Experimental models of coronary artery restenosis
DW Muller,
SG Ellis,
and
EJ Topol
Department of Internal Medicine, University of Michigan Medical Center, Ann Arbor 48109-0022.
The study of potentially effective drug therapies and mechanical devices for the prevention of restenosis after percutaneous coronary revascularization has relied heavily on the use of experimental animal models. To date, greater than 50 experimental studies have been reported and have suggested that at least nine different classes of pharmacologic agents inhibit the intimal proliferative response to arterial injury. However, no pharmacologic intervention has yet been shown to reproducibly reduce the incidence of restenosis after coronary balloon angioplasty in humans. To identify the reasons for the apparent nonspecificity of the animal models and to determine which model should most reliably predict the efficacy of individual therapies in humans, the distinguishing characteristics of the experimental models were compared. Particular attention was paid to the size and morphologic structure of the treated artery, the susceptibility of the species to spontaneous and diet-induced arterial disease, the nature of the stimulus to intimal proliferation and several practical and logistic considerations. Finally, the reported efficacies of specific drug therapies in the respective animal models and in humans were compared. This review suggests that significant interspecies and occasionally intraspecies differences do exist among the respective animal models, particularly in the extent and composition of the neointimal thickening.(ABSTRACT TRUNCATED AT 250 WORDS)
This article has been cited by other articles:

|
 |

|
 |
 
L. E. Leigh Perkins
Preclinical Models of Restenosis and Their Application in the Evaluation of Drug-Eluting Stent Systems
Veterinary Pathology,
January 1, 2010;
47(1):
58 - 76.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. E. Chadjichristos, S. Morel, J.-P. Derouette, E. Sutter, I. Roth, A. C. Brisset, M.-L. Bochaton-Piallat, and B. R. Kwak
Targeting Connexin 43 Prevents Platelet-Derived Growth Factor-BB-Induced Phenotypic Change in Porcine Coronary Artery Smooth Muscle Cells
Circ. Res.,
March 28, 2008;
102(6):
653 - 660.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Blindt, A.-K. Bosserhoff, J. Dammers, N. Krott, L. Demircan, R. Hoffmann, P. Hanrath, C. Weber, and F. Vogt
Downregulation of N-cadherin in the neointima stimulates migration of smooth muscle cells by RhoA deactivation
Cardiovasc Res,
April 1, 2004;
62(1):
212 - 222.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-H. Chen, L.-Y. Chau, M.-W. Lin, L.-C. Chen, M.-H. Yo, J.-W. Chen, and S.-J. Lin
Heme oxygenase-1 gene promotor microsatellite polymorphism is associated with angiographic restenosis after coronary stenting
Eur. Heart J.,
January 1, 2004;
25(1):
39 - 47.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Liu, M. Fisher, and P. Groves
Down-regulation of the ERK1 and ERK2 mitogen-activated protein kinases using antisense oligonucleotides inhibits intimal hyperplasia in a porcine model of coronary balloon angioplasty
Cardiovasc Res,
June 1, 2002;
54(3):
640 - 648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. C. Lowe, S. N. Oesterle, and L. M. Khachigian
Coronary in-stent restenosis: Current status and future strategies
J. Am. Coll. Cardiol.,
January 16, 2002;
39(2):
183 - 193.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Jorgensen, H. Kelbaek, S. Helqvist, G. V. H. Jensen, K. Saunamaki, J. Kastrup, O. Havndrup, H. Bundgaard, J. Kyst Madsen, M. Christiansen, et al.
Predictors of coronary in-stent restenosis: importance of angiotensin-converting enzyme gene polymorphism and treatment with angiotensin-converting enzyme inhibitors
J. Am. Coll. Cardiol.,
November 1, 2001;
38(5):
1434 - 1439.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. Lee, K. Yamada, S. L. Houser, K. L. Womer, M. E. Maloney, H. S. Rose, M. H. Sayegh, and J. C. Madsen
Indirect recognition of allopeptides promotes the development of cardiac allograft vasculopathy
PNAS,
March 13, 2001;
98(6):
3276 - 3281.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Christen, V. Verin, M.-L. Bochaton-Piallat, Y. Popowski, F. Ramaekers, P. Debruyne, E. Camenzind, G. van Eys, and G. Gabbiani
Mechanisms of Neointima Formation and Remodeling in the Porcine Coronary Artery
Circulation,
February 13, 2001;
103(6):
882 - 888.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Sasaki, Y. Tanahashi, Y. Yamasaki, N. Oda, Y. Nozawa, H. Terakawa, K. Miyoshi, Y. Muranaka, H. Miyake, and N. Matsuura
Inhibitory Effect of TAS-301, a New Synthesized Constrictive Remodeling Regulator, on Renarrowing after Balloon Overstretch Injury of Porcine Coronary Artery
J. Pharmacol. Exp. Ther.,
December 1, 2000;
295(3):
1043 - 1050.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
N Meneveau, F Schiele, G Grollier, B Farah, J.M Lablanche, K Khalife, J Machecourt, N Danchin, J.E Wolf, M Simpson, et al.
Local delivery of nadroparin for the prevention of neointimal hyperplasia following stent implantation: results of the IMPRESS Trial. A multicentre, randomized, clinical, angiographic and intravascular ultrasound study
Eur. Heart J.,
November 1, 2000;
21(21):
1767 - 1775.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
J. N. Topper
Genes, Matrix, and Restenosis
Arterioscler Thromb Vasc Biol,
October 1, 2000;
20(10):
2173 - 2174.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. R. Lijnen, B. Van Hoef, M. Dewerchin, and D. Collen
{alpha}2-Antiplasmin Gene Deficiency in Mice Does Not Affect Neointima Formation After Vascular Injury
Arterioscler Thromb Vasc Biol,
June 1, 2000;
20(6):
1488 - 1492.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Alt, I. Haehnel, C. Beilharz, K. Prietzel, D. Preter, A. Stemberger, T. Fliedner, W. Erhardt, and A. Schomig
Inhibition of Neointima Formation After Experimental Coronary Artery Stenting : A New Biodegradable Stent Coating Releasing Hirudin and the Prostacyclin Analogue Iloprost
Circulation,
March 28, 2000;
101(12):
1453 - 1458.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Morishige, H. Shimokawa, T. Yamawaki, K. Miyata, Y. Eto, T. Kandabashi, K. Yogo, T. Higo, K. Egashira, H. Ueno, et al.
Local adenovirus-mediated transfer of C-type natriuretic peptide suppresses vascular remodeling in porcine coronary arteries in vivo
J. Am. Coll. Cardiol.,
March 15, 2000;
35(4):
1040 - 1047.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I P Kay, M Sabate, G Van Langenhove, M A Costa, A J Wardeh, A L Gijzel, N V Deshpande, S G Carlier, V L M A Coen, P C Levendag, et al.
Outcome from balloon induced coronary artery dissection after intracoronary beta radiation
Heart,
March 1, 2000;
83(3):
332 - 337.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
W.-m. Cheung, M. R. D Andrea, P. Andrade-Gordon, and B. P. Damiano
Altered Vascular Injury Responses in Mice Deficient in Protease-Activated Receptor-1
Arterioscler Thromb Vasc Biol,
December 1, 1999;
19(12):
3014 - 3024.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J. Carter, D. Scott, L. Bailey, T. Hoopes, R. Jones, and R. Virmani
Dose-Response Effects of 32P Radioactive Stents in an Atherosclerotic Porcine Coronary Model
Circulation,
October 5, 1999;
100(14):
1548 - 1554.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Okamura, M. Ohishi, H. Rakugi, T. Katsuya, Y. Yanagitani, S. Takiuchi, Y. Taniyama, K. Moriguchi, H. Ito, Y. Higashino, et al.
Pharmacogenetic Analysis of the Effect of Angiotensin-Converting Enzyme Inhibitor on Restenosis After Percutaneous Transluminal Coronary Angioplasty
Angiology,
October 1, 1999;
50(10):
811 - 822.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Harada, Y. Toki, Y. Numaguchi, H. Osanai, T. Ito, K. Okumura, and T. Hayakawa
Prostacyclin synthase gene transfer inhibits neointimal formation in rat balloon-injured arteries without bleeding complications
Cardiovasc Res,
August 1, 1999;
43(2):
481 - 491.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Gallo, A. Padurean, T. Jayaraman, S. Marx, M. Roque, S. Adelman, J. Chesebro, J. Fallon, V. Fuster, A. Marks, et al.
Inhibition of Intimal Thickening After Balloon Angioplasty in Porcine Coronary Arteries by Targeting Regulators of the Cell Cycle
Circulation,
April 27, 1999;
99(16):
2164 - 2170.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Giese, M. M. H. Marijianowski, O. McCook, A. Hancock, V. Ramakrishnan, L. J. Fretto, C. Chen, A. B. Kelly, J. A. Koziol, J. N. Wilcox, et al.
The Role of Alpha and Beta Platelet-Derived Growth Factor Receptor in the Vascular Response to Injury in Nonhuman Primates
Arterioscler Thromb Vasc Biol,
April 1, 1999;
19(4):
900 - 909.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. A. de Vrey, G. S. Mintz, C. von Birgelen, T. Kimura, M. Noboyoshi, J. J. Popma, P. W. Serruys, and M. B. Leon
Serial volumetric (three-dimensional) intravascular ultrasound analysis of restenosis after directional coronary atherectomy
J. Am. Coll. Cardiol.,
December 1, 1998;
32(7):
1874 - 1880.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
O. Varenne, S. Pislaru, H. Gillijns, N. Van Pelt, R. D. Gerard, P. Zoldhelyi, F. Van de Werf, D. Collen, and S. P. Janssens
Local Adenovirus-Mediated Transfer of Human Endothelial Nitric Oxide Synthase Reduces Luminal Narrowing After Coronary Angioplasty in Pigs
Circulation,
September 1, 1998;
98(9):
919 - 926.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J. Lansky, G. S. Mintz, J. J. Popma, A. D. Pichard, K. M. Kent, L. F. Satler, D. S. Baim, R. E. Kuntz, C. Simonton, R. M. Bersin, et al.
Remodeling after directional coronary atherectomy (with and without adjunct percutaneous transluminal coronary angioplasty): a serial angiographic and intravascular ultrasound analysis from the optimal atherectomy restenosis study
J. Am. Coll. Cardiol.,
August 1, 1998;
32(2):
329 - 337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Lafont and D. Faxon
Why do animal models of post-angioplasty restenosis sometimes poorly predict the outcome of clinical trials?
Cardiovasc Res,
July 1, 1998;
39(1):
50 - 59.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Nikol, S. Esin, S. Nekolla, T. Y. Huehns, J. Schirmer, M. Schwaiger, and B. Hofling
Use of Nuclear Magnetic Resonance Imaging Angiography to Follow-Up Arterial Remodeling in an Animal Model
Angiology,
April 1, 1998;
49(4):
251 - 258.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. B. DeYoung and D. A. Dichek
Gene Therapy for Restenosis : Are We Ready?
Circ. Res.,
February 23, 1998;
82(3):
306 - 313.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Gallo, A. Padurean, V. Toschi, J. Bichler, J. T. Fallon, J. H. Chesebro, V. Fuster, and J. J. Badimon
Prolonged Thrombin Inhibition Reduces Restenosis After Balloon Angioplasty in Porcine Coronary Arteries
Circulation,
February 17, 1998;
97(6):
581 - 588.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Takagi, M. Ueda, A. E. Becker, K. Takeuchi, and T. Takeda
The Watanabe Heritable Hyperlipidemic Rabbit Is a Suitable Experimental Model to Study Differences in Tissue Response Between Intimal and Medial Injury After Balloon Angioplasty
Arterioscler Thromb Vasc Biol,
December 1, 1997;
17(12):
3611 - 3619.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
L. J Feldman and G. Steg
Optimal techniques for arterial gene transfer
Cardiovasc Res,
September 1, 1997;
35(3):
391 - 404.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kimura, S. Kaburagi, T. Tamura, H. Yokoi, Y. Nakagawa, H. Yokoi, N. Hamasaki, H. Nosaka, M. Nobuyoshi, G. S. Mintz, et al.
Remodeling of Human Coronary Arteries Undergoing Coronary Angioplasty or Atherectomy
Circulation,
July 15, 1997;
96(2):
475 - 483.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. M. Bosmans, M. M. Kockx, C. J. Vrints, H. Bult, G. R. Y. De Meyer, and A. G. Herman
Fibrin(ogen) and von Willebrand Factor Deposition Are Associated With Intimal Thickening After Balloon Angioplasty of the Rabbit Carotid Artery
Arterioscler Thromb Vasc Biol,
April 1, 1997;
17(4):
634 - 645.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
P. J. Bendick, R. S. Juleff, and J. L. Glover
Arterial Adaptation to Increased Wall Shear Stress
Vascular and Endovascular Surgery,
March 1, 1997;
31(2):
153 - 161.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Perlman, L. Maillard, K. Krasinski, and K. Walsh
Evidence for the Rapid Onset of Apoptosis in Medial Smooth Muscle Cells After Balloon Injury
Circulation,
February 18, 1997;
95(4):
981 - 987.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
H. Mudra, E. Regar, V. Klauss, F. Werner, K.-H. Henneke, E. Sbarouni, and K. Theisen
Serial Follow-up After Optimized Ultrasound-Guided Deployment of Palmaz-Schatz Stents: In-Stent Neointimal Proliferation Without Significant Reference Segment Response
Circulation,
January 21, 1997;
95(2):
363 - 370.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
C. Gerdes, V. Faber-Steinfeld, O. Yalkinoglu, and S. Wohlfeil
Comparison of the Effects of the Thrombin Inhibitor r-Hirudin in Four Animal Models of Neointima Formation After Arterial Injury
Arterioscler Thromb Vasc Biol,
October 1, 1996;
16(10):
1306 - 1311.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. C. Madsen, D. H. Sachs, J. T. Fallon, and N. J. Weissman
CARDIAC ALLOGRAFT VASCULOPATHY IN PARTIALLY INBRED MINIATURE SWINE. I. TIME COURSE, PATHOLOGY, AND DEPENDENCE ON IMMUNE MECHANISMS
J. Thorac. Cardiovasc. Surg.,
June 1, 1996;
111(6):
1230 - 1239.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
H. Rud Andersen, M. M ng, M. Thorwest, and E. Falk
Remodeling Rather Than Neointimal Formation Explains Luminal Narrowing After Deep Vessel Wall Injury : Insights From a Porcine Coronary (Re)stenosis Model
Circulation,
May 1, 1996;
93(9):
1716 - 1724.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
W. R. Huckle, M. D. Drag, W. R. Acker, M. Powers, R. C. McFall, D. J. Holder, T. Fujita, I. I. Stabilito, D. Kim, D. L. Ondeyka, et al.
Effects of Subtype-Selective and Balanced Angiotensin II Receptor Antagonists in a Porcine Coronary Artery Model of Vascular Restenosis
Circulation,
March 1, 1996;
93(5):
1009 - 1019.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S.-J. Chen, H. Li, J. Durand, S. Oparil, and Y.-F. Chen
Estrogen Reduces Myointimal Proliferation After Balloon Injury of Rat Carotid Artery
Circulation,
February 1, 1996;
93(3):
577 - 584.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. L. Wilensky, K. L. March, I. Gradus-Pizlo, G. Sandusky, N. Fineberg, and D. R. Hathaway
Vascular Injury, Repair, and Restenosis After Percutaneous Transluminal Angioplasty in the Atherosclerotic Rabbit
Circulation,
November 15, 1995;
92(10):
2995 - 3005.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
C. M. Newman, B. C. Bruun, K. E. Porter, P. K. Mistry, C. M. Shanahan, and P. L. Weissberg
Osteopontin Is Not a Marker for Proliferating Human Vascular Smooth Muscle Cells
Arterioscler Thromb Vasc Biol,
November 1, 1995;
15(11):
2010 - 2018.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. A. Moggio, J.-Z. Ding, C. J. Smith, R. R. Tota, M. B. Stemerman, and G. E. Reed
Immediate-early gene expression in human saphenous veins harvested during coronary artery bypass graft operations
J. Thorac. Cardiovasc. Surg.,
July 1, 1995;
110(1):
209 - 213.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. Recchia, D. R. Abendschein, J. E. Saffitz, and S. A. Wickline
The Biologic Behavior of Balloon Hyperinflation Induced Arterial Lesions in Hypercholesterolemic Pigs Depends on the Presence of Foam Cells
Arterioscler Thromb Vasc Biol,
July 1, 1995;
15(7):
924 - 929.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
A. Lafont, L. A. Guzman, P. L. Whitlow, M. Goormastic, J. F. Cornhill, and G. M. Chisolm
Restenosis After Experimental Angioplasty : Intimal, Medial, and Adventitial Changes Associated With Constrictive Remodeling
Circ. Res.,
June 1, 1995;
76(6):
996 - 1002.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. M. Isner, M. Kearney, S. Bortman, and J. Passeri
Apoptosis in Human Atherosclerosis and Restenosis
Circulation,
June 1, 1995;
91(11):
2703 - 2711.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
H. C. Lowe, R. G. Fahmy, M. M. Kavurma, A. Baker, C. N. Chesterman, and L. M. Khachigian
Catalytic Oligodeoxynucleotides Define a Key Regulatory Role for Early Growth Response Factor-1 in the Porcine Model of Coronary In-Stent Restenosis
Circ. Res.,
October 12, 2001;
89(8):
670 - 677.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|