(Circulation. 1999;100:793-798.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
From The Imperial College School of Medicine, National Heart & Lung Institute, Cardiology Department, Hammersmith Hospital, London, UK, and the Department of Cardiology (E.E., C.S., P.T.), Ippokration Hospital, Athens, Greece.
Correspondence to Petros Nihoyannopoulos, MD, FACC, FESC, Imperial College School of Medicine, National Heart & Lung Institute, Cardiology Department, Hammersmith Hospital, Du Cane Road, London W12 0NN, UK. E-mail petros{at}rpms.ac.uk
| Abstract |
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Methods and ResultsPlasma macrophage colony stimulating factor (MCSF), IL-1b, IL-6, and CRP were measured in 60 stable patients after 48-hour Holter monitoring and in 24 matched controls. All patients had angiographic documentation of disease and positive exercise ECGs. Patients with ischemia on Holter monitoring (n=40) received aspirin or placebo in a 6-week, randomized, double blind, crossover trial. Blood sampling was repeated at the end of each treatment phase (3 weeks). Compared to controls, patients had more than twice median MCSF (800 versus 372 pg/mL), IL-6 (3.9 versus 1.7 pg/mL), and CRP (1.25 versus 0.23 mg/L) levels (P<0.01 for all comparisons). MCSF was related to ischemia on Holter monitoring (P<0.01), to low ischemic threshold during exercise (P<0.01), and together with IL-1b to number of diseased vessels (P<0.05). MCSF, IL-6, and CRP were all reduced after 6 weeks of aspirin treatment (P<0.05).
ConclusionsThese findings suggest that cytokines are associated with both ischemia and anatomic extent of disease in patients with stable angina. Reduced cytokine and CRP levels by aspirin may explain part of aspirin's therapeutic action.
Key Words: interleukins atherosclerosis coronary disease ischemia aspirin
| Introduction |
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The plasma levels of MCSF, IL-6, and C-reactive protein (CRP) have been found elevated in patients with unstable angina20 21 22 and acute myocardial infarction22 23 24 but have not been carefully investigated in patients with chronic stable angina. We hypothesized that MCSF, IL-1b, and IL-6 plasma levels in patients with chronic stable coronary artery disease might be associated with the anatomic extent of disease and that aspirin administration might reduce cytokine plasma levels.
| Methods |
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Twenty-four clinically healthy subjects (17 men, 7 women, mean age
52±13 years, range 32 to 68 years) served as a control group. They had
normal baseline ECG, echocardiogram and treadmill test, no evidence of
active infection, and were taking no medications. Patients and controls
were matched for coronary artery disease risk factors
(Table 1
) to secure a similar
state of oxidative stress. The study protocol was approved by the
Hammersmith Hospital's Ethics Committee.
|
Exercise Testing
Treadmill exercise testing (Marquette Case 15) was
performed according to the Bruce or modified Bruce protocol within 3
months before enrollment (15 to 90 days). Antianginal therapy was
withheld for 48 hours before the test. The number of
metabolic equivalents (Mets) achieved at ST-segment
depression >0.1 mV, 60 ms after the J point, was used to indicate the
ischemic threshold.
Holter Monitoring
Patients underwent a 48-hour Holter monitoring (Marquette 8000
laser system) to assess the presence of ischemia during daily
activities. The Holter recording was performed no later than 3
months after the exercise test. Antianginal therapy was again withheld
for 48 hours before and during monitoring, although sublingual nitrates
were allowed if chest pain persisted beyond 3 minutes. Only 7 of 60
patients used sublingual nitrates. Antiplatelet drugs were not
administered during the preceding 2 weeks. ST-segment depression >0.1
mV, occurring 60 ms after the J point and lasting at least 1 minute,
was considered as indicative of ischemia.25 Forty
of the 60 enrolled patients (67%) showed signs of ischemia
during Holter monitoring.
Blood Sampling
Baseline morning blood samples were taken from the 60 patients,
at the end of Holter monitoring, and from controls. The samples were
drawn into plastic tubes containing 1:9 volumes of 0.103 mol/L
trisodium citrate and centrifuged at 2000g for 15
minutes at 40°C. Aliquots of plasma were stored at -700°C until
subsequent analysis.
Randomization to Aspirin or Placebo
The 40 patients with signs of ischemia during Holter
monitoring were randomized in a crossover, double blind trial to
receive either oral aspirin (300 mg/d) or placebo. Patients without
ischemia during the Holter recording were excluded to
achieve greater homogeneity of the study population. Aspirin and
placebo were provided by the hospital's pharmacy as identical
capsules. Each treatment phase lasted 3 weeks, to avoid any carry over
effects of aspirin. Thus, 20 patients received aspirin, and the
remaining 20 placebo for 3 weeks; all 40 patients were then crossed
over to the alternate treatment for another 3 weeks.
Blood sampling was repeated at the end of each 3-week phase. Antianginal medication, with the exception of sublingual nitrates, was withheld for 4 days before blood sampling. Patients and physicians involved in the trial were blinded to the type of medication (aspirin or placebo) assigned during each phase; the code was broken only after analysis of the data had been completed.
Laboratory Assays
The laboratory measurements were performed by personnel unaware
of the clinical data. Plasma MCSF concentrations were measured using a
commercial enzyme-linked immunoassay (human MCSF, Quantikinine R&D
system, Minneapolis, Minn). The sensitivity of the assay is 20
pg/mL. IL-6 and IL-1b were measured by high sensitivity immunoassays
(human IL-6 and IL-1b Quantikinine [high sensitivity] R&D systems)
which detect values as low as 0.094 pg/mL and 100 fg/mL, respectively.
CRP was measured using particle-enhanced immunonephelometry (N Latex
CRP mono, Behring Diagnostics). This assay detects values
as low as 0.175 mg/L. The intra-assay coefficient of variation was
<5% for all tests. Cytokine levels were within the assays'
detection limit in all patients and controls. CRP levels were below the
detection limit in 6 patients (10%) and 8 controls (33%). In such
cases, values were obtained by extrapolation of the assay's standard
curve using the equation: y=141.956+5070x.
Statistical Analysis
Biochemical data are expressed as medians and interquartiles.
Differences within and between groups were analyzed by
Wilcoxon signed rank test, Mann Whitney U test or
ANOVA (Kruskal-Wallis and Friedman test). Spearman's rank correlation
test was used to assess relations between variables. Multiple
relations were tested by stepwise regression analysis.
Categorical variables were compared by contingency c2 test.
P<0.05 (2-tailed) was considered statistically
significant.
| Results |
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Cytokines in Patients and Controls
Patients had more than twice the plasma concentrations of
MCSF, IL-6, and CRP compared with controls (Table 2
). ANOVA showed that MCSF and IL-1b
levels increased with the number of diseased vessels (Figure 1
). Thus, patients with 3- vessel disease
had 2- to 3-fold higher MCSF levels than patients with 2- and
single-vessel disease, whereas patients with 2-vessel disease had
higher levels than patients with single-vessel disease
(P<0.05). Similarly, patients with 3-vessel disease had
higher IL-1b levels than patients with single- and 2-vessel disease.
Only patients with 3-vessel disease had higher IL-1b plasma levels
compared with controls (P<0.05). MCSF and IL-1b
concentrations in patients with single-vessel disease did not differ
from controls. Furthermore, MCSF, IL-1b, and IL-6 levels did not differ
between patients with (n=31) or without previous myocardial
infarction.
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Relation Between Cytokines and CRP
IL-6 and MCSF concentrations were independently related to CRP
(r=0.58, P<0.01 and r=0.35,
P<0.05, respectively) in patients with chronic stable
angina. In controls, however, only IL-6 showed a significant relation
to CRP levels (r=0.55, P<0.05). Additionally,
MCSF values were related to IL-1b (r=0.47,
P<0.01). There was no relation between IL-6 and MCSF or
IL-6 and IL-1b levels in patients or controls (Figure 2
).
|
Cytokines and Ischemia
On Exercise
Predictably, the number of Mets achieved at the onset of
ischemia on effort decreased with the number of diseased
vessels (P<0.001). MCSF levels showed an inverse relation
to the number of Mets during ischemia (r=-0.50,
P<0.001). Median MCSF levels were 1100 pg/mL (range, 852 to
1390) in the 37 patients with ischemia <5 Mets versus 320
pg/mL (range, 308 to 686) in the 23 patients with ischemia >5
Mets (P<0.001) (5 mets=2nd stage of Bruce protocol). The 2
subgroups did not differ in age, sex, or risk factor distribution
(Figure 3
).
|
During Holter Monitoring
The 40 patients with ischemia on Holter had a higher
prevalence of multivessel disease compared with the 20 patients without
ischemia. Median MCSF levels were 1100 pg/mL (range, 860 to
1329) in the 40 patients with ischemia versus 330 pg/mL (range,
300 to 926) in the 20 patients without (P<0.01). Patients
with and without ischemia during Holter did not differ in age,
sex, risk factor distribution or in mean and maximum heart rate during
Holter monitoring. The median number and cumulative duration of
ischemic episodes was 8 (range, 6 to 11) and 33 minutes (range,
28 to 65), respectively. No significant relation was detected between
cytokine plasma levels and number or duration of
ischemic episodes.
Aspirin and Cytokine Levels
Although with substantial overlap, there was a significant
reduction of MCSF, IL-6, and CRP after 6 weeks of aspirin
administration compared with placebo (Table 3
). With aspirin, the levels of IL-6,
CRP, and MCSF were reduced by 37% (range, 31% to 53%), 29% (range,
9% to 60%) and 17% (range, 11% to 23%), respectively, compared
with placebo (P<0.05 for all comparisons). Cytokine
and CRP levels measured at the end of placebo phase did not differ from
the baseline values measured before randomization. IL-1b plasma levels
did not differ during the placebo and aspirin phases.
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| Discussion |
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Cytokines and Atherosclerosis
Atherogenetic risk factors, such as oxidized low density
lipoprotein,1 2 tobacco glucoprotein,26
chlamydial or viral infections,3 4 5 6 and several
cytokines3 5 6 27 may all induce the
endothelium to produce MCSF. MCSF stimulates the
production of IL-1b3 28 and of further MCSF
production3 by the local
endothelium, resident macrophages, and by
newly-recruited monocytes from peripheral blood.
Additionally, MCSF and IL-1b upregulate the expression of leukocyte
adhesion molecules on the endothelial surface and of
specific integrins on monocytes, leading to enhanced adhesion of
monocytes to the endothelium.5 6 7
Both, MCSF and IL-1b induce macrophage activation and proliferation which promote further release of cytokines.6 15 17 Cytokine-activated monocyte/macrophages produce increased amounts of IL-614 15 which may enter the systemic circulation and lead to increased production of CRP by hepatocytes.29 30 31 The above sequence of cytokine production derived from animal studies may explain, at least in part, the presence of increased MCSF, IL-1b, IL-6, and CRP levels in patients with known or suspected coronary artery disease.
In the present study, both MCSF and IL-1b plasma levels were associated with the extent of coronary artery disease at angiography. As a result, MCSF plasma levels in patients with 3-vessel disease were manyfold higher than in patients with single- or 2-vessel disease. MCSF and, to a lesser extent, IL-1b, enhance cholesterol uptake from human macrophages by upregulation of their oxidized LDL receptors, resulting in foam-cell formation9 10 11 and plaque growth. Indeed, mice genetically deficient in MCSF show decreased progression of atherosclerosis.32 Additionally, the messenger RNA and protein of MCSF and IL-1b have been isolated in human atherosclerotic lesions.3 4 8 9 Thus, the relation of MCSF and IL-1b to the anatomic extent of disease we found in this study may be suggestive of an important role of growth factors and inflammatory mediators in the progression of atherosclerosis in humans, confirming previous experimental findings.3 4 5 6 9 10 11 32
We found that MCSF levels were related to IL-1b and CRP levels in patients but not in controls. This suggests a relation between potentially atherogenic cytokines and acute phase proteins in the setting of atherosclerosis. IL-6 concentrations, however, were related to CRP levels in both patients and controls, as previously observed.29 30 31
Cytokines and Myocardial Ischemia
Patients with lower ischemic threshold, as assessed by
exercise testing and Holter monitoring, had markedly increased MCSF
levels compared with patients with a higher ischemic threshold.
MCSF stimulates the endothelium and
monocyte/macrophages to release several vasoactive
substances.3 4 5 6 15 17 In vitro studies also suggest that
MCSF promotes platelet adherence, platelet
activation,33 34 35 tissue factor expression,36
and production of procoagulant cytokines such as IL-1b
and IL-64 5 37 at sites of injured
endothelium. Therefore, MCSF, by increased
coronary tone,38 39 impaired
vasodilatation,19 and formation of
microthrombi40 41 may reduce coronary flow and
thus initiate, facilitate, or prolong ischemic
episodes.42 43 Alternatively, ischemic episodes
per se may induce an increase in circulating MCSF, as has been
demonstrated for IL-6.44
Effects of Aspirin
We investigated the effects of a 300 mg daily dose of aspirin on
cytokines and CRP, in a randomized, double-blind,
placebo-controlled, crossover trial. Compared with placebo, aspirin was
associated with a significant and concomitant reduction of IL-6, CRP,
and MCSF. The induction of macrophage/monocyte activation and
proliferation by MCSF and IL-1b involves
cyclooxygenase activity.3 18 19
Activated and proliferating vascular cells produce further MCSF
and IL-6,3 14 15 16 17 which may enter into the bloodstream.
Aspirin may prevent cyclooxygenase-mediated cell
activation and proliferation and reduce the release of these
cytokines in blood by acetylating
cyclooxygenase.45 Aspirin
administration in patients with chronic stable angina has been
associated with increased plasma levels of the antiproliferative
cytokine, transforming growth factor-b (TGF-b).46
Interestingly, an inverse relation between TGF-b and MCSF blood levels
has been found.22 Thus, an increase in TGF-b levels by
aspirin may downregulate MCSF and IL-6 production by vascular
cells. Alternatively, aspirin may reduce MCSF and IL-6 through
mechanisms related to platelet inhibition. The reduction of CRP by
aspirin is likely to be secondary to the reduction in IL-6, because
IL-6 is known to stimulate the synthesis of acute phase proteins by the
liver.29 30 31
The modest reduction in cytokine levels after 300 mg of aspirin administration may result from the fact that aspirin exhibits its greatest antinflammatory action at doses as high as 2 g. In support of this, Bhaghat et al19 found that aspirin inhibited the adverse effects of cytokines on endothelium-dependent dilatation in human veins only at a dose of 1 g and not at 75 mg. Several considerations indicate that the reductions in MCSF, IL-6, and CRP levels by aspirin are not fortuitous findings: (1) because of the strict study design (randomized, double-blind, crossover, placebo-controlled); (2) there was a concomitant reduction in MCSF, IL-6, and CRP; (3) there was a good reproducibility of measurements at baseline and during placebo; and (4) there is a reasonable mechanism behind it.
Study Limitations
The following limitations should be acknowledged. The study was
not designed to establish whether raised cytokine levels might
be a cause or a consequence of atherosclerosis and/or
ischemia. The control group did not undergo coronary
angiography and thus subclinical coronary artery disease cannot
be excluded. Cytokines were measured in peripheral
blood. This may have reduced the sensitivity of the measurements and
does not allow conclusions on the release of cytokines in the
coronary circulation. Sublingual nitrates are nitric oxide
donors and may have affected the plasma levels of cytokines in
the 7 patients who made use of them. However, there is no clear
evidence that nitrates could affect cytokine levels.
Conversely, nitric oxide may be a mediator of IL-6's
actions.6
Conclusions
This is the first study to demonstrate the presence of higher
circulating levels of the proinflammatory/atherogenic cytokines
MCSF, IL-6, and IL-1b levels in patients with chronic stable angina
compared with healthy controls. MCSF and IL-1b were related to anatomic
severity of disease and MCSF with low ischemic threshold. This
suggests a graded relation between these cytokines and severity
of coronary artery disease. In a randomized placebo-controlled
trial, aspirin reduced the circulating levels of MCSF, IL-6, and CRP.
This may explain part of the drug's therapeutic action in patients
with ischemic heart disease.
| Acknowledgments |
|---|
Received March 12, 1999; revision received May 19, 1999; accepted May 26, 1999.
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A. Duka, E. Kintsurashvili, I. Duka, D. Ona, T. A. Hopkins, M. Bader, I. Gavras, and H. Gavras Angiotensin-Converting Enzyme Inhibition After Experimental Myocardial Infarct: Role of the Kinin B1 and B2 Receptors Hypertension, May 1, 2008; 51(5): 1352 - 1357. [Abstract] [Full Text] [PDF] |
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S. Kim, T. O. Keku, C. Martin, J. Galanko, J. T. Woosley, J. C. Schroeder, J. A. Satia, S. Halabi, and R. S. Sandler Circulating Levels of Inflammatory Cytokines and Risk of Colorectal Adenomas Cancer Res., January 1, 2008; 68(1): 323 - 328. [Abstract] [Full Text] [PDF] |
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S. R. Steinhubl, J. J. Badimon, D. L. Bhatt, J.-M. Herbert, and T. F. Luscher Clinical evidence for anti-inflammatory effects of antiplatelet therapy in patients with atherothrombotic disease Vascular Medicine, May 1, 2007; 12(2): 113 - 122. [Abstract] [PDF] |
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NACB WRITING GROUP MEMBERS, D. A. Morrow, C. P. Cannon, R. L. Jesse, L. K. Newby, J. Ravkilde, A. B. Storrow, A. H.B. Wu, and R. H. Christenson National Academy of Clinical Biochemistry Laboratory Medicine Practice Guidelines: Clinical Characteristics and Utilization of Biochemical Markers in Acute Coronary Syndromes Circulation, April 3, 2007; 115(13): e356 - e375. [Full Text] [PDF] |
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H. Oren, A. R. Erbay, M. Balci, and S. Cehreli Role of Novel Biomarkers of Inflammation in Patients With Stable Coronary Heart Disease Angiology, April 1, 2007; 58(2): 148 - 155. [Abstract] [PDF] |
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NACB WRITING GROUP MEMBERS, D. A. Morrow, C. P. Cannon, R. L. Jesse, L. K. Newby, J. Ravkilde, A. B. Storrow, A. H.B. Wu, R. H. Christenson, NACB COMMITTEE MEMBERS, et al. National Academy of Clinical Biochemistry Laboratory Medicine Practice Guidelines: Clinical Characteristics and Utilization of Biochemical Markers in Acute Coronary Syndromes Clin. Chem., April 1, 2007; 53(4): 552 - 574. [Full Text] [PDF] |
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C. L. Carty, P. Heagerty, K. Nakayama, E. C. McClung, J. Lewis, D. Lum, E. Boespflug, C. McCloud-Gehring, B. R. Soleimani, J. Ranchalis, et al. Inflammatory Response After Influenza Vaccination in Men With and Without Carotid Artery Disease Arterioscler Thromb Vasc Biol, December 1, 2006; 26(12): 2738 - 2744. [Abstract] [Full Text] [PDF] |
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C. H. Hennekens, O. Sechenova, D. Hollar, and V. L. Serebruany Dose of Aspirin in the Treatment and Prevention of Cardiovascular Disease: Current and Future Directions. Journal of Cardiovascular Pharmacology and Therapeutics, September 1, 2006; 11(3): 170 - 176. [Abstract] [PDF] |
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R. P Raghavan, D. W Laight, K. M Shaw, and M. H Cummings Review: Aspirin and diabetes The British Journal of Diabetes & Vascular Disease, March 1, 2006; 6(2): 74 - 82. [Abstract] [PDF] |
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S. Rutschow, J. Li, H.-P. Schultheiss, and M. Pauschinger Myocardial proteases and matrix remodeling in inflammatory heart disease Cardiovasc Res, February 15, 2006; 69(3): 646 - 656. [Abstract] [Full Text] [PDF] |
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M. R. Pijak Rebound Inflammation and the Risk of Ischemic Stroke After Discontinuation of Aspirin Therapy Arch Neurol, February 1, 2006; 63(2): 300 - 301. [Full Text] [PDF] |
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J. S. Berger, M. C. Roncaglioni, F. Avanzini, I. Pangrazzi, G. Tognoni, and D. L. Brown Aspirin for the Primary Prevention of Cardiovascular Events in Women and Men: A Sex-Specific Meta-analysis of Randomized Controlled Trials JAMA, January 18, 2006; 295(3): 306 - 313. [Abstract] [Full Text] [PDF] |
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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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G. S. Ginsburg, M. P. Donahue, and L. K. Newby Prospects for Personalized Cardiovascular Medicine: The Impact of Genomics J. Am. Coll. Cardiol., November 1, 2005; 46(9): 1615 - 1627. [Abstract] [Full Text] [PDF] |
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N. Saleh, B. Svane, L.-O. Hansson, J. Jensen, T. Nilsson, O. Danielsson, and P. Tornvall Response of Serum C-Reactive Protein to Percutaneous Coronary Intervention Has Prognostic Value Clin. Chem., November 1, 2005; 51(11): 2124 - 2130. [Abstract] [Full Text] [PDF] |
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Z. T. Bloomgarden Inflammation, Atherosclerosis, and Aspects of Insulin Action Diabetes Care, September 1, 2005; 28(9): 2312 - 2319. [Full Text] [PDF] |
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D H Birnie, L E Vickers, W S Hillis, J Norrie, and S M Cobbe Increased titres of anti-human heat shock protein 60 predict an adverse one year prognosis in patients with acute cardiac chest pain Heart, September 1, 2005; 91(9): 1148 - 1153. [Abstract] [Full Text] [PDF] |
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I. Ikonomidis, J. Lekakis, I. Revela, F. Andreotti, and P. Nihoyannopoulos Increased circulating C-reactive protein and macrophage-colony stimulating factor are complementary predictors of long-term outcome in patients with chronic coronary artery disease Eur. Heart J., August 2, 2005; 26(16): 1618 - 1624. [Abstract] [Full Text] [PDF] |
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H.-J. Priebe Perioperative myocardial infarction--aetiology and prevention Br. J. Anaesth., July 1, 2005; 95(1): 3 - 19. [Abstract] [Full Text] [PDF] |
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H. Yamagami, K. Kitagawa, T. Hoshi, S. Furukado, H. Hougaku, Y. Nagai, and M. Hori Associations of Serum IL-18 Levels With Carotid Intima-Media Thickness Arterioscler Thromb Vasc Biol, July 1, 2005; 25(7): 1458 - 1462. [Abstract] [Full Text] [PDF] |
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Y. Mitani, H. Sawada, H. Hayakawa, K. Aoki, H. Ohashi, M. Matsumura, K. Kuroe, H. Shimpo, M. Nakano, and Y. Komada Elevated Levels of High-Sensitivity C-Reactive Protein and Serum Amyloid-A Late After Kawasaki Disease: Association Between Inflammation and Late Coronary Sequelae in Kawasaki Disease Circulation, January 4, 2005; 111(1): 38 - 43. [Abstract] [Full Text] [PDF] |
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Y F Cheung, M H K Ho, S C F Tam, and T C Yung Increased high sensitivity C reactive protein concentrations and increased arterial stiffness in children with a history of Kawasaki disease Heart, November 1, 2004; 90(11): 1281 - 1285. [Abstract] [Full Text] [PDF] |
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T. O. Obisesan, C. Leeuwenburgh, T. Phillips, R. E. Ferrell, D. A. Phares, S. J. Prior, and J. M. Hagberg C-Reactive Protein Genotypes Affect Baseline, but not Exercise Training-Induced Changes, in C-Reactive Protein Levels Arterioscler Thromb Vasc Biol, October 1, 2004; 24(10): 1874 - 1879. [Abstract] [Full Text] [PDF] |
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P. Bogaty, J. M. Brophy, M. Noel, L. Boyer, S. Simard, F. Bertrand, and G. R. Dagenais Impact of Prolonged Cyclooxygenase-2 Inhibition on Inflammatory Markers and Endothelial Function in Patients With Ischemic Heart Disease and Raised C-Reactive Protein: A Randomized Placebo-Controlled Study Circulation, August 24, 2004; 110(8): 934 - 939. [Abstract] [Full Text] [PDF] |
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H.-J. Priebe Triggers of perioperative myocardial ischaemia and infarction Br. J. Anaesth., July 1, 2004; 93(1): 9 - 20. [Abstract] [Full Text] [PDF] |
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H Teragawa, Y Fukuda, K Matsuda, K Ueda, Y Higashi, T Oshima, M Yoshizumi, and K Chayama Relation between C reactive protein concentrations and coronary microvascular endothelial function Heart, July 1, 2004; 90(7): 750 - 754. [Abstract] [Full Text] [PDF] |
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D. S. G. Conway, P. Buggins, E. Hughes, and G. Y. H. Lip Relationship of interleukin-6 and C-Reactive protein to the prothrombotic state in chronic atrial fibrillation J. Am. Coll. Cardiol., June 2, 2004; 43(11): 2075 - 2082. [Abstract] [Full Text] [PDF] |
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D. Monakier, M. Mates, M. W. Klutstein, J. A. Balkin, B. Rudensky, D. Meerkin, and D. Tzivoni Rofecoxib, a COX-2 Inhibitor, Lowers C-Reactive Protein and Interleukin-6 Levels in Patients With Acute Coronary Syndromes Chest, May 1, 2004; 125(5): 1610 - 1615. [Abstract] [Full Text] [PDF] |
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I Ikonomidis, F Andreotti, and P Nihoyannopoulos Reduction of daily life ischaemia by aspirin in patients with angina: underlying link between thromboxane A2 and macrophage colony stimulating factor Heart, April 1, 2004; 90(4): 389 - 393. [Abstract] [Full Text] [PDF] |
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D. L. Brown, K. K. Desai, B. A. Vakili, C. Nouneh, H.-M. Lee, and L. M. Golub Clinical and Biochemical Results of the Metalloproteinase Inhibition with Subantimicrobial Doses of Doxycycline to Prevent Acute Coronary Syndromes (MIDAS) Pilot Trial Arterioscler Thromb Vasc Biol, April 1, 2004; 24(4): 733 - 738. [Abstract] [Full Text] [PDF] |
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H. Yamagami, K. Kitagawa, Y. Nagai, H. Hougaku, M. Sakaguchi, K. Kuwabara, K. Kondo, T. Masuyama, M. Matsumoto, and M. Hori Higher Levels of Interleukin-6 Are Associated With Lower Echogenicity of Carotid Artery Plaques Stroke, March 1, 2004; 35(3): 677 - 681. [Abstract] [Full Text] [PDF] |
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K.J. Joshipura, H.C. Wand, A.T. Merchant, and E.B. Rimm Periodontal Disease and Biomarkers Related to Cardiovascular Disease Journal of Dental Research, February 1, 2004; 83(2): 151 - 155. [Abstract] [Full Text] [PDF] |
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J. M Backes, P. A Howard, and P. M Moriarty Role of C-Reactive Protein in Cardiovascular Disease Ann. Pharmacother., January 1, 2004; 38(1): 110 - 118. [Abstract] [Full Text] [PDF] |
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T. Dziedzic, A. Slowik, A. Szczudlik, M. Schwaninger, A. Grau, and D. Acalovschi Interleukin-6 and Stroke: Cerebral Ischemia Versus Nonspecific Factors Influencing Interleukin-6 * Response Stroke, December 1, 2003; 34 (12): e229 - e230. [Full Text] [PDF] |
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L. M. Title, K. Giddens, M. M. McInerney, M. J. McQueen, and B. A. Nassar Effect of cyclooxygenase-2 inhibition with rofecoxib on endothelial dysfunction and inflammatory markers in patients with coronary artery disease J. Am. Coll. Cardiol., November 19, 2003; 42(10): 1747 - 1753. [Abstract] [Full Text] [PDF] |
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R. Wolk, P. Berger, R. J. Lennon, E. S. Brilakis, and V. K. Somers Body Mass Index: A Risk Factor for Unstable Angina and Myocardial Infarction in Patients With Angiographically Confirmed Coronary Artery Disease Circulation, November 4, 2003; 108(18): 2206 - 2211. [Abstract] [Full Text] [PDF] |
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D.J. Brull, N. Serrano, F. Zito, L. Jones, H.E. Montgomery, A. Rumley, P. Sharma, G.D.O. Lowe, M.J. World, S.E. Humphries, et al. Human CRP Gene Polymorphism Influences CRP Levels: Implications for the Prediction and Pathogenesis of Coronary Heart Disease Arterioscler Thromb Vasc Biol, November 1, 2003; 23(11): 2063 - 2069. [Abstract] [Full Text] [PDF] |
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A. S. M. Shamsuzzaman, B. J. Gersh, and V. K. Somers Obstructive Sleep Apnea: Implications for Cardiac and Vascular Disease JAMA, October 8, 2003; 290(14): 1906 - 1914. [Abstract] [Full Text] [PDF] |
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A. D Timmis Plaque stabilisation in acute coronary syndromes: clinical considerations Heart, October 1, 2003; 89(10): 1268 - 1272. [Full Text] [PDF] |
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S. S Vasudevan, N. H.M Lopes, P. N Seshiah, T. Wang, C. B Marsh, D. J Kereiakes, C. Dong, and P. J Goldschmidt-Clermont Mac-1 and Fas activities are concurrently required for execution of smooth muscle cell death by M-CSF-stimulated macrophages Cardiovasc Res, September 1, 2003; 59(3): 723 - 733. [Abstract] [Full Text] [PDF] |
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S.-P. Yang, L.-J. Ho, Y.-L. Lin, S.-M. Cheng, T.-P. Tsao, D.-M. Chang, Y.-L. Hsu, C.-Y. Shih, T.-Y. Juan, and J.-H. Lai Carvedilol, a new antioxidative {beta}-blocker, blocks in vitro human peripheral blood T cell activation by downregulating NF-{kappa}B activity Cardiovasc Res, September 1, 2003; 59(3): 776 - 787. [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.P. Kopp, C.W. Kopp, A. Festa, K. Krzyzanowska, S. Kriwanek, E. Minar, R. Roka, and G. Schernthaner Impact of Weight Loss on Inflammatory Proteins and Their Association With the Insulin Resistance Syndrome in Morbidly Obese Patients Arterioscler Thromb Vasc Biol, June 1, 2003; 23(6): 1042 - 1047. [Abstract] [Full Text] [PDF] |
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A. Tomkins Assessing Micronutrient Status in the Presence of Inflammation J. Nutr., May 1, 2003; 133(5): 1649S - 1655. [Abstract] [Full Text] [PDF] |
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G. J. Blake and P. M. Ridker C-reactive protein and other inflammatory risk markers in acute coronary syndromes J. Am. Coll. Cardiol., February 19, 2003; 41(4_Suppl_S): 37S - 42S. [Abstract] [Full Text] [PDF] |
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E. J. Topol A guide to therapeutic decision-making in patients with non-ST-segment elevation acute coronary syndromes J. Am. Coll. Cardiol., February 19, 2003; 41(4_Suppl_S): 123S - 129S. [Abstract] [Full Text] [PDF] |
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S. Redondo, C. G. Santos-Gallego, P. Ganado, M. Garcia, L. Rico, M. Del Rio, and T. Tejerina Acetylsalicylic Acid Inhibits Cell Proliferation by Involving Transforming Growth Factor-{beta} Circulation, February 4, 2003; 107(4): 626 - 629. [Abstract] [Full Text] [PDF] |
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J. Kennedy and A.M. Buchan Ever Decreasing Circles: Advances in Antiplatelet Therapy and Anticoagulation Stroke, February 1, 2003; 34(2): 348 - 350. [Full Text] [PDF] |
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J. S. Forrester Prevention of Plaque Rupture: A New Paradigm of Therapy Ann Intern Med, November 19, 2002; 137(10): 823 - 833. [Abstract] [Full Text] [PDF] |
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J. Zhang, Y. Liu, J. Shi, D. F. Larson, and R. R. Watson Side-Stream Cigarette Smoke Induces Dose-Response in Systemic Inflammatory Cytokine Production and Oxidative Stress Experimental Biology and Medicine, October 1, 2002; 227(9): 823 - 829. [Abstract] [Full Text] [PDF] |
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T. P. Smith Atherosclerosis and Restenosis: An Inflammatory Issue Radiology, October 1, 2002; 225(1): 10 - 12. [Full Text] [PDF] |
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D. Nemet, Y. Oh, H.-S. Kim, M. Hill, and D. M. Cooper Effect of Intense Exercise on Inflammatory Cytokines and Growth Mediators in Adolescent Boys Pediatrics, October 1, 2002; 110(4): 681 - 689. [Abstract] [Full Text] [PDF] |
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D. L. Bhatt and E. J. Topol Need to Test the Arterial Inflammation Hypothesis Circulation, July 2, 2002; 106(1): 136 - 140. [Full Text] [PDF] |
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G.J. Blake and P.M. Ridker C-reactive protein and prognosis after percutaneous coronary intervention Eur. Heart J., June 2, 2002; 23(12): 923 - 925. [Full Text] [PDF] |
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J.M. Cotton, A. Mathur, Y. Hong, A.S. Brown, J.F. Martin, and J.D. Erusalimsky Acute rise of circulating vascular endothelial growth factor-A in patients with coronary artery disease following cardiothoracic surgery Eur. Heart J., June 2, 2002; 23(12): 953 - 959. [Abstract] [Full Text] [PDF] |
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P. R. Hebert, M. A. Pfeffer, and C. H. Hennekens Use of Statins and Aspirin to Reduce Risks of Cardiovascular Disease Journal of Cardiovascular Pharmacology and Therapeutics, June 1, 2002; 7(2): 77 - 80. [PDF] |
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R. S. Eidelman, G. A. Lamas, C. H. Hennekens, and P. M. Ridker Aspirin, Postmenopausal Hormones, and C-Reactive Protein Arch Intern Med, February 25, 2002; 162(4): 480 - 481. [Full Text] [PDF] |
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F Andreotti, I Porto, F Crea, and A Maseri Inflammatory gene polymorphisms and ischaemic heart disease: review of population association studies Heart, February 1, 2002; 87(2): 107 - 112. [Abstract] [Full Text] [PDF] |
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P. N. Seshiah, D. J. Kereiakes, S. S. Vasudevan, N. Lopes, B. Y. Su, N. A. Flavahan, and P. J. Goldschmidt-Clermont Activated Monocytes Induce Smooth Muscle Cell Death: Role of Macrophage Colony-Stimulating Factor and Cell Contact Circulation, January 15, 2002; 105(2): 174 - 180. [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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D. A. Vorchheimer and V. Fuster Inflammatory Markers in Coronary Artery Disease: Let Prevention Douse the Flames JAMA, November 7, 2001; 286(17): 2154 - 2156. [Full Text] [PDF] |
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G. J. Blake and P. M. Ridker Novel Clinical Markers of Vascular Wall Inflammation Circ. Res., October 26, 2001; 89(9): 763 - 771. [Abstract] [Full Text] [PDF] |
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K. SADAMATSU, H. SHIMOKAWA, H. TASHIRO, and K. YAMAMOTO Long term treatment with enalapril reduces plasma concentrations of macrophage colony stimulating factor in patients with coronary artery disease Heart, October 1, 2001; 86(4): 457a - 458. [Full Text] |
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T. A. Kent, V. M. Soukup, and R. H. Fabian Heterogeneity Affecting Outcome From Acute Stroke Therapy: Making Reperfusion Worse Stroke, October 1, 2001; 32(10): 2318 - 2327. [Abstract] [Full Text] [PDF] |
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P. A. Gum, M. Thamilarasan, J. Watanabe, E. H. Blackstone, and M. S. Lauer Aspirin Use and All-Cause Mortality Among Patients Being Evaluated for Known or Suspected Coronary Artery Disease: A Propensity Analysis JAMA, September 12, 2001; 286(10): 1187 - 1194. [Abstract] [Full Text] [PDF] |
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D. J Fleming, P. F Jacques, J. M Massaro, R. B D'Agostino Sr, P. W. Wilson, and R. J Wood Aspirin intake and the use of serum ferritin as a measure of iron status Am. J. Clinical Nutrition, August 1, 2001; 74(2): 219 - 226. [Abstract] [Full Text] [PDF] |
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J.C. Kaski and E.G. Zouridakis Inflammation, infection and acute coronary plaque events Eur. Heart J. Suppl., August 1, 2001; 3(suppl_I): I10 - I15. [Abstract] [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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L. S RALLIDIS, K. P THOMAIDIS, M. G ZOLINDAKI, A. H VELISSARIDOU, and E. G PAPASTERIADIS Elevated concentrations of macrophage colony stimulating factor predict worse in-hospital prognosis in unstable angina Heart, July 1, 2001; 86(1): 92 - 92. [Full Text] |
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M. Feldman, I. Jialal, S. Devaraj, and B. Cryer Effects of low-dose aspirin on serum C-reactive protein and thromboxane B2 concentrations: a placebo-controlled study using a highly sensitive C-reactive protein assay J. Am. Coll. Cardiol., June 15, 2001; 37(8): 2036 - 2041. [Abstract] [Full Text] [PDF] |
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K S Channer and P J Pugh Interfering with healing: the benefits of intervention during acute myocardial infarction Heart, June 1, 2001; 85(6): 620 - 622. [Full Text] |
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V. Pasceri, J. Chang, J. T. Willerson, and E. T. H. Yeh Modulation of C-Reactive Protein-Mediated Monocyte Chemoattractant Protein-1 Induction in Human Endothelial Cells by Anti-Atherosclerosis Drugs Circulation, May 29, 2001; 103(21): 2531 - 2534. [Abstract] [Full Text] [PDF] |
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I. Jialal, D. Stein, D. Balis, S. M. Grundy, B. Adams-Huet, and S. Devaraj Effect of Hydroxymethyl Glutaryl Coenzyme A Reductase Inhibitor Therapy on High Sensitive C-Reactive Protein Levels Circulation, April 17, 2001; 103(15): 1933 - 1935. [Abstract] [Full Text] [PDF] |
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M. Langlois, D. Duprez, J. Delanghe, M. De Buyzere, and D. L. Clement Serum Vitamin C Concentration Is Low in Peripheral Arterial Disease and Is Associated With Inflammation and Severity of Atherosclerosis Circulation, April 10, 2001; 103(14): 1863 - 1868. [Abstract] [Full Text] [PDF] |
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R. Voisard, R. Fischer, M. O{beta}wald, S. Voglic, R. Baur, M. Susa, W. Koenig, and V. Hombach Aspirin (5 mmol/L) Inhibits Leukocyte Attack and Triggered Reactive Cell Proliferation in a 3D Human Coronary In Vitro Model Circulation, March 27, 2001; 103(12): 1688 - 1694. [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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M. Cushman, J. P. Costantino, R. P. Tracy, K. Song, L. Buckley, J. D. Roberts, and D. N. Krag Tamoxifen and Cardiac Risk Factors in Healthy Women : Suggestion of an Anti-inflammatory Effect Arterioscler Thromb Vasc Biol, February 1, 2001; 21(2): 255 - 261. [Abstract] [Full Text] [PDF] |
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L. B. Goldstein, R. Adams, K. Becker, C. D. Furberg, P. B. Gorelick, G. Hademenos, M. Hill, G. Howard, V. J. Howard, B. Jacobs, et al. Primary Prevention of Ischemic Stroke : A Statement for Healthcare Professionals From the Stroke Council of the American Heart Association Circulation, January 2, 2001; 103(1): 163 - 182. [Full Text] [PDF] |
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L. B. Goldstein, R. Adams, K. Becker, C. D. Furberg, P. B. Gorelick, G. Hademenos, M. Hill, G. Howard, V. J. Howard, B. Jacobs, et al. Primary Prevention of Ischemic Stroke : A Statement for Healthcare Professionals From the Stroke Council of the American Heart Association Stroke, January 1, 2001; 32(1): 280 - 299. [Full Text] [PDF] |
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F.W.A. Verheugt How hot is inflammation in acute coronary syndrom? Eur. Heart J., December 2, 2000; 21(24): 1990 - 1992. [PDF] |
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A. Fischer, D. E Gutstein, Z. A Fayad, and V. Fuster Predicting plaque rupture: enhancing diagnosis and clinical decision-making in coronary artery disease Vascular Medicine, August 1, 2000; 5(3): 163 - 172. [Abstract] [PDF] |
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G. Sesmilo, B. M.K. Biller, J. Llevadot, D. Hayden, G. Hanson, N. Rifai, and A. Klibanski Effects of Growth Hormone Administration on Inflammatory and Other Cardiovascular Risk Markers in Men with Growth Hormone Deficiency: A Randomized, Controlled Clinical Trial Ann Intern Med, July 18, 2000; 133(2): 111 - 122. [Abstract] [Full Text] [PDF] |
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P. M. Ridker, N. Rifai, M. J. Stampfer, and C. H. Hennekens Plasma Concentration of Interleukin-6 and the Risk of Future Myocardial Infarction Among Apparently Healthy Men Circulation, April 18, 2000; 101(15): 1767 - 1772. [Abstract] [Full Text] [PDF] |
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