(Circulation. 1995;92:3431-3435.)
© 1995 American Heart Association, Inc.
Articles |
Modulation of Endothelium-Dependent Flow-Mediated Dilatation of the Brachial Artery by Sex and Menstrual Cycle
From the Department of Geriatrics and Department of Obstetrics and Gynecology (Y.S., Y.T.), Faculty of Medicine, University of Tokyo (Japan).
Correspondence to Yasuyoshi Ouchi, MD, PhD, Department of Geriatrics, Faculty of Medicine, University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113, Japan.
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Abstract |
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Background Estrogen has been reported to augment endothelium-dependent vasodilatation. The role of endogenous ovarian hormones in modulating endothelium-dependent vasodilatation, however, remains to be determined. The purpose of the present study was to investigate the effects of sex and menstrual cycle on endothelium-dependent flow-mediated vasodilatation.
Methods and Results Seventeen female volunteers 25.1±0.8
years old and 17 age-matched male volunteers were examined. We
measured brachial artery diameters noninvasively using a 7.5-MHz
ultrasound machine at rest, during reactive hyperemia, and
after sublingual nitroglycerin administration. All
female subjects were studied three times each, in three different
phases of one menstrual cycle (M, menstrual phase; F, follicular phase;
and L, luteal phase). Flow-mediated diameter (D) increase (%FMD;
D/Dx100) in M, when serum estradiol level was low
(121.9±12.5
pmol/L), was 11.22±0.58%, and the value was comparable to that in
male subjects (10.60±0.75%). %FMD increased in F (18.20±0.81%,
P<.01 versus M) and L (17.53±0.74%, P<.01
versus M), when serum estradiol level was high (F, 632.0±74.5 and L,
533.8±33.4 pmol/L, P<.01 versus M).
Endothelium-independent vasodilatation by
nitroglycerin increased in both F and L. However, the
increment was smaller than that of %FMD.
Conclusions Endothelium-dependent vasodilatation varies during the menstrual cycle. The endogenous estradiol may be involved in this menstrual cycle–related vasodilatation.
Key Words: vasodilation • women • endothelium
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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The lower incidence of atherosclerosis in women before menopause than in men is an established epidemiological observation.1 Ovarian hormones, especially estradiol, have been suggested to underlie the sex-related difference in atherogenesis because replacement of ovarian hormones in postmenopausal women is associated with a decrease in the occurrence of cardiovascular disease.2 3 4 In animal experiments, replacement of estrogen in ovariectomized monkeys or pregnancy in intact monkeys has been reported to decrease the severity of coronary atherosclerosis induced by a high-cholesterol diet.5 6 7 Recently, Lieberman et al8 found that estrogen replacement in postmenopausal women improves endothelium-dependent FMD. However, the effect of endogenous ovarian hormones on vasomotor functions has not been elucidated.
Evidence has accumulated that the impairment of vascular endothelial function is an initial step in the development of atherosclerosis.9 One of the important findings in endothelial dysfunction is the impairment of endothelium-derived relaxing factor release from endothelial cells.9 FMD induced by reactive hyperemia has been known to be endothelium dependent,10 11 12 13 14 15 and this can be detected during reactive hyperemia by high-resolution ultrasound in superficial arteries.16 17 We hypothesized that ovarian hormones may exert a positive effect on endothelium-dependent vasodilatation in humans. To test this hypothesis, we studied whether FMD varies depending on sex and female physiological menstrual cycle in healthy volunteers.
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Methods |
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TopAbstractIntroductionMethods Results Discussion References |
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Subjects
Seventeen male and 17 female subjects, all volunteers, were enrolled in this study. The 17 male subjects, 22 to 31 years old, were healthy medical students and hospital staff. The 17 female subjects were also healthy students and hospital staff 21 to 32 years old. These female subjects had regular menstrual cycles (26 to 35 days) for more than 3 months before this study. None had a history of pregnancy. All subjects were asymptomatic, normotensive, nondiabetic, and nonsmokers (except 1 female subject with a history of smoking a few cigarettes a day for several months). They had no significant medical history and were not on regular medication. Each subject gave written informed consent before enrollment in this study after thorough explanation of the study design and protocol.
Study Design
Each female subject was studied three times in
one menstrual
cycle. The three different phases in one menstrual cycle are M, F, and
L (L defined as 5 to 7 days after obvious elevation of morning body
temperature). The measurement was done once in each phase. To estimate
their menstrual cycles, they checked their body temperature every
morning during this study. Seven male subjects were also studied three
times (at 1 week and 3 weeks in addition to the initial scan) to
evaluate the "cycle" effect. The other 10 male subjects were
examined once.
Blood sampling was performed on the morning of the ultrasound examination after a 14-hour overnight fast to measure serum concentrations of estradiol and progesterone, serum lipid profile, and other biochemical parameters. Blood (10 mL) was drawn from the individuals at each time and was centrifuged at 1000g for 20 minutes. After the centrifugation, 2 mL of the serum was kept at 4°C and the remaining serum was kept at -20°C until the time of measurement of serum ovarian hormone concentrations, lipid profiles, and other biochemical parameters. All specimens were measured within 48 hours after the blood sampling. Serum estradiol and progesterone concentrations were measured by sensitive radioimmunoassay. Serum total cholesterol and triglyceride concentrations were measured enzymatically, and serum HDL cholesterol concentration was measured by heparin–Ca2+/Ni2+ precipitation.18
Measurement of FMD and NTG-Induced Dilatation of the Brachial
Artery
FMD and NTG-induced dilatation of the brachial artery were
measured by an examiner who was unaware of the women's menstrual
cycles. Studies were done according to the method described by
Celermajer et al16 in a quiet and
temperature-controlled (22°C to 23°C) room. The examinations
were conducted by the same examiner throughout this study. The diameter
of the artery was measured from high-resolution,
two-dimensional ultrasound images obtained by an SSA-270A
ultrasound machine (Toshiba) with a 7.5-MHz linear array
transducer.16 17 19 Machine-operating
parameters were kept constant during each study.
A subject reclined on the examination bed 15 minutes before the initial ultrasound scanning of the brachial artery. The right brachial artery was scanned over a longitudinal section 3 to 5 cm above the right elbow, where the clearest image was obtained. The transmit (focus) zone was set to the depth of the anterior vessel wall. Depth and gain settings were optimized to identify the lumen-to–vessel wall interface. Blood pressure was monitored in the left arm every 2 minutes during the study by an automated blood pressure recorder. An ECG monitor equipped with the ultrasound machine was also applied to a subject's right wrist and both ankles.
The changes in diameter of
the right brachial artery were measured at
rest, during reactive hyperemia, again at rest, and after
sublingual NTG administration, which causes
endothelium-independent vasodilatation. When a
reasonable image was obtained, the surface of the skin was marked, and
the arm was kept in the same position throughout the study. A pneumatic
tourniquet placed around the forearm distal to the target artery was
inflated to a pressure of 250 mm Hg, and the pressure was held for 5
minutes. Increased flow was then induced by sudden cuff deflation. A
second scan was performed continuously for 30 seconds before and for 90
seconds after cuff deflation. Fig 1
shows the actual
scans of the brachial artery of 1 female subject at rest and during
reactive hyperemia. Then, 15 minutes later, a further resting
scan was recorded to confirm the vessel recovery. Sublingual NTG
spray (300 µg; Myocol Spray, Toa Eiyo Co) was then administered, and
3 to 4 minutes later the last scan was performed.
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The ultrasound images were recorded on S-VHS videotape with an SLV-RS7 videocassette recorder (SONY). The diameter of the brachial artery was measured from the anterior to the posterior interface between the media and adventitia ("m line") at a fixed distance.19 The mean diameter was calculated from four cardiac cycles synchronized with the R-wave peaks on the ECG. All measurements were made at end diastole to avoid possible errors resulting from variable arterial compliance.20 The time course change of the brachial artery diameter after cuff release was studied in 9 male subjects. Our preliminary study showed that maximal vasodilatation was observed 45 to 60 seconds after the cuff release, as previously reported.16 The diameter change caused by FMD was expressed as the percent change relative to that at the initial resting scan (%FMD). The diameter change caused by NTG administration was also expressed in the same way as the percent change relative to that at the recovery scan (%NTG). Simultaneously with vessel diameter measurement, the pulse wave velocity profile of blood flow in the brachial artery was recorded. Mean flow velocity was calculated by measurement of the area under this velocity profile curve. Blood flow (mL/min) was then calculated by multiplying the cross-sectional area of the brachial artery and was based on the diameter and the mean flow velocity.
Previous studies confirmed that changes in diameter of 0.1 to 0.2 mm can be detected accurately with this method.17 21 22 23 In the present study, the variability of the ultrasound measurements was studied for both %FMD and %NTG by repeated measurements from the same video records in 6 volunteers. The CV for measurements of absolute value of brachial artery diameter at flow-mediated dilatation was 0.45±0.01%, and that of %FMD was 5.84±0.25%. The CV for the measurements of absolute value of brachial artery diameter after NTG administration was 0.49±0.01%, and that of %NTG was 3.97±0.24%. To evaluate the reproducibility of this ultrasound examination, the examinations were repeated five times in 1 month in 8 male subjects. The CV for repeated measurements of brachial artery diameter at flow-mediated dilatation was 1.37±0.03%, and that of %FMD was 9.77±0.82%. The CV of repeated measurements of NTG administration was 1.34±0.03%, and that of %NTG was 7.24±0.49%. No vasodilatation was seen with the placebo for NTG sublingual spray, which was given to 6 male subjects. Further, to investigate the sequence effect of forearm occlusion and NTG administration, the NTG spray was administered to 5 male subjects at rest without forearm occlusion. No %NTG changes were observed between %NTG without forearm occlusion and %NTG after 15 minutes of recovery following forearm occlusion. This indicates that the 15-minute recovery period was enough for vessels to react to NTG after forearm occlusion.
Statistical Analysis
The data were analyzed by ANOVA. When
statistically
significant effects were found, the Newman-Keuls test was used to
isolate the differences between groups. A value of P<.05
was considered significant. All data in the text, tables, and figures
are expressed as mean±SEM.
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Results |
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All subjects tolerated the studies well. There were no significant blood pressure changes during the ultrasound examination. No subject showed any ultrasound evidence of arterial narrowing in the vessels studied. Table 1
shows the clinical
characteristics, including serum lipid profile and serum
ovarian hormone concentrations. Age and total
cholesterol, LDL-cholesterol, and
HDL-cholesterol levels showed no difference between the
male and female groups at any phase of the menstrual cycle. Body mass
index and serum triglyceride levels in male subjects were
significantly higher than those in female subjects, although they were
within normal ranges. Serum estradiol and progesterone levels were
appropriate to each menstrual phase as estimated by the subjects'
previous menstrual cycle, morning body temperature, and actual
menstruation during this study; serum estradiol level increased in the
F phase, and serum estradiol level remained high and serum progesterone
level increased in the L phase. In the M phase, serum levels of these
ovarian hormones decreased dramatically to the same levels as
in male subjects.
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As shown in Fig 2, %FMD in female subjects varied
depending on the menstrual phase. %FMD in the M phase was
11.22±0.58%, and the value was comparable to that in male
subjects (10.60±0.75%). %FMD increased in the F and L phases
(18.20±0.81% and 17.53±0.74%, respectively, P<.01
versus M phase). No statistical significance was found between the F
and L phases. %NTG, which reflects
endothelium-independent vasodilatation,
significantly increased in the F and L phases compared with those in
male subjects and in the M phase in female subjects. The increment,
however, was smaller than that of %FMD. As shown in Table 2,
blood pressure measurements were similar in male and
female subjects in each menstrual phase. Both vessel diameter and basal
blood flow were significantly greater in male than in female subjects.
However, no differences in these hemodynamic
parameters were observed in female subjects at any
menstrual phase. The increase in blood flow was similar in male and
female subjects.
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In 7 male subjects, we conducted ultrasound examination three times in 1 month at a timing corresponding to the women's menstrual phase (1 week and 3 weeks apart from the initial scan). We found that %FMD and %NTG remained unchanged.
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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FMD induced by reactive hyperemia is known to be dependent on the presence of endothelial cells.9 10 11 12 13 14 We found that FMD varies according to sex and to menstrual cycle in female subjects and that the variation was associated with the increase in serum estradiol concentration during a menstrual cycle. We also found that FMD in male subjects was comparable to that in female subjects only in the M phase, when serum levels of both estrogen and progesterone in the female subjects were similar to those in the male subjects. These findings suggest that endothelial function is positively modulated in part by endogenous ovarian hormones, especially estradiol. However, the possible involvement of factors other than estradiol cannot be excluded, because we have no evidence indicating that estradiol directly modulates endothelial function.
We estimated the phase of menstrual cycle, M, F, or L, on the basis of the subjects' previous menstrual cycle, morning body temperature, and actual menstruation. This estimation was confirmed by the appropriate serum concentrations of ovarian hormones corresponding to each phase of the menstrual cycle. Especially the F phase was carefully estimated, because this phase just preceding ovulation is only a short period when serum concentration of estradiol is elevated and that of progesterone is low. The observed changes in endothelial function during the menstrual cycle were not attributable to other factors such as serum lipid profiles and blood pressure, because they remained constant at any phase of the menstrual cycle. Previous studies have suggested that estrogen augments endothelium-dependent vasodilatation.6 24 25 26 27 The present study clearly shows that serum estrogen level correlates endothelium-dependent vasodilatation in a physiological condition. Miller and Vanhoutte28 suggested that progesterone antagonizes the effects of estrogen in canine coronary arteries. On the basis of our results, however, no obvious antagonizing effect of progesterone on endothelium-dependent vasodilatation was found.
Previous studies showed that smaller vessels dilate more than larger ones.16 In female subjects, arterial diameter at rest did not vary during the menstrual cycle. Since there were no vessel size changes, the results of %FMD and %NTG in female subjects were not affected by them. Therefore, the modulation of endothelium-dependent vasodilatation during the menstrual cycle certainly exists, as demonstrated in the present study. In contrast, in the present study, we found a significant difference in arterial diameter at rest between male and female subjects. Accordingly, it might be difficult to directly compare the results from these two groups, even though %FMD was similar in male subjects and in female subjects in the M phase.
The effect of estradiol on endothelium-independent vasodilatation is controversial. Jiang et al29 reported that estradiol induces dilatation of rabbit coronary arteries by an endothelium-independent mechanism. On the other hand, Gilligan et al30 reported that the acute administration of estradiol potentiates the forearm vasodilatation in postmenopausal women with risk factors for vascular dysfunction but not in healthy women. In the present study, we found that the variation of endothelium-independent vasodilatation induced by NTG during the menstrual cycle shows a pattern similar to that of FMD, because %NTG increased in the F and L phases, when serum estradiol levels were high. The magnitude of increment of FMD, however, was greater than that of NTG-induced endothelium-independent vasodilatation. That is, the ratio of %FMD to %NTG, which indicates the ratio of endothelium-dependent to endothelium-independent vasodilatation, was significantly greater in the F and L phases (P<.01 versus male, P<.05 versus M phase). These findings suggest that estradiol may dominantly modulate endothelium-dependent vasodilatation.
The increased production of NO induced by increased flow has been proposed as the main mechanism underlying the FMD induced by reactive hyperemia.13 14 15 NO is well characterized as endothelium-derived relaxing factor and is known to be released in response to increased flow induced by reactive hyperemia. Moreover, some kinds of NO synthase inhibitor have been demonstrated to inhibit endothelium-dependent vasodilatation in the human radial artery,31 human coronary artery,13 14 and hindlimb vessels in dogs.15 However, the effect of ovarian hormones on NO synthesis in vascular endothelial cells is still controversial. Hayashi et al32 suggested that basal release of NO in endothelium-preserved aortic rings from rabbits is regulated by ovarian hormones. They found that endothelium-dependent dilatation of aortic rings from female rabbits by superoxide dismutase is greater than that in rings from male rabbits and that contraction of aortic rings from female rabbits by NO synthase inhibitor, N-methyl-L-arginine acetate, is also greater than that from male rabbits. Furthermore, 17ß-estradiol has recently been reported to enhance expression of constitutive NO synthase in cultured vascular endothelial cells.33 34 In contrast, Sayegh et al35 reported that 17ß-estradiol has no effect on expression of constitutive NO synthase in cultured vascular endothelial cells. The result in the present study favors the positive effect of estrogen on NO synthesis in vascular endothelial cells. This point, however, needs further clarification. Another candidate is prostacyclin, a vasodilator prostanoid, whose production increases in response to increase in flow.36 However, the involvement of prostacyclin seems unlikely, because Holtz et al37 and Rubanyi et al10 demonstrated that indomethacin does not affect FMD in canine coronary arteries.
The method used in the present study to investigate endothelial function in vivo can be applied only to superficial arteries such as the brachial artery and the femoral artery. The investigation of endothelium-dependent vasodilatation in the coronary artery and the cerebral artery is clinically important. An invasive technique is necessary to investigate this issue,38 since no noninvasive method is available at present. The endothelial function in the brachial artery, however, might reflect that in the coronary artery, because the endothelial function in the brachial artery has been reported to be impaired in patients with coronary artery disease,16 and a close relationship of endothelial dysfunction has been reported in coronary and brachial arteries in humans.39
In conclusion, the present investigation demonstrates that the endothelium-dependent vasodilatation varies during the menstrual cycle. The serum levels of endogenous ovarian hormones, especially estradiol, correlate with vascular endothelial function in vivo. This might be involved in the sex-related difference in atherogenesis.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This work was supported by a grant from the Sankyo Foundation of Life Science. We thank all the volunteers who participated in the present study. We also thank Kiyoko Mizutani for her help in conducting this study and Masae Watanabe for her expert technical assistance.
Received November 14, 1994; revision received July 26, 1995; accepted August 6, 1995.
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