Goserelin (Zoladex*) depot in the treatment of endometriosist
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1 FERTILITY AND STERILITY Copyright 1992 The American Fertility Society Printed on acid-free paper in U.S.A. Goserelin (Zoladex*) depot in the treatment of endometriosist Romeo P. Reichel, M.D.* Karl-W. Schweppe, M.D. Zoladex Endometriosis Study Group II University of Vienna, Vienna, Austria, and District Hospital Ammerland, Westerstede, Germany Study Objective: To evaluate the safety and efficacy of Goserelin (Zoladex depot; ICI Pharmaceuticals, Macclesfield, Cheshire, United Kingdom) in the treatment of endometriosis. Design: Open study. Setting: Eleven centers in Germany and 1 center in Austria. Patients: One hundred forty-six patients with pelvic endometriosis. Intervention: Goserelin (Zoladex depot) therapy, one depot (3.6 mg) subcutaneously every 4 weeks for 6 months. Results: Total subjective score and total pelvic symptom score showed a reduction by 86% and 93%, respectively, at the end of the treatment and did not exceed one fifth of the pretreatment value throughout the follow-up period of 48 weeks. One hundred seven women underwent a second laparoscopy at the end of the therapy for determination of objective efficacy: 54% of the patients showed a reduction of implants and adhesions by at least 50% or more, and 31.5% had a complete resolution of visible deposits. The mean reduction of implants and adhesions was 50%, and the mean reduction of implants 72%. Twenty of 64 (31.3%) previously infertile patients successfully conceived within 12 months after discontinuation of the therapy. Goserelin led to a down regulation of the pituitary ovarian axis and as a pharmacological effect of this hypoestrogenism most patients had hot flushes and vaginal dryness. Conclusions: Zoladex depot therapy proved to be safe and effective in the medical treatment of endometriosis. Fertil Steril1992;57: Key Words: Goserelin, Zoladex depot, gonadotropin-releasing hormone agonist, endometriosis Received October 15, 1991; revised and accepted February 26, * ICI Pharmaceuticals, Macclesfield, Cheshire, United Kingdom. t Supported by ICI Pharmaceuticals, Macclesfield, Cheshire, United Kingdom, and by ICI Pharma, Heidelberg, Germany and Vienna, Austria. * Reprint requests: Romeo P. Reichel, M.D., First Department of Gynecology and Obstetrics, University of Vienna, Spitalgasse 23, A-1090, Vienna, Austria. District Hospital Ammerland. II The following investigators (The Zoladex Endometriosis Study Group) and centers participated in the conduct and analysis of this study: Liselotte Mettler, M.D., Helga Steinmueller, M.D., Kiel, Germany; Alfred S. Wolf, M.D., Volker Sasse, M.D., Ulm, Germany; Gunther Bastert, M.D., Peter Rosenbaum, M.D., Homburg/Saar, Germany; Stefan Niesert, Ph.D., Hannover, Germany; Wolfgang Distler, M.D., Moenchengladbach-Rheydt, Germany; Manfred Kaufmann, M.D., Johannes Gauwerky, Ph.D., Heidelberg, Germany; Fritz Jaenicke, Ph.D., Muenchen, Germany; Paul Doerdelmann, M.D., Claus Grumbrecht, M.D., Hans F. Staiger, M.D., Karlsruhe, Germany; Eduard Daume, M.D., Marburg, Germany; and Jiirgen Spona, Ph.D., Vienna, Austria. Continuous administration of a gonadotropin-releasing hormone agonist (GnRH-a) leads to a down regulation of pituitary GnRH receptors and subsequently inhibits ovarian hormone production. This reversible hypoestrogenism has become a more recent therapeutic approach for hormonal therapy of endometriosis (1, 2). In a previous study, treatment with GnRH-a was found to be as effective as with danazol but with a more favorable safety profile (3). The aim of the present noncomparative trial was to evaluate the safety and efficacy of a monthly subcutaneous (SC) administration of Goserelin (Zoladex depot; ICI Pharmaceuticals, Macclesfield, Cheshire, United Kingdom) in the treatment of endometriosis. MATERIALS AND METHODS Patients Between June 1987 and May 1988, 146 patients (mean age of 30.2 years and range of 19 to 39 years) Reichel and Schweppe Zoladex depot in endometriosis 1197
2 with pelvic endometriosis were admitted into an open multicenter study (11 centers in Germany, 1 in Austria). Inclusion criteria were patients with normal menstrual periods suffering from endometriosis with a revised American Fertility Society (AFS) score (4) of ~2 determined by laparoscopy with either a total pelvic symptom score of ~3 with or without infertility or with a total pelvic symptom score of <3 with concurrent sterility or infertility for at least 2 years probably because of endometriosis. Informed consent was obtained from all patients before the start ofthe therapy. Criteria for exclusion were: (1) pregnancy or breast-feeding; (2) severe concurrent disease; (3) specific therapy of sterility within the last month; (4) oral contraceptives within the last 2 months; and (5) gestagen, danazol, or GnRH-a therapy within the last 6 months. Selected characteristics of the patients and the characteristics for withdrawals are listed in Table 1. Assessments and Response Criteria For the assessment of objective efficacy, a laparoscopy was performed and the extent of endometriosis documented using both the revised AFS classification (4) and the additive diameter of implants before and after 24 weeks of treatment. The additive diameter of implants is the estimated sum of the diameters of implants. During the pretreatment laparoscopy, no surgical interventions were made that would have affected the subsequent assessment of the disease. When biopsies were taken for histologic examination, the pretreatment revised AFS score was determined after the biopsy. The pretreatment and post-treatment laparoscopies had to be made by the same observer. Treatment success was defined as a decrease in the total revised AFS score of >50% between the pretreatment and posttreatment laparoscopy. A decrease of <50%, no change, or any increase in total revised AFS score, or a withdrawal from the study for any reason at any time before the second laparoscopy were considered a treatment failure. For subjective response, the pelvic symptoms (dysmenorrhea, dyspareunia, and pelvic pain) and the physical findings (pelvic tenderness and ii,lduration) were scored (range 0 to 3) (5). The scores for each of the three symptoms were added to calculate the total pelvic symptom score, and the scores for each of the three symptoms, and the two physical findings were added to define the total subjective score. Subjective and endocrinologic assessments (luteinizing hormone [LH), follicle-stimulating hormone [FSH), estradiol [E 2), progesterone [P], testosterone [T), prolactin [PRL), Table 1 Selected Characteristics of Patients and of Withdrawals Pretreatment total revised AFS score Pretreatment implant score Pretreatment adhesion score Pretreatment additive diameter of implants, mm No. of patients entered Symptomatic Asymptomatic No. of patients who underwent 2nd laparoscopy Pretreatment revised AFS stage I II III IV Total no. of patients withdrawn Patients with protocol violations Withdrawals during treatment Lack of effect Unable/unwilling to continue Adverse experience Pregnancy Other Withdrawals during follow-up Return of symptoms Amenorrheic 3 months post-treatment Pregnancy Other Characteristics 20.6 ± 23.5* 11.4 ± ± ± (100.0lt 105 (71.9) 39 (26.7) 107 (73.3) 25 (17.1) 59 (4004) 46 (31.5) 16 (11.0) 61 (41.8) 8 (5.5) 17 (11.6) 0(0.0) 5 (304) 8 (5.5) 0(0.0) 4 (2.7) 44 (30.1) 0(0) 1 (0.7) 11 (7.5) 32 (21.9) * Values are means ± SD. t Values are the number of patients with percents in parentheses. dehydroepiandrosterone sulfate [DHEAS], and sex hormone-binding globulin [SHBG]) were made before the treatment and every 4 weeks until the end of the study. Hematologic (hemoglobin, hematocrit, red blood cell count, white blood cell count, and platelet count) and biochemical parameters (creatinine, urea, total bilirubin, aspartate transaminase, alanine transaminase, alkaline phosphatase, total protein, albumin, gamma-glutamyl transpeptidase, electrolytes, cholesterol, triglycerides, high-density lipoproteins [HDL], and low-density lipoproteins [LDL]) were assessed before the treatment, in weeks 4, 12, and 24 during the treatment, and 8 and 24 weeks after the end of the treatment period. Possible side effects were elicited and documented. After 24 weeks of the treatment, patients had to be followed up for additional 24 weeks (visits every 8th week) and those patients desiring pregnancy for 12 months. Luteinizing hormone, FSH, E 2, P, PRL, and DHEAS serum concentrations were determined by a solid-phase coated tube radioimmunoassay (RIA). Determination of SHBG was carried out via a double-antibody RIA. Interassay and intra-assay vari Reichel and Schweppe Zoladex depot in endometriosis Fertility and Sterility
3 ation coefficients ranged between 5% and 9%. For statistical analysis the t-test was used. Therapy Goserelin was presented in a cylindrical rod of biodegradable and biocompatible d,l-lactide-glycolide copolymer. The rod that is approximately 1.2 mm in diameter and 1 cm in length contains 3.6 mg goserelin and is supplied in a prefilled sterile applicator. The depot was injected SC into the anterior abdominal wall. Therapy has to be started within the first 7 days ofthe menstrual cycle. The treatment schedule was to administer one depot every 4 weeks for 24 weeks. Objective Efficacy RESULTS In 107 of the 146 patients, a second laparoscopy was performed after 24 weeks of the therapy. The mean total revised AFS score showed a sharp decline by 50% and varied with the stage of the disease (a 92.7% reduction in stage I, 68.8% in stage II, 56.4% in stage III, and 34% in stage IV). This reduction of the mean total revised AFS score by 50% was because of a reduction of the mean implant score by 71.9%. Correspondingly, the mean total additive diameter of implants was reduced by 78% (all stages) with consistent changes regardless of the stage of disease. Seventy-nine patients (54.1 %) presented a reduction of the total revised AFS score of >50%. Therefore treatment success as defined by the protocol amounted to 54%. A complete resolution of visible deposits was achieved in 46 (31.5 %) patients. Treatment failures were ascertained in 67 patients (45.5%): 23 (16%) ofthem showed a decrease of the pretreatment revised AFS score of <50%, in 5 patients (3.4%) no change took place, 32 patients (21.9%) had no second laparoscopy performed, and 8 patients (5.5%) were protocol violators (in 1 patient there was a treatment failure for 2 reasons). Subjective Efficacy The changes of the subjective scores are shown in Figure 1. There was a reduction of 38% of the total subjective score during the 1st month of therapy and a further reduction during the treatment. At the end of the therapy, the improvement of the total pelvic symptom score and of the total subjective score was 93% and 86%, respectively. After the cessation of the therapy, both scores increased but remained below one fifth of the pretreatment value throughout the 24 weeks ofthe post-treatment follow-up. Endocrinology After the goserelin treatment, we observed a reduction of the mean serum LH and FSH concentration that in turn led to a suppression of the mean serum E2 concentration (Fig. 2). These hormones remained suppressed throughout the therapy and normalized during the follow-up period. Progesterone levels that had dropped during the therapy were consistent with the return of the ovulatory cycles after the cessation of the treatment. Serum T and PRL declined during the therapy. This change achieved statistical significance (P < 0.005) at week 4 for T and at week 8 for PRL (Fig. 2); however, DHEAS and SHBG remained unchanged. Bleeding Pattern One hundred eight (91 %) of the 119 patients with complete data on bleeding episodes became amen- 0rrheic (defined as no menstruation or no more than 2 days of spotting per month from the 8th week of the study until completion of the treatment). Menstruation returned after a mean time of 74.4 days (range 25 to 127 days) after the last application of a Zoladex depot. Pregnancies Sixty-four patients were infertile at the beginning and desired pregnancy at the end of the treatment period. Twenty of them (31.3%) successfully conceived within 12 months after the cessation of the therapy. Three of 6 patients who had been fertile at 7 Score O~-' r-'r-' ~ Week ~1~ l~lm W % ~ ~ ~ Figure 1 Mean (SEM) total subjective score (.) and total pelvic symptom score (0) before the treatment (week 0), during the treatment (weeks 4 to 24), and during the follow-up period (weeks 32 to 48). (No.) is the number of the evaluated patients. Reichel and Schweppe Zoladex depot in endometriosis 1199
4 14 lull LH I FSH LH PG/ML E Week Week NG/ML T 14 NG/ML PRL Week Week Figure 2 Mean (SEM) LH/FSH, E 2, T, and PRL before the treatment (week 0), during the treatment (weeks 4 to 24), and during the follow-up period (weeks 32 to 48). the entry and desired pregnancy successfully conceived during the post-treatment follow-up. The mean time from the date of last depot application to the confirmation of the pregnancy was 237 days (range 94 to 361 days). In addition, 4 patients in whom we did not know whether they desired pregnancy or not conceived. A total of 27 patients conceived, 23 had live births, 2 had spontaneous abortions, 1 had a still birth, and 1 pregnancy outcome remains unknown. Elicited Recognized Side Effects All 146 patients were assessed for safety. Because of the pharmacological effect of GnRH -a, the most common elicited recognized side effects were hot flushes, sweating, and vaginal dryness. The elicited recognized side effects are listed in Table 2. Spontaneously Reported Side Effects The most frequently reported adverse events were hot flushes (3%), dry skin, headache, alopecia, and depression (2% each). No other adverse event exceeded 1 % incidence. Adverse events considered severe and probably related to treatment were reported in two patients. The adverse event in one of these patients, sweating and hot flushes, was a recognized pharmacological effect of GnRH -a and led to the withdrawal of the patient. The other patient was withdrawn after 3 weeks of therapy because of anxiety, dyspnea, insomnia, nervousness, and palpitation. After 54 days, these symptoms had disappeared. Table 2 Side effects Hot flushes Sweating Dry vagina Libido changes Headache Mood swings Breast size changes Depressions Ankle edema Seborrhea Acne Voice changes Hirsutism Elicited Recognized Side Effects Before treatment 2 (1)* 4 (3) 3 (2) 17 (12)t 28 (19) 22 (15) NA:j: 13 (9) 4 (3) 17 (12) 16 (11) NA NA During treatment 145 (99) 140 (96) 92 (63) 86 (59) 80 (55) 75 (51) 49 (34) 41 (28) 23 (16) 21 (14) 18 (12) 7 (5) 6 (4) * Values are the number of patients in whom side effects occurred with percents in parentheses. t Libido impaired before treatment. :j: NA, not assessed Reichel and Schweppe Zoladex depot in endometriosis Fertility and Sterility
5 Local Tolerance and Other Changes A total of 848 Zoladex depot injections were given, and local reactions were registered four times (0.5%) affecting three patients (2.1%). There were two patients with weight gain who had not returned to pretreatment weights by the end of the study. Two patients had an increase in systolic and two in diastolic blood pressure at one occasion during the study. No clinically significant abnormalities or changes in laboratory parameters were reported as adverse events. Serum cholesterol, triglycerides, HDL, and LDL did not show any statistically significant differences during the treatment. DISCUSSION In the treatment of endometriosis, various hormonal preparations like gestagens, estrogens (Es), contraceptives, or danazol have been used during the last decades. Danazol treatment proved to be significantly more effective than gestagen treatment (6). The androgenic and anabolic properties of danazol, however, were associated with weight gain, edema, myalgia, hepatocellular damage, and negative effects on serum lipid profile. Meanwhile, several studies have shown that GnRH -as are as effective as danazol, but with a better tolerability and fewer side effects. The disadvantage of daily parenteral administration of GnRH -a presently available has been overcome with long-acting depot preparations such as Zoladex depot. This drug with its monthly SC injections guarantees reliable drug concentrations during the therapy and ensures compliance. This open phase II clinical trial evaluated the safety and efficacy of the GnRH-a Zoladex depot for the hormonal treatment of endometriosis. Women with endometriosis were successfully treated with Zoladex, 3.6 mg depot administered once every 28 days over a period of 6 months. The response as determined by the total revised AFS score varied with the stage of the disease. Because the mean additive diameter of implants was reduced by 72% regardless of the revised AFS stage, the effect of goserelin on the total revised AFS score is affected by the extent of adhesion formation. Moreover, goserelin therapy successfully improved the pelvic symptoms throughout the therapy and at least for another 6 months thereafter. During the 6 months of post-treatment follow-up, the decreasing number of patients complicated the interpretation of the subjective scores. However, in at least 63 of 78 patients the mean values did not exceed 1.3 (total subjective score) or 0.9 (total pelvic symptom score) throughout the 6-month follow-up (Fig. 1). Because most patients are treated because of their symptoms and not because of their implants, the improvement of symptoms during the therapy and thereafter is the most important clinical result of our study. Goserelin down regulates the pituitary ovarian axis to a complete postmenopausal hypoestrogenic status. In contrast to other investigators (7) who showed an FSH decrease only during the 1st month, we observed a significant reduction of FSH and LH during the whole treatment period. Different laboratory methods measuring total FSH or biologically active FSH might explain these differences. As a result of the endocrine changes, most patients presented menopausal side effects such as hot flushes, sweating, and vaginal dryness. These side effects were considered tolerable and only led to one withdrawal from the therapy. In fact, 44 ofthe 61 patients who were withdrawn from the study dropped out for nonmedical reasons during the follow-up period. In this study, a low incidence of irregular vaginal bleeding was observed during the treatment, which is considerably lower than the known 20% to 40% bleeding proportion with the use of intranasal (IN) application of GnRH-a such as buserelin acetate (8, 9). Goserelin leads to a steadier hypothalamic down regulation and ovarian suppression because of its continuous and constant release from the depot formulation. Other investigators (10) showed that the sustained release of buserelin acetate from depot preparations was more effective in the resolution of endometriotic lesions than the IN route of administration. This is probably caused by the more profound and consistent inhibition of the pituitary ovarian axis by a depot preparation. These authors (10) also demonstrated that lower circulatory E2 levels during therapy correlated with a better resolution of the endometriotic disease. Thus depot preparations of GnRH-a seem to be more suitable in the treatment of endometriosis than daily applications. In spite of the sharp fall in E2levels, SHBG levels remained unchanged. With regard to the decrease of total T, the biologically active free T is reduced. Nevertheless, the frequency of androgenic symptoms (seborrhea and acne) did not show significant changes in comparison with the pretreatment situation. The changed T:E2 ratio in favor of a less decrease of androgens might be responsible for the unchanged proportion of patients with androgenic symptoms. Although the ovarian suppression achieved by administering Zoladex depot is more pronounced than by using other drugs such as danazol (11) or Reichel and Schweppe Zoladex depot in endometriosis 1201
6 - nasal application of GnRH-a (12), the clinical and pelviscopic results are similar at the end of the treatment as well as during the follow-up. Therefore, the use of these different drugs for the treatment of endometriosis is determined by the side effect profile and the individual tolerance. Metabolic changes, especially in lipid metabolism, are observed during a danazol therapy (13), but no influences of GnRH-a on these parameters could be established (14). Bone mineral loss during the treatment with GnRH-a represents a major concern. In the literature, controversial data exist about the reversibility of the demineralization after cessation of the medication (15, 16). Therefore a treatment that lasts longer than 6 months cannot be recommended at this point in time. More precise data using new techniques (dual energy x-ray absorptiometry) will answer the questions about the degree of bone loss during the GnRH-a treatment and about bone resorption after the therapy. A hormone replacement therapy with low-dose E may be a therapeutic principle to prevent hypoestrogeneic side effects and yet is low enough not to interfere with goserelin efficacy concerning the regression of endometriotic implants and relief of endometriotic symptoms. According to another investigation (17), there is no correlation between the degree of E2 decrease and the degree of regression of endometriosis using different hormonal medications. Our data on cumulative pregnancy proportion of 0.31 in patients with endometriosis and sterility or infertility are in accordance with the results of another study (18). On the basis of our findings, we conclude that goserelin therapy, one depot every 4 weeks for 6 months, is safe, well tolerated, and effective in the medical treatment of endometriosis. The subjective complaints associated with the disease improved significantly, and the relief of symptoms is maintained for at least 6 months after the discontinuation of the therapy. Gonadotropinreleasing hormone agonists offer patients a new treatment modality, especially when applying the monthly depot injection. REFERENCES 1. Meldrum DR, Chang RJ, Lu J, Vale W, Rivier J, Judd HL. "Medical oophorectomy" using a long-acting GnRH agonista possible new approach to the treatment of endometriosis. J Clin Endocrinol Metab 1982;54: Shaw RW, Fraser AC, Boyle H. Intranasal treatment with luteinising hormone releasing hormone agonist in women with endometriosis. Br Med J 1983;287: Henzl MR, Kwei L. Efficacy and safety of nafarelin in the treatment of endometriosis. Am J Obstet Gynecol 1990;162: The American Fertility Society. Revised American Fertility Society classification of endometriosis: Fertil Steril 1985;43: Franssen AMHW, Kauer FM, Chadha DR, Zijlstra JA, Rolland R. Endometriosis: treatment with gonadotropin-releasing hormone agonist buserelin. Fertil Steril1989;51: Mettler L. Vergleich der medikamentosen Behandlung der Endometriosis genitalis externa mit Gestrinon, Lynestrenol und Danazol in Rahmen der Drei-Stufen-Behandlung. Fertilitiit 1987;3: Venturini PL, Fasce V, Constantini S, Anserini P, Cucuccio S, de Cecco L. Treatment of endometriosis with goserelin depot, a long-acting gonadotropin-releasing hormone agonist analog: endocrine and clinical results. Fertil Steril 1990;54: Lemay A, Maheux R, Faure N, Jean C, Fazekas ATA. Reversible hypogonadism induced by a luteinizing hormonereleasing hormone (LH-RH) agonist (buserelin) as a new therapeutic approach for endometriosis. Fertil Steril 1984;41: Raitz V, Frentz M, Schweppe K-W. Ovarielle Suppression durch das GnRH-Analogon Buserelin zur Behandlung der Endometriose. Geburtschilfe Frauenheilkd 1990;50: Donnez J, Nisolle-Pochet M, Clerckx-Braun F, Sandow J, Casanas-Roux F. Administration of nasal buserelin as compared with subcutaneous buserelin implant for endometriosis. Fertil Steril 1989;52: Jelly RJ. Multicentre open comparative study of buserelin and danazol in the treatment of endometriosis. Br J Clin Pract 1986;41(Suppl): Henzl MR, Corson SL, Moghissi K, Buttram VC, Bergquist Ch, Jacobson J. Administration of nasal nafarelin as compared with oral danazol for endometriosis. N Engl J Med 1989;318: Schweppe K-W, Assman G. Changes of plasma lipids and lipoprotein levels during danazol treatment for endometriosis. Horm Metab Res 1984;16: Cirkel U, Schweppe K-W, Ochs H, Hanker JP, Schneider HPG. LH-RH agonist (buserelin): treatment of endometriosis; clinical, laparoscopic, endocrine and metabolic evaluation. Arch Gynecol Obstet 1989;246: Stevenson JC, Lees B, Gardner R, Shaw RW. A comparison of sceletal effects of goserelin and danazol in premenopausal women with endometriosis. Horm Res 1989;32(1 Suppl): Dodin S, Lemay A, Maheux R, Dumont M, Turcot-Iemay L. Bone mass in endometriosis patients treated with GnRH agonist implant or danazol. Obstet GynecoI1991;77(Pt 3): Matta WH, Shaw RW. A comparative study between buserelin and danazol in the treatment of endometriosis. Br J Clin Pract 1987;41(48 Suppl): Barlow DH. Nafarelin in the treatment of infertility caused by endometriosis. Am J Obstet GynecoI1990;162: Reichel and Schweppe Zoladex depot in endometriosis Fertility and Sterility
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