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Prognostic Value of Coronary Vascular Endothelial Dysfunction
Abstract
Background — Whether patients at increased risk can be identified from a relatively low-risk population by coronary vascular function testing remains unknown. We investigated the relationship between coronary endothelial function and the occurrence of acute unpredictable cardiovascular events (cardiovascular death, myocardial infarction, stroke, and unstable angina) in patients with and without coronary atherosclerosis (CAD). Methods and Results — We measured the change in coronary vascular resistance (ΔCVR) and epicardial diameter with intracoronary acetylcholine (ACh, 15 μg/min) to test endothelium-dependent function and sodium nitroprusside (20 μg/min) and adenosine (2.2 mg/min) to test endothelium-independent vascular function in 308 patients undergoing cardiac catheterization (132 with and 176 without CAD). Patients underwent clinical follow-up for a mean of 46±3 months. Acute vascular events occurred in 35 patients. After multivariate analysis that included CAD and conventional risk factors for atherosclerosis, ΔCVR with ACh ( P =0.02) and epicardial constriction with ACh ( P =0.003), together with increasing age, CAD, and body mass index, were independent predictors of adverse events. Thus, patients in the tertile with the best microvascular responses with ACh and those with epicardial dilation with ACh had improved survival by Kaplan-Meier analyses in the total population, as did those in the subset without CAD. Similar improvement in survival was also observed when all adverse events, including revascularization, were considered. Endothelium-independent responses were not predictive of outcome. Conclusions — Epicardial and microvascular coronary endothelial dysfunction independently predict acute cardiovascular events in patients with and without CAD, providing both functional and prognostic information that complements angiographic and risk factor assessment.
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“Endothelial dysfunction occurs early in the pathogenesis of atherosclerosis, and predicts future cardiovascular events.”
From The Vasculature in Prediabetes (2018) · cites this paper as [32]
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Is Flow-Mediated Dilation Nitric Oxide Mediated?
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Invasive Evaluation of Patients With Angina in the Absence of Obstructive Coronary Artery Disease
Lee, B., Lim, H., Fearon, W. F., Yong, A. S. C., Yamada, R., Tanaka, S., Lee, D. P., Yeung, A. C., & Tremmel, J. A. (2015) · Circulation · doi:10.1161/circulationaha.114.012636 · Cited by 360
2007 ESH‐ESC Guidelines for the management of arterial hypertension
Mansia, G., Backer, G. D., Dominiczak, A. F., Cífková, R., Fagard, R. H., Germanò, G., Grassi, G. M., Heagerty, A. M., Kjeldsen, S. E., Laurent, S., et al. (2007) · Blood Pressure · doi:10.1080/08037050701461084 · Cited by 361
“Endothelial dysfunction predicts outcome in several cardiovascular diseases, (237,238) although data on hypertension are still rather scant.”
BackgroundEndothelial Function Predicts Future Development of Coronary Artery Disease
Bugiardini, R., Manfrini, O., Pizzi, C., Fontana, F., & Morgagni, G. (2004) · Circulation · doi:10.1161/01.cir.0000128208.22378.e3 · Cited by 347
Endothelial dysfunction over the course of coronary artery disease
Gutiérrez, E., Flammer, A. J., Lerman, L. O., Elı́zaga, J., Lerman, A., & Fernández‐Avilés, F. (2013) · European Heart Journal · doi:10.1093/eurheartj/eht351 · Cited by 334
“Abnormal response to selective intracoronary acetylcholine infusion, both in the epicardial and microvascular circulation, was an independent predictor of MACE, even after adjusting for the presence of CAD.51 Another study in 281 patients with documented CAD showed that peripheral endothelial dysfunction also identifi…”
BackgroundAge-related Impairment of Vascular Structure and Functions
Xu, X., Wang, B. Z., Ren, C., Hu, J., Greenberg, D. A., Chen, T., Xie, L., & Jin, K. (2017) · Aging and Disease · doi:10.14336/ad.2017.0430 · Cited by 365
“Endothelial dysfunction is a key antecedent of clinical vascular disease and may serve as a predictive and potential diagnostic marker of disease [221, 222].”
BackgroundSaam, T., Hatsukami, T. S., Takaya, N., Chu, B., Underhill, H. R., Kerwin, W. S., Cai, J., Ferguson, M. S., & Yuan, C. (2007) · Radiology · doi:10.1148/radiol.2441051769 · Cited by 329
“Studies have shown that endothelial dysfunction is associated with coronary heart disease and stroke (88,89).”
BackgroundGutterman, D. D., Chabowski, D. S., Kadlec, A. O., Durand, M. J., Freed, J. K., Ait‐Aissa, K., & Beyer, A. (2016) · Circulation Research · doi:10.1161/circresaha.115.305364 · Cited by 336
Chan, S., Mancini, G. B. J., Kuramoto, L., Schulzer, M., Frohlich, J. J., & Ignaszewski, A. P. (2003) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(03)00927-6 · Cited by 327
“(5), using coronary infusions of acetylcholine at the time”
MethodEndothelial Function Predicts Progression of Carotid Intima-Media Thickness
Halcox, J., Donald, A. E., Ellins, E. A., Witte, D. R., Shipley, M. J., Brunner, E. J., Marmot, M. G., & Deanfield, J. E. (2009) · Circulation · doi:10.1161/circulationaha.108.765701 · Cited by 322
“This is in keeping with our previous findings that the negative predictive value of the test results was most powerful.(16) Our data do not currently support a role for FMD testing in routine cardiovascular risk assessment, but wider evaluation with standardized, high-quality testing protocols is warranted.”
ResultSelf-citationLekakis, J. P., Abraham, P., Balbarini, A., Blann, A. D., Boulanger, C. M., Cockcroft, J., Cosentino, F., Deanfield, J. E., Gallino, A., Ikonomidis, I., et al. (2011) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1177/1741826711398179 · Cited by 322
“Epicardial and microvascular coronary endothelial dysfunction is an independent predictor of acute cardiovascular events irrespective of presence or absence of angiographically detectable coronary lesions.(9,10) Assessment of coronary endothelial function is particularly important in cardiac transplant recipients beca…”
BackgroundObesity, Insulin Resistance, and the Metabolic Syndrome
Lteif, A. A., Han, K., & Mather, K. J. (2005) · Circulation · doi:10.1161/circulationaha.104.520130 · Cited by 308
Montezano, A. C. I., & Touyz, R. M. (2011) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2011.00785.x · Cited by 320
Regulation of Coronary Blood Flow
Goodwill, A. G., Dick, G. M., Kiel, A. M., & Tune, J. D. (2017) · Comprehensive physiology · doi:10.1002/cphy.c160016 · Cited by 358
“As such, coronary endothelial dysfunction is associated with many cardiovascular-related diseases (71, 614, 644, 779, 780) and thus it is not surprising that impaired endothelial function independently predicts acute cardiovascular events in patients with and without atherosclerotic disease (433).”
Padró, T., Manfrini, O., Bugiardini, R., Canty, J. M., Cenko, E., Luca, G. D., Duncker, D. J., Eringa, E. C., Koller, Á., Tousoulis, D., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa003 · Cited by 298
“Thus, endothelial dysfunction is significantly associated with diffuse epicardial vasoconstrictor response following intracoronary infusion of acetylcholine with adverse cardiovascular events.(66) Assessment of endothelial function may identify early changes in vasoactive functions relevant in the development of ather…”
BackgroundCoronary Endothelial Dysfunction Is Associated With an Increased Risk of Cerebrovascular Events
Targonski, P. V., Bonetti, P. O., Pumper, G. M., Higano, S. T., Holmes, D. R., & Lerman, A. (2003) · Circulation · doi:10.1161/01.cir.0000072765.93106.ee · Cited by 296
“Hypercholesterolemia, n (%) 66 (33) 133 (44) Hypertension, n (%) 66 (33) 103 (34) Diabetes, n (%) 14 (7) 25 (8) Smoking, n (%) 32 (16) 53 (17) Obesity, n (%) 43 (22) 79 (26) Myocardial infarction, n (%) 15 (8) 29 (10) Atrial fibrillation, n (%) 7 (4) 16 (5) Aspirin, n (%) 68 (34) 130 (43) Warfarin, n (%) 7 (4) 21 (7)…”
Assessment of atherosclerosis: the role of flow-mediated dilatation
Charakida, M., Masi, S., Lüscher, T. F., Kastelein, J. J. P., & Deanfield, J. E. (2010) · European Heart Journal · doi:10.1093/eurheartj/ehq340 · Cited by 292
“The value of FMD as an intermediated phenotype and as an outcome measure in trials is based on its relationship with CV risk factors (see above), with progression of arterial disease and adverse prognosis.(4,30,62) Evidence that endothelial function is on the causal pathway for”
BackgroundBisoendial, R. J., Hovingh, G. K., Levels, J. H. M., Lerch, P. G., Andresen, I., Hayden, M. R., Kastelein, J. J. P., & Stroes, E. S. G. (2003) · Circulation · doi:10.1161/01.cir.0000070934.69310.1a · Cited by 287
Surrogate Markers for Cardiovascular Disease
Cohn, J. N., Quyyumi, A. A., Hollenberg, N. K., & Jamerson, K. (2004) · Circulation · doi:10.1161/01.cir.0000133442.99186.39 · Cited by 288
Self-citationNADPH oxidase and endothelial cell function
Ray, R., & Shah, A. M. (2005) · Clinical Science · doi:10.1042/cs20050067 · Cited by 280
Hyde, E. R., Andrade, F., Vaksman, Z., Parthasarathy, K., Jiang, H., Parthasarathy, D. K., Torregrossa, A. C., Tribble, G., Kaplan, H. B., Petrosino, J. F., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088645 · Cited by 275
“cardiovascular risk factors [5], is causal for endothelial dysfunction, and serves as a profound predictive factor for future atherosclerotic disease progression [6,7,8,9] and cardiovascular events [10,11].”
BackgroundIndoor Particles Affect Vascular Function in the Aged
Bräuner, E. V., Forchhammer, L., Möller, P., Barregård, L., Gunnarsen, L., Afshari, A., Wåhlin, P., Glasius, M., Dragsted, L. O., Basu, S., et al. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200704-632oc · Cited by 264
“EF constitutes an independent predictor of cardiovascular events (24, 25), and the clinical implications of endothelial dysfunction and the association between endothelial cell dysfunction and cardiac events are well established (26, 27).”
BackgroundObstructive Coronary Atherosclerosis and Ischemic Heart Disease: An Elusive Link!
Marzilli, M., Merz, C. N. B., Boden, W. E., Bonow, R. O., Capozza, P., Chilian, W. M., DeMaria, A. N., Guarini, G., Huqi, A., Morrone, D., et al. (2012) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2012.02.082 · Cited by 265
Roman, M. J., Naqvi, T. Z., Gardin, J. M., Gerhard‐Herman, M. D., Jaff, M. R., & Mohler, E. R. (2006) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2006.04.020 · Cited by 260
Endothelial function, inflammation, and prognosis in cardiovascular disease
Gonzalez, M. A., & Selwyn, A. P. (2003) · The American Journal of Medicine · doi:10.1016/j.amjmed.2003.09.016 · Cited by 263
Endothelium‐dependent contractions and endothelial dysfunction in human hypertension
Versari, D., Daghini, E., Virdis, A., Ghiadoni, L., & Taddei, S. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00240.x · Cited by 260
“, 2003) and central circulation (Schachinger et al., 2000; Suwaidi et al., 2000; Halcox et al., 2002; Schindler et al., 2003; Targonski et al., 2003), in microcirculation (Heitzer et al.”
BackgroundInfluentialPrognostic Value of Systemic Endothelial Dysfunction in Patients With Acute Coronary Syndromes
Fichtlscherer, S., Breuer, S., & Zeiher, A. M. (2004) · Circulation · doi:10.1161/01.cir.0000143378.58099.8c · Cited by 251
Endothelial dysfunction and coronary artery disease: assessment, prognosis, and treatment
Matsuzawa, Y., & Lerman, A. (2014) · Coronary Artery Disease · doi:10.1097/mca.0000000000000178 · Cited by 249
Testing Endothelial Vasomotor Function
Ganz, P., & Vita, J. A. (2003) · Circulation · doi:10.1161/01.cir.0000089507.19675.f9 · Cited by 246
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“Moreover, it has been shown to be an independent predictor of future CV events providing valuable prognostic information additional to that derived from traditional risk factors [54].”
BackgroundGonzález‐Juanatey, C., Llorca, J., Testa, A., Revuelta, J., Garcı́a-Porrúa, C., & González-Gay, M. Á. (2003) · Medicine · doi:10.1097/01.md.0000101572.76273.60 · Cited by 238
Metadata
- Authors
- Halcox, J. P. J., Schenke, W. H., Zalos, G., Mincemoyer, R., Prasad, A., Waclawiw, M. A., Nour, K. R. A., & Quyyumi, A. A.
- Affiliations
- National Institutes of Health (US)
- Venue
- Circulation
- Published
- 2002-08-06
- Volume
- 106
- Issue
- 6
- Pages
- 653-658
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W2019338486
- Cited by
- 1,385
- References
- 24
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 25 · 2023: 33 · 2022: 21 · 2021: 33 · 2020: 49 · 2019: 50 · 2018: 56 · 2017: 51 · 2016: 51 · 2015: 70 · 2014: 87 · 2013: 59 · 2012: 70
- FWCI
- 51.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Cardiac Imaging and Diagnostics
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Keywords
- coronary endothelial dysfunction, coronary artery disease, acetylcholine provocation test, sodium nitroprusside, adenosine, coronary vascular resistance, cardiovascular events, prognosis, myocardial infarction, unstable angina, stroke, cardiovascular mortality, revascularization
- MeSH terms
- Angina, Unstable, Coronary Artery Disease, Coronary Circulation, Coronary Vessels, Endothelium, Vascular, Female, Follow-Up Studies, Humans, Male, Microcirculation, Middle Aged, Myocardial Infarction, Pericardium, Prognosis, Vascular Resistance, Vasodilator Agents, Disease-Free Survival, Stroke
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