Original Article
Abnormal Endothelium-Dependent Vascular Relaxation in Patients with Essential Hypertension
N Engl J Med 1990; 323:22-27July 5, 1990
- Abstract
- Abstract
Background.
Endothelium regulates vascular tone by influencing the contractile activity of vascular smooth muscle. This regulatory effect of the endothelium on blood vessels has been shown to be impaired in atherosclerotic arteries in humans and animals and in animal models of hypertension.
Methods.
To determine whether patients with essential hypertension have an endothelium-dependent abnormality in vascular relaxation, we studied the response of the forearm vasculature to acetylcholine (an endotheliumdependent vasodilator) and sodium nitroprusside (a direct dilator of smooth muscle) in 18 hypertensive patients (mean age[±SD], 50.7± 10 years; 10 men and 8 women) two weeks after the withdrawal of antihypertensive medications and in 18 normal controls (mean age, 49.9±9; 9 men and 9 women). The drugs were infused at increasing concentrations into the brachial artery, and the response in forearm blood flow was measured by strain-gauge plethysmography.
Results.
The basal forearm blood flow was similar in the patients and controls (mean ±SD, 3.4±1.3 and 3.7±0.8 ml per minute per 100 ml of forearm tissue, respectively; P not significant). The responses of blood flow and vascular resistance to acetylcholine were significantly reduced in the hypertensive patients (P<0.0001); maximal forearm flow was 9.1 ±5 ml per minute per 100 ml in the patients and 20.0±8 ml per minute per 100 ml in the controls (P<0.0002). However, there were no significant differences between groups in the responses of blood flow and vascular resistance to sodium nitroprusside. Because the vasodilator effect of acetylcholine might also be due to presynaptic inhibition of the release of norepinephrine by adrenergic nerve terminals, the effect of acetylcholine was assessed during phentolamine-induced α-adrenergic blockade. Under these conditions, it was also evident that the responses to acetylcholine were significantly blunted in the hypertensive patients (P<0.03).
Conclusions.
Endothelium-mediated vasodilation is impaired in patients with essential hypertension. This defect may play an important part in the functional abnormalities of resistance vessels that are observed in hypertensive patients. (N Engl J Med 1990; 323:22–7.)
Media in This Article
Figure 1
Responses of Forearm Blood Flow and Vascular Resistance to Acetylcholine in 18 Normal Controls (Open Circles) and 18 Hypertensive Patients (Solid Circles).Figure 2
Responses of Forearm Blood Flow and Vascular Resistance to Sodium Nitroprusside in 18 Normal Controls (Open Circles) and 18 Hypertensive Patients (Solid Circles).Article Activity
- Article
The importance of the endothelium in modulating the activity of vascular smooth muscle and therefore in regulating vascular tone was first suggested by the pioneering studies of Furchgott and Zawadzki.1 These authors reported that the damage or absence of endothelial cells curtails the vasodilator action of acetylcholine and other substances2 that is normally observed when the endothelium is intact. Endothelium-depcndent relaxation has subsequently been shown to occur in most mammalian species,2 and has also been demonstrated in humans by in vitro studies using arterial preparations.3 4 5 More recently, studies in normal humans have confirmed these observations and have indicated that this regulatory action of the endothelium is also exerted at the level of the resistance vessels.6 The presence of such a mechanism suggests not only that it may play a part in modulating normal vascular tone, but also that its impairment may contribute to or even cause various disease processes. This possibility is suggested by the results of several studies. Thus, endothelial-mediated vasodilatation is reduced in atherosclerotic arteries of animals7 8 9 and humans9 , 10 and in several animal models of hypertension.11 12 13 14 The present investigation was undertaken to determine whether patients with essential hypertension have an endothelium-dependent abnormality of vascular relaxation that might cause or exacerbate the hypertensive process.
Methods
Study Population
Twenty-two patients with essential hypertension who were followed at the outpatient department of the National Heart, Lung, and Blood Institute were recruited for the study. Each patient had a well-established history of chronically elevated blood pressure (≥145/95 mm Hg) without any apparent underlying cause and had been treated for at least five years with one or more antihypertensive agents. Patients were asked to discontinue all antihypertensive medications two weeks before the day of the study; during that time, they were closely monitored for any evidence of accelerated or malignant hypertension. Patients in whom the withdrawal of antihypertensive agents was considered hazardous (mostly because of severely elevated blood pressure despite medication) were not included in the study. After therapy was discontinued, 4 of the 22 patients were excluded from the analysis because they did not have systemic hypertension. Thus, a total of 18 patients (10 men and 8 women) with essential hypertension were studied. None of them had a history of diabetes, hyperlipidemia, peripheral vascular disease, coagulopathy, or any disease predisposing them to vasculitis or Raynaud's phenomenon.
A population of nine men and nine women, matched with the patients for approximate age, was selected as a control group. Histories, physical examination, electrocardiograms, chest x-ray films, and routine chemical analyses showed that the controls had no evidence of present or past hypertension, cardiovascular disease, or any other systemic condition and were taking no medications.
All participants gave written informed consent for all procedures. This study was approved by the National Institutes of Health Investigational Review Board.
Protocol
All studies were performed in the morning in a quiet room with a temperature of approximately 22°C (72°F). All participants were asked to refrain from drinking alcohol or beverages containing caffeine and from smoking for at least 24 hours before the study.
While the participants were supine, a needle was inserted in the brachial artery of the nondominant arm (left, in most cases). This arm was slightly elevated above the level of the right atrium, and a mercury-filled Silastic strain gauge was placed on the widest part of the forearm.15 , 16 The strain gauge was connected to a plethysmograph (model EC-4, D.E. Hokanson, Issaquah, Wash.)17 calibrated to measure the percent change in volume; the plethysmograph in turn was connected to a Gould chart recorder (Oxnard, Calif.) to record the forearm flow measurements. For each measurement, a cuff placed on the upper arm was inflated to 40 mm Hg with a rapid cuff inflator (model E-10, Hokanson) to occlude venous outflow from the extremity. A wrist cuff was inflated to suprasystolic pressures one minute before each measurement to exclude the hand circulation.18 Flow measurements were recorded for approximately 7 seconds every 15 seconds; seven readings were obtained for each mean value.
Basal measurements were obtained after a three-minute infusion of 5 percent dextrose solution at 1 ml per minute. Forearm flows were then measured after the infusion of sodium nitroprusside at 0.8, 1.6, and 3.2 μg per minute and acetylcholine chloride (Sigma Chemical, St. Louis) at 7.5, 15, and 30 μg per minute (infusion rates, 0.25, 0.5, and 1 ml per minute, respectively, for each drug). Forearm flow was measured after each three-minute infusion. In the first 20 subjects (10 patients and 10 controls), the infusion of sodium nitroprusside preceded that of acetylcholine; in the remaining 16 subjects, the order of administration was reversed. A 30-minute rest period ensued, and another basal measurement was obtained between the infusion of the two drugs.
Since acetylcholine, either released from cholinergic terminals or administered exogenously, may inhibit the release of norepinephrine by adrenergic nerve endings,19 , 20 the infusion of acetylcholine was repeated in eight patients and eight controls during sympathetic α-adrenergic blockade. Thirty minutes after the primary study, basal measurements were repeated, and phentolamine was then infused (12 μg per minute per 100 ml of forearm volume) over a 10-minute period at a rate of 0.6 ml per minute. At these doses, phentolamine produces effective and complete α-adrenergic blockade.21 Immediately after the phentolamine infusion, another cumulative dose–response curve to acetylcholine was obtained with the same doses and infusion rates used in the earlier study.
To determine whether vasodilation reached a plateau in the hypertensive patients, five patients also received the highest dose of sodium nitroprusside (3.2 μg per minute for 3 minutes) within 10 minutes of the completion of the acetylcholine infusion, while the α-adrenergic blockade induced by phentolamine was still in effect.
During the study, the participants did not know which drugs were being infused. All blood pressures were recorded in the contralateral arm by sphygmomanometry immediately before each measurement. Mean arterial pressure was calculated by adding one third of the pulse pressure to the diastolic pressure. Forearm blood flow is expressed as milliliters per minute per 100 ml of forearm volume. Forearm vascular resistance was calculated as the mean arterial pressure divided by the forearm blood flow.
Statistical Analysis
Student's t-test for paired or unpaired data, as appropriate, was used to compare two means. The response to sodium nitroprusside and acetylcholine in hypertensive patients and normal controls was compared by analysis of variance for repeated measures. Because the basal resistance was significantly different in the two groups, the change in vascular resistance was expressed as the percentage of the base-line value for all comparisons, except for the assessment of the response to acetylcholine during α-adrenergic blockade, since the resistance after the administration of phentolamine was similar in the two groups. All calculated P values are two-tailed. All P values less than 0.05 were considered to indicate significance. All group data are reported as means ±SD unless otherwise indicated.
Results
Population Characteristics
The base-line characteristics of the normal controls and the patients with hypertension were similar, except for mean arterial blood pressure and resting forearm vascular resistance, which as expected were significantly higher in the patients (Table 1Table 1
Characteristics of the Study Population.*).Response to Acetylcholine and Sodium Nitroprusside
The increase in blood flow and percent change in vascular resistance with acetylcholine were significantly reduced in hypertensive patients as compared with controls (P<0.0001) (Fig. 1Figure 1
Responses of Forearm Blood Flow and Vascular Resistance to Acetylcholine in 18 Normal Controls (Open Circles) and 18 Hypertensive Patients (Solid Circles).). At the highest dose (30 μg per minute), forearm blood flow was 20.0±8 ml per minute per 100 ml in the controls and 9.1 ±5 ml per minute per 100 ml in the patients (P<0.0001).No significant differences in the response of forearm blood flow and vascular resistance to sodium nitroprusside were found between the two groups (Fig. 2Figure 2
Responses of Forearm Blood Flow and Vascular Resistance to Sodium Nitroprusside in 18 Normal Controls (Open Circles) and 18 Hypertensive Patients (Solid Circles).). Although the controls had a higher flow at the highest infusion rate (3.2 μg per minute), this difference (12.2±4 vs. 11.0±4ml per minute per 100 ml) was not significant.To substantiate further the finding of an impaired response to acetylcholine in hypertensive patients, the data were plotted so that the response to acetylcholine was compared with the response to sodium nitroprusside within each group. The results of this analysis showed that although in normal controls the increase in flow induced by acetylcholine was significantly greater than that induced by sodium nitroprusside (P<0.02), in the hypertensive patients the response to acetylcholine was significantly blunted and sodium nitroprusside produced the greater degree of vascular relaxation (P<0.03).
Effect of α-Adrenergic Blockade
Although the infusion of phentolamine caused significant vasodilation in both groups, the patients with essential hypertension had a greater response. Thus, forearm vascular resistance was similar in the two groups once α-adrenergic blockade was achieved. The subsequent infusion of acetylcholine resulted in substantial further vasodilation in the normal controls; however, the response to this drug was significantly blunted in the hypertensive patients, in terms of both blood flow (P<0,03) and vascular resistance (P<0.005) (Fig. 3Figure 3
Responses of Forearm Blood Flow and Vascular Resistance to Phentolamine and Subsequent Acetylcholine Infusion in Eight Normal Controls (Open Circles) and Eight Hypertensive Patients (Solid Circles).).Further vasodilation occurred in each of the five hypertensive patients who received sodium nitroprusside (3.2 μg per minute for three minutes) during αAdrenergic blockade. The vasodilation was significantly greater than that induced by the maximal dose of acetylcholine during α-adrenergic blockade in these patients (P<0.01) (Fig. 3).
Discussion
Furchgott and Zawadzki first demonstrated that an intact endothelium is necessary for acetylcholine to induce vasodilation; when the endothelium is damaged or removed, the relaxing effect of acetylcholine is lost.1 These observations were subsequently extended to a variety of other substances,2 thus demonstrating that the endothelium can actively modulate the effects of many agents on the contractile state of vascular smooth muscle, and therefore their effects on the vascular tone of blood vessels. The endothelium has been shown to exert its vasoregulatory action by releasing a substance (or substances)1 that induces smooth-muscle relaxation by increasing the production of intracellular cyclic guanosine monophosphate.22 , 23 The factor released by the endothelium that causes vascular relaxation is called endothelium-derived relaxing factor,2 , 24 and nitric oxide is believed to be one such relaxing factor.25
The potential clinical implications of these discoveries were emphasized by studies showing that there is an endothelium-dependent mechanism that causes relaxation of the large arteries in vitro3 4 5 and of systemic resistance vessels in normal humans6 and that this mechanism may be impaired in the epicardial vessels of patients with coronary artery disease.9 , 10 , 26 The endothelium-dependent relaxing mechanism was also found to be impaired in animal models of hypertension.11 12 13 14 The present investigation further extends the concept of endothelial dysfunction as a possible contributor to human disease.
Our study was designed to test the hypothesis that patients with essential hypertension have a functional abnormality of endothelium-mediated vascular relaxation. We studied the response of the forearm arterial vessels to acetylcholine, an agent that causes an endothelium-mediated vasodilator response.1 , 2 , 6 The effects of acetylcholine were compared with those of sodium nitroprusside, an agent that produces vasodilation by direct activation of guanylate cyclase in vascular smooth-muscle cells.27 28 29 The advantage of direct infusion of drugs into the forearm arterial bed is that the drugs do not reach the general circulation in concentrations sufficient to cause any systemic effect; therefore, the infusion does not activate reflex mechanisms that would make it impossible to assess the intrinsic action of the drugs on vascular smooth muscle.
Our results are consistent with the concept that there is a defect of endothelium-mediated vascular relaxation in essential hypertension. Thus, although the vasodilator response of hypertensive patients to sodium nitroprusside was similar to that of controls, the response to acetylcholine was blunted (Fig. 1 and 2). Furthermore, although acetylcholine increased the blood flow significantly more than sodium nitroprusside did in normal subjects at the doses used in this study, the response to it was significantly attenuated relative to the response to sodium nitroprusside in hypertensive patients.
Acetylcholine, either liberated from cholinergic terminals or exogenously administered, inhibits the release of norepinephrine by adrenergic nerve endings.19 , 20 This prejunctional action of acetylcholine appears to be the principal mechanism by which parasympathetic neural stimulation produces vasodilation. Hence, the impaired vasodilator response we found in hypertensive patients could be caused by some abnormality in this mechanism, rather than by an endothelial defect. To rule out this possibility, the effect of acetylcholine was also assessed during pharmacologic α-adrenergic blockade induced by the infusion of phentolamine. Phentolamine caused greater vasodilation in hypertensive patients, suggesting that this group may have greater basal vasoconstrictor tone related to α-adrenergic influences. Most important, the vasodilator response to acetylcholine during α-adrenergic blockade was still significantly lower in the hypertensive patients than in the normal controls. Hence, the presynaptic inhibition of the release of norepinephrine induced by acetylcholine cannot be invoked to explain the impaired response to its administration. Recent studies6 have shown that the vasodilator action of acetylcholine in normal humans can be effectively blunted by an arginine analogue, a specific inhibitor of the synthesis of endothelium-derived nitric oxide, further supporting the view that the vasodilator effect of acetylcholine is largely mediated by the action of the endothelial cells.
The observations that the forearm vascular responses to sodium nitroprusside were similar in hypertensive patients and controls and that this drug can further dilate the vessels of hypertensive patients that appeared to have reached an acetylcholine-induced plateau in blood flow during α-adrenergic blockade (Fig. 3) indicate that the impaired response of these patients to acetylcholine is not part of a generalized decrease in vasodilator capacity of the vascular system. Moreover, because both endothelium-derived relaxing factor and sodium nitroprusside produce vasodilation by a similar mechanism (stimulation of guanylate cyclase and consequent increase in cyclic guanosine monophosphate concentrations in vascular smooth muscle),30 the defective response to acetylcholine appears to be a consequence of the release by endothelial cells of less endothelium-derived relaxing factor or other relaxing factors, rather than a low responsiveness of vascular smooth-muscle cells to normal levels of relaxing factors.
Endothelial cells also release a constricting factor31 and a hyperpolarizing factor.32 Although these substances may also play an important part in the modulation of vascular smooth-muscle tone by endothelial cells, it has been repeatedly demonstrated that the endothelium-dependent response to acetylcholine is mediated through the release of a relaxing factor.1 , 2 , 6 Therefore, the defective response to acetylcholine we observed in hypertensive patients is probably due to the decreased release of a relaxing factor by endothelial cells. However, the design of our study does not allow us to exclude the possibility that these findings are a consequence of the increased release of constricting factors in these patients.
The original studies demonstrating a role of endothelium in mediating the vasodilator responses of blood vessels employed in vitro preparations of large arteries.1 , 2 Subsequent investigations demonstrated that the endothelium also regulates the activity of the smooth muscle of small vessels,6 , 33 34 35 36 which may be critical in the regulation of vascular resistance. Moreover, a decreased endothelium-dependent relaxation in resistance arteries of hypertensive animals has recently been reported.37 It is unlikely that the endothelial abnormality we found in the forearms of hypertensive patients exists only in the larger vessels, since major alterations in the caliber of such arteries would be required to produce changes in forearm blood flow and vascular resistance.38 Hence, our demonstration of a defect of the endothelium-mediated vasodilator response to acetylcholine suggests that the regulatory action of the endothelium also affects vascular smooth muscle at the level of resistance vessels in humans and is impaired in patients with essential hypertension.
The results of this investigation may have important implications. The demonstration of an endothelial abnormality in patients with hypertension that can be detected by assessing the responses of blood flow and vascular resistance suggests that this abnormality may contribute to the increased vascular resistance and elevated systemic blood pressure present in these patients. On the basis of these findings we cannot determine, however, whether the endothelial dysfunction we found is primary or secondary to the hypertensive process. Studies in animals have demonstrated that endothelium can be injured by short-term39 and long-term40 elevations in arterial pressure, impairing the response to endothelium-dependent vasodilating agents. Other studies using hypertensive animals that had impaired endothelium-mediated vasodilator responses have shown that antihypertensive treatment normalizes endothelium-dependent vasodilation.41 Thus, the endothelial abnormality we found in hypertensive patients may be a consequence and not a cause of the elevated blood pressure. Nevertheless, the endothelial dysfunction, even as a secondary phenomenon, may exacerbate the existing vascular abnormality and establish a vicious circle that contributes to the final consequences of systemic hypertension.
We are indebted to Carol J. Folio, R.N., for technical assistance.
Source Information
From the Cardiology Branch, National Heart, Lung, and Blood Institute, Bethesda, Md. Address reprint requests to Dr. Panza at the National Institutes of Health, Bldg. 10, Rm. 7B–15, Bethesda, MD 20892.
- References
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Edward M Boyle, Sean T Lille, Eric Allaire, Alexander W Clowes, Edward D Verrier. (1997) Endothelial Cell Injury in Cardiovascular Surgery: Atherosclerosis 1 1Recent discoveries in the field of vascular biology have led to an expanded understanding of the pathogenesis of many of the immediate and long-term complications of patients undergoing cardiovascular operations and interventional cardiologic procedures. In particular, the vascular endothelium has emerged as the central focus of many of the biologic events that affect the preoperative, operative, and postoperative course of nearly all heart surgery patients. A recurring theme in the study of endothelial cell biology is the crucial role that endothelial cell injury plays in the difficulties that our patients encounter. The deleterious effects of endothelial cell injury are most evident in the acute syndromes of vasospasms, coagulopathy, ischemia/reperfusion injury, and the systemic inflammatory response to cardiopulmonary bypass. In addition, chronic endothelial cell injury contributes to the development of anastomotic narrowing and the progression of atherosclerosis, both of which limit the long-term success of coronary artery bypass grafting. Because of the increasingly recognized role of the endothelium in cardiovascular function there is a tremendous amount of basic science information detailing the response of the endothelium to injury. This is the last in a series of seven reviews intended as an introduction to the major topics of endothelial cell biology that are of importance to the practicing cardiothoracic surgeon. In particular, the authors have focused on the role that the endothelium has on the development of vasomotor dysfunction, bleeding and thrombosis, neutrophil-endothelial cell interaction, and obstructive arteriopathy. The aim of these reviews is to provide a concise reference point for cardiothoracic surgeons as they evaluate the ever-accumulating research findings and new therapies that stem from the study of the endothelium in response to the insults encountered in cardiothoracic surgery.Edward D. Verrier, MD. The Annals of Thoracic Surgery 63:3, 885-894
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