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Circulation. 2002;106:679-684
Published online before print July 15, 2002, doi: 10.1161/01.CIR.0000025403.20953.23
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(Circulation. 2002;106:679.)
© 2002 American Heart Association, Inc.


Clinical Investigation and Reports

Effect of Rosiglitazone Treatment on Nontraditional Markers of Cardiovascular Disease in Patients With Type 2 Diabetes Mellitus

Steven M. Haffner, MD; Andrew S. Greenberg, MD; Wayde M. Weston, PhD; Hongzi Chen, PhD; Ken Williams, MS; Martin I. Freed, MD

From University of Texas Health Science Center at San Antonio (S.M.H., K.W.), San Antonio, Tex; Tufts-New England Medical Center (A.S.G.), Boston, Mass; and GlaxoSmithKline (W.M.W., H.C., M.I.F.), Collegeville, Philadelphia, Pa.

Correspondence to Steven M. Haffner, MD, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, MC 7873, San Antonio, TX 78229-3900. E-mail haffner{at}uthscsa.edu


*    Abstract
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Background Markers of systemic inflammation (eg, C-reactive protein [CRP] and interleukin-6 [IL-6]) have been proposed to be "nontraditional" risk factors for cardiovascular disease in patients with type 2 diabetes mellitus. Matrix metalloproteinase-9 (MMP-9) has been implicated in the pathogenesis of atherosclerotic plaque rupture, which raises the possibility of the use of MMP-9 levels as a marker for future myocardial infarction or unstable angina. In vitro and animal studies suggest that thiazolidinediones can reduce the expression of these markers. The purpose of this analysis was to determine whether rosiglitazone alters serum concentrations of CRP, IL-6, MMP-9, and white blood cell count (WBC) and to examine the relationship of these effects with demographic and disease variables.

Methods and Results CRP, IL-6, MMP-9, and WBC were analyzed from stored frozen serum samples obtained from patients with type 2 diabetes who completed a 26-week randomized, double-blind, placebo-controlled study. After 26 weeks of rosiglitazone treatment, the percentage reductions in mean CRP, MMP-9, and WBC levels were statistically significant compared with baseline and placebo (P<0.01). The percentage reduction in mean IL-6 was small and similar in the rosiglitazone and placebo groups. The change in each inflammatory marker from baseline to week 26 was significantly correlated (P<0.05) with each of the other markers, as well as with the homeostasis model assessment estimate of insulin resistance.

Conclusions Rosiglitazone reduces serum levels of MMP-9 and the proinflammatory marker CRP in patients with type 2 diabetes, which indicates potentially beneficial effects on overall cardiovascular risk.


Key Words: atherosclerosis • cardiovascular diseases • diabetes mellitus • inflammation • risk factors


*    Introduction
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Cardiovascular disease (CVD) accounts for {approx}50% of all deaths worldwide. Type 2 diabetes mellitus is one of the most potent independent risk factors for the development of CVD and is seemingly related to accelerated atherosclerosis compared with the nondiabetic population.1,2 It is clear that alterations in traditional risk factors (eg, abnormal lipids and raised blood pressure) alone cannot explain the excess incidence of CVD in patients with type 2 diabetes.3

There is increasing recognition that chronic subclinical vascular inflammation plays a role in the pathogenesis of atherosclerosis, insulin resistance, and type 2 diabetes.46 Markers of subclinical inflammation, in particular C-reactive protein (CRP) and interleukin-6 (IL-6), have been shown to be powerful independent predictors of diabetes and CVD risk.5,7,8 In addition, elevated white blood cell count (WBC) may be a marker for inflammation and may predict future coronary heart disease and mortality.9

Preclinical studies demonstrate that peroxisome proliferator-activated receptor-{gamma} (PPAR-{gamma}) agonists may affect inflammatory pathways through transcriptional mechanisms. These effects, seen in monocytes, macrophages, T-lymphocytes, and vascular smooth muscle cells, include decreases in cytokines, chemokines, and matrix metalloproteinases (MMPs).10 Treatment with troglitazone, a PPAR-{gamma} agonist, is associated with declines in plasminogen activator inhibitor-1 levels.11 Taken together, these anti-inflammatory effects raise the prospect of reduced cardiovascular risk, either through improved metabolism or directly by activation of PPAR-{gamma} in vascular or atherosclerosis-associated cells.12 To follow up these preclinical observations, we investigated the effects of rosiglitazone (RSG) on markers of inflammation (CRP and IL-6) and plaque stability (MMP-9) in patients with type 2 diabetes. Effects on WBC were analyzed as well. Potential relationships between effects on these markers and variables associated with type 2 diabetes were also examined.


*    Methods
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Subject Material
Serum biomarkers were analyzed with samples obtained from 357 patients with type 2 diabetes mellitus who completed a 26-week randomized, double-blind, placebo-controlled study to assess the efficacy and safety of RSG (4 or 8 mg/d).13 Patients received instruction on a weight-maintenance diet throughout the study. Prior antidiabetic medications taken by patients were discontinued for a minimum of 4 weeks before randomization. Serum samples were obtained on the day of randomization (baseline) and at week 26 and stored at -70°C until analyzed.

Analyses
Serum levels of IL-6 and MMP-9 were measured by ELISA (R&D Systems), and serum levels of CRP were assayed by another ELISA (Diagnostic Systems Laboratory Inc). Baseline and week 26 paired samples for any patient were assayed in the same batch to minimize interassay variability. The marker of insulin resistance, homeostasis model assessment estimate of insulin resistance (HOMA-IR),14 is defined as follows: equation


Statistical Analyses
Within-treatment comparisons of mean change from baseline to week 26 of CRP, MMP-9, IL-6, and WBC levels; point estimates; and 95% CIs were presented for different treatment groups. For the assessment of differences between each RSG dosage group and placebo group with regard to continuous variables, an ANCOVA (using PROC MIXED in SAS software) with terms for treatment and baseline measurement was used that was based on log-transformed data. To determine whether analysis of only those who completed the study might bias our results, the same comparisons were also made for the study population as a whole. Patients missing values for an analyte were assumed to have had no change in that analyte.15

Pearson correlation coefficients were calculated to examine the relationships of analyte levels at baseline with prespecified disease and metabolic variables (Table 1). Correlations were determined for baseline variables (Table 2) and the relationship of percentage changes from baseline to week 26 with CRP, IL-6, MMP-9, and WBC with the prespecified changes in metabolic variables (Table 3). Baseline levels of analytes and the changes in analytes were nonnormally distributed; therefore, log-transformed data were used for determination of Pearson correlation coefficients.


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Table 1. Demography and Baseline Characteristics


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Table 2. Baseline Pearson Correlations in the Entire Population (n=357)


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Table 3. Pearson Correlations in Changes Among All Individuals


*    Results
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Each treatment group displayed similar demographic and baseline characteristics (Table 1), and there was no difference between this patient cohort and the original intent-to-treat study population (n=493) in terms of the magnitude of improvement in mean [SD] of glycosylated hemoglobin (HbA1c; RSG 4 mg/d, -0.6% [1.2%]; RSG 8 mg/d, -0.9% [1.2%]; placebo 0.6% [1.1%]) and fasting plasma glucose (RSG 4 mg/d, -2.5 [2.6] mmol/L; RSG 8 mg/d, -3.1 [2.9] mmol/L; placebo 0.2 [2.6] mmol/L).13 Median CRP levels were higher in women than in men (0.76 versus 0.39 mg/dL, P<0.001). There were no sex differences in IL-6, WBC, or MMP-9 levels.

Relationship of Baseline Values With Metabolic and Disease Variables
As shown in Table 2, the natural logarithm (ln) of CRP was significantly (P<0.001) correlated with ln IL-6 (r=0.44) and ln MMP-9 (r=0.17) at baseline. Baseline ln CRP and ln IL-6 both correlated positively with body mass index (r=0.30 and r=0.11, respectively) and WBC (r=0.28 and r=0.27, respectively). Ln CRP was correlated with ln HOMA-IR (r=0.21), as was reported in other studies.6 Additionally, ln HOMA-IR was correlated with WBC (r=0.13) and ln IL-6 (r=0.13). Baseline ln MMP-9 showed a statistically significant positive correlation with baseline ln WBC (r=0.47) but was only weakly correlated with baseline triglycerides (r=0.07) and LDL cholesterol (r=0.07).

Effects of RSG Treatment on Weight, CRP, IL-6, MMP-9, and WBC
After 26 weeks of RSG treatment, patients in the placebo group lost 1.1 kg as opposed to a 1.8-kg increase in the RSG 4 mg/d group and a 3.5-kg increase in the RSG 8 mg/d group (P<0.001 compared with baseline). Both RSG treatment groups showed statistically significant (P<0.05) mean percentage reductions in CRP levels from baseline and placebo (Figure, A). The reductions in CRP did not appear to be dose related. There was no significant difference between the percentage reductions in CRP in the RSG 4- and 8-mg/d groups. After adjustment for the greater weight increases in the RSG groups, the decline in CRP was -0.15 mg/dL in the placebo group, -0.52 mg/dL in the RSG 4-mg/d group, and -0.54 mg/dL in the RSG 8-mg/d group. There was no significant percentage change in CRP from baseline in the placebo group (Figure, A). Mean percentage changes in IL-6 level were small and similar between the RSG and placebo groups (Figure, B). Statistically significant (P<0.05) and dose-ordered reductions from baseline and placebo were observed for MMP-9 in the RSG treatment groups, whereas no change was observed in the placebo group (Figure, C). WBC also declined significantly with RSG (Figure, D).



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Effect of RSG on levels of CRP (A), IL-6 (B), MMP-9 (C), and WBC (D). All percentages represent 1 subtracted from antilogs of mean difference between baseline and week 26 log-transformed levels.

To determine whether focusing this analysis on only those who completed the study introduced a bias into the results, the analysis of changes from baseline and treatment effects was repeated with the total study population (n=493), assuming no change from baseline to week 26 where analytical values were missing. As expected, this secondary analysis of the data also demonstrated slightly smaller but still significant reductions from baseline and placebo for CRP and MMP-9 in both RSG treatment groups compared with the analysis shown in the Figure.

Correlations Between Changes From Baseline to Week 26 in CRP, IL-6, and MMP-9 and Metabolic Variables
The change in ln CRP from baseline to week 26 was significantly (P<0.05) positively correlated with changes in IL-6 (r=0.53), MMP-9 (r=0.19), WBC (r=0.19), and HOMA-IR (r=0.13) and inversely correlated with changes in HDL cholesterol (r=-0.17; Table 3). The change in MMP-9 was significantly correlated with change in IL-6 (r=0.22), WBC (r=0.40), HbA1c (r=0.14), fasting plasma glucose (r=0.19), and free fatty acids (r=0.11). Change in IL-6 was correlated with change in WBC (r=0.36), HDL cholesterol (r=-0.12), and HOMA-IR (r=0.09). Multivariate analyses of the change from weeks 0 to 26 also illustrated that the strongest correlates of change were between CRP, MMP-9, WBC, and IL-6 (data not shown).


*    Discussion
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*Discussion
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These data show that RSG treatment significantly reduced serum CRP, MMP-9, and WBC compared with placebo. Elevation in CRP levels has been associated with both the development of type 2 diabetes and an increased risk of CVD.58,16 MMPs, in addition to being a known acute-phase reactant that increases inflammation, have also been implicated in plaque rupture.17 Interestingly, thiazolidinediones have been shown to decrease MMP-9 expression in vascular smooth muscle cells,10 with evidence for a transcriptional mechanism demonstrated by changes in protein and mRNA levels. Despite these intriguing data, there is no evidence to suggest elevated serum MMP-9 levels reflect MMP-9 levels in the arterial walls and only limited evidence to suggest an increased propensity for plaque rupture. Increased blood levels of MMP-9 have been reported in premature atherosclerosis18 and in patients with acute coronary syndrome.19 After the initiation of cardiopulmonary bypass (a high-stress condition), circulating MMP-9 increased more than 6-fold.20 Reductions of MMP-9, CRP, and WBC could thus possibly be interpreted as reflecting a reduction in overall CVD risk, although this possibility should be tested in clinical controlled studies.

The percentage reductions in CRP with RSG in the present study were of a similar magnitude to those seen with the lipid-lowering statins.21 However, patients in the present study were diabetic and were more obese than in the typical CRP study with statins,21 and direct comparisons between the effect of statins and PPAR-{gamma} agonists in CRP levels should be done with a factorial study design. It is possible that the decrease of CRP in obese diabetic patients could reflect changes in insulin resistance rather than a vasculoprotective effect. Changes in CRP were independent of changes in LDL cholesterol, similar to the effect of statins on CRP. Additionally, RSG treatment effects on CRP and MMP-9 were still evident in a second, more conservative analysis of the study data in which patients with missing values were assumed to have no change in that parameter, which increases our confidence in these results.

CRP levels in the present report were higher than in some previous reports,6,7 which may reflect the present study population, who had diabetes and who were quite obese. In data from the Women’s Health Study report,7 which examined CRP in relation to the incidence of diabetes, median CRP was 0.67 mg/dL in patients who developed diabetes compared with 0.26 mg/dL in patients who did not develop diabetes. Median CRP in women in the present study was 0.76 mg/dL. Because glucose levels were also associated with higher CRP levels,6 it would be expected that the present population might have even higher levels than the obese prediabetic patients in the Women’s Health Study.7

Although there was a positive correlation between changes in CRP and IL-6 in both the RSG and placebo treatment groups, there was no apparent effect of either treatment on serum IL-6 levels. Thiazolidinediones have been shown to reduce mRNA induction and expression of IL-6 in a mouse model of type 2 diabetes.22 Subcutaneous adipose tissue is a significant source of IL-6 expression,23 whereas thiazolidinedione treatment has been associated with weight gain and increases in subcutaneous fat. It is possible that our inability to detect differences between RSG and placebo with respect to this parameter may be related to the observed weight decrease in the placebo group (possibly leading to reductions in subcutaneous fat) and weight gain in the RSG group.

The correlations we observed between changes in CRP, IL-6, and MMP-9 were consistent with potential anti-inflammatory and antiatherogenic actions of various PPAR-{gamma} agonists observed in preclinical and clinical studies.2426 The correlation between HOMA-IR and the inflammatory markers IL-6 and MMP-9 at baseline in diabetic patients may suggest a relationship between insulin resistance and a chronic inflammatory state, as shown for CRP and insulin resistance with the frequently sampled intravenous glucose tolerance test in nondiabetic individuals.6

The decrease of WBC with RSG is consistent with the positive correlation of WBC with decreased insulin sensitivity in the Insulin Resistance Atherosclerosis Study (IRAS).8 In the West of Scotland Coronary Prevention Study (WOSCOPS),27 WBC was associated with the development of type 2 diabetes16,27 in univariate models. Additionally, WBC has been shown to predict CVD.6

Relatively few data are available on correlations of circulating MMP-9 with demographic or metabolic variables. In the present report, MMP-9 was correlated with WBC, IL-6, and CRP at baseline. Baseline MMP-9 was positively but weakly correlated with baseline triglyceride and LDL cholesterol levels. However, changes in MMP-9 were correlated with changes in several other variables. Changes in MMP-9 were correlated with changes in CRP, IL-6, WBC, HbA1c, fasting plasma glucose, insulin resistance, and body mass index. The strongest correlations between 0 and 26 weeks for CRP were with other inflammatory factors. In one report, baseline MMP-9 was associated with lower HDL cholesterol, 19 but no association of MMP-9 and HDL cholesterol was observed in another report.28 A positive association of MMP-9 and WBC was observed in one report.28

These data support the potential beneficial effects of insulin-sensitizing interventions such as use of thiazolidinediones on levels of markers for cardiovascular risk. Additional investigations of the effects of antidiabetic agents on cardiovascular outcomes are ongoing.


*    Acknowledgments
 
This study was funded by SmithKlineBeecham Pharmaceuticals. We thank Diane Fuell, GlaxoSmithKline, for her valuable contribution to this study.


*    Footnotes
 
Drs Weston, Chen, and Freed are employees of GlaxoSmithKline.

Received March 21, 2002; revision received May 22, 2002; accepted May 23, 2002.


*    References
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*References
 
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23. Kern PA, Ranganathan S, Li C, et al. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2001; 280: E745–E751.[Abstract/Free Full Text]

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Vasc MedHome page
A. S. Kelly, A. M. Thelen, D. R. Kaiser, J. M. Gonzalez-Campoy, and A. J. Bank
Rosiglitazone improves endothelial function and inflammation but not asymmetric dimethylarginine or oxidative stress in patients with type 2 diabetes mellitus
Vascular Medicine, November 1, 2007; 12(4): 311 - 318.
[Abstract] [PDF]


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J. Nutr.Home page
H. Shen, R. MacDonald, D. Bruemmer, A. Stromberg, A. Daugherty, X.-a. Li, M. Toborek, and B. Hennig
Zinc Deficiency Alters Lipid Metabolism in LDL Receptor Deficient Mice Treated with Rosiglitazone
J. Nutr., November 1, 2007; 137(11): 2339 - 2345.
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Arterioscler. Thromb. Vasc. Bio.Home page
B. Gustafson, A. Hammarstedt, C. X. Andersson, and U. Smith
Inflamed Adipose Tissue: A Culprit Underlying the Metabolic Syndrome and Atherosclerosis
Arterioscler Thromb Vasc Biol, November 1, 2007; 27(11): 2276 - 2283.
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Ther Adv Cardiovasc DisHome page
C. Schindler
Review: The metabolic syndrome as an endocrine disease: is there an effective pharmacotherapeutic strategy optimally targeting the pathogenesis?
Therapeutic Advances in Cardiovascular Disease, October 1, 2007; 1(1): 7 - 26.
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Diabetes and Vascular Disease ResearchHome page
B. Goke, I. Gause-Nilsson, and A. Persson
The effects of tesaglitazar as add-on treatment to metformin in patients with poorly controlled type 2 diabetes
Diabetes and Vascular Disease Research, September 1, 2007; 4(3): 204 - 213.
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J. Clin. Endocrinol. Metab.Home page
Z. Berberoglu, A. Gursoy, N. Bayraktar, A. C. Yazici, N. Bascil Tutuncu, and N. Guvener Demirag
Rosiglitazone Decreases Serum Bone-Specific Alkaline Phosphatase Activity in Postmenopausal Diabetic Women
J. Clin. Endocrinol. Metab., September 1, 2007; 92(9): 3523 - 3530.
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Diabetes CareHome page
N. P.E. Kadoglou, F. Iliadis, C. D. Liapis, D. Perrea, N. Angelopoulou, and M. Alevizos
Beneficial Effects of Combined Treatment With Rosiglitazone and Exercise on Cardiovascular Risk Factors in Patients With Type 2 Diabetes
Diabetes Care, September 1, 2007; 30(9): 2242 - 2244.
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J. Thorac. Cardiovasc. Surg.Home page
A. Momin, N. Melikian, S. B. Wheatcroft, D. Grieve, L. C. John, A. El Gamel, M. T. Marrinan, J. B. Desai, C. Driver, R. Sherwood, et al.
The association between saphenous vein endothelial function, systemic inflammation, and statin therapy in patients undergoing coronary artery bypass surgery
J. Thorac. Cardiovasc. Surg., August 1, 2007; 134(2): 335 - 341.
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Arch Intern MedHome page
P. Hollander, D. Yu, and H. S. Chou
Low-Dose Rosiglitazone in Patients With Insulin-Requiring Type 2 Diabetes
Arch Intern Med, June 25, 2007; 167(12): 1284 - 1290.
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British Journal of Diabetes & Vascular DiseaseHome page
A. H Barnett
Summarising the use of thiazolidinediones with insulin
The British Journal of Diabetes & Vascular Disease, March 1, 2007; 7(2): 75 - 80.
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Cardiovasc ResHome page
A. Fischoeder, H. Meyborg, D. Stibenz, E. Fleck, K. Graf, and P. Stawowy
Insulin augments matrix metalloproteinase-9 expression in monocytes
Cardiovasc Res, March 1, 2007; 73(4): 841 - 848.
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CirculationHome page
J. D. Brown and J. Plutzky
Peroxisome Proliferator Activated Receptors as Transcriptional Nodal Points and Therapeutic Targets
Circulation, January 30, 2007; 115(4): 518 - 533.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
C.-K. Chiang, T.-I. Ho, Y.-S. Peng, S.-P. Hsu, M.-F. Pai, S.-Y. Yang, K.-Y. Hung, and K.-D. Wu
Rosiglitazone in Diabetes Control in Hemodialysis Patients With and Without Viral Hepatitis Infection: Effectiveness and side effects
Diabetes Care, January 1, 2007; 30(1): 3 - 7.
[Abstract] [Full Text] [PDF]


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JAMAHome page
T. Mazzone, P. M. Meyer, S. B. Feinstein, M. H. Davidson, G. T. Kondos, R. B. D'Agostino Sr, A. Perez, J.-C. Provost, and S. M. Haffner
Effect of Pioglitazone Compared With Glimepiride on Carotid Intima-Media Thickness in Type 2 Diabetes: A Randomized Trial
JAMA, December 6, 2006; 296(21): 2572 - 2581.
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Diabetes and Vascular Disease ResearchHome page
R. A Ajjan and P. J Grant
Cardiovascular disease prevention in patients with type 2 diabetes: the role of oral anti-diabetic agents
Diabetes and Vascular Disease Research, December 1, 2006; 3(3): 147 - 158.
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Pharmacol. Rev.Home page
P. Germain, B. Staels, C. Dacquet, M. Spedding, and V. Laudet
Overview of Nomenclature of Nuclear Receptors
Pharmacol. Rev., December 1, 2006; 58(4): 685 - 704.
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Br J AnaesthHome page
G. M. Howard-Alpe, J. W. Sear, and P. Foex
Methods of detecting atherosclerosis in non-cardiac surgical patients; the role of biochemical markers
Br. J. Anaesth., December 1, 2006; 97(6): 758 - 769.
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Arterioscler. Thromb. Vasc. Bio.Home page
S. Kapiotis, G. Holzer, G. Schaller, M. Haumer, H. Widhalm, D. Weghuber, B. Jilma, G. Roggla, M. Wolzt, K. Widhalm, et al.
A Proinflammatory State Is Detectable in Obese Children and Is Accompanied by Functional and Morphological Vascular Changes
Arterioscler Thromb Vasc Biol, November 1, 2006; 26(11): 2541 - 2546.
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J Am Coll CardiolHome page
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.
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Eur Heart JHome page
S. Ahmed, C. P. Cannon, S. A. Murphy, and E. Braunwald
Acute coronary syndromes and diabetes: is intensive lipid lowering beneficial? Results of the PROVE IT-TIMI 22 trial
Eur. Heart J., October 1, 2006; 27(19): 2323 - 2329.
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Am. J. Pathol.Home page
S. E. Feldon, C. W. O'Loughlin, D. M. Ray, S. Landskroner-Eiger, K. E. Seweryniak, and R. P. Phipps
Activated Human T Lymphocytes Express Cyclooxygenase-2 and Produce Proadipogenic Prostaglandins that Drive Human Orbital Fibroblast Differentiation to Adipocytes
Am. J. Pathol., October 1, 2006; 169(4): 1183 - 1193.
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Diabetes and Vascular Disease ResearchHome page
C. B Patle, J. A De Lemos, K. L Wyne, and D. K McGuire
Thiazolidinediones and risk for atherosclerosis: pleiotropic effects of PPAR{gamma} agonism
Diabetes and Vascular Disease Research, September 1, 2006; 3(2): 65 - 71.
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J. Clin. Endocrinol. Metab.Home page
H. Ghanim, S. Dhindsa, A. Aljada, A. Chaudhuri, P. Viswanathan, and P. Dandona
Low-Dose Rosiglitazone Exerts an Antiinflammatory Effect with an Increase in Adiponectin Independently of Free Fatty Acid Fall and Insulin Sensitization in Obese Type 2 Diabetics
J. Clin. Endocrinol. Metab., September 1, 2006; 91(9): 3553 - 3558.
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J. Clin. Endocrinol. Metab.Home page
S. Shadid, C. D. A. Stehouwer, and M. D. Jensen
Diet/Exercise Versus Pioglitazone: Effects of Insulin Sensitization with Decreasing or Increasing Fat Mass on Adipokines and Inflammatory Markers
J. Clin. Endocrinol. Metab., September 1, 2006; 91(9): 3418 - 3425.
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DiabetesHome page
S. E. Kahn, B. Zinman, S. M. Haffner, M. C. O'Neill, B. G. Kravitz, D. Yu, M. I. Freed, W. H. Herman, R. R. Holman, N. P. Jones, et al.
Obesity is a major determinant of the association of C-reactive protein levels and the metabolic syndrome in type 2 diabetes.
Diabetes, August 1, 2006; 55(8): 2357 - 2364.
[Abstract] [Full Text] [PDF]


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Clin. DiabetesHome page
M. Blaha and T. A. Elasy
Clinical Use of the Metabolic Syndrome: Why the Confusion?
Clin. Diabetes, July 1, 2006; 24(3): 125 - 131.
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J Am Coll CardiolHome page
R. Marfella, M. D'Amico, C. Di Filippo, A. Baldi, M. Siniscalchi, F. C. Sasso, M. Portoghese, O. Carbonara, B. Crescenzi, P. Sangiuolo, et al.
Increased Activity of the Ubiquitin-Proteasome System in Patients With Symptomatic Carotid Disease Is Associated With Enhanced Inflammation and May Destabilize the Atherosclerotic Plaque: Effects of Rosiglitazone Treatment
J. Am. Coll. Cardiol., June 20, 2006; 47(12): 2444 - 2455.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
K. Esposito, M. Ciotola, D. Carleo, B. Schisano, F. Saccomanno, F. C. Sasso, D. Cozzolino, R. Assaloni, D. Merante, A. Ceriello, et al.
Effect of Rosiglitazone on Endothelial Function and Inflammatory Markers in Patients With the Metabolic Syndrome
Diabetes Care, May 1, 2006; 29(5): 1071 - 1076.
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Diabetes CareHome page
A. I. Vinik, J. Ullal, H. K. Parson, P. M. Barlow, and C. M. Casellini
Pioglitazone Treatment Improves Nitrosative Stress in Type 2 Diabetes
Diabetes Care, April 1, 2006; 29(4): 869 - 876.
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Arterioscler. Thromb. Vasc. Bio.Home page
F. Meisner, D. Walcher, F. Gizard, X. Kapfer, R. Huber, A. Noak, L. Sunder-Plassmann, H. Bach, C. Haug, M. Bachem, et al.
Effect of Rosiglitazone Treatment on Plaque Inflammation and Collagen Content in Nondiabetic Patients: Data From a Randomized Placebo-Controlled Trial
Arterioscler Thromb Vasc Biol, April 1, 2006; 26(4): 845 - 850.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
R. Marfella, M. D'Amico, K. Esposito, A. Baldi, C. Di Filippo, M. Siniscalchi, F. C. Sasso, M. Portoghese, F. Cirillo, F. Cacciapuoti, et al.
The Ubiquitin-Proteasome System and Inflammatory Activity in Diabetic Atherosclerotic Plaques: Effects of Rosiglitazone Treatment
Diabetes, March 1, 2006; 55(3): 622 - 632.
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G. D. Barish
Peroxisome Proliferator-Activated Receptors and Liver X Receptors in Atherosclerosis and Immunity
J. Nutr., March 1, 2006; 136(3): 690 - 694.
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Arterioscler. Thromb. Vasc. Bio.Home page
F. F. Samaha, P. O. Szapary, N. Iqbal, M. M. Williams, L. T. Bloedon, A. Kochar, M. L. Wolfe, and D. J. Rader
Effects of Rosiglitazone on Lipids, Adipokines, and Inflammatory Markers in Nondiabetic Patients With Low High-Density Lipoprotein Cholesterol and Metabolic Syndrome
Arterioscler Thromb Vasc Biol, March 1, 2006; 26(3): 624 - 630.
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Am. J. Physiol. Renal Physiol.Home page
R. Agarwal
Anti-inflammatory effects of short-term pioglitazone therapy in men with advanced diabetic nephropathy
Am J Physiol Renal Physiol, March 1, 2006; 290(3): F600 - F605.
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British Journal of Diabetes & Vascular DiseaseHome page
N. Sattar
High sensitivity C-reactive protein in cardiovascular disease and type 2 diabetes: evidence for a clinical role?
The British Journal of Diabetes & Vascular Disease, January 1, 2006; 6(1): 5 - 8.
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Arterioscler. Thromb. Vasc. Bio.Home page
F. Blaschke, Y. Takata, E. Caglayan, R. E. Law, and W. A. Hsueh
Obesity, Peroxisome Proliferator-Activated Receptor, and Atherosclerosis in Type 2 Diabetes
Arterioscler Thromb Vasc Biol, January 1, 2006; 26(1): 28 - 40.
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Arterioscler. Thromb. Vasc. Bio.Home page
P. O. Szapary, L. T. Bloedon, F. F. Samaha, D. Duffy, M. L. Wolfe, D. Soffer, M. P. Reilly, J. Chittams, and D. J. Rader
Effects of Pioglitazone on Lipoproteins, Inflammatory Markers, and Adipokines in Nondiabetic Patients with Metabolic Syndrome
Arterioscler Thromb Vasc Biol, January 1, 2006; 26(1): 182 - 188.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
K. K. Koh, S. H. Han, and M. J. Quon
Inflammatory Markers and the Metabolic Syndrome: Insights From Therapeutic Interventions
J. Am. Coll. Cardiol., December 6, 2005; 46(11): 1978 - 1985.
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Clin. Chem.Home page
U. Singh, J. Tabibian, S. K. Venugopal, S. Devaraj, and I. Jialal
Development of an In Vitro Screening Assay to Test the Antiinflammatory Properties of Dietary Supplements and Pharmacologic Agents
Clin. Chem., December 1, 2005; 51(12): 2252 - 2256.
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CirculationHome page
P. W.F. Wilson, R. B. D'Agostino, H. Parise, L. Sullivan, and J. B. Meigs
Metabolic Syndrome as a Precursor of Cardiovascular Disease and Type 2 Diabetes Mellitus
Circulation, November 15, 2005; 112(20): 3066 - 3072.
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CirculationHome page
N. Marx, J. Wohrle, T. Nusser, D. Walcher, A. Rinker, V. Hombach, W. Koenig, and M. Hoher
Pioglitazone Reduces Neointima Volume After Coronary Stent Implantation: A Randomized, Placebo-Controlled, Double-Blind Trial in Nondiabetic Patients
Circulation, November 1, 2005; 112(18): 2792 - 2798.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
K. K. Ray, C. P. Cannon, R. Cairns, D. A. Morrow, N. Rifai, A. J. Kirtane, C. H. McCabe, A. M. Skene, C. M. Gibson, P. M. Ridker, et al.
Relationship Between Uncontrolled Risk Factors and C-Reactive Protein Levels in Patients Receiving Standard or Intensive Statin Therapy for Acute Coronary Syndromes in the PROVE IT-TIMI 22 Trial
J. Am. Coll. Cardiol., October 18, 2005; 46(8): 1417 - 1424.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
Z. T. Bloomgarden
2nd International Symposium on Triglycerides and HDL: Metabolic syndrome
Diabetes Care, October 1, 2005; 28(10): 2577 - 2584.
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J Am Coll CardiolHome page
P. Calabro, D. W. Chang, J. T. Willerson, and E. T.H. Yeh
Release of C-Reactive Protein in Response to Inflammatory Cytokines by Human Adipocytes: Linking Obesity to Vascular Inflammation
J. Am. Coll. Cardiol., September 20, 2005; 46(6): 1112 - 1113.
[Full Text] [PDF]


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ANN INTERN MEDHome page
J. P.H. van Wijk, E. J.P. de Koning, M. C. Cabezas, J. op't Roodt, J. Joven, T. J. Rabelink, and A. I. Hoepelman
Comparison of Rosiglitazone and Metformin for Treating HIV Lipodystrophy: A Randomized Trial
Ann Intern Med, September 6, 2005; 143(5): 337 - 346.
[Abstract] [Full Text] [PDF]


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LupusHome page
A Consoli and E Devangelio
Thiazolidinediones and inflammation
Lupus, September 1, 2005; 14(9): 794 - 797.
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Diabetes CareHome page
R. Kahn, J. Buse, E. Ferrannini, and M. Stern
The Metabolic Syndrome: Time for a Critical Appraisal: Joint statement from the American Diabetes Association and the European Association for the Study of Diabetes
Diabetes Care, September 1, 2005; 28(9): 2289 - 2304.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
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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J. Clin. Endocrinol. Metab.Home page
S. Dhindsa, D. Tripathy, N. Sanalkumar, S. Ravishankar, H. Ghanim, A. Aljada, and P. Dandona
Free Fatty Acid-Induced Insulin Resistance in the Obese Is Not Prevented by Rosiglitazone Treatment
J. Clin. Endocrinol. Metab., September 1, 2005; 90(9): 5058 - 5063.
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Arterioscler. Thromb. Vasc. Bio.Home page
J. Hetzel, B. Balletshofer, K. Rittig, D. Walcher, W. Kratzer, V. Hombach, H.-U. Haring, W. Koenig, and N. Marx
Rapid Effects of Rosiglitazone Treatment on Endothelial Function and Inflammatory Biomarkers
Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1804 - 1809.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
Z. T. Bloomgarden
Second World Congress on the Insulin Resistance Syndrome: Hypertension, cardiovascular disease, and treatment approaches
Diabetes Care, August 1, 2005; 28(8): 2073 - 2080.
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DiabetesHome page
B. Staels and J.-C. Fruchart
Therapeutic Roles of Peroxisome Proliferator-Activated Receptor Agonists
Diabetes, August 1, 2005; 54(8): 2460 - 2470.
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Eur J EndocrinolHome page
I. Tarkun, B. Cetinarslan, E. Turemen, T. Sahin, Z. Canturk, and B. Komsuoglu
Effect of rosiglitazone on insulin resistance, C-reactive protein and endothelial function in non-obese young women with polycystic ovary syndrome
Eur. J. Endocrinol., July 1, 2005; 153(1): 115 - 121.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
S. E. Inzucchi, F. A. Masoudi, Y. Wang, M. Kosiborod, J. M. Foody, J. F. Setaro, E. P. Havranek, and H. M. Krumholz
Insulin-Sensitizing Antihyperglycemic Drugs and Mortality After Acute Myocardial Infarction: Insights from the National Heart Care Project
Diabetes Care, July 1, 2005; 28(7): 1680 - 1689.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
H. Zhang, A. Zhang, D. E. Kohan, R. D. Nelson, F. J. Gonzalez, and T. Yang
Collecting duct-specific deletion of peroxisome proliferator-activated receptor {gamma} blocks thiazolidinedione-induced fluid retention
PNAS, June 28, 2005; 102(26): 9406 - 9411.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
A. Pfutzner, N. Marx, G. Lubben, M. Langenfeld, D. Walcher, T. Konrad, and T. Forst
Improvement of Cardiovascular Risk Markers by Pioglitazone Is Independent From Glycemic Control: Results From the Pioneer Study
J. Am. Coll. Cardiol., June 21, 2005; 45(12): 1925 - 1931.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
P. M. Ridker, D. A. Morrow, L. M. Rose, N. Rifai, C. P. Cannon, and E. Braunwald
Relative Efficacy of Atorvastatin 80 mg and Pravastatin 40 mg in Achieving the Dual Goals of Low-Density Lipoprotein Cholesterol <70 mg/dl and C-Reactive Protein <2 mg/l: An Analysis of the PROVE-IT TIMI-22 Trial
J. Am. Coll. Cardiol., May 17, 2005; 45(10): 1644 - 1648.
[Abstract] [Full Text] [PDF]


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CirculationHome page
M.R. Langenfeld, T. Forst, C. Hohberg, P. Kann, G. Lubben, T. Konrad, S.D. Fullert, C. Sachara, and A. Pfutzner
Pioglitazone Decreases Carotid Intima-Media Thickness Independently of Glycemic Control in Patients With Type 2 Diabetes Mellitus: Results From a Controlled Randomized Study
Circulation, May 17, 2005; 111(19): 2525 - 2531.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
A. H. Berg and P. E. Scherer
Adipose Tissue, Inflammation, and Cardiovascular Disease
Circ. Res., May 13, 2005; 96(9): 939 - 949.
[Abstract] [Full Text] [PDF]


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British Journal of Diabetes & Vascular DiseaseHome page
B. Cariou, J.-C. Fruchart, and B. Staels
Review: Vascular protective effects of peroxisome proliferator-activated receptor agonists
The British Journal of Diabetes & Vascular Disease, May 1, 2005; 5(3): 126 - 132.
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DiabetesHome page
The Diabetes Prevention Program Research Group
Intensive Lifestyle Intervention or Metformin on Inflammation and Coagulation in Participants With Impaired Glucose Tolerance
Diabetes, May 1, 2005; 54(5): 1566 - 1572.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
S. B. Kritchevsky, M. Cesari, and M. Pahor
Inflammatory markers and cardiovascular health in older adults
Cardiovasc Res, May 1, 2005; 66(2): 265 - 275.
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Clin. DiabetesHome page
B. Kimmel and S. E. Inzucchi
Oral Agents for Type 2 Diabetes: An Update
Clin. Diabetes, April 1, 2005; 23(2): 64 - 76.
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J. Clin. Endocrinol. Metab.Home page
A. H. Xiang, R. K. Peters, S. L. Kjos, C. Ochoa, A. Marroquin, J. Goico, S. Tan, C. Wang, S. P. Azen, C.-r. Liu, et al.
Effect of Thiazolidinedione Treatment on Progression of Subclinical Atherosclerosis in Premenopausal Women at High Risk for Type 2 Diabetes
J. Clin. Endocrinol. Metab., April 1, 2005; 90(4): 1986 - 1991.
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Nephrol Dial TransplantHome page
E. M. Stuveling, S. J. L. Bakker, H. L. Hillege, P. E. de Jong, R. O. B. Gans, and D. de Zeeuw
Biochemical risk markers: a novel area for better prediction of renal risk?
Nephrol. Dial. Transplant., March 1, 2005; 20(3): 497 - 508.
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ANGIOLOGYHome page
N. P. Kadoglou, S. S. Daskalopoulou, D. Perrea, and C. D. Liapis
Matrix Metalloproteinases and Diabetic Vascular Complications
Angiology, March 1, 2005; 56(2): 173 - 189.
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Am. J. Physiol. Heart Circ. Physiol.Home page
E. L. Schiffrin
Peroxisome proliferator-activated receptors and cardiovascular remodeling
Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1037 - H1043.
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J Am Coll CardiolHome page
A. V. Finn, I. F. Palacios, A. Kastrati, and H. K. Gold
Drug-eluting stents for diabetes mellitus: A rush to judgment?
J. Am. Coll. Cardiol., February 15, 2005; 45(4): 479 - 483.
[Abstract] [Full Text] [PDF]


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CirculationHome page
F. A. Masoudi, S. E. Inzucchi, Y. Wang, E. P. Havranek, J. M. Foody, and H. M. Krumholz
Thiazolidinediones, Metformin, and Outcomes in Older Patients With Diabetes and Heart Failure: An Observational Study
Circulation, February 8, 2005; 111(5): 583 - 590.
[Abstract] [Full Text] [PDF]


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Diabetes and Vascular Disease ResearchHome page
J. W Chu, F. Abbasi, C. Lamendola, T. McLaughlin, G. M Reaven, and P. S Tsao
Effect of rosiglitazone treatment on circulating vascular and inflammatory markers in insulin-resistant subjects
Diabetes and Vascular Disease Research, February 1, 2005; 2(1): 37 - 41.
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Vasc MedHome page
S. S. Signorelli, G. Malaponte, M. Libra, L. D. Pino, G. Celotta, V. Bevelacqua, M. Petrina, G. S Nicotra, M. Indelicato, P. M Navolanic, et al.
Plasma levels and zymographic activities of matrix metalloproteinases 2 and 9 in type II diabetics with peripheral arterial disease
Vascular Medicine, February 1, 2005; 10(1): 1 - 6.
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Vasc MedHome page
A. Tedgui
The role of inflammation in atherothrombosis: implications for clinical practice
Vascular Medicine, February 1, 2005; 10(1): 45 - 53.
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J. Clin. Endocrinol. Metab.Home page
M. Recasens, A. Lopez-Bermejo, W. Ricart, J. Vendrell, R. Casamitjana, and J. M. Fernandez-Real
An Inflammation Score Is Better Associated with Basal than Stimulated Surrogate Indexes of Insulin Resistance
J. Clin. Endocrinol. Metab., January 1, 2005; 90(1): 112 - 116.
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ASH Education BookHome page
M. A. Crowther
Pathogenesis of Atherosclerosis
Hematology, January 1, 2005; 2005(1): 436 - 441.
[Abstract] [Full Text] [PDF]


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The year in atherothrombosis
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G. Schernthaner, D. R. Matthews, B. Charbonnel, M. Hanefeld, P. Brunetti, and on Behalf of the Quarter Study Group
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D. Choi, S.-K. Kim, S.-H. Choi, Y.-G. Ko, C.-W. Ahn, Y. Jang, S.-K. Lim, H.-C. Lee, and B.-S. Cha
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