Original Article

Circulating and Tissue Endothelin Immunoreactivity in Advanced Atherosclerosis

Amir Lerman, M.D., Brooks S. Edwards, M.D., John W. Hallett, M.D., Denise M. Heublein, Sharon M. Sandberg, and John C. Burnett, Jr., M.D.

N Engl J Med 1991; 325:997-1001October 3, 1991

Abstract

Abstract

Background.

Atherosclerosis is characterized by endothelial injury and the proliferation of arterial smooth-muscle cells. The latter may be a result of the release of growth factors from the vessel wall; such growth factors may include an endothelium-derived vasoconstrictor peptide with mitogenic properties. We tested the hypothesis that plasma endothelin concentrations are elevated in persons with symptomatic atherosclerosis, independently of age.

Full Text of Background....

Methods.

We measured plasma endothelin levels in 100 normal subjects and in 40 patients with atherosclerosis predominantly of the following types: aortic and peripheral vascular disease (14 patients), renovascular disease (9 patients), coronary artery disease (9 patients), and carotid disease (8 patients). We also performed immunohistochemical staining for endothelin in the walls of atherosclerotic vessels.

Full Text of Methods....

Results.

In the normal subjects, the mean (±SD) plasma endothelin concentration was 1.4±0.2 pmol per liter, with no correlation between age and plasma endothelin concentration (r = 0.13, P = 0.2). In the patients with symptomatic atherosclerosis, the mean plasma endothelin concentration was 3.2±1.2 pmol per liter (P<0.001), and there was a significant correlation between plasma endothelin and the number of sites of disease involvement (r = 0.89, P<0.001). In the immunohistochemical studies, endothelin-1-like immunoreactivity was observed in vascular smooth muscle as well as in endothelial cells.

Full Text of Results....

Conclusions.

Endothelin may be a marker for arterial vascular disease. Whether it participates in the atherogenic process or is merely released from damaged endothelial cells is unclear. (N Engl J Med 1991;325:997–1001.)

Full Text of Conclusions....

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Media in This Article

Figure 1Plasma Endothelin Concentrations as a Function of Age in the 100 Normal Subjects Studied.

Figure 2Plasma Endothelin Concentrations in 100 Normal Subjects and 40 Patients with Symptomatic Atherosclerosis.

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Article

ATHEROSCLEROSIS may be initiated by endothelial injury, which then leads to the proliferation of intimal smooth-muscle cells.1 The atherogenic smooth-muscle proliferation could be the result of the release of growth factors from platelets, leukocytes, or cells of the vessel wall.2 3 4 This hypothesis is supported by the isolation of a large number of endogenous molecules that are mitogenic for smooth-muscle cells in vitro.5

Recent investigations have documented the existence of an endothelium-derived contracting peptide, which has been termed endothelin.6 The administration of synthetic endothelin in animals results in systemic, coronary, and renal vasoconstriction.7 , 8 In addition to its vasoconstrictor properties, endothelin has mitogenic properties in vitro, suggesting that it has a role as a growth factor.9

Endothelin is present in plasma, perhaps as a result of spillover from the interface of endothelial and vascular smooth muscle.10 , 11 Plasma endothelin concentrations are high in conditions associated with endothelial-cell injury, as well as in essential hypertension and congestive heart failure.12 13 14 An elevation of plasma endothelin levels in association with endothelial injury would be consistent with in vitro studies demonstrating that endothelial-cell injury due to hypoxia or other factors may stimulate the synthesis of messenger RNA by endothelin and the enhanced secretion of endothelin.15 Although the activation of endothelin could occur as a secondary phenomenon in atherosclerosis in response to endothelial injury, endothelin could also serve as a participant in atherogenesis.

This study was designed to test the hypothesis that circulating levels of endothelin are increased in humans with symptomatic atherosclerosis, independently of age. We therefore measured plasma endothelin concentrations in normal subjects and in patients with symptomatic atherosclerosis involving the coronary, renal, carotid, or peripheral arterial circulations. Furthermore, to assess the localization of endothelin in the blood-vessel wall, aortic tissue from a group of patients undergoing surgical vascularization was studied by an immunohistochemical technique to identify endothelin-1.

Methods

This investigation was performed at the Mayo Clinic with the approval of the institutional review board. Informed consent was obtained from all subjects.

Study Subjects

One hundred normal subjects served as a control group. None had a history or physical or laboratory findings of any cardiovascular, renal, liver, or metabolic disease during the six months before the study, and none were taking any medication. Fifteen were in the same age range as the patients with symptomatic atherosclerosis.

Forty patients who were referred to the Mayo Clinic between September 1989 and May 1991 for the evaluation of symptomatic atherosclerotic vascular disease were studied. All the patients had a complete physical and laboratory evaluation and were studied after appropriate diagnostic procedures had been performed. Patients with diabetes mellitus, acute renal failure, or abnormal liver-function tests were excluded from the study. The study patients were classified according to the principal site of vascular disease requiring surgical or medical intervention at the time of the study, as determined clinically and radiographically. The location of vascular disease in the 40 patients was determined at the time of the study or during the preceding year. Fourteen patients had aortic and peripheral vascular disease, as documented by abdominal angiography; nine had renovascular disease, as documented by renal angiography; nine had coronary artery disease, as documented by coronary angiography or a proved myocardial infarction; and eight had carotid disease, as documented by carotid angiography or ultrasonography with Doppler analysis.

All the patients with renovascular disease had hypertension, as did eight (57 percent) of the patients with peripheral vascular disease, four (44 percent) of those with coronary artery disease, and five (62 percent) of those with carotid disease. Cardiovascular medications were discontinued at least 12 hours before blood was collected for the measurement of plasma endothelin. At the time of the study, 8 patients (20 percent) were taking angiotensin-converting—enzyme inhibitors, 13 (33 percent) were taking calcium-channel blockers, 19 (48 percent) were taking short-acting nitrates, and 9 (23 percent) were taking alpha- or beta-adrenergic—antagonist agents; some of the patients were receiving combinations of these medications. Dietary intake was not controlled.

Test Procedures

Arterial pressure was measured twice by sphygmomanometry at the time of the blood collection, with the patient in the supine position, and mean arterial pressure was calculated as one third of the pulse pressure plus the diastolic blood pressure. Serum creatinine was measured by standard laboratory methods. Plasma endothelin concentrations were determined with radioimmunoassay kits (Peninsula Laboratories, Belmont, Calif). Venous-blood samples were drawn from the patients after they had been supine for at least 20 minutes. The samples were collected in tubes containing chilled potassium EDTA and immediately placed on ice until they were centrifuged at 4°C. The plasma was separated and frozen at -20°C until the assay. Before assay, the plasma was acidified with 0.5 percent trifluoroacetic acid and applied to a C8 Bond Elut cartridge previously washed with 4 ml of methanol and then 4 ml of water. After the plasma was applied, the cartridge was washed with 2 ml of normal saline and 6 ml of water. Endothelin was eluted from the cartridge with 2 ml of 90 percent methanol in 1 percent trifluoroacetic acid. The eluted endothelin was dried and reconstituted for radioimmunoassay. The recovery rate for the extraction procedure was 81 percent, as determined by the addition of synthetic endothelin to plasma. The results presented here were not corrected for the recovery rate. The interassay and intraassay coefficients of variation were 9 percent and 5 percent, respectively, as determined in pooled plasma. The lower level of detection of the assay was 0.2 pmol per liter (range, 0.2 to 170). The cross-reactivity of endothelin-2, endothelin-3, and proendothelin in this assay was less than 5 percent, less than 3 percent, and less than 37 percent, respectively, according to the manufacturer of the assay kits.

For the immunohistochemical analysis, atherosclerotic abdominal aortic tissue obtained during surgery from five patients undergoing bypass revascularization for peripheral vascular disease was fixed in 10 percent buffered formalin. The tissue was embedded in paraffin, and sections 6 μm thick were cut and mounted on slides treated with silica. The slides were incubated overnight at 60°C and deparaffinized with graded concentrations of xylene and ethanol. The slides were washed with 0.6 percent hydrogen peroxide in methanol for 20 minutes at room temperature in order to block the activity of endogenous peroxidase. They were subsequently incubated with 5 percent goat serum (Dako, Santa Barbara, Calif.) for 10 minutes at room temperature to reduce nonspecific background staining and were then incubated with rabbit polyclonal endothelin1 antiserum (Peninsula) at a dilution of 1:1600 in humidified chambers for 24 hours at room temperature. The control slides were treated with dilute rabbit serum (Dako). All the treated slides were exposed for 30 minutes to goat antirabbit antiserum at a dilution of 1:100 (Tago, Burlingame, Calif.) to which peroxidase had been covalently linked. Peroxidase activity was visualized with 3-amino-9-ethylcarbazole (Sigma, St. Louis) dissolved in dimethylformamide and sodium acetate. The sections were counterstained with hematoxylin, mounted, and reviewed with an Olympus microscope. This technique has been validated previously.16

Statistical Analysis

All results are given as means ±SD. The statistical analysis was performed with repeated measurement of analysis of variance and by the t-test for unpaired observations. A P value less than 0.05 was considered statistically significant.

Results

Normal Subjects

The mean age of the 100 normal subjects was 40 years (range, 8 to 78) (Table 1Table 1Demographic and Clinical Characteristics of the Patients with Atherosclerosis and the Normal Subjects.). Their mean plasma endothelin concentration was 1.4±0.2 pmol per liter (range, 0.9 to 2.1). There was no correlation between age and the plasma endothelin concentration in these subjects (r = 0.13, P = 0.2) (Fig. 1Figure 1Plasma Endothelin Concentrations as a Function of Age in the 100 Normal Subjects Studied.), and there was no significant difference with respect to plasma endothelin concentration between men and women or between subjects with a history of smoking and subjects who did not smoke. In the subgroup of 15 normal subjects whose ages were similar to those of the patients (mean age, 66 years; range, 56 to 78), the mean plasma endothelin concentration was 1.5±0.2 pmol per liter (range, 1.2 to 1.9).

Patients with Symptomatic Atherosclerotic Vascular Disease

The demographic and clinical characteristics of the 40 patients with symptomatic atherosclerotic vascular disease are shown in Table 1. Their mean age was 66 years (range, 46 to 81). Overall, 26 (65 percent) had a history of hypertension. Eight patients (20 percent) were nonsmokers, 14 (36 percent) were active smokers, and 18 (44 percent) had discontinued smoking.

The plasma endothelin concentrations in these patients ranged from 1.6 to 6.3 pmol per liter (mean, 3.2±1.2), significantly higher (P<0.001) than in either the 15 age-matched normal subjects or the entire group of normal subjects (Fig. 2Figure 2Plasma Endothelin Concentrations in 100 Normal Subjects and 40 Patients with Symptomatic Atherosclerosis.). There was a significant correlation between plasma endothelin concentrations and the number of sites of disease involvement (r = 0.89, P<0.001) (Fig. 3Figure 3Correlation between Plasma Endothelin Concentration and Number of Atherosclerotic Sites.). The patients had a mean arterial pressure of 103±2 mm Hg and a mean serum creatinine level of 123±57 μmol per liter (range, 53 to 336) (normal, <110).

There was no correlation between plasma endothelin concentration and age, serum creatinine level, or mean arterial pressure either in the patients as a whole or according to the site of involvement. There was no difference in plasma endothelin concentration between the patients who had a history of hypertension and those who did not, or between the patients who were smokers and those who were nonsmokers or former smokers.

Endothelin-1—like immunoreactivity was localized to endothelial cells and to the cytoplasm of vascular smooth-muscle cells of the medial blood vessels of the aorta (Fig. 4Figure 4Photomicrograph Showing the Distribution of Endothelin-like Immunoreactivity in 6-μm Sections of Atherosclerotic Aorta.), as well as the medial smooth-muscle cells of the aorta itself (Fig. 4). Control studies with nonimmune rabbit serum gave negative results (Fig. 4). The results were similar in the tissue from all five patients studied.

Discussion

These studies extend the findings of previous reports that have documented the presence of endothelin in the circulation in humans,17 18 19 20 21 and they raise the possibility of a role for endothelin in the pathophysiologic process of atherosclerosis. The mechanism of the increased plasma endothelin concentrations in patients with atherosclerosis may be multifactorial. The increase may reflect a rise in vascular production of endothelin in response to endothelial-cell injury, shear stress, impaired release of endothelium-derived relaxing factor,22 ischemia, and perhaps hyperlipoproteinemia.23 Alternatively, the increase may indicate a more basic role for endothelin in the atherosclerotic process. The replication of vascular smooth-muscle cells by growth factors may depend on factors synthesized by the vessel wall. There is intimal vascular smooth-muscle proliferation in occluded arteries, despite the absence of platelets in the vascular lumen,24 and in organ cultures vascular smooth-muscle cells initiate DNA synthesis without interacting with platelets or leukocytes.25 Growing evidence suggests that endothelin possesses mitogenic properties.9 ^' 26 ^' 27 It stimulates DNA synthesis in cultured vascular smooth-muscle cells in a dose-dependent manner,26 and DNA synthesis is markedly inhibited by antiendothelin antibodies.27 On the basis of these results, increases in the circulating endothelin level could reflect an increase in the local concentration of endothelin that in atherogenesis promotes the proliferation of vascular smooth-muscle cells.

This hypothesis is underscored by the demonstration of endothelin-1—like immunoreactivity in atherosclerotic endothelial cells as well as smooth-muscle cells. Such immunoreactivity was demonstrated earlier in normal arteries,28 , 29 but only in endothelial cells, and no immunoreactivity was seen in the neighboring tissues, including medial smooth-muscle cells and adventitial fibroblasts. The presence of endothelin-1—like immunoreactivity in the vascular smooth-muscle cells could reflect an internalization by these cells of endothelin produced in endothelial cells30 or the active production of endothelin by the smooth-muscle cells.31

Plasma endothelin levels may be increased in patients with essential hypertension, a risk factor for the development of atherosclerosis, but neither we nor Sai to et al.13 found a correlation between arterial pressure and plasma endothelin concentrations. We also found no relation between age and plasma endothelin concentrations. We did find a significant correlation between the number of regional sites of symptomatic atherosclerosis and plasma endothelin concentrations, which may indicate a relation between plasma endothelin concentrations and the severity of the atherosclerotic process. Although the cross-reactivity of proendothelin in the assay was less than 37 percent, part of the endothelin immunoreactivity in plasma in both groups may reflect the presence of proendothelin.

The elevation of plasma endothelin levels in atherosclerosis may have functional importance. Endothelin is a potent systemic, renal, and coronary vasoconstrictor,7 , 8 and a doubling of circulating concentrations of endothelin by exogenous administration in dogs resulted in substantial increases in systemic and renal vascular resistance, whereas coronary blood flow and arterial pressure did not change.32 Furthermore, atherosclerosis may result in endothelial dysfunction,33 34 35 36 characterized by enhanced vascular vasoconstrictor responses to stimuli such as endothelin and norepinephrine.37 , 38 Finally, in human arteries, threshold concentrations of endothelin amplify the contractions induced by other vasoconstrictors, such as norepinephrine.39 Thus, in patients with symptomatic atherosclerosis, endothelin could potentiate the acceleration of vascular smooth-muscle-cell proliferation and also enhance vascular tone, therefore leading to arterial spasm.36 , 39 , 40 Our studies suggest a role of endothelin in human atherosclerosis as a marker for arterial vascular disease and perhaps as a participant in the atherogenic process.

Supported by a grant (HL36634) from the National Institutes of Health and a grant from the Mayo Foundation. Dr. Lerman was supported by a Cardiovascular Training Grant (HL07 111) from the National Institutes of Health. Dr. Burnett is an Established Investigator of the American Heart Association.

We are indebted to William D. Edwards, M.D., for reviewing the pathological material.

Source Information

From the Cardiorenal Research Laboratory, the Department of Internal Medicine, and the Division of Cardiovascular Disease (A.L., B.S.E., D.M.H., S.M.S., J.C.B.), and the Department of Surgery (J.W.H.), the Mayo Clinic and Foundation, Rochester, Minn. Address reprint requests to Dr. Lerman at the Mayo Clinic, 200 First St., SW, Rochester, MN 55905.

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