Sex Hormones in Postmenopausal Women Receiving Low-Dose Hormone Therapy: The Effect of BMI

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1 nature publishing group Sex Hormones in Postmenopausal Women Receiving Low-Dose Hormone Therapy: The Effect of BMI Irene Lambrinoudaki 1, Eleni Armeni 1, Demetrios Rizos 2, Eythimios Deligeoroglou 1, Panagiotis Kofinakos 1, George Kaparos 2, Andreas Alexandrou 3, Maria Creatsa 1, Emmanuel Logothetis 2 and Evangelia Kouskouni 2 The aim of our study was to evaluate the effect of BMI on the change in circulating sex hormone in postmenopausal women during 6 months of oral continuous combined low-dose hormone therapy (HT). Fifty postmenopausal women were allocated to receive daily one tablet containing combination of 17β-estradiol (1 mg)/norethindrone acetate (0.5 mg) for 6 months. Serum levels of follicle-stimulating hormone (FSH), estradiol, total testosterone, sex hormone-binding globulin (SHBG), free androgen index (FAI), free estrogen index (FEI), Δ4-androstendione (Δ4A), and dehydroepiandrosterone sulfate were assessed at baseline and at the end of 6 months. Mean absolute values and percent changes from baseline were compared between lean and overweight women. Mean FSH decreased and mean 17β-estradiol increased significantly in both groups (FSH lean: 82.3 ± 26.7 decreased to 45.0 ± 17.0 miu/ml, P = ; FSH overweight: 85.5 ± 22.1 decreased to 52.3 ± 23.8 miu/ml, P = 0.003; P between groups = 0.661; E2 lean: ± increased to ± pg/ml, P = 0.006; E2 overweight: ± increased to ± pg/ml, P = ; P between groups = 0.619). Lean individuals had statistically significant higher increments of FAI and specifically FEI compared to overweight (FEI lean; 0.14 ± 0.09 increased to 0.29 ± 0.14, P = 0.009; overweight 0.23 ± 0.18 increased to 0.52 ± 0.40, P = 0.126; P between groups = 0.034). Although BMI does not affect total 17β-estradiol changes, free sex steroid concentrations increase more steeply in lean compared to overweight women receiving oral low-dose HT. Obesity (2011) 19, doi: /oby Introduction Menopause occurs as a result of ovarian senescence at an average age of 51 years. An abrupt drop of serum levels of endogenous estradiol characterizes this changing hormonal milieu. Testosterone concentrations show little change during the menopausal transition, whereas dehydroepiandrosterone (DHEA) declines gradually with increasing age (1). Specifically in patients with bilateral oophorectomy, the decline in circulating estradiol occurs dramatically to undetectable levels, while these women experience a reduction in androstendione levels up to 50%, as well as a 70% decline in DHEA and testosterone levels (2). Hormone therapy (HT) is indicated for treatment of climacteric symptoms and urogenital atrophy and for improvement of the quality of life in postmenopausal women (3). The efficacy of HT is evaluated usually by the adequacy of relief of climacteric symptoms, while sex hormone concentrations are not commonly measured (4). Circulating estrogens in postmenopausal women under HT exhibit a wide fluctuation and are influenced by various factors related either to the regimen (active substance, dose, route of administration) or to the individual (4,5). The importance of measuring free steroid indices, as biologically active hormones has been repeatedly demonstrated (6,7). Furthermore, the concept that the biological effect of circulating hormones should be evaluated in the context of their change is increasingly being appreciated (8,9). In a recent analysis of the Estrogen in the Prevention of Atherosclerosis Trial population, the authors demonstrated that the progression of subclinical atherosclerosis was dependent on the change in circulating estradiol, testosterone, and sex hormone-binding globulin (SHBG) (6). BMI appears to influence circulating sex steroids in postmenopausal women under HT. The majority of the existing studies, however, focus on the association between the final 1 Second Department of Obstetrics and Gynecology, University of Athens, Aretaieio Hospital, Athens, Greece; 2 Hormonal and Biochemical Laboratory, University of Athens, Aretaieio Hospital, Athens, Greece; 3 First Department of Surgery, University of Athens, Laiko Hospital, Athens, Greece. Correspondence: Irene Lambrinoudaki (ilambrinoudaki@aretaieio.uoa.gr) Received 8 April 2010; accepted 15 August 2010; published online 14 October doi: /oby VOLUME 19 NUMBER 5 May

2 absolute levels of circulating sex hormones and not percent changes (4,10,11). A possible interaction of BMI with the effect of HT on circulating estrogens may have clinical relevance in HT-related breast cancer risk. A collaborative reanalysis of data from 51 epidemiological studies (12) as well as the Million Women Study reported a higher relative risk of breast cancer in women of lower BMI, without, however, evaluating sex hormone levels (13). The aim of our study was to evaluate the effect of BMI on the change in sex steroid levels in postmenopausal women during 6 months of continuous combined low-dose HT. Methods and Procedures Subjects This prospective open label study included originally 50 healthy women, eligible to receive HT from the Menopause Clinic of the Second Department of Obstetrics and Gynecology, University of Athens, Aretaieion Hospital. The women recruited for this study had been postmenopausal for at least 1 year and had intact ovaries and uterus. All women had moderate to severe vasomotor symptomatology. Before recruitment, patients underwent a gynecological and biochemical evaluation which included: Bimanual examination, breast examination, and mammography, PAP smear and transvaginal sonography, thyroid liver renal function, and bone densitometry. Inclusion criteria in the study were a sonographically assessed endometrial thickness 5 mm, and the absence of current or previous exposure to HT, gynecological malignancy, ischemic heart disease, thromboembolism, diabetes mellitus, nontreated thyroid dysfunction, or a history of estrogen-related cancer. Women with adherence and retention concerns (e.g., alcoholism) were not included in the study. Protocol study procedures A detailed medical history was recorded for every subject. Data regarding demographic and lifestyle parameters, cardiovascular risk, obstetrical, and gynecological history were collected through questionnaires. Subsequently, blood pressure, and anthropometric parameters were estimated. Eligible women were treated with continuous combined low-dose HT (E2 1 mg/norethindrone acetate (NETA) 0.5 mg, Activelle, Novo Nordisk, Copenhagen, Denmark), which was provided in the form of one daily tablet. Serum levels of hormones were measured at baseline and at 6 months after the start of HT. Finally, symptoms were assessed and compliance has been ensured through monthly telephone interviews with the subjects. Blood pressure and anthropometric components were measured in the morning and in light clothing in order to estimate the BMI. The presence of hypertension was defined as two blood pressure measurements of 140/90 mmhg. Weight was measured on an electronic scale and height was measured by using a stadiometer in the upright position. BMI was calculated using the following equation: BMI = body weight (kg)/height 2 (m). Subsequently, fasting venous blood samples were drawn at 8:30 9:30 am for the determination of levels of follicle- stimulating hormone (FSH), luteinizing hormone, estradiol, testo sterone, Δ4-androstendione (Δ4A), SHBG and dehydroepiandrosterone sulfate and the serum was stored at 80 C until assessment, which was performed in duplicate for each sample. All participants signed an informed consent. Institutional review board of Ethics Committee of Aretaieion Hospital approved this study. The same procedure was repeated at the end of the 6-month study. Hormone assays The plasma levels of FSH and luteinizing hormone were measured with the microparticle enzyme immunoassay kits on an Axsym analyzer (Abbott Laboratories, Abbott Park, IL). The lower limits of detection for FSH and luteinizing hormone were 0.37 and 0.50 miu/ml, respectively. The total coefficient of variation ranged from 5.3 to 8.5% for FSH and from 5.2 to 10.0% for luteinizing hormone. Estradiol was measured with the commercial enzyme immunoassay kit DSL (Diagnostic Systems Laboratories, Webster, TX). The total coefficient of variation ranged from 4.3 to 6.1%, with an intra- and interassay variability of 5 and 8%, respectively, and a sensitivity of 7 pg/ml. Δ4A was measured with the enzyme-linked immunosorbent assay kit (IBL androstendione enzyme-linked immunosorbent assay ; IBL, Hamburg, Germany). The inter-assay coefficient of variation ranged from 6.5 to 8.1%, the analytical sensitivity of the assay was 1.9 ng/dl. Total testosterone and DHEA-SO 4 were measured with the DPC kits total testosterone and DHEA-SO 4 on Immulite analyzer (Diagnostic Products, Los Angeles, CA). The total coefficient of variation ranged from 8.0 to 16.0% and from 8.1 to 15.0%, respectively. The analytical sensitivity was 0.05 ng/ml and 3 μg/dl, for the testosterone and the DHEA-SO 4 assay, respectively. SHBG concentrations were measured with a DPC Immulite SHBG chemiluminescent enzyme immunometric assay kit (Diagnostic Products) on an Immulite analyzer. The total coefficient of variation ranged from 4.1 to 9.2%, the sensitivity of the assay was 0.2 nmol/l. The free estrogen index (FEI) was calculated using total estradiol and SHBG values by the following equation: FEI = estradiol (pg/ml) 0.367/SHBG (μmol/l) (14) The free androgen index (FAI) (15) was calculated using total testosterone and SHBG values by the following equation: FAI = testosterone (ng/ml) /SHBG (nmol/l). The menopausal reference range of FSH and E 2 were FSH miu/ml and E 2 <30 pg/ml. Statistical analysis Statistical analysis was performed by SPSS version 17.0 (SPSS, Chicago, IL). Data are expressed as mean ± s.d. and percent changes. Aiming to examine the gradient between endogenous sex hormones between baseline and after 6 months of treatment, we dichotomized our study group according to the median BMI of the participants ( overweight and lean, respectively). Means of continuous variables were compared within groups by Student s paired t-test and between groups by ANOVA. Log-transformation was used in skewed data. Percent changes in hormones were computed by the equation: (follow-up hormone baseline hormone) 100/baseline hormone. Geometric means of percent changes were compared between groups by analyses of variances. The association between BMI and serum hormone values as continuous variables has been evaluated using Spearman s correlation coefficient. Statistical significance was set at the 0.05 level. Results Thirty-six women completed the 6-month study. Table 1 shows the anthropometric characteristics of the study group. The BMI of the subjects ranged from 18.2 to The menopausal age ranged from 1 to 8 years in the group of lean women, and from 1 to 9 years in the group of overweight women. Reasons for drop-out were vaginal bleeding (n = 6), breast tenderness (n = 2) and loss to follow-up (n = 6). Baseline characteristics were not different between women who dropped out and women who completed the study. Women were stratified according to the baseline median BMI (24.6 kg/m 2 ). The group of overweight women included 18 patients with BMI >24.6 kg/m 2 (range ), whereas the group of lean women BMI included 18 women with BMI 24.6 kg/m 2 (range ). The mean hormone levels for lean women vs. overweight women at baseline and final levels are presented in Table 2. Lean women had higher percent changes in FEI compared to overweight women (287.1% vs %, P = 0.034; Figure 1). BMI exhibited a borderline negative linear correlation with ΔFEI (r = 0.39, P = 0.07). Weight and BMI was stable throughout the study in both groups. Specifically, in lean women mean BMI was obesity VOLUME 19 NUMBER 5 May

3 Table 1 Anthropometric characteristics of lean and overweight postmenopausal women at baseline, presented as mean ± s.d. or percent values Anthropometric characteristics Lean (n = 18) Overweight (n = 18) P Age 48.4 ± ± Age at menarche 13.1 ± ± Months since menopause 23.6 ± ± BMI (kg/m 2 ) 21.7 ± ± Age at 1st delivery 25.7 ± ± Lactation ( 3 months) 8% 9% 0.80 First degree relative with breast cancer Alcohol consumption (daily) 0.0% 0.0% 1% 2% 0.56 Current smoking 3% 1% 0.32 One or more full-term deliveries 15% 9% ± 2.89 kg/m 2 at baseline and ± 2.73 kg/m 2 at the end of the study (P = 0.215); mean weight was 52.0 ± 8.49 kg at baseline and ± 8.13 kg at the end of the study (P = 0.205). In overweight women mean BMI levels was ± 1.49 kg/ m 2 at baseline and ± 1.50 kg/m 2 at the end of the study (P = 0.786); mean weight was ± 4.45 kg at baseline and ± 4.20 kg at the end of the study (P = 0.952). The mean change in BMI was ± 0.15 kg/m 2 for the group of lean women and ± 1.27 kg/m 2 for the group of overweight women. Climacteric symptomatology, based on the Greene Climacteric Scale (16), improved in both groups at the end of 6 months (lean women baseline 2.9 ± 2.2, followup 1.1 ± 1.9, P < overweight women baseline 2.7 ± 2.0, follow-up 1.3 ± 1.6, P < 0.001). Discussion The results of this study indicate that although absolute levels of FEI are higher in overweight women under oral low-dose HT, percent increase in FEI is more pronounced in lean women. Adipose tissue plays an important role in determining at least a part of serum estradiol levels. After the menopausal cessation of the ovarian production, estrogens are produced in a number of extragonadal sites, through the aromatization of testosterone. The ovaries and the adrenals are responsible for the synthesis of circulating androgens, in the form of androstendione, DHEA, dehydroepiandrosterone sulfate, and testosterone. Extragonadal aromatization sites include principally mesenchymal cells of adipose tissue, osteoblasts, and numerous sites in the brain, the vascular endothelium and aortic smooth muscle cells. Postmenopausal estradiol levels, therefore, depend mainly on androgen precursors (17). The bioavailability of estradiol to the tissues, furthermore, depends also on circulating SHBG. Higher BMI and insulin levels correlate negatively with SHBG concentration, resulting in higher levels of free sex steroids (18). FEI represents the proportion of circulating estradiol (2% of the total) which is protein free, and therefore is able to cross the endothelial barrier and bind to estrogen receptors in target cells. Serum levels of estradiol are higher among postmenopausal women treated with HT compared to nonusers (19). The recent Norwegian Women and Cancer study (10) revealed a dose- depended relation between the E2 content of HT and concentrations of estradiol and FSH in users of both oral and transdermal HT. Data, however, on the interaction of BMI with the percent changes of circulating estradiol in women on HT is sparse. Gavaler et al. (4) aiming to evaluate factors that may influence estradiol levels in postmenopausal women under HT, demonstrated that only 51.1% of women under oral HT achieved estradiol levels of at least 45 pg/ml, which was characterized as therapeutic. The odds of being an achiever decreased significantly with increasing BMI. A similar study was performed by Yasui et al. (20), who evaluated 84 postmenopausal and 50 bilaterally ovariectomized women, treated with mg oral conjugated equine estrogen and 2.5 mg medroxyprogesterone acetate daily and every other day. While BMI had no effect on the low-dose regimen, total estradiol and estrone levels were higher in obese women compared to the lean group taking the standard dose regimen. Additionally, Tworoger et al. (11), examining the association between circulating hormone levels and breast cancer risk, reported among their other findings the presence of a positive association between BMI and absolute final levels of free estradiol, and total estradiol as well as an inverse association between BMI and absolute final levels of SHBG, in users of conjugated equine estrogens only or plus progestin. The results of these two studies, however, are not directly comparable to ours, since the authors are addressing total estradiol concentration, and not percent increase from baseline in FEI. Furthermore the evaluated regimen, conjugated equine estrogens, may differ in pharmaco dynamics and pharmacokinetics compared to the 17β-estradiol used in our study. Karim et al. (21) evaluating the impact of obesity on estrogen levels, in postmenopausal women receiving oral low-dose 17β-estradiol, reported that free and total estradiol associated significantly with BMI; percent changes in free steroids, however, were not assessed between lean and overweight individuals. On the contrary, the recent Norwegian Women and Cancer study (10) revealed no association between endogenous hormone levels with BMI in postmenopausal women under HT. The study was characterized by a lack in homogeneity regarding the types of HT that were used. The utilized preparations consisted of oral combined HT, oral E2-only treatment, E2-only patches, as well as progestin-only treatment. After adjustment for estrogen dosage and age, there was no significant association of BMI with any of the evaluated sex steroids. Similarly to the previously mentioned studies, the Norwegian Women and Cancer study (10) targeted only the final post-ht absolute hormone levels, while percent changes from baseline in free steroid concentrations were not assessed. The mechanisms responsible for the HT-BMI interaction on circulating sex hormone levels have not been determined yet. The individual response in ET/HT has been associated with 990 VOLUME 19 NUMBER 5 May

4 Table 2 Mean hormone levels at baseline and at 6 months of low-dose oral HT in lean (n = 18) and overweight (n = 18) postmenopausal women Hormones Baseline mean ± s.d. (range) 6 Months mean ± s.d. (range) Δ% (95% CI) P FSH (miu/ml) Lean 82.3 ± 26.7 ( ) 45.0 ± 17.0 ( ) 45.9% ( 56.8 to 35.1) Overweight 85.5 ± 22.1 ( ) 52.3 ± 23.8 ( ) 43.0% ( 59.6 to 26.5) Δ% Lean vs. overweight Estradiol (pg/ml) Lean ± (5 43) ± (10 114) 194.4% (58.0 to 330.8) Overweight ± (2 47) ± (20 250) 437.4% ( to ) Δ% Lean vs. overweight Testosterone (ng/ml) Lean 0.37 ± 0.13 ( ) 0.31 ± 0.19 ( ) 1.0% ( 34.5 to 36.6) Overweight 0.31 ± 0.11 ( ) 0.35 ± 0.20 ( ) 5.6% ( 42.9 to 54.2) Δ% Lean vs. overweight Δ4A (ng/dl) Lean ± 35.2 ( ) ± 24.8 (69 165) 617.7% ( to ) Overweight 96.8 ± 27.0 (1 288) 93.7 ± 38.3 (58 375) % ( to 859.0) Δ% Lean vs. overweight DHEAS (µg/dl) Lean ± ( ) ± ( ) 15.6% ( 49.2 to 17.9) Overweight ± ( ) ± ( ) 21.4% ( 80.9 to 123.8) Δ% Lean vs. overweight SHBG (nmol/l) Lean ± (30 180) ± (44 158) 7.7% ( 49.5 to 34.1) Overweight ± (17 108) 52.8 ± ( ) 29.7% ( 12.0 to 71.5) Δ% Lean vs. overweight FAI Lean 1.94 ± 1.38 ( ) 1.53 ± 1.09 ( ) 30.7% ( 30.0 to 91.5) Overweight 2.55 ± 1.75 ( ) 2.75 ± 2.33 ( ) 13.6% ( 46.5 to 19.2) Δ% Lean vs. overweight FEI Lean 0.14 ± 0.09 ( ) 0.29 ± 0.14 ( ) 287.1% ( 67.1 to 641.5) Overweight 0.23 ± 0.18 ( ) 0.52 ± 0.40 ( ) 110.3% (14.1 to 206.5) Δ% Lean vs. overweight CI, confidence interval; DHEAS, dehydroepiandrosterone sulfate; FAI, free androgen index; FEI, free estrogen index; FSH, follicle-stimulating hormone; HT, hormone therapy; SHBG, sex hormone-binding globulin. Boldface indicates statistical significance (P < 0.05). differences in estrogen s oxidative metabolism (22). According to recent evidence in ERα-deficient mice, estrogen s metabolic pathways may be altered by an impaired oxidative metabolism, which is associated with obesity-related insulin resistance (23). Furthermore, the observed difference in the pharmaco kinetics of HT in lean and overweight individuals might be due to plasma volume expansion related to obesity (24). It is known that intravascular volume is increased in overweight subjects (25,26). Plasma volume expansion could lead to a plasmatic drop of serum levels of several markers, a phenomenon known as hemodilution. Recent studies report that lower prostatespecific antigen levels are associated with an increase in BMI, hypothesizing that hemodilution might be responsible for this phenomenon (27,28). According to this hypothesis, the same estradiol dose may produce a lesser percent increase in an individual with larger plasma volume. Serum levels of SHBG during the menopause are dependent on the route of estrogen treatment and on the type and dose of progestin. The effect of the low-dose E2/NETA regimen, regarding circulating SHBG, has not been extensively investigated yet. One study (29) evaluated alterations in serum levels of insulin-like growth factor 1, insulin-like growth factor obesity VOLUME 19 NUMBER 5 May

5 Levels of free estrogen index according to BMI 0.29 ± ± 0.40 absolute post-treatment hormone levels. This study suggests that although absolute FEI is higher in heavier women on HT, percent changes from baseline values are higher in lean women on HT. These preliminary findings need to be confirmed by larger prospective studies ± 0.09 Lean 0.23 ± 0.13 Overweight Baseline 6 Months Disclosure The authors declared no conflict of interest. Acknowledgments The authors wish to thank Dr. Rebecca Troisi for her fruitful suggestions on the interpretation of our data The Obesity Society Figure 1 Mean levels of free estrogen index before and after 6 months of oral low-dose hormone therapy in lean and overweight postmenopausal women. binding proteins and SHBG, after treatment with different HT regimens. The study reported minor nonsignificant changes in circulating SHBG after 6 months of treatment with continuous combined oral estrogens plus androgenic progestins at low doses. On the contrary in another report, women under treatment with oral E2/NETA exhibited increased concentrations of SHBG (30). In the present study, the subjects exhibited minor, nonsignificant alterations in circulating SHBG. Treatment with higher doses of NETA is associated with significant decreases in SHBG levels in postmenopausal women, possibly due to the androgenic properties of NETA (31). The androgenicity of NETA might counteract the stimulatory effect of estrogen on SHBG production. As we described in an earlier study (32), postmenopausal women receiving 2 mg 17β-estradiol/1 mg norethisterone acetate had levels of SHBG and FAI similar to women not on HT. Our study bears certain limitations. The sample size was small and the compliance was ensured by monthly telephone calls and not by visits in the clinic. In addition, we measured only estradiol and not estrone (E1) concentrations, which may be a better biomarker of estrogen synthesis and action in postmenopausal women, although concentrations of estrone and endogenous estradiol are highly correlated with each other (33). Furthermore, the large coefficient of variation of the assays for DHEA-SO 4 and SHBG might have influenced our results. SHBG changes might have affected the differences in changes of FEI and FAI between the two groups to some extent. However, the change of SHBG was small and nonsignificant in both groups, while a larger statistical analysis including percent changes of FAI, FEI and SHBG between the two groups could not be performed due to the small sample size. In addition, it was not possible to measure norethisterone levels, which may also have been different between lean and overweight individuals. Finally, the use of FEI is not the most accurate way to assess true free estradiol levels; however, it allows the evaluation of relative levels of free estradiol in postmenopausal women (14). The interaction between BMI and sex hormone levels in HT users has been examined by various studies until know, but the majority of them aimed to identify a correlation of BMI with REFERENCES 1. Burger HG, Dudley EC, Cui J, Dennerstein L, Hopper JL. A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopause transition. J Clin Endocrinol Metab 2000;85: Al-Azzawi F, Palacios S. Hormonal changes during menopause. Maturitas 2009;63: Canderelli R, Leccesse LA, Miller NL, Unruh Davidson J. Benefits of hormone replacement therapy in postmenopausal women. J Am Acad Nurse Pract 2007;19: Gavaler JS. 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6 20. Yasui T, Uemura H, Umino Y et al. Serum estrogen level after hormone replacement therapy and body mass index in postmenopausal and bilaterally ovariectomized women. Maturitas 2005;50: Karim R, Mack WJ, Hodis HN, Roy S, Stanczyk FZ. Influence of age and obesity on serum estradiol, estrone, and sex hormone-binding globulin concentrations following oral estrogen administration in postmenopausal women. J Clin Endocrinol Metab 2009;94: Armamento-Villareal RC, Napoli N, Klug T, Civitelli R. The oxidative metabolism of estrogen modulates response to ERT/HRT in postmenopausal women. Bone 2004;35: Ribas V, Nguyen MTA, Henstridge DC et al. Impaired oxidative metabolism and inflammation are associated with insulin resistance in ERα-deficient mice. Am J Physiol Endocrinol Metab 2010;298:E304 E Salpeter SR, Walsh JM, Ormiston TM et al. Meta-analysis: Effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes Metab 2006;8: Redon J. Hypertension in obesity. Nutr Metab Cardiovasc Dis 2001;11: Messerli FH, Christie B, DeCarvalho JG et al. Obesity and essential hypertension. Hemodynamics, intravascular volume, sodium excretion, and plasma renin activity. Arch Intern Med 1981;141: Fowke JH, Matthews CE. PSA and body composition by dual X-ray absorptiometry (DXA) in NHANES. Prostate 2010;70: Banez LL, Hamilton RJ, Partin AW et al. Obesity related plasma hemodilution and PSA concentration among men with prostate cancer. JAMA 2007;298: Biglia N, Ambroggio S, Ponzone R et al. Modification of serum IGF-I, IGFBPs and SHBG levels by different HRT regimens. Maturitas 2003;45: Dören M, Rübig A, Coelingh Bennink HJ, Holzgreve W. Differential effects on the androgen status of postmenopausal women treated with tibolone and continuous combined estradiol and norethindrone acetate replacement therapy. Fertil Steril 2001;75: Onobrakpeya OA, Fall PM, Willard A et al. Effect of norethindrone acetate on hormone levels and markers of bone turnover in estrogen-treated postmenopausal women. Endocr Res 2001;27: Christodoulakos G, Lambrinoudaki I, Panoulis C et al. Serum androgen levels and insulin resistance in postmenopausal women: Association with hormone therapy, tibolone and raloxifene. Maturitas 2005;50: Schairer C, Hill D, Sturgeon SR et al. Serum concentrations of estrogens, sex hormone-binding globulin, and androgens and risk of breast hyperplasia in postmenopausal women. Cancer Epidemiol Biomarkers Prev 2005;14: obesity VOLUME 19 NUMBER 5 May

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