Coronary microvascular dysfunction in the clinical setting: From mystery to reality

European Heart Journal

Volumn 33, Issue 22, 2012, Pages 2771-2781

  Herrmann, Joerg ^a   Kaski, Juan Carlos ^b   Lerman, Amir ^a  

^a MAYO CLINIC   (United States)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cardiac syndrome X; Coronary flow reserve; Microvascular angina; Prognosis

Indexed keywords

ACUTE CORONARY SYNDROME; ACUTE HEART INFARCTION; ANGINA PECTORIS; CARDIAC IMAGING; CARDIOMYOPATHY; CHRONIC DISEASE; CLINICAL ASSESSMENT; CLINICAL FEATURE; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; FUNCTIONAL ANATOMY; HEART FAILURE; HUMAN; MICROCIRCULATION; MICROSCOPIC ANATOMY; MICROVASCULATURE; PATHOGENESIS; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; PROGNOSIS; REVIEW; SYNDROME X;

ACUTE CORONARY SYNDROME; CARDIAC IMAGING TECHNIQUES; CARDIOMYOPATHIES; CHRONIC DISEASE; HEART FAILURE; HEMODYNAMICS; HUMANS; MICROCIRCULATION; MICROVASCULAR ANGINA; MYOCARDIAL INFARCTION; PERCUTANEOUS CORONARY INTERVENTION; PROGNOSIS;

EID: 84869444107     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehs246     Document Type: Review

References (112)

1. Kemp HG Jr, Vokonas PS, Cohn PF, Gorlin R. The anginal syndrome associated with normal coronary arteriograms. Report of a six year experience. Am J Med 1973;54:735-742.
2. Kaski JC. Pathophysiology and management of patients with chest pain and normal coronary arteriograms (cardiac syndrome X). Circulation 2004;109:568-572. (Pubitemid 38198862)
3. Patel B, Fisher M. Therapeutic advances in myocardial microvascular resistance: unravelling the enigma. Pharmacol Ther 2010;127:131-147.
4. Camici PG, Crea F. Coronary microvascular dysfunction. N Engl J Med 2007;356:830-840.
5. Kuo L, Chilian WM, Davis MJ. Coronary arteriolar myogenic response is independent of endothelium. Circ Res 1990;66:860-866. (Pubitemid 20086923)
6. van 't Hof AW, Liem A, Suryapranata H, Hoorntje JC, de Boer MJ, Zijlstra F. Angiographic assessment of myocardial reperfusion in patients treated with primary angioplasty for acute myocardial infarction: myocardial blush grade. Zwolle Myocardial Infarction Study Group. Circulation 1998;97:2302-2306. (Pubitemid 28280383)
7. Wu KC, Zerhouni EA, Judd RM, Lugo-Olivieri CH, Barouch LA, Schulman SP, Blumenthal RS, Lima JA. Prognostic significance of microvascular obstruction by magnetic resonance imaging in patients with acute myocardial infarction. Circulation 1998;97:765-772. (Pubitemid 28135339)
8. Leung DY, Leung M. Non-invasive/invasive imaging: significance and assessment of coronary microvascular dysfunction. Heart 2011;97:587-595.
9. Cassar A, Chareonthaitawee P, Rihal CS, Prasad A, Lennon RJ, Lerman LO, Lerman A. Lack of correlation between noninvasive stress tests and invasive coronary vasomotor dysfunction in patients with nonobstructive coronary artery disease. Circ Cardiovasc Interv 2009;2:237-244.
10. Gibson CM, Cannon CP, Daley WL, Dodge JT Jr, Alexander B Jr, Marble SJ, McCabe CH, Raymond L, Fortin T, Poole WK, Braunwald E. TIMI frame count: a quantitative method of assessing coronary artery flow. Circulation 1996;93:879-888. (Pubitemid 26074824)
11. Kern MJ. Coronary physiology revisited: practical insights from the cardiac cath-eterization laboratory. Circulation 2000;101:1344-1351. (Pubitemid 30158625)
12. Pijls NH, De Bruyne B, Smith L, Aarnoudse W, Barbato E, Bartunek J, Bech GJ, Van De Vosse F. Coronary thermodilution to assess flow reserve: validation in humans. Circulation 2002;105:2482-2486. (Pubitemid 34568968)
13. Fearon WF, Balsam LB, Farouque HM, Caffarelli AD, Robbins RC, Fitzgerald PJ, Yock PG, Yeung AC. Novel index for invasively assessing the coronary microcirculation. Circulation 2003;107:3129-3132. (Pubitemid 36793080)
14. Melikian N, Kearney MT, Thomas MR, De Bruyne B, Shah AM, MacCarthy PA. A simple thermodilution technique to assess coronary endothelium-dependent microvascular function in humans: validation and comparison with coronary flow reserve. Eur Heart J 2007;28:2188-2194. (Pubitemid 47428940)
15. Yong AS, Ho M, Shah MG, Ng MK, Fearon WF. Coronary microcirculatory resistance is independent of epicardial stenosis. Circ Cardiovasc Interv 2012;5:103-108, S1-2.
16. Herrmann J, Lerman A. The endothelium: dysfunction and beyond. J Nucl Cardiol 2001;8:197-206. (Pubitemid 32401086)
17. Newby DE. Intracoronary infusions and the assessment of coronary blood flow in clinical studies. Heart 2000;84:118-120. (Pubitemid 30619721)
18. Summers MR, Lerman A, Lennon RJ, Rihal CS, Prasad A. Myocardial ischaemia in patients with coronary endothelial dysfunction: insights from body surface ECG mapping and implications for invasive evaluation of chronic chest pain. Eur Heart J 2011;32:2758-2765.
19. Hirohata A, Nakamura M, Waseda K, Honda Y, Lee DP, Vagelos RH, Hunt SA, Valantine HA, Yock PG, Fitzgerald PJ, Yeung AC, Fearon WF. Changes in coronary anatomy and physiology after heart transplantation. Am J Cardiol 2007;99:1603-1607. (Pubitemid 46770649)
20. Di Carli MF, Tobes MC, Mangner T, Levine AB, Muzik O, Chakroborty P, Levine TB. Effects of cardiac sympathetic innervation on coronary blood flow. N Engl J Med 1997;336:1208-1215. (Pubitemid 27183650)
21. Wildhirt SM, Weis M, Schulze C, Conrad N, Rieder G, Enders G, Hoepp C, von Scheidt W, Reichart B. An association between microvascular endothelial dysfunction, transcardiac nitric oxide production and pro-inflammatory cytokines after heart transplantation in humans. Transpl Int 2000;13(Suppl. 1):S228-S234.
22. Xu Y, Chester AH, Hariri B, McCormack A, Sarathchandra P, Rose ML. The indirect alloimmune response causes microvascular endothelial dysfunction-a possible role for alloantibody. Transplantation 2010;90:1157-1164.
23. Osto E, Castellani C, Fadini GP, Baesso I, Gambino A, Agostini C, Avogaro A, Gerosa G, Thiene G, Iliceto S, Angelini A, Tona F. Impaired endothelial progenitor cell recruitment may contribute to heart transplant microvasculopathy. J Heart Lung Transplant 2011;30:70-76.
24. Lanza GA, Crea F. Primary coronary microvascular dysfunction: clinical presentation, pathophysiology, and management. Circulation 2010;121:2317-2325.
25. Takeuchi M, Kuroiwa A. Alteration of coronary flow velocity during spontaneous angina in a patient with microvascular angina. Catheter Cardiovasc Interv 2000;50:63-67. (Pubitemid 30249777)
26. Cannon RO III, Epstein SE. 'Microvascular angina' as a cause of chest pain with angiographically normal coronary arteries. Am J Cardiol 1988;61:1338-1343.
27. Kaski JC, Aldama G, Cosin-Sales J. Cardiac syndrome X. Diagnosis, pathogenesis and management. Am J Cardiovasc Drugs 2004;4:179-194. (Pubitemid 38780004)
28. Maseri A, Crea F, Kaski JC, Davies G. Mechanisms and significance of cardiac is-chemic pain. Prog Cardiovasc Dis 1992;35:1-18.
29. Nihoyannopoulos P, Kaski JC, Crake T, Maseri A. Absence of myocardial dysfunction during stress in patients with syndrome X. J Am Coll Cardiol 1991;18:1463-1470.
30. Douglas PS, Patel MR, Bailey SR, Dai D, Kaltenbach L, Brindis RG, Messenger J, Peterson ED. Hospital variability in the rate of finding obstructive coronary artery disease at elective, diagnostic coronary angiography. J Am Coll Cardiol 2011;58:801-809.
31. Jespersen L, Hvelplund A, Abildstrom SZ, Pedersen F, Galatius S, Madsen JK, Jorgensen E, Kelbaek H, Prescott E. Stable angina pectoris with no obstructive coronary artery disease is associated with increased risks of major adverse cardiovascular events. Eur Heart J 2012;33:734-744.
32. Ong P, Athanasiadis A, Borgulya G, Mahrholdt H, Kaski JC, Sechtem U. High prevalence of a pathological response to acetylcholine testing in patients with stable angina pectoris and unobstructed coronary arteries. The ACOVA Study (Abnormal COronary VAsomotion in patients with stable angina and unobstructed coronary arteries). J Am Coll Cardiol 2012;59:655-662.
33. Cosin-Sales J, Pizzi C, Brown S, Kaski JC. C-reactive protein, clinical presentation, and ischemic activity in patients with chest pain and normal coronary angio-grams. J Am Coll Cardiol 2003;41:1468-1474. (Pubitemid 36543361)
34. Kanatsuka H, Eastham CL, Marcus ML, Lamping KG. Effects of nitroglycerin on the coronary microcirculation in normal and ischemic myocardium. J Cardiovasc Pharmacol 1992;19:755-763.
35. Clarke JG, Davies GJ, Kerwin R, Hackett D, Larkin S, Dawbarn D, Lee Y, Bloom SR, Yacoub M, Maseri A. Coronary artery infusion of neuropeptide Y in patients with angina pectoris. Lancet 1987;1:1057-1059. (Pubitemid 17061330)
36. Beltrame JF, Limaye SB, Horowitz JD. The coronary slow flow phenomenon-a new coronary microvascular disorder. Cardiology 2002;97:197-202.
37. Fineschi M, Gori T. Coronary slow flow: description of a new 'cardiac Y' syndrome. Int J Cardiol 2009;137:308-310.
38. Fragasso G, Chierchia SL, Arioli F, Carandente O, Gerosa S, Carlino M, Palloshi A, Gianolli L, Calori G, Fazio F, Margonato A. Coronary slow-flow causing transient myocardial hypoperfusion in patients with cardiac syndrome X: long-term clinical and functional prognosis. Int J Cardiol 2009;137:137-144.
39. Beltrame JF, Limaye SB, Wuttke RD, Horowitz JD. Coronary hemodynamic and metabolic studies of the coronary slow flow phenomenon. Am Heart J 2003;146:84-90. (Pubitemid 36851304)
40. Fineschi M, Bravi A, Gori T. The 'slow coronary flow' phenomenon: evidence of preserved coronary flow reserve despite increased resting microvascular resistances. Int J Cardiol 2008;127:358-361. (Pubitemid 351885085)
41. Melikian N, Vercauteren S, Fearon WF, Cuisset T, MacCarthy PA, Davidavicius G, Aarnoudse W, Bartunek J, Vanderheyden M, Wyffels E, Wijns W, Heyndrickx GR, Pijls NH, de Bruyne B. Quantitative assessment of coronary microvascular function in patients with and without epicardial atherosclerosis. EuroIntervention 2010;5:939-945.
42. Zeiher AM, Drexler H, Wollschlager H, Just H. Endothelial dysfunction of the coronary microvasculature is associated with coronary blood flow regulation in patients with early atherosclerosis. Circulation 1991;84:1984-1992.
43. Schindler TH, Schelbert HR, Quercioli A, Dilsizian V. Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health. JACC Cardiovasc Imaging 2010;3:623-640.
44. Tonino PA, De Bruyne B, Pijls NH, Siebert U, Ikeno F, van't Veer M, Klauss V, Manoharan G, Engstrom T, Oldroyd KG, Ver Lee PN, MacCarthy PA, Fearon WF. Fractional flow reserve versus angiography for guiding percutaneous coronary intervention. N Engl J Med 2009;360:213-224.
45. Herrmann J. Peri-procedural myocardial injury:2005 update. Eur Heart J 2005; 26:2493-2519. (Pubitemid 41679359)
46. Prasad A, Herrmann J. Myocardial infarction due to percutaneous coronary intervention. N Engl J Med 2011;364:453-464.
47. Marcus ML, Doty DB, Hiratzka LF, Wright CB, Eastham CL. Decreased coronary reserve: a mechanism for angina pectoris in patients with aortic stenosis and normal coronary arteries. N Engl J Med 1982;307:1362-1366. (Pubitemid 13233012)
48. Eberli FR, Ritter M, Schwitter J, Bortone A, Schneider J, Hess OM, Krayenbuehl HP. Coronary reserve in patients with aortic valve disease before and after successful aortic valve replacement. Eur Heart J 1991;12:127-138.
49. Davies JE, Sen S, Broyd C, Hadjiloizou N, Baksi J, Francis DP, Foale RA, Parker KH, Hughes AD, Chukwuemeka A, Casula R, Malik IS, Mikhail GW, Mayet J. Arterial pulse wave dynamics after percutaneous aortic valve replacement: fall in coronary diastolic suction with increasing heart rate as a basis for angina symptoms in aortic stenosis. Circulation 2011;124:1565-1572.
50. Hamm CW, Bassand JP, Agewall S, Bax J, Boersma E, Bueno H, Caso P, Dudek D, Gielen S, Huber K, Ohman M, Petrie MC, Sonntag F, Uva MS, Storey RF, Wijns W, Zahger D, Bax JJ, Auricchio A, Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Knuuti J, Kolh P, McDonagh T, Moulin C, Poldermans D, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Torbicki A, Vahanian A, Windecker S, Achenbach S, Badimon L, Bertrand M, Botker HE, Collet JP, Crea F, Danchin N, Falk E, Goudevenos J, Gulba D, Hambrecht R, Herrmann J, Kastrati A, Kjeldsen K, Kristensen SD, Lancellotti P, Mehilli J, Merkely B, Montalescot G, Neumann FJ, Neyses L, Perk J, Roffi M, Romeo F, Ruda M, Swahn E, Valgimigli M, Vrints CJ, Widimsky P. ESC Guidelines for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation: The Task Force for the management of acute coronary syndromes (ACS) in patients presenting without persistent ST-segment elevation of the European Society of Cardiology (ESC). Eur Heart J 2011;32:2999-3054.
51. Lagerqvist B, Safstrom K, Stahle E, Wallentin L, Swahn E. Is early invasive treatment of unstable coronary artery disease equally effective for both women and men? FRISC II Study Group Investigators. J Am Coll Cardiol 2001;38:41-48. (Pubitemid 32613826)
52. Germing A, Lindstaedt M, Ulrich S, Grewe P, Bojara W, Lawo T, von Dryander S, Jager D, Machraoui A, Mugge A, Lemke B. Normal angiogram in acute coronary syndrome-preangiographic risk stratification, angiographic findings and follow-up. Int J Cardiol 2005;99:19-23. (Pubitemid 40261019)
53. Gibson CM, Ryan KA, Murphy SA, Mesley R, Marble SJ, Giugliano RP, Cannon CP, Antman EM, Braunwald E. Impaired coronary blood flow in noncul-prit arteries in the setting of acute myocardial infarction. The TIMI Study Group. Thrombolysis in myocardial infarction. J Am Coll Cardiol 1999;34:974-982. (Pubitemid 29500526)
54. Lerman A, Holmes DR, Herrmann J, Gersh BJ. Microcirculatory dysfunction in ST-elevation myocardial infarction: cause, consequence, or both? Eur Heart J 2007;28:788-797. (Pubitemid 47343589)
55. Marzilli M, Sambuceti G, Fedele S, L'Abbate A. Coronary microcirculatory vasoconstriction during ischemia in patients with unstable angina. J Am Coll Cardiol 2000;35:327-334. (Pubitemid 30125521)
56. Herrmann J, Haude M, Lerman A, Schulz R, Volbracht L, Ge J, Schmermund A, Wieneke H, von Birgelen C, Eggebrecht H, Baumgart D, Heusch G, Erbel R. Abnormal coronary flow velocity reserve after coronary intervention is associated with cardiac marker elevation. Circulation 2001;103:2339-2345. (Pubitemid 32448797)
57. Hoole SP, White PA, Heck PM, Khan SN, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O'Sullivan M, Dutka DP. Primary coronary microvascular dysfunction and poor coronary collaterals predict post-percutaneous coronary intervention cardiac necrosis. Coron Artery Dis 2009;20:253-259.
58. Prasad A, Stone GW, Stuckey TD, Costantini CO, Zimetbaum PJ, McLaughlin M, Mehran R, Garcia E, Tcheng JE, Cox DA, Grines CL, Lansky AJ, Gersh BJ. Impact of diabetes mellitus on myocardial perfusion after primary angioplasty in patients with acute myocardial infarction. J Am Coll Cardiol 2005;45:508-514. (Pubitemid 40222243)
59. Roe MT, Ohman EM, Maas AC, Christenson RH, Mahaffey KW, Granger CB, Harrington RA, Califf RM, Krucoff MW. Shifting the open-artery hypothesis downstream: the quest for optimal reperfusion. J Am Coll Cardiol 2001;37:9-18. (Pubitemid 32051713)
60. Yamamuro A, Akasaka T, Tamita K, Yamabe K, Katayama M, Takagi T, Morioka S. Coronary flow velocity pattern immediately after percutaneous coronary intervention as a predictor of complications and in-hospital survival after acute myo-cardial infarction. Circulation 2002;106:3051-3056. (Pubitemid 35440287)
61. Elesber A, Lerman A, Bybee KA, Murphy JG, Barsness G, Singh M, Rihal CS, Prasad A. Myocardial perfusion in apical ballooning syndrome correlate of myo-cardial injury. Am Heart J 2006;152:469 e9-13.
62. Meimoun P, Malaquin D, Sayah S, Benali T, Luycx-Bore A, Levy F, Zemir H, Tribouilloy C. The coronary flow reserve is transiently impaired in tako-tsubo cardiomyopathy: a prospective study using serial Doppler transthoracic echocar-diography. J Am Soc Echocardiogr 2008;21:72-77.
63. Rigo F, Sicari R, Citro R, Ossena G, Buja P, Picano E. Diffuse, marked, reversible impairment in coronary microcirculation in stress cardiomyopathy: a Doppler transthoracic echo study. Ann Med 2009;41:462-470.
64. Kurowski V, Kaiser A, von Hof K, Killermann DP, Mayer B, Hartmann F, Schunkert H, Radke PW. Apical and midventricular transient left ventricular dysfunction syndrome (tako-tsubo cardiomyopathy): frequency, mechanisms, and prognosis. Chest 2007;132:809-816.
65. Feola M, Rosso GL, Casasso F, Morena L, Biggi A, Chauvie S, Ribichini F, Uslenghi E. Reversible inverse mismatch in transient left ventricular apical ballooning: perfusion/metabolism positron emission tomography imaging. J Nuclear Cardiol 2006;13:587-590. (Pubitemid 44204151)
66. 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.
67. Barletta G, Del Pace S, Boddi M, Del Bene R, Salvadori C, Bellandi B, Coppo M, Saletti E, Gensini GF. Abnormal coronary reserve and left ventricular wall motion during cold pressor test in patients with previous left ventricular ballooning syndrome. Eur Heart J 2009;30:3007-3014.
68. Martin EA, Prasad A, Rihal CS, Lerman LO, Lerman A. Endothelial function and vascular response to mental stress are impaired in patients with apical ballooning syndrome. J Am Coll Cardiol 2010;56:1840-1846.
69. Demir H, Kahraman G, Isgoren S, Tan YZ, Kilic T, Berk F. Evaluation of post-stress left ventricular dysfunction and its relationship with perfusion abnormalities using gated SPECT in patients with cardiac syndrome X. Nuc Med Commun 2008;29:208-214. (Pubitemid 351499296)
70. Peix A, Gonzalez A, Garcia EJ, Valiente J, Cabrera LO, Sixto S, Filgueiras CE, Cabale B, Hechavarria S, Gonzalez I, Carrillo R, Garcia-Barreto D. Left ventricular dysfunction secondary to ischemia in women with angina and normal coronary angiograms. J Womens Health 2009;18:155-161.
71. Morishima I, Sone T, Okumura K, Tsuboi H, Kondo J, Mukawa H, Matsui H, Toki Y, Ito T, Hayakawa T. Angiographic no-reflow phenomenon as a predictor of adverse long-term outcome in patients treated with percutaneous translum-inal coronary angioplasty for first acute myocardial infarction. J Am Coll Cardiol 2000;36:1202-1209.
72. Bolognese L, Carrabba N, Parodi G, Santoro GM, Buonamici P, Cerisano G, Antoniucci D. Impact of microvascular dysfunction on left ventricular remodeling and long-term clinical outcome after primary coronary angioplasty for acute myocardial infarction. Circulation 2004;109:1121-1126. (Pubitemid 38332616)
73. Olivotto I, Cecchi F, Gistri R, Lorenzoni R, Chiriatti G, Girolami F, Torricelli F, Camici PG. Relevance of coronary microvascular flow impairment to long-term remodeling and systolic dysfunction in hypertrophic cardiomyopathy. J Am Coll Cardiol 2006;47:1043-1048.
74. Pereira VF, de Carvalho Frimm C, Rodrigues AC, Curi M. Coronary reserve impairment prevents the improvement of left ventricular dysfunction and adversely affects the long-term outcome of patients with hypertensive dilated cardiomy-opathy. JASH 2010;4:14-21.
75. Strauer BE, Motz W, Vogt M, Schwartzkopff B. Evidence for reduced coronary flow reserve in patients with insulin-dependent diabetes. A possible cause for diabetic heart disease in man. Exp Clin Endocrinol Diabetes 1997;105:15-20. (Pubitemid 27116835)
76. Galderisi M. Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J Am Coll Cardiol 2006;48:1548-1551. (Pubitemid 44528192)
77. Yoon YS, Uchida S, Masuo O, Cejna M, Park JS, Gwon HC, Kirchmair R, Bahlman F, Walter D, Curry C, Hanley A, Isner JM, Losordo DW. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation 2005;111:2073-2085. (Pubitemid 40577902)
78. Gill RM, Jones BD, Corbly AK, Wang J, Braz JC, Sandusky GE, Shen W. Cardiac diastolic dysfunction in conscious dogs with heart failure induced by chronic coronary microembolization. Am J Physiol Heart Circ Physiol 2006;291: H3154-H3158. (Pubitemid 44904119)
79. Bemiller CR, Pepine CJ, Rogers AK. Long-term observations in patients with angina and normal coronary arteriograms. Circulation 1973;47:36-43.
80. Day LJ, Sowton E. Clinical features and follow-up of patients with angina and normal coronary arteries. Lancet 1976;2:334-337.
81. Kaski JC, Rosano GM, Collins P, Nihoyannopoulos P, Maseri A, Poole-Wilson PA. Cardiac syndrome X: clinical characteristics and left ventricular function. Long-term follow-up study. J Am Coll Cardiol 1995;25:807-814.
82. Romeo F, Rosano GM, Martuscelli E, Lombardo L, Valente A. Long-term follow-up of patients initially diagnosed with syndrome X. Am J Cardiol 1993;71:669-673. (Pubitemid 23085816)
83. Sicari R, Palinkas A, Pasanisi EG, Venneri L, Picano E. Long-term survival of patients with chest pain syndrome and angiographically normal or near-normal coronary arteries: the additional prognostic value of dipyridamole echocardiog-raphy test (DET). Eur Heart J 2005;26:2136-2141. (Pubitemid 41407996)
84. Britten MB, Zeiher AM, Schachinger V. Microvascular dysfunction in angiographi-cally normal or mildly diseased coronary arteries predicts adverse cardiovascular long-term outcome. Coron Artery Dis 2004;15:259-264. (Pubitemid 39061609)
85. Pepine CJ, Anderson RD, Sharaf BL, Reis SE, Smith KM, Handberg EM, Johnson BD, Sopko G, Bairey Merz CN. Coronary microvascular reactivity to adenosine predicts adverse outcome in women evaluated for suspected ischemia results from the National Heart, Lung and Blood Institute WISE (Women's Ischemia Syndrome Evaluation) study. J Am Coll Cardiol 2010;55:2825-2832.
86. Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR Jr, Lerman A. Long-term follow-up of patients with mild coronary artery disease and endothe-lial dysfunction. Circulation 2000;101:948-954. (Pubitemid 30131694)
87. Halcox JP, Schenke WH, Zalos G, Mincemoyer R, Prasad A, Waclawiw MA, Nour KR, Quyyumi AA. Prognostic value of coronary vascular endothelial dysfunction. Circulation 2002;106:653-658. (Pubitemid 34851922)
88. Marks DS, Gudapati S, Prisant LM, Weir B, diDonato-Gonzalez C, Waller JL, Houghton JL. Mortality in patients with microvascular disease. J Clin Hypertens 2004;6:304-309.
89. Sicari R, Rigo F, Cortigiani L, Gherardi S, Galderisi M, Picano E. Additive prognostic value of coronary flow reserve in patients with chest pain syndrome and normal or near-normal coronary arteries. Am J Cardiol 2009;103:626-631.
90. von Mering GO, Arant CB, Wessel TR, McGorray SP, Bairey Merz CN, Sharaf BL, Smith KM, Olson MB, Johnson BD, Sopko G, Handberg E, Pepine CJ, Kerensky RA. Abnormal coronary vasomotion as a prognostic indicator of cardiovascular events in women: results from the National Heart, Lung, and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE). Circulation 2004;109:722-725. (Pubitemid 38222890)
91. Herzog BA, Husmann L, Valenta I, Gaemperli O, Siegrist PT, Tay FM, Burkhard N, Wyss CA, Kaufmann PA. Long-term prognostic value of 13N-ammonia myocardial perfusion positron emission tomography added value of coronary flow reserve. J Am Coll Cardiol 2009;54:150-156.
92. Schindler TH, Nitzsche EU, Schelbert HR, Olschewski M, Sayre J, Mix M, Brink I, Zhang XL, Kreissl M, Magosaki N, Just H, Solzbach U. Positron emission tomography-measured abnormal responses of myocardial blood flow to sympathetic stimulation are associated with the risk of developing cardiovascular events. J Am Coll Cardiol 2005;45:1505-1512. (Pubitemid 40615626)
93. Fearon WF, Shah M, Ng M, Brinton T, Wilson A, Tremmel JA, Schnittger I, Lee DP, Vagelos RH, Fitzgerald PJ, Yock PG, Yeung AC. Predictive value of the index of microcirculatory resistance in patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 2008;51:560-565.
94. Lim HS, Yoon MH, Tahk SJ, Yang HM, Choi BJ, Choi SY, Sheen SS, Hwang GS, Kang SJ, Shin JH. Usefulness of the index of microcirculatory resistance for inva-sively assessing myocardial viability immediately after primary angioplasty for anterior myocardial infarction. Eur Heart J 2009;30:2854-2860.
95. Sorajja P, Gersh BJ, Costantini C, McLaughlin MG, Zimetbaum P, Cox DA, Garcia E, Tcheng JE, Mehran R, Lansky AJ, Kandzari DE, Grines CL, Stone GW. Combined prognostic utility of ST-segment recovery and myocardial blush after primary percutaneous coronary intervention in acute myocardial infarction. Eur Heart J 2005;26:667-674. (Pubitemid 40516878)
96. Poli A, Fetiveau R, Vandoni P, del Rosso G, D'Urbano M, Seveso G, Cafiero F, De Servi S. Integrated analysis of myocardial blush and ST-segment elevation recovery after successful primary angioplasty: Real-time grading of microvascular reperfusion and prediction of early and late recovery of left ventricular function. Circulation 2002;106:313-318. (Pubitemid 34778954)
97. de Waha S, Desch S, Eitel I, Fuernau G, Zachrau J, Leuschner A, Gutberlet M, Schuler G, Thiele H. Impact of early vs. late microvascular obstruction assessed by magnetic resonance imaging on long-term outcome after ST-elevation myo-cardial infarction: a comparison with traditional prognostic markers. Eur Heart J 2010;31:2660-2668.
98. Nijveldt R, Beek AM, Hofman MB, Umans VA, Algra PR, Spreeuwenberg MD, Visser CA, van Rossum AC. Late gadolinium-enhanced cardiovascular magnetic resonance evaluation of infarct size and microvascular obstruction in optimally treated patients after acute myocardial infarction. J Cardiovasc Magn Reson 2007;9:765-770. (Pubitemid 47463905)
99. Grube E, Gerckens U, Yeung AC, Rowold S, Kirchhof N, Sedgewick J, Yadav JS, Stertzer S. Prevention of distal embolization during coronary angioplasty in sa-phenous vein grafts and native vessels using porous filter protection. Circulation 2001;104:2436-2441. (Pubitemid 33108377)
100. Bahrmann P, Werner GS, Heusch G, Ferrari M, Poerner TC, Voss A, Figulla HR. Detection of coronary microembolization by Doppler ultrasound in patients with stable angina pectoris undergoing elective percutaneous coronary interventions. Circulation 2007;115:600-608. (Pubitemid 46226170)
101. Kleinbongard P, Bose D, Baars T, Mohlenkamp S, Konorza T, Schoner S, Elter-Schulz M, Eggebrecht H, Degen H, Haude M, Levkau B, Schulz R, Erbel R, Heusch G. Vasoconstrictor potential of coronary aspirate from patients undergoing stenting of saphenous vein aortocoronary bypass grafts and its pharmacological attenuation. Circ Res 2011;108:344-352.
102. Baim DS, Wahr D, George B, Leon MB, Greenberg J, Cutlip DE, Kaya U, Popma JJ, Ho KK, Kuntz RE. Randomized trial of a distal embolic protection device during percutaneous intervention of saphenous vein aorto-coronary bypass grafts. Circulation 2002;105:1285-1290. (Pubitemid 34260417)
103. Neglia D, Michelassi C, Trivieri MG, Sambuceti G, Giorgetti A, Pratali L, Gallopin M, Salvadori P, Sorace O, Carpeggiani C, Poddighe R, L'Abbate A, Parodi O. Prognostic role of myocardial blood flow impairment in idiopathic left ventricular dysfunction. Circulation 2002;105:186-193. (Pubitemid 34084317)
104. Rigo F, Gherardi S, Galderisi M, Sicari R, Picano E. The independent prognostic value of contractile and coronary flow reserve determined by dipyridamole stress echocardiography in patients with idiopathic dilated cardiomyopathy. Am J Cardiol 2007;99:1154-1158. (Pubitemid 46578201)
105. Anantharam B, Janardhanan R, Hayat S, Hickman M, Chahal N, Bassett P, Senior R. Coronary flow reserve assessed by myocardial contrast echocardiog-raphy predicts mortality in patients with heart failure. Eur J Echocardiogr 2011;12:69-75.
106. Cecchi F, Olivotto I, Gistri R, Lorenzoni R, Chiriatti G, Camici PG. Coronary microvascular dysfunction and prognosis in hypertrophic cardiomyopathy. N Engl J Med 2003;349:1027-1035. (Pubitemid 37087617)
107. Maron MS, Olivotto I, Maron BJ, Prasad SK, Cecchi F, Udelson JE, Camici PG. The case for myocardial ischemia in hypertrophic cardiomyopathy. J Am Coll Cardiol 2009;54:866-875.
108. Weis M, Hartmann A, Olbrich HG, Hor G, Zeiher AM. Prognostic significance of coronary flow reserve on left ventricular ejection fraction in cardiac transplant recipients. Transplantation 1998;65:103-108. (Pubitemid 28100440)
109. Hollenberg SM, Klein LW, Parrillo JE, Scherer M, Burns D, Tamburro P, Oberoi M, Johnson MR, Costanzo MR. Coronary endothelial dysfunction after heart transplantation predicts allograft vasculopathy and cardiac death. Circulation 2001;104:3091-3096. (Pubitemid 34014063)
110. Tona F, Caforio AL, Montisci R, Gambino A, Angelini A, Ruscazio M, Toscano G, Feltrin G, Ramondo A, Gerosa G, Iliceto S. Coronary flow velocity pattern and coronary flow reserve by contrast-enhanced transthoracic echocardiography predict long-term outcome in heart transplantation. Circulation 2006;114(1 Suppl):I49-I55. (Pubitemid 44297128)
111. Berry C, Balachandran KP, L'Allier PL, Lesperance J, Bonan R, Oldroyd KG. Importance of collateral circulation in coronary heart disease. Eur Heart J 2007;28:278-291.
112. Porto I, Hamilton-Craig C, Brancati M, Burzotta F, Galiuto L, Crea F. Angio-graphic assessment of microvascular perfusion-myocardial blush in clinical practice. Am Heart J 2010;160:1015-1022.