Skip to main content
Top
Published in: Cardiovascular Intervention and Therapeutics 2/2023

Open Access 18-10-2022 | Angiography | Original Article

Heterogeneous vascular response after implantation of bare nitinol self-expanding stents in the swine femoropopliteal artery

Authors: Osami Kawarada, Fumiyuki Otsuka, Kojiro Miki, Masayasu Ikutomi, Kozo Okada, Soshiro Ogata, Kunihiro Nishimura, Peter J. Fitzgerald, Yasuhiro Honda

Published in: Cardiovascular Intervention and Therapeutics | Issue 2/2023

Login to get access

Abstract

Background

Mechanism of femoropopliteal in-stent restenosis has been underappreciated.

Aim

The aim of this animal study was to elucidate vascular response after femoropopliteal bare nitinol self-expanding stents (SESs) implantation.

Methods

Misago, Smart Flex, or Innova stent was randomly implanted in 36 swine femoropopliteal arteries. At week 4, quantitative vessel analysis (QVA) was performed on 36 legs, of which 18 underwent histological evaluation after angiography. The remaining 18 legs underwent QVA and histological evaluation at week 13.

Results

Fibrin deposition was excessive at week 4. Internal elastic lamina (IEL) progressively enlarged over time, and vessel injury developed from mild level at week 4 to moderate level at week 13. Vessel inflammatory reaction was mild to moderate at week 4, and was moderate to severe at week 13. Increased fibrin deposition was an early-acting, IEL enlargement and increased vessel inflammation were long-acting, and increased vessel injury and giant cells infiltration were late-acting contributors to neointimal hyperplasia (NIH). Stent type altered time-dependent process of vessel injury, vessel inflammation, eosinophils and giant cells infiltration. Misago had less fibrin deposition and vessel enlargement, and less progressive vessel injury, vessel inflammation, and eosinophils and giant cells infiltration. Net lumen as assessed by percent diameter stenosis or minimum lumen diameter was preserved with Misago, but was not preserved with the other stents.

Conclusions

In the context of bare nitinol SES platform with less progressive mechanical stress and inflammatory reaction, the advantage of less NIH outweighed the disadvantage of less vessel enlargement, leading to net lumen preservation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gouëffic Y, Sauguet A, Desgranges P, Feugier P, Rosset E, Ducasse E, Kaladji A. Salomon du Mont L, Pernès JM, Commeau P, Lermusiaux P, Leclere B, Guyomarc’h B, Hoffmann CT, Maurel B. A polymer-free paclitaxel-eluting stent versus a bare-metal stent for de novo femoropopliteal lesions: the BATTLE trial. JACC Cardiovasc Interv. 2020;13:447–57.CrossRefPubMed Gouëffic Y, Sauguet A, Desgranges P, Feugier P, Rosset E, Ducasse E, Kaladji A. Salomon du Mont L, Pernès JM, Commeau P, Lermusiaux P, Leclere B, Guyomarc’h B, Hoffmann CT, Maurel B. A polymer-free paclitaxel-eluting stent versus a bare-metal stent for de novo femoropopliteal lesions: the BATTLE trial. JACC Cardiovasc Interv. 2020;13:447–57.CrossRefPubMed
2.
go back to reference Ding Y, Zhou M, Wang Y, Cai L, Shi Z. Comparison of drug-eluting stent with bare-metal stent implantation in femoropopliteal artery disease: a systematic review and meta-analysis. Ann Vasc Surg. 2018;50:96–105.CrossRefPubMed Ding Y, Zhou M, Wang Y, Cai L, Shi Z. Comparison of drug-eluting stent with bare-metal stent implantation in femoropopliteal artery disease: a systematic review and meta-analysis. Ann Vasc Surg. 2018;50:96–105.CrossRefPubMed
3.
go back to reference Müller-Hülsbeck S, Benko A, Soga Y, Fujihara M, Iida O, Babaev A, O’Connor D, Zeller T, Dulas DD, Diaz-Cartelle J, Gray WA. Two-year efficacy and safety results from the IMPERIAL randomized study of the Eluvia polymer-coated drug-eluting stent and the Zilver PTX polymer-free drug-coated stent. Cardiovasc Intervent Radiol. 2021;44:368–75.CrossRefPubMed Müller-Hülsbeck S, Benko A, Soga Y, Fujihara M, Iida O, Babaev A, O’Connor D, Zeller T, Dulas DD, Diaz-Cartelle J, Gray WA. Two-year efficacy and safety results from the IMPERIAL randomized study of the Eluvia polymer-coated drug-eluting stent and the Zilver PTX polymer-free drug-coated stent. Cardiovasc Intervent Radiol. 2021;44:368–75.CrossRefPubMed
4.
go back to reference Mozersky DJ, Sumner DS, Hokanson DE, Strandness DE Jr. Transcutaneous measurement of the elastic properties of the human femoral artery. Circulation. 1972;46:948–55.CrossRefPubMed Mozersky DJ, Sumner DS, Hokanson DE, Strandness DE Jr. Transcutaneous measurement of the elastic properties of the human femoral artery. Circulation. 1972;46:948–55.CrossRefPubMed
5.
go back to reference MacTaggart J, Poulson W, Seas A, Deegan P, Lomneth C, Desyatova A, Maleckis K, Kamenskiy A. Stent design affects femoropopliteal artery deformation. Ann Surg. 2019;270:180–7.CrossRefPubMed MacTaggart J, Poulson W, Seas A, Deegan P, Lomneth C, Desyatova A, Maleckis K, Kamenskiy A. Stent design affects femoropopliteal artery deformation. Ann Surg. 2019;270:180–7.CrossRefPubMed
6.
go back to reference Otsuka F, Nakano M, Sakakura K, Ladich E, Kolodgie FD, Virmani R. Unique demands of the femoral anatomy and pathology and the need for unique interventions. J Cardiovasc Surg (Torino). 2013;54:191–210.PubMed Otsuka F, Nakano M, Sakakura K, Ladich E, Kolodgie FD, Virmani R. Unique demands of the femoral anatomy and pathology and the need for unique interventions. J Cardiovasc Surg (Torino). 2013;54:191–210.PubMed
7.
go back to reference Gasior P, Cheng Y, Valencia AF, McGregor J, Conditt GB, Kaluza GL, Granada JF. Impact of fluoropolymer-based paclitaxel delivery on neointimal Proliferation and vascular healing: a comparative peripheral drug-eluting stent study in the familial hypercholesterolemic swine model of femoral restenosis. Circ Cardiovasc Interv. 2017;10:e004450.CrossRefPubMed Gasior P, Cheng Y, Valencia AF, McGregor J, Conditt GB, Kaluza GL, Granada JF. Impact of fluoropolymer-based paclitaxel delivery on neointimal Proliferation and vascular healing: a comparative peripheral drug-eluting stent study in the familial hypercholesterolemic swine model of femoral restenosis. Circ Cardiovasc Interv. 2017;10:e004450.CrossRefPubMed
8.
go back to reference Sakamoto A, Torii S, Jinnouchi H, Fuller D, Cornelissen A, Sato Y, Kuntz S, Mori M, Kawakami R, Kawai K, Fernandez R, Paek KH, Gadhoke N, Guo L, Kolodgie FD, Young B, Ragheb A, Virmani R, Finn AV. Vascular response of a polymer-free paclitaxel-coated stent (Zilver PTX) versus a polymer-coated paclitaxel-eluting stent (Eluvia) in healthy swine femoropopliteal arteries. J Vasc Interv Radiol. 2021;32:792-801.e5.CrossRefPubMed Sakamoto A, Torii S, Jinnouchi H, Fuller D, Cornelissen A, Sato Y, Kuntz S, Mori M, Kawakami R, Kawai K, Fernandez R, Paek KH, Gadhoke N, Guo L, Kolodgie FD, Young B, Ragheb A, Virmani R, Finn AV. Vascular response of a polymer-free paclitaxel-coated stent (Zilver PTX) versus a polymer-coated paclitaxel-eluting stent (Eluvia) in healthy swine femoropopliteal arteries. J Vasc Interv Radiol. 2021;32:792-801.e5.CrossRefPubMed
9.
go back to reference Wressnegger A, Kaider A, Funovics MA. Self-expanding nitinol stents of high versus low chronic outward force in de novo femoropopliteal occlusive arterial lesions (BIOFLEX-COF trial): study protocol for a randomized controlled trial. Trials. 2017;18:594.CrossRefPubMedPubMedCentral Wressnegger A, Kaider A, Funovics MA. Self-expanding nitinol stents of high versus low chronic outward force in de novo femoropopliteal occlusive arterial lesions (BIOFLEX-COF trial): study protocol for a randomized controlled trial. Trials. 2017;18:594.CrossRefPubMedPubMedCentral
10.
go back to reference Schwartz RS, Huber KC, Murphy JG, Edwards WD, Camrud AR, Vlietstra RE, Holmes DR. Restenosis and the proportional neointimal response to coronary artery injury: results in a porcine model. J Am Coll Cardiol. 1992;19:267–74.CrossRefPubMed Schwartz RS, Huber KC, Murphy JG, Edwards WD, Camrud AR, Vlietstra RE, Holmes DR. Restenosis and the proportional neointimal response to coronary artery injury: results in a porcine model. J Am Coll Cardiol. 1992;19:267–74.CrossRefPubMed
11.
go back to reference Otsuka F, Vorpahl M, Nakano M, Foerst J, Newell JB, Sakakura K, Kutys R, Ladich E, Finn AV, Kolodgie FD, Virmani R. Pathology of second-generation everolimus-eluting stents versus first-generation sirolimus- and paclitaxel-eluting stents in humans. Circulation. 2014;129:211–23.CrossRefPubMed Otsuka F, Vorpahl M, Nakano M, Foerst J, Newell JB, Sakakura K, Kutys R, Ladich E, Finn AV, Kolodgie FD, Virmani R. Pathology of second-generation everolimus-eluting stents versus first-generation sirolimus- and paclitaxel-eluting stents in humans. Circulation. 2014;129:211–23.CrossRefPubMed
12.
go back to reference Chaabane C, Otsuka F, Virmani R, Bochaton-Piallat ML. Biological responses in stented arteries. Cardiovasc Res. 2013;99:353–63.CrossRefPubMed Chaabane C, Otsuka F, Virmani R, Bochaton-Piallat ML. Biological responses in stented arteries. Cardiovasc Res. 2013;99:353–63.CrossRefPubMed
13.
go back to reference Tsai YT, Zhou J, Weng H, Tang EN, Baker DW, Tang L. Optical imaging of fibrin deposition to elucidate participation of mast cells in foreign body responses. Biomaterials. 2014;35:2089–96.CrossRefPubMed Tsai YT, Zhou J, Weng H, Tang EN, Baker DW, Tang L. Optical imaging of fibrin deposition to elucidate participation of mast cells in foreign body responses. Biomaterials. 2014;35:2089–96.CrossRefPubMed
14.
go back to reference Farb A, Sangiorgi G, Carter AJ, Walley VM, Edwards WD, Schwartz RS, Virmani R. Pathology of acute and chronic coronary stenting in humans. Circulation. 1999;99:44–52.CrossRefPubMed Farb A, Sangiorgi G, Carter AJ, Walley VM, Edwards WD, Schwartz RS, Virmani R. Pathology of acute and chronic coronary stenting in humans. Circulation. 1999;99:44–52.CrossRefPubMed
15.
go back to reference Carter AJ, Laird JR, Farb A, Kufs W, Wortham DC, Virmani R. Morphologic characteristics of lesion formation and time course of smooth muscle cell proliferation in a porcine proliferative restenosis model. J Am Coll Cardiol. 1994;24:1398–405.CrossRefPubMed Carter AJ, Laird JR, Farb A, Kufs W, Wortham DC, Virmani R. Morphologic characteristics of lesion formation and time course of smooth muscle cell proliferation in a porcine proliferative restenosis model. J Am Coll Cardiol. 1994;24:1398–405.CrossRefPubMed
16.
go back to reference Steigerwald K, Ballke S, Quee SC, Byrne RA, Vorpahl M, Vogeser M, Kolodgie F, Virmani R, Joner M. Vascular healing in drug-eluting stents: differential drug-associated response of limus-eluting stents in a preclinical model of stent implantation. EuroIntervention. 2012;8:752–9.CrossRefPubMed Steigerwald K, Ballke S, Quee SC, Byrne RA, Vorpahl M, Vogeser M, Kolodgie F, Virmani R, Joner M. Vascular healing in drug-eluting stents: differential drug-associated response of limus-eluting stents in a preclinical model of stent implantation. EuroIntervention. 2012;8:752–9.CrossRefPubMed
17.
go back to reference Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002;105:2974–80.CrossRefPubMed Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002;105:2974–80.CrossRefPubMed
18.
go back to reference Otsuka F, Pacheco E, Perkins LE, Lane JP, Wang Q, Kamberi M, Frie M, Wang J, Sakakura K, Yahagi K, Ladich E, Rapoza RJ, Kolodgie FD, Virmani R. Long-term safety of an everolimus-eluting bioresorbable vascular scaffold and the cobalt-chromium XIENCE V stent in a porcine coronary artery model. Circ Cardiovasc Interv. 2014;7:330–42.CrossRefPubMed Otsuka F, Pacheco E, Perkins LE, Lane JP, Wang Q, Kamberi M, Frie M, Wang J, Sakakura K, Yahagi K, Ladich E, Rapoza RJ, Kolodgie FD, Virmani R. Long-term safety of an everolimus-eluting bioresorbable vascular scaffold and the cobalt-chromium XIENCE V stent in a porcine coronary artery model. Circ Cardiovasc Interv. 2014;7:330–42.CrossRefPubMed
19.
go back to reference Buszman PP, Michalak MJ, Pruski M, Fernandez C, Jelonek M, Janas A, Savard C, Gwiazdowska-Nowotka B, Żurakowski A, Wojakowski W, Buszman PE, Milewski K. Comparable vascular response of a new generation sirolimus eluting stents when compared to fluoropolymer everolimus eluting stents in the porcine coronary restenosis model. Cardiol J. 2016;23:657–66.CrossRefPubMed Buszman PP, Michalak MJ, Pruski M, Fernandez C, Jelonek M, Janas A, Savard C, Gwiazdowska-Nowotka B, Żurakowski A, Wojakowski W, Buszman PE, Milewski K. Comparable vascular response of a new generation sirolimus eluting stents when compared to fluoropolymer everolimus eluting stents in the porcine coronary restenosis model. Cardiol J. 2016;23:657–66.CrossRefPubMed
20.
go back to reference Karas SP, Gravanis MB, Santoian EC, Robinson KA, Anderberg KA, King SB III. Coronary intimal proliferation after balloon injury and stenting in swine: an animal model of restenosis. J Am Coll Cardiol. 1992;20:467–74.CrossRefPubMed Karas SP, Gravanis MB, Santoian EC, Robinson KA, Anderberg KA, King SB III. Coronary intimal proliferation after balloon injury and stenting in swine: an animal model of restenosis. J Am Coll Cardiol. 1992;20:467–74.CrossRefPubMed
21.
go back to reference Hoffmann R, Mintz GS, Mehran R, Kent KM, Pichard AD, Satler LF, Leon MB. Tissue proliferation within and surrounding Palmaz-Schatz stents is dependent on the aggressiveness of stent implantation technique. Am J Cardiol. 1999;83:1170–4.CrossRefPubMed Hoffmann R, Mintz GS, Mehran R, Kent KM, Pichard AD, Satler LF, Leon MB. Tissue proliferation within and surrounding Palmaz-Schatz stents is dependent on the aggressiveness of stent implantation technique. Am J Cardiol. 1999;83:1170–4.CrossRefPubMed
22.
go back to reference Kobayashi Y, Honda Y, Christie GL, Teirstein PS, Bailey SR, Brown CL 3rd, Matthews RV, De Franco AC, Schwartz RS, Goldberg S, Popma JJ, Yock PG, Fitzgerald PJ. Long-term vessel response to a self-expanding coronary stent: a serial volumetric intravascular ultrasound analysis from the ASSURE Trial. A Stent vs. Stent ultrasound remodeling evaluation. J Am Coll Cardiol. 2001;37:1329–34.CrossRefPubMed Kobayashi Y, Honda Y, Christie GL, Teirstein PS, Bailey SR, Brown CL 3rd, Matthews RV, De Franco AC, Schwartz RS, Goldberg S, Popma JJ, Yock PG, Fitzgerald PJ. Long-term vessel response to a self-expanding coronary stent: a serial volumetric intravascular ultrasound analysis from the ASSURE Trial. A Stent vs. Stent ultrasound remodeling evaluation. J Am Coll Cardiol. 2001;37:1329–34.CrossRefPubMed
23.
go back to reference Gunn J, Arnold N, Chan KH, Shepherd L, Cumberland DC, Crossman DC. Coronary artery stretch versus deep injury in the development of in-stent neointima. Heart. 2002;88:401–5.CrossRefPubMedPubMedCentral Gunn J, Arnold N, Chan KH, Shepherd L, Cumberland DC, Crossman DC. Coronary artery stretch versus deep injury in the development of in-stent neointima. Heart. 2002;88:401–5.CrossRefPubMedPubMedCentral
24.
go back to reference Russo RJ, Silva PD, Yeager M. Coronary artery overexpansion increases neointimal hyperplasia after stent placement in a porcine model. Heart. 2007;93:1609–15.CrossRefPubMedPubMedCentral Russo RJ, Silva PD, Yeager M. Coronary artery overexpansion increases neointimal hyperplasia after stent placement in a porcine model. Heart. 2007;93:1609–15.CrossRefPubMedPubMedCentral
25.
go back to reference Kornowski R, Hong MK, Tio FO, Bramwell O, Wu H, Leon MB. In-stent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J Am Coll Cardiol. 1998;31:224–30.CrossRefPubMed Kornowski R, Hong MK, Tio FO, Bramwell O, Wu H, Leon MB. In-stent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J Am Coll Cardiol. 1998;31:224–30.CrossRefPubMed
26.
go back to reference Joner M, Finn AV, Farb A, Mont EK, Kolodgie FD, Ladich E, Kutys R, Skorija K, Gold HK, Virmani R. Pathology of drug-eluting stents in humans: delayed healing and late thrombotic risk. J Am Coll Cardiol. 2006;48:193–202.CrossRefPubMed Joner M, Finn AV, Farb A, Mont EK, Kolodgie FD, Ladich E, Kutys R, Skorija K, Gold HK, Virmani R. Pathology of drug-eluting stents in humans: delayed healing and late thrombotic risk. J Am Coll Cardiol. 2006;48:193–202.CrossRefPubMed
27.
go back to reference Mori H, Atmakuri DR, Torii S, Braumann R, Smith S, Jinnouchi H, Gupta A, Harari E, Shkullaku M, Kutys R, Fowler D, Romero M, Virmani R, Finn AV. Very late pathological responses to cobalt-chromium everolimus-eluting, stainless steel sirolimus-eluting, and cobalt-chromium bare metal stents in humans. J Am Heart Assoc. 2017;6:e007244.CrossRefPubMedPubMedCentral Mori H, Atmakuri DR, Torii S, Braumann R, Smith S, Jinnouchi H, Gupta A, Harari E, Shkullaku M, Kutys R, Fowler D, Romero M, Virmani R, Finn AV. Very late pathological responses to cobalt-chromium everolimus-eluting, stainless steel sirolimus-eluting, and cobalt-chromium bare metal stents in humans. J Am Heart Assoc. 2017;6:e007244.CrossRefPubMedPubMedCentral
28.
go back to reference Niccoli G, Montone RA, Ferrante G, Crea F. The evolving role of inflammatory biomarkers in risk assessment after stent implantation. J Am Coll Cardiol. 2010;56:1783–93.CrossRefPubMed Niccoli G, Montone RA, Ferrante G, Crea F. The evolving role of inflammatory biomarkers in risk assessment after stent implantation. J Am Coll Cardiol. 2010;56:1783–93.CrossRefPubMed
29.
go back to reference Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20:86–100.CrossRefPubMed Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20:86–100.CrossRefPubMed
30.
go back to reference Palmaz JC, Bailey S, Marton D, Sprague E. Influence of stent design and material composition on procedure outcome. J Vasc Surg. 2002;36:1031–9.CrossRefPubMed Palmaz JC, Bailey S, Marton D, Sprague E. Influence of stent design and material composition on procedure outcome. J Vasc Surg. 2002;36:1031–9.CrossRefPubMed
Metadata
Title
Heterogeneous vascular response after implantation of bare nitinol self-expanding stents in the swine femoropopliteal artery
Authors
Osami Kawarada
Fumiyuki Otsuka
Kojiro Miki
Masayasu Ikutomi
Kozo Okada
Soshiro Ogata
Kunihiro Nishimura
Peter J. Fitzgerald
Yasuhiro Honda
Publication date
18-10-2022
Publisher
Springer Nature Singapore
Published in
Cardiovascular Intervention and Therapeutics / Issue 2/2023
Print ISSN: 1868-4300
Electronic ISSN: 1868-4297
DOI
https://doi.org/10.1007/s12928-022-00889-5

Other articles of this Issue 2/2023

Cardiovascular Intervention and Therapeutics 2/2023 Go to the issue