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Circulation. 1994;89:2816-2821

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Circulation, Vol 89, 2816-2821, Copyright © 1994 by American Heart Association


ARTICLES

The relative importance of arterial remodeling compared with intimal hyperplasia in lumen renarrowing after balloon angioplasty. A study in the normal rabbit and the hypercholesterolemic Yucatan micropig

MJ Post, C Borst and RE Kuntz
Department of Cardiology, Utrecht University Hospital, The Netherlands.

BACKGROUND: Although arterial renarrowing after angioplasty has been attributed largely to intimal hyperplasia, there has been no systematic effort to correlate the actual hyperplastic tissue mass with angiographic lumen reduction. Using balloon angioplasty in various animal restenosis models, we quantitatively assessed the separate contributions of intimal hyperplasia and arterial remodeling to angiographic late lumen loss. METHODS AND RESULTS: Data used for this study were obtained from experiments of conventional and thermal (37 degrees C or 55 degrees to 90 degrees C) balloon angioplasty-treated femoral and iliac arteries in normal rabbits and conventional balloon angioplasty-treated iliac arteries in Yucatan micropigs fed either a normal or an atherogenic diet. Quantitative angiography was performed immediately before and after intervention and at 3 or 8 weeks thereafter, and late loss in lumen diameter was taken as the difference between arterial diameter immediately after treatment and at 3 or 8 weeks of follow-up. Intimal hyperplasia was quantified histologically as the area of tissue mass within the internal elastic lamina. We observed a consistent discrepancy between the actual late loss seen with angiography and the diameter reduction that could be explained by histological intimal thickness alone in both animal models. This discrepancy ranged from 86 +/- 3% of the late loss in the 8 weeks/37 degrees C group to 77 +/- 22% in the conventional group for rabbits and 52 +/- 23% in an atherogenic diet group (n = 10) to 89 +/- 11% in a normal diet group (n = 6) for pigs. This discrepancy appeared to be due predominantly to reduction of the area circumscribed by the internal elastic membrane, a process that is tentatively designated as arterial remodeling. In both the rabbit femoral artery and in the Yucatan iliac artery, remodeling, not intimal hyperplasia, correlated with angiographic late loss. CONCLUSIONS: In both the normal rabbit and the normal and atherosclerotic pig, restenosis after angioplasty results from both intimal hyperplasia and arterial remodeling. The exact etiology of arterial renarrowing after angioplasty has important implications on the design of antirestenosis drugs and new coronary devices.


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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]


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Cardiovasc ResHome page
B.J.G.L de Smet, J van der Zande, Y.J.M van der Helm, R.E Kuntz, C Borst, and M.J Post
The atherosclerotic Yucatan animal model to study the arterial response after balloon angioplasty: the natural history of remodeling
Cardiovasc Res, July 1, 1998; 39(1): 224 - 232.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
D. W. Courtman, S. M. Schwartz, and C. E. Hart
Sequential Injury of the Rabbit Abdominal Aorta Induces Intramural Coagulation and Luminal Narrowing Independent of Intimal Mass : Extrinsic Pathway Inhibition Eliminates Luminal Narrowing
Circ. Res., May 19, 1998; 82(9): 996 - 1006.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
B. J. G. L. de Smet, G. Pasterkamp, Y. J. van der Helm, C. Borst, and M. J. Post
The Relation Between De Novo Atherosclerosis Remodeling and Angioplasty-Induced Remodeling in an Atherosclerotic Yucatan Micropig Model
Arterioscler Thromb Vasc Biol, May 1, 1998; 18(5): 702 - 707.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
E. Van Belle, C. Bauters, T. Asahara, and J. M. Isner
Endothelial regrowth after arterial injury: from vascular repair to therapeutics
Cardiovasc Res, April 1, 1998; 38(1): 54 - 68.
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HeartHome page
P C Smits, L Bos, M A Q. van Ufford, F D Eefting, G Pasterkamp, and C Borst
Shrinkage of human coronary arteries is an important determinant of de novo atherosclerotic luminal stenosis: an in vivo intravascular ultrasound study
Heart, February 1, 1998; 79(2): 143 - 147.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
T. Kakuta, M. Usui, W. D. Coats Jr, J. W. Currier, F. Numano, and D. P. Faxon
Arterial Remodeling at the Reference Site After Angioplasty in the Atherosclerotic Rabbit Model
Arterioscler Thromb Vasc Biol, January 1, 1998; 18(1): 47 - 51.
[Abstract] [Full Text] [PDF]


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CirculationHome page
A. Kumar, J. L. Hoover, C. A. Simmons, V. Lindner, and R. J. Shebuski
Remodeling and Neointimal Formation in the Carotid Artery of Normal and P-Selectin–Deficient Mice
Circulation, December 16, 1997; 96(12): 4333 - 4342.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
H. S. Seo, D. M. Lombardi, P. Polinsky, L. Powell-Braxton, S. Bunting, S. M. Schwartz, and M. E. Rosenfeld
Peripheral Vascular Stenosis in Apolipoprotein E-Deficient Mice : Potential Roles of Lipid Deposition, Medial Atrophy, and Adventitial Inflammation
Arterioscler Thromb Vasc Biol, December 1, 1997; 17(12): 3593 - 3601.
[Abstract] [Full Text]


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Cardiovasc ResHome page
S.D. Gertz, W. L Barry, L. W Gimple, Shmuel Banai, L. S Perez, C. A McNamara, E. R Powers, M. Ragosta, G. K Owens, W. C Roberts, et al.
Predictors of luminal narrowing by neointima after angioplasty in atherosclerotic rabbits
Cardiovasc Res, December 1, 1997; 36(3): 396 - 407.
[Abstract] [Full Text] [PDF]


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CirculationHome page
M. K. Barron, R. S. Lake, A. J. Buda, and A. N. Tenaglia
Intimal Hyperplasia After Balloon Injury Is Attenuated by Blocking Selectins
Circulation, November 18, 1997; 96(10): 3587 - 3592.
[Abstract] [Full Text]


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CirculationHome page
M. W. Liu, P. G. Anderson, J. F. Luo, and G. S. Roubin
Local Delivery of Ethanol Inhibits Intimal Hyperplasia in Pig Coronary Arteries After Balloon Injury
Circulation, October 7, 1997; 96(7): 2295 - 2301.
[Abstract] [Full Text]


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CirculationHome page
R. Waksman, J. C. Rodriguez, K. A. Robinson, G. D. Cipolla, I. R. Crocker, N. A. Scott, S. B. King III, and J. N. Wilcox
Effect of Intravascular Irradiation on Cell Proliferation, Apoptosis, and Vascular Remodeling After Balloon Overstretch Injury of Porcine Coronary Arteries
Circulation, September 16, 1997; 96(6): 1944 - 1952.
[Abstract] [Full Text]


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CirculationHome page
E. Van Belle, C. Bauters, E. Hubert, J.-C. Bodart, K. Abolmaali, T. Meurice, E. P. McFadden, J.-M. Lablanche, and M. E. Bertrand
Restenosis Rates in Diabetic Patients : A Comparison of Coronary Stenting and Balloon Angioplasty in Native Coronary Vessels
Circulation, September 2, 1997; 96(5): 1454 - 1460.
[Abstract] [Full Text]


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ANGIOLOGYHome page
M. E. Staab, R. D. Simari, S. S. Srivatsa, D. Hasdai, V. J. Pompili, D. R. Holmes, R. S. Schwartz, and R. S. Schwartz
Enhanced Angiogenesis and Unfavorable Remodeling in Injured Porcine Coronary Artery Lesions: Effects of Local Basic Fibroblast Growth Factor Delivery
Angiology, September 1, 1997; 48(9): 753 - 760.
[Abstract] [PDF]


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CirculationHome page
J. A. Ormiston, F. M. Stewart, A. H. G. Roche, B. J. Webber, R. M. L. Whitlock, and M. W. I. Webster
Late Regression of the Dilated Site After Coronary Angioplasty : A 5-Year Quantitative Angiographic Study
Circulation, July 15, 1997; 96(2): 468 - 474.
[Abstract] [Full Text]


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CirculationHome page
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]


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J. Thorac. Cardiovasc. Surg.Home page
J. E. O'Brien Jr., Y. Shi, A. Fard, T. Bauer, A. Zalewski, and J. D. Mannion
WOUND HEALING AROUND AND WITHIN SAPHENOUS VEIN BYPASS GRAFTS
J. Thorac. Cardiovasc. Surg., July 1, 1997; 114(1): 38 - 45.
[Abstract] [Full Text]


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CirculationHome page
D. P. Faxon
Identifying the Predictors of Restenosis: Do We Need New Glasses?
Circulation, May 6, 1997; 95(9): 2244 - 2246.
[Full Text]


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CirculationHome page
G. S. Mintz, K. M. Kent, A. D. Pichard, L. F. Satler, J. J. Popma, and M. B. Leon
Contribution of Inadequate Arterial Remodeling to the Development of Focal Coronary Artery Stenoses : An Intravascular Ultrasound Study
Circulation, April 1, 1997; 95(7): 1791 - 1798.
[Abstract] [Full Text]


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CirculationHome page
S. P. Schwarzacher, T. T. Lim, B. Wang, R. S. Kernoff, J. Niebauer, J. P. Cooke, and A. C. Yeung
Local Intramural Delivery of L-Arginine Enhances Nitric Oxide Generation and Inhibits Lesion Formation After Balloon Angioplasty
Circulation, April 1, 1997; 95(7): 1863 - 1869.
[Abstract] [Full Text]


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CirculationHome page
W. D. Coats, P. Whittaker, D. T. Cheung, J. W. Currier, B. Han, and D. P. Faxon
Collagen Content Is Significantly Lower in Restenotic Versus Nonrestenotic Vessels After Balloon Angioplasty in the Atherosclerotic Rabbit Model
Circulation, March 4, 1997; 95(5): 1293 - 1300.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
A. Zalewski and Y. Shi
Vascular Myofibroblasts : Lessons From Coronary Repair and Remodeling
Arterioscler Thromb Vasc Biol, March 1, 1997; 17(3): 417 - 422.
[Full Text]


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CirculationHome page
Y. Shi, J. E. O'Brien, L. Ala-Kokko, W. Chung, J. D. Mannion, and A. Zalewski
Origin of Extracellular Matrix Synthesis During Coronary Repair
Circulation, February 18, 1997; 95(4): 997 - 1006.
[Abstract] [Full Text]


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CirculationHome page
E. Van Belle, F. O. Tio, T. Couffinhal, L. Maillard, J. Passeri, and J. M. Isner
Stent Endothelialization: Time Course, Impact of Local Catheter Delivery, Feasibility of Recombinant Protein Administration, and Response to Cytokine Expedition
Circulation, January 21, 1997; 95(2): 438 - 448.
[Abstract] [Full Text]


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CirculationHome page
M. K. Hong, K. M. Kent, R. Mehran, G. S. Mintz, F. O. Tio, M. Foegh, S. C. Wong, S. S. Cathapermal, and M. B. Leon
Continuous Subcutaneous Angiopeptin Treatment Significantly Reduces Neointimal Hyperplasia in a Porcine Coronary In-Stent Restenosis Model
Circulation, January 21, 1997; 95(2): 449 - 454.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
H. Luo, T. Nishioka, N. L. Eigler, J. S. Forrester, M. C. Fishbein, H. Berglund, and R. J. Siegel
Coronary Artery Restenosis After Balloon Angioplasty in Humans Is Associated With Circumferential Coronary Constriction
Arterioscler Thromb Vasc Biol, November 1, 1996; 16(11): 1393 - 1398.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
Y. Shi, J. E. O'Brien, A. Fard, and A. Zalewski
Transforming Growth Factor-ß1 Expression and Myofibroblast Formation During Arterial Repair
Arterioscler Thromb Vasc Biol, October 1, 1996; 16(10): 1298 - 1305.
[Abstract] [Full Text]


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CirculationHome page
Y. Shi, J. E. O'Brien, A. Fard, J. D. Mannion, D. Wang, and A. Zalewski
Adventitial Myofibroblasts Contribute to Neointimal Formation in Injured Porcine Coronary Arteries
Circulation, October 1, 1996; 94(7): 1655 - 1664.
[Abstract] [Full Text]


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CirculationHome page
R. Hoffmann, G. S. Mintz, G. R. Dussaillant, J. J. Popma, A. D. Pichard, L. F. Satler, K. M. Kent, J. Griffin, and M. B. Leon
Patterns and Mechanisms of In-Stent Restenosis: A Serial Intravascular Ultrasound Study
Circulation, September 15, 1996; 94(6): 1247 - 1254.
[Abstract] [Full Text]


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CirculationHome page
G. S. Mintz, J. J. Popma, A. D. Pichard, K. M. Kent, L. F. Satler, S. Chiu Wong, M. K. Hong, J. A. Kovach, and M. B. Leon
Arterial Remodeling After Coronary Angioplasty : A Serial Intravascular Ultrasound Study
Circulation, July 1, 1996; 94(1): 35 - 43.
[Abstract] [Full Text]


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CirculationHome page
N. A. Scott, G. D. Cipolla, C. E. Ross, B. Dunn, F. H. Martin, L. Simonet, and J. N. Wilcox
Identification of a Potential Role for the Adventitia in Vascular Lesion Formation After Balloon Overstretch Injury of Porcine Coronary Arteries
Circulation, June 15, 1996; 93(12): 2178 - 2187.
[Abstract] [Full Text]


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CirculationHome page
H. Rud Andersen, M. Mæng, 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]


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CirculationHome page
R. Riessen, T. N. Wight, C. Pastore, C. Henley, and J. M. Isner
Distribution of Hyaluronan During Extracellular Matrix Remodeling in Human Restenotic Arteries and Balloon-Injured Rat Carotid Arteries
Circulation, March 15, 1996; 93(6): 1141 - 1147.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
L. A. Guzman, M. J. Mick, A. M. Arnold, F. Forudi, and P. L. Whitlow
Role of Intimal Hyperplasia and Arterial Remodeling After Balloon Angioplasty : An Experimental Study in the Atherosclerotic Rabbit Model
Arterioscler Thromb Vasc Biol, March 1, 1996; 16(3): 479 - 487.
[Abstract] [Full Text]


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CirculationHome page
Y. Shi, M. Pieniek, A. Fard, J. O'Brien, J. D. Mannion, and A. Zalewski
Adventitial Remodeling After Coronary Arterial Injury
Circulation, January 15, 1996; 93(2): 340 - 348.
[Abstract] [Full Text]


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Arterioscler. Thromb. Vasc. Bio.Home page
R. L. Geary, J. K. Williams, D. Golden, D. G. Brown, M. E. Benjamin, and M. R. Adams
Time Course of Cellular Proliferation, Intimal Hyperplasia, and Remodeling Following Angioplasty in Monkeys With Established Atherosclerosis : A Nonhuman Primate Model of Restenosis
Arterioscler Thromb Vasc Biol, January 1, 1996; 16(1): 34 - 43.
[Abstract] [Full Text]


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CirculationHome page
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]