doi: 10.1016/j.msec.2014.10.027.

18. LaPorte RJ. Hydrophilic polymer coatings for medical devices. Routledge. 2017; 11–16. doi: 10.1201/9780203751381.

19. Kheradvar A, Groves EM, Dasi LP, Alavi SH, Tranquillo R, Grande-Allen KJ et al. Emerging trends in heart valve engineering: Part I. Solutions for future. Ann Biomed Eng. 2015; 43 (4): 833–843. doi: 10.1007/s10439-014-1209-z.

20. Bergmeister H, Grasl C, Walter I, Plasenzotti R, Stoiber M, Schreiber C et al. Electrospun small-diameter polyurethane vascular grafts: ingrowth and differentiation of vascular-specific host cells. Artif Organs. 2012; 36 (1): 54–61. doi: 10.1111/j.1525-1594.2011.01297.x.

21. Grasl C, Bergmeister H, Stoiber M, Schima H, Weigel G. Electrospun polyurethane vascular grafts: in vitro mechanical behavior and endothelial adhesion molecule expression. J Biomed Mater Res A. 2010; 93 (2): 716–723. doi: 10.1002/jbm.a.32584.

22. Bergmeister H, Schreiber C, Grasl C, Walter I, Plasenzotti R, Stoiber M et al. Healing characteristics of electrospun polyurethane grafts with various porosities. Acta Biomater. 2013; 9 (4): 6032–6040. doi: 10.1016/j.actbio.2012.12.009.

23. Schleimer K, Jalaie H, Afify M, Woitok A, Barbati ME, Hoeft K et al. Sheep models for evaluation of novel patch and prosthesis material in vascular surgery: tips and tricks to avoid possible pitfalls. Acta Vet Scand. 2018; 60 (1): 42. doi: 10.1186/s13028-018-0397-1.

24. Antonova LV, Mironov AV, Yuzhalin AE, Krivkina EO, Shabaev AR, Rezvova MA et al. A Brief Report on an Implantation of Small-Caliber Biodegradable Vascular Grafts in a Carotid Artery of the Sheep. Pharmaceuticals (Basel). 2020 May 21; 13 (5): 101. doi: 10.3390/ph13050101.

25. Antonova L, Kutikhin A, Sevostianova V, Lobov A, Repkin E, Krivkina E et al. Controlled and Synchronised Vascular Regeneration upon the Implantation of Iloprost- and Cationic Amphiphilic Drugs-Conjugated Tissue-Engineered Vascular Grafts into the Ovine Carotid Artery: A Proteomics-Empowered Study. Polymers (Basel). 2022 Nov 26; 14 (23): 5149. doi: 10.3390/polym14235149.

26. Antonova L, Kutikhin A, Sevostianova V, Velikanova E, Matveeva V, Glushkova T et al. bFGF and SDF-1α Improve In Vivo Performance of VEGF-Incorporating SmallDiameter Vascular Grafts. Pharmaceuticals (Basel). 2021 Mar 28; 14 (4): 302. doi: 10.3390/ph14040302.

27. Terakawa K, Yamauchi H, Lee Y, Ono M. A Novel Knitted Polytetrafluoroethylene Patch for Cardiovascular Surgery. Int Heart J. 2022; 63 (1): 122–130. doi: 10.1536/ihj.21-564.

28. Liesker DJ, Gareb B, Looman RS, Donners SJA, de Borst GJ, Zeebregts CJ, Saleem BR. Patch angioplasty during carotid endarterectomy using different materials has similar clinical outcomes. J Vasc Surg. 2023; 77 (2): 559–566.e1. doi: 10.1016/j.jvs.2022.09.027.

29. 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.

30. Fadeeva IS, Sorkomov MN, Zvyagina AI, Britikov DV, Sachkov AS, Evstratova YaV et al. Study of Biointegration and Elastic-Strength Properties of a New Xenopericardium-Based Biomaterial for Reconstructive Cardiovascular Surgery. Bull Exp Biol Med. 2019; 167 (4): 496–499. doi: 10.1007/s10517-019-04558-1.

31. Lejay A, Bratu B, Kuntz S, Neumann N, Heim F, Chakfé N. Calcification of Synthetic Vascular Grafts: A Systematic Review. EJVES Vasc Forum. 2023; 29 (60): 1–7. doi: 10.1016/j.ejvsvf.2023.05.013.

32. Collins MJ, Li X, Lv W, Yang C, Protack CD, Muto A et al. Therapeutic strategies to combat neointimal hyperplasia in vascular grafts. Expert Rev Cardiovasc Ther. 2012; 10 (5): 635–647. doi: 10.1586/erc.12.33.

33. Senokosova EA, Prokudina ES, Matveeva VG, Velikanova EA, Glushkova TV, Koshelev VA et al. Tissue engineering matrix based on polyurethane: in vitro research. Complex Issues of Cardiovascular Diseases. 2023; 12 (4S): 120–130. [In Russ.]. doi: 10.17802/2306-1278-2023-12-4S-120-130.