Vol. 24 No. 4 (2020)
EXPERIMENTAL STUDIES

Tissue-engineered patch modified by vascular endothelial growth factor for reconstruction of vascular wall

PDF (Русский)
  • V. Sevostianova,
  • A. Mironov,
  • L. Antonova,
  • E. Krivkina,
  • V. Matveeva,
  • E. Velikanova,
  • R. Tarasov,
  • T. Glushkova,
  • L. Barbarash
V. Sevostianova
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
Bio
A. Mironov
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
L. Antonova
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
E. Krivkina
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
V. Matveeva
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
E. Velikanova
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
R. Tarasov
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
T. Glushkova
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
L. Barbarash
Research Institute For Complex Problems Of Cardiovascular Diseases, Kemerovo
DOI: https://doi.org/10.21688/1681-3472-2020-4-114-128

Published 2020-12-30

Keywords

  • biodegradable polymer,
  • endothelialisation,
  • tissue engineering,
  • vascular endothelial growth factor,
  • vascular patch

How to Cite

Sevostianova, V., Mironov, A., Antonova, L., Krivkina, E., Matveeva, V., Velikanova, E., Tarasov, R., Glushkova, T., & Barbarash, L. (2020). Tissue-engineered patch modified by vascular endothelial growth factor for reconstruction of vascular wall. Patologiya Krovoobrashcheniya I Kardiokhirurgiya, 24(4), 114–128. https://doi.org/10.21688/1681-3472-2020-4-114-128

Copyright (c) 2020 Sevostianova V.V., Mironov A.V., Antonova L.V., Krivkina E.O., Matveeva V.G., Velikanova E.A., Tarasov R.S., Glushkova T.V., Barbarash L.S.

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Abstract

Background. Commercially available synthetic and animal-derived vascular patches used in patch angioplasty during carotid endarterectomy have several disadvantages, such as postoperative thrombosis or occlusion and restenosis. This problem may be resolved by the development of biologically active materials that are biodegradable and can stimulate tissue regeneration.
Aim. To evaluate the properties and efficacy of a biodegradable patch based on poly(3-hydroxybutyrate-co-3-hydroxyvalerate) (PHBV) and poly(ε-caprolactone) (PCL) into which vascular endothelial growth factor (VEGF) is incorporated, in comparison with unmodified PHBV/PCL and commercial vascular patches.
Methods. Porous patches were fabricated by emulsion electrospinning from a mixture of PHBV and PCL, into which VEGF was incorporated. The morphological and mechanical properties of these patches were tested, and they were implanted into the wall of rat abdominal aortas for 1, 3, 6 and 12 months. Histological and immunofluorescence examinations were performed to evaluate endothelisation, cellular composition and calcification.
Results. PHBV / PCL patches with VEGF had a highly porous structure and demonstrated tensile strength similar to that of the aorta in rats and the internal thoracic artery in humans. After 3 months of implantation, an endothelial monolayer was formed on the inner surface of these patches. The patches were populated by cells that secreted the extracellular matrix faster than did cells of patches from the xenopericardium. Remodelling with PHBV / PCL patches was not accompanied by chronic inflammation; in contrast, inflammation was observed with long-term implantation of unmodified PHBV / PCL samples.
Conclusion. VEGF incorporated into biodegradable PHBV / PCL patches stimulated their endothelisation, increased their biocompatibility and promoted remodelling and formation of the components of the blood vessel. PHBV / PCL / VEGF patches thus have a high potential for use in tissue engineering of the vascular wall.

Received 2 June 2020. Revised 27 June 2020. Accepted 16 July 2020.

Funding: This study was supported by the Complex Program of Basic Research under the Siberian Branch of the Russian Academy of Sciences within the Basic Research Topic of Research Institute for Complex Issues of Cardiovascular Diseases № 0546-2019-0002 “Pathogenetic basis for the development of cardiovascular implants from biocompatible materials using patient-oriented approach, mathematical modeling, tissue engineering, and genomic predictors”.

Conflict of interest: Authors declare no conflict of interest.

Author contributions
Conception and study design: V.V. Sevostianova, A.V. Mironov, L.V. Antonova, R.S. Tarasov, L.S. Barbarash
Data collection and analysis: V.V. Sevostianova, A.V. Mironov, L.V. Antonova, E.O. Krivkina, V.G. Matveeva, E.A. Velikanova, T.V. Glushkova
Statistical analysis: V.V. Sevostianova, T.V. Glushkova
Drafting the article: V.V. Sevostianova, A.V. Mironov
Critical revision of the article: L.V. Antonova, R.S. Tarasov, L.S. Barbarash
Final approval of the version to be published: V.V. Sevostianova, A.V. Mironov, L.V. Antonova, E.O. Krivkina, V.G. Matveeva, E.A. Velikanova, R.S. Tarasov, T.V. Glushkova, L.S. Barbarash

PDF (Русский)

References

  1. Мартынчик С.А., Соколова О.В. Медико-экономическая оценка и обоснование совершенствования организационных форм оказания стационарной помощи при мозговом инсульте. Социальные аспекты здоровья населения. 2013;2(30):10. [Martynchik S.A., Sokolova O.V. Medical and economic assessment and rationale for improving organization of inpatient care for cerebral stroke. Social Aspects of Population Health. 2013;2(30):10. (In Russ.)]
  2. Леменев В.Л., Лукьянчиков В.А., Беляев А.А. Цереброваскулярные заболевания и стенотическое поражение брахиоцефальных артерий: эпидемиология, клиническая картина, лечение. Consilium Medicum. 2019;21(9):29-32 [Lemenev V.L., Luk'ianchikov V.A., Beliaev A.A. Cerebrovascular disease and stenotic lesion of the brachiocephalic arteries: epidemiology, clinical manifestations, treatment. Consilium Medicum. 2019;21(9):29–32. (In Russ.)]. http://dx.doi.org/10.26442/20751753.2019.9.190611
  3. Bonati L.H., Dobson J., Featherstone R.L., Ederle J., van der Worp H.B., de Borst G.J., Mali W.P.Th.M., Beard J.D., Cleveland T., Engelter S.T., Lyrer P.A., Ford G.A., Dorman P.J., Brown M.M., International Carotid Stenting Study investigators. Long-term outcomes after stenting versus endarterectomy for treatment of symptomatic carotid stenosis: the International Carotid Stenting Study (ICSS) randomised trial. Lancet. 2015;385(9967):529-538. PMID: 25453443, PMCID: PMC4322188. http://dx.doi.org/10.1016/S0140-6736(14)61184-3
  4. Naylor A.R., Ricco J.-B., de Borst G.J., Debus S., de Haro J., Halliday A., Hamilton G., Kakisis J., Kakkos S., Lepidi S., Markus H.S., McCabe D.J., Roy J., Sillesen H., van den Berg J.C., Vermassen F., Esvs Guidelines Committee, Kolh P., Chakfe N., Hinchliffe R.J., Koncar I., Lindholt J.S., Vega de Ceniga M., Verzini F., Esvs Guideline Reviewers, Archie J., Bellmunt S., Chaudhuri A., Koelemay M., Lindahl A.-K., Padberg F., Venermo M. Editor’s choice - management of atherosclerotic carotid and vertebral artery disease: 2017 clinical practice guidelines of the European society for vascular surgery (ESVS). Eur J Vasc Endovasc Surg. 2018;55(1):3-81. PMID: 28851594. http://dx.doi.org/10.1016/j.ejvs.2017.06.021
  5. Печенкин А.А., Лызиков А.А. Каротидная эндартерэктомия: исходы и перспективы. Новости хирургии. 2014;22(2):231-238. [Pechenkin A.A., Lyzikov A.A. Carotid endarterectomy: outcomes and prospects. Novosti Khirurgii. 2014;22(2):231-238. (In Russ.)]
  6. Huizing E., Vos C.G., Hulsebos R.G., van den Akker P.J., Borst G.J., Ünlü Ç. Patch angioplasty or primary closure following carotid endarterectomy for symptomatic carotid artery stenosis. Surg J (N Y). 2018;4(2):e96-e101. PMID: 29915809, PMCID: PMC6003887. http://dx.doi.org/10.1055/s-0038-1655757
  7. Bond R., Rerkasem K., AbuRahma A.F., Naylor A.R., Rothwell P.M. Patch angioplasty versus primary closure for carotid endarterectomy. Cochrane Database Syst Rev. 2004;(2):CD000160. PMID: 15106145. http://dx.doi.org/10.1002/14651858.CD000160.pub2
  8. Rerkasem K., Rothwell P.M. Patch angioplasty versus primary closure for carotid endarterectomy. Cochrane Database Syst Rev. 2009;2009(4):CD000160. PMID: 19821267, PMCID: PMC7078573. http://dx.doi.org/10.1002/14651858.CD000160.pub3
  9. Rerkasem K., Rothwell P.M. 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. PMID: 21515211. http://dx.doi.org/10.1016/S1015-9584(11)60016-X
  10. Olsen S.B., Mcquinn W.C., Feliciano P. Results of carotid endarterectomy using bovine pericardium patch closure, with a review of pertinent literature. Am Surg. 2016;82(3):221-226. PMID: 27099058.
  11. Weber S.S., Annenberg A.J., Wright C.B., Braverman T.S., Mesh C.L. Early pseudoaneurysm degeneration in biologic extracellular matrix patch for carotid repair. J Vasc Surg. 2014;59(4):1116-1118. PMID: 23809202. http://dx.doi.org/10.1016/j.jvs.2013.05.012
  12. 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. PMID: 19563972, PMCID: PMC2759680. http://dx.doi.org/10.1016/j.jvs.2009.01.062
  13. Texakalidis P., Giannopoulos S., Charisis N., Giannopoulos S., Karasavvidis T., Koullias G., Jabbour P. A meta-analysis of randomized trials comparing bovine pericardium and other patch materials for carotid endarterectomy. J Vasc Surg. 2018;68(4):1241-1256. PMID: 30244928. http://dx.doi.org/10.1016/j.jvs.2018.07.023
  14. Harrison G.J., How T.V., Poole R.J., Brennan J.A., Naik J.B., Vallabhaneni S.R., Fisher R.K. Closure technique after carotid endarterectomy influences local hemodynamics. J Vasc Surg. 2014;60(2):418-427. PMID: 24657293. http://dx.doi.org/10.1016/j.jvs.2014.01.069
  15. Talacua H., Smits A.I.P.M., Muylaert D.E.P., van Rijswijk J.W., Vink A., Verhaar M.C., Driessen-Mol A., van Herwerden L.A., Bouten C.V.C., Kluin J., Baaijens F.P.T. In situ tissue engineering of functional small-diameter blood vessels by host circulating cells only. Tissue Eng Part A. 2015;21(19-20):2583-2594. PMID: 26200255. http://dx.doi.org/10.1089/ten.TEA.2015.0066
  16. Lee K.-W., Johnson N.R., Gao J., Wang Y. Human progenitor cell recruitment via SDF-1α coacervate-laden PGS vascular grafts. Biomaterials. 2013;34(38):9877-9885. PMID: 24060423, PMCID: PMC3882008. http://dx.doi.org/10.1016/j.biomaterials.2013.08.082
  17. Smith R.J. Jr, Yi T., Nasiri B., Breuer C.K., Andreadis S.T. Implantation of VEGF-functionalized cell-free vascular grafts: regenerative and immunological response. FASEB J. 2019;33(4):5089-5100. PMID: 30629890, PMCID: PMC6436645. http://dx.doi.org/10.1096/fj.201801856R
  18. Shin Y.M., Lee Y.B., Kim S.J., Kang J.K., Park J.-C., Jang W., Shin H. Mussel-inspired immobilization of vascular endothelial growth factor (VEGF) for enhanced endothelialization of vascular grafts. Biomacromolecules. 2012;13(7):2020-2028. PMID: 22617001. http://dx.doi.org/10.1021/bm300194b
  19. Севостьянова В.В., Васюков Г.Ю., Борисов В.В., Бураго А.Ю., Формокидова Ю.Н., Головкин А.С. Стимуляция ангиогенеза матрицами из поликапролактона, содержащими VEGF. Комплексные проблемы сердечно-сосудистых заболеваний. 2013;4:28-34. [Sevostyanova V.V., Vasukov G.Y., Borisov V.V., Burago A.Y., Formokidova Y.N., Golovkin A.S. Polycaprolactone scaffolds containing VEGF for angiogenesis stimulation. Complex Issues of Cardiovascular Diseases. 2013;4:28-34. (In Russ.)]
  20. Antonova L.V., Sevostyanova V.V., Mironov A.V., Krivkina E.O., Velikanova E.A., Matveeva V.G., Glushkova T.V., Elgudin Y.L., Barbarash L.S. In situ vascular tissue remodeling using biodegradable tubular scaffolds with incorporated growth factors and chemoattractant molecules. Complex Issues of Cardiovascular Diseases. 2018;7(2):25-36. https://doi.org/10.17802/2306-1278-2018-7-2-25-36
  21. Яриков А.В., Балябин А.В., Яшин К.С., Мухин А.С. Хирургические методы лечения стеноза сонных артерий (обзор). Современные технологии в медицине. 2015;7(4):189-200. [Yarikov A.V., Balyabin A.V., Yashin К.S., Mukhin A.S. Surgical treatment modalities of carotid artery stenosis (review). Sovremennye tehnologii v medicine = Modern Technologies in Medicine. 2015;7(4):189-200. (In Russ.)] https://doi.org/10.17691/stm2015.7.4.25
  22. Neethling W.M.L., Hodge A.J., Clode P., Glancy R. A multi-step approach in anti-calcification of glutaraldehyde-preserved bovine pericardium. J Cardiovasc Surg (Torino). 2006;47(6):711-778. PMID: 17043620
  23. Saporito W.F., Pires A.C., Cardoso S.H., Correa J.A., de Abreu L.C., Valenti V.E., Miller L.M.R., Colombari E. Bovine pericardium retail preserved in glutaraldehyde and used as a vascular patch. BMC Surg. 2011;11:37. PMID: 22192162, PMCID: PMC3258210. https://doi.org/10.1186/1471-2482-11-37
  24. 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. PMID: 23383053, PMCID: PMC3561447. https://doi.org/10.1371/journal.pone.0055050
  25. Wu J., Hong Yi. Enhancing cell infiltration of electrospun fibrous scaffolds in tissue regeneration. Bioact Mater. 2016;1(1):56-64. PMID: 29744395, PMCID: PMC5883964. https://doi.org/10.1016/j.bioactmat.2016.07.001
  26. Roussis P.C., Giannakopoulos A.E., Charalambous H.P. Analytical side-to-side related anastomotic strategies and artery patching. Open Biomed Eng J. 2015;9:1-9. PMID: 25949745, PMCID: PMC4415203. https://doi.org/10.2174/1874120701509010001
  27. Глушкова Т.В., Севостьянова В.В., Антонова Л.В., Клышников К.Ю., Овчаренко Е.А., Сергеева Е.А., Васюков Г.Ю., Сейфалиан А.М., Барбараш Л.С. Биомеханическое ремоделирование биодеградируемых сосудистых графтов малого диаметра in situ. Вестник трансплантологии и искусственных органов. 2016;18(2):99-109. [Glushkova T.V., Sevostyanova V.V., Antonova L.V., Klyshnikov K.Y., Ovcharenko E.A., Sergeeva E.A., Vasyukov G.Yu., Seifalian A.M., Barbarash L.S. Biomechanical remodeling of biodegradable small-diameter vascular grafts in situ. Russian Journal of Transplantology and Artificial Organs. 2016;18(2):99-109. (In Russ.)] https://doi.org/10.15825/1995-1191-2016-2-99-109
  28. Pandis L., Zavan B., Bassetto F., Ferroni L., Iacobellis L., Abatangelo G., Lepidi S., Cortivo R., Vindigni V. Hyaluronic acid biodegradable material for reconstruction of vascular wall: a preliminary study in rats. Microsurgery. 2011;31(2):138-145. PMID: 21268111. https://doi.org/10.1002/micr.20856
  29. Ichihara Y., Shinoka T., Matsumura G., Ikada Y., Yamazaki K. A new tissue-engineered biodegradable surgical patch for high-pressure systems. Interact CardioVasc Thorac Surg. 2015;20:768–76. https://doi.org/10.1093/icvts/ivv017
  30. Kim C.-W., Kim M.-K., Kim S.-G., Park Y.-W., Park Y.-T., Kim D.-W., Seok H. Angioplasty using 4-hexylresorcinol-incorporated silk vascular patch in rat carotid defect model. Appl Sci. 2018;8(12):2388. https://doi.org/10.3390/app8122388
  31. Карпенко А.А., Стародубцев В.Б., Игнатенко П.В., Кужугет Р.А., Ким И.Н., Горбатых В.Н. Непосредственные и отдаленные результаты различных методов реконструкции каротидной бифуркации. Патология кровообращения и кардиохирургия. 2013;17(1):21-24. [Karpenko A.A., Starodubtsev V.B., Ignatenko P.V., Kuzhuget R.A., Kim I.N., Gorbatykh V.N. Immediate and long-term outcomes of carotid bifurcation remodeling. Patologiya krovoobrashcheniya i kardiokhirurgiya = Circulation Pathology and Cardiac Surgery. 2013;17(1):21-24. (In Russ.)] http://dx.doi.org/10.21688/1681-3472-2013-1-21-24
  32. Должиков А.А., Колпаков А.Я., Ярош А.Л., Молчанова А.С., Должикова И.Н. Гигантские клетки инородных тел и тканевые реакции на поверхности имплантатов. Курский научно-практический вестник «Человек и его здоровье». 2017;(3):86-94. [Dolzhikov A.A., Kolpakov A.Ya., Yarosh A.L., Molchanova A.S., Dolzhikova I.N. Giant foreign body cells and tissue reactions on the surface of implants. Kursk Scientific and Practical Bulletin «Man and His Health». 2017;(3):86-94. (In Russ.)] https://doi.org/10.21626/vestnik/2017-3/15
  33. Anderson J.M., Jones J.F. Phenotypic dichotomies in the foreign body reaction. Biomaterials. 2007;28(34):5114-5120. PMID: 17706278, PMCID: PMC2248374. https://doi.org/10.1016/j.biomaterials.2007.07.010
  34. Mehta R.I., Mukherjee A.K., Patterson T.D., Fishbein M.C. Pathology of explanted polytetrafluoroethylene vascular grafts. Cardiovasc Pathol. 2011;20(4):213-221. PMID: 20619685. https://doi.org/10.1016/j.carpath.2010.06.005
  35. Li X., Guo Y., Ziegler K.R., Model L.S., Eghbalieh S.D.D., Brenes R.A., Kim S.T., Shu C., Dardik A. Current usage and future directions for the bovine pericardial patch. Ann Vasc Surg. 2011;25(4):561-568. PMID: 21276709, PMCID: PMC3085588. https://doi.org/10.1016/j.avsg.2010.11.007
  36. de Valence S., Tille J.-C., Mugnai D., Mrowczynski W., Gurny R., Möller M., Walpoth B.H. Long term performance of polycaprolactone vascular grafts in a rat abdominal aorta replacement model. Biomaterials. 2012;33(1):38-47. PMID: 21940044. https://doi.org/10.1016/j.biomaterials.2011.09.024
  37. Sugiura T., Tara S., Nakayama H., Yi T., Lee Y.-U., Shoji T., Breuer C.K., Shinoka T. Fast-degrading bioresorbable arterial vascular graft with high cellular infiltration inhibits calcification of the graft. J Vasc Surg. 2017;66(1):243-250. PMID: 27687327, PMCID: PMC5366287. https://doi.org/10.1016/j.jvs.2016.05.096
  38. Fukunishi T., Best C.A., Sugiura T., Shoji T., Yi T., Udelsman B., Ohst D., Ong C.S., Zhang H., Shinoka T., Breuer C.K., Johnson J., Hibino N. Tissue-engineered small diameter arterial vascular grafts from cell-free nanofiber PCL/chitosan scaffolds in a sheep model. PLoS One. 2016;11(7):e0158555. PMID: 27467821, PMCID: PMC4965077. https://doi.org/10.1371/journal.pone.0158555