Results of long-term patency and lifetime visualization of vascular patches from silk fibroin

• Kolesnikov A.Yu.
• Prokudina E.S.
• Senokosova E.A.
• Arnt A.A.
• Antonova L.V.
• Mironov A.V.
• Krivkina E.O.
• Kochergin N.A.

Abstract

Background. Vascular patches used in reconstructive operations are not optimal due to the differences in the compliance of the material and tissues of the artery wall. The main disadvantages are frequent thrombosis, aneurysms and restenosis in the anastomosis zone. The problem of assessing their functioning and endothelialization at different periods after implantation is also relevant. One of the solutions is optical coherence tomography (OCT).

Aim of the study was to evaluate the results of long-term patency and lifetime visualization of vessels with silk fibroin (SF) patches, as well as to substantiate the possibility of using OCT to assess the functioning and endothelialization of vascular patches in an experiment on large laboratory animals.

Material and methods. SF vascular patches were made by electrospinning. For comparison, flaps from the bovine xenopericardium (XP) were used. Vascular patches (n=4) were implanted into the carotid artery wall of sheep for a period of 2 and 6 months. A lifetime assessment of patched vascular patency was performed using ultrasound. The functioning and endothelialization of the vascular patches in the carotid artery were studied using OCT. After explantation, patches of SF and XP were studied using histological examination methods.

Results. According to ultrasound data, all vessels with patches at the time of 2 and 6 months were passable, hematomas and aneurysms were not detected. According to OCT data, after 2 months of implantation, neointimal hyperplasia was observed in the projection of SF patch (mean thickness of neointima 370 µm); on the inner surface of the XP patch, the neointima is heterogeneous, expressed in the anastomotic zone with a thickness of 230 µm. After 6 months of implantation, hyperplasia of the neointima of the carotid artery with a patch of SF was detected (the average thickness of the neointima was 350 µm). Neointima hyperplasia was also detected throughout the inner surface of the XP patch (mean thickness of neointima was 265 µm). The results of the histological examination coincided with the obtained OCT data at all follow-up periods. After 2 months of implantation, uniform hyperplasia of the neointima of the SF patch was detected (neointima thickness from 48 to 122 µm). Hyperplasia of the neointima in the projection of the XP patch was found only in the areas of anastomoses. After 6 months of implantation, a pronounced neointimal hyperplasia was observed on the SF patch (layer thickness up to 835 µm). On the patch from the XP, after 6 months of implantation, neointimal hyperplasia was not pronounced (average 156 μm).

Conclusion. Vascular patches from SF demonstrate their stability within 6 months of implantation into the carotid artery wall, did not violate patency and did not cause vascular aneurysms, but contributed to neointima hyperplasia, without signs of calcification and acute inflammation in the implantation area, which is confirmed by both OCT data and histological examination. Along with this, OCT is an effective method of in vivo evaluation of the functioning and endothelialization of vascular prostheses in the experiment.

Keywords:vascular patches; intravascular imaging methods; optical coherence tomography; experimental medicine; neointima

References

1.     Sevostyanova V.V., Mironov A.V., Antonova L.V., Tarasov R.S. Vascular patches for arterial reconstruction, challenges and advanced technologies. Kompleksnye problemy serdechno-sosudistykh zabolevaniy [Complex Problems of Cardiovascular Diseases]. 2019; 8 (3): 116–29. DOI: https://doi.org/10.17802/2306-1278-2019-8-3-116-129  (in Russian)

2.     Hrbáč T., Fiedler J., Procházka V., Jonszta T., Roubec M., Pakizer D., et al. Comparison of carotid endarterectomy and repeated carotid angioplasty and stenting for in-stent restenosis (CERCAS trial): a randomised study. Stroke Vasc Neurol. 2023; Mar 27: svn-2022-002075. DOI: https://doi.org/10.1136/svn-2022-002075  Epub ahead of print. PMID: 36972920.

3.     Paraskevas K.I., Dardik A., Gloviczki P. Management of restenosis after carotid endarterectomy or stenting. Angiology. 2023; 74 (4): 305–7. DOI: https://doi.org/10.1177/00033197221133945 Epub 2022 Oct 14. PMID: 36239036.

4.     Yarikov A.V., Balyabin A.V., Yashin К.S., Mukhin A.S. Surgical treatment modalities of carotid artery stenosis (review). Sovremennye tekhnologii v meditsine [Modern Technologies in Medicine]. 2015; 7 (4): 189–200. DOI: https://doi.org/10.17691/stm2015.7.4.25  (in Russian)

5.     Fang Q., Gu T., Fan J., Zhang Y., Wang Y., Zhao Y., et al. Evaluation of a hybrid small caliber vascular graft in a rabbit model. J Thorac Cardiovasc Surg. 2020; 159 (2): 461–73. DOI: https://doi.org/10.1016/j.jtcvs.2019.02.083  Epub 2019 Mar 6. PMID: 30981517.

6.     Heindel P., Feliz J.D., Fitzgibbon J.J., Rouanet E., Belkin M., Hentschel D.M., et al. Comparative effectiveness of bovine carotid artery xenograft and polytetrafluoroethylene in hemodialysis access revision. J Vasc Access. 2023; Apr 26: 11297298231170654. DOI: https://doi.org/10.1177/11297298231170654   Epub ahead of print. PMID: 37125779.

7.     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): 221–6. PMID: 27099058.

8.     Singh R., Eitler D., Morelle R., et al. Optimization of cell seeding on electrospun PCL-silk fibroin scaffolds. Eur Polymer J. 2020; 134: 109838.

9.     Sun W., Zhang Y., Gregory D.A., Jimenez-Franco A., Tomeh M.A., Lv S., et al. Patterning the neuronal cells via inkjet printing of self-assembled peptides on silk scaffolds. Prog Nat Sci Mater Int. 2020; 30: 686–96.

10. Kopp A., Smeets R., Gosau M., Kröger N., et al. Effect of process parameters on additive-free electrospinning of regenerated silk fibroin nonwovens. Bioact Mater. 2020; 5 (2): 241–52. DOI: https://doi.org/10.1016/j.bioactmat.2020.01.010  

11. Zhang C., Zhang Y., Shao H., Hu X. Hybrid silk fibers dry-spun from regenerated silk fibroin/graphene oxide aqueous solutions. ACS Appl Mater Interfaces. 2016; 8: 3349–58.

12. Kitpipatkun P., Sutummaporn K., Kato K., Murakami T., Kobayashi K., Nakazawa Y., et al. Silk fibroin/polyurethane patch implantation in hyperglycemic rat model. J Biomater Appl. 2021; 36 (4): 701–13. DOI: https://doi.org/10.1177/0885328221999227  Epub 2021 Mar 2. PMID: 33653156.

13. Bai J., Li H., Wang L., Shi Y., Su X., Xu C., et al. Effect of silk fibroin scaffold loaded with 17-β estradiol on the proliferation and differentiation of BMSCs. Regen Ther. 2023; 23: 76–83. DOI: https://doi.org/10.1016/j.reth.2023.03.002  PMID: 37131535; PMCID: PMC10149272.

14. Raber L., Mintz G.S., Koskinas K.C., Johnson T.W., Holm N.R., Onuma Y., et al.; ESC Scientific Document Group. Clinical use of intracoronary imaging. Part 1: guidance and optimization of coronary interventions. An expert consensus document of the European Association of Percutaneous Cardiovascular Interventions. Eur Heart J. 2018; 39: 3281–300. DOI: https://doi.org/10.1093/eurheartj/ehy285  

15. Tarkin J.M., Dweck M.R., Evans N.R., et al. Imaging atherosclerosis. Circ Res. 2016; 118: 750–69. DOI: https://doi.org/10.1161/CIRCRESAHA.115.306247  

16. Yabushita H., Bouma B.E., Houser S.L., et al. Characterization of human atherosclerosis by optical coherence tomography. Circulation. 2002; 106: 1640–5. DOI: https://doi.org/10.1161/01.cir.0000029927.92825.f6  

17. Kochergin N.A., Kochergina A.M. Potential of optical coherence tomography and intravascular ultrasound in the detection of vulnerable plaques in coronary arteries. Kardiovaskulyarnaya terapiya i profilaktika [Cardiovascular Therapy and Prevention]. 2022; 21 (1): 101–6. DOI: https://doi.org/10.15829/1728-8800-2022-2909  (in Russian)

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