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J Am Coll Cardiol, 2006; 48:193-202, doi:10.1016/j.jacc.2006.03.042 (Published online 4 May 2006).
© 2006 by the American College of Cardiology Foundation
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EXPEDITED REVIEW

Pathology of Drug-Eluting Stents in Humans

Delayed Healing and Late Thrombotic Risk

Michael Joner, MD*,1, Aloke V. Finn, MD{dagger},1, Andrew Farb, MD§, Erik K. Mont, MD{ddagger}, Frank D. Kolodgie, PhD*, Elena Ladich, MD*, Robert Kutys, MS*, Kristi Skorija, BS*, Herman K. Gold, MD{dagger} and Renu Virmani, MD*,*

* CVPath, International Registry of Pathology, Gaithersburg, Maryland
{dagger} Cardiac Unit, Department of Internal Medicine, Massachusetts General Hospital, Boston, Massachusetts
{ddagger} Miami Dade County Medical Examiner Department, Heart Radiology, Miami, Florida
§ Interventional Cardiology Devices Branch, U.S. Food and Drug Administration, Rockville, Maryland

Manuscript received January 26, 2006; revised manuscript received March 10, 2006, accepted March 16, 2006.

* Reprint requests and correspondence: Dr. Renu Virmani, CVPath, International Registry of Pathology, 19 Firstfield Road, Gaithersburg, Maryland 20878 (Email: rvirmani{at}cvpath.org).

OBJECTIVES: This study examined human drug-eluting stents (DES) to determine the long-term effects of these stents on coronary arterial healing and identified mechanisms underlying late stent thrombosis (LST).

BACKGROUND: Although DES reduce the need for repeat revascularization compared with bare-metal stents (BMS), data suggest the window of thrombotic risk for Cypher (Cordis Corp., Miami Lakes, Florida) and Taxus (Boston Scientific Corp., Natick, Massachusetts) DES extends far beyond that for BMS.

METHODS: From a registry of 40 autopsies of DES (68 stents), 23 DES cases of >30 days duration were compared with 25 matched autopsies of BMS implantation. Late stent thrombosis was defined as an acute thrombus within a stent >30 days old.

RESULTS: Of 23 patients with DES >30 days old, 14 had evidence of LST. Cypher and Taxus DES showed greater delayed healing characterized by persistent fibrin deposition (fibrin score 2.3 ± 1.1 vs. 0.9 ± 0.8, p = 0.0001) and poorer endothelialization (55.8 ± 26.5%) compared with BMS (89.8 ± 20.9, p = 0.0001). Moreover, DES with LST showed more delayed healing compared with patent DES. In 5 of 14 patients suffering LST, antiplatelet therapy had been withdrawn. Additional procedural and pathologic risk factors for LST were: 1) local hypersensitivity reaction; 2) ostial and/or bifurcation stenting; 3) malapposition/incomplete apposition; 4) restenosis; and 5) strut penetration into a necrotic core.

CONCLUSIONS: The Cypher and Taxus DES result in delayed arterial healing when compared with BMS of similar implant duration. The cause of DES LST is multifactorial with delayed healing in combination with other clinical and procedural risk factors playing a role.

Abbreviations and Acronyms
  BMS = bare-metal stents
  DES = drug-eluting stents
  FDA = Food and Drug Administration
  LST = late stent thrombosis




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S. S. Brar, J. Kim, S. K. Brar, R. Zadegan, M. Ree, I.-L. A. Liu, P. Mansukhani, V. Aharonian, R. Hyett, and A. Y.-J. Shen
Long-term outcomes by clopidogrel duration and stent type in a diabetic population with de novo coronary artery lesions.
J. Am. Coll. Cardiol., June 10, 2008; 51(23): 2220 - 2227.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
S.-H. Choi, A. Prasad, and S. Tsimikas
The evolution of thienopyridine therapy clopidogrel duration, diabetes, and drug-eluting stents.
J. Am. Coll. Cardiol., June 10, 2008; 51(23): 2228 - 2229.
[Full Text] [PDF]

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 J Am Coll CardiolHome page
M. I. Hamilos, M. Ostojic, B. Beleslin, D. Sagic, L. Mangovski, S. Stojkovic, M. Nedeljkovic, D. Orlic, B. Milosavljevic, D. Topic, et al.
Differential effects of drug-eluting stents on local endothelium-dependent coronary vasomotion.
J. Am. Coll. Cardiol., June 3, 2008; 51(22): 2123 - 2129.
[Abstract] [Full Text] [PDF]

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 J Am Coll Cardiol IntvHome page
M. H. Shishehbor, R. Amini, L. P.J. Oliveria, I. M. Singh, P. Kelly, D. L. Bhatt, S. R. Kapadia, S. G. Ellis, P. L. Whitlow, and S. J. Brener
Comparison of Drug-Eluting Stents Versus Bare-Metal Stents for Treating ST-Segment Elevation Myocardial Infarction
J. Am. Coll. Cardiol. Intv., June 1, 2008; 1(3): 227 - 232.
[Abstract] [Full Text] [PDF]

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 J Am Coll Cardiol IntvHome page
C. S. Rihal
Drug-Eluting Stents for ST-Segment Elevation Myocardial Infarction: Treatment of Choice or Is Discretion the Better Part of Valor?
J. Am. Coll. Cardiol. Intv., June 1, 2008; 1(3): 233 - 235.
[Full Text] [PDF]

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 Cardiovasc ResHome page
A. Barilli, R. Visigalli, R. Sala, G. C. Gazzola, A. Parolari, E. Tremoli, S. Bonomini, A. Simon, E. I. Closs, V. Dall'Asta, et al.
In human endothelial cells rapamycin causes mTORC2 inhibition and impairs cell viability and function
Cardiovasc Res, June 1, 2008; 78(3): 563 - 571.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
H. Kelbaek, L. Klovgaard, S. Helqvist, J. F. Lassen, L. R. Krusell, T. Engstrom, H. E. Botker, E. Jorgensen, K. Saunamaki, S. Aljabbari, et al.
Long-Term Outcome in Patients Treated With Sirolimus-Eluting Stents in Complex Coronary Artery Lesions: 3-Year Results of the SCANDSTENT (Stenting Coronary Arteries in Non-Stress/Benestent Disease) Trial
J. Am. Coll. Cardiol., May 27, 2008; 51(21): 2011 - 2016.
[Abstract] [Full Text] [PDF]

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 The Annals of PharmacotherapyHome page
S. H Bhatt and T. H Hauser
Very Late Stent Thrombosis After Dual Antiplatelet Therapy Discontinuation in a Patient with a History of Acute Stent Thrombosis
Ann. Pharmacother., May 1, 2008; 42(5): 708 - 712.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
M. W. Krucoff, D. J. Kereiakes, J. L. Petersen, R. Mehran, V. Hasselblad, A. J. Lansky, P. J. Fitzgerald, J. Garg, M. A. Turco, C. A. Simonton III, et al.
A novel bioresorbable polymer paclitaxel-eluting stent for the treatment of single and multivessel coronary disease: primary results of the COSTAR (Cobalt Chromium Stent With Antiproliferative for Restenosis) II study.
J. Am. Coll. Cardiol., April 22, 2008; 51(16): 1543 - 1552.
[Abstract] [Full Text] [PDF]

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 J Am Coll Cardiol IntvHome page
Y. Suzuki, F. Ikeno, T. Koizumi, F. Tio, A. C. Yeung, P. G. Yock, P. J. Fitzgerald, and W. F. Fearon
In Vivo Comparison Between Optical Coherence Tomography and Intravascular Ultrasound for Detecting Small Degrees of In-Stent Neointima After Stent Implantation
J. Am. Coll. Cardiol. Intv., April 1, 2008; 1(2): 168 - 173.
[Abstract] [Full Text] [PDF]

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 J Am Coll Cardiol IntvHome page
B. L. van der Hoeven, S.-S. Liem, J. Dijkstra, S. C. Bergheanu, H. Putter, M. L. Antoni, D. E. Atsma, M. Bootsma, K. Zeppenfeld, J. W. Jukema, et al.
Stent Malapposition After Sirolimus-Eluting and Bare-Metal Stent Implantation in Patients with ST-Segment Elevation Myocardial Infarction: Acute and 9-Month Intravascular Ultrasound Results of the MISSION! Intervention Study
J. Am. Coll. Cardiol. Intv., April 1, 2008; 1(2): 192 - 201.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
T. L. Pinto Slottow and R. Waksman
Overview of the 2007 Food and Drug Administration Circulatory System Devices Panel Meeting on the Endeavor Zotarolimus-Eluting Coronary Stent
Circulation, March 25, 2008; 117(12): 1603 - 1608.
[Full Text] [PDF]

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 J Am Coll CardiolHome page
G. Nakazawa, Q. Cheng, X. Xu, A. V. Finn, F. D. Kolodgie, and R. Virmani
Drug-eluting stent implantation may not affect vasomotor function in early phase.
J. Am. Coll. Cardiol., March 18, 2008; 51(11): 1124 - 1125.
[Full Text] [PDF]

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 J Am Coll CardiolHome page
D. P. Taggart, S. Kaul, W. E. Boden, T. B. Ferguson Jr, R. A. Guyton, M. J. Mack, P. T. Sergeant, R. J. Shemin, P. K. Smith, and S. Yusuf
Revascularization for unprotected left main stem coronary artery stenosis stenting or surgery.
J. Am. Coll. Cardiol., March 4, 2008; 51(9): 885 - 892.
[Abstract] [Full Text] [PDF]

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 Eur Heart JHome page
B.-K. Koo, K.-W. Park, H.-J. Kang, Y.-S. Cho, W.-Y. Chung, T.-J. Youn, I.-H. Chae, D.-J. Choi, S.-J. Tahk, B.-H. Oh, et al.
Physiological evaluation of the provisional side-branch intervention strategy for bifurcation lesions using fractional flow reserve
Eur. Heart J., March 2, 2008; 29(6): 726 - 732.
[Abstract] [Full Text] [PDF]

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 Eur Heart JHome page
D. P. Taggart
Does prior PCI increase the risk of subsequent CABG?
Eur. Heart J., March 1, 2008; 29(5): 573 - 575.
[Full Text] [PDF]

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 HeartHome page
A. Colombo and A. Latib
Late incomplete stent apposition after drug-eluting stent implantation: a true risk factor or "an innocent bystander"?
Heart, March 1, 2008; 94(3): 253 - 254.
[Full Text] [PDF]

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 HeartHome page
R Hoffmann, M-C Morice, J W Moses, P J Fitzgerald, L Mauri, G Breithardt, J Schofer, P W Serruys, H-P Stoll, and M B Leon
Impact of late incomplete stent apposition after sirolimus-eluting stent implantation on 4-year clinical events: intravascular ultrasound analysis from the multicentre, randomised, RAVEL, E-SIRIUS and SIRIUS trials
Heart, March 1, 2008; 94(3): 322 - 328.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
P. Ortolani, M. Balducelli, P. Marzaroli, G. Piovaccari, A. Menozzi, V. Guiducci, P. Sangiorgio, F. Tarantino, G. Geraci, F. Castriota, et al.
Two-Year Clinical Outcomes With Drug-Eluting Stents for Diabetic Patients With De Novo Coronary Lesions: Results From a Real-World Multicenter Registry
Circulation, February 19, 2008; 117(7): 923 - 930.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
B. L. van der Hoeven, S.-S. Liem, J. W. Jukema, N. Suraphakdee, H. Putter, J. Dijkstra, D. E. Atsma, M. Bootsma, K. Zeppenfeld, P. V. Oemrawsingh, et al.
Sirolimus-eluting stents versus bare-metal stents in patients with ST-segment elevation myocardial infarction: 9-month angiographic and intravascular ultrasound results and 12-month clinical outcome results from the MISSION! Intervention Study.
J. Am. Coll. Cardiol., February 12, 2008; 51(6): 618 - 626.
[Abstract] [Full Text] [PDF]

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 Ther Adv Cardiovasc DisHome page
F. Saia, A. Marzocchi, and A. Branzi
Review: The safety of drug-eluting stents
Therapeutic Advances in Cardiovascular Disease, February 1, 2008; 2(1): 43 - 52.
[Abstract] [PDF]

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 J Am Coll Cardiol IntvHome page
J. Aoki, A. Kirtane, M. B. Leon, and G. Dangas
Coronary artery aneurysms after drug-eluting stent implantation.
J. Am. Coll. Cardiol. Intv., February 1, 2008; 1(1): 14 - 21.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
J. H. Brasen, O. Leppanen, M. Inkala, T. Heikura, M. Levin, F. Ahrens, J. Rutanen, H. Pietsch, D. Bergqvist, A.-L. Levonen, et al.
Extracellular Superoxide Dismutase Accelerates Endothelial Recovery and Inhibits In-Stent Restenosis in Stented Atherosclerotic Watanabe Heritable Hyperlipidemic Rabbit Aorta
J. Am. Coll. Cardiol., December 4, 2007; 50(23): 2249 - 2253.
[Abstract] [Full Text] [PDF]

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 HeartHome page
M. Takano, M. Yamamoto, Y. Xie, D. Murakami, S. Inami, K. Okamatsu, K. Seimiya, T. Ohba, Y. Seino, and K. Mizuno
Serial long-term evaluation of neointimal stent coverage and thrombus after sirolimus-eluting stent implantation by use of coronary angioscopy
Heart, December 1, 2007; 93(12): 1533 - 1536.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
K. Egashira, K. Nakano, K. Ohtani, K. Funakoshi, G. Zhao, Y. Ihara, J.-i. Koga, S. Kimura, R. Tominaga, and K. Sunagawa
Local Delivery of Anti-Monocyte Chemoattractant Protein-1 by Gene-Eluting Stents Attenuates In-Stent Stenosis in Rabbits and Monkeys
Arterioscler. Thromb. Vasc. Biol., December 1, 2007; 27(12): 2563 - 2568.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
A. V. Finn, M. C. John, H. K. Gold, J. Newell, G. Nakazawa, M. Joner, F. D. Kolodgie, and R. Virmani
Response to Letter Regarding Article, "Pathological Correlates of Late Drug-Eluting Stent Thrombosis: Strut Coverage as a Marker of Endothelialization"
Circulation, November 27, 2007; 116(22): e550 - e550.
[Full Text] [PDF]

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 CirculationHome page
B. Doyle, C. S. Rihal, C. J. O'Sullivan, R. J. Lennon, H. J. Wiste, M. Bell, J. Bresnahan, and D. R. Holmes Jr
Outcomes of Stent Thrombosis and Restenosis During Extended Follow-Up of Patients Treated With Bare-Metal Coronary Stents
Circulation, November 20, 2007; 116(21): 2391 - 2398.
[Abstract] [Full Text] [PDF]

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 HeartHome page
M. Takano, M. Yamamoto, Y. Xie, D. Murakami, S. Inami, K. Okamatsu, K. Seimiya, T. Ohba, Y. Seino, and K. Mizuno
Serial long-term evaluation of neointimal stent coverage and thrombus after sirolimus-eluting stent implantation by use of coronary angioscopy
Heart, November 1, 2007; 93(11): 1353 - 1356.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
G. J. Wilson, J. E. Polovick, B. A. Huibregtse, and B. C. Poff
Overlapping paclitaxel-eluting stents: Long-term effects in a porcine coronary artery model
Cardiovasc Res, November 1, 2007; 76(2): 361 - 372.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
L. A. Fleisher, J. A. Beckman, K. A. Brown, H. Calkins, E. L. Chaikof, K. E. Fleischmann, W. K. Freeman, J. B. Froehlich, E. K. Kasper, J. R. Kersten, et al.
ACC/AHA 2007 Guidelines on Perioperative Cardiovascular Evaluation and Care for Noncardiac Surgery: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines on Perioperative Cardiovascular Evaluation for Noncardiac Surgery) Developed in Collaboration With the American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Rhythm Society, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, and Society for Vascular Surgery
J. Am. Coll. Cardiol., October 23, 2007; 50(17): e159 - e242.
[Full Text] [PDF]

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 CirculationHome page
S. Windecker and B. Meier
Late Coronary Stent Thrombosis
Circulation, October 23, 2007; 116(17): 1952 - 1965.
[Full Text] [PDF]


 
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