Coronary microvascular dysfunction in chronic inflammatory rheumatoid diseases

European Heart Journal

Volumn 37, Issue 23, 2016, Pages 1799-1806

  Faccini, Alessia ^a   Kaski, Juan Carlos ^b   Camici, Paolo G ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Coronary microvascular dysfunction; Inflammation; Microvascular angina; Rheumatic diseases; Rheumatoid arthritis; Systemic lupus erythematosus; Systemic sclerosis

Indexed keywords

ATORVASTATIN; C REACTIVE PROTEIN; CANAKINUMAB; CD28 ANTIGEN; DARAPLADIB; ENDOTHELIN 1; INCLACUMAB; INTERLEUKIN 1; INTERLEUKIN 6; METHOTREXATE; PADGEM PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UROKINASE RECEPTOR; CYTOKINE;

ANGINA PECTORIS; ANTIINFLAMMATORY ACTIVITY; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATORY RHEUMATOID DISEASE; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DISEASE; CORONARY MICROVASCULAR DYSFUNCTION; DISEASE ASSOCIATION; HUMAN; ISCHEMIC HEART DISEASE; META ANALYSIS (TOPIC); MONOCYTE; NATURAL KILLER CELL; NON ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN TARGETING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; SYSTEMATIC REVIEW (TOPIC); SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; T LYMPHOCYTE; THORAX PAIN; ANTAGONISTS AND INHIBITORS; CARDIOMYOPATHY; CHRONIC DISEASE; FEMALE; HEART MUSCLE ISCHEMIA; MALE; MICROCIRCULATION; MICROVASCULATURE; PHYSIOLOGY; RHEUMATIC HEART DISEASE; SYNDROME X;

ARTHRITIS, RHEUMATOID; CARDIOMYOPATHIES; CHRONIC DISEASE; CORONARY ARTERY DISEASE; CORONARY CIRCULATION; CYTOKINES; FEMALE; HUMANS; KILLER CELLS, NATURAL; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICROCIRCULATION; MICROVASCULAR ANGINA; MICROVESSELS; MONOCYTES; MYOCARDIAL ISCHEMIA; OXIDATIVE STRESS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RHEUMATIC HEART DISEASE; SCLERODERMA, SYSTEMIC; T-LYMPHOCYTES;

EID: 84976473187     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehw018     Document Type: Review

References (117)

1. Prasad M, Hermann J, Gabriel SE, Weyand CM, Mulvagh S, Mankad R, Oh JK, Matteson EL, Lerman A. Cardiorheumatology: cardiac involvement in systemic rheumatic disease. Nat Rev Cardiol 2015;12:168-176.
2. Dregan A, Charlton J, Chowienczyk P, Gulliford MC. Chronic inflammatory disorders and risk of type 2 diabetes mellitus, coronary heart disease, and stroke: a population-based cohort study. Circulation 2014;130:837-844.
3. Gargiulo P, Marsico F, Parente A, Paolillo S, Cecere M, Casaretti L, Pellegrino AM, Formisano T, Fabiani I, Soricelli A, Trimarco B, Perrone-Filardi P. Ischemic heart disease in systemic inflammatory diseases. An appraisal. Int J Cardiol 2014;170: 286-290.
4. Mason JC, Libby P. Cardiovascular disease in patients with chronic inflammation: mechanisms underlying premature cardiovascular events in rheumatologic conditions. Eur Heart J 2015;36:482-489.
5. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999;340: 115-126.
6. Liao KP, Solomon DH. Mechanistic insights into the link between inflammation and cardiovascular disease: rheumatoid arthritis as a human model of inflammation. Circ Cardiovasc Imaging 2014;7:575-577.
7. Leung DY, Leung M. Non-invasive/invasive imaging: significance and assessment of coronary microvascular dysfunction. Heart 2011;97:587-595.
8. Camici PG, D'Amati G, Rimoldi O. Coronary microvascular dysfunction: mechanisms and functional assessment. Nat Rev Cardiol 2015;12:48-62.
9. Pries AR, Habazettl H, Ambrosio G, Hansen PR, Kaski JC, Schächinger V, Tillmanns H, Vassalli G, Tritto I,Weis M, de Wit C, Bugiardini R. A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings. Cardiovasc Res 2008;80:165-174.
10. Kaufmann PA, Camici PG. Myocardial blood flow measurement by PET: technical aspects and clinical applications. J Nucl Med 2005;46:75-88.
11. Marcus ML, Wilson RF, White CW. Methods of measurement of myocardial blood flow in patients: a critical review. Circulation 1987;76:245-253.
12. Camici PG, Rimoldi OE. The clinical value of myocardial blood flow measurement. J Nucl Med 2009;50:1076-1087.
13. Taqueti VR, Everett BM, Murthy VL, Gaber M, Foster CR, Hainer J, Blankstein R, Dorbala S, Di Carli MF. Interaction of impaired coronary flow reserve and cardiomyocyte injury on adverse cardiovascular outcomes in patients without overt coronary artery disease. Circulation 2015;131:528-535.
14. Crea F, Camici PG, Bairey Merz CN. Coronary microvascular dysfunction: an update. Eur Heart J 2014;35:1101-1111.
15. 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.
16. 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.
17. Cohen DJ, Van Hout B, Serruys PW, Mohr FW, Macaya C, den Heijer P, Vrakking MM, Wang K, Mahoney EM, Audi S, Leadley K, Dawkins KD, Kappetein AP; Synergy between PCI with Taxus and Cardiac Surgery Investigators. Quality of life after PCI with drug-eluting stents or coronary-artery bypass surgery. N Engl J Med 2011;364:1016-1026.
18. 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.
19. Neill WA, Oxendine J, Phelps N, Anderson RP. Subendocardial ischemia provoked by tachycardia in conscious dogs with coronary stenosis. Am J Cardiol 1975;35:30-36.
20. Sossalla S,Wagner S, Rasenack EC, Ruff H,Weber SL, Schöndube FA, Tirilomis T, Tenderich G, Hasenfuss G, Belardinelli L, Maier LS. Ranolazine improves diastolic dysfunction in isolated myocardium from failing human hearts-role of late sodium current and intracellular ion accumulation. J Mol Cell Cardiol 2008;45:32-43.
21. Herrmann J, Kaski JC, Lerman A. Coronary microvascular dysfunction in the clinical setting: from mystery to reality. Eur Heart J 2012;33:2771-2782.
22. Agullò L, Garcia-Dorado D, Escalona N, Inserte J, Ruiz-Meana M, Barrabés JA, Mirabet M, Pina P, Soler-Soler J. Hypoxia and acidosis impair cGMP synthesis in microvascular coronary endothelial cells. Am J Physiol Heart Circ Physiol 2002; 283:H917-H925.
23. Britten MB, Zeiher AM, Schächinger V. Microvascular dysfunction in angiographically normal or mildly diseased coronary arteries predicts adverse cardiovascular long-term outcome. Coron Artery Dis 2004;15:259-264.
24. Camici PG, Crea F. Coronary microvascular dysfunction. N Engl J Med 2007;365: 830-840.
25. Gabriel SE. Cardiovascular morbidity and mortality in rheumatoid arthritis. Am J Med 2008;121(Suppl. 1):S9-S14.
26. Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, Stampfer MJ, Curhan GC. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 2003;107:1303-1307.
27. Avina-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Care Res 2008;59:1690-1697.
28. Yurkovich M, Vostretsova K, Chen W, Aviña-Zubieta JA. Overall and causespecific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res 2014;66:608-616.
29. Mankad R. Atherosclerotic vascular disease in the autoimmune rheumatologic patient. Curr Atheroscler Rep 2015;17:21.
30. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TAJ, Jansen-McWilliams L, D'Agostino RB, Kuller LH. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus comparison with the Framingham Study. Am J Epidemiol 1997;145:408-415.
31. Ungprasert P, Charoenpong P, Ratanasrimetha P, Thongprayoon C, Cheungpasitporn W, Suksaranjit P. Risk of coronary artery disease in patients with systemic sclerosis: a systematic review and meta-analysis. Clin Rheumatol 2014;33:1099-1104.
32. Nordin A, Jensen-Urstad K, Björnadal L, Pettersson S, Larsson A, Svenungsson E. Ischemic arterial events and atherosclerosis in patients with systemic sclerosis: a population-based case-control study. Arthritis Res Ther 2013;15:R87.
33. Sattar N, McCareyDW, Capell H, McInnes IB. Explaining how 'high-grade' systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 2003; 108:2597-2663.
34. Roldan PC, Ratliff M, Snider R, Macias L, Rodriguez R, SibbittW, Roldan CA. Aortic atherosclerosis in systemic lupus erythematosus. Rheumatology (Sunnyvale) 2014;(Suppl. 5):S5-006.
35. Ciftci O, Yilmaz S, Topcu S, Caliskan M, Gullu H, Erdogan D, Pamuk BO, Yildirir A, Muderrisoglu H. Impaired coronary microvascular function and increased intimamedia thickness in rheumatoid arthritis. Atherosclerosis 2008;198:332-337.
36. Hirata K, Kadirvelu A, Kinjo M, Sciacca R, Sugioka K, Otsuka R, Choy A, Chow SK, Yoshiyama M, Yoshikawa J, Homma S, Lang CC. Altered coronary vasomotor function in young patients with systemic lupus erythematosus. Arthritis Rheum 2007;56:1904-1909.
37. Recio-Mayoral A, Mason JC, Kaski JC, Rubens MB, Harari OA, Camici PG. Chronic inflammation and coronary microvascular dysfunction in patients without risk factors for coronary artery disease. Eur Heart J 2009;30:1837-1843.
38. Faccini A, Agricola E, Oppizzi M, Margonato A, Galderisi M, Sabbadini MG, Franchini S, Camici PG. Coronary microvascular dysfunction in asymptomatic patients affected by systemic sclerosis-limited vs. diffuse form. Circ J 2015;79: 825-829.
39. Sandoo A, Veldhuijzen van Zanten JJ, Metsios GS, Carroll D, Kitas GD. Vascular function and morphology in rheumatoid arthritis: a systematic review. Rheumatology 2011;50:2125-2139.
40. Bonetti PO. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2002;23:168-175.
41. Steyers CM, Miller FJJ. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci 2014;15:11324-11349.
42. Zhang J, Chen L, Delzell E, Muntner P, Hillegass WB, Safford MM, Millan IY, Crowson CS, Curtis JR. The association between inflammatory markers, serum lipids and the risk of cardiovascular events in patients with rheumatoid arthritis. Ann Rheum Dis 2014;73:1301.
43. Cannarile F, Valentini V, Mirabelli G, Alunno A, Terenzi R, Luccioli F, Gerli R, Bartoloni E. Cardiovascular disease in systemic sclerosis. Ann Transl Med 2015; 3:8.
44. Montecucco F, Mach F. Common inflammatory mediators orchestrate pathophysiological processes in rheumatoid arthritis and atherosclerosis. Rheumatology (Oxford) 2009;48:11-22.
45. Vaccarino V, Khan D, Votaw J, Faber T, Veledar E, Jones DP, Goldberg J, Raggi P, Quyyumi AA, Bremner JD. Inflammation is related to coronary flow reserve detected by positron emission tomography in asymptomatic male twins. J Am Coll Cardiol 2011;57:1271-1279.
46. Korbecki J, Baranowska-Bosiacka I, Gutowska I, Chlubek D. The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. J Physiol Pharmacol 2013;64:409-421.
47. Y?lmaz S, Caliskan M, Kulaks?zoglu S, Ciftci O, Caliskan Z, Gullu H, Guven A, Muderrisoglu H. Association between serum total antioxidant status and coronary microvascular functions in patients with SLE. Echocardiography 2012;29: 1218-1223.
48. Zhang S, Zhao Y, Xu M, Yu L, Zhao Y, Chen J, Yuan Y, Zheng Q, Niu X. FoxO3a modulates hypoxia stress induced oxidative stress and apoptosis in cardiac microvascular endothelial cells. PLoS One 2013;8:e80342.
49. Leonard S, Croy BA, Murrant CL. Arteriolar reactivity in lymphocyte-deficient mice. Am J Physiol Heart Circ Physiol 2011;301:H1276-H1285.
50. Jurewicz M, McDermott DH, Sechler JM, Tinckam K, Takakura A, Carpenter CB, Milford E, Abdi R. Human T and natural killer cells possess a functional renin-angiotensin system: further mechanisms of angiotensin II-induced inflammation. J Am Soc Nephrol 2007;18:1093-1102.
51. Dumitriu IE. The life (and death) of CD4+/CD28null T cells in inflammatory diseases. Immunology 2015;146:185-193.
52. Weyand CM, Brandes JC, Schmidt D, Fulbright JW, Goronzy JJ. Functional properties of CD4+ CD28-T cells in the aging immune system. Mech Ageing Dev 1998; 102:131-147.
53. Kovalcsik E, Antunes RF, Baruah P, Kaski JC, Dumitriu IE. Proteasome-mediated reduction in proapoptotic molecule Bim renders CD4(+)CD28null T cells resistant to apoptosis in acute coronary syndrome. Circulation 2015;131:709-720.
54. Namekawa T,Wagner UG, Goronzy JJ,Weyand CM. Functional subsets of CD4T cells in rheumatoid synovitis. Arthritis Rheum 1998;41:2108-2116.
55. Dumitriu IE, Araguás ET, Baboonian C, Kaski JC. CD4+ CD28 null T cells in coronary artery disease: when helpers become killers. Cardiovasc Res 2009;81:11-19.
56. Fasth AE, Snir O, Johansson AA, Nordmark B, Rahbar A, Af Klint E, Bjö rkström NK, Ulfgren AK, van Vollenhoven RF, Malmström V, Trollmo C. Skewed distribution of proinflammatory CD4+CD28null T cells in rheumatoid arthritis. Arthritis Res Ther 2007;9:R87.
57. Pipp F, Heil M, Issbrucker K, Ziegelhoeffer T, Martin S, van den Heuvel J,Weich H, Fernandez B, Golomb G, Carmeliet P, Schaper W, Clauss M. VEGFR-1-selective VEGF homologue PlGF is arteriogenic: evidence for a monocyte-mediated mechanism. Circ Res 2003;92:378-385.
58. Tchaikovski V, Olieslagers S, Böhmer FD,Waltenberger J. Diabetes mellitus activates signal transduction pathways resulting in vascular endothelial growth factor resistance of human monocytes. Circulation 2009;120:150-159.
59. Waltenberger J, Lange J, Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: a potential predictor for the individual capacity to develop collaterals. Circulation 2000; 102:185-190.
60. Czepluch FS, Bergler A, Waltenberger J. Hypercholesterolaemia impairs monocyte function in CAD patients. J Intern Med 2007;261:201-204.
61. Stadler N, Eggermann J, Vöö S, Kranz A,Waltenberger J. Smoking-induced monocyte dysfunction is reversed by vitamin C supplementation in vivo. Arterioscler Thromb Vasc Biol 2007;27:120-126.
62. Ruscitti P, Cipriani P, Di Benedetto P, Liakouli V, Berardicurti O, Carubbi F, Ciccia F, Alvaro S, Triolo G, Giacomelli R. Monocytes from patients with rheumatoid arthritis and type 2 diabetes mellitus display an increased production of interleukin (IL)-1b via the nucleotide-binding domain and leucine-rich repeat containing family pyrin 3(NLRP3)-inflammasome activation: a possible implication for therapeutic decision in these patients. Clin Exp Immunol 2015;182:35-44.
63. Winchester R, Giles JT, Nativ S, Downer K, Zhang HZ, Bag-Ozbek A, Zartoshti A, Bokhari S, Bathon JM. Association of elevations of specific T cell and monocyte subpopulations in rheumatoid arthritis with subclinical coronary artery atherosclerosis. Arthritis Rheumatol 2016;68:92-102.
64. Miko?ajczyk TP, Osmenda G, Batko B, Wilk G, Krezelok M, Skiba D, Sliwa T, Pryjma JR, Guzik TJ. Heterogeneity of peripheral blood monocytes, endothelial dysfunction and subclinical atherosclerosis in patients with systemic lupus erythematosus. Lupus 2016;25:18-27.
65. Mekonnen G, Corban MT, Hung OY, Eshtehardi P, Eapen DJ, Al-Kassem H, Rasoul-Arzrumly E, Gogas BD, McDaniel MC, Pielak T, Thorball CW, Sperling L, Quyyumi AA, Samady H. Plasma soluble urokinase-type plasminogen activator receptor level is independently associated with coronary microvascular function in patients with non-obstructive coronary artery disease. Atherosclerosis 2015;239:55-60.
66. Toldi G, Szalay B, Beko G, Bocskai M, Deák M, Kovács L, Vásárhelyi B, Balog A. Plasma soluble urokinase plasminogen activator receptor (suPAR) levels in systemic lupus erythematosus. Biomarkers 2012;17:758-763.
67. Thunø M, Macho B, Eugen-Olsen J. suPAR: the molecular crystal ball. Dis Markers 2009;27:157-172.
68. Backes Y, van der Sluijs KF, Mackie DP, Tacke F, Koch A, Tenhunen JJ, Schultz MJ. Usefulness of suPAR as a biological marker in patients with systemic inflammation or infection: a systematic review. Intensive Care Med 2012;38:1418-1428.
69. Gkaliagkousi E, Gavriilaki E, Doumas M, Petidis K, Aslanidis S, Stella D. Cardiovascular risk in rheumatoid arthritis: pathogenesis, diagnosis, and management. J Clin Rheumatol 2012;18:422-430.
70. Arosio E, De Marchi S, Rigoni A, Prior M, Delva P, Lechi A. Forearm haemodynamics, arterial stiffness and microcirculatory reactivity in rheumatoid arthritis. J Hypertens 2007;25:1273-1278.
71. Sandoo A, Carroll D, Metsios GS, Kitas GD, Veldhuijzen van Zanten JJ. The association between microvascular and macrovascular endothelial function in patients with rheumatoid arthritis: a cross-sectional study. Arthritis Res Ther 2011;13:R99.
72. Datta D, Ferrell WR, Sturrock RD, Jadhav ST, Sattar N. Inflammatory suppression rapidly attenuates microvascular dysfunction in rheumatoid arthritis. Atherosclerosis 2007;192:391-395.
73. Turiel M, Atzeni F, Tomasoni L, de Portu S, Delfino L, Bodini BD, Longhi M, Sitia S, Bianchi M, Ferrario P, Doria A, De Gennaro Colonna V, Sarzi-Puttini P. Noninvasive assessment of coronary flow reserve and ADMA levels: a case-control study of early rheumatoid arthritis patients. Rheumatology (Oxford) 2009;48: 834-839.
74. D'Cruz DP, Khamashta MA, Hughes GR. Systemic lupus erythematosus. Lancet 2007;369:587-596.
75. Laganà B, Schillaci O, Tubani L, Gentile R, Danieli R, Coviello R, Baratta L, Scopinaro F. Lupus carditis: evaluation with technetium-99 m MIBI myocardial SPECT and heart rate variability. Angiology 1999;50:143-148.
76. Ishimori ML, Martin R, Berman DS, Goykhman P, Shaw LJ, Shufelt C, Slomka PJ, Thomson LE, Schapira J, Yang Y,Wallace DJ,Weisman MH, Bairey Merz CN. Myocardial ischemia in the absence of obstructive coronary artery disease in systemic lupus erythematosus. JACC Cardiovasc Imaging 2011;4:27-33.
77. Lima DS, Sato EI, Lima VC, Miranda FJ, Hatta FH. Brachial endothelial function is impaired in patients with systemic lupus erythematosus. J Rheumatol 2002;29: 292-297.
78. Wigley FM. Vascular disease in scleroderma. Clin Rev Allerg Immunol 2009;36: 150-175.
79. Kahan A, Nitenberg A, Foult JM, Amor B, Menkes CJ, Devaux JY, Blanchet F, Perennec J, Lutfalla G, Roucayrol JC. Decreased coronary reserve in primary scleroderma myocardial disease. Arthritis Rheum 1985;28:637-646.
80. Montisci R, Vacca A, Garau P, Colonna P, Ruscazio M, Passiu G, Iliceto S, Mathieu A. Detection of early impairment of coronary flow reserve in patients with systemic sclerosis. Ann Rheum Dis 2003;62:890-893.
81. Turiel M, Gianturco L, Ricci C, Sarzi-Puttini P, Tomasoni L, Colonna VG, Ferrario P, Epis O, Atzeni F. Silent cardiovascular involvement in patients with diffuse systemic sclerosis: a controlled cross-sectional study. Arthritis Care Res 2013; 65:274-280.
82. Vacca A, Montisci R, Garau P, Siotto P, Piga M, Cauli A, Ruscazio M, Meloni L, Iliceto S, Mathieu A. Prognostic impact of coronary microcirculation abnormalities in systemic sclerosis: a prospective study to evaluate the role of noninvasive tests. Arthritis Res Ther 2013;15:R8.
83. Kaski JC. Pathophysiology and management of patients with chest pain and normal coronary arteriograms (cardiac syndrome X). Circulation 2004;109:268-272.
84. Crea F, Lanza GA. Angina pectoris and normal coronary arteries: cardiac syndrome X. Heart 2004;90:457-463.
85. Recio-Mayoral A, Rimoldi OE, Camici PG, Kaski JC. Inflammation and microvascular dysfunction in cardiac syndrome X patients without conventional risk factors for coronary artery disease. JACC Cardiovasc Imaging 2013;6:660-667.
86. Pasqui AL, Puccetti L, Di Renzo M, Bruni F, Camarri A, Palazzuoli A, Biagi F, Servi M, Bischeri D, Auteri A, Pastorelli M. Structural and functional abnormality of systemic microvessels in cardiac syndrome X. Nutr Metab Cardiovasc Dis 2005; 15:56-64.
87. Tondi P, Santoliquido A, Di Giorgio A, Sestito A, Sgueglia GA, Flore R, Careri G, Pinnacchio G, Lanza GA, Crea F. Endothelial dysfunction as assessed by flowmediated dilation in patients with cardiac syndrome X: role of inflammation. Eur Rev Med Pharmacol Sci 2011;15:1074-1077.
88. Ridker PM, Lüscher TF. Anti-inflammatory therapies for cardiovascular disease. Eur Heart J 2014;35:1782-1791.
89. Ridker PM, Howard CP,Walter V, Everett B, Libby P, Hensen J, Thuren T; CANTOS Pilot Investigative Group. Effects of interleukin-1b inhibition with canakinumab on hemoglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: a phase IIb randomized, placebo-controlled trial. Circulation 2012;126:2739-2748.
90. Ridker PM. Closing the loop on inflammation and atherothrombosis: why perform the CIRT and CANTOS trials? Trans Am Clin Climatol Assoc 2013;124:174-190.
91. Ridker PM. Testing the inflammatory hypothesis of atherothrombosis: scientific rationale for the cardiovascular inflammation reduction trial (CIRT). J Thromb Haemost 2009;7(Suppl. 1):332-339.
92. Roubille C, Richer V, Starnino T, McCourt C, McFarlane A, Fleming P, Siu S, Kraft J, Lynde C, Pope J, Gulliver W, Keeling S, Dutz J, Bessette L, Bissonnette R, Haraoui B. The effects of tumour necrosis factor inhibitors, methotrexate, nonsteroidal anti-inflammatory drugs and corticosteroids on cardiovascular events in rheumatoid arthritis, psoriasis and psoriatic arthritis: a systematic review and meta-analysis. Ann Rheum Dis 2015;74:480-489.
93. Micha R, Imamura F, Wyler von Ballmoos M, Solomon DH, Hernán MA, Ridker PM, Mozaffarian D. Systematic review and meta-analysis of methotrexate use and risk of cardiovascular disease. Am J Cardiol 2011;108:1362-1370.
94. Protogerou AD, Zampeli E, Fragiadaki K, Stamatelopoulos K, Papamichael C, Sfikakis PP. A pilot study of endothelial dysfunction and aortic stiffness after interleukin-6 receptor inhibition in rheumatoid arthritis. Atherosclerosis 2011; 219:734-736.
95. Serruys PW, Garcia-Garcia HM, Buszman P, Erne P, Verheye S, Aschermann M, Duckers H, Bleie O, Dudek D, Botker HE, von Birgelen C, D'Amico D, Hutchinson T, Zambanini A, Mastik F, van Es GA, van der Steen AF, Vince DG, Ganz P, Hamm CW, Wijns W, Zalewski A. Effects of the direct lipoprotein-associated phospholipase A(2) inhibitor darapladib on human coronary atherosclerotic plaque. Circulation 2008;118:1172-1182.
96. Nicholls SJ, Kastelein JJ, Schwartz GG, Bash D, Rosenson RS, Cavender MA, Brennan DM, Koenig W, Jukema JW, Nambi V, Wright RS, Menon V, Lincoff AM, Nissen SE. Varespladib and cardiovascular events in patients with an acute coronary syndrome: the VISTA-16 randomized clinical trial. JAMA 2014;311:252-262.
97. STABILITY Investigators, White HD, Held C, Stewart R, Tarka E, Brown R, Davies RY, Budaj A, Harrington RA, Steg PG, Ardissino D, Armstrong PW, Avezum A, Aylward PE, Bryce A, Chen H, Chen MF, Corbalan R, Dalby AJ, Danchin N, De Winter RJ, Denchev S, Diaz R, Elisaf M, Flather MD, Goudev AR, Granger CB, Grinfeld L, Hochman JS, Husted S, Kim HS, Koenig W, Linhart A, Lonn E, López-Sendón J, Manolis AJ, Mohler ER III, Nicolau JC, Pais P, Parkhomenko A, Pedersen TR, Pella D, Ramos-Corrales MA, Ruda M, Sereg M, Siddique S, Sinnaeve P, Smith P, Sritara P, Swart HP, Sy RG, Teramoto T, Tse HF, Watson D, Weaver WD, Weiss R, Viigimaa M, Vinereanu D, Zhu J, Cannon CP, Wallentin L. Darapladib for preventing ischemic events in stable coronary heart disease. N Engl J Med 2014;370:1702-1711.
98. O'Donoghue ML, Braunwald E, White HD, Lukas MA, Tarka E, Steg PG, Hochman JS, Bode C, Maggioni AP, Im K, Shannon JB, Davies RY, Murphy SA, Crugnale SE, Wiviott SD, Bonaca MP, Watson DF, Weaver WD, Serruys PW, Cannon CP; SOLID-TIMI 52 Investigators, Steen DL. Effect of darapladib on major coronary events after an acute coronary syndrome: the SOLID-TIMI 52 randomized clinical trial. JAMA 2014;312:1006-1015.
99. Tremoulet AH. The role of statins in inflammatory vasculitides. Autoimmunity 2015;48:177-180.
100. Heart Protection Study Collaborative Group, Bulbulia R, Bowman L,Wallendszus K, Parish S, Armitage J, Peto R, Collins R. Effects on 11-year mortality and morbidity of lowering LDL cholesterol with simvastatin for about 5 years in 20,536 high-risk individuals: a randomised controlled trial. Lancet 2011;378:2013-2020.
101. Ridker PM, Danielson E, Fonseca FA, Genest J, Gotto AM Jr, Kastelein JJ, Koenig W, Libby P, Lorenzatti AJ, MacFadyen JG, Nordestgaard BG, Shepherd J, Willerson JT, Glynn RJ; JUPITER Study Group. Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med 2008;359: 2195-2207.
102. Ridker PM, Rifai N, Pfeffer MA, Sacks FM, Moye LA, Goldman S, Flaker GC, Braunwald E. Inflammation, pravastatin, and the risk of coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events (CARE) Investigators. Circulation 1998;98:839-844.
103. McCarey DW, McInnes IB, Madhok R, Hampson R, Scherbakov O, Ford I, Capell HA, Sattar N. Trial of Atorvastatin in Rheumatoid Arthritis (TARA): double-blind, randomised placebo-controlled trial. Lancet 2004;363:2015-2021.
104. Lv S, Liu Y, Zou Z, Li F, Zhao S, Shi R, Bian R, Tian H. The impact of statins therapy on disease activity and inflammatory factor in patients with rheumatoid arthritis: a meta-analysis. Clin Exp Rheumatol 2014;33:69-76.
105. Danninger K, Hoppe UC, Pieringer H. Do statins reduce the cardiovascular risk in patients with rheumatoid arthritis? Int J Rheum Dis 2014;17:606-611.
106. Ardoin SP, Schanberg LE, Sandborg CI, Barnhart HX, Evans GW, Yow E, Mieszkalski KL, Ilowite NT, Eberhard A, Imundo LF, Kimura Y, Levy D, von Scheven E, Silverman E, Bowyer SL, Punaro L, Singer NG, Sherry DD, McCurdy DK, Klein-Gitelman M, Wallace C, Silver RM, Wagner-Weiner L, Higgins GC, Brunner HI, Jung L, Soep JB, Reed AM, Thompson SD; APPLE investigators. Secondary analysis of APPLE study suggests atorvastatin may reduce atherosclerosis progression in pubertal lupus patients with higher C reactive protein. Ann Rheum Dis 2014;73:557-566.
107. Erkan D, Willis R, Murthy VL, Basra G, Vega J, Ruiz-Limó n P, Carrera AL, Papalardo E, Martínez-Martínez LA, González EB, Pierangeli SS. A prospective open-label pilot study of fluvastatin on proinflammatory and prothrombotic biomarkers in antiphospholipid antibody positive patients. Ann Rheum Dis 2014;73: 1176-1180.
108. Timár O, Szekanecz Z, Kerekes G, Végh J, Oláh AV, Nagy G, Csiki Z, Dankó K, Szamosi S, NémethÁ , Soltész P, Szücs G. Rosuvastatin improves impaired endothelial function, lowers high sensitivity CRP, complement and immuncomplex production in patients with systemic sclerosis-a prospective case-series study. Arthritis Res Ther 2013;15:R105.
109. Sadik HY, Moore TL, Vail A, Murray A, Anderson M, Blann A, Herrick AL. Lack of effect of 8 weeks atorvastatin on microvascular endothelial function in patients with systemic sclerosis. Rheumatology (Oxford) 2010;49:990-996.
110. Kayikcioglu M, Payzin S, Yavuzgil O, Kultursay H, Can LH, Soydan I. Benefits of statin treatment in cardiac syndrome-X1. Eur Heart J 2003;24:1999-2005.
111. Tardif JC, Tanguay JF, Wright SS, Duchatelle V, Petroni T, Grégoire JC, Ibrahim R, Heinonen TM, Robb S, Bertrand OF, Cournoyer D, Johnson D, Mann J, Guertin MC, L'Allier PL. Effects of the P-selectin antagonist inclacumab on myocardial damage after percutaneous coronary intervention for non-ST-segment elevation myocardial infarction: results of the SELECT-ACS trial. J Am Coll Cardiol 2013;61:2048-2055.
112. Chen G. Immunotherapy of rheumatoid arthritis targeting inflammatory cytokines and autoreactive T cells. Arch Immunol Ther Exp (Warsz) 2010;58:27-36.
113. Alunno A, Manetti M, Caterbi S, Ibba-Manneschi L, Bistoni O, Bartoloni E, Valentini V, Terenzi R, Gerli R. Altered immunoregulation in rheumatoid arthritis: the role of regulatory T cells and proinflammatory Th17 cells and therapeutic implications. Mediators Inflamm 2015;2015:751793.
114. Ong P, Athanasiadis A, Borgulya G, Vokshi I, Bastiaenen R, Kubik S, Hill S, Schäufele T, Mahrholdt H, Kaski JC, Sechtem U. Response to letters regarding article, 'Clinical usefulness, angiographic characteristics, and safety evaluation of intracoronary acetylcholine provocation testing among 921 consecutive white patients with unobstructed coronary arteries'. Circulation 2015;131:e325.
115. Hozumi T, Yoshida K, Akasaka T, Asami Y, Ogata Y, Takagi T, Kaji S, Kawamoto T, Ueda Y, Morioka S. Noninvasive assessment of coronary flow velocity and coronary flow velocity reserve in the left anterior descending coronary artery by Doppler echocardiography: comparison with invasive technique. J Am Coll Cardiol 1998;32:1251-1259.
116. Lethen H, P Tries H, Kersting S, Lambertz H. Validation of noninvasive assessment of coronary flow velocity reserve in the right coronary artery. A comparison of transthoracic echocardiographic results with intracoronary Doppler flow wire measurements. Eur Heart J 2003;24:1567-1575.
117. Lethen H, Tries HP, Brechtken J, Kersting S, Lambertz H. Comparison of transthoracic Doppler echocardiography to intracoronary Doppler guidewire measurements for assessment of coronary flow reserve in the left anterior descending artery for detection of restenosis after coronary angioplasty. Am J Cardiol 2003;91:412-417.