Key Words: Endometriosis, GnRH-a, goserelin, Zoladex, estrogen, sex-steroid add-back therapy,
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1 FERTLTY AND STERLTY Copyright 1995 American Society for Reproductive Medicine Vol. 64, No. 5, November 1995 Printed on acid free paper in U. S. A. Comparison of the gonadotropin-releasing hormone agonist goserelin acetate alone versus goserelin combined with estrogen-progestogen add-back therapy in the treatment of endometriosis*+ Pentti Kiilholma, M.D.:j: Risto Tuimala, M.D. Seppo Kivinen, M.D. Mikko Korhonen, M.D.** Eelis Hagman, M.D.i'i' University Hospital of Turku, Turku; University Hospital of Tampere, Tampere; University Hospital of Kuopio, Kuopio; Central Hospital of Kanta-Hame, Hameenlinna; and Central Hospital of Etela-Pohjanmaa, Seinajoki, Finland Objective: To investigate whether the addition oflow-dose estrogen-p combination hormone replacement therapy () to GnRH agonist (GnRH-a) treatment for endometriosis reduces the pharmacologic side effects of such treatment without reducing efficacy and to determine the endocrinologic changes during treatment. Design: Prospective, randomized, double-blind, placebo-controlled, comparative study of two drug regimens: 3.6 mg goserelin acetate in a 28-day SC depot formulation once monthly for 6 months plus either a combination of 2 mg 17 {3-E2 and 1 mg norethisterone acetate (NET) 1 mg or matching placebo tablets once daily for 6 months. Setting: Multicenter study in three tertiary referral centers at university teaching hospitals and two central hospitals. Patients: Women with laparoscopically confirmed symptomatic endometriosis were included in the study. Results: Of the total of 19 patients screened, 93 were recruited and 88 patients were randomized to either the or the placebo group. Four women were withdrawn because of various medical reasons, and 76 patients were followed-up for a total of 12 months. n terms of efficacy, there was no difference between the two drug regimens for objective or subjective response. There were significantly less postmenopausal symptoms in the patients treated with goserelin plus compared with those treated with goserelin plus placebo. Conclusion: Goserelin diminished significantly the symptoms and laparoscopic scores of endometriosis. The addition of did not reduce the efficacy of goserelin but diminished the postmenopausal symptoms during treatment. Fertil Steri1995;64:93-8 Key Words: Endometriosis, GnRH-a, goserelin, Zoladex, estrogen, sex-steroid add-back therapy, Kliogest Since 1982, when the first clinical trial in humans using GnRH agonist (GnRH-a) for the treatment of Received November 14, 1994; revised and accepted May 12, * Presented at the Second nternational Symposium on GnRH analogues in Cancer and Human reproduction, Geneva, Switzerland, November 7 to 1, 199 and at the X World Congress of Gynecology and Obstetrics, Singapore, September 15 to 2, t Supported by Zeneca Pharma, Helsinki, Finland. :j: Department of Obstetrics and Gynecology, University Hospital of Turku. Reprint requests: Pentti Kiilholma, M.D., Department of Obstetrics and Gynecology, University Hospital ofturku, FN-252 Turku, Finland (FAX: ). endometriosis was reported (1), multiple studies have demonstrated consistent gonadal suppression with both subjective and objective improvement in patients with endometriosis (2, 3). Several randomized studies have shown that GnRH-a are at least as Department of Obstetrics and Gynecology, University Hospital of Tampere. Department of Obstetrics and Gynecology, Central Hospital of Kanta-Hame. ** Department of Obstetrics and Gynecology, University Hospital of Kuopio. tt Department of Obstetrics and Gynecology, Central Hospital of Etela-Pohjanmaa. Vol. 64, No.5, November 1995 Kiilholma et a. GnRH-a versus GnRH-a plus in endometriosis 93
2 effective as danazol in reducing subjective symptoms and in achieving resolution of endometriotic deposits (4-7). Furthermore, it has been suggested that the hypoestrogenic side effects of GnRH-a can be reduced or inhibited by the addition of estrogen-p to the treatment regimen without any subsequent loss in efficacy (8). The purpose of the present study was to investigate whether low-dose estrogen-p combination hormone replacement therapy () reduces the hypoestrogenic side effects of GnRH-a without compromising the efficacy of the GnRH-a in the treatment of endometriosis and to determine the endocrinologic changes. Patients MATERALS AND METHODS Women with endometriosis confirmed by laparoscopy before randomization underwent subjective assessments of pelvic symptoms: dysmenorrhea, dyspareunia, and pelvic pain. The severity of each symptom was graded on a scale of to 3 (absent, mild, moderate, and severe) and summed to give a total pelvic symptoms score. Only symptomatic patients with total pelvic symptoms score of ;;:::3 with or without infertility were included in the study. Patients also were examined to assess pelvic tenderness and induration, the severity of which also was graded on a scale of to 3. Endometriosis was confirmed by laparoscopy within 3 months before initiation of treatment. No attempt for endometriosis reduction other than biopsy was made. At laparoscopy the disease was staged according to the revised American Fertility Society (AFS) classification (9) and the Additive Diameter of mplants (1). Study Design After the confirmation of endometriosis by laparoscopy, patients were randomized to a 6-month treatment with 3.6 mg goserelin acetate in a 28-day SC depot formulation (Zoladex; Zeneca Pharmaceuticals, Macclesfield, United Kingdom) plus either a combination of 2 mg 17(3-E2 and 1 mg norethisterone acetate (NET; Kliogest; Novo Nordisk AS, Bagsvrerd, Denmark) or placebo once daily for 6 months. The trial medication was initiated at visit 1, and visits 2 to 6 were at 1, 3, 6, 9, and 12 months, respectively. Therapy was started during menstruation, preferably on the 1st day. Assessment of pelvic symptoms and physical examination were carried out pretreatment, at 1, 3 and 6 months after the start of treatment, and at 3 and 6 months post-treatment, i.e., 9 and 12 months after initiation of the treatment. The score montha Figure 1 The pelvic symptoms scores before and after 1, 6, and 12 months of treatment with goserelin acetate plus (1lT) and goserelin acetate plus placebo (li.\1). Values are means with range (upper and lower limits). P <.1: 6-month values significantly different from pretreatment values within both treatment groups. patients completed a menstrual, hot flush, and bleeding chart daily throughout the study until the first menstrual period after cessation of therapy. The investigator summarized the findings from the chart on the record forms at each visit. A second-look laparoscopy was performed 1 month after the last goserelin acetate injection. Total Additive Diameter of mplants and revised AFS scores were calculated at the post-treatment laparoscopy and compared with those at entry. An objective response was defined as a decrease of ;;::: 5% in the revised AFS score for peritoneal plus ovarian endometriosis. A decrease of <5% or withdrawal from the study for any reason at any time before the second laparoscopy assessment was considered as a treatment failure. Objective progression was defined as an increase of ;;:::25% in the score. The date of resumption of menses after cessation of treatment was documented. The written approval for the study was obtained from the Ethics Committee of each hospital. nformed consent was obtained from all patients and documented. Patients were provided with written information about the trial in the form of a patient information sheet. Hormone Measurements Serum concentrations of LH and FSH were determined fluoroimmunometrically by using commercial kits (DELFA LH and FSH) supplied by Wallac Co. (Turku, Finland). Serum 17 (3-E2 was measured using RA supplied by Baxter Dade Ag (Dudingen, Switzerland). Serum hormone concentrations were determined pretreatment, at 4 and 12 weeks during the treatment period, at the end of the treatment period, and at 3 and 6 months post-treatment. 94 Kiilholma et al. GnRH-a versus GnRH-a plus in endometriosis Fertility and Sterility
3 A.CDr. 3 *** GOSERELlN+ B mm *** GOSEREUN+PLACEBO them did not fulfill the criteria (pelvic symptom score <3). n addition, five further patients were protocol violators and they were excluded. Thus, 88 women were randomized to trial medication. Forty-three patients aged 2 to 48 years (mean 32 years) were allocated to goserelin acetate plus treatment and 45 patients aged 21 to 47 years (mean 34 years) were allocated to goserelin acetate plus placebo regimen. Patient demographics did not differ between groups in terms of age, weight at entry and at 6 months, average duration of menses, number of pregnancies, or number of live births. Altogether, 76 patients completed the study protocol at 12 months (35 in the goserelin acetate plus group and 41 in the goserelin acetate plus placebo group). Two patients discontinued the treatment because of side effects that were considered to be related to the treatment. One of them (goserelin acetate plus placebo) experienced severe depression and the other one had continuous bleeding (goserelin GOSERELlN+ GOSERELlN+PLACEBO A % 1 *** *** Figure 2 Total revised AFS (A) and total Additive Diameter of mplants (B) scores before (!ill) and 6 months after (l1li) treatment with goserelin acetate plus (bars at left) and goserelin plus placebo (bars at right). Values are means ± SEM. ***p <.1: significance of differences between and 6 months within treatment groups Statistical Analysis The comparison of objective response between the groups was made by using analysis of variance (generallinear method) and t-test using least significant difference method, which was used to test means between treatment groups. The t-test was used in the within-group test (Ho hypothesis was that the difference between the means between visits is ). For subjective scoring, the analysis of variance was used. The comparison of side effects was made by using the analysis of variance (between groups) and X 2 (within groups). For the comparison of hormone levels and restarting of menstruation the analysis of variance (general linear method) and t-test was used. All statistical analyses were performed by Research nternational Finland Oy, (Helsinki, Finland). RESULTS The total number of patients recruited was 93. Altogether, 19 patients were screened, but 16 of monilia B % *** *** montha Figure 3 The percentage of patients reporting hot flushes (A) and sweating (B) before and after 1, 3, 6, 9, and 12 months of treatment with goserelin acetate plus (!ill) and goserelin acetate plus placebo (l1li). **p =.3, ***p <.1: significance of differences between the treatment groups. Vol. 64, No.5, November 1995 Kiilholma et al. GnRH-a versus GnRH-a plus in endometriosis 95
4 % of pat. 1 - fll fl ** *** F F e.& o. 19 o l p F!i. 1 p % V 1. % f g.al ::ij 6 p P 12 months L- Figure 4 The percentage of patients reporting hot flushes ( no flushes; El less than once daily; i!! one to three times daily; i!! more than three times daily) before and after 1, 6, and 12 months of treatment with goserelin acetate plus and goserelin acetate plus placebo. **p <.1, ***p <.1: significance of differences between the treatment groups. acetate plus ). Three women had pregnancy confirmed during the post-treatment follow-up period. Two patients underwent surgery for endometriosis, one woman started hormonal contraception, two women were treated with hormonal or VF therapy for infertility, one patient needed hormonal therapy for a disease other than endometriosis, and one patient did not return. Forty and 43 patients with and without, respectively, completed the 6-month active treatment period. All patients showed subjective improvement on goserelin acetate therapy. The response was equally good in patients with or without (P = not significant [NS]). The pelvic symptoms score decreased from 4.7 and 4.7 in goserelin acetate plus and goserelin acetate plus placebo patients to.9 and.5 after 6 months, respectively (Fig. 1). There already was a marked fall in the score after 4 weeks of treatment. The within-group difference from pretreatment to 6-month treatment in both treatment groups was highly significant (P <.1). The scores six months after the cessation of the treatment were still significantly lower compared with those at entry, being 1.4 and 1.6 (Fig. 1). The objective response in terms of changes in total revised AFS and total Additive Diameter ofmplants scores with and without was also comparable (Fig. 2). Total revised AFS score decreased statistically significantly (P <.1) from 22.3 and 19.9 on goserelin acetate plus and goserelin acetate plus placebo, respectively, to 1.7 and 9.2 at secondlook laparoscopy. There were no significant differences between the two drug regimens. Total Additive Diameter of mplants score showed a similar decrease (P <.1) from 31.8 and 33.6 mm to 12.1 and 8. mm, respectively. Sixty-seven percent of patients allocated to goserelin acetate plus therapy and 73% ofthe patients treated with goserelin acetate plus placebo showed an objective response. The results were 26 and 22 in terms of treatment failure and 7 and 5 for objective progression, respectively. The difference between the two drug regimens was not statistically significant. The percentage of patients reporting hot flushes and sweating before and after 1, 3, 6, 9, and 12 months of treatment with both drug regimens is shown in Figure 3. The difference between patients treated with or without in addition to GnRH-a is statistically significant after treatment of 1 (P =.3), 3, and 6 months (P <.1). Hot flushes were reported more frequently by the patients receiving goserelin acetate plus placebo than by those receiving, as seen in Figure 4. The difference was significant (P <.1) after 4 weeks of trial medication and highly significant at 6 months (P <.1). There was no difference between the mean onset times of menstruation after the last injection of goserelin acetate depot. t was 69.5 days in the patients treated with goserelin acetate plus and 69.4 days in those treated with goserelin acetate plus placebo. Serum LH, FSH, and E2 concentrations (mean :±: SEM) before, during, and after treatment are shown in Figure 5. Serum LH and FSH levels were low during the treatment period. A statistically sig- 96 Kiilholma et a!. GnRH-a versus GnRH-a plus in endometriosis Fertility and Sterility
5 A lull 12 i 1 1 i! 8 " E 4 > 2 B lull 1 i " 8 8 " 8 :: e 4 E S > 2 C nmoll,5,4.,3 Ci 2 E ' j, *.* \, - - "t- - - ;",,,,,,, 12 months J 12 months Pllml 12 1 O r 'r-O o months Figure 5 Serum LH (A), FSH (B), and E 2, (C) levels before, during, and after treatment with goserelin acetate plus (_) and goserelin acetate plus placebo (A) at, 1, 6, and 12 months. Values are means ± SEM. *p <.5, ***p <.1: significance of differences between the treatment groups. nificant difference between the two drug regimens was noted in serum FSH levels, which were lower after 1, 3, and 6 months in the patients treated with goserelin acetate plus than goserelin acetate plus placebo (P <.5 at 1 and 6 months; P <.1 at 3 months between the groups). Serum E2 levels were low during the treatment period, but they were significantly higher in the patients treated with goserelin acetate plus than those with goserelin acetate plus placebo (P <.1) at 4 weeks and at 3 and 6 months The within-group differences in hormone serum concentrations from pretreatment to 6-months treatment were highly significant (P =.1) except for E2 in the goserelin acetate plus group (P =.29) (Fig. 5). For the 23 patients wishing to become pregnant, there were three pregnancies (13%). DSCUSSON Although several studies have been published investigating the use of so-called add-back therapy together with GnRH-a in the various gynecological conditions (11-13), there is little information on the use of such combinations in the patients with endometriosis. The first studies were performed by combining GnRH-a with progestins. n one study (14), patients treated with a combination of goserelin acetate and medroxyprogesterone acetate (MPA) had significantly less hot flushes than patients given goserelin acetate alone and no bone loss was seen. Unfortunately, this regimen failed to reduce significantly the subjective symptoms of endometriosis and there was no improvement in the revised AFS scores in contrast to a 5% to 6% improvement with the GnRH-a alone. n another study (15), NET, a progestin with less estrogenic activity than MPA, was combined with the GnRH-a histrelin. The addition of NET did not affect adversely the efficacy of histrelin on endometriosis. This combination was associated with a lower incidence of side effects than in the control group given histrelin alone. The reduction in vasomotor symptoms occurred despite a reduction in serum E2 concentrations into the castrate range and was dependent on the dose of NET. Progestins, however, are not ideal add-back regimens. They may result in symptoms similar to those of premenstrual syndrome and adversely affect lipid profile (11, 13). A recent study reported by Edmonds and Howell (16) combining goserelin acetate with.25 mg 17(3- E2 via an estraderm patch resulted in smaller loss in bone mineral density than in patients treated with goserelin acetate alone; however, the dose of estrogen was too low to prevent bone loss completely. Some of the pharmacologic side effects were reduced and efficacy was identical in both treatment groups. The present study using a larger dose of 17 (3-E2 showed that the long-acting GnRH-a goserelin acetate significantly diminished symptoms and laparoscopic scores of endometriosis and that combination of goserelin acetate and low-dose does not prevent the beneficial effect of GnRH-a on endometriosis. Based on these findings and the recent report of Leather et al (17), we believe that in conjunction with long-term GnRH-a therapy should reduce the risk of osteoporosis. Vol. 64, No.5, November 1995 Kiilholma et al. GnRH-a versus GnRH-a plus in endometriosis 97
6 Serum LH, FSH, and E2 values in the patients without were consistent with a previous report (18). The fall in serum LH levels after GnRH-a was the same in the placebo and groups and serum FSH levels were only moderately higher in the patients who received placebo than in those who received. Unlike most protocols using GnRH-a with addback therapy, we initiated at the beginning of GnRH-a treatment rather than after a period of several months GnRH-a alone. The relatively modest reduction of E2 in women with is not what most would consider to be adequate for the treatment of endometriosis (19). There are, however, suggestions that cyclical changes of ovarian hormones rather than their absolute concentrations are important in the genesis of menstrually related disorders such as endometriosis (2). Because it is known that low-dose continuous estrogen-p combination therapy causes endometrial atrophy and accordingly may result in regression of endometrial implants, we chose this combination for the add-back treatment regimen. t is possible that, without cyclical elevations in E2, the E2 levels in the patients treated with are below the estrogen "threshold" for endometriotic implants (19). n our study, GnRH-a appeared to be well tolerated by the patients. Only two patients discontinued the treatment for drug-related side effects. Even if postmenopausal symptoms caused by goserelin acetate without were quite bothersome for many patients they were, however, willing to continue the treatment. We think that patient compliance is better with long-acting depot implants than with frequently administered GnRH-a formulations. Goserelin acetate also provides a more steady hypothalamic down-regulation and ovarian suppression (18). n conclusion, the present study demonstrates that the long-acting GnRH-a goserelin acetate significantly diminishes symptoms and laparoscopic scores of endometriosis. The combination of goserelin acetate and low-dose estrogen-p add-back therapy while preventing postmenopausal-type symptoms during the treatment does not affect adversely its efficacy. Acknowledgment. The authors appreciate the assistance of Mr. Oli Lehti, M.Sc. (Pharm.) in the preparation of this manuscript. REFERENCES 1. Meldrum DR, Chang RJ, Vale W, Rivier J, Judd HL. "Medical oophorectomy" using a long-acting GnRH agonist: a possible new approach to the treatment of endometriosis. J Clin Endocrinol 1982;54: Lemay A, Maheux R, Faure N, Jean C, Fazekas ATA. Reversible hypogonadism induced by a luteinizing hormone-releasing hormone (LH-RH) agonist (Buserelin) as a new therapeutic approach for endometriosis. Fertil Steril1984;41: Erickson LD, Ory SJ. GnRH analogues in the treatment of endometriosis. Obstet Gynecol Clin North Am 1989; 16: Henzl MR, Corson SL, Moghissi K, Buttram VC, Berqvist C, Jacobson J. Administration of nasal nafarelin as compared with oral danazol for endometriosis: a multicentre doubleblind comparative clinical trial. N Engl J Med 1988;318: Shaw RW, Zoladex Endometriosis Study Team. A randomized, comparative study of the effect of goserelin depot and danazol in the treatment of endometriosis. Fertil Steril 1992; 58: Kennedy SH, Williams la, Brodribb J, Barlow DH, Shaw RW. A comparison of nafarelin acetate and danazol in the treatment of endometriosis. Fertil Steril 199;53: Rock JA, Truglia JA, Caplan RJ, Study Group. Zoladex (goserelin acetate implant) in the treatment of endometriosis: a randomized comparison with danazol. Obstet Gynecol 1993; 82: Barbieri RL. Hormone treatment of endometriosis: the estrogen threshold hypothesis. Am J Obstet Gynecol 1992; 166: The American Fertility Society. Revised American Fertility Society Classification of Endometriosis: Fertil Steril 1985;43: Doberl A, Bergqvist A, Jeppsson S, Koskimies A, Ronnberg L, Segerbrand E, et al. Regression of endometriosis following shorter treatment with or lower dose of danazol. Acta Obstet Gynecol Scand Supp1984;123: Barbieri RL. Gonadotropin releasing hormone agonists and estrogen-progestogen replacement therapy. Am J Obstet Gynecol 199; 162: Judd HL. Gonadotropin-releasing hormone agonists: strategies for managing the hypoestrogenic effects of therapy. Am J Obstet Gynecol 1992; 166: Lemay A, Surrey ES, Friedman AJ. Extending the use of gonadotropin-releasing hormone agonists: the emerging role of steroidal and non-steroidal agents. Fertil Steril 1994; 61: Cedars M, Meldrum DR, Judd HL. Treatment of endometriosis with a long-acting gonadotropin-releasing hormone agonists plus medroxyprogesterone acetate. Obstet Gynecol 199; 75: Surrey ES, Gambone JC, Lu JKH, Judd HL. The effect of combining norethindrone with a gonadotropin-releasing hormone agonist in the treatment of symptomatic endometriosis. Fertil Steril199;53: Edmonds DK, Howell R. Can hormone replacement therapy be used during medical therapy of endometriosis? Br J Obstet Gynaecol 1994; 11 Suppl 1: Leather AT, Studd JWW, Watson NR, Holland EFN. The prevention of bone loss in young women treated with GnRH analogues with "add-back" estrogen therapy. Obstet Gynecol 1993;81: 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 199; 54: Barbieri RL. Gonadotropin-releasing hormone agonists: treatment of endometriosis. Clin Obstet Gynecol 1993;36: Reid BA, Gangar KF, Beard RW. Severe endometriosis treated with gonadotrophin releasing hormone agonist and continuous combined hormone replacement therapy. Br J Obstet Gynaecol 1992; 99: Kiilholma et al. GnRH-a versus GnRH-a plus in endometriosis Fertility and Sterility
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