(Circulation. 1996;94:874-877.)
© 1996 American Heart Association, Inc.
Articles |
Elevated Levels of Interleukin-6 in Unstable Angina
the Institute of Cardiology, Catholic University of the Sacred Heart, Rome, Italy, and Istituto di Richerche di Biologia Molecolare "P Angeletti" (A.V., S.A., G. Ciliberto), Pomezia, Italy.
Correspondence to Luigi M. Biasucci, Istituto di Cardiologia, Universita' Cattolica, Largo Francesco Vito 1, 00168 Roma, Italy.
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Abstract |
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Background Elevated plasma levels of C-reactive protein have been found in the majority of patients with unstable angina. The evidence of elevated levels of acute-phase proteins in unstable angina is in line with a growing body of evidence that suggests that inflammation plays a role in this syndrome and is an indirect sign of increased production of interleukin-6, which is the major determinant of acute-phase–protein production by the liver. However, in unstable angina, there is no direct proof of the role played by interleukin-6.
Methods and Results We measured levels of interleukin-6 in 38 patients with unstable angina at the time of their admission to the coronary care unit and in 29 patients with stable angina. In the same groups of patients, we also measured C-reactive protein. Interleukin-6 (undetectable, ie, <3 pg/mL, in healthy volunteers) was detectable in 23 (61%) of 38 patients with unstable angina but in only 6 (21%) of 29 with stable angina (P<.01). Median interleukin-6 levels were 5.25 pg/mL (range, 0 to 90 pg/mL) in patients with unstable angina but were below the detection limit of the assay in patients with stable angina (range, 0 to 7 pg/mL). A significant correlation was observed between interleukin-6 and C-reactive protein levels (r=.4, P=.013).
Conclusions Our study demonstrates that raised levels of interleukin-6 are common in unstable angina, correlate with C-reactive protein, and are associated with prognosis, thus confirming the importance of the cytokine pathway for the production by the liver of acute-phase proteins and strengthening the importance of inflammation in this syndrome. Further studies are required to elucidate better the role of interleukins in unstable angina.
Key Words: interleukins • angina • proteins • prognosis • pathophysiology
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Introduction |
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Elevated plasma levels of C-reactive protein, a pro-totypical acute-phase reactant, have been found in the majority of patients with unstable angina1 2 3 ; we have also observed that raised levels of acute-phase proteins are strongly associated with an unfavorable outcome.3 The evidence of elevated levels of acute-phase proteins in unstable angina is in line with a growing body of evidence suggesting that inflammation plays a pivotal role in acute coronary syndromes4 5 6 7 8 and is an indirect sign of the increased production of interleukins from monocytes, macrophages, and endothelial cells. IL-6 and, to a lesser extent, IL-1, are in fact the major determinants for the liver production of acute-phase proteins via direct stimulation of the hepatocytes.9 10 11 IL-6 is also involved in a number of other processes, because it has proinflammatory9 10 and procoagulant12 properties that may have a role in the pathophysiology of acute coronary syndromes. An alternative pathway for production of acute-phase proteins by the liver implies the generation of oxidized LDL, which may also be involved in the pathogenesis of acute coronary syndromes.13 It is also possible that the hepatic environment itself can modulate the anabolic response of the liver to this cytokine.9 The present study was undertaken to assess levels of IL-6 in unstable angina and to assess its relation to CRP and prognosis to achieve direct proof of the role that cytokines play in the pathogenesis of unstable angina. We reasoned that if IL-6 is involved directly in the mechanisms that lead to instability, it should be elevated in unstable angina and should be related to levels of CRP and therefore to prognosis.
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Methods |
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Patient Population
Between March 1994 and March 1995, we studied 38 patients (31 men, 7 women) aged 61±9 years (range, 45 to 74 years) from a total of 162 patients admitted to our CCU with a diagnosis of unstable angina. The inclusion criteria were angina at rest with at least two ischemic episodes or one episode lasting >20 minutes during the preceding 24 hours, with diagnostic ST-segment shift and no evidence of myocardial infarction detected with the use of enzymatic techniques. The exclusion criteria were dilated cardiomyopathy, valvular heart disease, myocardial infarction within the previous 4 weeks, atrial fibrillation, the presence of any ECG abnormality invalidating ST-segment analysis, and major surgery or trauma within the previous month. All patients with known or suspected thrombotic disorders (other than unstable angina), malignancy, or inflammatory diseases were also excluded. All patients were treated with various combinations of aspirin, intravenous nitrates, intravenous heparin, calcium antagonists, and/or ß-blockers (Table
). All admission samples were taken under aspirin cover. The mean time from the last ischemic episode to blood sampling was 12±8 hours. In 7 patients, additional samples were taken at 6, 24, 48, and 72 hours after admission for a serial evaluation of levels of IL-6 and CRP. We also studied 29 patients (24 men; mean age, 58±9 years old) with chronic stable effort angina of at least 6 months' duration and evidence of coronary artery disease at coronary angiography. The study was approved by the Ethics Committee of the Catholic University, and all patients gave their written informed consent.
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Design of the Study
Blood samples were taken as soon as possible after patients with unstable angina had been admitted to our CCU to assess serum levels of IL-6, CRP, and troponin T, which we measured to rule out the possible role of myocardial cell damage in inducing the inflammatory response. Patients were monitored continuously in the CCU, and all patients underwent coronary angiography. All patients with stable angina had a positive exercise stress test under therapy cover (see Table), and all underwent coronary angiography. We also evaluated the in-hospital outcome of the patients with unstable angina and considered the following events as a complicated in-hospital course: death, acute myocardial infarction, and refractory angina (ie, angina refractory to full medical therapy, including intravenous heparin) requiring urgent revascularization.
Laboratory Assays
IL-6 was measured by a commercially available assay (Quantikine human IL-6, R&D Systems). IL-6 measurements were performed in duplicate, and the interassay variability was <10%. The IL-6 ELISA gave a linear response in a range from 3 (low concentration) to 300 (high concentration) pg/mL.
CRP was assayed in an automated monoclonal antibody solid-phase sandwich enzyme immunoassay (Abbott Laboratories). Troponin T was measured by use of a commercially available enzyme immunoassay (Boehringer Mannheim).
Statistical Analysis
Because data were not distributed normally, nonparametric tests were used. Results are expressed as median and range. The Mann-Whitney U test was used to evaluate differences among groups. The Friedmann test was used to evaluate differences within the same group. Spearman's rank test was used for correlations, and discontinuous variables were tested by contingency 
2 test. A probability value of P<.05 was assumed to be significant.
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Results |
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IL-6 levels, which were undetectable (ie, <3 pg/mL) in healthy volunteers in our laboratory, were detectable in 23 (61%) of 38 patients with unstable angina but in only 6 (21%) of 29 patients with stable angina (P<.01). Median levels of IL-6 were 5.25 pg/mL (range, 0 to 90 pg/dL) in patients with unstable angina and were below the detection limit (range, 0 to 7 pg/dL) in patients with stable angina (Fig 1
; P<.005). No differences in the demographic and angiographic characteristics of stable and unstable angina patients were observed (Table
). In patients with unstable angina, levels of CRP were elevated (ie, >3 mg/L) in 28 of 38 patients (and in 20 of 23 patients with detectable levels of IL-6), and a significant correlation was found between levels of IL-6 and CRP (r=.4, P=.013; Fig 2). The median level of CRP was 6.4 µg/L (range, 0.7 to 99 mg/L). Troponin T measured <0.1 mg/dL in all samples tested. We also evaluated the outcome of patients with unstable angina according to the entry levels of IL-6. Nineteen (83%) of 23 patients with detectable levels of IL-6 at entry had a complicated in-hospital course; myocardial infarction occurred in 3 patients (1 of whom died), and 16 patients had angina refractory to full medical therapy, requiring PTCA in 7 and CABG surgery in 9. Conversely, only 6 (40%) of 15 patients with undetectable levels of IL-6 had refractory angina; of these 6 patients, 3 required PTCA and the other 3 required CABG. No myocardial infarctions or deaths were observed in this group.
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In the seven patients from whom we took serial samples of IL-6 and CRP, no differences were observed over time (P=.8), with IL-6 levels remaining within a narrow range, from undetectable to 10.4 pg/mL.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Our study demonstrates that elevated levels of IL-6 (1) are common in unstable angina, (2) are associated with prognosis, and (3) correlate with levels of CRP. Thus, our study suggests the importance of IL-6 in the pathophysiology of unstable angina and confirms the hypothetical assumption that in this syndrome, elevated levels of acute-phase proteins come from the cytokine-inflammatory pathway.10 11 The finding that IL-6 is detectable in 61% of patients with unstable angina (and, more specifically, in 83% of those having a complicated in-hospital course) in the absence of any rise in levels of creatine kinase and troponin T and is detectable in only 21% of patients with stable angina clearly supports our assumption that detectable levels of IL-6 are a typical feature of unstable angina and that they are not secondary to myocardial cell damage. Sturk et al14 and Neumann et al15 have described raised levels of IL-6 in acute myocardial infarction after necrosis or reperfusion. However, Neumann et al15 reported elevated levels of IL-6 on admission, before reperfusion by PTCA and before the appearance of detectable signs of necrosis, suggesting a possible primary role of IL-6 in the pathogenesis of the event. A very strict correlation between IL-6 and CRP has been reported by Sturk et al,14 and we have also observed a significant, although weak, correlation between IL-6 and CRP, with the majority (87%) of patients with detectable levels of IL-6 also having elevated levels of CRP. Although these studies confirm the occurrence of a cytokine response in acute coronary syndromes, they can be compared only partially with our work because the pathological events in acute myocardial infarction, including myocardial cell necrosis and reperfusion after prolonged coronary artery occlusion, are clearly different from those in unstable angina. In the present study, the dissociation between levels of IL-6 and CRP observed in some patients likely occurred because of the differences in their half-lives (4 hours for IL-616 and 19 hours for CRP17 ) and because of the time lag (
6 hours) in the hepatic synthesis of acute-phase proteins, although in these cases, roles for the hepatic environment9 and the stimulation of liver cells from oxidized LDL18 cannot be excluded.
IL-6 is induced by a variety of stimuli, including interferon-
,19 tumor necrosis factor,19 20 IL-1,20 platelet-derived growth factor,21 viruses,22 and bacterial endotoxin.23 In turn, IL-6 has proinflammatory properties, with stimulatory effects on T and B lymphocytes,10 and it induces the synthesis of acute-phase proteins such as CRP and fibrinogen.9 Intriguingly, procoagulant properties for IL-6 have also been demonstrated.12 Apart from the importance of the activation of the coagulation system,24 lymphocyte activation5 and raised levels of acute-phase proteins3 have also been proposed as important factors in the pathogenesis of unstable angina.
Conclusions
Our study demonstrates that raised levels of IL-6 are common in unstable angina and are associated with prognosis, thus confirming the importance of the cytokine pathway for the production by the liver of acute-phase proteins and strengthening previous observations on the importance of inflammation in this syndrome.3 4 5 6 7 8 However, it cannot answer questions such as the following: Is IL-6 the only determinant of plasma levels of CRP? Is the inflammatory response observed in unstable angina a primary component of the disease? What is the cause of raised levels of IL-6, and is it localized in the coronary tree or is it systemic? Further studies are required to elucidate better the role of interleukins in unstable angina.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This study was supported in part by the National Research Council, targeted project "Prevention and Control Disease Factors," Rome, Italy (research grant 94,00518,PF41), and in part by the European Community (Biomed 2 research grant PL951505). We are indebted to Prof Mark B. Pepys and to Ruth Gallimore for the CRP measurements, to the nurses of the CCU at Policlinico Gemelli for their assistance, and to Vanessa Perrin for her assistance in the preparation of the manuscript.
Received May 28, 1996; revision received June 26, 1996; accepted July 2, 1996.
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I. Ikonomidis, G. Athanassopoulos, J. Lekakis, K. Venetsanou, M. Marinou, K. Stamatelopoulos, D. V. Cokkinos, and P. Nihoyannopoulos Myocardial Ischemia Induces Interleukin-6 and Tissue Factor Production in Patients With Coronary Artery Disease: A Dobutamine Stress Echocardiography Study Circulation, November 22, 2005; 112(21): 3272 - 3279. [Abstract] [Full Text] [PDF]
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C. Antoniades, D. Tousoulis, C. Vasiliadou, C. Pitsavos, C. Chrysochoou, D. Panagiotakos, C. Tentolouris, K. Marinou, N. Koumallos, and C. Stefanadis Genetic Polymorphism on Endothelial Nitric Oxide Synthase Affects Endothelial Activation and Inflammatory Response During the Acute Phase of Myocardial Infarction J. Am. Coll. Cardiol., September 20, 2005; 46(6): 1101 - 1109. [Abstract] [Full Text] [PDF]
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G Liuzzo, G Giubilato, and M Pinnelli T cells and cytokines in atherogenesis Lupus, September 1, 2005; 14(9): 732 - 735. [Abstract] [PDF]
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L M Biasucci, G Giubilato, F Graziani, and M Piro CRP is or is not a reliable marker of ischaemic heart disease? Lupus, September 1, 2005; 14(9): 752 - 755. [Abstract] [PDF]
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G. K. Hansson Inflammation, Atherosclerosis, and Coronary Artery Disease N. Engl. J. Med., April 21, 2005; 352(16): 1685 - 1695. [Full Text] [PDF]
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C. Monaco, E. Rossi, D. Milazzo, F. Citterio, F. Ginnetti, G. D'Onofrio, D. Cianflone, F. Crea, L. M. Biasucci, and A. Maseri Persistent systemic inflammation in unstable angina is largely unrelated to the atherothrombotic burden J. Am. Coll. Cardiol., January 18, 2005; 45(2): 238 - 243. [Abstract] [Full Text] [PDF]
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M. S. Sabatine and E. Braunwald Another look at the age-old question: Which came first, the elevated c-reactive protein or the atherothrombosis? J. Am. Coll. Cardiol., January 18, 2005; 45(2): 244 - 245. [Full Text] [PDF]
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L. M. Biasucci CDC/AHA Workshop on Markers of Inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: Clinical Use of Inflammatory Markers in Patients With Cardiovascular Diseases: A Background Paper Circulation, December 21, 2004; 110(25): e560 - e567. [Abstract] [Full Text] [PDF]
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B. Schieffer, T. Selle, A. Hilfiker, D. Hilfiker-Kleiner, K. Grote, U. J.F. Tietge, C. Trautwein, M. Luchtefeld, C. Schmittkamp, S. Heeneman, et al. Impact of Interleukin-6 on Plaque Development and Morphology in Experimental Atherosclerosis Circulation, November 30, 2004; 110(22): 3493 - 3500. [Abstract] [Full Text] [PDF]
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B. Schieffer, C. Bunte, J. Witte, K. Hoeper, R. H. Boger, E. Schwedhelm, and H. Drexler Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease J. Am. Coll. Cardiol., July 21, 2004; 44(2): 362 - 368. [Abstract] [Full Text] [PDF]
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C. Smith, A. Yndestad, B. Halvorsen, T. Ueland, T. Waehre, K. Otterdal, H. Scholz, K. Endresen, L. Gullestad, S. S. Froland, et al. Potential anti-inflammatory role of activin A in acute coronary syndromes J. Am. Coll. Cardiol., July 21, 2004; 44(2): 369 - 375. [Abstract] [Full Text] [PDF]
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Y. Murase, Y. Yamada, A. Hirashiki, S. Ichihara, H. Kanda, M. Watarai, F. Takatsu, T. Murohara, and M. Yokota Genetic risk and gene-environment interaction in coronary artery spasm in Japanese men and women Eur. Heart J., June 1, 2004; 25(11): 970 - 977. [Abstract] [Full Text] [PDF]
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A.D. Booth, D.R.W. Jayne, R.K. Kharbanda, C.M. McEniery, I.S. Mackenzie, J. Brown, and I.B. Wilkinson Infliximab Improves Endothelial Dysfunction in Systemic Vasculitis: A Model of Vascular Inflammation Circulation, April 13, 2004; 109(14): 1718 - 1723. [Abstract] [Full Text] [PDF]
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L S Rallidis, M G Zolindaki, P C Pentzeridis, K P Poulopoulos, A H Velissaridou, and T S Apostolou Raised concentrations of macrophage colony stimulating factor in severe unstable angina beyond the acute phase are strongly predictive of long term outcome Heart, January 1, 2004; 90(1): 25 - 29. [Abstract] [Full Text] [PDF]
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S. Kinlay, G. G. Schwartz, A. G. Olsson, N. Rifai, S. J. Leslie, W. J. Sasiela, M. Szarek, P. Libby, P. Ganz, and for the Myocardial Ischemia Reduction with Aggress High-Dose Atorvastatin Enhances the Decline in Inflammatory Markers in Patients With Acute Coronary Syndromes in the MIRACL Study Circulation, September 30, 2003; 108(13): 1560 - 1566. [Abstract] [Full Text] [PDF]
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D Tousoulis, G Davies, C Stefanadis, P Toutouzas, and J A Ambrose Inflammatory and thrombotic mechanisms in coronary atherosclerosis Heart, September 1, 2003; 89(9): 993 - 997. [Abstract] [Full Text] [PDF]
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C. M.L. Chapman, J. P. Beilby, S. E. Humphries, L. J. Palmer, P. L. Thompson, and J. Hung Association of an allelic variant of interleukin-6 with subclinical carotid atherosclerosis in an Australian community population Eur. Heart J., August 2, 2003; 24(16): 1494 - 1499. [Abstract] [Full Text] [PDF]
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T. B. Ledue and N. Rifai Preanalytic and Analytic Sources of Variations in C-reactive Protein Measurement: Implications for Cardiovascular Disease Risk Assessment Clin. Chem., August 1, 2003; 49(8): 1258 - 1271. [Abstract] [Full Text] [PDF]
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G. Luc, J.-M. Bard, I. Juhan-Vague, J. Ferrieres, A. Evans, P. Amouyel, D. Arveiler, J.-C. Fruchart, and P. Ducimetiere C-Reactive Protein, Interleukin-6, and Fibrinogen as Predictors of Coronary Heart Disease: The PRIME Study Arterioscler Thromb Vasc Biol, July 1, 2003; 23(7): 1255 - 1261. [Abstract] [Full Text] [PDF]
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H. Soejima, A. Irie, S. Miyamoto, I. Kajiwara, S. Kojima, J. Hokamaki, T. Sakamoto, T. Tanaka, M. Yoshimura, Y. Nishimura, et al. Preference Toward a T-Helper Type 1 Response in Patients With Coronary Spastic Angina Circulation, May 6, 2003; 107(17): 2196 - 2200. [Abstract] [Full Text] [PDF]
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C. Heeschen, S. Dimmeler, C. W. Hamm, S. Fichtlscherer, E. Boersma, M. L. Simoons, A. M. Zeiher, and for the CAPTURE Study Investigators Serum Level of the Antiinflammatory Cytokine Interleukin-10 Is an Important Prognostic Determinant in Patients With Acute Coronary Syndromes Circulation, April 29, 2003; 107(16): 2109 - 2114. [Abstract] [Full Text] [PDF]
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S. Matetzky, M. Domingo, S. Kar, M. Noc, P. K. Shah, S. Kaul, E. Daar, and B. Cercek Acute Myocardial Infarction in Human Immunodeficiency Virus-Infected Patients Arch Intern Med, February 24, 2003; 163(4): 457 - 460. [Abstract] [Full Text] [PDF]
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S. Chia, C. A. Ludlam, K. A. A. Fox, and D. E. Newby Acute systemic inflammation enhances endothelium-dependent tissue plasminogen activator release in men J. Am. Coll. Cardiol., January 15, 2003; 41(2): 333 - 339. [Abstract] [Full Text] [PDF]
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J Oldgren, L Wallentin, L Grip, R Linder, B.L Norgaard, and A Siegbahn Myocardial damage, inflammation and thrombin inhibition in unstable coronary artery disease Eur. Heart J., January 1, 2003; 24(1): 86 - 93. [Abstract] [Full Text] [PDF]
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M. E. Korkmaz, E. Tayfun, H. Muderrisoglu, A. Yildirir, B. Ozin, M. Ulucam, and M. Turan Carbon Coating of Stents Has No Effect on Inflammatory Response to Primary Stent Deployment Angiology, September 1, 2002; 53(5): 563 - 568. [Abstract] [PDF]
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R. Altman, H. L. Luciardi, J. Muntaner, F. Del Rio, S. G. Berman, R. Lopez, and C. Gonzalez Efficacy Assessment of Meloxicam, a Preferential Cyclooxygenase-2 Inhibitor, in Acute Coronary Syndromes Without ST-Segment Elevation: The Nonsteroidal Anti-Inflammatory Drugs in Unstable Angina Treatment-2 (NUT-2) Pilot Study Circulation, July 9, 2002; 106(2): 191 - 195. [Abstract] [Full Text] [PDF]
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A. Buffon, L. M. Biasucci, G. Liuzzo, G. D'Onofrio, F. Crea, and A. Maseri Widespread Coronary Inflammation in Unstable Angina N. Engl. J. Med., July 4, 2002; 347(1): 5 - 12. [Abstract] [Full Text] [PDF]
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C. D. Spies, H. Kern, T. Schroder, M. Sander, H. Sepold, P. Lang, K. Stangl, S. Behrens, P. Sinha, W. Schaffartzik, et al. Myocardial Ischemia and Cytokine Response Are Associated with Subsequent Onset of Infections After Noncardiac Surgery Anesth. Analg., July 1, 2002; 95(1): 9 - 18. [Abstract] [Full Text] [PDF]
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F. Basso, G. D.O. Lowe, A. Rumley, A. D. McMahon, and S. E. Humphries Interleukin-6 -174G>C Polymorphism and Risk of Coronary Heart Disease in West of Scotland Coronary Prevention Study (WOSCOPS) Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 599 - 604. [Abstract] [Full Text] [PDF]
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R. Kell, A. Haunstetter, T.J. Dengler, C. Zugck, W. Kubler, and M. Haass Do cytokines enable risk stratification to be improved in NYHA functional class III patients?. Comparison with other potential predictors of prognosis Eur. Heart J., January 1, 2002; 23(1): 70 - 78. [Abstract] [Full Text] [PDF]
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M. S. Elkind, J. Cheng, B. Boden-Albala, T. Rundek, J. Thomas, H. Chen, L. E. Rabbani, R. L. Sacco, and A. G. Thrift Tumor Necrosis Factor Receptor Levels Are Associated With Carotid Atherosclerosis * Editorial Comment Stroke, January 1, 2002; 33(1): 31 - 38. [Abstract] [Full Text] [PDF]
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N. Lamblin, C. Bauters, and N. Helbecque Gene polymorphisms of pro- (or anti-) inflammatory cytokines and vascular disease Eur. Heart J., December 2, 2001; 22(24): 2219 - 2220. [PDF]
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S.E. Humphries, L.A. Luong, M.S. Ogg, E. Hawe, and G.J. Miller The interleukin-6 -174 G/C promoter polymorphism is associated with risk of coronary heart disease and systolic blood pressure in healthy men Eur. Heart J., December 2, 2001; 22(24): 2243 - 2252. [Abstract] [PDF]
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C D Garlichs, S Eskafi, D Raaz, A Schmidt, J Ludwig, M Herrmann, L Klinghammer, W G Daniel, and A Schmeisser Patients with acute coronary syndromes express enhanced CD40 ligand/CD154 on platelets Heart, December 1, 2001; 86(6): 649 - 655. [Abstract] [Full Text] [PDF]
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E. Lindmark, E. Diderholm, L. Wallentin, and A. Siegbahn Relationship Between Interleukin 6 and Mortality in Patients With Unstable Coronary Artery Disease: Effects of an Early Invasive or Noninvasive Strategy JAMA, November 7, 2001; 286(17): 2107 - 2113. [Abstract] [Full Text] [PDF]
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T. Tokunou, T. Ichiki, K. Takeda, Y. Funakoshi, N. Iino, H. Shimokawa, K. Egashira, and A. Takeshita Thrombin Induces Interleukin-6 Expression Through the cAMP Response Element in Vascular Smooth Muscle Cells Arterioscler Thromb Vasc Biol, November 1, 2001; 21(11): 1759 - 1763. [Abstract] [Full Text] [PDF]
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M. I. Furman, M. R. Barnard, L. A. Krueger, M. L. Fox, E. A. Shilale, D. M. Lessard, P. Marchese, A. L. Frelinger III, R. J. Goldberg, and A. D. Michelson Circulating monocyte-platelet aggregates are an early marker of acute myocardial infarction J. Am. Coll. Cardiol., October 1, 2001; 38(4): 1002 - 1006. [Abstract] [Full Text] [PDF]
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D.J. Brull, H.E. Montgomery, J. Sanders, S. Dhamrait, L. Luong, A. Rumley, G.D.O. Lowe, and S.E. Humphries Interleukin-6 Gene -174G>C and -572G>C Promoter Polymorphisms Are Strong Predictors of Plasma Interleukin-6 Levels After Coronary Artery Bypass Surgery Arterioscler Thromb Vasc Biol, September 1, 2001; 21(9): 1458 - 1463. [Abstract] [Full Text] [PDF]
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D. A. Smith, S. D. Irving, J. Sheldon, D. Cole, and J. C. Kaski Serum Levels of the Antiinflammatory Cytokine Interleukin-10 Are Decreased in Patients With Unstable Angina Circulation, August 14, 2001; 104(7): 746 - 749. [Abstract] [Full Text] [PDF]
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G. Valen, Z.-q. Yan, and G.o. K. Hansson Nuclear factor kappa-B and the heart J. Am. Coll. Cardiol., August 1, 2001; 38(2): 307 - 314. [Abstract] [Full Text] [PDF]
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R. J. Simpson Jr Placing PRINCE in Perspective JAMA, July 4, 2001; 286(1): 91 - 93. [Full Text] [PDF]
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T O'malley, C.A Ludlam, R.A Riemermsa, and K.A.A Fox Early increase in levels of soluble inter-cellular adhesion molecule-1 (sICAM-1). Potential risk factor for the acute coronary syndromes Eur. Heart J., July 2, 2001; 22(14): 1226 - 1234. [Abstract] [PDF]
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G. G. Neri Serneri, M. Boddi, L. Poggesi, I. Simonetti, M. Coppo, M. L. Papa, G. F. Lisi, M. Maccherini, R. Becherini, A. Boncompagni, et al. Activation of cardiac renin-angiotensin system in unstable angina J. Am. Coll. Cardiol., July 1, 2001; 38(1): 49 - 55. [Abstract] [Full Text] [PDF]
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S. Blankenberg, H. J. Rupprecht, C. Bickel, C. Espinola-Klein, G. Rippin, G. Hafner, M. Ossendorf, K. Steinhagen, and J. Meyer Cytomegalovirus Infection With Interleukin-6 Response Predicts Cardiac Mortality in Patients With Coronary Artery Disease Circulation, June 19, 2001; 103(24): 2915 - 2921. [Abstract] [Full Text] [PDF]
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G. Liuzzo, D. J. Angiolillo, A. Buffon, V. Rizzello, C. Colizzi, F. Ginnetti, L. M. Biasucci, and A. Maseri Enhanced Response of Blood Monocytes to In Vitro Lipopolysaccharide-Challenge in Patients With Recurrent Unstable Angina Circulation, May 8, 2001; 103(18): 2236 - 2241. [Abstract] [Full Text] [PDF]
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A Mazzone, S De Servi, I Mazzucchelli, I Bossi, E Ottini, M Vezzoli, F Meloni, M Lotzinker, and G Mariani Increased concentrations of inflammatory mediators in unstable angina: correlation with serum troponin T Heart, May 1, 2001; 85(5): 571 - 575. [Abstract] [Full Text]
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G. Liuzzo, A. N. Vallejo, S. L. Kopecky, R. L. Frye, D. R. Holmes, J. J. Goronzy, and C. M. Weyand Molecular Fingerprint of Interferon-{{gamma}} Signaling in Unstable Angina Circulation, March 20, 2001; 103(11): 1509 - 1514. [Abstract] [Full Text] [PDF]
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S. Volpato, J. M. Guralnik, L. Ferrucci, J. Balfour, P. Chaves, L. P. Fried, and T. B. Harris Cardiovascular Disease, Interleukin-6, and Risk of Mortality in Older Women : The Women's Health and Aging Study Circulation, February 20, 2001; 103(7): 947 - 953. [Abstract] [Full Text] [PDF]
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J. A. Shaw, J. P. F. Chin-Dusting, B. A. Kingwell, and A. M. Dart Diurnal Variation in Endothelium-Dependent Vasodilatation Is Not Apparent in Coronary Artery Disease Circulation, February 13, 2001; 103(6): 806 - 812. [Abstract] [Full Text] [PDF]
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J. Figueras, Y. Monasterio, R. M. Lidon, E. Nieto, and J. Soler-Soler Thrombin formation and fibrinolytic activity in patients with acute myocardial infarction or unstable angina: in-hospital course and relationship with recurrent angina at rest J. Am. Coll. Cardiol., December 1, 2000; 36(7): 2036 - 2043. [Abstract] [Full Text] [PDF]
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D. R. Taaffe, T. B. Harris, L. Ferrucci, J. Rowe, and T. E. Seeman Cross-sectional and Prospective Relationships of Interleukin-6 and C-Reactive Protein With Physical Performance in Elderly Persons: MacArthur Studies of Successful Aging J. Gerontol. A Biol. Sci. Med. Sci., December 1, 2000; 55(12): 709M - 715. [Abstract] [Full Text]
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R. Rauramaa, S. B. Vaisanen, L.-A. Luong, A. Schmidt-Trucksass, I. M. Penttila, C. Bouchard, J. Toyry, and S. E. Humphries Stromelysin-1 and Interleukin-6 Gene Promoter Polymorphisms Are Determinants of Asymptomatic Carotid Artery Atherosclerosis Arterioscler Thromb Vasc Biol, December 1, 2000; 20(12): 2657 - 2662. [Abstract] [Full Text] [PDF]
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D. Zanger, B. K. Yang, J. Ardans, M. A. Waclawiw, G. Csako, L. M. Wahl, and R. O. Cannon III Divergent effects of hormone therapy on serum markers of inflammation in postmenopausal women with coronary artery disease on appropriate medical management J. Am. Coll. Cardiol., November 15, 2000; 36(6): 1797 - 1802. [Abstract] [Full Text] [PDF]
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A. Woods, D.J. Brull, S.E. Humphries, and H.E. Montgomery Genetics of inflammation and risk of coronary artery disease: the central role of interleukin-6 Eur. Heart J., October 1, 2000; 21(19): 1574 - 1583. [PDF]
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E. Braunwald, E. M. Antman, J. W. Beasley, R. M. Califf, M. D. Cheitlin, J. S. Hochman, R. H. Jones, D. Kereiakes, J. Kupersmith, T. N. Levin, et al. ACC/AHA guidelines for the management of patients with unstable angina and non-st-segment elevation myocardial infarction: A report of the american college of cardiology/ american heart association task force on practice guidelines (committee on the management of patients with unstable angina) J. Am. Coll. Cardiol., September 1, 2000; 36(3): 970 - 1062. [Full Text] [PDF]
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