Acute coronary syndromes: The way forward from mechanisms to precision treatment

Circulation

Volumn 136, Issue 12, 2017, Pages 1155-1166

  Crea, Filippo ^a   Libby, Peter ^b  

^a CATHOLIC UNIVERSITY   (Italy)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Atherosclerotic; Erosion; Inflammation; Microvessels; Myocardial infarction; Plaque; Thrombosis

Indexed keywords

LIPID; ANTIINFLAMMATORY AGENT; C REACTIVE PROTEIN;

ACUTE CORONARY SYNDROME; ACUTE HEART INFARCTION; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL RUPTURE; CORONARY ARTERY OBSTRUCTION; CORONARY ARTERY THROMBOSIS; ELECTROCARDIOGRAM; EPICARDIUM; HEART INFARCTION; HUMAN; INFLAMMATION; LIPID METABOLISM; MICROANGIOPATHY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PERSONALIZED MEDICINE; PRIORITY JOURNAL; ST SEGMENT ELEVATION; ADAPTIVE IMMUNITY; COMPLICATION; DIAGNOSTIC IMAGING; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; THROMBOSIS;

ACUTE CORONARY SYNDROME; ADAPTIVE IMMUNITY; ANTI-INFLAMMATORY AGENTS; C-REACTIVE PROTEIN; HUMANS; PLAQUE, ATHEROSCLEROTIC; THROMBOSIS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 85030781847     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.117.029870     Document Type: Article

References (98)

1. Libby P. Molecular bases of the acute coronary syndromes. Circulation. 1995;91:2844-2850.
2. Libby P. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation. 2001;104:365-372.
3. Libby P. Mechanisms of acute coronary syndromes and their implications for therapy. N Engl J Med. 2013;368:2004-2013. doi: 10.1056/NEJMra1216063.
4. Libby P, Pasterkamp G. Requiem for the "vulnerable plaque." Eur Heart J. 2015;36:2984-2987. doi: 10.1093/eurheartj/ehv349.
5. Pasterkamp G, den Ruijter HM, Libby P. Temporal shifts in clinical presentation and underlying mechanisms of atherosclerotic disease. Nat Rev Cardiol. 2017;14:21-29. doi: 10.1038/nrcardio.2016.166.
6. Davies MJ, Thomas A. Thrombosis and acute coronary-artery lesions in sudden cardiac ischemic death. N Engl J Med. 1984;310:1137-1140. doi: 10.1056/NEJM198405033101801.
7. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation. 1995;92:657-671.
8. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol. 2010;30:1282-1292. doi: 10.1161/ATVBAHA.108.179739.
9. Motoyama S, Ito H, Sarai M, Kondo T, Kawai H, Nagahara Y, Harigaya H, Kan S, Anno H, Takahashi H, Naruse H, Ishii J, Hecht H, Shaw LJ, Ozaki Y, Narula J. Plaque characterization by coronary computed tomography angiography and the likelihood of acute coronary events in mid-term follow-up. J Am Coll Cardiol. 2015;66:337-346. doi: 10.1016/j.jacc.2015.05.069.
10. Mann J, Davies MJ. Mechanisms of progression in native coronary artery disease: role of healed plaque disruption. Heart. 1999;82:265-268.
11. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW; PROSPECT Investigators. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226-235. doi: 10.1056/NEJMoa1002358.
12. Kubo T, Maehara A, Mintz GS, Doi H, Tsujita K, Choi SY, Katoh O, Nasu K, Koenig A, Pieper M, Rogers JH, Wijns W, Böse D, Margolis MP, Moses JW, Stone GW, Leon MB. The dynamic nature of coronary artery lesion morphology assessed by serial virtual histology intravascular ultrasound tissue characterization. J Am Coll Cardiol. 2010;55:1590-1597. doi: 10.1016/j.jacc.2009.07.078.
13. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105:1135-1143.
14. Cristell N, Cianflone D, Durante A, Ammirati E, Vanuzzo D, Banfi M, Calori G, Latib A, Crea F, Marenzi G, De Metrio M, Moretti L, Li H, Uren NG, Hu D, Maseri A; FAMI Study Investigators. High-sensitivity C-reactive protein is within normal levels at the very onset of first ST-segment elevation acute myocardial infarction in 41% of cases: a multiethnic case-control study. J Am Coll Cardiol. 2011;58:2654-2661. doi: 10.1016/j.jacc.2011.08.055.
15. Scalone G, Niccoli G, Refaat H, Vergallo R, Porto I, Leone AM, Burzotta F, D'Amario D, Liuzzo G, Fracassi F, Trani C, Crea F. Not all plaque ruptures are born equal: an optical coherence tomography study [published online ahead of print December 24, 2016]. Eur Heart J Cardiovasc Imaging. doi: 10.1093/ehjci/jew208.
16. Arbustini E, Dal Bello B, Morbini P, Burke AP, Bocciarelli M, Specchia G, Virmani R. Plaque erosion is a major substrate for coronary thrombosis in acute myocardial infarction. Heart. 1999;82:269-272.
17. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res. 2014;114:1852-1866. doi: 10.1161/CIRCRESAHA.114.302721.
18. Niccoli G, Montone RA, Cataneo L, Cosentino N, Gramegna M, Refaat H, Porto I, Burzotta F, Trani C, Leone AM, Severino A, Crea F. Morphological- biohumoral correlations in acute coronary syndromes: pathogenetic implications. Int J Cardiol. 2014;171:463-466. doi: 10.1016/j.ijcard.2013.12.238.
19. Jia H, Abtahian F, Aguirre AD, Lee S, Chia S, Lowe H, Kato K, Yonetsu T, Vergallo R, Hu S, Tian J, Lee H, Park SJ, Jang YS, Raffel OC, Mizuno K, Uemura S, Itoh T, Kakuta T, Choi SY, Dauerman HL, Prasad A, Toma C, McNulty I, Zhang S, Yu B, Fuster V, Narula J, Virmani R, Jang IK. In vivo diagnosis of plaque erosion and calcified nodule in patients with acute coronary syndrome by intravascular optical coherence tomography. J Am Coll Cardiol. 2013;62:1748-1758. doi: 10.1016/j.jacc.2013.05.071.
20. Crea F, Liuzzo G. Pathogenesis of acute coronary syndromes. J Am Coll Cardiol. 2013;61:1-11. doi: 10.1016/j.jacc.2012.07.064.
21. Liuzzo G, Biasucci LM, Gallimore JR, Grillo RL, Rebuzzi AG, Pepys MB, Maseri A. The prognostic value of C-reactive protein and serum amyloid A protein in severe unstable angina. N Engl J Med. 1994;331:417-424. doi: 10.1056/NEJM199408183310701.
22. Schönbeck U, Mach F, Sukhova GK, Murphy C, Bonnefoy JY, Fabunmi RP, Libby P. Regulation of matrix metalloproteinase expression in human vascular smooth muscle cells by T lymphocytes: a role for CD40 signaling in plaque rupture? Circ Res. 1997;81:448-454.
23. Liuzzo G, Kopecky SL, Frye RL, O'Fallon WM, Maseri A, Goronzy JJ, Weyand CM. Perturbation of the T-cell repertoire in patients with unstable angina. Circulation. 1999;100:2135-2139.
24. Liuzzo G, Goronzy JJ, Yang H, Kopecky SL, Holmes DR, Frye RL, Weyand CM. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation. 2000;101:2883-2888.
25. Chen S, Crother TR, Arditi M. Emerging role of IL-17 in atherosclerosis. J Innate Immun. 2010;2:325-333. doi: 10.1159/000314626.
26. Gisterå A, Robertson AK, Andersson J, Ketelhuth DF, Ovchinnikova O, Nilsson SK, Lundberg AM, Li MO, Flavell RA, Hansson GK. Transforming growth factor-β signaling in T cells promotes stabilization of atherosclerotic plaques through an interleukin-17-dependent pathway. Sci Transl Med. 2013;5:196ra100. doi: 10.1126/scitranslmed.3006133.
27. Brusko TM, Putnam AL, Bluestone JA. Human regulatory T cells: role in autoimmune disease and therapeutic opportunities. Immunol Rev. 2008;223:371-390. doi: 10.1111/j.1600-065X.2008.00637.x.
28. Liuzzo G, Montone RA, Gabriele M, Pedicino D, Giglio AF, Trotta F, Galiffa VA, Previtero M, Severino A, Biasucci LM, Crea F. Identification of unique adaptive immune system signature in acute coronary syndromes. Int J Cardiol. 2013;168:564-567. doi: 10.1016/j.ijcard.2013.01.009.
29. Flego D, Severino A, Trotta F, Previtero M, Ucci S, Zara C, Pedicino D, Massaro G, Biasucci LM, Liuzzo G, Crea F. Altered CD31 expression and activity in helper T cells of acute coronary syndrome patients. Basic Res Cardiol. 2014;109:448. doi: 10.1007/s00395-014-0448-3.
30. Flego D, Severino A, Trotta F, Previtero M, Ucci S, Zara C, Massaro G, Pedicino D, Biasucci LM, Liuzzo G, Crea F. Increased PTPN22 expression and defective CREB activation impair regulatory T-cell differentiation in non-ST-segment elevation acute coronary syndromes. J Am Coll Cardiol. 2015;65:1175-1186. doi: 10.1016/j.jacc.2015.01.027.
31. Nidorf SM, Eikelboom JW, Budgeon CA, Thompson PL. Low-dose colchicine for secondary prevention of cardiovascular disease. J Am Coll Cardiol. 2013;61:404-410. doi: 10.1016/j.jacc.2012.10.027.
32. Tardif J-C, L'Allier P. Colchicine Cardiovascular Outcomes Trial (COLCOT). https://clinicaltrials.gov/ct2/show/NCT02551094. 2017. Accessed June 1, 2017.
33. Everett BM, Pradhan AD, Solomon DH, Paynter N, Macfadyen J, Zaharris E, Gupta M, Clearfield M, Libby P, Hasan AA, Glynn RJ, Ridker PM. Rationale and design of the Cardiovascular Inflammation Reduction Trial: a test of the inflammatory hypothesis of atherothrombosis. Am Heart J. 2013;166:199-207.e15. doi: 10.1016/j.ahj.2013.03.018.
34. Morton AC, Rothman AM, Greenwood JP, Gunn J, Chase A, Clarke B, Hall AS, Fox K, Foley C, Banya W, Wang D, Flather MD, Crossman DC. The effect of interleukin-1 receptor antagonist therapy on markers of inflammation in non-ST elevation acute coronary syndromes: the MRC-ILA Heart Study. Eur Heart J. 2015;36:377-384. doi: 10.1093/eurheartj/ehu272.
35. Ridker PM, Thuren T, Zalewski A, Libby P. Interleukin-1β inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-inflammatory Thrombosis Outcomes Study (CANTOS). Am Heart J. 2011;162:597-605. doi: 10.1016/j.ahj.2011.06.012.
36. Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, Fonseca F, Nicolau J, Koenig W, Anker SD, Kastelein JJP, Cornel JH, Pais P, Pella D, Genest J, Cifkova R, Lorenzatti A, Forster T, Kobalava Z, Vida-Simiti L, Flather M, Shimokawa H, Ogawa H, Dellborg M, Rossi PRF, Troquay RPT, Libby P, Glynn RJ and Group CT. Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease [published online ahead of print August 27, 2017]. N Engl J Med. 2017. doi: 10.1056/NEJMoa1707914.
37. Ridker PM, MacFadyen JG, Thuren T, Everett BM, Libby P, Glynn RJ, Ridker P, Lorenzatti A, Krum H, Varigos J, Siostrzonek P, Sinnaeve P, Fonseca F, Nicolau J, Gotcheva N, Genest J, Yong H, Urina-Triana M, Milicic D, Cifkova R, Vettus R, Koenig W, Anker SD, Manolis AJ, Wyss F, Forster T, Sigurdsson A, Pais P, Fucili A, Ogawa H, Shimokawa H, Veze I, Petrauskiene B, Salvador L, Kastelein J, Cornel JH, Klemsdal TO, Medina F, Budaj A, Vida-Simiti L, Kobalava Z, Otasevic P, Pella D, Lainscak M, Seung K-B, Commerford P, Dellborg M, Donath M, Hwang J-J, Kultursay H, Flather M, Ballantyne C, Bilazarian S, Chang W, East C, Everett B, Forgosh L, Glynn R, Harris B, Libby P, Ligueros M, Thuren T, Bohula E, Charmarthi B, Cheng S, Chou S, Danik J, McMahon G, Maron B, Ning M, Olenchock B, Pande R, Perlstein T, Pradhan A, Rost N, Singhal A, Taqueti V, Wei N, Burris H, Cioffi A, Dalseg AM, Ghosh N, Gralow J, Mayer T, Rugo H, Fowler V, Limaye AP, Cosgrove S, Levine D, Lopes R, Scott J, Thuren T, Ligueros M, Hilkert R, Tamesby G, Mickel C, Manning B, Woelcke J, Tan M, Manfreda S, Ponce T, Kam J, Saini R, Banker K, Salko T, Nandy P, Tawfik R, O'Neil G, Manne S, Jirvankar P, Lal S, Nema D, Jose J, Collins R, Bailey K, Blumenthal R, Colhoun H, Gersh B and Glynn RJ. Effect of interleukin-1β inhibition with canakinumab on incident lung cancer in patients with atherosclerosis: exploratory results from a randomised, double- blind, placebo-controlled trial [published online ahead of print August 25, 2017]. The Lancet. doi: 10.1016/S0140-6736(17)32247-X.
38. Fornasa G, Clement M, Groyer E, Gaston AT, Khallou-Laschet J, Morvan M, Guedj K, Kaveri SV, Tedgui A, Michel JB, Nicoletti A, Caligiuri G. A CD31-derived peptide prevents angiotensin II-induced atherosclerosis progression and aneurysm formation. Cardiovasc Res. 2012;94:30-37. doi: 10.1093/cvr/cvs076.
39. Stanford SM, Krishnamurthy D, Falk MD, Messina R, Debnath B, Li S, Liu T, Kazemi R, Dahl R, He Y, Yu X, Chan AC, Zhang ZY, Barrios AM, Woods VL Jr, Neamati N, Bottini N. Discovery of a novel series of inhibitors of lymphoid tyrosine phosphatase with activity in human T cells. J Med Chem. 2011;54:1640-1654. doi: 10.1021/jm101202j.
40. Putnam AL, Brusko TM, Lee MR, Liu W, Szot GL, Ghosh T, Atkinson MA, Bluestone JA. Expansion of human regulatory T-cells from patients with type 1 diabetes. Diabetes. 2009;58:652-662. doi: 10.2337/db08-1168.
41. Shah PK, Chyu KY, Dimayuga PC, Nilsson J. Vaccine for atherosclerosis. J Am Coll Cardiol. 2014;64:2779-2791. doi: 10.1016/j.jacc.2014.10.018.
42. Koskinas KC, Sukhova GK, Baker AB, Papafaklis MI, Chatzizisis YS, Coskun AU, Quillard T, Jonas M, Maynard C, Antoniadis AP, Shi GP, Libby P, Edelman ER, Feldman CL, Stone PH. Thin-capped atheromata with reduced collagen content in pigs develop in coronary arterial regions exposed to persistently low endothelial shear stress. Arterioscler Thromb Vasc Biol. 2013;33:1494-1504. doi: 10.1161/ATVBAHA.112.300827.
43. Chatzizisis YS, Baker AB, Sukhova GK, Koskinas KC, Papafaklis MI, Beigel R, Jonas M, Coskun AU, Stone BV, Maynard C, Shi GP, Libby P, Feldman CL, Edelman ER, Stone PH. Augmented expression and activity of extracellular matrix-degrading enzymes in regions of low endothelial shear stress colocalize with coronary atheromata with thin fibrous caps in pigs. Circulation. 2011;123:621-630. doi: 10.1161/CIRCULATIONAHA.110.970038.
44. Shiomi M, Ishida T, Kobayashi T, Nitta N, Sonoda A, Yamada S, Koike T, Kuniyoshi N, Murata K, Hirata K, Ito T, Libby P. Vasospasm of atherosclerotic coronary arteries precipitates acute ischemic myocardial damage in myocardial infarction-prone strain of the Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb Vasc Biol. 2013;33:2518-2523. doi: 10.1161/ATVBAHA.113.301303.
45. Libby P, Nahrendorf M, Swirski FK. Leukocytes link local and systemic inflammation in ischemic cardiovascular disease: an expanded "cardiovascular continuum". J Am Coll Cardiol. 2016;67:1091-1103. doi: 10.1016/j.jacc.2015.12.048.
46. Burke AP, Farb A, Malcom GT, Liang Y, Smialek JE, Virmani R. Plaque rupture and sudden death related to exertion in men with coronary artery disease. JAMA. 1999;281:921-926.
47. Janoudi A, Shamoun FE, Kalavakunta JK, Abela GS. Cholesterol crystal induced arterial inflammation and destabilization of atherosclerotic plaque. Eur Heart J. 2016;37:1959-1967. doi: 10.1093/eurheartj/ehv653.
48. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nuñez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010;464:1357-1361. doi: 10.1038/nature08938.
49. Nakamura S, Inami S, Murai K, Takano M, Takano H, Asai K, Yasutake M, Shimizu W, Mizuno K. Relationship between cholesterol crystals and culprit lesion characteristics in patients with stable coronary artery disease: an optical coherence tomography study. Clin Res Cardiol. 2014;103:1015-1021. doi: 10.1007/s00392-014-0748-5.
50. Liu L, Gardecki JA, Nadkarni SK, Toussaint JD, Yagi Y, Bouma BE, Tearney GJ. Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography. Nat Med. 2011;17:1010-1014. doi: 10.1038/nm.2409.
51. Loree HM, Tobias BJ, Gibson LJ, Kamm RD, Small DM, Lee RT. Mechanical properties of model atherosclerotic lesion lipid pools. Arterioscler Thromb. 1994;14:230-234.
52. Huang H, Virmani R, Younis H, Burke AP, Kamm RD, Lee RT. The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation. 2001;103:1051-1056.
53. Virmani R, Joner M, Sakakura K. Recent highlights of ATVB: calcification. Arterioscler Thromb Vasc Biol. 2014;34:1329-1332. doi: 10.1161/ATVBAHA.114.304000.
54. Ruiz JL, Weinbaum S, Aikawa E, Hutcheson JD. Zooming in on the genesis of atherosclerotic plaque microcalcifications. J Physiol. 2016;594:2915-2927. doi: 10.1113/JP271339.
55. Camici PG, Rimoldi OE, Gaemperli O, Libby P. Non-invasive anatomic and functional imaging of vascular inflammation and unstable plaque. Eur Heart J. 2012;33:1309-1317. doi: 10.1093/eurheartj/ehs067.
56. Libby P. How does lipid lowering prevent coronary events? New insights from human imaging trials. Eur Heart J. 2015;36:472-474. doi: 10.1093/eurheartj/ehu510.
57. Abela GS, Vedre A, Janoudi A, Huang R, Durga S, Tamhane U. Effect of statins on cholesterol crystallization and atherosclerotic plaque stabilization. Am J Cardiol. 2011;107:1710-1717. doi: 10.1016/j.amjcard. 2011.02.336.
58. Patel R, Janoudi A, Vedre A, Aziz K, Tamhane U, Rubinstein J, Abela OG, Berger K, Abela GS. Plaque rupture and thrombosis are reduced by lowering cholesterol levels and crystallization with ezetimibe and are correlated with fluorodeoxyglucose positron emission tomography. Arterioscler Thromb Vasc Biol. 2011;31:2007-2014. doi: 10.1161/ATVBAHA.111.226167.
59. Zimmer S, Grebe A, Bakke SS, Bode N, Halvorsen B, Ulas T, Skjelland M, De Nardo D, Labzin LI, Kerksiek A, Hempel C, Heneka MT, Hawxhurst V, Fitzgerald ML, Trebicka J, Björkhem I, Gustafsson JÅ, Westerterp M, Tall AR, Wright SD, Espevik T, Schultze JL, Nickenig G, Lütjohann D, Latz E. Cyclodextrin promotes atherosclerosis regression via macrophage reprogramming. Sci Transl Med. 2016;8:333ra50. doi: 10.1126/scitranslmed. aad6100.
60. Mohammadpour AH, Akhlaghi F. Future of cholesteryl ester transfer protein (CETP) inhibitors: a pharmacological perspective. Clin Pharmacokinet. 2013;52:615-626. doi: 10.1007/s40262-013-0071-8.
61. HPS/TIMI55-REVEAL Collaborative Group. Effects of Anacetrapib in Patients with Atherosclerotic Vascular Disease [published online ahead of print August 28, 2017]. N Engl J Med. doi: 10.1056/NEJMoa1706444.
62. Meuwese MC, de Groot E, Duivenvoorden R, Trip MD, Ose L, Maritz FJ, Basart DC, Kastelein JJ, Habib R, Davidson MH, Zwinderman AH, Schwocho LR, Stein EA; CAPTIVATE Investigators. ACAT inhibition and progression of carotid atherosclerosis in patients with familial hypercholesterolemia: the CAPTIVATE randomized trial. JAMA. 2009;301:1131-1139. doi: 10.1001/jama.301.11.1131.
63. Lüscher TF. Substrates of acute coronary syndromes: new insights into plaque rupture and erosion. Eur Heart J. 2015;36:1347-1349. doi: 10.1093/eurheartj/ehv149.
64. Ferrante G, Nakano M, Prati F, Niccoli G, Mallus MT, Ramazzotti V, Montone RA, Kolodgie FD, Virmani R, Crea F. High levels of systemic myeloperoxidase are associated with coronary plaque erosion in patients with acute coronary syndromes: a clinicopathological study. Circulation. 2010;122:2505-2513. doi: 10.1161/CIRCULATIONAHA.110.955302.
65. Yahagi K, Kolodgie FD, Lutter C, Mori H, Romero ME, Finn AV, Virmani R. Pathology of human coronary and carotid artery atherosclerosis and vascular calcification in diabetes mellitus. Arterioscler Thromb Vasc Biol. 2017;37:191-204. doi: 10.1161/ATVBAHA.116.306256.
66. Hansson GK, Libby P, Tabas I. Inflammation and plaque vulnerability. J Intern Med. 2015;278:483-493. doi: 10.1111/joim.12406.
67. Quillard T, Araújo HA, Franck G, Shvartz E, Sukhova G, Libby P. TLR2 and neutrophils potentiate endothelial stress, apoptosis and detachment: implications for superficial erosion. Eur Heart J. 2015;36:1394-1404. doi: 10.1093/eurheartj/ehv044.
68. Franck G, Mawson T, Sausen G, Salinas M, Masson GS, Cole A, Beltrami- Moreira M, Chatzizisis Y, Quillard T, Tesmenitsky Y, Shvartz E, Sukhova GK, Swirski FK, Nahrendorf M, Aikawa E, Croce KJ, Libby P. Flow perturbation mediates neutrophil recruitment and potentiates endothelial injury via TLR2 in mice: implications for superficial erosion. Circ Res. 2017;121:311. doi: 10.1161/CIRCRESAHA.117.310694.
69. Kolodgie FD, Burke AP, Wight TN, Virmani R. The accumulation of specific types of proteoglycans in eroded plaques: a role in coronary thrombosis in the absence of rupture. Curr Opin Lipidol. 2004;15:575-582.
70. Day AJ. The structure and regulation of hyaluronan-binding proteins. Biochem Soc Trans. 1999;27:115-121.
71. Butler LM, Rainger GE, Nash GB. A role for the endothelial glycosaminoglycan hyaluronan in neutrophil recruitment by endothelial cells cultured for prolonged periods. Exp Cell Res. 2009;315:3433-3441. doi: 10.1016/j.yexcr.2009.08.012.
72. Döring Y, Soehnlein O, Weber C. Neutrophil extracellular traps in atherosclerosis and atherothrombosis. Circ Res. 2017;120:736-743. doi: 10.1161/CIRCRESAHA.116.309692.
73. Libby P. Triglycerides on the rise: should we swap seats on the seesaw? Eur Heart J. 2015;36:774-776. doi: 10.1093/eurheartj/ehu500.
74. Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenböck 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. doi: 10.1161/CIRCRESAHA.116.304944.
75. Aguirre-Alvarado C, Segura-Cabrera A, Velázquez-Quesada I, Hernández-Esquivel MA, García-Pérez CA, Guerrero-Rodríguez SL, Ruiz-Moreno AJ, Rodríguez-Moreno A, Pérez-Tapia SM, Velasco-Velázquez MA. Virtual screening-driven repositioning of etoposide as CD44 antagonist in breast cancer cells. Oncotarget. 2016;7:23772-23784. doi: 10.18632/oncotarget.8180.
76. Jia H, Dai J, Hou J, Xing L, Ma L, Liu H, Xu M, Yao Y, Hu S, Yamamoto E, Lee H, Zhang S, Yu B, Jang IK. Effective anti-thrombotic therapy without stenting: intravascular optical coherence tomography-based management in plaque erosion (the EROSION study). Eur Heart J. 2017;38:792-800. doi: 10.1093/eurheartj/ehw381.
77. Libby P. Superficial erosion and the precision management of acute coronary syndromes: not one-size-fits-all. Eur Heart J. 2017;38:801-803. doi: 10.1093/eurheartj/ehw599.
78. Beltrame JF, Crea F, Kaski JC, Ogawa H, Ong P, Sechtem U, Shimokawa H, Bairey Merz CN; Coronary Vasomotion Disorders International Study Group (COVADIS). The who, what, why, when, how and where of vasospastic angina. Circ J. 2016;80:289-298. doi: 10.1253/circj.CJ-15-1202.
79. Ong P, Athanasiadis A, Borgulya G, Voehringer M, Sechtem U. 3-Year follow- up of patients with coronary artery spasm as cause of acute coronary syndrome: the CASPAR (Coronary Artery Spasm in Patients With Acute Coronary Syndrome) study follow-up. J Am Coll Cardiol. 2011;57:1471. doi: 10.1016/j.jacc.2010.08.626.
80. Sato K, Kaikita K, Nakayama N, Horio E, Yoshimura H, Ono T, Ohba K, Tsujita K, Kojima S, Tayama S, Hokimoto S, Matsui K, Sugiyama S, Yamabe H, Ogawa H. Coronary vasomotor response to intracoronary acetylcholine injection, clinical features, and long-term prognosis in 873 consecutive patients with coronary spasm: analysis of a single-center study over 20 years. J Am Heart Assoc. 2013;2:e000227. doi: 10.1161/JAHA.113.000227.
81. Bertrand ME, LaBlanche JM, Tilmant PY, Thieuleux FA, Delforge MR, Carre AG, Asseman P, Berzin B, Libersa C, Laurent JM. Frequency of provoked coronary arterial spasm in 1089 consecutive patients undergoing coronary arteriography. Circulation. 1982;65:1299-1306.
82. Pristipino C, Beltrame JF, Finocchiaro ML, Hattori R, Fujita M, Mongiardo R, Cianflone D, Sanna T, Sasayama S, Maseri A. Major racial differences in coronary constrictor response between Japanese and Caucasians with recent myocardial infarction. Circulation. 2000;101:1102-1108.
83. Camici PG, Crea F. Coronary microvascular dysfunction. N Engl J Med. 2007;356:830-840. doi: 10.1056/NEJMra061889.
84. Galiuto L, De Caterina AR, Porfidia A, Paraggio L, Barchetta S, Locorotondo G, Rebuzzi AG, Crea F. Reversible coronary microvascular dysfunction: a common pathogenetic mechanism in apical ballooning or tako-tsubo syndrome. Eur Heart J. 2010;31:1319-1327. doi: 10.1093/eurheartj/ehq039.
85. Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, Cammann VL, Sarcon A, Geyer V, Neumann CA, Seifert B, Hellermann J, Schwyzer M, Eisenhardt K, Jenewein J, Franke J, Katus HA, Burgdorf C, Schunkert H, Moeller C, Thiele H, Bauersachs J, Tschöpe C, Schultheiss HP, Laney CA, Rajan L, Michels G, Pfister R, Ukena C, Böhm M, Erbel R, Cuneo A, Kuck KH, Jacobshagen C, Hasenfuss G, Karakas M, Koenig W, Rottbauer W, Said SM, Braun-Dullaeus RC, Cuculi F, Banning A, Fischer TA, Vasankari T, Airaksinen KE, Fijalkowski M, Rynkiewicz A, Pawlak M, Opolski G, Dworakowski R, MacCarthy P, Kaiser C, Osswald S, Galiuto L, Crea F, Dichtl W, Franz WM, Empen K, Felix SB, Delmas C, Lairez O, Erne P, Bax JJ, Ford I, Ruschitzka F, Prasad A, Lüscher TF. Clinical features and outcomes of takotsubo (stress) cardiomyopathy. N Engl J Med. 2015;373:929-938. doi: 10.1056/NEJMoa1406761.
86. Arrebola-Moreno AL, Arrebola JP, Moral-Ruiz A, Ramirez-Hernandez JA, Melgares-Moreno R, Kaski JC. Coronary microvascular spasm triggers transient ischemic left ventricular diastolic abnormalities in patients with chest pain and angiographically normal coronary arteries. Atherosclerosis. 2014;236:207-214. doi: 10.1016/j.atherosclerosis.2014.07.009.
87. Kaski JC, Maseri A, Vejar M, Crea F, Hackett D. Spontaneous coronary artery spasm in variant angina is caused by a local hyperreactivity to a generalized constrictor stimulus. J Am Coll Cardiol. 1989;14:1456-1463.
88. Lanza GA, Pedrotti P, Pasceri V, Lucente M, Crea F, Maseri A. Autonomic changes associated with spontaneous coronary spasm in patients with variant angina. J Am Coll Cardiol. 1996;28:1249-1256. doi: 10.1016/S0735-1097(96)00309-9.
89. Shimokawa H, Tomoike H, Nabeyama S, Yamamoto H, Araki H, Nakamura M, Ishii Y, Tanaka K. Coronary artery spasm induced in atherosclerotic miniature swine. Science. 1983;221:560-562.
90. Ito A, Shimokawa H, Nakaike R, Fukai T, Sakata M, Takayanagi T, Egashira K, Takeshita A. Role of protein kinase C-mediated pathway in the pathogenesis of coronary artery spasm in a swine model. Circulation. 1994;90:2425-2431.
91. Shimokawa H, Seto M, Katsumata N, Amano M, Kozai T, Yamawaki T, Kuwata K, Kandabashi T, Egashira K, Ikegaki I, Asano T, Kaibuchi K, Takeshita A. Rho-kinase-mediated pathway induces enhanced myosin light chain phosphorylations in a swine model of coronary artery spasm. Cardiovasc Res. 1999;43:1029-1039.
92. Shimokawa H. 2014 Williams Harvey Lecture: importance of coronary vasomotion abnormalities: from bench to bedside. Eur Heart J. 2014;35:3180-3193. doi: 10.1093/eurheartj/ehu427.
93. Dai Z, Aoki T, Fukumoto Y, Shimokawa H. Coronary perivascular fibrosis is associated with impairment of coronary blood flow in patients with non-ischemic heart failure. J Cardiol. 2012;60:416-421. doi: 10.1016/j.jjcc.2012.06.009.
94. Kaski JC, Crea F, Meran D, Rodriguez L, Araujo L, Chierchia S, Davies G, Maseri A. Local coronary supersensitivity to diverse vasoconstrictive stimuli in patients with variant angina. Circulation. 1986;74:1255-1265.
95. Lanza GA, Careri G, Crea F. Mechanisms of coronary artery spasm. Circulation. 2011;124:1774-1782. doi: 10.1161/CIRCULATIONAHA.111.037283.
96. Abbate A, Hamza M, Cassano AD, Melchior R, Roberts C, Grizzard J, Shah K, Hastillo A, Kasirajan V, Crea F, Lanza GA, Vetrovec GW. Sympathectomy as a treatment for refractory coronary artery spasm. Int J Cardiol. 2012;161:e7-e9. doi: 10.1016/j.ijcard.2012.03.006.
97. Masumoto A, Mohri M, Shimokawa H, Urakami L, Usui M, Takeshita A. Suppression of coronary artery spasm by the Rho-kinase inhibitor fasudil in patients with vasospastic angina. Circulation. 2002;105:1545-1547.
98. King K, Grazette LP, Paltoo DN, McDevitt JT, Sia SK, Barrett PM, Apple FS, Gurbel PA, Weissleder R, Leeds H, Iturriaga EJ, Rao A, Adhikari B, Desvigne-Nickens P, Galis ZS, Libby P. Point-of-care technologies for precision cardiovascular care and clinical research: National Heart, Lung, and Blood Institute Working Group. JACC Basic Transl Sci. 2016;1:73-86. doi: 10.1016/j.jacbts.2016.01.008.