Serono Inc., Rockland, Massachusetts, and Serono International, Geneva, Switzerland
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1 FERTILITY AND STERILITY VOL. 82, NO. 6, DECEMBER 2004 Copyright 2004 American Society for Reproductive Medicine Published by Elsevier Inc. Printed on acid-free paper in U.S.A. A phase I study of the pharmacokinetics, pharmacodynamics, and safety of singleand multiple-dose anastrozole in healthy, premenopausal female volunteers Donald R. Tredway, M.D., a Mauro Buraglio, M.D., b George Hemsey, M.B.A., a and Geoff Denton, B.S. b Serono Inc., Rockland, Massachusetts, and Serono International, Geneva, Switzerland Objective: To evaluate the pharmacokinetic, pharmacodynamic, and safety profiles of the aromatase inhibitor anastrozole in healthy, premenopausal women. Design: Phase I, single-center study. Setting: Infertility clinic. Patient(s): Twenty-six women with regular ovulatory cycles: 20 received either a single dose of 5 mg, 10 mg, 15 mg, or 20 mg anastrozole, or remained untreated; 6 received five daily doses of 10 mg or 15 mg anastrozole. Intervention(s): Anastrozole was administered on cycle day 2 for the single-dose groups and on days 2 6 for the multiple-dose groups. Ultrasound follicular development and endometrial biopsies were performed. Safety was determined from adverse event reports and laboratory parameters. Main Outcome Measure(s): Pharmacokinetics, pharmacodynamics, and safety. Result(s): The pharmacokinetics of anastrozole were linear, predictable, and consistent with previously published data in healthy volunteers. In the single-dose groups, E 2 levels reached their nadir 3 6 hours after administration, decreasing by an average of 39% from baseline. Follicle-stimulating hormone levels rose by 13%, 52%, 49%, and 75% in the 5-mg, 10-mg, 15-mg, and 20-mg groups, respectively, at approximately 24 hours after dosing. Most subjects recruited just one mature follicle, with no apparent effect on endometrial maturation. No safety concerns were noted. Conclusion(s): Anastrozole was well tolerated and suppressed E 2 levels, with a resultant increase in FSH. (Fertil Steril 2004;82: by American Society for Reproductive Medicine.) Key Words: Aromatase inhibitors, anastrozole, ovulation, infertility Received December 18, 2003; revised and accepted April 22, Reprint requests: Donald R. Tredway, M.D., Serono Inc., 1 Technology Place, Rockland, MA (FAX: (781) ; donald.tredway@serono. com). a Reproductive Health and Global Product Development Unit, Serono Inc., Rockland, Massachusetts. b Human Pharmacology Group, Serono International, Geneva, Switzerland /04/$30.00 doi: /j.fertnstert Anovulation is thought to be the cause of up to 20% of human infertility (1). The causes of anovulation fall into three main categories (1, 2), of which World Health Organization classification group II (hypothalamic pituitary failure) is the largest. First-line fertility treatment in World Health Organization group II anovulatory women typically involves an antiestrogen agent, such as clomiphene citrate (CC). This is because increasing estrogen (E) levels during the follicular phase of the menstrual cycle negatively regulates the production of FSH. Thus, use of an E antagonist should result in increased levels of FSH. Although ovulation is restored in approximately 72% of CC-treated patients, only approximately 35% of CC treatments result in pregnancy (3). This difference between ovulation and pregnancy rates is thought to be due to antiestrogen side effects of CC, including reduced endometrial development (believed to be due to depletion of endometrial E receptors [4]) and vaginal dryness (due to changes in cervical mucus). Furthermore, CC has a long half-life (several weeks [5]) and is associated with an increased incidence of ovarian cysts and multiple pregnancies (6). Clomiphene citrate might also decrease uterine blood flow during the early luteal and peri-implantation stages (5). Recently, inhibitors of aromatase, the key enzyme responsible for the production of E, have been used to stimulate ovarian follicles in 1587
2 CC-resistant patients (4). This novel approach seeks to mimic the effects of CC by releasing the hypothalamic pituitary axis from the negative feedback effects of E, without the adverse effects of E receptor depletion and impaired endometrial development. Third-generation nonsteroidal aromatase inhibitors, such as anastrozole (Arimidex; AstraZeneca, Waltham, MA) and letrozole (Femara; Novartis, East Hanover, NJ), have a short circulating half-life (approximately 40 hours), are well tolerated, relatively inexpensive, and can be administered orally (5). Anastrozole at a dose of 1 mg/day inhibits E levels by 97% but has no effect on E receptors or antiestrogenic side effects (5). Studies in animals have provided several lines of evidence to support the use of aromatase inhibitors for ovulation induction in anovulatory women. Primates treated with an aromatase inhibitor have been found to have decreased levels of serum E and increased levels of serum androstenedione, with no effect on either the number of follicles developed or their size (7, 8). Furthermore, treatment during the follicular phase resulted in the development of multiple mature follicles, which could be induced to ovulate with hcg (8). On the basis of these investigations, Shetty et al. (8) proposed that letrozole used clinically in the treatment of breast cancer could be used to obtain multiple follicles for IVF. In addition, studies in mice have shown that anastrozole does not damage chromosome spindle formation and, once fertilized, preimplantation embryo development was not different from the control (9). Also, animal toxicology studies indicate that anastrozole, in contrast to letrozole and CC, is nonteratogenic (10). Preliminary clinical studies of aromatase inhibitors for ovulation induction suggest that they might offer an effective and well-tolerated alternative to CC (4, 11), as well as a superior uterine environment for implantation over CC (12). In addition, local accumulation of androgens in the ovary is believed to increase follicular sensitivity to FSH (4). Anastrozole, which is a potent and highly selective nonsteroidal aromatase inhibitor, is currently used at a dose of 1 mg/day in the treatment of advanced breast cancer in postmenopausal women. This study was performed to evaluate the safety, pharmacokinetics, and pharmacodynamics of higher-dose anastrozole when administered in single- and multiple-dose regimens to healthy, premenopausal female volunteers. MATERIALS AND METHODS This was a phase I, single-center study of the effects of single and multiple doses of anastrozole in premenopausal women, conducted between December 12, 2001 and July 8, The trial was open-label, with the exception of the ultrasound operatives. This study was approved by the institutional review board at the LCG Laboratories Clinics Group Bioscience, Bourn Hall Clinic at Bourn, Cambridge, United Kingdom. The study was supported by Serono Inc. (Rockland, MA), and the authors are employees of Serono. The study sample size was not based on statistical considerations but was considered adequate to allow estimation of the pharmacokinetic/pharmacodynamic profile and confirmation of the published profile for anastrozole in postmenopausal women (13, 14). All subjects were healthy, premenopausal women (aged years, inclusive) with regular ovulatory cycles (25 35 days), a body mass index 30 kg/m 2, both ovaries present, normal vital signs, normal cervical cytology, and who were to use barrier contraception during the study period. Exclusion criteria included clinically significant systemic disease; known infection with HIV or hepatitis B or C viruses; a positive result for recreational drug use (including alcohol); clinically significant abnormal laboratory results; and any medical condition that might interfere with the absorption, distribution, metabolism, or excretion of the study drug. In addition, the use of androgens, danazol, progesterone (P), a gonadotropin-releasing hormone agonist, or oral contraceptives during or within 3 months of study entry; intrauterine contraceptive device; and parenteral depot contraception in the previous 6 months were criteria for exclusion. Any volunteers with abnormal, undiagnosed gynecologic bleeding and known current substance abuse, including an average use of 5 cigarettes per day, were denied study entry. Anastrozole (Arimidex) tablets for oral administration were used in this study. Each tablet contained 1 mg anastrozole, a nonsteroidal aromatase inhibitor, along with excipients. Oral treatment administration occurred on cycle day 2 for the single-dose groups and on cycle days 2 6 for the multiple-dose groups. All doses were given in the morning. Pharmacokinetic parameters were assessed by serial measurements of anastrozole plasma concentrations before dosing and at 0.5, 1, 1.5, 2, 3, 4, 6, 8, 12, 16, 24, and 48 hours after single, oral dosing. In the multiple-dose group, measurements were taken before dosing and at uniform daily intervals from 1 day after the initial daily dose until 2 days after the last dose. Anastrozole plasma concentration vs. time curves were produced to estimate the area under the curve AUC 0 last, AUC 0, maximum concentration (C max ), time of C max (t max ), and half-life (t 1/2 ). Pharmacodynamics were assessed from serial measurements of androstenedione, E 2, FSH, LH, and T before the study, before dosing, and at 3, 6, and 12 hours after dosing on days 3, 4, 6, 8, and 10 of the cycle, and then daily until ovulation was confirmed in the single-dose groups. In the multiple-dose groups, measurements were taken before the study, before dosing, daily from day 3 to day 8 of the cycle, and then daily from day 10 until ovulation. Progesterone and 17 -hydroxyprogesterone levels were monitored daily from 1588 Treadway et al. Anastrozole in premenopausal women Vol. 82, No. 6, December 2004
3 FIGURE 1 Anastrozole mean plasma concentration vs. time plot in healthy premenopausal women after a single oral dose (n 4 per group). (A) Normal scale; (B) semilog scale. Error bars have been omitted for clarity. day 10 until ovulation and at the midluteal stage. Ovulation was demonstrated by a midluteal (cycle days 18 35, depending on the cycle length) P level of 4 ng/ml. Ultrasound examination of the ovaries and uterus was performed before the study, before dosing, on days 6, 8, and 10 of the cycle, and then daily until ovulation, at the midluteal stage, and after the study in both groups. In addition, the multiple-dose groups were also examined on day 4. Response to anastrozole treatment was monitored by evaluating both ovaries, including the length in three planes, the number of follicles 11 mm present on the largest section through the ovary, the size of any follicles 11 mm, the number of mature follicles ( 14 mm), and the size of any ovarian cysts during the treatment cycle or subsequent cycle. The size of the uterus (length, height, and width), its appearance, and endometrial thickness (from endometrial biopsies) were also recorded. Ovulation, as demonstrated by a midluteal (days 21 23) P level of 4 ng/ml, was recorded as part of the screening process. Safety was determined through the monitoring of adverse events, vital signs, and routine blood analyses, as previously stated. Safety assessments included incidence and severity of adverse events and ovarian hyperstimulation syndrome related symptoms; tolerance of anastrozole administration; clinically significant changes in routine laboratory parameters; and changes in vital signs. Endometrial biopsies were performed during the luteal phase for evaluation of endometrial maturation and synchrony and the incidence and severity of ovarian cysts in subsequent menstrual cycles. RESULTS A total of 39 subjects were booked for prestudy screening. Of these, 26 were enrolled into the clinical phase. The distribution of ages, weights, and heights was similar between dose groups. The first 20 subjects were randomized to receive a single dose of 5 mg, 10 mg, 15 mg, or 20 mg anastrozole, or kept as untreated controls (4 in each group). Subjects and were assigned to receive five daily doses of 10 mg and 15 mg anastrozole, respectively. One subject withdrew from the study on the day of dosing but was monitored for safety. The prestudy screening values for the volunteers were obtained on days 2 4 of the previous menstrual cycle. These baseline values (mean SD) were as follows: FSH: IU/L; LH: IU/L; E 2 : pmol/l; P: nmol/l; androstendione: nmol/l; T: ng/dl. The pharmacokinetic profile of anastrozole was linear, predictable, and consistent with previously published data on healthy male and postmenopausal female volunteers (13), with relatively low intersubject variability. After single oral doses of 5 20 mg, anastrozole was well and rapidly absorbed, with C max achieved within 2 hours (Fig. 1). The sampling schedule of this study did not allow a complete assessment of t 1/2 and AUC 0. However, the interim parameters, AUC 0 last and C max, confirm the pharmacokinetic linearity for doses up to 20 mg. Furthermore, C min fluctuations after repeat doses in a volunteer subgroup (10 mg and 15 mg u.i.d. [once daily]) were consistent with the reported half-life of hours (Fig. 2) and not suggestive of unexpected accumulation. Suppression of E 2 levels was rapid in all anastrozoletreated patients, although there was a high level of interindividual variability. For the single-dose group, E 2 levels reached their nadir approximately 3 6 hours after administration and decreased by an average of 39% from baseline. Mean reductions of 21%, 46%, 55%, and 37% were seen in FERTILITY & STERILITY 1589
4 FIGURE 2 Dose-normalized C min plasma concentrations (red circles) vs. time profiles for anastrozole after multiple-dose (u.i.d) administration of 10 mg and 15 mg in healthy female subjects. (A) Normal scale; (B) semilog scale. Mean standard deviation (n 3 per group). the 5-mg, 10-mg, 15-mg, and 20-mg-dose groups, respectively (Fig. 3). Levels for the control group were essentially unchanged. Estradiol typically returned to pretreatment levels within 24 hours. The multiple-dose groups saw similar rapid declines, and the levels typically returned to baseline by day 2 and day 3 of treatment. Follicle-stimulating hormone levels also varied between subjects but rose in the anastrozole-treated patients, peaking approximately 24 hours after treatment (Fig. 4). At 24 hours, FSH increased from baseline in an apparent dose-dependent relationship by 13%, 52%, 49%, and 75% in the 5-mg, 10-mg, 15-mg, and 20-mg-dose groups, respectively, and returned to FIGURE 3 Mean serum levels of E 2 after single oral doses of anastrozole, 5 20 mg. CD cycle day Treadway et al. Anastrozole in premenopausal women Vol. 82, No. 6, December 2004
5 FIGURE 4 Mean serum levels of FSH after single oral doses of anastrozole, 5 20 mg. CD cycle day. baseline within 3 4 days. Levels were essentially unchanged from baseline in the control group. In the multiple-dose treatment groups (10 mg and 15 mg), FSH levels increased from baseline by an average of 39% from before dosing to day 4 (after first dosing), as compared with 9% in the control group. Levels returned to baseline by the last day of treatment (Fig. 5). No treatment-related effects were seen on the levels of LH, androstenedione, P, 17 -hydroxyprogesterone, or T. In each group, the number of mature follicles recruited was low, with most subjects recruiting a single follicle. It is interesting to note that the group with the highest mean number of follicles was the group with highest exposure to the study drug (15 mg/day for 5 days). However, individual data show this difference to be due largely to the fact that one patient in this group developed three mature follicles. FIGURE 5 Mean serum levels of FSH after multiple oral doses of anastrozole, 10 mg and 15 mg. CD cycle day. FERTILITY & STERILITY 1591
6 TABLE 1 Endometrial biopsy assessments. Endometrial biopsy results In phase (n) Out of phase (n) Out of phase (%) Control 2/4 2/4 50 Anastrozole Single dose 10/15 5/15 33 Multiple dose 5/6 1/6 17 Total 15/21 6/21 29 Endometrial maturation in the midluteal phase was not different among the groups. Histologic evaluation of the endometrium revealed that all patients (controls and treatment groups) ovulated, as verified by secretory endometrium. Compared with the control group, there was no apparent effect on maturation of the endometrium during the luteal phase for all single and multiple doses of anastrozole tested. Biopsies were dated with regard to day of luteal phase. Table 1 summarizes which biopsies were in phase with the actual date of the cycle. In the control group, 2 of 4 biopsies were considered not in phase. In the single-dose groups, 5 of 15 biopsies were not in phase (2 in the 5-mg group, 2 in the 15-mg group, and 1 in the 20-mg group). Among the multiple-dose groups, 1 of 6 were not in phase (10-mg group). In total in the anastrozole treatment groups, 6 of 21 were not in phase. With regard to general histologic findings, no subjects had any evidence of endometritis, hyperplasia, or neoplasia. One subject in the control group had fragments of benign endometrial polyp on biopsy. A total of 96 adverse events were recorded, of which 60 (63%) were considered to be possibly (58) or probably (2, hot flushes and mood swings) related to the study drug. The majority of adverse events (71%) were mild; the rest were moderate. Of the 28 moderate adverse events, 18 were considered to be possibly related to the study drug. There were no severe, serious, or other significant adverse events. One subject withdrew from the study while experiencing adverse events, and one had an adverse event that was unresolved by the time of study completion. The most frequently reported adverse events were headache (24 episodes in 13 subjects), disturbance of menstrual function (8 occasions by 6 subjects), and various gastrointestinal symptoms. There was no evidence of a dose relationship, and these adverse events were also reported in control subjects. Most events were mild and transient in nature. Psychological events (depression, excessive tiredness, mood swings, emotional episodes, and poor concentration) were reported only in anastrozole-treated subjects (7 events in 5 subjects), although no dose relationship was evident. One subject withdrew while experiencing depression and excessive tiredness. There were no clinically significant changes in vital signs or hematologic or biochemical markers. On ultrasonography, residual ovarian cysts 20 mm in the subsequent menstrual cycle were noted in 3 of the 22 subjects treated. Two subjects (one who had received a 5-mg single dose and the other a 15-mg single dose) were noted to have ovarian cysts at the follow-up examination. However, these were resolved at the repeat ultrasound and did not require any further follow-up. One additional subject, who had received a 10-mg multiple dose, was found to have a cystic area near the left ovary. This was first noted on study day 6 and persisted throughout the remainder of the study. Although this was considered as possibly related to treatment, the subject had a history of unexplained infertility, which could, potentially, have been associated with such a lesion. She was referred to her family practitioner for further investigation. No clinically significant abnormalities or changes were noted in other subjects. DISCUSSION The pharmacokinetics of anastrozole in this study were linear, predictable, and consistent with previously published data from healthy volunteers (13, 14). In the single-dose groups, anastrozole was well and rapidly absorbed, with C max occurring within 2 hours. In the multiple-dose groups, the C min vs. time profiles were consistent with linear kinetics and with a compound with a plasma t 1/2 30 hours. The experiment duration was insufficient to definitively evaluate t 1/2 and AUC 0 ; however, the interim parameters AUC 0 last and C max, and C min and T max were all considered sufficient to meet the study objective and to confirm the published profile for anastrozole in postmenopausal women (13, 14). The probable pharmacodynamic mechanism of action is evident upon consideration of the E decrease, with the resulting response of an increase in FSH. Compared with the control group, a rapid decline in E levels occurred at 3 6 hours and persisted for approximately 24 hours with the single-dose regimen and hours in the multiple-dose regimen. This E decline resulted in an FSH increase at 24 hours, persisting for 3 4 days in the single-dose regimen and 4 5 days in the multiple-dose regimen. Surprisingly, no change was noted in LH levels, but this could be owing to the low number of volunteers involved in this study. As the development of this product continues, it will be interesting to compare this E/gonadotropin profile of the normal volunteer to that noted in anovulatory patients. With regard to follicular development, the concern at the beginning of this study was the safety issue of multifollicular development, because it is a common occurrence in female patients with aromatase deficiency (15). With both the single- and multiple-dose regimens, monofollicular develop Treadway et al. Anastrozole in premenopausal women Vol. 82, No. 6, December 2004
7 ment occurred in the healthy volunteers of this study. However, in the interpretation of the follicle data, it should be noted that the subjects recruited into this study differ from the intended target population, inasmuch as the subjects in this study were known to have normal menstrual function before enrollment. The effect of the study drug on endocrine function and follicular development in subjects with anovulatory cycles might differ from that demonstrated in this study and would be worthy of further investigation. Residual ovarian cysts 20 mm in the subsequent menstrual cycle were noted in 3 of the 22 subjects treated, but 1 probably represents a parovarian cyst. Depending on the determination of this paraovarian cyst, the incidence of residual cysts was 9% 13.6%. This rate is less than that reported recently for ultrasound determination of ovarian cysts in subsequent cycles after CC treatment (21.5%) (16) and of clinical ovarian enlargement (13.6%) noted in the original Merrill registration file (17). As noted previously, the antiestrogen effects of CC result in reduced endometrial development. This study noted no delay in endometrial maturation in comparisons of both the single- and the multiple-dose groups with the control group. It is important to note that the endometrial sampling was not done in two consecutive menstrual cycles, which is the accepted practice for the diagnosis of luteal-phase defect, as determined by endometrial biopsy (18). Taking this reservation into account, the potential benefit of anastrozole with regard to the endometrial delay reported with CC is substantiated in this study (5). Anastrozole was well tolerated during this study. The pattern of adverse events observed was broadly similar to that expected on the basis of the known safety profile of the drug. Any adverse events were generally mild, transient, and well tolerated by subjects. There were no serious or other significant adverse events and no clinically significant findings in any of the other safety parameters. Anastrozole was thus considered to be safe in this study when administered in single doses of up to 20 mg and also in repeated doses of up to 15 mg/day for 5 days. In summary, anastrozole was well tolerated at the doses tested. The results demonstrated the expected effects of aromatase inhibitors, which are suppression of endogenous E 2 levels, with a resultant increase in FSH levels. The duration of action was consistent with the half-life of the drug and does not seem to affect overall menstrual function. Clinical effects included monofollicular development, minimal residual cyst formation in the subsequent cycle, and no adverse effects on endometrial maturation. Although the data are promising, the clinical effect on anovulatory cycles cannot be assessed from these limited data. Acknowledgments: The authors thank the Bourn Hall research staff, Bourn, United Kingdom. References 1. Speroff L, Glass RH, Kase NG. Clinical gynecologic endocrinology and infertility. 3rd ed. Baltimore: William and Wilkins, Insler V, Lunenfeld B. Infertility: male and female. New York: Churchill Livingstone, Isaacs JD. Ovulation induction: clomiphene citrate and menotropins. In: Cowan BD, Seifer DB, Cowan R, eds. Clinical reproductive medicine. Philadelphia: Lippincott-Raven, 1997: Mitwally MFM, Casper RF. Use of an aromatase inhibitor for induction of ovulation in patients with an inadequate response to clomiphene citrate. Fertil Steril 2001;75: Mitwally MFM, Casper RF. Aromatase inhibitors for the treatment of infertility. Expert Opin Investig Drugs 2003;12: Gysler M, March CM, Mishell DR Jr, Bailey EJ. A decade s experience with an individualized clomiphene treatment regimen including its effect on the postcoital test. Fertil Steril 1982;37: Zelinski-Wooten MB, Hess DL, Baughman WL, Molskness TA, Wolf DP, Stouffer RL. Administration of an aromatase inhibitor during the late follicular phase of gonadotropin-treated cycles in rhesus monkeys: effects on follicle development, oocyte maturation, and subsequent luteal function. J Clin Endocrinol Metab 1993;76: Shetty G, Krishnamurthy H, Krishnamurthy HN, Bhatnagar S, Moudgal RN. Effect of estrogen deprivation on the reproductive physiology of male and female primates. J Steroid Biochem Mol Biol 1997; 61: Hu Y, Cortvrindt R, Smitz J. Effects of aromatase inhibition on in vitro follicle and oocyte development analyzed by early preantral mouse follicle culture. Mol Reprod Dev 2002;61: Physicians desk reference. 57th ed. Montvale, New Jersey: Medical Economics, Fisher SA, Reid RL, Van Vugt DA, Casper RF. A randomized doubleblind comparison of the effects of clomiphene citrate and the aromatase inhibitor letrozole on ovulatory function in normal women. Fertil Steril 2002;78: Sammour A, Biljan MM, Tan SL, Tulandi T. Prospective randomized trial comparing the effects of letrozole (LE) and clomiphene citrate (CC) on follicular development, endometrial thickness and pregnancy rate in patients undergoing super-ovulation prior to intrauterine insemination (IUI) [abstract]. Fertil Steril 2001;76(Suppl 1):S Plourde PV, Dyroff M, Dukes M. Arimdex: a potent and selective fourth-generation aromatase inhibitor. Breast Cancer Res Treat 1994; 30: Boeddinghaus IM, Dowsett M. Comparative clinical pharmacology and pharmacokinetic interactions of aromatase inhibitors. J Steroid Biochem Mol Biol 2001;79: Bulun SE. Aromatase deficiency and estrogen resistance: from molecular genetics to clinic. Semin Reprod Med 2000;18: Frattarelli JL. Incidence of baseline ovarian cysts in clomiphene citrate ovulation induction cycles [abstract]. Fertil Steril 2001;76(Suppl 1): S Clomid (clomiphene citrate tablets USP), Hoechst Marion Roussel. In: Physicians desk reference. 57th ed. Montvale, New Jersey: Medical Economics, 2003: Wentz AC. Luteal phase inadequacy. In: Sciarra JJ, ed. Gynecology and obstetrics, vol 56. Philadelphia: Lippincott-Raven, 1991:1 10. FERTILITY & STERILITY 1593
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