Original Article
Evidence of Impaired Endothelium-Dependent Coronary Vasodilatation in Patients with Angina Pectoris and Normal Coronary Angiograms
N Engl J Med 1993; 328:1659-1664June 10, 1993
- Abstract
Background
A group of patients has been described who have chest pain resembling angina and positive exercise tests, but normal coronary angiograms and no coronary-artery spasm. This constellation of features has sometimes been called syndrome X or microvascular angina. We attempted to determine whether endothelium-dependent vasodilatation of the coronary vasculature was impaired in patients with this syndrome.
Methods
We infused the endothelium-dependent vasodilator acetylcholine and the endothelium-independent vasodilators papaverine and isosorbide dinitrate into the left coronary artery of 9 patients and 10 control subjects. The diameter of the left anterior descending coronary artery was assessed by quantitative angiography, and changes in coronary blood flow were estimated with the use of an intracoronary Doppler catheter.
Results
Acetylcholine, given in doses of 1, 3, 10, and 30 μg per minute, increased coronary blood flow in a dose-dependent manner in both groups. However, the mean (±SD) acetylcholine-induced increases in coronary blood flow were significantly less (P<0.001) in the patients (8 ±14, 37 ±37, 59 ±67, and 103 ±77 percent, respectively) than in the controls (62 ±52, 186 ±93, 341 ±128, and 345 ±78 percent, respectively). The changes in coronary blood flow in response to 2 mg of isosorbide dinitrate (236 ±66 percent vs. 280 ±56 percent) and 10 mg of papaverine (366 ±168 percent vs. 411 ±92 percent) did not differ significantly between the patients and controls. The administration of papaverine resulted in myocardial lactate production in the patients but not in the controls. The three lower doses of acetylcholine caused a similar degree of dilatation of the left anterior descending coronary artery in the two groups, and the highest dose caused a similar degree of constriction in the two groups. Isosorbide dinitrate and papaverine caused a similar degree of dilatation in both groups.
Conclusions
These findings suggest that endothelium-dependent dilatation of the resistance coronary arteries is defective in patients with anginal chest pain and normal coronary arteries, which may contribute to the altered regulation of myocardial perfusion in these patients.
Media in This Article
Figure 1
Change in the Diameter of Proximal and Distal Coronary Arteries Produced by an Intracoronary Infusion of Graded Doses of Acetylcholine in Control Subjects and Patients with Microvascular Angina.Figure 2
Increase in Coronary Blood Flow Evoked by Graded Doses of Acetylcholine in Control Subjects and Patients with Microvascular Angina.Article Activity
- Article
A group of patients who have angina-like chest pain, ischemic ST-segment depressions on their electrocardiograms during exercise testing, angiographically normal coronary arteries without coronary-artery spasm, and normal ventricular function has been described by many investigators1-3. Some patients with this constellation of findings (sometimes called syndrome X) have attenuated coronary flow reserve in response to metabolic or pharmacologic vasodilator stimuli (i.e., microvascular angina)2,3. The implication is that an abnormality in the microvasculature may be the cause of this syndrome. The impairment of coronary flow reserve may result from either abnormal vasomotion of the coronary microcirculation or structural microvascular disease, since the increase in myocardial blood flow evoked by atrial pacing or intravenous dipyridamole is limited in these patients2-6. The mechanisms underlying the abnormal vasomotion in these patients are unknown, but they may relate to defective endothelial function, inappropriate vasoconstriction, or both.
There is now ample evidence indicating that endothelium-derived vasoactive substances play an important part in regulating not only the vasomotion of the large epicardial coronary arteries but also coronary blood flow (which is regulated by the small resistance vessels)7-9. Recently, it has been suggested that endothelium-dependent dilatation of resistance vessels in coronary and other vascular beds is impaired in hypertension and hypercholesterolemia10-13. Therefore, altered endothelium-dependent vasomotion of coronary resistance vessels may contribute to the cause of angina-like chest pain in patients with normal coronary arteries. The present study attempted to determine whether endothelium-dependent vasodilatation of coronary resistance vessels was impaired in patients with this syndrome.
Methods
Study Patients
Nine patients with angina-like chest pain and normal coronary arteries and 10 control subjects with atypical chest pain and normal coronary arteries were studied. The criteria that we used to define the syndrome were angina-like chest pain, positive exercise tests (>0.1 mV of ST-segment depression in two or more leads), angiographically normal coronary arteries, and no spasm of the large epicardial coronary arteries. In this study, we enrolled patients with this syndrome in whom an intracoronary infusion of 10 mg of papaverine evoked the myocardial production of lactate. The control subjects had atypical chest pain, normal exercise tests, and angiographically normal coronary arteries without spasm. In six control subjects, myocardial lactate was not produced in response to intracoronary papaverine; in the other four control subjects, sampling of arterial and coronary sinus venous blood could not be done.
All patients were normotensive and had no evidence of left ventricular hypertrophy as assessed by electrocardiography, echocardiography, and contrast left ventriculography. None of the patients were receiving antihypertensive or cholesterol-lowering drugs. The left-ventricular-mass index was determined by biplanar left ventriculography14. Patients with hypercholesterolemia (total cholesterol level, >220 mg per deciliter [5.7 mmol per liter]), diabetes mellitus, cardiomyopathy, valvular heart disease, or a conduction disturbance on electrocardiography were excluded. Hypercholesterolemia was assessed from duplicate measurements of serum total cholesterol levels performed within a month of each other. We confirmed that all patients had a total cholesterol level of less than 220 mg per deciliter three months after the study. Patients who had angiographically documented coronary-artery spasm in any coronary-artery segment (reduction in the diameter to <50 percent of the base line) in response to the intracoronary infusion of acetylcholine (100 μg per minute) or ergonovine (50 μg per minute) were also excluded.
The research proposal was approved by the institutional review committee for clinical research. Written informed consent was obtained from each patient after the study protocol was explained.
Quantitative Coronary Arteriography
Coronary cineangiograms were recorded on 35-mm cinefilm (60 frames per second) with a cineangiographic system (Siemens, Erlangen, Germany). Non-ionic contrast material (iohexol 350) was used. An appropriate view that allowed the best visualization of the left anterior descending coronary artery (the study artery) was selected.
An end-diastolic frame was selected on the cineprojector, and the arterial segments under study were scanned with a video camera. The images were digitized and analyzed with a videodensitometric analysis system15 (Kontron Instruments, Dortmund, Germany). The diameter of the segment of interest (3 to 4 mm in length) was measured four times, and the average value was used for analysis. The diameter of the Judkins catheter was used to calibrate the arterial diameter in millimeters. The arterial diameters were measured blindly.
We measured the changes in the luminal diameter of the proximal and distal segments of the left anterior descending coronary artery. The proximal segment was defined as a segment 3 to 4 mm distal to the tip of the Doppler catheter, and the distal segment as that distal to the second or third diagonal branch.
Measurements of Coronary Blood Flow Velocity and Blood Flow
An 8-French angioplasty-guiding catheter was introduced into the left main coronary artery by a femoral approach. A 3-French Doppler flow-velocity catheter (model DC-201, Millar Instruments, Houston) was introduced into the proximal left anterior descending coronary artery. The Doppler catheter was then connected to a DC-101 velocimeter (Millar Instruments) to measure mean and phasic velocity signals. The use of this device to assess coronary blood flow velocity in humans has been described elsewhere13,16-18. Coronary blood flow was estimated from the product of the mean coronary blood flow velocity and the cross-sectional area of the proximal arterial segment at the tip of the Doppler catheter.
Study Protocol
Cardiac catheterization was performed in the patients after an overnight fast; the patients were premedicated with a 5-mg oral dose of diazepam. All antianginal medications were discontinued at least 24 hours before the study.
After the diagnostic catheterization was completed, the following interventions were performed in a random order: a bolus injection of papaverine (10 mg per 5 ml; Dai-Nippon Pharmaceutical, Tokyo, Japan) was administered through the guiding catheter, saline (0.5 ml per minute for two minutes) was infused through the Doppler catheter, and acetylcholine (0.5 ml per minute; Dai-Ichi Pharmaceutical, Tokyo) was infused at doses of 1, 3, 10, and 30 μg per minute (for two minutes at each dose) through the Doppler catheter. Finally, a 2-mg dose of isosorbide dinitrate (2 mg per 4 ml; Ei-Zai Pharmaceutical, Tokyo) was infused through the guiding catheter over a one-minute period. In three patients who had a limited response of coronary blood flow (<300 percent -- the lower limit of the normal range in our laboratory) to a 10-mg dose of papaverine, we administered an additional 14-mg dose of papaverine and found that the response of coronary blood flow to this dose was not greater than that to the 10-mg dose. Thus, the data obtained with the 10-mg dose of papaverine were used for analysis.
After completing the protocol with one drug, we waited for at least five minutes before beginning the infusion of the next drug, by which time the coronary diameter and coronary blood flow velocity had returned to the base-line values. Coronary arteriography was performed before and two minutes after the administration of each agent. Coronary blood flow velocity, arterial pressure, heart rate, and electrocardiograms were continuously monitored and recorded on a polygraph system (Nihon-Kohden, Tokyo). The values obtained during a steady-state condition were used for analysis.
In all nine patients and six of the control subjects, a catheter was inserted into the coronary sinus vein. Paired samples of arterial and coronary sinus venous blood were taken before and two minutes after the administration of papaverine (10 mg) and acetylcholine (30 μg per minute) for the measurement of plasma lactate. The plasma lactate concentration was measured immediately after sampling with a calibrated lactate analyzer (OMRON, Tokyo). The average value of duplicate measurements was used for analysis.
Statistical Analysis
Data are expressed as means ±SD. When serial changes in the arterial pressure, heart rate, arterial diameter, and coronary blood flow were compared within a group or between the groups, analysis of variance for repeated measures followed by Bonferroni's multiple-comparison test was used19. Student's t-tests were used to compare paired or unpaired data. A two-tailed probability level of less than 0.05 was considered to indicate significance.
Results
Clinical Characteristics and Measurements
Clinical characteristics such as age, sex, arterial pressure, smoking status, left-ventricular-mass index, and previous medications are presented in Table 1Table 1
Clinical Characteristics of the Control Subjects and the Patients with Microvascular Angina., all of which were comparable between the two groups. The base-line mean arterial pressure was 89 ±11 mm Hg in the control subjects and 84 ±11 mm Hg in the patients (P>0.5). A 10-mg dose of papaverine insignificantly decreased the mean arterial pressure in the control subjects (to 82 ±6 mm Hg, P = 0.13) and in the patients (to 80 ±7 mm Hg, P = 0.4). An infusion of acetylcholine (1 to 30 μg per minute) did not affect the mean arterial pressure in either group.The base-line heart rate was 69 ±12 beats per minute in the control subjects and 72 ±12 beats per minute in the patients (P>0.5). The heart rate did not change significantly during the study.
Changes in the Diameter of the Left Anterior Descending Coronary Artery
The base-line diameters of the proximal and distal arterial segments were 2.9 ±0.4 and 1.8 ±0.3 mm, respectively, in the control subjects and 3.0 ±0.4 mm and 1.9 ±0.4 mm, respectively, in the patients (P>0.5 for the difference between groups). An intracoronary infusion of saline did not change the arterial diameters. The administration of acetylcholine produced biphasic changes in the arterial diameters. In both groups, the diameter of the proximal and distal segments of the study artery increased significantly after the infusion of acetylcholine at a dose of 10 μg per minute (P = 0.01) and decreased after a dose of 30 μg per minute (P<0.01 by one-way analysis of variance). The percent changes in the arterial diameter induced by the graded doses of acetylcholine did not differ significantly between the two groups (Figure 1Figure 1
Change in the Diameter of Proximal and Distal Coronary Arteries Produced by an Intracoronary Infusion of Graded Doses of Acetylcholine in Control Subjects and Patients with Microvascular Angina.). A 2-mg dose of isosorbide dinitrate caused a comparable degree of dilatation of the proximal and distal arterial diameters in the control subjects (21.2 ±3.8 percent and 25.0 ±5.4 percent, respectively) and the patients (29.1 ±4.5 percent and 31.9 ±6.6 percent, respectively) (P>0.5 for the difference between groups). A 10-mg dose of papaverine also caused a comparable degree of dilatation of the proximal and distal arterial segments in the patients (8.1 ±4.0 percent and 11.3 ±4.6 percent, respectively) and the controls (6.4 ±3.9 percent and 9.2 ±3.6 percent, respectively) (P>0.5 for the difference between groups).Changes in Coronary Blood Flow
The percent increases in estimated coronary blood flow evoked by acetylcholine, papaverine, and isosorbide dinitrate in each patient are presented in Table 2Table 2
Changes in Estimated Coronary Blood Flow Produced by Papaverine, Acetylcholine, and Isosorbide Dinitrate in the Control Subjects and Patients with Microvascular Angina.. The infusion of saline did not alter coronary blood flow (Figure 2Figure 2Increase in Coronary Blood Flow Evoked by Graded Doses of Acetylcholine in Control Subjects and Patients with Microvascular Angina.). The administration of graded doses of acetylcholine resulted in dose-dependent increases in coronary blood flow, but the progressive increases in coronary blood flow in the patients were significantly (P<0.001 by analysis of variance) less than those in the control subjects (Figure 2). There was no significant difference in the percent increases in coronary blood flow in response to papaverine between the control subjects and the patients (411 ±92 percent vs. 366 ±168 percent, P = 0.47). The percent increase in coronary blood flow produced by isosorbide dinitrate did not differ significantly between the control subjects and the patients (280 ±56 percent vs. 236 ±66 percent, P = 0.2).Plasma Lactate Concentrations
Paired samples of coronary arterial and coronary sinus venous blood were obtained from six of the control subjects and all nine of the patients. The plasma concentrations of lactate in arterial and coronary sinus venous blood before the administration of papaverine were 7.3 ±2.0 and 5.3 ±1.4 mg per deciliter, respectively, in the control subjects and 6.2 ±1.8 and 4.4 ±0.9 mg per deciliter, respectively, in the patients (P>0.5 for the difference between groups). The lactate-extraction ratio ([arterial lactate concentration - venous lactate concentration]/arterial lactate concentration × 100 [%]) before and after the intracoronary infusion of papaverine was 24.0 ±8.1 percent (range, 10 to 32 percent) and 14.0 ±4.2 percent (range, 8 to 18 percent) in the control subjects and 25.9 ±7.5 percent (range, 15 to 41 percent) and -13.4 ±11.2 percent (range, -1 to -30 percent) in the patients, indicating that myocardial production of lactate occurred in response to papaverine in the patients but not in the control subjects.
After the intracoronary infusion of papaverine, six of the nine patients had anginal chest pain, with ischemic ST-segment depression ( ≥ 0.2 mV) in leads V3 through V6, II, III, and aVF, whereas none of the control subjects had chest pain or ST-segment changes. Ventricular tachycardia developed in one of the patients after a 14-mg dose of papaverine and resolved spontaneously. No other adverse events, except prolongation of the QT interval, occurred after the administration of papaverine.
Discussion
In this study, we assumed that acetylcholine increased coronary blood flow by causing endotheliumdependent dilatation of the coronary vasculature. This assumption is tenable because the vasodilative responses of the coronary and forearm vascular beds in humans to acetylcholine can be prevented by methylene blue, which inhibits guanylate cyclase in vascular smooth muscle,20 and by L-arginine analogues, which inhibit the synthesis of nitric oxide (an endothelium-derived relaxing factor) from L-arginine in endothelial cells21,22.
Our most important finding was that in patients with angina and normal coronary arteries, there was marked attenuation of the increase in coronary blood flow evoked by intracoronary acetylcholine, whereas the increase in coronary blood flow in response to isosorbide dinitrate and papaverine was not affected. These findings suggest that endothelium-dependent vasodilatation of resistance coronary vessels was impaired in our patients with angina and normal coronary arteries.
Motz et al.23 examined the responses of coronary blood flow to acetylcholine and dipyridamole in 23 patients with angina and normal coronary arteries. They showed that in eight patients the response to acetylcholine was less than the response to dipyridamole, suggesting defective endothelium-dependent vasodilatation. Another 12 patients had similar responses to the two agents, whereas 3 had coronary spasm provoked by acetylcholine. Their findings are suggestive of defective endothelium-dependent vasodilatation in some patients with angina and normal coronary arteries and are consistent with our results. However, many of their patients had arterial hypertension and diabetes mellitus, which are known to impair endothelium-dependent vasodilatation7-9,11-13. We excluded patients with hypertension, hypercholesterolemia, diabetes mellitus, and other coronary risk factors from the study. Thus, the difference between the results of Motz et al. and our own might be related to the patient populations.
We observed myocardial lactate production in our patients during the infusion of papaverine -- a response that suggests myocardial ischemia results from a microvascular abnormality not dependent on the endothelium. Thus, our patients represent a subgroup of patients with angina and normal coronary arteries who met strict inclusion criteria. Myocardial production of lactate and increased coronary blood flow during the infusion of papaverine may seem paradoxical. With the use of cardiac positron-emission tomography, Galassi et al.6 demonstrated that the increase in myocardial perfusion after the administration of dipyridamole was not uniform in patients with angina and normal coronary arteries but was uniform in the control subjects. Other investigators have proposed that the abnormality of the coronary microcirculation responsible for myocardial ischemia in patients with microvascular angina may be distributed unevenly in the heart2,3,24. Thus, we consider that uneven dilatation of prearteriolar coronary arteries resulting in inhomogeneous myocardial perfusion during the infusion of papaverine may have resulted in a “steal phenomenon,” with ensuing ischemia in patients with microvascular angina. Anginal pain developed in six of our nine patients in association with ST-segment depression during the infusion of papaverine, suggesting that they indeed had myocardial ischemia. However, further studies, such as radionuclide ventriculography during the infusion of papaverine or exercise, are needed to confirm that myocardial ischemia results from a microvascular abnormality in these patients.
Christensen et al. have recently shown in dogs that the intracoronary infusion of papaverine caused myocardial lactate production and an abnormal contractile pattern despite the increase in coronary blood flow25. This result suggests that lactate production during papaverine infusion may not be a pathologic finding. However, other studies in normal dogs did not report abnormal myocardial systolic function during the intracoronary infusion of papaverine26,27. Importantly, we found that the infusion of papaverine evoked myocardial lactate production only in the patients, suggesting that this response was related to an abnormality in the coronary microcirculation.
In addition to studying endothelium-dependent vasodilatation of resistance coronary arteries, we also examined the effects of acetylcholine on the caliber of a large epicardial coronary artery. As shown in previous studies,28-31 lower doses of acetylcholine induced vasodilatation, but a high dose caused vasoconstriction. This biphasic response of the large coronary artery to acetylcholine did not differ between the patients and the control subjects. These results suggest that the endothelium-dependent vasodilatation of large coronary arteries produced by acetylcholine was not altered in the patients with angina and normal coronary arteries. More important, the results indicate that the attenuated response of coronary blood flow to acetylcholine in our patients did not result from excessive vasoconstriction of the large coronary arteries. Our results differ in part from those of Vrints et al.,32 who found that patients with angina pectoris and normal coronary arteries had a loss of endothelium-dependent dilatation of the large coronary arteries with acetylcholine. The reason for the different responses in our study and the study by Vrints et al.32 is not known, but it may be related either to differences in the patient populations or to differences in the dose of acetylcholine. It has been shown that many factors, such as coronary risk factors, age, and the presence of atherosclerosis, alter the response of epicardial coronary arteries to acetylcholine10-13.
We consider that the attenuated response of coronary blood flow to acetylcholine, but the intact response of coronary blood flow to papaverine and isosorbide dinitrate, in our patients suggests defective endothelium-dependent vasodilatation of resistance coronary arteries. However, we must consider the possibility that the impaired response of coronary blood flow to acetylcholine may have resulted from augmented microvascular vasoconstriction, because acetylcholine not only releases endothelium-derived relaxing factors but also has a direct vasoconstricting action7-9. Acetylcholine-induced coronary-artery spasm may be caused by direct vasoconstriction, defective endothelium-dependent vasodilatation, or both33-35. It is also possible that the impaired response of coronary blood flow to acetylcholine could be related to the concomitant release of endothelium-derived constricting factors7-9. Further studies are needed to clarify the underlying mechanisms of the attenuated response of coronary blood flow to acetylcholine in patients with microvascular angina. The use of a drug such as substance P35 would be more appropriate to assess dysfunction of the coronary microvascular endothelium, since substance P does not act directly on vascular smooth muscle.
In conclusion, our results indicate that a subgroup of patients with angina and normal coronary arteries (microvascular angina) have an attenuated response of coronary blood flow to acetylcholine. Defective endothelium-dependent dilatation in the coronary microcirculation may contribute to the altered regulation of myocardial perfusion and the ischemic manifestations in these patients.
Supported in part by grants-in-aid for scientific research (02404045 and 02454259); by a grant-in-aid for scientific research on priority areas (03268226) from the Ministry of Education, Science and Culture, Tokyo, Japan; by a research development award from the Japan Heart Foundation, Tokyo; and by a research grant for 1992 from the Naito Memorial Foundation, Tokyo.
Source Information
From the Research Institute of Angiocardiology and the Cardiovascular Clinic, Kyushu University School of Medicine, 3-1-1, Maidashi, Higashi-ku, Fukuoka 812, Japan, where reprint requests should be addressed to Dr. Egashira.
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