CLINICAL STUDY: INTERVENTIONAL CARDIOLOGY
Preprocedural C-reactive protein levels and cardiovascular events after coronary stent implantation
Dirk H. Walter, MDa,
Stephan Fichtlscherer, MDa,
Marc Sellwig, BSa,
Wolfgang Auch-Schwelk, MDa,
Volker Schächinger, MDa and
Andreas M. Zeiher, MDa
a Department of Internal Medicine IV, Division of Cardiology, University of Frankfurt, Frankfurt, Germany
Manuscript received February 9, 2000;
revised manuscript received September 29, 2000,
accepted November 3, 2000.
Reprint requests and correspondence: Dr. Dirk H. Walter, Department of Internal Medicine IV, Division of Cardiology, University of Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany
D.Walter{at}em.uni-frankfurt.de
 |
Abstract
|
|---|
OBJECTIVES
This study assessed the predictive value of preprocedural C-reactive protein (CRP) levels on six-month clinical and angiographic outcome in patients undergoing coronary stent implantation.
BACKGROUND
Recent data indicate that low-grade inflammation as detected by elevated CRP serum levels predicts the risk of recurrent coronary events.
METHODS
We prospectively investigated the predictive value of preprocedural CRP-levels on restenosis and six-month clinical outcome in 276 patients after coronary stent implantation. The primary combined end point was death due to cardiac causes, myocardial infarction related to the target vessel and repeat intervention of the stented vessel.
RESULTS
Grouping patients into tertiles according to preprocedural CRP-levels revealed that, despite identical angiographic and clinical characteristics at baseline and after stent implantation, a primary end point event occurred in 24 (26%) patients of the lowest tertile, in 42 (45.6%) of the middle tertile and in 38 (41.3%) of the highest CRP tertile, p = 0.01. On multivariate analysis, tertiles of CRP levels were independently associated with a higher risk of adverse coronary events (relative risk = 2.0 [1.1 to 3.5], tertile I vs. II and III, p = 0.01) in addition to the minimal lumen diameter after stent (p = 0.04). In addition, restenosis rates were significantly higher in the two upper tertiles compared with CRP levels in the lowest tertile (45.5% vs. 38.3% vs. 18.5%, respectively, p = 0.002).
CONCLUSIONS
Low-grade inflammation as evidenced by elevated preprocedural serum CRP-levels is an independent predictor of adverse outcome after coronary stent implantation, suggesting that a systemically detectable inflammatory activity is associated with proliferative responses within successfully implanted stents.
|
Abbreviations and Acronyms
| | CRP | = C-reactive protein | | MI | = myocardial infarction | | MLD | = minimal luminal diameter | | PTCA | = percutaneous transluminal coronary angioplasty | | RR | = relative risk | | TVR | = target vessel revascularization |
|
Atherosclerosis is believed to be a chronic inflammatory disease of the vessel wall (1). Recent data indicate that low-grade inflammation as detected by elevated C-reactive protein (CRP) serum levels predicts the risk of recurrent coronary events not only in patients with myocardial infarction (MI) (2,3), stable or unstable angina (4,5) but also in apparently healthy men (6). These observations suggest that an individual’s reactivity to inflammatory stimuli plays an important pathophysiologic role in coronary disease progression (7,8).
Coronary angioplasty (9) or coronary stent implantation (10) has been shown to elicit an inflammatory response by itself. In addition, preprocedural CRP levels appear to be a powerful predictor of both early and late outcome in patients undergoing conventional balloon angioplasty (11), suggesting that preprocedural activation of inflammatory cells may play a role in the modulation of vessel wall response to the injury induced by balloon angioplasty.
Stent implantation provides a useful model to assess the role of inflammation for atherosclerotic disease progression that is primarily determined by neointimal hyperplasia and not affected by the chronic shrinking process after conven-tional balloon angioplasty (12). In addition, stent implantation may modify the biological response of a dilated lesion by providing a more homogeneous lesion geometry compared with balloon dilation.
Therefore, we prospectively investigated the predictive value of preprocedural CRP-levels on six-month angiographic and clinical outcome in 276 consecutive patients undergoing coronary stent implantation.
|
Methods
|
|---|
Study population.
The study population consisted of 276 patients undergoing coronary stent implantation for objective evidence of ischemia in patients with angina. Indications for stenting were: coronary dissection after percutaneous transluminal coronary angioplasty (PTCA), suboptimal results ( 30% residual stenosis) after PTCA, lesions in venous bypass grafts and restenotic lesions. In addition, all patients undergoing percutaneous coronary intervention for acute MI were treated by stent implantation. All patients with a stent successfully inserted in the target lesion were included in the analysis except for those undergoing stent implantation during cardiogenic shock or as a bridge to emergency aortocoronary bypass surgery. Patients with intercurrent inflammatory conditions, local hematoma or malignancies were excluded. At the time of stenting, all patients were scheduled for a six-month follow-up angiogram, regardless of symptomatic status. All patients gave informed consent, and the study was approved by our institutional ethics committee.
Laboratory analysis.
In all patients, serum was collected immediately before the initial percutaneous coronary intervention after insertion of the arterial sheath for measuring CRP levels with a commercially available kit (Turbidimetric test, Boehringer Mannheim, Germany). The measuring range is 0.3 to 24 mg/dl, with intraassay variation coefficients ranging from 0.6% to 1.3% and interassay variations from 1.3% to 6% at different levels of CRP.
Stent implantation procedure.
Stent implantation was performed as previously described (13). In brief, all patients were on chronic aspirin (100 mg/day) therapy or received 500 mg of aspirin intravenously before the procedure. Fifteen thousand units of heparin was given after insertion of the arterial sheath, and if necessary, a repeat bolus of 5,000 U was administered to maintain the activated clotting time >250 s. Intracoronary glycerol trinitrate (0.2 to 0.3 mg) was given at the start of the procedure, before the final angiogram and before follow-up angiography. High-pressure balloon catheters were used for stent implantation with inflation pressures >10 atm. If necessary, multiple stents were used for complete coverage of the lesion.
Quantitative coronary angiography.
Quantitative measurements were assessed by fully computerized quantitative angiography (CMS, Medis, Nuenen, Netherlands) (14). Minimal luminal diameter (MLD), reference diameter and percent diameter stenosis were measured in identical views before PTCA, immediately after stent insertion and at follow-up. Lesions were classified according to the modified American College of Cardiology/American Heart Association criteria (15). Analyses were performed per patient (only one randomly selected lesion per subject). Stent restenosis was defined as a dichotomous outcome (50% diameter stenosis within the stent or stents at follow-up). Acute gain was defined as the difference between MLD after stent implantation and the MLD before PTCA. Late loss was defined as the difference between the MLD after stent insertion and the MLD at follow-up, and net gain was defined as the difference between acute gain and late loss.
Postprocedure medication protocol.
Ticlopidine 250 mg to 500 mg per day or Clopidogrel 75 mg/day (n = 15) was given for four weeks and aspirin 100 mg/day indefinitely. Glycoprotein IIb/IIIa inhibitors were administered in 15 patients (5.3%).
Definition of events and follow-up.
The primary combined end point was death due to cardiac causes, MI related to the target vessel and repeat intervention of the stented vessel (PTCA or aortocoronary bypass surgery). The diagnosis of MI was based on typical symptoms and electrocardiographic changes plus an increase in creatine kinase twice the upper limit of normal with a concomitant rise in the MB isoenzyme or a positive troponin T test. Blood samples were routinely drawn 24 h after the procedure in all patients to detect the occurrence of myocardial necrosis regardless of symptoms.
Thirty-day clinical follow-up and six-month follow-up was available in all 276 patients on an outpatient basis. The cumulative incidence of the primary combined end point, including death due to cardiac causes, MI related to the target vessel or repeat intervention of the stented vessel were assessed by Kaplan-Meier survival curves. Follow-up coronary angiograms to evaluate angiographic stent restenosis rates were performed in 229 of 267 (85.7%) patients eligible for planned reangiography between four and six months after stent placement. Patients who had no-control angiography were contacted to obtain clinical follow-up. Target vessel revascularization (TVR) was defined as repeat intervention of restenotic lesions, which included the target site of the stent implantation or proximal and distal in the same major coronary artery. Target vessel revascularization was driven by the presence of ischemia indicated either by the recurrence of typical symptoms of angina or a positive exercise stress test.
Data and statistical analysis.
Data are expressed as percentages for discrete variables and as mean ± standard deviation for continuous variables. C-reactive protein values were divided into tertiles and compared by Kruskal-Wallis test or by analysis of variance for multiple comparisons within all three groups. Categorical variables between two groups were compared by means of the chi-square test or Fisher exact test.
Continuous variables were tested for normal distribution with the Kolmogorov-Smirnov test and compared by means of Student t test. In case of nonnormal distribution, nonparametric methods were used (Mann-Whitney U test). Univariate and stepwise multivariate analysis was performed using the logistic regression model on SPSS version 8.0, SPSS Inc. All potential risk factors for stent restenosis were included. Chi-square analysis or logistic regression was used to estimate relative risk (RR) and 95% confidence intervals. Long-term clinical adverse events, death due to cardiac causes and MI of the target vessel were compared by Kaplan-Meier survival curves, and the corresponding p value was obtained from the log-rank test. Cumulative distribution curves of MLD before stenting, immediately after stenting and at follow-up were expressed as a function of CRP tertiles. For graphical reasons, the two upper tertiles were combined and compared with the lowest tertile of CRP values. Statistical significance was assumed at p < 0.05.
|
Results
|
|---|
Baseline characteristics.
The baseline clinical and procedural characteristics of the study population are summarized in Tables 1 and 2. Patients were grouped into tertiles according to the CRP values. Elevated CRP levels were defined as those in the two upper tertiles (0.5 mg/dl). The range of CRP values was 0.0 to 8.0 mg/dl.
Clinical parameters did not differ between the three tertiles of CRP, with the exception that significantly more patients with elevated levels of CRP (0.5 mg/dl) presented with an acute coronary syndrome (defined as unstable angina Braunwald class IIIB or acute MI, p = 0.02). In addition, more patients with CRP levels in tertiles II and III were diabetic. The quantitative angiographic data at baseline and immediately after coronary stent implantation are summarized in Table 3. Angiographic parameters were identical in all three groups.
Angiographic follow-up.
Table 4 summarizes the quantitative angiographic data obtained at follow-up angiography. Patients with elevated CRP levels had significantly higher restenosis rates. When the categorical criterion of 50% diameter stenosis at follow-up was used to assess restenosis development, the difference between the three groups was highly significant (p < 0.005), with a restenosis rate of 19% in the lowest tertile compared with 36.7% and 45.1% in the upper tertiles, respectively. Figure 1, illustrating the cumulative frequency distribution curves of the MLD, demonstrates that late lumen loss was significantly greater in the patients with elevated CRP levels (two upper tertiles 0.5 mg/dl) compared with patients in the lowest tertile (<0.5 mg/dl) as indicated by a leftward shift of the cumulative frequency distribution curve at follow-up angiography (Table 5).
View larger version (20K):
[in this window]
[in a new window]
|
Figure 1 Cumulative frequency distribution curves of the MLD for tertiles of CRP levels pre-, post-stent implantation and at six-month follow-up angiography. For graphical reasons, the two upper tertiles (0.5 mg/dl) were combined (dotted line with circles) and compared with the lowest tertile (<0.5 mg/dl). CRP = C-reactive protein; MLD = minimal lumen diameter.
|
|
Clinical follow-up.
Table 5 shows the major adverse events during the one- and six-month follow-up period. To account for local lesion-related outcomes, only MIs in the territory of the target vessel, TVR and death due to cardiac causes were included in the end point analysis. A primary end point event occurred in 24 (26%) patients of the lowest tertile, 42 (45.6%) patients of the middle tertile and in 38 (41.3%) patients of the highest CRP-tertile, p = 0.01. Thirteen early adverse events were observed within 30 days after stent implantation. No event (MI or death) occurred in the lowest tertile of CRP (<0.5 mg/dl). Importantly, subacute stent thrombosis occurred exclusively in patients with elevated CRP levels (upper tertiles). Six-month clinical follow-up was completed in all patients. At six months, MI or cardiac death occurred only in patients with preprocedural CRP levels 0.5 mg/dl (p = 0.01). None of the patients died of noncardiac causes. In addition, Figure 2 illustrates that survival free of MI and TVR was significantly worse in patients with elevated preprocedural CRP levels.
View larger version (13K):
[in this window]
[in a new window]
|
Figure 2 Long-term clinical adverse events (death due to cardiac causes, myocardial infarction of the target vessel and target vessel revascularization) within tertiles of CRP levels are compared by Kaplan-Meier survival curves, and the corresponding p value was obtained from the log-rank test. CRP = C-reactive protein.
|
|
Multivariate analysis.
Restenosis
Logistic regression analysis (Tables 6 and 7), including the classical previously described predictors of restenosis after coronary stent implantation, demonstrated that elevated preprocedural CRP levels are independently associated with increased restenosis rates (p = 0.006) in addition to MLD immediately after stent implantation (p = 0.04) and the number of stents implanted (p = 0.02), whereas reference segment diameter (p = 0.6), diabetes (p = 0.3) and total serum cholesterol levels (p = 0.3) did not independently predict subsequent restenosis development. Interestingly, the presence of an acute coronary syndrome that correlated with elevated CRP levels was not an independent predictor for subsequent recurrence rates (p = 0.9). Thus, independent of classical clinical and procedural risk factors, elevated preprocedural CRP serum levels are associated with an increased risk for in-stent restenosis, irrespective of the presence of an acute coronary syndrome before stenting (RR 3.6 [1.7 to 7.7], tertile III vs. I, p < 0.001).
Clinical events
Tertiles of CRP levels were also independently associated with a higher risk of adverse coronary events including MI, cardiac death and TVR (RR = 2.0 [1.1 to 3.5], tertile I vs. II and III, p = 0.01) in addition to the MLD after stent (p = 0.04). Since, in patients with acute MI, circulating CRP levels might be elevated due to myocardial necrosis, we repeated the analysis after excluding patients with acute MI. However, an almost identical RR of 2.3 ([1.2 to 4.2], tertile I vs. II and III, p = 0.006) was observed for elevated CRP levels in this subset of 208 patients, thus excluding a potential confounding effect of MI patients being more frequently distributed in the upper tertiles of CRP levels.
In contrast, stent length, reference vessel size, hypercholesterolemia, diabetes or acute coronary syndromes did not appear to be of predictive value for subsequent adverse events.
|
Discussion
|
|---|
The results of this study demonstrate that elevated preprocedural CRP levels are associated with enhanced restenosis development after coronary stent implantation. Most importantly, the increased restenosis rate associated with elevated CRP levels is accompanied by a worse event-free survival.
The results of this study extend previous observations, demonstrating the predictive value of measuring CRP levels for cardiovascular events after coronary interventions. In patients undergoing conventional single-vessel balloon angioplasty, preprocedural CRP levels have been shown to be a powerful predictor of early and late clinical outcome (11). In addition, in patients with stable angina and one-vessel disease, normalization of CRP plasma levels after coronary stenting identified patients who do not develop cardiovascular events (10). In line with a previous study in patients undergoing balloon angioplasty (11), in our population, no adverse coronary event such as MI or death within six months occurred in the subset of patients with CRP levels in the lowest tertile. Thus, preprocedural measurement of CRP levels might allow stratification of patients with respect to the individual risk for both early and late complications after coronary stent implantation.
Previous studies revealed that, in patients with unstable angina undergoing PTCA, increased baseline levels of acute-phase proteins are a marker for the hyperresponsiveness of the inflammatory system to nonspecific stimuli (9).
In-hospital complications after coronary stent implantation are mainly due to subacute stent thrombosis or occlusions caused by procedural parameters such as residual dissections (16,17). Indeed, in our study, all early complications after stent implantation within 30 days were events due to subacute thrombus formation at the stented site. Activation of inflammatory cells and cytokines can aggravate local thrombotic complications by increasing procoagulant or platelet activity or promoting thrombin generation (18–20). The finding of this study, that subacute stent thrombosis was exclusively observed in patients with elevated CRP levels, suggests an important role for low-grade systemic inflammation to amplify local thrombotic complications in patients undergoing coronary stent implantation (21).
Although the presence of an acute coronary syndrome correlated with elevated baseline CRP levels, by multivariate analysis it was not an independent predictor for subsequent clinical and angiographic outcome in our patient population consisting of a consecutive series of patients with various clinical conditions, including stable and unstable angina as well as MI. Likewise, diabetes did not appear to be an independent predictor, once preprocedural CRP levels were included in the analysis. Thus, since elevated CRP levels cluster in patients with diabetes (22), it is tempting to speculate that the systemic inflammatory activity as measured by CRP serum levels might be more informative than classical risk factors with respect to predicting the clinical and angiographic outcome after coronary stent implantation.
Experimental and clinical studies demonstrated that a systemic inflammatory reaction plays a pivotal role for neointima formation within stents in addition to the local vessel wall injury with the subsequent release of chemotactic and growth factors (9,23). Stent implantation has been shown to provide superior late results compared with conventional balloon angioplasty (24,25), which has been attributed to the elimination of chronic vessel wall shrinkage even at the expense of increased neointimal proliferation. Thus, coronary stent implantation provides an ideal scenario to assess the role of inflammation in atherosclerotic disease progression that is primarily determined by neointimal hyperplasia and not affected by a chronic shrinking process after conventional balloon angioplasty (12). In addition, stenting provides a more homogenous lesion geometry by covering plaque fractures and reducing exposure of atheromatous material, which might locally modify the biological response of a dilated lesion. However, the concordant finding that preprocedural CRP levels predict clinical and angiographic outcome both after balloon dilation (11) and after stent implantation suggests that—in both conditions—the preprocedural activation of inflammatory cells (26) may play a major role in the modulation of the vessel-wall response to injury.
Study limitations.
In this study, CRP values were measured by a turbidimetric method and not with the recently recommended latex-enhanced high-sensitive CRP assay. However, comparison of the two assays in our institution not only revealed a very close correlation but, more importantly, demonstrated that CRP levels 0.5 mg/dl (upper limit of the lowest tertile) can be reliably detected using the turbidimetric method (data not shown). Although we achieved a high repeat angiography rate of 85.7%, we cannot fully exclude a potential bias related to incomplete angiographic follow-up. However, such bias is unlikely to be of relevance since the prospective design of the study allowed to assure that the patients without angiographic follow-up did not differ with respect to CRP distribution and clinical outcome.
Conclusions.
Our study shows that low-grade inflammation measured by elevated preprocedural CRP-levels is an important and independent predictor of acute and six-month adverse outcome after coronary stent implantation, suggesting that a systemic inflammatory activity is associated with thrombotic and proliferative responses within successfully implanted stents.
Measurement of CRP levels could provide a rationale for risk stratification before coronary intervention and, thus, may offer a useful tool to target aggressive antiaggregatory or anti-inflammatory therapy to patients that are exposed to the highest risk for ischemic complications or restenosis development after coronary stent implantation.
|
Acknowledgments
|
|---|
The authors gratefully acknowledge the expert technical assistance of Beate Jung and Marga Müller-Ardogan.
|
References
|
|---|
1. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–126[Free Full Text]
2. Ridker PM, Glynn RJ, Hennekens CH. C-reactive protein adds to the predictive value of total and HDL cholesterol in determining risk of first myocardial infarction. Circulation. 1998;97:2007–2011[Abstract/Free Full Text]
3. Ridker PM, Rifai N, Pfeffer MA, et al. 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[Abstract/Free Full Text]
4. Haverkate F, Thompson SG, Pyke SD, Gallimore JR, Pepys MB. Production of C-reactive protein and risk of coronary events in stable and unstable angina. European Concerted Action on Thrombosis and Disabilities Angina Pectoris study group. Lancet. 1997;349:462–466[CrossRef][Medline]
5. Liuzzo G, Biasucci LM, Gallimore JR, et al. The prognostic value of C-reactive protein and serum amyloid A protein in severe unstable angina. N Engl J Med. 1994;331:417–424[Abstract/Free Full Text]
6. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH. Inflammation, aspirin and the risk of cardiovascular disease in apparently healthy men. N Engl J Med. 1997;336:973–979[Abstract/Free Full Text]
7. Libby P, Ridker PM. Novel inflammatory markers of coronary risk: theory versus practice. Circulation. 1999;100:1148–1150[Free Full Text]
8. Lagrand WK, Visser CA, Hermens WT, et al. C-reactive protein as a cardiovascular risk factor: more than an epiphenomenon? Circulation. 1999;100:96–102[Abstract/Free Full Text]
9. Liuzzo G, Buffon A, Biasucci LM, et al. Enhanced inflammatory response to coronary angioplasty in patients with severe unstable angina. Circulation. 1998;98:2370–2376[Abstract/Free Full Text]
10. Gaspardone A, Crea F, Versaci F, et al. Predictive value of C-reactive protein after successful coronary-artery stenting in patients with stable angina. Am J Cardiol. 1998;82:515–518[CrossRef][Medline]
11. Buffon A, Liuzzo G, Biasucci LM, et al. Preprocedural serum levels of C-reactive protein predict early complications and late restenosis after coronary angioplasty. J Am Coll Cardiol. 1999;34:1512–1521[Abstract/Free Full Text]
12. Hoffmann R, Mintz GS, Dussaillant GR, et al. Patterns and mechanisms of in-stent restenosis: a serial intravascular ultrasound study. Circulation. 1996;94:1247–1254[Abstract/Free Full Text]
13. Walter DH, Schachinger V, Elsner M, Dimmeler S, Zeiher AM. Platelet glycoprotein IIIa polymorphisms and risk of coronary stent thrombosis. Lancet. 1997;350:1217–1219[CrossRef][Medline]
14. Reiber JH, Serruys PW, Kooijman CJ, et al. Assessment of short-, medium- and long-term variations in arterial dimensions from computer-assisted quantitation of coronary cineangiograms. Circulation. 1985;71:280–288[Abstract/Free Full Text]
15. Schachinger V, Allert M, Kasper W, Just H, Vach W, Zeiher AM. Adjunctive intracoronary infusion of antithrombin III during percutaneous transluminal coronary angioplasty: results of a prospective, randomized trial. Circulation. 1994;90:2258–2266[Abstract/Free Full Text]
16. Schuhlen H, Kastrati A, Dirschinger J, et al. Intracoronary stenting and risk for major adverse cardiac events during the first month. Circulation. 1998;98:104–111[Abstract/Free Full Text]
17. Baim DS, Carrozza JP Jr. Stent thrombosis: closing in on the best preventive treatment. Circulation. 1997;95:1098–1100[Free Full Text]
18. Ott I, Neumann FJ, Kenngott S, Gawaz M, Schomig A. Procoagulant inflammatory responses of monocytes after direct balloon angioplasty in acute myocardial infarction. Am J Cardiol. 1998;82:938–942[CrossRef][Medline]
19. Inoue T, Hoshi K, Yaguchi I, Iwasaki Y, Takayanagi K, Morooka S. Serum levels of circulating adhesion molecules after coronary angioplasty. Cardiology. 1999;91:236–242[CrossRef][Medline]
20. Oltrona L, Eisenberg PR, Lasala JM, Sewall DJ, Shelton ME, Winters KJ. Association of heparin-resistant thrombin activity with acute ischemic complications of coronary interventions. Circulation. 1996;94:2064–2071[Abstract/Free Full Text]
21. Neumann FJ, Kastrati A, Miethke T, Pogatsa-Murray G, Seyfarth M, Mig A. Previous cytomegalovirus infection and risk of coronary thrombotic events after stent placement. Circulation. 2000;101:11–13[Abstract/Free Full Text]
22. Ford ES. Body mass index, diabetes and C-reactive protein among U.S. adults. Diabetes Care. 1999;22:1971–1977[Abstract/Free Full Text]
23. Kornowski R, Hong MK, Tio FO, Bramwell O, Wu H, Leon MB. In-stent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J Am Coll Cardiol. 1998;31:224–230[Abstract/Free Full Text]
24. Serruys PW, de Jaegere P, Kiemeneij F, et al. A comparison of balloon-expandable stent implantation with balloon angioplasty in patients with coronary artery disease: Benestent study group. N Engl J Med. 1994;331:489–495[Abstract/Free Full Text]
25. Fischman DL, Leon MB, Baim DS, et al. A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease: stent restenosis study investigators. N Engl J Med. 1994;331:496–501[Abstract/Free Full Text]
26. Pietersma A, Kofflard M, de Wit LE, et al. Late lumen loss after coronary angioplasty is associated with the activation status of circulating phagocytes before treatment. Circulation. 1995;91:1320–1325[Abstract/Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
S. G. Ellis and S. Anwaruddin
Recapturing the Magic: Revisiting the Pleiotropic Effects of Statins in Percutaneous Coronary Revascularization
J. Am. Coll. Cardiol.,
July 1, 2009;
(2009)
j.jacc.2009.04.070v1.
[Full Text]
[PDF]
|
|
|
|
|
|
|
R Iijima, R A Byrne, G Ndrepepa, S Braun, J Mehilli, P B Berger, A Schomig, and A Kastrati
Pre-procedural C-reactive protein levels and clinical outcomes after percutaneous coronary interventions with and without abciximab: pooled analysis of four ISAR trials
Heart,
January 15, 2009;
95(2):
107 - 112.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D.-W. Park, C. W. Lee, S.-C. Yun, Y.-H. Kim, M.-K. Hong, J.-J. Kim, S.-W. Park, and S.-J. Park
Prognostic impact of preprocedural C reactive protein levels on 6-month angiographic and 1-year clinical outcomes after drug-eluting stent implantation
Heart,
September 1, 2007;
93(9):
1087 - 1092.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. M. Ridker
C-Reactive Protein and the Prediction of Cardiovascular Events Among Those at Intermediate Risk: Moving an Inflammatory Hypothesis Toward Consensus
J. Am. Coll. Cardiol.,
May 29, 2007;
49(21):
2129 - 2138.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Assmus, D. H. Walter, R. Lehmann, J. Honold, H. Martin, S. Dimmeler, A. M. Zeiher, and V. Schachinger
Intracoronary infusion of progenitor cells is not associated with aggravated restenosis development or atherosclerotic disease progression in patients with acute myocardial infarction
Eur. Heart J.,
December 2, 2006;
27(24):
2989 - 2995.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Cappabianca, D. Paparella, G. Visicchio, G. Capone, G. Lionetti, F. Numis, P. Ferrara, C. D'Agostino, and L. de Luca Tupputi Schinosa
Preoperative C-Reactive Protein Predicts Mid-Term Outcome After Cardiac Surgery
Ann. Thorac. Surg.,
December 1, 2006;
82(6):
2170 - 2178.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Libby and P. M. Ridker
Inflammation and Atherothrombosis: From Population Biology and Bench Research to Clinical Practice
J. Am. Coll. Cardiol.,
October 27, 2006;
48(9_Suppl_A):
A33 - A46.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Groschel, U. Ernemann, J. B. Schulz, T. Nagele, C. Terborg, and A. Kastrup
Statin Therapy at Carotid Angioplasty and Stent Placement: Effect on Procedure-related Stroke, Myocardial Infarction, and Death.
Radiology,
July 1, 2006;
240(1):
145 - 151.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Susen, K. Sautiere, F. Mouquet, F. Cuilleret, A. Chmait, E. P. McFadden, B. Hennache, F. Richard, P. de Groote, J.-M. Lablanche, et al.
Serum hepatocyte growth factor levels predict long-term clinical outcome after percutaneous coronary revascularization
Eur. Heart J.,
November 2, 2005;
26(22):
2387 - 2395.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S.-J. Park
Inflammatory Biomarkers for Prediction of Outcomes After Unprotected Left Main Coronary Intervention
Circulation,
October 11, 2005;
112(15):
2226 - 2227.
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Palmerini, A. Marzocchi, C. Marrozzini, P. Ortolani, F. Saia, L. Bacchi-Reggiani, S. Virzi, S. Gianstefani, and A. Branzi
Preprocedural Levels of C-Reactive Protein and Leukocyte Counts Predict 9-Month Mortality After Coronary Angioplasty for the Treatment of Unprotected Left Main Coronary Artery Stenosis
Circulation,
October 11, 2005;
112(15):
2332 - 2338.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. P Marso, J. W Murphy, J. A House, D. M Safley, and W. S Harris
Metabolic syndrome-mediated inflammation following elective percutaneous coronary intervention
Diabetes and Vascular Disease Research,
February 1, 2005;
2(1):
31 - 36.
[Abstract]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
K. Toutouzas, A. Colombo, and C. Stefanadis
Inflammation and restenosis after percutaneous coronary interventions
Eur. Heart J.,
October 1, 2004;
25(19):
1679 - 1687.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. Morrow
Preprocedural C-Reactive Protein for Risk Prediction Before Percutaneous Coronary Intervention (PCI): A US Perspective
Clin. Chem.,
September 1, 2004;
50(9):
1489 - 1491.
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Biasucci and G. G.L. Biondi-Zoccai
Preprocedural C-Reactive Protein for Risk Prediction Before Percutaneous Coronary Intervention (PCI): A European Perspective
Clin. Chem.,
September 1, 2004;
50(9):
1492 - 1494.
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Z.H. Rittersma, R. J. de Winter, K. T. Koch, C. E. Schotborgh, M. Bax, G. S. Heyde, J. P. van Straalen, K. J. Mulder, J. G.P. Tijssen, G. T. Sanders, et al.
Preprocedural C-Reactive Protein Is Not Associated with Angiographic Restenosis or Target Lesion Revascularization after Coronary Artery Stent Placement
Clin. Chem.,
September 1, 2004;
50(9):
1589 - 1596.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Pasceri, G. Patti, A. Nusca, C. Pristipino, G. Richichi, G. Di Sciascio, and on behalf of the ARMYDA Investigators
Randomized Trial of Atorvastatin for Reduction of Myocardial Damage During Coronary Intervention: Results From the ARMYDA (Atorvastatin for Reduction of MYocardial Damage during Angioplasty) Study
Circulation,
August 10, 2004;
110(6):
674 - 678.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Segev, S. Kassam, C. E Buller, H. K Lau, J. D Sparkes, P. W Connelly, P. H Seidelin, M. K Natarajan, E. A Cohen, and B. H Strauss
Pre-procedural plasma levels of C-reactive protein and interleukin-6 do not predict late coronary angiographic restenosis after elective stenting
Eur. Heart J.,
June 2, 2004;
25(12):
1029 - 1035.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M N Zairis, J A Ambrose, A G Lyras, M A Thoma, P K Psarogianni, P G Psaltiras, A D Kardoulas, G P Bibis, E G Pissimissis, P C Batika, et al.
C Reactive protein, moderate alcohol consumption, and long term prognosis after successful coronary stenting: four year results from the GENERATION study
Heart,
April 1, 2004;
90(4):
419 - 424.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Y. Hsue, K. Giri, S. Erickson, J. S. MacGregor, N. Younes, A. Shergill, and D. D. Waters
Clinical Features of Acute Coronary Syndromes in Patients With Human Immunodeficiency Virus Infection
Circulation,
January 27, 2004;
109(3):
316 - 319.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. D. Danenberg, G. Golomb, A. Groothuis, J. Gao, H. Epstein, R. V. Swaminathan, P. Seifert, and E. R. Edelman
Liposomal Alendronate Inhibits Systemic Innate Immunity and Reduces In-Stent Neointimal Hyperplasia in Rabbits
Circulation,
December 2, 2003;
108(22):
2798 - 2804.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Biancari, J. Lahtinen, S. Lepojarvi, P. Rainio, E. Salmela, R. Pokela, M. Lepojarvi, J. Satta, and T. S. Juvonen
Preoperative C-reactive protein and outcome after coronary artery bypass surgery
Ann. Thorac. Surg.,
December 1, 2003;
76(6):
2007 - 2012.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Verma, M. V. Badiwala, R. D. Weisel, S.-H. Li, C.-H. Wang, P. W. M. Fedak, R.-K. Li, and D. A. G. Mickle
C-reactive protein activates the nuclear factor-{kappa}B signal transduction pathway in saphenous vein endothelial cells: implications for atherosclerosis and restenosis
J. Thorac. Cardiovasc. Surg.,
December 1, 2003;
126(6):
1886 - 1891.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T.-M. Lu, Y.-A. Ding, S.-J. Lin, W.-S. Lee, and H.-C. Tai
Plasma levels of asymmetrical dimethylarginine and adverse cardiovascular events after percutaneous coronary intervention
Eur. Heart J.,
November 1, 2003;
24(21):
1912 - 1919.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. M. Rahel, F. L.J. Visseren, M.-J. Suttorp, T. H.W. Plokker, J. C. Kelder, B. M. de Jongh, K.P. Bouter, and R. J.A. Diepersloot
Preprocedural serum levels of acute-phase reactants and prognosis after percutaneous coronary intervention
Cardiovasc Res,
October 15, 2003;
60(1):
136 - 140.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. W. Chan, D. J. Moliterno, P. B. Berger, G. W. Stone, P. M. DiBattiste, S. L. Yakubov, S. K. Sapp, K. Wolski, D. L. Bhatt, E. J. Topol, et al.
Triple antiplatelet therapy during percutaneous coronary intervention is associated withimproved outcomes including one-year survival: Results from the do tirofiban and reoprogive similar efficacy outcome trial (TARGET)
J. Am. Coll. Cardiol.,
October 1, 2003;
42(7):
1188 - 1195.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. G. Hackam and S. S. Anand
Emerging Risk Factors for Atherosclerotic Vascular Disease: A Critical Review of the Evidence
JAMA,
August 20, 2003;
290(7):
932 - 940.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. W. Chan, D. L. Bhatt, D. P. Chew, J. Reginelli, J. P. Schneider, E. J. Topol, and S. G. Ellis
Relation of Inflammation and Benefit of Statins After Percutaneous Coronary Interventions
Circulation,
April 8, 2003;
107(13):
1750 - 1756.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A.J.J IJsselmuiden, P.W Serruys, A Scholte, F Kiemeneij, T Slagboom, L.R v/d Wieken, G.J Tangelder, and G.J Laarman
Direct coronary stent implantation does not reduce the incidence of in-stent restenosis or major adverse cardiac events: Six month results of a randomized trial
Eur. Heart J.,
March 1, 2003;
24(5):
421 - 429.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Versaci, A. Gaspardone, F. Tomai, F. Ribichini, P. Russo, I. Proietti, A. S. Ghini, V. Ferrero, L. Chiariello, P. Agostino Gioffre, et al.
Immunosuppressive therapy for the prevention of restenosis after coronary artery stent implantation (IMPRESS study)
J. Am. Coll. Cardiol.,
December 4, 2002;
40(11):
1935 - 1942.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. N. Zairis, J. A. Ambrose, S. J. Manousakis, A. S. Stefanidis, O. A. Papadaki, H. I. Bilianou, M. C. DeVoe, C. N. Fakiolas, E. G. Pissimissis, C. D. Olympios, et al.
The impact of plasma levels of C-reactive protein, lipoprotein (a) and homocysteine on the long-term prognosis after successful coronary stenting: The global evaluation of new events and restenosis after stent implantation study
J. Am. Coll. Cardiol.,
October 16, 2002;
40(8):
1375 - 1382.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. P. Smith
Atherosclerosis and Restenosis: An Inflammatory Issue
Radiology,
October 1, 2002;
225(1):
10 - 12.
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
D. H. Walter, S. Fichtlscherer, M. B. Britten, P. Rosin, W. Auch-Schwelk, V. Schachinger, and A. M. Zeiher
Statin therapy, inflammation and recurrent coronary events in patients following coronary stent implantation
J. Am. Coll. Cardiol.,
December 1, 2001;
38(7):
2006 - 2012.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
Top
Abstract
Methods