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Clinical Centers: University of Michigan (J.F.R., M.S.), Ann Arbor, Michigan 48109; Massachusetts General Hospital (J.S.F.), Boston, Massachusetts 02114; Rush University, Rush-Presbyterian-St. Luke’s Medical Center (J.L.), Chicago, Illinois 60612; University of California (E.B.G., B.S., B.L.L.), Davis, California 95616; University of California (S.G.K.), Los Angeles, California 90024; University of Medicine and Dentistry/New Jersey Medical School (N.S.), Newark, New Jersey 07103; University of Pittsburgh (K.A.M.), Pittsburgh, Pennsylvania 15213; Laboratories: University of Michigan (D.S.M.), Ann Arbor, Michigan 48109; and Medical Research Laboratories, Highland Heights, Kentucky 41076; Coordinating Centers: University of Pittsburgh, Pittsburgh, Pennsylvania 15261; and New England Research Institute (B.A.M.), Watertown, Massachusetts 02172
Address all correspondence and requests for reprints to: John F. Randolph, Jr., M.D., L4228 Women’s Hospital, University of Michigan Health System, 1500 East Medical Center Drive, Ann Arbor, Michigan 48109-0276.
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Abstract |
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Introduction |
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No study, whether cross-sectional (6) or longitudinal (1, 7, 8), has investigated ethnic differences in reproductive hormones in midlife women. However, ethnic variation in hormone concentrations has been observed in menopausal women, as serum E2 levels are lower in Chinese women than in Caucasian women (9). In addition, host factors, such as body size and smoking behavior, are related to hormonal characteristics of the transition. These factors have not been studied in relation to ethnic differences in reproductive hormone concentrations during the menopausal transition.
The Study of Women’s Health Across the Nation (SWAN) is a community-based longitudinal, prospective, multiethnic, multidisciplinary study of the natural history of the menopausal transition. Participants were recruited from five self-designated groups: African-American, Caucasian, Chinese, Japanese, and Hispanic women. The purpose of this report is to determine whether reproductive hormone concentrations differ by race/ethnicity in premenopausal and early perimenopausal women and, if there are differences, to determine whether these differences can be explained by individual host factors, including body mass index (BMI), age, smoking, alcohol use, and physical activity.
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Subjects and Methods |
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SWAN is a multisite, longitudinal cohort study being conducted in community-based groups of women. At baseline, 3302 women who belonged to one of 5 ethnic/racial groups were recruited: Caucasian (n = 1550), African-American (n = 935), Japanese (n = 281), Chinese (n = 250), and Hispanic (n = 286). Eligibility criteria for entry into the SWAN longitudinal cohort were: age of 42–52 yr, intact uterus and at least 1 ovary, no current use of estrogens or other medications known to affect ovarian function, at least one menstrual period in the 3 months before screening, and self-identification as a member of 1 of the 5 eligible ethnic groups. Cohort recruitment and enrollment have been described in detail (10). In brief, participants were enrolled at 7 clinical sites in the following geographic areas: Boston, Massachusetts; Chicago, Illinois; the Detroit area, Michigan; Los Angeles, California; Hudson County, New Jersey; Oakland, California; and Pittsburgh, Pennsylvania. Recruitment techniques were designed to generate a representative sample of women at each of the 7 sites. All 7 sites enrolled Caucasians, and each site also enrolled women belonging to 1 prespecified minority ethnic group. African-American women were enrolled in Boston, Chicago, the Detroit area, and Pittsburgh, whereas Japanese, Chinese, and Hispanic women were enrolled in Los Angeles, Oakland, and Hudson County, respectively. Institutional review board approval was obtained at each study site.
Measures
Common assessment protocols were observed across the seven clinical sites, supported by a written manual of operations, common training, and standardization of research staff.
Primary race/ethnicity was self-defined as Black or African-American, non-Hispanic Caucasian, Chinese or Chinese-American, Japanese or Japanese-American, or Hispanic (Central American, Cuban or Cuban-American, Dominican, Mexican or Mexican-American, Puerto Rican, South American, Spanish, or other Hispanic). Non-Hispanic Caucasians were used as the reference group. Height (centimeters) and weight (kilograms) were measured using a stadiometer and calibrated scales. The BMI was calculated as weight (kilograms)/height (meters)2.
Age, smoking behavior, alcohol use, and physical activity were self-reported. Seven smoking questions were adapted from the American Thoracic Society standards (11). Cigarette smoking was categorized as never, former, or current smoker and number of cigarettes currently smoked per day. Alcohol intake was categorized as none, less than the median of nonzero intake, and more than or equal to the median of nonzero intake. Physical activity was assessed in four domains, recreational, household/caregiving, routine daily living, and occupational, using an adaptation of the Baecke questionnaire (12, 13). A summary measure representing total nonoccupational activity was computed by summing the scores for the first three domains. Menopausal status was based on self-report of decreased predictability in the time between menses in the prior 3 months (early perimenopausal) or no decreased predictability in the same time period (premenopausal) (14).
Phlebotomy was performed in the morning after an overnight fast. Women were scheduled for venipuncture on d 2–5 of a spontaneous menstrual cycle occurring within 60 d of recruitment. Two attempts were made to obtain the d 2–5 sample. If a timed sample could not be obtained, a random fasting sample was taken within the 90-d period of recruitment. Blood was refrigerated 1–2 h after phlebotomy, and after centrifugation, the serum was aliquoted, frozen, and batched for shipment to the central laboratory. At the central laboratory, samples were catalogued and assayed continuously upon arrival.
Hormone assays were conducted in singlicate using an ACS-180 automated analyzer (Bayer Corp., Norwood, MA). Serum E2 concentrations were measured with a modified, off-line ACS-180 (E2–6) immunoassay. Inter- and intraassay coefficients of variation averaged 10.6% and 6.4%, respectively, over the assay range, and the lower limit of detection was 1 pg/ml. Serum FSH concentrations were measured with a two-site chemiluminometric immunoassay using constant amounts of two monoclonal antibodies provided by Bayer Corp. Each antibody is directed to different regions on the ß-subunit [one coupled to paramagnetic particles, and the other labeled with dimethyl-acridinium ester (DMAE)] with specificity for intact FSH. Inter- and intraassay coefficients of variation were 12.0% and 6.0%, respectively, and the lower limit of detection was 1.1 IU/liter. Serum testosterone (T) concentrations were determined by competitive binding of a DMAE-labeled T derivative to a rabbit polyclonal anti-T antibody premixed with monoclonal antirabbit immunoglobulin G antibody immobilized on the solid phase paramagnetic particles. Inter- and intraassay coefficients of variation were 10.5% and 8.5%, respectively, and the lower limit of detection was 2 ng/dl.
The de novo two-site chemiluminescent assays for serum SHBG and DHEAS concentrations involved competitive binding of DMAE-labeled SHBG or DHEAS to a commercially available rabbit anti-SHBG or anti-DHEAS antibody and a solid phase of goat antirabbit IgG conjugated to paramagnetic particles. Inter- and intraassay coefficients of variation for SHBG were 9.9% and 6.1%, respectively, and the lower limit of detection was 2 nM. Inter- and intraassay coefficients of variation for DHEAS were 11.3% and 7.6%, respectively, and the lower limit of detection was 2 µg/dl.
Total T was indexed to SHBG to calculate the free T index (FTI = 100 x T (ng/dl)/28.84 x SHBG (nM). Likewise, total E2 was indexed to SHBG to calculate the free E2 index (FEI = 100 x E2 (pg/ml)/272.11 x SHBG (nM) (15).
Women who had missing hormone data (n = 9), phlebotomy outside the 3-month blood collection window (n = 53), phlebotomy on an unknown day of the menstrual cycle (n = 57), or reported use of oral or inhaled steroids (n = 253) were excluded from this analysis, yielding a sample of 2930 participants. Those women with data excluded for reasons other than steroid use were more likely to be Hispanic and less likely to be Japanese. Women with excluded data also had lower DHEAS and higher E2 concentrations, and were more likely to be classified as early perimenopausal or in the middle to end of the transition. They were also less likely to report that their cycles were the same as the previous year (data not shown) than women included in the analysis. These indications are consistent with the interpretation that these women may have been further along in the menopausal transition.
Analysis
Unadjusted hormone distributions were compared by ethnicity and other categorical covariates using ANOVA or t tests. Pearson correlations were used to describe the strength and direction of the relationships between the hormones and the continuously distributed host factors (age, BMI, physical activity, and actual day of cycle). Because the distributions of the hormone concentrations, BMI, and physical activity were skewed, these variables were log-transformed for analysis. However, untransformed results are reported, unless indicated. Analysis of covariance was used to estimate and compare mean hormone concentrations by ethnicity, before and after including host factors. Adjusted means were computed and then back-transformed from the logarithmic scale to their original scale for presentation (16). All adjusted models included ethnicity, clinical site, menopausal status, BMI, age, smoking, alcohol intake, and the day of menstrual cycle when phlebotomy was undertaken. Day was categorized as d 1–2, 3, 4, 5, and 6–7, and not on d 1–7. The interaction between ethnicity and BMI was controlled for if statistically significant. Because physical activity was not associated with the hormones in preliminary multivariable models and did not appear to have any confounding effects, it was dropped from the final models. To adjust for multiple comparisons, P values for categorical covariates were adjusted using the Bonferroni method. Tertile cut-off points based on the full sample were used for Fig. 1
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Results |
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, the mean age and median BMI of the population were 46 yr and 26.5 kg/m2, respectively. All hormones, but particularly E2 and FSH, had great variability. The mean E2 level was almost 40% greater than the median, and the mean FSH level was 50% greater than the median, indicating the significant right skew of measured concentrations.
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. Chinese and Japanese women had the lowest unadjusted serum E2 concentrations, whereas Hispanic and Caucasian women had the highest levels. No differences in unadjusted serum FSH concentrations were observed among ethnic groups. Unadjusted serum T concentrations varied significantly among ethnic groups, with the lowest levels in Hispanic women. Serum DHEAS concentrations were 60% higher in Chinese women than in African-American women. Chinese women had the lowest serum SHBG concentrations, whereas Japanese women had the highest. Significant group differences were noted as well in FTI and FEI (data not shown).
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Table 3 shows the modest correlations between log hormone concentrations and selected host characteristics. The strongest associations were between BMI and SHBG (r = -0.29), BMI and FTI (r = 0.29), and age and FSH (r = 0.30).
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). Disproportionately few African-American and Hispanic women fell in the lowest tertile of BMI, and few Chinese and Japanese women fell in the highest tertile (Fig. 2). Thus, we examined the interaction of BMI (as a continuous variable) and ethnicity for each hormone. Except for SHBG and FTI, we found no significant interactions, indicating that the relation of BMI to hormone levels did not differ by ethnic group.
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shows the mean serum hormone concentrations by ethnicity and menopausal status after adjustment for ethnicity, status, site, day of cycle, log BMI, age, smoking, and alcohol use. In contrast to unadjusted E2 levels, the adjusted mean serum E2 levels did not differ significantly by ethnicity or menopausal status, although there was a trend toward lower concentrations in Chinese and Japanese women. Moreover, whereas there were no ethnic differences in unadjusted FSH levels, adjusted serum FSH concentrations were significantly higher in African-American and Hispanic women than in Caucasian and Asian women (P < 0.05) and were higher in early perimenopausal women than in premenopausal women (P < 0.0001). Adjusted serum DHEAS levels were 73% higher in Chinese women than in African-American women (P < 0.0001). African-American and Hispanic women had slightly lower adjusted mean serum T levels than Caucasian or Asian women (P < 0.05). Neither mean serum SHBG concentrations nor FTI differed by status.
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Discussion |
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These results confirm earlier observations that unadjusted serum E2 levels are significantly lower in Chinese women than in Caucasian women (9), but emphasize the importance of adjusting for other host characteristics, such as BMI. Adjusting for these variables eliminated significant differences in serum E2 concentrations among ethnic groups, although adjusted serum E2 levels were 13% lower in Asian women than in Caucasian women. Lower unadjusted E2 concentrations may be related to earlier observations of reduced symptom reporting, especially for hot flashes, in Asian women (17, 18, 19, 20, 21, 22, 23), an observation also identified in SWAN (24), possibly because serum E2 levels may fall less markedly as Asian women become menopausal. Both unadjusted and adjusted serum T concentrations were lower, and adjusted serum FSH concentrations were higher in Hispanic women than in Asian and Caucasian women. Adjusted serum FSH levels were higher, and serum T levels were lower in African-American women than in Asian and Caucasian women. These findings may be due to an earlier menopause in African-American women (25, 26, 27).
BMI had important effects on all hormones. With increasing BMI, serum E2, FSH, DHEAS, and SHBG levels decreased, and serum T levels increased in each ethnic group. However, the lack of overlap in body size across ethnicities was problematic for comparing hormones by ethnicity. Despite the discrepant ranges of body size, only SHBG concentrations varied differently by BMI across ethnic groups. These data demonstrate that body size is an important factor in making hormonal assessments, and that ethnic discrepancies in body size can confound such analyses.
As expected, serum FSH levels were higher in early perimenopausal women than in premenopausal women, whereas serum E2 levels did not differ by menopausal status (6). Serum FSH, but not serum E2, concentrations were higher in current smokers, whereas neither E2 nor FSH levels differed between women who did or did not consume alcohol (28, 29). Serum T, DHEAS, and SHBG levels were higher in current smokers than in nonsmokers and in women whose alcohol consumption was above the median (28, 29). Physical activity had little or no effect on reproductive hormone concentrations.
Serum FSH concentrations varied by day of cycle due to a slight rise on d 6 and 7 and a greater increase in samples drawn outside the d 1–7 window. Serum FSH concentrations are stable across d 2–5 in normally cycling young women (30, 31), but it was not clear whether they remained so in older women (32, 33). Our data demonstrate that early follicular FSH levels are stable in older cycling women. The increase in serum FSH levels in perimenopausal women and not in premenopausal women despite similar serum E2 levels suggests an escape from ovarian negative feedback and is consistent with a decline of another negative feedback modulator of FSH, such as inhibin B (34, 35, 36).
There was marked variability in the serum concentrations of the two hormones measured most commonly in the clinical evaluation of perimenopausal women, FSH, and E2, both before and after controlling for potential confounding variables. This variability emphasizes the limitation in using these hormones, particularly single time assessments, as endocrine markers of the menopausal transition. It is likely that variability in serum FSH and E2 levels will increase as the cohort ages and transitions through the menopause.
Serum concentrations of DHEAS were negatively correlated with menopausal status in the unadjusted model, but the correlation was no longer significant when adjusted for age and other host factors. DHEAS is the most commonly measured serum androgen in studies of aging. In cross-sectional studies, the aging process is associated with a progressive and steady decline in circulating adrenal androgens (3, 4). One recent longitudinal study also found that DHEAS levels decline with age, and that this decline was independent of the final menstrual period (26). In contrast, serum DHEAS levels increased transiently during the first 2 yr of SWAN as some women transitioned from late perimenopause to postmenopause (5). Thus, although data from cross-sectional studies suggest that DHEAS is a useful marker of the aging process, longitudinal studies are conflicting regarding a strict age-related decline across the menopausal transition.
Serum T levels did not vary by menopausal status, consistent with some cross-sectional and longitudinal (27) studies, but in contrast with other cross-sectional analyses (7, 37, 38). SHBG and calculated free steroid indexes also did not vary, as reported in some studies (38), but not others (8, 39). The largest longitudinal study to date (26) noted a decline in SHBG and a rise in FTI in conjunction with the fall in E2 beginning within 2 yr of the final menstrual period. Because all subjects in the SWAN cohort were still menstruating at the time of this baseline study, differences relative to the final menstrual period cannot be assessed until longitudinal data are complete.
We conclude that 1) unadjusted mean serum E2 and SHBG concentrations are lower in Chinese women, and mean serum T concentrations are lower in Hispanic women, in the early perimenopause; 2) when adjusted for body size and other host characteristics, mean serum E2 concentrations are not significantly different by ethnicity, but mean FSH levels are higher, and mean T levels are lower, in African-American and Hispanic women; 3) body size, as measured by BMI, is significantly correlated with all reproductive and somatic hormones measured in the perimenopause; 4) mean serum FSH levels increase, whereas serum E2, T, and SHBG concentrations and free steroid indexes do not vary over the early stages of the perimenopause; 5) mean serum DHEAS concentrations are negatively correlated with age, but not menopausal status; and 6) serum FSH and E2 concentrations in the early perimenopause are highly variable. These data raise the possibility that ethnic differences in menopausal symptoms and health outcomes are related to ethnic differences in reproductive hormones, but are highly confounded by body size. Moreover, these data emphasize that the clinical utilization of single measurements of FSH and E2 in perimenopausal women is limited by significant variability and is of questionable utility in the care of women at midlife.
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Footnotes |
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Abbreviations: BMI, Body mass index; DHEAS, dehydroepiandrosterone sulfate; DMAE, dimethyl-acridinium ester; E2, estradiol; FEI, free estradiol index; FTI, free testosterone index; SWAN, Study of Women’s Health Across the Nation; T, testosterone.
Received May 20, 2002.
Accepted January 7, 2003.
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