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Journal of Clinical Endocrinology & Metabolism, doi:10.1210/jc.2004-1897
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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 8 4516-4520
Copyright © 2005 by The Endocrine Society

Differences in Serum Sex Hormone and Plasma Lipid Levels in Caucasian and African-American Premenopausal Women

Stefania Lamon-Fava, Junaidah B. Barnett, Margo N. Woods, Christina McCormack, Judith R. McNamara, Ernst J. Schaefer, Christopher Longcope1, Bernard Rosner and Sherwood L. Gorbach

Lipid Metabolism Laboratory, Jean Mayer United States Department of Agriculture Human Nutrition Research Center on Aging (S.L.-F., J.R.M., E.J.S.), Gerald J. and Dorothy R. Friedman School of Nutrition Science and Policy (S.L.-F., J.B.B., M.N.W., E.J.S., S.L.G.), and Department of Family Medicine and Community Health, School of Medicine (J.B.B., M.N.W., C.M., S.L.G.), Tufts University, Boston, Massachusetts 02111; Department of Medicine (C.L.), University of Massachusetts Medical School, Worcester, Massachusetts 01655; and Harvard Medical School (B.R.), Boston, Massachusetts 02115

Address all correspondence and requests for reprints to: Stefania Lamon-Fava, M.D., Ph.D., Lipid Metabolism Laboratory, Jean Mayer United States Department of Agriculture Human Nutrition Research Center on Aging, Tufts University, 711 Washington Street, Boston, Massachusetts 02111. E-mail: stefania.lamon-fava{at}tufts.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Risk of coronary heart disease is higher in African-American than in Caucasian women.

Objective: The aim of this study was to evaluate the contribution of sex hormone levels, race, and measures of body fat to the variation in plasma lipid levels, a well-established risk factor for coronary heart disease.

Design: This was a cross-sectional study.

Setting: The study was conducted in the general community.

Study Participants: Sixty Caucasian and 117 African-American premenopausal women participated.

Main Outcome Measures: Body weight, body mass index (BMI), and waist to hip circumference ratio (WHR), as well as plasma lipid and serum sex hormone levels, were assessed.

Results: Relative to Caucasian women, African-American women had significantly higher mean BMI (23.92 ± 3.87 vs. 26.99 ± 5.87 kg/m2, respectively; P < 0.001), and WHR (0.733 ± 0.052 vs. 0.757 ± 0.068; P < 0.03). Also, plasma triglyceride (TG) levels were significantly lower in African-American women (81 ± 61 vs. 55 ± 24 mg/dl; P < 0.0001). Serum estrone sulfate (556 ± 323 vs. 442 ± 332 pg/ml, Caucasian vs. African-American; P < 0.001), estradiol (E2) (55.1 ± 43.6 vs. 35.8 ± 17.7 pg/ml; P < 0.0001), androstenedione (2.6 ± 0.9 vs. 1.6 ± 0.7 ng/ml; P < 0.0001), and testosterone (0.36 ± 0.12 vs. 0.31 ± 0.19 ng/ml; P < 0.002) levels were significantly lower in African-American women than in Caucasian women. After correction for the effects of age, BMI, and WHR, serum E2 levels were significantly and positively associated with plasma high-density lipoprotein cholesterol levels in all women, and serum estrone sulfate levels with plasma total cholesterol and TG levels in African-American women.

Conclusions: Our results indicate that race is an important determinant of plasma TG and serum sex hormone levels, even after adjustment for differences in body size. A significant association between endogenous E2 and high-density lipoprotein cholesterol levels exists in premenopausal women, independent of their race.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
CORONARY HEART DISEASE (CHD) is the leading cause of death in women in the United States (1). In women, as well as in men, there are racial/ethnic differences in the rate of CHD, with African-Americans having higher rates than Caucasians (1, 2, 3). Established risk factors for CHD in all populations include hypertension, smoking, diabetes mellitus, family history of premature CHD, elevated plasma levels of low-density lipoprotein cholesterol (LDL-C) and low levels of high-density lipoprotein cholesterol (HDL-C) (4, 5). Elevated plasma triglyceride (TG) levels have also been shown to be a risk factor for CHD, especially in women (6, 7). Hypertension, diabetes mellitus and elevated body mass index (BMI) are more frequently observed in African-American women than in Caucasian women (8). However, African-American women tend to have lower plasma TG and higher plasma HDL-C levels than Caucasian women (9, 10, 11). A higher rate of TG clearance in African-Americans may account, at least in part, for these racial differences in plasma lipid levels (12). Also, levels of endogenous sex hormones play some role in the determination of plasma lipid levels, with estrogen levels being positively associated with HDL-C levels in Caucasian women (13, 14). The contribution of serum sex hormone levels, BMI, and waist to hip circumference ratio (WHR) to the difference in plasma lipid levels in African-American and Caucasian women has not been studied in detail.

The current study examines the effect of sex hormones, race, BMI, and WHR on plasma lipid levels in young premenopausal women. Because previous studies had shown sex hormone-related fluctuations in plasma lipid levels during the menstrual cycle (15), all subjects were studied during the midfollicular phase of the cycle.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

A total of 60 Caucasian and 117 African-American premenopausal female volunteers aged 18–36 yr were enrolled into the study. The study was approved by the Institutional Review Board of Tufts University-New England Medical Center, and all subjects gave written informed consent before starting the study. Subjects were screened initially by a questionnaire exploring various aspects of their health status and diet. Subjects were excluded if they were pregnant, lactating within the last 3 months, or had heart disease, hypertension, diabetes mellitus, renal or liver disease, or any other major illness. Other criteria for exclusion were: irregular menstrual cycles (women qualified only if they had been menstruating regularly for at least the past 3 months), menstrual cycle lengths of less than 21 d or more than 35 d. To avoid biases due to lifestyle or medication effects on plasma lipid and hormone levels, women who consumed a diet different from the average American diet (i.e. with <30% total fat) or a vegetarian diet, or who were binging, consuming alcohol on a regular basis (>5 ounces per week), smoking (within the last 3 months), or using prescribed medications or oral contraceptives (during the last 3 months) were excluded from the study. Women with extreme levels of physical activity (i.e. those who were in training for any athletic competition) were also excluded from the study. A relative overrepresentation of African-Americans in subject recruitment was due to specific efforts to enroll subjects from this minority population and additional funding from the National Institutes of Health.

Body weight and height were measured using only underwear and a hospital gown, without any footwear. WHR was the average of three measurements of waist circumference (the smallest horizontal circumference between the lowest rib and the iliac crest), and hip circumference (the horizontal circumference around the largest protrusion of the buttocks) (16).

Blood samples were collected on either three (n = 86) or two (n = 91) consecutive mornings (20 ml on each day for hormone determinations and an additional 20 ml on the day of lipid and hormone determinations) between d 4 and 7 of the follicular phase of the subject’s menstrual cycle. Subjects fasted overnight for 8 h before each blood drawing for hormone determinations, and for 14 h before blood drawing for lipid and lipoprotein determinations.

Laboratory analyses of endogenous hormones

Blood samples were collected each day on d 4–7 of the cycle and centrifuged at 1000 x g for 25 min at 4 C, and serum samples were stored at –70 C for not more than 6 months before sample analysis for sex hormones and SHBG levels. The blood samples collected on consecutive mornings from the first 104 subjects were analyzed as individual samples. However, the blood samples collected on consecutive mornings from the remaining 73 subjects were pooled and analyzed as 73 pooled samples due to budgetary limitations. Estrone (E1), estrone sulfate (E1SO4), and estradiol (E2) were measured by RIA involving solvent extraction and celite column chromatography as previously described (17, 18). Androstenedione (A) was measured by RIA using a kit from Diagnostic Systems Laboratory (Webster, TX). Testosterone (T) was measured by RIA using a kit from Diagnostic Products (Los Angeles, CA). Free E2 and free T were measured by using an ultrafiltration technique (19). The diethylaminoethyl cellulose filter technique was used to measure levels of SHBG (20). All samples were coded using a random number system, and blinded duplicates were included as a quality control measure. The coefficients of variation (CV) for all assays were as follows (hormone, interassay CV and intraassay CV, respectively): E1, 5.28 and 3.32; E1SO4, 9.83 and 3.55; E2, 6.85 and 4.95; A, 8.96 and 3.54; T, 8.77 and 5.07; and SHGB, 10.9 and 8.0. These coefficients are comparable in magnitude to other published coefficients (21).

Measurement of plasma lipids and lipoproteins

Blood samples for lipid measurements were collected in 0.1% EDTA, centrifuged for 25 min at 1000 x g at 4 C, and analyzed within 48 h. Determination of plasma total cholesterol (TC) and TG levels was performed by automated enzymatic methodology using an Abbott Diagnostics Spectrum CCX Chemistry analyzer and Abbott reagents (Abbott Laboratories, North Chicago, IL) (22). HDL-C levels were determined in the supernatants obtained after precipitation of the apolipoprotein B-containing lipoproteins using a dextran sulfate-Mg2+ procedure, as previously described (23). The TC and HDL-C measurements have been standardized with the Centers for Disease Control and Prevention-National Heart, Lung, and Blood Institute Standardization Program. In subjects with TG levels less than 400 mg/dl, the very low-density lipoprotein cholesterol concentrations were calculated as TG/5, and the plasma LDL-C concentrations were obtained with the following equation: LDL-C = TC – (TG/5 + HDL-C) (24). Only one subject had fasting TG levels above 400 mg/dl. The TC/HDL-C ratio was also computed. CVs were less than 2% for TC, and less than 3% for TG and HDL-C.

Statistical analyses

Data entry and statistical analyses were performed using SPSS for Windows 12 (SPSS Inc., Chicago, IL). Differences in mean age, anthropometric characteristics (body weight, height, BMI, and WHR), and plasma lipid and serum hormone levels between Caucasian and African-American women were tested using Mann-Whitney U test. Due to their skewed distribution, a logarithmic transformation was applied to TC, TG, LDL-C, and all hormone variables, and a square root transformation was applied to HDL-C. Multiple regression analyses, with age, BMI, WHR, and race in the model, were used to assess the contribution of these parameters to plasma lipid and serum hormone levels. Multiple regression analysis models were used to assess the contribution of hormone levels to plasma lipid levels. BMI and WHR were entered in the same model because of mild collinearity (r = 0.53).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
The age and anthropometric measures in the two groups of study participants are shown in Table 1Go. Premenopausal women in the Caucasian and African-American groups had similar mean age. Although the average height in the two groups was similar, African-American women had significantly higher body weight, BMI, and WHR than Caucasian women (Table 1Go).


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  		TABLE 1. Characteristics of young premenopausal women by ethnic group

 
The plasma lipid profiles in the two groups of young women were similar, with the exception of significantly lower mean plasma TG levels in African-American women than in Caucasian women (Table 2Go). Although plasma LDL-C levels tended to be higher in African-American women compared with Caucasian women, this difference was not statistically significant.


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  		TABLE 2. Plasma lipid and serum hormone concentrations by ethnic group

 
Serum hormone levels were affected by race, with African-American women having significantly lower serum levels of all estrogenic hormones but also lower A and T levels than Caucasian women (Table 2Go). Serum levels of SHBG were not affected by race.

Multiple linear regression analyses indicated a significant association of both BMI and WHR with plasma TG, HDL-C levels, and the TC to HDL ratio, and of BMI with LDL-C levels (Table 3Go). Age was significantly associated with TC, LDL-C, and HDL-C levels. Only plasma TG levels were significantly associated with race. Results were not affected when serum E1, E1SO4, E2, A, and T levels were entered into the model (data not shown). Race was strongly associated with levels of all sex hormones even after the effect of age, BMI, and WHR was taken into account (Table 3Go). Only the concentrations of androgenic hormones were significantly and inversely associated with age. A significant inverse association between SHBG levels and BMI was observed as well.


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  		TABLE 3. Relationship of plasma lipid and serum hormone levels with age and anthropometric variables using multiple linear regression analysis

 
After controlling for the effect of age, BMI, WHR, and race, serum E1SO4 levels were significantly associated with plasma TC and TG levels (Table 4Go). However, separate analyses in the two racial groups indicated that this positive association was mostly observed in the African-American women (TC: ß coefficient = 0.187, P < 0.04; TG: ß coefficient = 0.205, P < 0.2) and not in the Caucasian women (TC: ß coefficient = 0.006, NS; TG: ß coefficient = 0.015, NS).


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  		TABLE 4. Relationship between plasma lipids and sex hormones and SHBG using multiple linear regression analyses

 
Serum E2 levels (Table 4Go) were significantly associated with plasma HDL-C levels and this association remained significant after SHBG levels were entered into the model (ß = 0.182, P = 0.024). A similar contribution of serum E2 levels to plasma HDL-C levels was observed in both African-American and in Caucasian women (ß coefficient = 0.142, P = 0.112 and ß coefficient = 0.151, P = 0.222, respectively). No contribution of sex hormone levels to other plasma lipid and lipoprotein levels was observed.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Young African-American women in this study had higher BMI and WHR than Caucasian women. This finding is consistent with previous observations (11). Lifestyle factors may play some role in the difference in BMI and predisposition to CHD between African-American and Caucasian women, and higher dietary fat intake and lower physical exercise have been reported in African-American than in Caucasian young women (11).

In our study, serum hormone levels were clearly affected by race, with African-American women having significantly lower serum levels of all estrogenic hormones but also lower A and T levels than Caucasian women, whereas serum levels of SHBG were not affected by race. This finding of African-American women having lower serum levels of estrogenic hormones including E1, E2, and E1so4 during the follicular phase of the menstrual cycle, compared with Caucasian women, is somewhat unexpected, because BMI and WHR are typically positively associated with estrogen levels in women (25) and in this, as well as in other studies, African-American women had higher BMI and WHR than Caucasian women (11, 26). Some, but not all, previous studies have indicated similar sex hormone differences in African-American and Caucasian women (27, 28). Reutman et al. (29) have shown significantly lower urinary LH to FSH ratios during the follicular phase in African-American than in Caucasian women, supporting the possibility of racial differences in serum sex hormone levels. Differences in E2 levels have been observed in other racial groups, with Chinese and Japanese women showing lower unadjusted E2 levels than Caucasian women and Hispanic women having similar E2 levels to Caucasian women (30). Lower T levels have been reported in African-American than in Caucasian perimenopausal women after adjustment for BMI, age, and smoking status (30), consistent with the findings in our subjects.

The plasma lipid profiles in the two groups of young women were similar, with the exception of significantly lower mean plasma TG levels in African-American women than in Caucasian women, and a trend toward higher plasma LDL-C levels in African-American women compared with Caucasian women. This observation is consistent with previous studies showing lower TG levels in both African-American men and women than in Caucasian men and women (9, 10, 11, 31). African-American women have been found to have less visceral fat or metabolically active fat, and have more sc fat compared with white women with similar age, WHR, and BMI (32). This may account for lower TG and higher HDL-C levels observed in African-American women in those studies. Also, racial differences in lipoprotein metabolism may help explain the difference in TG levels between these two groups, because a more efficient TG clearance has been shown in African-Americans than in Caucasians (12). This is mediated by a higher activity of lipoprotein lipase, the enzyme that mediates the catabolism of TG in VLDL and in chylomicrons, in African-Americans (12).

In our study, in contrast with previous studies (31), but in agreement with others (33), we did not find a difference in HDL-C between the two groups of women. It is possible that, due to the significant relationship between E2 levels and HDL-C levels observed in this study, lower E2 levels in our African-American women may account in part for the lower HDL-C levels in this group.

In our study, endogenous serum E2 levels were positively associated with plasma HDL-C levels after controlling for the effects of age, BMI, WHR, and race. These findings are consistent with our previous observation of a significant correlation between levels of E2 and apolipoprotein A-I, the major protein component of HDL, in young Caucasian athletes (13). A positive association between plasma E2 and HDL2 levels in Pima Indian women has been reported as well (34). Our study indicates that such association is also present in African-American premenopausal women. The role of exogenous E2 in regulating HDL-C levels has been studied in pre- and in postmenopausal women (35, 36, 37). Oral treatment with E2 in both groups resulted in increased HDL-C levels, due to increased production of apolipoprotein A-I (35, 36, 37). Our data suggest that also endogenous E2 may modulate HDL-C levels. The contribution of E2 to HDL-C levels was of similar magnitude in both racial groups.

We also found that serum E1SO4 levels significantly contributed to plasma TC and TG levels, but this contribution was mostly due to significant associations in African-American but not Caucasian women. A significant positive association between serum estrone and plasma TC and TG levels, which disappeared after adjustment for fat mass and plasma insulin and free fatty acid levels, has been previously reported in a group of 67 men (38). The significance of these associations in African-American women is not known, and is complicated by the fact that we cannot assume that these relationships are necessarily instantaneous.

Both BMI and WHR were significantly associated with plasma lipid and lipoprotein levels, with TG and LDL-C levels being increased by increases in these measures, and HDL-C being negatively associated with BMI. These results emphasize the fact that body weight and central adiposity are major contributors of plasma lipid levels, independent of race, and are consistent with our previous observation that BMI is a significant predictor of both LDL-C and HDL-C levels (39).

The main limitation of our study is the small sample size (n = 177), which is associated with a relatively higher risk of a type I error. However, our findings concerning racial differences in TG are consistent with those of previous larger studies (9, 10, 11, 31). The characterization of hormone and lipid concentrations in a larger population is warranted. Another limitation of our study concerns the fact that hormone levels were assessed only at a single point during the menstrual cycle and that only one menstrual cycle was assessed. Our conclusions are based on the assumption that the hormonal differences that we have observed in the mid-follicular phase of these women are likely representing hormonal differences across the menstrual cycle and across menstrual cycles. Finally, an additional limitation of our study is that data on both phytoestrogen intake and physical activity were not available on our subjects.

In conclusion, this study indicates that race is a significant predictor of plasma TG and sex hormone levels. In addition, endogenous E2 levels are positively associated with HDL-C levels in both Caucasian and African-American premenopausal women. Also, BMI and WHR play an important role in determining plasma lipid levels in both African-American and Caucasian women.


   Footnotes
 
This work was supported by the National Institutes of Health Minority Investigator Award R37CA45128-0952 from the National Cancer Institute (to J.B.B.), and the Massachusetts Department of Public Health Breast Cancer Research Award Grant SCDPH 3408699 D001. Support was also provided by the Agriculture Research Service contract 53-3K06-5-10, National Institutes of Health Grant HL03209, and the General Clinical Research Center funded by the Division of Research Resources of the National Institutes of Health under Grant MO1-RR00054.

First Published Online May 10, 2005

1 C.L. is deceased. Back

Abbreviations: A, Androstenedione; BMI, body mass index; CHD, coronary heart disease; CV, coefficient of variation; E1, estrone; E1SO4, estrone sulfate; E2, estradiol; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; T, testosterone; TC, total cholesterol; TG, triglyceride; WHR, waist to hip circumference ratio.

Received September 27, 2004.

Accepted April 28, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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