Histopathological evaluation of thrombus in patients presenting with stent thrombosis. A multicenter European study: A report of the prevention of late stent thrombosis by an interdisciplinary global European effort consortium†

European Heart Journal

Volumn 37, Issue 19, 2016, Pages 1538-1549

  Riegger, Julia ^a,b   Byrne, Robert A ^b,c   Joner, Michael ^c,d   Chandraratne, Sue ^a,b   Gershlick, Anthony H ^e   Ten Berg, Jurrien M ^f   Adriaenssens, Tom ^g,h   Guagliumi, Giulio ⁱ   Godschalk, Thea C ^f   Neumann, Franz Josef ^j   Trenk, Dietmar ^j   Feldman, Laurent J ^k,l,m   Steg, Philippe Gabriel ^k,l,m,n   Desmet, Walter ^g,h   Alfonso, Fernando ^o   Goodall, Alison H ^e   Wojdyla, Roman ^p   Dudek, Dariusz ^p   Philippi, Vanessa ^a,b   Opinaldo, Sheryl ^a,b   Titova, Anna ^a,b   Malik, Nikesh ^e   Cotton, James ^q   Jhagroe, Darshni A ^f   Heestermans, Antonius A C M ^r,t   Sinnaeve, Peter ^g,h   Vermeersch, Paul ^s   Valina, Christian ^j   Schulz, Christian ^a,b   Kastrati, Adnan ^b,c   Massberg, Steffen ^a,b   Buysschaert, Ian ^t   Chausson, Mickaël ^t   De Cock, Dries ^t   Dens, Jo ^t   Barbato, Emanuele ^t   Gautier, Sandrine ^t   Abergel, Helene ^t   Jandrot Perrus, Martine ^t   Letourneur, Didier ^t   Mangin, Pierre ^t   Olivier, Veronique ^t   Roques, Caroline ^t   Gratz, Matthias ^t   Kennerknecht, Elisabeth ^t   Konrad, Ildiko ^t   Koppara, Tobias ^t   Ntziachristos, Vasilis ^t   Rosenthal, Amir ^t   Rzany, Alexander ^t   Steigerwald, Kristin ^t   Tada, Tomohiso ^t   Vogelsang, Andreas ^t   Xhepa, Erion ^t   Bernelli, Chiara ^t   Coccato, Micol ^t   Komukai, Kenichi ^t   Sirbu, Vasile ^t   Kerch, Garry ^t   Amoroso, Giovanni ^t   Dewilde, Willem J M ^t   Wykrzykowska, Joanne J ^t   Winkens, Mark H M ^t   Rzeszutko, Aukasz ^t   Zasada, Wojciech ^t   Cuesta, Javier ^t   Medina, Miguel ^t   Berry, Colin ^t   Curzen, Nick ^t   McEntegart, Margaret ^t   Gerber, Robert ^t   Hetherington, Simon ^t   Hill, Jonathan ^t   Kelly, Damian ^t   Oldroyd, Keith ^t   Routledge, Helen ^t   Shannon, Joanne ^t   Suresh, Venkatesan ^t   Zahman, Azfar ^t   more..

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d CVPATH INSTITUTE   (United States)

^e UNIVERSITY OF LEICESTER   (United Kingdom)

^f ST ANTONIUS HOSPITAL   (Netherlands)

^g UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^h UNIVERSITY OF LEUVEN   (Belgium)

ⁱ Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

^j UNIVERSITY HEART CENTER FREIBURG BAD KROZINGEN   (Germany)

^k Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^l BICHAT HOSPITAL   (France)

^m UNIVERSITÉ PARIS DESCARTES   (France)

ⁿ ROYAL BROMPTON HOSPITAL   (United Kingdom)

^o HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^p UNIVERSITY HOSPITAL IN KRAKOW   (Poland)

^q NEW CROSS HOSPITAL   (United Kingdom)

^r Location Alkmaar   (Netherlands)

^s Antwerp Cardiovascular Institute   (Belgium)

^t NONE

more..

Author keywords

Eosinophils; Histopathology; Neutrophil extracellular traps; Neutrophils; Platelets; Stent thrombosis; Thrombus aspiration

Indexed keywords

ACETYLSALICYLIC ACID; CLOPIDOGREL; EOSIN; FIBRIN DEGRADATION PRODUCT; FIBRINOGEN; HEMATOXYLIN; PRASUGREL; TICAGRELOR;

ADULT; ANTICOAGULANT THERAPY; ARTICLE; BARE METAL STENT; BIOLIMUS ELUTING CORONARY STENT; CELL INFILTRATION; CLINICAL EVALUATION; CONTROLLED STUDY; EUROPE; EVEROLIMUS ELUTING CORONARY STENT; EXTRACELLULAR TRAP; FEMALE; HEART INFARCTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; NEUTROPHIL; PACLITAXEL ELUTING CORONARY STENT; PRIORITY JOURNAL; SIROLIMUS ELUTING CORONARY STENT; STENT THROMBOSIS; THROMBOSIS PREVENTION; THROMBUS ASPIRATION; ZOTAROLIMUS ELUTING CORONARY STENT; AGED; CLINICAL TRIAL; CORONARY ARTERY THROMBOSIS; DRUG ELUTING STENT; EOSINOPHIL; GRAFT OCCLUSION; LYMPHOCYTE SUBPOPULATION; METABOLISM; PERCUTANEOUS CORONARY INTERVENTION; PROCEDURES; PROSPECTIVE STUDY; PROSTHESIS COMPLICATION; STENT; THROMBECTOMY; THROMBOCYTE;

AGED; BLOOD PLATELETS; CORONARY THROMBOSIS; DRUG-ELUTING STENTS; EOSINOPHILS; FEMALE; FIBRINOGEN; GRAFT OCCLUSION, VASCULAR; HUMANS; LEUKOCYTE COUNT; LYMPHOCYTE SUBSETS; MALE; NEUTROPHILS; PERCUTANEOUS CORONARY INTERVENTION; PROSPECTIVE STUDIES; PROSTHESIS FAILURE; STENTS; THROMBECTOMY;

EID: 84975782915     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehv419     Document Type: Article

References (27)

1. Tada T, Byrne RA, Simunovic I, King LA, Cassese S, Joner M, Fusaro M, Schneider S, Schulz S, Ibrahim T, Ott I, Massberg S, Laugwitz KL, Kastrati A. Risk of stent thrombosis among bare-metal stents, first-generation drug-eluting stents, and secondgeneration drug-eluting stents: results from a registry of 18,334 patients. JACC Cardiovasc Interv 2013;6:1267-1274.
2. Raber L, Magro M, Stefanini GG, Kalesan B, van Domburg RT, Onuma Y, Wenaweser P, Daemen J, Meier B, Juni P, Serruys PW, Windecker S. Very late coronary stent thrombosis of a newer-generation everolimus-eluting stent compared with early-generation drug-eluting stents: A prospective cohort study. Circulation 2012;125:1110-1121.
3. Schulz S, Schuster T, Mehilli J, Byrne RA, Ellert J, Massberg S, Goedel J, Bruskina O, Ulm K, Schomig A, Kastrati A. Stent thrombosis after drug-eluting stent implantation: incidence, timing, and relation to discontinuation of clopidogrel therapy over a 4-year period. Eur Heart J 2009;30:2714-2721.
4. Windecker S, Kolh P, Alfonso F, Collet JP, Cremer J, Falk V, Filippatos G, Hamm C, Head SJ, Juni P, Kappetein AP, Kastrati A, Knuuti J, Landmesser U, Laufer G, Neumann FJ, Richter DJ, Schauerte P, Sousa Uva M, Stefanini GG, Taggart DP, Torracca L, Valgimigli M, Wijns W, Witkowski A, Authors/Task Force m. 2014 ESC/EACTS Guidelines on myocardial revascularization: The Task Force on Myocardial Revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS)Developed with the special contribution of the European Association of Percutaneous Cardiovascular Interventions (EAPCI). Eur Heart J 2014;35:2541-2619.
5. Cook S, Ladich E, Nakazawa G, Eshtehardi P, Neidhart M, Vogel R, Togni M, Wenaweser P, Billinger M, Seiler C, Gay S, Meier B, Pichler WJ, Juni P, Virmani R, Windecker S. Correlation of intravascular ultrasound findings with histopathological analysis of thrombus aspirates in patients with very late drug-eluting stent thrombosis. Circulation 2009;120:391-399.
6. Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013;13:34-45.
7. Otsuka F, Yahagi K, Ladich E, Kutys R, Alexander R, Fowler D, Virmani R, Joner M. Hypersensitivity reaction in the US Food and Drug Administration-approved second-generation drug-eluting stents: histopathological assessment with ex vivo optical coherence tomography. Circulation 2015;131:322-324.
8. Otsuka F, Byrne RA, Yahagi K, Mori H, Ladich E, Fowler DR, Kutys R, Xhepa E, Kastrati A, Virmani R, Joner M. Neoatherosclerosis: overview of histopathologic findings and implications for intravascular imaging assessment. Eur Heart J 2015; doi:10.1093/eurheartj/ehv205.
9. Finn AV, Joner M, Nakazawa G, Kolodgie F, Newell J, John MC, Gold HK, Virmani R. Pathological correlates of late drug-eluting stent thrombosis: strut coverage as a marker of endothelialization. Circulation 2007;115:2435-2441.
10. 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.
11. PRESTIGE Consortium, Adriaenssens T, Byrne R. Prevention of late stent thrombosis by an interdisciplinary global European effort: PRESTIGE. Eur Heart J 2014;35: 2128-2129.
12. Luna L. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology, 3rd ed. New York: Blakiston Division, McGraw-Hill, 1968, p114-115.
13. Carstairs KC. The identification of platelets and platelet antigens in histological sections. J Pathol Bacteriol 1965;90:225-231.
14. von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012;209:819-835.
15. Crea F, Liuzzo G. Pathogenesis of acute coronary syndromes. J Am Coll Cardiol 2013; 61:1-11.
16. Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med 2008;359: 938-949.
17. Reinhardt C, von Bruhl ML, Manukyan D, Grahl L, Lorenz M, Altmann B, Dlugai S, Hess S, Konrad I, Orschiedt L, Mackman N, Ruddock L, Massberg S, Engelmann B. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008;118:1110-1122.
18. Wyss CA, Neidhart M, Altwegg L, Spanaus KS, Yonekawa K, Wischnewsky MB, Corti R, Kucher N, Roffi M, Eberli FR, Amann-Vesti B, Gay S, von Eckardstein A, Luscher TF, MaierW. Cellular actors, Toll-like receptors, and local cytokine profile in acute coronary syndromes. Eur Heart J 2010;31:1457-1469.
19. Klingenberg R, Brokopp CE, Grives A, Courtier A, Jaguszewski M, Pasqual N, Vlaskou Badra E, Lewandowski A, Gaemperli O, Hoerstrup SP, Maier W, Landmesser U, Luscher TF, Matter CM. Clonal restriction and predominance of regulatory T cells in coronary thrombi of patients with acute coronary syndromes. Eur Heart J 2015;36:1041-1048.
20. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, Konrad I, Kennerknecht E, Reges K, Holdenrieder S, Braun S, Reinhardt C, Spannagl M, Preissner KT, Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010;16:887-896.
21. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532-1535.
22. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood 2014;123: 2768-2776.
23. Schulz C, Engelmann B, Massberg S. Crossroads of coagulation and innate immunity: The case of deep vein thrombosis. J Thromb Haemost 2013;11(Suppl. 1): 233-241.
24. Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenbock A, Simon D, Laimer D, Bangert C, Kammerlander A, Mascherbauer J, Winter MP, Distelmaier K, Adlbrecht C, Preissner KT, Lang IM. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 2015;116:1182-1192.
25. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010;107:15880-5.
26. Virmani R, Guagliumi G, Farb A, Musumeci G, Grieco N, Motta T, Mihalcsik L, Tespili M, Valsecchi O, Kolodgie FD. Localized hypersensitivity and late coronary thrombosis secondary to a sirolimus-eluting stent: should we be cautious? Circulation 2004;109:701-705.
27. Wilson GJ, Nakazawa G, Schwartz RS, Huibregtse B, Poff B, Herbst TJ, Baim DS, Virmani R. Comparison of inflammatory response after implantation of sirolimusand paclitaxel-eluting stents in porcine coronary arteries. Circulation 2009;120: 141-149, 1, 2.