Raloxifene: A Selective Estrogen Receptor Modulator (SERM) with Multiple Target System Effects
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1 The Oncologist N ews B ulletin NCI All Ireland Cancer Conference Raloxifene: A Selective Estrogen Receptor Modulator (SERM) with Multiple Target System Effects DOUGLAS B. MUCHMORE Lilly Research Laboratories, Indianapolis, Indiana, USA ABSTRACT Key Words. Raloxifene Selective estrogen receptor modulators Osteoporosis Cholesterol Uterus Estrogen Tamoxifen Selective estrogen receptor modulators (SERMs) exhibit a pharmacologic profile characterized by estrogen agonist activity in some tissues with estrogen antagonist activity in other tissues. These compounds were initially called antiestrogens, but it was subsequently recognized that this inadequately described their spectrum of activities. The first widely used SERM, tamoxifen, has estrogen antagonist activity in breast tissue but shows estrogen-like activity in other tissues. Raloxifene INTRODUCTION By definition, selective estrogen receptor modulators (SERMs) exert estrogen agonist action in some target tissues while acting as estrogen antagonists in others. Some members of the SERM class were initially called antiestrogens because of their high-affinity binding to estrogen receptors (ERs) and ability to counteract estrogen action. However, this nomenclature has proved inadequate to fully describe the actions of these agents. Thus, tamoxifen, which was introduced into clinical use on the basis of its now well-recognized estrogen antagonist activity in the breast, has demonstrated activity consistent with estrogen agonism in bone [1], lipids [2], and partial agonism in the uterus [3]. Such estrogen agonism in the uterus may be responsible for the increase in uterine cancer observed with prolonged tamoxifen use [4], and has led to the search for other SERMs with different pharmacologic profiles. Clinically available SERMs fall into two chemical classes: triphenylethylenes and benzothiophenes. Tamoxifen, is another SERM in clinical use, and it was developed to avoid some of the undesirable estrogen agonist actions of other SERMs to improve the drug safety profile. Raloxifene has been introduced for clinical use in treatment and prevention of postmenopausal osteoporosis. This review will explore the preclinical and clinical pharmacology of raloxifene, and compare it to other SERMs currently available for clinical use. The Oncologist 2000;5: a triphenylethylene, is indicated for treatment of breast cancer and risk reduction in women at high risk for breast cancer. Other triphenylethylene SERMs in clinical use include clomiphene (used to induce ovulation) and toremifene (used for breast cancer treatment). Raloxifene, a benzothiophene, was developed specifically to avoid the uterotrophic effects of other SERMs. Raloxifene has been approved for the treatment and prevention of postmenopausal osteoporosis and is currently under study for other potential indications. This review will compare raloxifene s preclinical pharmacology and clinical profile to those of the other clinically available SERMs. SERM MECHANISM OF ACTION Although the mechanism by which SERMs exhibit their complex profiles is not completely understood, characterization of the x-ray crystallographic structure of the ER, when bound to raloxifene, provided insight into this receptor/ligand interaction [5]. While raloxifene binds to the receptor in the Correspondence: Douglas B Muchmore, M.D., Eli Lilly and Company, Lilly Corporate Center, Indianapolis, Indiana 46285, USA. Telephone: ; Fax: ; Dmuch@lilly.com Received March 22, 2000; accepted for publication April 27, AlphaMed Press /2000/$5.00/0 The Oncologist 2000;5:
2 389 Raloxifene: A SERM with Multiple Target System Effects same ligand-binding pocket as estradiol, it causes the C-terminal alpha helix of the receptor to change its conformation such that it blocks access to the activation function-2 region of the receptor. This, in turn, likely blocks access to transcriptional coactivators necessary to facilitate the turn-on of estrogen-responsive genes. Such conformational changes may explain the estrogen antagonist activities of raloxifene (e.g., in the uterus), and why structurally different SERMs may have differing effects in the same tissues. The estrogen agonist actions of raloxifene are less well characterized at a molecular level, but likely depend on raloxifene-bound ERs interacting with nontraditional estrogen response elements at different sets of gene targets [6]. SERM EFFECTS ON BONE Raloxifene has been extensively studied and data support an estrogen agonist profile in the skeletal system. In the ovariectomized rat model, raloxifene acts as an antiresorptive, with preservation of both bone mineral density and bone strength identical in magnitude to that seen with ethinyl estradiol. Table 1 shows results from the large Multiple Outcomes of Raloxifene Evaluation (MORE) trial conducted in postmenopausal women with osteoporosis. In this trial, raloxifene increased bone mineral density by 2%-3% and reduced the incidence of new vertebral fractures by 30% and 50% (in women with and without prevalent vertebral fractures, respectively) compared to placebo [7]. While tamoxifen also increases bone density in postmenopausal women [1], its effects on osteoporotic fracture are limited to secondary endpoint data from the large U.S. Breast Cancer Prevention Trial (BCPT), which showed trends toward reduction in vertebral fracture rates in the treated versus control subjects [4]. Toremifene did not increase bone density in a very small study of postmenopausal breast cancer patients [8], but this result may reflect lack of statistical power rather than underlying pharmacology. SERM EFFECTS ON THE CARDIOVASCULAR SYSTEM Another major target system for the estrogen agonist activities of SERMs is the cardiovascular system. Raloxifene has demonstrated estrogen agonist activities in both lipid and nonlipid animal model systems [9]. For example, in an ovariectomized rat model system, raloxifene had effects equal to ethinyl estradiol in reducing serum cholesterol to levels observed in sham-operated control animals [10]. In human studies, raloxifene [11], tamoxifen [12], and toremifene [13] have demonstrated decreases in total and low density lipoprotein-cholesterol in postmenopausal women. In contrast to some estrogen therapy regimens that increase high density lipoprotein-cholesterol (HDL-C) and triglycerides, raloxifene, and tamoxifen did not significantly change HDL-C or triglycerides [11, 12]. Toremifene increased HDL-C and decreased triglycerides in postmenopausal breast cancer patients [13]. After six months of treatment, raloxifene significantly decreased serum homocysteine levels similarly to HRT, but, unlike HRT, did not increase C-reactive protein levels, both recognized as important nonlipid risk factors for atherosclerosis [14]. Although encouraging, these modifications in surrogate endpoints do not substitute for clinical outcomes such as effect on coronary death and nonfatal myocardial infarction. However, this question is the subject of the Raloxifene Use for the Heart (RUTH) clinical trial, now enrolling 10,000 postmenopausal women. It will compare raloxifene to placebo for rates of myocardial infarction and cardiac sudden death in postmenopausal women at high risk for cardiovascular disease. The study will assess both primary and secondary prevention of coronary events [9]. Specific, large cardiovascular outcomes studies have not been reported for tamoxifen. Results from the BCPT failed to suggest a benefit for tamoxifen in either stroke or myocardial infarction; however, the study group was generally at low risk for these outcomes, and thus the event rates were very low [4]. Studies in breast cancer patients have suggested possible benefits of tamoxifen on cardiac death in postmenopausal women [15], but the death rate from cancer was very high in some of these studies. The cardioprotective potential of this agent also remains unproven. Table 1. Effects of raloxifene on incidence of new vertebral fracture and invasive breast cancer in women with osteoporosis [7] Placebo Raloxifene 60 mg/d Raloxifene 120 mg/d Fracture incidence n of evaluable women/group 2,292 2,259 2,277 Total n (%) of women with 1 new vertebral fracture 231 (10.1) 148 (6.6) 124 (5.4) Placebo Raloxifene (Pooled doses) Breast cancer incidence n of women at risk/group 2,576 5,129 Total n (%) of women with incident invasive breast cancer 27 (1.0) 13 (0.25)
3 Muchmore 390 SERM EFFECTS ON THE UTERUS SERMs also have differing effects on the female genital tract. Raloxifene acts as a complete estrogen antagonist in its effects on uterine wet weight in estrogen replete ovariectomized rats [16]. In human studies, raloxifene does not cause any increase in vaginal bleeding [17] nor does it significantly increase endometrial thickness as assessed by transvaginal ultrasonography [18]. In contrast, triphenylethylene SERMs act as partial estrogen agonists in estrogen replete ovariectomized rats, and toremifene and tamoxifen increase endometrial thickness and uterine volume [3], while raloxifene does not [19]. Importantly, tamoxifen is known to increase the risk of endometrial cancer in postmenopausal women [4] while raloxifene has not shown this effect [17]. SERM EFFECTS ON THE BREAST In an in vitro model of breast cancer, raloxifene is devoid of estrogenic activity in MCF-7 cells that are grown in estrogen-free, serum-free media, in contrast to the agonist effects of tamoxifen observed in this system [20]. Tamoxifen has been extensively studied for treatment of both early stage and advanced breast cancer, and evaluation of these data is beyond the scope of this review. Observations regarding reduction in the incidence of contralateral breast cancer in tamoxifen-treated breast cancer patients [21] led to formal tests of the ability of tamoxifen to reduce the incidence of breast cancer in high-risk women, including both pre- and postmenopausal women. The results of the U.S. BCPT showed an approximate 50% reduction in new invasive breast cancers in tamoxifen-treated subjects compared to controls [4]. These results were discordant with those reported by two separate European trials [22, 23], but significant study design differences may account for these differences. Breast cancer incidence was a planned secondary endpoint in the large raloxifene osteoporosis treatment (MORE) trial [17]. To be eligible for the MORE trial, patients must have had normal baseline (within one year of subject randomization) breast imaging results. Mammograms were repeated at 12 months (optional), and at 24 and 36 months (both required) after randomization. Patients were randomly assigned to receive raloxifene 60 mg/d, raloxifene 120 mg/d, or placebo. All reported breast cancers were confirmed by pathology report, and, whenever possible, by central pathologic review. After 40 months of median follow-up, a total of 40 invasive breast cancers were observed: 27 invasive breast cancers were observed among the one-third of subjects randomized to placebo and 13 cases among the two-thirds of subjects randomized to raloxifene, resulting in an overall relative risk for newly diagnosed invasive breast cancer of 0.24 on raloxifene versus placebo (Table 1) [17]. The observed rate of invasive breast cancer was 0.9/1,000 patient-years in the combined raloxifene groups and 3.6/1,000 patient-years in the placebo group. There was no dose effect seen between the two doses of raloxifene, and time-to-event plotting demonstrated a treatment effect after the first year of observation. Whenever possible, analysis of the cancers by ER status was performed. Of the 24 ER-positive cases, 20 were on placebo and four on raloxifene (relative risk = 0.10 for raloxifene versus placebo). Breast cancer incidence results of the BCPT and the MORE trials cannot be directly compared because of substantial differences in the study populations (i.e., pre- and postmenopausal women at high risk for breast cancer versus postmenopausal women with osteoporosis). However, the consistency of the results strongly supports the hypothesis that these SERMs reduce the incidence of breast cancer in a targeted population of women. Recent modeling results suggest that the duration of the BCPT (i.e., ~4 years) was sufficient for expression of a true prevention effect [24] rather than simply an early treatment effect, although this is a matter of dispute. Longer-term studies will be required to verify these modeling results. Another similarity between the BCPT and MORE trial results is the restriction of the therapy benefit to subjects with ER-positive tumors: tamoxifen demonstrated an 80% reduction in ER-positive invasive cancers (BCPT), while raloxifene demonstrated a 90% reduction in ER-positive invasive cancers (MORE). In neither of these studies did active therapy result in a reduction or increase in ER-negative tumors compared with placebo. SAFETY OF SERMS SERMs have many potential uses, and are currently approved for use by women with breast cancer (tamoxifen, toremifene), at risk for breast cancer (tamoxifen), and also postmenopausal women with or at risk for osteoporosis (raloxifene). The safety profile of these agents is thus of great interest. Like hormone replacement therapy [25], both tamoxifen [4] and raloxifene [17] are associated with a twoto threefold increase in venous thromboembolic events. Lesser adverse events that are causally related to these drugs include leg cramps [4, 17, 26] and an increase in reports of hot flashes [4, 17]. Tamoxifen is associated with a fourfold increase in endometrial carcinoma in women over age 50, although this risk was not observed in younger women nor was it seen with raloxifene [4, 17]. NEW STUDIES OF BREAST CANCER INCIDENCE Additional large scale, long-term studies are under way to further clarify the effects of SERMs on breast cancer incidence (Table 2). The Study of Tamoxifen and Raloxifene (STAR) is a two-arm, active comparator trial in postmenopausal women at high risk for breast cancer.
4 391 Raloxifene: A SERM with Multiple Target System Effects Table 2. Long-term raloxifene trials Study Approximate n of subjects Planned duration Endpoints Status STAR 22, years Invasive breast cancer Enrolling MORE 7, years Bone density, fractures, breast cancer, others Completed CORE 3, years Invasive breast cancer Enrolling (8 year total) RUTH 10, years Coronary death, myocardial infarction, breast cancer, venous thromboembolism Enrolling Its outcome will be one of the following: A) raloxifene is superior to tamoxifen; B) tamoxifen is superior to raloxifene, or C) the two drugs are equivalent in their effects on breast cancer incidence. Secondary endpoints include safety outcomes, including incidence of endometrial cancer and venous thromboembolic events. Enrollment in this large (22,000 subject) trial began in July, Planned duration of the STAR trial is five years, subject to periodic review by a Data Safety Monitoring Board. As noted above, it is generally accepted that longerterm study will be needed to conclude that SERMs may prevent breast cancer. The BCPT cohort will be followed though seven years post randomization, although therapy will be stopped per protocol after five years. A number of the BCPT placebo subjects will be enrolling in the STAR trial, and it is thus uncertain to what extent follow-up beyond the previously report 4+ years will be available for tamoxifen effects of breast cancer incidence. To assess the long-term effects of raloxifene, another study is currently enrolling. This study, called the Continuing Outcomes Relevant to Evista (CORE), will enroll as many MORE participants as possible, with the plan to continue randomized, placebo-controlled follow-up through a total of eight years. In contrast to the MORE osteoporosis trial, the REFERENCES 1 Powles TJ, Hickish T, Kanis JA et al. Effect of tamoxifen on bone mineral density measured by dual-energy x-ray absorptiometry in healthy premenopausal and postmenopausal women. J Clin Oncol 1996;14: Decensi A, Bonanni B, Guerrieri-Gonzaga A et al. Biologic activity of tamoxifen at low doses in healthy women. J Natl Cancer Inst 1998;90: Tomas E, Kauppila A, Blanco G et al. Comparison between the effects of tamoxifen and toremifene on the uterus in postmenopausal breast cancer patients. Gynecol Oncol 1995;59: Fisher B, Costantino JP, Wickerham DL et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 1998;90: primary endpoint of the CORE trial will be incidence of invasive breast cancer. The ongoing cardiovascular outcomes study, RUTH, is studying the effects of raloxifene in 10,000 women with or at high risk for cardiovascular disease. Breast cancer is a secondary endpoint of the trial. SUMMARY AND CONCLUSIONS SERMs are pharmacologic agents which have demonstrated utility in several target organ systems. Current labeling indications for SERMs include use in breast (tamoxifen, toremifene) and bone (raloxifene). In clinical trials, tamoxifen and raloxifene have significantly reduced the incidence of breast cancer in selected populations, and raloxifene prevents bone loss and reduces fracture risk. Unlike tamoxifen, however, raloxifene does not stimulate the uterus or increase the risk of endometrial carcinoma. Additional large, long-term studies of raloxifene are under way to further confirm the reported current breast cancer incidence observations. ACKNOWLEDGMENT D. M. is an employee and shareholder in Eli Lilly & Co., the manufacturer of raloxifene. 5 Brzozowski AM, Pike AC, Dauter Z et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997;389: Yang NN, Venugopalan M, Hardikar S et al. Identification of an estrogen response element activated by 17beta-estradiol and raloxifene. Science 1996;273: Ettinger B, Black DM, Mitlak BH et al. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. JAMA 1999;282: Marttunen MB, Hietanen P, Tiitinen A et al. Comparison of effects of tamoxifen and toremifene on bone biochemistry and bone mineral density in postmenopausal breast cancer patients. J Clin Endocrinol Metab 1998;83:
5 Muchmore Barrett-Connor E, Wenger NK, Grady D et al. Hormone and nonhormone therapy for the maintenance of postmenopausal health: the need for randomized controlled trials of estrogen and raloxifene. J Womens Health 1998;7: Kauffman RF, Bensch WR, Roudebush RE et al. Hypocholesterolemic activity of raloxifene (LY139481): pharmacological characterization as a selective estrogen receptor modulator. J Pharmacol Exp Ther 1997;280: Walsh BW, Kuller LH, Wild RA et al. Effects of raloxifene on serum lipids and coagulation factors in healthy postmenopausal women. JAMA 1998;279: Love RR, Newcomb PA, Wiebe DA et al. Effects of tamoxifen therapy on lipid and lipoprotein levels in postmenopausal patients with node-negative breast cancer. J Natl Cancer Inst 1990;82: Saarto T, Blomqvist C, Ehnholm C et al. Antiatherogenic effects of adjuvant antiestrogens: a randomized trial comparing the effects of tamoxifen and toremifene on plasma lipid levels in postmenopausal women with node-positive breast cancer. J Clin Oncol 1996;14: Paul S, Dean RA, Tracy RP et al. Effects of raloxifene and hormone replacement therapy on homocysteine and C-reactive protein levels in postmenopausal women. Circulation 1998;98:(suppl): Costantino JP, Kuller LH, Ives DG et al. Coronary heart disease mortality and adjuvant tamoxifen therapy. J Natl Cancer Inst 1997;89: Bryant HU, Wilson PK, Adrian MD et al. Selective estrogen receptor modulators: pharmacological profile in the rat uterus. J Soc Gynecol Invest 1996;3:152a. 17 Cummings S, Eckert S, Krueger K et al. The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. JAMA 1999;281: Cohen FJ, Watts S, Shah A et al. Uterine effects of three-year raloxifene therapy in postmenopausal women younger than age 60. Obstet Gynecol 2000;95: Goldstein SR, Scheele WH, Rajagopalan SK et al. A 12-month comparative study of raloxifene, estrogen, and placebo on the postmenopausal endometrium. Obstet Gynecol 2000;95: Sato M, Glasebrook AL, Bryant HU. Raloxifene: a selective estrogen receptor modulator. J Bone Miner Metab 1994;12:S9-S Fisher B, Dignam JJ, Bryant J et al. Five versus more than five years of tamoxifen therapy for breast cancer patients with negative lymph nodes and estrogen receptor-positive tumors. J Natl Cancer Inst 1996;88: Powles T, Eeles R, Ashley S et al. Interim analysis of the incidence of breast cancer in the Royal Marsden Hospital tamoxifen randomised chemoprevention trial. Lancet 1998;352: Veronesi U, Maisonneuve P, Costa A et al. Prevention of breast cancer with tamoxifen: preliminary findings from the Italian randomised trial among hysterectomised women. Italian Tamoxifen Prevention Study. Lancet 1998;352: Radmacher MD, Simon R. Estimation of tamoxifen's efficacy for preventing the formation and growth of breast tumors. J Natl Cancer Inst 2000;92: Hulley S, Grady D, Bush T et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA 1998;280: Davies GC, Huster WJ, Lu Y. The side effect profile in post menopausal women treated with raloxifene, HRT, estrogen (ERT) or placebo. IV European Congress on Menopause Abstract Book, 8-12 October Paris, FR: Editions ESKA, 1999:68. Countryside Village, Northern Ireland Davi Ellen Chabner
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