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(Hypertension. 1996;27:962-967.)
© 1996 American Heart Association, Inc.

Articles

Menstrual Cycle Effects on Catecholamine and Cardiovascular Responses to Acute Stress in Black but Not White Normotensive Women

Paul J. Mills; Richard A. Nelesen; Michael G. Ziegler; Barbara L. Parry; Charles C. Berry; Elaine Dillon; Joel E. Dimsdale

From the Departments of Psychiatry, Medicine, and Family and Preventive Medicine, University of California, San Diego.

Correspondence to Paul J. Mills, UCSD Medical Center, 200 W Arbor Dr, San Diego, CA 92103-0804.

	Abstract

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Abstract This study examined cardiovascular and catecholamine responses to two standardized laboratory stressors in 33 healthy age- and weight-matched black and white normotensive women (mean age, 32 years) during two phases of the menstrual cycle. Subjects were studied in a randomized order at the same time of day on two separate occasions approximately 6 weeks apart, once during the follicular phase (days 7 to 10 after menses) and once during the luteal phase (days 7 to 10 after the leutenizing hormone surge) of the menstrual cycle. Black women had higher systolic (P=.01) and diastolic (P=.01) pressures compared with white women. Black women showed greater diastolic pressure (P<.01) and plasma epinephrine (P<.05) responses to stress during the follicular compared with the luteal phase of the menstrual cycle; white women showed no significant changes in these variables. The findings extend the literature on race differences in responsivity to stress and indicate that in contrast to white women, reproductive hormones do influence cardiovascular and catecholamine responsivity to stress in black women.

Key Words: menstrual cycle • race • blood pressure • norepinephrine • epinephrine • stress

	Introduction

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Both race and sex affect blood pressure; blacks and men have more frequent and severe hypertension.^{1 2 3} Both sympathetic nervous system physiology and cardiovascular regulation during acute stress could mediate racial differences in blood pressure. Blacks, for example, have elevated levels of adrenergic agonists such as epinephrine and alterations in adrenergic receptor sensitivity and norepinephrine kinetics.^{4 5 6 7} Stress studies typically show greater peripheral vascular resistance–mediated pressor responses to psychological stress in blacks,^{8 9 10} perhaps because blacks evidence less ß-adrenergic receptor–mediated vasodilation compared with whites.⁶ With few exceptions, such studies have examined only men, and the generalizability of findings to women is uncertain.¹¹

Examination of possible mechanisms underlying sex differences in hypertension have naturally been directed toward reproductive hormones. Of the approaches available, examination of the cyclic variations of estrogen and progesterone during the menstrual cycle has been methodologically easy and relatively noninvasive. Studies examining blood pressure and heart rate responsivity to stress typically contrast the follicular and luteal phases of the menstrual cycle. Early studies in this area used between-subjects rather than within-subjects designs and failed to verify menstrual phase through the determination of reproductive hormone levels. Such studies report inconsistent findings of both increases and decreases in cardiovascular responses to stress during the luteal phase compared with the follicular phase of the menstrual cycle.^{12 13 14} Later studies using within-subjects designs report more consistent findings, suggesting no significant effect of menstrual cycle phase on blood pressure or heart rate responsivity,^{15 16 17 18} even when menstrual phase was verified via reproductive hormone blood levels.^{15 16} In contrast to blood pressure or heart rate responsivity, few studies have examined menstrual cycle phase effects on the hemodynamics underlying blood pressure.^{19 20}

Throughout these studies, little attention has been paid to possible cardiovascular differences between blacks and whites during the menstrual cycle phase. This is surprising because, as noted above, race exerts significant effects on hypertension and stress reactivity in men.^{1 2 10} Therefore, the purpose of this study was to examine whether the menstrual cycle differentially affects catecholamine, blood pressure, or underlying hemodynamic responsivity to acute stress in black compared with white women. We used two highly standardized psychological stressors, a within-subjects design, and urine and blood chemistries to verify menstrual phase.

	Methods

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Volunteers, primarily employees at the University of California, San Diego, Medical Center, were located through advertisement or word-of-mouth referral. Women were considered eligible if they were healthy, normotensive (pressures <140/90 mm Hg), between 90% and 120% of ideal weight,²¹ medication free (including oral contraceptives), not pregnant, and had menstrual cycle lengths between 26 and 34 days over the last 3 months. Premenstrual syndrome was retrospectively ruled out through the use of a menstrual assessment questionnaire.²² Of the women who met these eligibility criteria and began the study, 1 subject was dropped later because she became pregnant. Completed data were gathered on 17 black and 20 white women. All subjects were studied after written informed consent was obtained. The protocol was approved by the University of California, San Diego, Institutional Review Board.

Testing sessions were conducted at the same time of day, approximately 9 AM, during two consecutive cycles: once during the midfollicular phase (days 7 to 10 after menses) and once during the midluteal phase (days 7 to 10 after the leutenizing hormone surge) of the menstrual cycle. The leutenizing hormone surge was determined in urine by laboratory personnel with an enzyme immunoassay (OvuKit, Quidel). The menstrual cycle phase order of testing was randomized.

For the day of testing, subjects were instructed to eat a light breakfast and refrain from caffeinated beverages 12 hours before study. On arrival at the laboratory, an appropriately sized blood pressure cuff was placed on the nondominant arm, and a 19-gauge catheter was placed for blood sampling. Blood pressure was recorded with an automated monitor (Dinamap 845 XT; Critikon, Inc). Blood pressures obtained from the Dinamap correlate well (r>.95) with mercury sphygmomanometric readings.²³ For recording of impedance cardiography measures, impedance cardiographic tape was applied in a tetrapolar configuration.²⁴ The Z₂ electrode was attached around the base of the neck just superior to the suprasternal notch of the thorax. The Z₁ electrode was placed 3 cm above Z₂. Electrode Z₃ used the xiphoid process as the anatomic landmark. The electrode tape was placed over the xiphoid process circumscribing the thorax, with the tape kept parallel to the floor. The Z₄ electrode was placed about 5 cm below and parallel to Z₃. The Z₂-to-Z₃ length was also determined while the subject stood. After application of the impedance cardiographic electrodes, the electrocardiograph electrodes were applied in a modified lead I or lead II configuration. Electrodes were placed in the identical position for both testing sessions. The electrocardiographic (HP-78352C, Hewlett-Packard), phonocardiogram, Z_o, and dZ/dt (304B Minnesota Impedance Cardiograph) signals were relayed to an analog-to-digital convertor (DT2801, Data Translations) sampling at 1 kHz per channel.

After instrumentation, subjects rested for 30 minutes before baseline to acclimate to the monitoring equipment and testing environment. After a 3-minute baseline period, subjects were given instructions for a mirror star tracing task and a speaking task. The mirror star tracing task involved tracing the outline of a star using its mirror image for a 3-minute interval. The speaking task required preparation (3 minutes) and presentation (3 minutes) of a speech in front of a video camera.^{25 26} Subjects were told that the speech would be evaluated and rated by experts. If subjects stopped speaking before the 3 minutes were up, they were reminded to continue talking by reiterating and summarizing their points. Different versions of the two tasks were presented at each testing session. For the mirror star, two different stars were given for outlining. For the speech task, one version involved defending oneself from being falsely accused of shoplifting and the other involved standing up for oneself against a disreputable automobile sales and repair shop. We have found in our laboratory that the slightly different versions of these tasks produce equivalent reactivity (unpublished observation, 1995). The tasks (mirror star versus speech) were imposed in a counterbalanced fashion. A 20-minute rest period separated the two tasks to reduce carryover. These tasks have been used in prior studies examining race and menstrual cycle phase effects on stress physiology^{15 19} and are considered to elicit two different types of pressor response. Responses to the mirror star task are considered more -adrenergically mediated; ie, pressor response is attributed primarily to increases in peripheral vascular resistance.^{26 27} The pressor response accompanying the preparation phase of the speaking task is considered more ß-adrenergically mediated; ie, pressor response is attributed to increases in stroke volume and heart rate. Blood pressure responses accompanying the actual speaking phase are considered mixed in that both - and ß-mediated pressor characteristics are evident.^{26 27}

Blood pressure and heart rate were measured every minute for 3 minutes during the baseline, mirror star, speaking preparation, and speaking tasks: 1-minute readings were averaged to form baseline, mirror star, preparatory phase, and speaking phase values, respectively. Impedance was ensemble averaged by a computer program that summed the digitized beat-by-beat waveforms, time synchronized to the R wave of the electrocardiogram and divided by the number of cardiac cycles (University of Miami, Behavioral Medicine Research Center). The ensemble average was then graphically displayed, and the waveform events were scored by computer signal processing techniques.²⁸ Collection was time synchronized to the blood pressure readings.

Blood was sampled for catecholamines after the 3-minute baseline and mirror star task and again after the speaking task. Progesterone and estradiol were determined from blood sampled after the 3-minute baseline. Blood was collected in chilled anticoagulated tubes and separated in a refrigerated centrifuge, and the plasma was frozen at -80°C until assay. Plasma catecholamines were analyzed with a radioenzymatic assay.²⁹ Progesterone and 17ß-estradiol were determined by radioimmunoassay (ICN Biomedical).

Reproductive hormones might alter mood³⁰ and stress reactivity³¹ so we administered the Profile of Moods States (POMS) before each testing session. In addition, the Speilberger state anger and anxiety scales were administered at baseline and after each task for both testing sessions.³²

Statistical Analyses
Preliminary inspection of the data revealed that the epinephrine and total peripheral resistance data were not normally distributed, so these data were log normalized for statistical analyses. Preliminary analyses indicated that despite the randomization of the order of menstrual cycle phase testing, there was a significant testing sequence effect for systolic pressure. Therefore, in addition to race, testing sequence was used as a between-subjects factor for the repeated measures ANOVAs. Separate four-way (racextesting sequencextaskxphase) ANOVAs were used for examination of baseline and reactivity effects of each task on blood pressure, heart rate, cardiac output, stroke volume, total peripheral resistance, plasma norepinephrine, and plasma epinephrine. Menstrual cycle phase (follicular versus luteal) and task (baseline for the baseline analyses) and baseline versus task (mirror star, speech preparation, or speech presentation for the reactivity analyses) were within-subjects factors. Significant interactions were followed up by simple effects analysis. Variables that were significantly different between the groups at baseline were used as covariates. Data were analyzed with BMDP statistical software.

	Results

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At the conclusion of the study, each woman's estrogen and progesterone values were reviewed to verify that they were indeed tested at the correct phase of their menstrual cycle. Progesterone levels during the luteal phase fell below the expected values (<9 nmol/L) for 3 of the white and 1 of the black women, indicating an anovulatory cycle.¹⁹ Data from these 4 participants were therefore dropped from further analyses.

Plasma progesterone and estradiol values as well as age, weight, and number of cigarette smokers per group for the remaining women are shown in Table 1. There were no significant group differences in these variables. Randomization of the order of menstrual cycle phase testing yielded 8 white and 9 black subjects being tested at the follicular phase of the menstrual cycle first.

View this table: [in this window] [in a new window]   Table 1. Sample Characteristics

Baseline
Black and white women were similar at baseline for all physiological variables except that black women had higher diastolic pressures (F=8.02, P=.008) (Table 2). There were no significant menstrual cycle phase main effects nor significant menstrual cycle phase–by-race interactions for any baseline variables.

View this table: [in this window] [in a new window]   Table 2. Cardiovascular, Hemodynamic, and Catecholamine Measures by Group and Menstrual Cycle Phase

Mirror Star
The mirror star task resulted in significant increases over baseline for all variables (F values >5.6, P values <.05) except for cardiac output and plasma epinephrine.

Speech Preparation
The speech preparation task resulted in significant increases over baseline for all variables (F values >4.7, P values <.05). Black women had higher mean systolic pressures compared with white women (F=4.51, P=.014). Tests for simple effects of a stress-by–menstrual cycle phase–by-race interaction (F=6.16, P=.018) indicated that black women's diastolic pressure responses were greater during the follicular versus luteal phase (P=.023); white women's responses did not differ significantly across the two phases. Tests for simple effects of a stress-by–menstrual cycle phase–by–testing sequence interaction (F=5.13, P=.031) indicated that subjects tested during their luteal phase first had greater systolic reactivity during the luteal phase compared with those tested during the follicular phase first (P=.042).

Speech Presentation
The speech presentation task resulted in significant increases over baseline for all variables (F values >9.13, P values <.05). Tests of simple effects of a stress-by–menstrual cycle phase–by-race interaction (F=5.1, P=.031) indicated that black women had higher diastolic pressure responses during the follicular versus luteal phase (P=.008); white women showed little change (Figure). Tests of simple effects of a stress-by–menstrual cycle phase–by-race interaction (F=4.99, P=.035) indicated that black women had higher epinephrine responses during the follicular versus luteal phase (P<.05); white women showed no significant change (Figure). A significant main effect for testing sequence indicated that subjects who were tested during their luteal phase first had higher mean systolic pressures (F=4.83, P=.036). Tests for simple effects of a stress-by–menstrual cycle phase–by–testing sequence interaction (F=5.33, P=.028) indicated that subjects tested during their luteal phase first had greater systolic reactivity compared with those tested during their follicular phase first (P=.039).

View larger version (38K): [in this window] [in a new window]   Figure 1. Diastolic pressure and plasma epinephrine responses to a standardized laboratory stressor. Black women showed greater diastolic pressure (P=.008) and epinephrine (P<.05) reactivity (change scores, stress level minus baseline) during the follicular compared with the luteal phase of the menstrual cycle; these responses were not significantly different for white women across the menstrual cycle.

Psychological Measures
Across both groups, there was a marginally significant decrease in depression scores during the luteal phase compared with the follicular phase of the menstrual cycle (11.2 [SD=11.2] versus 14.3 [SD=11.5], respectively; F=4.12, P=.054). For both groups, the mirror star and speaking tasks resulted in significant increases over baseline in anger and anxiety, respectively (F values >6.7, P values <.01) and (F values >21, P values<.001); there were no significant main effects nor interactions for menstrual cycle phase.

	Discussion

Top Abstract Introduction Methods Results Discussion References

 
We examined whether existing data on menstrual cycle phase effects on responsivity to stress in white women were generalizeable to black women. We used a within-subjects design and verified targeted menstrual cycle phase by quantifying reproductive hormone levels. The findings replicate prior negative studies for white women^{14 15 16 17 18} but indicate that for black women, blood pressure and catecholamine responsivity to stress are affected by menstrual cycle phase. These effects were present despite similar blood levels of estrogen and progesterone in black and white women in both phases of the menstrual cycle.

The stressors we used in this study have been used in prior studies examining menstrual cycle phase effects on stress physiology as well as in stress studies in black and white men.^{15 19 33} Black men typically show greater peripheral vascular resistance–mediated pressor responses compared with white men to tasks such as the mirror star, which are considered more -adrenergically rather than ß-adrenergically mediated.^{26 27 33} Unlike men, however, and consistent with a prior study,³⁴ the present study showed no differences between white and black women in peripheral vascular resistance reactivity. The blood pressure and epinephrine effects for the black women were task specific in that they were evident only during the speaking task and not the mirror star task. Investigators suggest that the speaking task is a more gender-relevant type of stressor for women.³⁵

Prior studies on heart rate responsivity to acute stress in different racial groups call attention to the need to consider the race of the experimenter, noting that this might affect the interpretation of the task and thus reactivity to stress.³⁶ In the present study, the same white clinical nurse conducted the laboratory sessions for black and white subjects alike. We attempted to evaluate possible differences in emotional interpretation of the tasks by gathering pretest and posttest data on anxiety and anger ratings and did not find any significant group differences. In addition, one would expect that any possible experimenter effect on reactivity would be present during both sessions, but reactivity differences were found only during one of the testing sessions. We also attempted to take into account possible cycle-associated changes in mood and their influence on stress reactivity^{30 31} by administering the Profile of Moods States. We found no differences between black and white women on any of these scores.

We did not evaluate diet factors such as sodium and cholesterol, which can exert effects on the sympathetic nervous and cardiovascular systems.^{37 38 39} However, we have no reason to believe that the subjects' diets changed during their menstrual cycle.

Given the between-group similarities in blood levels of estrogen and progesterone, what might account for the menstrual cycle phase–related stress responsivity changes in black women? The answer may lie in fundamental differences between black and white women in reproductive hormone physiology. Estrogen, for example, alters catecholamine kinetics^{40 41} and blood pressure responses to acute stress,⁴² and black women show differences in estrogen receptor expression compared with white women.^{43 44} In addition, black women show differences in the hypothalamic-pituitary-adrenal axis compared with white women.⁴⁵ Although the possible relationship between this latter observation and cyclic changes in reproductive hormones has not been specifically evaluated, the menstrual cycle has been associated with changes in adrenocortical reactivity to acute stress.⁴⁶ Other studies suggest that the relative androgen/estrogen balance is more important than total estradiol (or testosterone) levels alone when considering cardiovascular-related physiology and cardiovascular disease risk.^{47 48 49} Falkner et al,^{48 49} for example, demonstrated that degree of androgenicity (defined as the ratio of free testosterone to estradiol) is related to higher blood pressure and insulin resistance in black women; estradiol levels alone were unrelated to either end point. Together, these data indicate fundamental differences between black and white women in the relationship between reproductive hormone physiology and cardiovascular regulation.

Prior studies of menstrual cycle effects on plasma or urinary catecholamine responses to stress that did not explicitly examine race have provided inconsistent findings.^{15 16 50} Part of the inconsistencies in prior studies may also be due to technical difficulties with the epinephrine assay. Plasma epinephrine levels in resting subjects are often at the lower limit of sensitivity for most assays. We used an assay that is much more sensitive than prior methods²⁹ and perhaps as a result were able to detect epinephrine changes in black women. Using this same assay, we previously found reduced epinephrine levels in black compared with white men.⁵

Black women had increased epinephrine reactivity in the follicular compared with the luteal phase of the menstrual cycle. Catecholamines can cause both -adrenergically mediated vasoconstriction and ß-adrenergically mediated vasodilation. Recent studies indicate that ß-receptor–mediated vasodilation is blunted in blacks.⁶ Black women in the follicular phase developed the greatest increase in diastolic pressure during the speaking task, perhaps as a response to the -adrenergic effects of their catecholamines without a compensating ß-mediated vasodilation.

In summary, the findings suggest that unlike white women, black women do evidence menstrual cycle phase–related changes in catecholamine and cardiovascular stress-induced responsivity. These data may help clarify inconsistencies in prior studies of menstrual cycle effects on stress reactivity in which the subjects' race was not explicitly evaluated. The findings underscore the need for consideration of an individual's race when reproductive hormone effects on catecholamine and cardiovascular physiology are being evaluated and suggest a differential role of reproductive hormones on blood pressure regulation between black and white women. The findings also suggest that reproductive hormones may mitigate against racial differences in stress reactivity that are often observed in men.

	Acknowledgments

 
This work was supported by grants MO1RR-00827, HL-36005, and HL-47074 from the National Institutes of Health.

Received October 3, 1995; first decision November 6, 1995; accepted January 8, 1996.

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				R. R. Freedman and R. Girgis Effects of Menstrual Cycle and Race on Peripheral Vascular {alpha}-Adrenergic Responsiveness Hypertension, March 1, 2000; 35(3): 795 - 799. [Abstract] [Full Text] [PDF]

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