Cited by 664Adipokines, Inflammation, and Metabolic DiseasesLipoproteins and Cardiovascular HealthDiabetes, Cardiovascular Risks, and Lipoproteins

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C-Reactive Protein, the Metabolic Syndrome, and Prediction of Cardiovascular Events in the Framingham Offspring Study

Rutter, Martin K., Meigs, James B., Sullivan, Lisa M., D’Agostino, Ralph B., Wilson, Peter W.F.·2004·Circulation

DOI 10.1161/01.cir.0000136581.59584.0e

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Abstract

Background— Inflammation (assessed by C-reactive protein [CRP]) and the metabolic syndrome (MetS) are associated with cardiovascular disease (CVD), but population-based data are limited. Methods and Results— We assessed the cross-sectional relations of CRP to the MetS (National Cholesterol Education Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults, Adult Treatment Panel III definition) in 3037 subjects (1681 women; mean age, 54 years) and the utility of CRP and the MetS to predict new CVD events (n=189) over 7 years. MetS (≥3 of 5 traits) was present in 24% of subjects; mean age-adjusted CRP levels for those with 0, 1, 2, 3, 4, or 5 MetS traits were 2.2, 3.5, 4.2, 6.0, or 6.6 mg/L, respectively ( P trend <0.0001). In persons with MetS, age-adjusted CRP levels were higher in women than men (7.8 versus 4.6 mg/L; P <0.0001). MetS and baseline CRP were individually related to CVD events (for MetS: age-sex-adjusted hazard ratio [HR], 2.1; 95% CI, 1.5 to 2.8; for highest versus lowest CRP quartile: HR, 2.2; 95% CI, 1.4 to 3.5). Greater risk of CVD persisted for MetS and CRP even after adjustment in a model including age, sex, MetS (HR, 1.8; 95% CI, 1.4 to 2.5), and CRP (HR, 1.9; 95% CI, 1.2 to 2.9). The c-statistic associated with the age- and sex-adjusted model including CRP was 0.72; including MetS, 0.74; and including CRP and MetS, 0.74. Conclusions— Elevated CRP levels are related to insulin resistance and the presence of the MetS, especially in women. Although discrimination of subjects at risk of CVD events using both MetS and CRP is not better than using either phenotype alone, both CRP and MetS are independent predictors of new CVD events.

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“Ad-ditionally to the traditional markers, white blood cell (WBC) count, 17 high-sensitivity C-reactive protein 18 (hsCRP; as a marker of inﬂammation), homeostasis model assessment of insulin resistance (HOMA-IR) index 19 (as a marker of insulin resistance), homocysteine 21 (as a marker of…”
Effects of Yoga on Sexual Function in Women with Metabolic Syndrome: A Randomized Controlled Trial
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Serum C-Reactive Protein and Its Relation to Cardiovascular Risk Factors and Adipocytokines in Japanese Children
Yoshida, T., Kaneshi, T., Shimabukuro, T., Sunagawa, M., & Ohta, T. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2856 · Cited by 37
Association Among C-Reactive Protein, Fatty Liver Disease, and Cardiovascular Risk
Lizardi-Cervera, J., Chávez-Tapia, N. C., Pérez-Bautista, O., Ramos, M. H., & Uribe, M. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9262-6 · Cited by 37
“cardiovascular problems [33], but it is unknown whether this risk extends to subjects with NAFLD.”
N-Glycosylation Profiles of Immunoglobulin G and Future Cardiovascular Events
Hoshi, R. A., Plavša, B., Liu, Y., Trbojević‐Akmačić, I., Glynn, R. J., Ridker, P. M., Cummings, R. D., Gudelj, I., Lauc, G., Demler, O., et al. (2024) · Circulation Research · doi:10.1161/circresaha.123.323623 · Cited by 37
“57 58–68 Correlations between IgG N -glycans and clinical biomarkers were concordant in terms of sign and magnitude across studies for most IgG-GPs, and several were significant in both cohorts (Figure S5).”
Background
Insulin resistance and systemic inflammation, but not metabolic syndrome phenotype, predict 9 years mortality in older adults
Zuliani, G., Morieri, M. L., Volpato, S., Maggio, M. G., Cherubini, A., Francesconi, D., Bandinelli, S., Paolisso, G., Guralnik, J. M., & Ferrucci, L. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.05.959 · Cited by 36
Suppression of estrogen-related receptor α and medium-chain acyl-coenzyme A dehydrogenase in the acute-phase response
Kim, M. S., Shigenaga, J. K., Moser, A. H., Feingold, K. R., & Grünfeld, C. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500217-jlr200 · Cited by 36
Sex based levels of C-reactive protein and white blood cell count in subjects with metabolic syndrome: Isfahan Healthy Heart Program.
Gharipour, M., Ramezani, M. A., Sadeghi, M., Khosravi, A., Masjedi, M., Khosravi‐Boroujeni, H., Rafieian‐Kopaei, M., & Sarrafzadegan, N. (2013) · Europe PMC (PubMed Central) · Cited by 35
Gender-Specific Association Between the Metabolic Syndrome and Arterial Stiffness in 8,300 Subjects
Weng, C., Yang, K., Tang, X., Huang, Z., Huang, L., Chen, W., Yuan, H., Chen, F., Chen, Z., & Yang, P. (2013) · The American Journal of the Medical Sciences · doi:10.1097/maj.0b013e3182732e97 · Cited by 35
“1).(1,4) Before onset of CVD, the MetS is often present.”
Background
Fiber's impact on high‐sensitivity C‐reactive protein levels in cardiovascular disease
Butcher, J. L., & Beckstrand, R. L. (2010) · Journal of the American Academy of Nurse Practitioners · doi:10.1111/j.1745-7599.2010.00555.x · Cited by 36
Visceral adipose tissue, adiponectin levels and insulin resistance are related to atherosclerosis as assessed by whole-body magnetic resonance angiography in an elderly population
Hansen, T., Ahlström, H. K., Söderberg, S., Hulthe, J., Wikström, J., Lind, L., & Johansson, L. (2008) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2008.11.007 · Cited by 35
Prevalence of the Metabolic Syndrome in Patients With Hypertension Treated in General Practice in Spain: An Assessment of Blood Pressure and Low‐Density Lipoprotein Cholesterol Control and Accuracy of Diagnosis
Barrios, V., Escobar, C., Calderón, A., Llisterri, J. L., Alegría, E., Muñiz, J., & Matalí, A. (2007) · Journal of the CardioMetabolic Syndrome · doi:10.1111/j.1559-4564.2007.06313.x · Cited by 35
Severity of obesity and cardiometabolic risk factors in adults: Sex differences and role of physical activity. The HERMEX study
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Association of C-reactive protein (CRP) gene allelic variants with serum CRP levels and hypertension in Turkish adults
Kömürcü-Bayrak, E., Erginel‐Ünaltuna, N., Onat, A., Ozsait, B., Eklund, C., Hurme, M., Mononen, N., Laaksonen, R., Hergenç, G., & Lehtimäki, T. J. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.03.030 · Cited by 34
Fiber intake and inflammation in type 1 diabetes
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High sensitive C-reactive protein and serum amyloid A are inversely related to serum bilirubin: effect-modification by metabolic syndrome
Deetman, P. E., Bakker, S. J. L., & Dullaart, R. P. F. (2013) · Cardiovascular Diabetology · doi:10.1186/1475-2840-12-166 · Cited by 34
C‐Reactive Protein Identifies Low‐Risk Metabolically Healthy Obese Persons: The European Prospective Investigation of Cancer–Norfolk Prospective Population Study
van Wijk, D. F., Boekholdt, S. M., Arsenault, B. J., Ahmadi‐Abhari, S., Wareham, N. J., Stroes, E. S. G., & Khaw, K. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.115.002823 · Cited by 33
“prevalence of the metabolically healthy but obese phenotype was somewhat higher in our population compared with previous studies,(19) probably because we defined abdominal obesity by waist circumference, whereas other studies used other measures to determine obesity (eg, body mass index).(12) It must be noted that in…”
Result
High-Sensitivity C-Reactive Protein Leads to Increased Incident Metabolic Syndrome in Women but Not in Men: A Five-Year Follow-Up Study in a Chinese Population
Hong, G., Gao, P., Chen, Y., Xia, Y. Y., Ke, X., Shao, X., Xiong, C., Chen, H.-S., Xiao, H., Ning, J., et al. (2020) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s241774 · Cited by 33
Long-term C-Reactive Protein Variability and Prediction of Metabolic Risk
Chen, T.-H., Gona, P. N., Sutherland, P. A., Benjamin, E. J., Wilson, P. W. F., Larson, M. G., Vasan, R. S., & Robins, S. J. (2008) · The American Journal of Medicine · doi:10.1016/j.amjmed.2008.08.023 · Cited by 33
Self-citation
The Proinflammatory Mediator CD40 Ligand Is Increased in the Metabolic Syndrome and Modulated by Adiponectin
Natal, C., Restituto, P., Iñigo, C., Colina, I., Dı́ez, J., & Varo, N. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2491 · Cited by 33
Intracranial atherosclerotic stroke: Specific focus on the metabolic syndrome and inflammation
Bang, O. Y. (2006) · Current Atherosclerosis Reports · doi:10.1007/s11883-006-0012-1 · Cited by 33
Sex differences and cardiovascular risk
Cordero, A., & Alegria, E. (2006) · Heart · doi:10.1136/hrt.2005.069187 · Cited by 33
C-reactive protein and cardiovascular diseases: a synthesis of studies based on different designs
Liu, C., & Li, C. (2023) · European Journal of Preventive Cardiology · doi:10.1093/eurjpc/zwad116 · Cited by 37
Group of Serum Inflammatory Markers and Periodontitis–Metabolic Syndrome Coexistence in Koreans
Han, D., Shin, H., Kim, M., Paek, D., & Kim, H. (2011) · Journal of Periodontology · doi:10.1902/jop.2011.110304 · Cited by 32
Metabolic syndrome, cardiovascular risk and screening for subclinical atherosclerosis
Malik, S., & Wong, N. D. (2009) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.7.3.273 · Cited by 32
Clinical Use of the Metabolic Syndrome: Why the Confusion?
Blaha, M. J., & Elasy, T. A. (2006) · Clinical Diabetes · doi:10.2337/diaclin.24.3.125 · Cited by 32
Metabolic syndrome and incident peripheral artery disease – the Multi-Ethnic Study of Atherosclerosis
Vidula, H., Liu, K., Criqui, M. H., Szklo, M., Allison, M., Sibley, C. T., Ouyang, P., Tracy, R. P., Chan, C., & McDermott, M. M. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.08.044 · Cited by 32
Metabolic Syndrome, C-Reactive Protein and Increased Arterial Stiffness in Japanese Subjects
Saijo, Y., Yoshioka, E., FUKUI, T., Kawaharada, M., & Kishi, R. (2006) · Hypertension Research · doi:10.1291/hypres.29.589 · Cited by 32
“However, another report insisted that combining CRP and MS data added little to overall cardiovascular disease risk prediction (14).”
Background
Urinary PGDS levels are associated with vascular injury in type 2 diabetes patients
Yoshikawa, R., Wada, J., Seiki, K., Matsuoka, T., Miyamoto, S., Takahashi, K., Ota, S., Taniai, K., Hida, K., Yamakado, M., et al. (2006) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2006.09.004 · Cited by 31
Multiple biomarkers and their relative contributions to identifying metabolic syndrome
Lee, J. G., Lee, S. Y., Kim, Y. J., Jin, H. K., Cho, B. M., Kim, Y. J., Jeong, D. W., Park, H. J., & Kim, J. E. (2009) · Clinica Chimica Acta · doi:10.1016/j.cca.2009.07.006 · Cited by 31
Association between paraoxonase-1 gene polymorphisms and risk of metabolic syndrome
Kordi-Tamandani, D. M., Hashemi, M. M., Sharifi, N., Kaykhaei, M. A., & Torkamanzehi, A. (2011) · Molecular Biology Reports · doi:10.1007/s11033-011-0819-x · Cited by 31
“In addition, MS has also been reported to be linked with elevated serum high-sensitive C-reactive protein (hsCRP) [5, 6], endothelial dysfunction [7], increased carotid intima media thickness (IMT) [8], cardiovascular disorder and mortality [9, 10].”
Background
In Addition to Insulin Resistance and Obesity, Brachial-Ankle Pulse Wave Velocity is Strongly Associated with Metabolic Syndrome in Chinese - A Population-Based Study (Taichung Community Health Study, TCHS)
Lin, W.-Y., Lai, M.-M., Li, C., Lin, C., Li, T., Chen, C., Lin, T., & Liu, C.-S. (2009) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.e603 · Cited by 30
The influence of inflammation on cardiovascular disease in women
Kottilil, S., & Mathur, P. (2022) · Frontiers in Global Women s Health · doi:10.3389/fgwh.2022.979708 · Cited by 32
Elevated Plasma Homocysteine in Older Shift‐Workers: A Potential Risk Factor for Cardiovascular Morbidity
Lavie, L., & Lavie, P. (2007) · Chronobiology International · doi:10.1080/07420520601139797 · Cited by 30
“Increased BMI, dyslipidemia, hyperglycaemia, and decreased HDL are components of the “metabolic syndrome,” of which CRP has been suggested to be an additional component (Rutter et al., 2004).”
Background
Evaluating the role of biomarkers for cardiovascular risk prediction: focus on CRP, BNP and urinary microalbumin
May, A., & Wang, T. J. (2007) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.7.6.793 · Cited by 31
C-Reactive Protein and Metabolic Syndrome in Elderly Women
Hassinen, M., Lakka, T. A., Komulainen, P., Gylling, H., Nissinen, A. M., & Rauramaa, R. (2006) · Diabetes Care · doi:10.2337/diacare.29.04.06.dc05-2508 · Cited by 30
“Cross-sectional studies have found associations of CRP with metabolic syndrome (6–9) and its components, including obesity (10), insulin resistance (6,7,10), dyslipidemia (10), elevated blood pressure (11), and endothelial dysfunction (10).”
Background
Soluble endothelial protein C receptor and high sensitivity C reactive protein levels as markers of endothelial dysfunction in patients with type 1 and type 2 diabetes mellitus: Their role in the prediction of vascular complications
Zaghloul, A., Albukhari, T. A., AL-Pakistani, H. A., Shalaby, M., Halawani, S. H., Bajuaifer, N., & Teama, S. H. (2014) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2014.09.007 · Cited by 29
Combined lowering of low grade systemic inflammation and insulin resistance in metabolic syndrome patients treated with Ginkgo biloba
Siegel, G., Ermilov, E. A., Knes, O., & Rodríguez, M. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.10.023 · Cited by 29
The relation between hostility and concurrent levels of inflammation is sex, age, and measure dependent
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The Framingham Study on Cardiovascular Disease Risk and Stress-Defenses: A Historical Review
Abohelwa, M., Kopel, J. J., Shurmur, S. W., Ansari, M. M., Awasthi, S., & Awasthi, S. (2023) · Journal of Vascular Diseases · doi:10.3390/jvd2010010 · Cited by 43
“The simultaneous occurrence of HTN and obesity is a characteristic of metabolic syndrome [28,32,164,337].”
Background
Prevalence and factors associated with metabolic syndrome in university students and academic staff in Bangladesh
Ali, N., Samadder, M., Shourove, J. H., Taher, A., & Islam, F. (2023) · Scientific Reports · doi:10.1038/s41598-023-46943-x · Cited by 29
“It has been demonstrated that BMI is associated with an increased risk of developing MetS in adulthood 39 .”
Background
The therapeutic modulation of atherogenic dyslipidemia and inflammatory markers in the metabolic syndrome: what is the clinical relevance?
Rizzo, M., Rizvi, A. A., Rini, G. B., & Berneis, K. K. (2008) · Acta Diabetologica · doi:10.1007/s00592-008-0057-4 · Cited by 29
“Intriguingly, the role of CRP in the prediction of cardiovascular events [29, 30] and its association with insulin resistance [31] and hyperinsulinaemia [32] may provide clues to more definitive answers.”
Background
Association between fasting glucose and C-reactive protein in a Japanese population: the Minoh study
Nakanishi, N., SHIRAISHI, T., & Wada, M. (2005) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2004.11.009 · Cited by 29

Authors: Rutter, M. K., Meigs, J. B., Sullivan, L. M., D’Agostino, R. B., & Wilson, P. W. F.
Affiliations: Boston University (US)
ORCID: Rutter, Martin K.
Meigs, James B.
Sullivan, Lisa M.
D’Agostino, Ralph B.
Wilson, Peter W.F.
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2004-07-27
Volume: 110
Issue: 4
Pages: 380-385
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/01.cir.0000136581.59584.0e
OpenAlex: W1983997573
Cited by: 664
References: 36
Citations by year: 2026: 4 · 2025: 7 · 2024: 9 · 2023: 15 · 2022: 19 · 2021: 9 · 2020: 8 · 2019: 11 · 2018: 15 · 2017: 13 · 2016: 19 · 2015: 20 · 2014: 36 · 2013: 36 · 2012: 26
FWCI: 48.38
Type: journal article
Language: en
Open access: closed
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Research Explorer (The University of Manchester) (submittedVersion)
Funders: National Institutes of Health (n01hc25195-41-0-1)
National Heart, Lung, and Blood Institute (R01HL073272, N01‐HC25195, R01-HL 073272-01)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Keywords: C-reactive protein, metabolic syndrome, cardiovascular risk prediction, inflammation, insulin resistance, sex differences, Framingham Offspring Study, cardiovascular events, risk discrimination, cardiovascular risk in women, NCEP ATP III criteria, Framingham risk score, Framingham risk equation
MeSH terms: Adult, Aged, Aged, 80 and over, C-Reactive Protein, Cardiovascular Diseases, Cross-Sectional Studies, Female, Follow-Up Studies, Humans, Inflammation, Insulin Resistance, Male, Middle Aged, Predictive Value of Tests, Risk, Sex Factors, Cohort Studies, Metabolic Syndrome

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C-Reactive Protein, the Metabolic Syndrome, and Prediction of Cardiovascular Events in the Framingham Offspring Study

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