Cited by 665Nitric Oxide and Endothelin EffectsCardiovascular Health and Disease PreventionAtherosclerosis and Cardiovascular Diseases

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Elevated C-Reactive Protein Levels and Impaired Endothelial Vasoreactivity in Patients With Coronary Artery Disease

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Fichtlscherer, Stephan, Rosenberger, Gunter, Walter, Dirk H., Breuer, Susanne, Dimmeler, Stefanie, Zeiher, Andreas M.·2000·Circulation

DOI 10.1161/01.cir.102.9.1000

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Abstract

Background —Elevated C-reactive protein (CRP) serum levels, an exquisitely sensitive objective marker of inflammation, relate to long-term prognosis in patients with coronary artery disease and in apparently healthy men. Because abnormalities of endothelial regulation of vascular function may contribute to the occurrence of coronary events, we tested the hypothesis that elevated CRP levels are associated with an abnormal systemic endothelial vascular reactivity. Methods and Results —Endothelium-dependent (10 to 50 μg/min acetylcholine) and endothelium-independent (2 to 8 μg/min sodium nitroprusside) forearm blood flow responses were measured with venous occlusion plethysmography in 60 male patients with angiographically documented coronary artery disease. Forearm blood flow responses to acetylcholine were inversely correlated with CRP serum levels ( r =−0.46, P =0.001). With multivariate analysis that included the classic risk factors for coronary artery disease, elevated CRP serum level remained a statistically significant independent predictor of a blunted endothelial vasodilator capacity. Most important, normalization of elevated CRP levels over time was associated with a normalization of endothelium-mediated forearm blood flow responses after 3 months. Conclusions —Thus, elevated CRP serum levels indicative of a systemic inflammatory response are associated with a blunted systemic endothelial vasodilator function. The identification of elevated CRP levels as a transient independent risk factor for endothelial dysfunction might provide an important clue to link a systemic marker of inflammation to atherosclerotic disease progression.

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C-Reactive Protein as a Cardiovascular Risk Factor
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10.1161/circ.96.11.4095 · DOI
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Background
Low-grade Inflammatory Marker Profile May Help to Differentiate Patients With LADA, Classic Adult-Onset Type 1 Diabetes, and Type 2 Diabetes
Castelblanco, E., Hernández, M., Castelblanco, A., Gratacòs, M., Esquerda, A., Molló, À., Ramírez‐Morros, A., Real, J., Franch‐Nadal, J., Fernández‐Real, J. M., et al. (2018) · Diabetes Care · doi:10.2337/dc17-1662 · Cited by 43
Association between inflammation and skeletal muscle proteolysis, skeletal mass and strength in elderly heart failure patients and their prognostic implications
Koshikawa, M., Harada, M., Noyama, S., Kiyono, K., Motoike, Y., Nomura, Y., Nishimura, A., Izawa, H., Watanabe, E., & Ozaki, Y. (2020) · BMC Cardiovascular Disorders · doi:10.1186/s12872-020-01514-0 · Cited by 43
The yin and yang of arterial inflammation**Editorials published in the Journal of the American College of Cardiologyreflect the views of the authors and do not necessarily represent the views of JACCor the American College of Cardiology.
Mills, R. M., & Bhatt, D. L. (2004) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2004.04.002 · Cited by 43
C-reactive protein and white blood cell are associated with frailty progression: a longitudinal study
Cheng, Z., He, D., Li, J., Wu, Q. H., Liu, Z., & Zhu, Y. (2022) · Immunity & Ageing · doi:10.1186/s12979-022-00280-1 · Cited by 44
“Moreover, inflammation impairs endothelial reactivity and muscle perfusion, interferes with the uptake of long branched chain amino acids, and consequently reduces muscle energy and protein anabolism [43].”
Background
Leukocyte count is associated with reduced endothelial reactivity
Elkind, M. S. V., Sciacca, R. R., Boden-Albala, B. M., Tondella, M. L., Feikin, D. R., Fields, B. S., Sacco, R. L., Tullio, M. R. D., & Homma, S. (2005) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.01.013 · Cited by 42
Endothelial Function Varies According to Insulin Resistance Disease Type
Beckman, J. A., Goldfine, A. B., Dunaif, A. E., Gerhard‐Herman, M. D., & Creager, M. A. (2007) · Diabetes Care · doi:10.2337/dc06-2142 · Cited by 42
Leukocyte count and vascular function in Type 2 diabetic subjects with treated hypertension
Woodman, R. J., Watts, G. F., Puddey, I. B., Burke, V., Mori, T. A., Hodgson, J. M., & Beilin, L. J. (2002) · Atherosclerosis · doi:10.1016/s0021-9150(01)00770-5 · Cited by 41
Pathological Changes in Acute Coronary Syndromes: The Role of Statin Therapy in the Modulation of Inflammation, Endothelial Function and Coagulation
Ray, K., & Cannon, C. (2004) · Journal of Thrombosis and Thrombolysis · doi:10.1007/s11239-004-0205-9 · Cited by 43
“Statins reduce CRP levels and some of the beneficial effects of statins on flow may be mediated via this route, as CRP has been shown to reduce e-NOS and impair flow mediated dilatation (FMD) [92,93].”
Background
Rofecoxib, a COX-2 Inhibitor, Lowers C-Reactive Protein and Interleukin-6 Levels in Patients With Acute Coronary Syndromes
Monakier, D., Mates, M., Klutstein, M. W., Balkin, J., Rudensky, B., Meerkin, D., & Tzivoni, D. (2004) · CHEST Journal · doi:10.1378/chest.125.5.1610 · Cited by 42
Benefits of immediate initiation of statin therapy following successful coronary stent implantation in patients with stable and unstable angina pectoris and Q-wave acute myocardial infarction
Walter, D. H., Fichtlscherer, S., Britten, M. B., Auch–Schwelk, W., Schächinger, V., & Zeiher, A. M. (2002) · The American Journal of Cardiology · doi:10.1016/s0002-9149(01)02153-1 · Cited by 42
Self-citation
The relationship between plasma asymmetrical dimethyl-l-arginine and inflammation and adhesion molecule levels in subjects with normal, impaired, and diabetic glucose tolerance
Konukoğlu, D., Fırtına, S., & Serin, O. (2007) · Metabolism · doi:10.1016/j.metabol.2007.08.013 · Cited by 40
Correlates of endothelial function and their relationship with inflammation in patients with familial hypercholesterolaemia
van Haelst, P. L., van Doormaal, J. J., Asselbergs, F. W., van Roon, A. M., Veeger, N. J. G. M., Henneman, M. M., Smit, A. J., Tervaert, J. W. C., May, J. F., & Gans, R. O. B. (2003) · Clinical Science · doi:10.1042/cs20020293 · Cited by 41
“patients with proven coronary artery disease [ 21 ].”
Background
Coxibs, non‐steroidal anti‐inflammatory drugs and cardiovascular risk
Hermann, M., & Ruschitzka, F. T. (2006) · Internal Medicine Journal · doi:10.1111/j.1445-5994.2006.01056.x · Cited by 42
Supplementation with tocotrienol-rich fraction alters the plasma levels of Apolipoprotein A-I precursor, Apolipoprotein E precursor, and C-reactive protein precursor from young and old individuals
Heng, E. C., Karsani, S. A., Rahman, M. A., Hamid, N. A. A., Hamid, Z., & Ngah, W. Z. W. (2013) · European Journal of Nutrition · doi:10.1007/s00394-012-0485-3 · Cited by 40
“A strong correlation between increased plasma CRP level and impaired endothelial function has been reported in patients with coronary artery disease [36].”
Background
C-reactive protein is released in the coronary circulation and causes endothelial dysfunction in patients with acute coronary syndromes
Forte, L., Cimmino, G., Loffredo, F. S., Palma, R. D., Abbate, G., Calabrò, P., Ingrosso, D., Galletti, P., Carangio, C., Casillo, B., et al. (2011) · International Journal of Cardiology · doi:10.1016/j.ijcard.2011.05.062 · Cited by 40
“increased CRP levels have been shown to be associated with an impairment of forearm endothelial vascular reactivity; interestingly, normalization of CRP levels was associated with a significant improvement in endothelial responses [12].”
Background
Atherogenesis--recent insights into basic mechanisms and their clinical impact
Schächinger, V. (2002) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/17.12.2055 · Cited by 40
“Thus, C-reactive protein (CRP), an unspecific marker of inflammation, is related to endothelial dysfunction in the forearm microcirculation of patients with coronary artery disease [17], due to enhanced oxidative stress and reduced NO bioavailability [18].”
Background
Endothelial dysfunction of peripheral arteries in patients with immunohistologically confirmed myocardial inflammation correlates with endothelial expression of human leukocyte antigens and adhesion molecules in myocardial biopsies
Vallbracht, K. B., Schwimmbeck, P. L., Seeberg, B., Kühl, U., & Schultheiß, H. (2002) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)01990-3 · Cited by 40
“It has been correlated with levels of C-reactive protein (8).”
Background
Highly effective reduction of C-reactive protein in patients with coronary heart disease by extracorporeal low density lipoprotein apheresis
Wieland, E., Schettler, V. J. J., & Armstrong, V. W. (2002) · Atherosclerosis · doi:10.1016/s0021-9150(01)00698-0 · Cited by 40
Relationship between C reactive protein and pulse pressure is not mediated by atherosclerosis or aortic stiffness
Amar, J., Ruidavets, J., Sollier, C. B. D., Bongard, V., Boccalon, H., Chamontin, B., Drouet, L. O., & Ferrières, J. (2004) · Journal of Hypertension · doi:10.1097/00004872-200402000-00019 · Cited by 40
Significant Relationship Between Serum High-sensitivity C-Reactive Protein, High-density Lipoprotein Cholesterol Levels and Children With Kawasaki Disease and Coronary Artery Lesions
Ou, C., Tseng, Y., Lee, C., Chiou, Y., & Hsieh, K. (2009) · Journal of the Formosan Medical Association · doi:10.1016/s0929-6646(09)60395-8 · Cited by 39
Structural and functional abnormality of systemic microvessels in cardiac syndrome X
Pasqui, A. L., Puccetti, L., Renzo, M. D., Bruni, F., Camarri, A., Palazzuoli, A., Biagi, F., Servi, M., Bischeri, D., Auteri, A., et al. (2005) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2004.05.001 · Cited by 39
“In particular, CPR is considered an independent risk factor of coronary artery disease and CRP plasma levels are known to be associated with coronary dysfunction and with endothelial cell activation [33,34].”
Background
The assessment of endothelial function in humans
Farouque, H. M. O., & Meredith, I. T. (2001) · Coronary Artery Disease · doi:10.1097/00019501-200109000-00003 · Cited by 39
The endothelial function biomarker soluble E‐selectin is associated with nonalcoholic fatty liver disease
Simons, N., Bijnen, M., Wouters, K., Rensen, S. S., Beulens, J. W. J., van Greevenbroek, M. M. J., Hart, L. M. ‘., Greve, J. W. M., Kallen, C., Schaper, N. C., et al. (2020) · Liver International · doi:10.1111/liv.14384 · Cited by 40
Reconstituted HDL in Acute Coronary Syndromes
Chenevard, R., Hürlimann, D., Spieker, L. E., Béchir, M., Enseleit, F., Hermann, M., Flammer, A. J., Sudano, I., Corti, R., Lüscher, T. F., et al. (2010) · Cardiovascular Therapeutics · doi:10.1111/j.1755-5922.2010.00221.x · Cited by 37
“Despite these favorable effects of rHDL on lipid profile, inflammation, and oxidative stress, all of which alone would have predicted a beneficial impact on vascular function [7,23], the latter remained unexpectedly unchanged under the conditions of the present study.”
Background
Serum matrix metalloproteinase‐9 is elevated in men with a history of myocardial infarction
Renko, J., Kalela, A., Jaakkola, O., Laine, S., Höyhtyä, M., Alho, H., & Nikkari, S. T. (2004) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365510410006054 · Cited by 37
Sleep disordered breathing and risk factors for cardiovascular disease
Phillips, B. G., & Somers, V. K. (2002) · Current Opinion in Pulmonary Medicine · doi:10.1097/00063198-200211000-00006 · Cited by 37
Palmitate induces C-reactive protein expression in human aortic endothelial cells. Relevance to fatty acid–induced endothelial dysfunction
Mugabo, Y., Mukaneza, Y., & Renier, G. (2010) · Metabolism · doi:10.1016/j.metabol.2010.06.014 · Cited by 36
C-Reactive Protein and Retinal Microvascular Caliber in a Multiethnic Asian Population
Cheung, C. Y.-L., Wong, T. Y., Lamoureux, E. L., Sabanayagam, C., Li, J., Lee, J., & Tai, E. S. (2009) · American Journal of Epidemiology · doi:10.1093/aje/kwp357 · Cited by 36
Pre-hypertension: Is it an inflammatory state?
Nandeesha, H., Bobby, Z., Selvaraj, N., & Rajappa, M. (2015) · Clinica Chimica Acta · doi:10.1016/j.cca.2015.10.022 · Cited by 35
Interleukin-6 Correlates with Endothelial Dysfunction in Young Post-Myocardial Infarction Patients
Eržen, B., Šabović, M., Šebeštjen, M., Keber, I., & Poredoš, P. (2006) · Cardiology · doi:10.1159/000094588 · Cited by 39
“In the group of post-myocardial patients we have found a significant negative correlation between ED and IL-6, but not between ED and other inflammatory markers. The correlation between vascular inflammation and ED is most likely the consequence of the fact that local inflammation probably decreases the biological act…”
Background
Obstructive Sleep Apnea Syndrome, Vascular Pathology, Endothelial Function and Endothelial Cells and Circulating Microparticles
Stiefel, P., Sánchez-Armengol, M. Á., Villar, J. R., Vallejo‐Vaz, A. J., Moreno‐Luna, R., & Capote, F. (2013) · Archives of Medical Research · doi:10.1016/j.arcmed.2013.08.005 · Cited by 35
Lipoxins, resolvins, protectins, maresins and nitrolipids, and their clinical implications with specific reference to diabetes mellitus and other diseases: part II
Das, U. N. (2013) · Clinical Lipidology · doi:10.2217/clp.13.32 · Cited by 35
Endothelial dysfunction and inflammation after percutaneous coronary intervention
Blum, A., Schneider, D. J., Sobel, B. E., & Dauerman, H. L. (2004) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2004.07.146 · Cited by 35
Effect of tamoxifen at low doses on ultrasensitive C-reactive protein in healthy women
Bonanni, B., Johansson, H. A., Gandini, S., Guerrieri‐Gonzaga, A., Sandri, M. T., Mariette, F., Lien, E. A., & DeCensi, A. (2003) · Journal of Thrombosis and Haemostasis · doi:10.1046/j.1538-7836.2003.00392.x · Cited by 35
Persistent endothelial dysfunction is related to elevated C-reactive protein (CRP) levels in Type II diabetic patients after acute myocardial infarction
Nyström, T., Nygren, A., & Sjöholm, Å. (2005) · Clinical Science · doi:10.1042/cs20040243 · Cited by 34
Identifying Cardiovascular Risk Factors in a Patient Population With Coronary Artery Ectasia
Sağlam, M., Karakaya, O., Barutçu, İ., Esen, A. M., Türkmen, M., Kargın, R., Esen, Ö., Özdemir, N., & Kaymaz, C. (2007) · Angiology · doi:10.1177/0003319707309119 · Cited by 34
“It has also been shown that serum CRP concentration is related to endothelial dysfunction, a key early event in atherogenesis.(32) In our study, we found that in patients with isolated CAE, CRP level was as high as that in patients with obstructive CAD.”
Result
Harnessing polyphenol power by targeting eNOS for vascular diseases
Das, M., Devi, K. P., Belwal, T., Devkota, H. P., Tewari, D., Sahebnasagh, A., Nabavi, S. F., Kashani, H. R. K., Rasekhian, M., Xu, S., et al. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1971153 · Cited by 35
Vascular changes, Cardiovascular Disease and Obstructive Sleep Apnea
Ramar, K., & Caples, S. M. (2011) · Future Cardiology · doi:10.2217/fca.10.123 · Cited by 33
“There is also evidence that elevated CRP levels are independent predictors for vascular endothelial dysfunction by resulting in a blunted vascular dilation in response to acetylcholine [68], and as OSA can lead to cardiovascular disorders, it is natural to implicate a role for CRP in OSA patients.”
Background
Macrophage migration inhibitory factor is associated with vascular dysfunction in patients with end-stage renal disease
Rammos, C., Hendgen-Cotta, U. B., Sobierajski, J., Adamczyk, S., Hetzel, G. R., Kleophas, W., Dellanna, F., Kelm, M., & Rassaf, T. (2013) · International Journal of Cardiology · doi:10.1016/j.ijcard.2013.08.021 · Cited by 33
“This findings support the concept that vascular inflammation is a central orchestrator of endothelial function and atherosclerotic lesion formation, progression, and eventual rupture [32,33].”
B-type natriuretic peptide is an independent predictor of endothelial function in man
Pauriah, M., Khan, F., Lim, T. K., Elder, D. H. J., Godfrey, V., Kennedy, G., Belch, J. J. F., Booth, N. A., Struthers, A. D., & Lang, C. C. (2012) · Clinical Science · doi:10.1042/cs20110168 · Cited by 33
Lipoxins, resolvins, protectins, maresins and nitrolipids, and their clinical implications with specific reference to cancer: part I
Das, U. N. (2013) · Clinical Lipidology · doi:10.2217/clp.13.31 · Cited by 33
C-reactive protein and red cell aggregation correlate with late venous function after acute deep venous thrombosis
Krieger, E., van der Loo, B., Amann-Vesti, B. R., Rousson, V., & Koppensteiner, R. (2004) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2004.07.004 · Cited by 33

Authors: Fichtlscherer, S., Rosenberger, G., Walter, D. H., Breuer, S., Dimmeler, S., & Zeiher, A. M.
Affiliations: Goethe University Frankfurt (DE)
ORCID: Walter, Dirk H.
Dimmeler, Stefanie
Zeiher, Andreas M.
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2000-08-29
Volume: 102
Issue: 9
Pages: 1000-1006
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/01.cir.102.9.1000
OpenAlex: W2076633296
Cited by: 665
References: 25
Citations by year: 2026: 3 · 2025: 4 · 2024: 5 · 2023: 8 · 2022: 9 · 2021: 14 · 2020: 11 · 2019: 11 · 2018: 17 · 2017: 16 · 2016: 18 · 2015: 18 · 2014: 26 · 2013: 27 · 2012: 21
FWCI: 23.45
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Keywords: C-reactive protein, coronary artery disease, endothelial dysfunction, endothelium-dependent vasodilation, acetylcholine response, forearm blood flow, systemic inflammation, cardiovascular risk factors, atherosclerosis, sodium nitroprusside
MeSH terms: Acetylcholine, Adrenergic beta-Antagonists, Aspirin, Brachial Artery, C-Reactive Protein, Coronary Disease, Endothelium, Vascular, Follow-Up Studies, Forearm, Humans, Inflammation, Infusions, Intra-Arterial, Male, Middle Aged, Nitroprusside, Regional Blood Flow, Risk Factors, Vasodilation, Vasodilator Agents, Biomarkers, Multivariate Analysis

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Elevated C-Reactive Protein Levels and Impaired Endothelial Vasoreactivity in Patients With Coronary Artery Disease

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