Henk R. Franke, M.D., Ph.D., a Peter H. M. van de Weijer, M.D., Ph.D., b Ton M. M. Pennings, M.D., c and Marius J. van der Mooren, M.D., Ph.D.

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1 FERTILITY AND STERILITY VOL. 74, NO. 3, SEPTEMBER 2000 Copyright 2000 American Society for Reproductive Medicine Published by Elsevier Science Inc. Printed on acid-free paper in U.S.A. Gonadotropin-releasing hormone agonist plus add-back hormone replacement therapy for treatment of endometriosis: a prospective, randomized, placebocontrolled, double-blind trial Henk R. Franke, M.D., Ph.D., a Peter H. M. van de Weijer, M.D., Ph.D., b Ton M. M. Pennings, M.D., c and Marius J. van der Mooren, M.D., Ph.D. d Medisch Spectrum Twente Hospital Group, Enschede; ZCA Hospital Center, Apeldoom; Gemini Hospital, Den Helder; and Academic Hospital Vrije Universiteit, Amsterdam, The Netherlands Received November 18, 1999; accepted March 8, Supported by AstraZeneca and Novo Nordisk, who also supplied active drugs and placebo. Reprint requests: Henk R. Franke, M.D., Ph.D., Department of Obstetrics and Gynecology, Medisch Spectrum Twente Hospital Group, P.O. Box 50000, 7500 KA Enschede, The Netherlands (FAX: ; a Department of Obstetrics and Gynecology, Medisch Spectrum Twente Hospital Group, Enschede. b Department of Obstetrics and Gynecology, ZCA Hospital Center, Apeldoorn. c Department of Obstetrics and Gynecology, Gemini Hospital, Den Helder. d Department of Obstetrics and Gynecology, Academic Hospital Vrije Universiteit, Amsterdam /00/$20.00 PII S (00) Objective: To assess the effect of add-back therapy with continuous combined estrogen-progestin on the GnRH agonist induced hypoestrogenic state and its effectiveness in healing of endometriotic lesions. Design: A prospective, randomized, placebo-controlled, double-blind trial. Setting: Multiple centers in The Netherlands. Patient(s): 41 premenopausal women with laparoscopically diagnosed endometriosis (revised American Fertility Society scores 2). Intervention(s): Patients were randomly assigned to receive a subcutaneous depot formulation of goserelin, 3.6 mg, every 4 weeks, plus oral placebo or oral continuous combined estradiol-norethisterone acetate add-back therapy daily for 24 weeks. Main Outcome Measure(s): Endometriosis response, bone mineral density, transvaginal ultrasonographic changes, endocrinologic effects, and subjective side effects. Result(s): The number of endometriotic implants was significantly reduced in both groups. In the group that received GnRH agonist plus placebo, bone mineral density of the lumbar spine decreased by 5.02%. Conclusion(s): The effectiveness of GnRH agonist treatment for endometriosis was not decreased by the addition of add-back continuous combined hormone replacement therapy. Bone mineral density of the lumbar spine was maintained and subjective side effects were diminished. (Fertil Steril 2000;74: by American Society for Reproductive Medicine.) Key Words: Endometriosis, gonadotropin-releasing hormone agonist, add-back, second-look laparoscopy, bone mineral density The exact etiology of endometriosis still remains unknown. In 1921, Sampson (1) suggested that endometriosis develops as a result of menstrual regurgitation and subsequent implantation of endometrial tissue on the peritoneal surface. More recently, genetic and immunologic factors have been proposed (2). Endometriosis is the second most common gynecologic condition, after fibroids. It affects about 10% of all women of reproductive age. Pelvic pain, infertility, dysmenorrhea, abnormal bleeding, dyspareunia, and backache are primarily associated with endometriosis. It has been suggested that the frequency of this disease has increased in recent years, although this is probably the result of greater use of diagnostic laparoscopy and better recognition of the more subtle laparoscopic signs of endometriosis. The benefits of GnRH agonist for treatment of endometriosis are well established (3 9). Continued administration of GnRH agonist desensitizes GnRH receptors of the pituitary gland, which causes an initial stimulation of the pituitary ovarian axis followed by suppression of gonadotropin secretion and hypoestrogenism. Until recently, GnRH agonist administration was limited to 6 months because of con- 534

2 cerns about the long-term impact of the chronic hypoestrogenic state that these agents induce. Adverse effects of GnRH therapy are subjective vasomotor symptoms, such as hot flushes and increased sweating often accompanied by sleeplessness, and objective findings, such as vaginal dryness and loss of bone mineral density. The bone loss induced by GnRH agonist is greater than that after natural menopause, averaging 1% per month during 6 months of treatment (10). This induced loss of the trabecular component of bone may be associated with adverse effects on the cancellous microstructure that are unlikely to be reversed by cessation of therapy (11 13). Add-back hormone replacement therapy (HRT), in which various agents are combined with GnRH agonist therapy, has been recommended as a means of maintaining a therapeutic response and ameliorating potential adverse effects of GnRH agonist therapy. The rationale for this approach is the estrogen threshold hypothesis (14). The hypothesis states that low levels of circulating estradiol levels are associated with regression of estrogen-sensitive tissues (e.g., endometriotic implants) and that adding back small amounts of estrogen will increase circulating levels enough to maintain the integrity of some tissues, such as bone, with relief of vasomotor symptoms, while causing other tissues (e.g., endometriotic lesions) to remain in a state of regression. We sought to investigate whether administration of addback therapy with a continuous combined estrogen-progestin preparation reduces the vasomotor symptoms and bone loss associated with GnRH agonist therapy without compromising its efficacy in the treatment of endometriosis. MATERIALS AND METHODS Design and Patients We performed a prospective, randomized, placebo-controlled, double-blind, multicenter trial. Written approval for the study was obtained from the Institutional Review Board of each participating hospital. We included 41 women with endometriosis confirmed by laparoscopy in the 3 months before initiation of treatment. At the time of laparoscopy, endometriosis was scored according to the revised American Fertility Society (AFS-R) classification (15); patients in our study had AFS-R scores of 2 or more. No attempt was made to reduce the endometriotic lesions. All patients gave written informed consent before inclusion. Treatment After the presence of endometriosis was confirmed by laparoscopy, patients were randomly assigned in blocks of 4 to 24 weeks of treatment with a subcutaneous depot formulation of goserelin acetate (Zoladex; AstraZeneca, Zoetermeer, the Netherlands), 3.6 mg, every 4 weeks plus either an oral combination of 2 mg 17 -E 2 and 1 mg norethisterone acetate (Kliogest; Novo Nordisk, Alphen aan de Rijn, The Netherlands) or oral placebo (identical in appearance to Kliogest) daily for 24 weeks. Therapy was started during menstruation. Outcome Measures Endometriosis Response All patients underwent laparoscopy in the 3 months before initiation of therapy and again between 4 and 6 weeks after the final injections of goserelin acetate. If indicated on follow-up laparoscopy, laser vaporization, electrocautery or ultracision of the endometriotic lesions or adhesions was performed. Bone Mineral Density Bone mineral density was measured by using dual-energy X-ray absorptiometry (Lunar DPXL, Old Delft, Delft, The Netherlands; or Hologic QDR-4500A, Hologic, Waltham, MA, U.S.A.) of the lumbar spine (L2 to L4) and is expressed in g/cm 2. Bone mass was measured after the initial laparoscopy but before the first goserelin depot was given and at completion of 24 weeks of therapy. Transvaginal Ultrasonography Transvaginal ultrasonography was performed just before starting treatment and at completion of 24 weeks of therapy. The endometrial thickness, calculated as the maximum distance between the echogenic interfaces of the myometrium and the endometrium, was measured in the plane through the central axis of the uterus. The mean area of both the ovaries was estimated by using the measurements of the maximum diameters of the ovaries in the transversal plane under the assumption that the ovaries were elliptical. The formula used to calculate the mean area of the ovaries is as follows: 1/4 long right trans right ) (1/4 long left trans left ) 2 in which long is the longitudinal axis and trans is the transverse axis. Endocrinologic Effects Serum FSH and E 2 concentrations were measured on day 3 of the cycle immediately before initiation of treatment and at 24 weeks, 1 day after ingestion of the last tablet. Subjective Side Effects The Kupperman index was used to characterize climacteric symptoms. The following symptoms were scored: hot flushes, sweats, sleep, nervousness, depression, vertigo, asthenia, arthralgia, headaches, palpitations, and vaginal dry- FERTILITY & STERILITY 535

3 TABLE 1 Baseline characteristics of the study groups. Variable GnRH agonist plus placebo (n 23) GnRH agonist plus HRT (n 18) a Age (yrs) Body mass index (kg/m 2 ) Systolic blood pressure (mm hg) Diastolic blood pressure (mm Hg) Heart rate (bpm) No. of smokers (%) 7 (30.4) 6 (33.3).84 Note: Values are given as mean SD or as number (percentages) of patients. Therapy with GnRH agonist consisted of goserelin acetate; HRT consisted of 17 E 2 and norethisterone acetate. a Differences between groups were determined by using the Student t-test, the 2 test, or the Mann-Whitney U test. FIGURE 1 Mean revised American Fertility Society (AFS-R) score, before treatment (white bars) and after 24 weeks of treatment (black bars), in patients receiving GnRH agonist plus placebo or GnRH agonist plus HRT with 17 -E 2 norethisterone acetate. The decrease in AFS-R differed significantly within groups (P.05) but not between the groups (P.54). ness. The total Kupperman index score is the sum of the values of the eleven symptoms. Statistical Analysis For endometriosis response, bone mineral density, transvaginal ultrasonography, endocrinologic effects, and subjective side effects, we used the Mann Whitney U test, the unpaired Student t-test, or 2 test to compare betweengroups differences at baseline and after treatment. The Wilcoxon matched-pairs signed-rank test or paired Student t-test was used to compare within-group differences. The percentage changes from baseline in bone mineral density of the lumbar spine were calculated because the various participating hospitals used different equipment (Lunar or Hologic ). To analyze Kupperman index scores, we used Friedman two-way analysis of variance to test for within-group changes and analysis of covariance for repeated measures with the pretreatment value as constant covariate for between-group differences in changes. Statistical significance was defined as P.05. RESULTS Between April 1, 1997, and July 1, 1999, 41 patients were enrolled and assigned to study groups. The GnRH agonist plus placebo group included 23 patients and the GnRH agonist plus HRT (17 -E 2 and norethisterone acetate) included 18 patients. Baseline characteristics of the two groups did not differ significantly (Table 1). Only one patient (in the GnRH agonist plus placebo group) discontinued treatment because of severe climacteric symptoms. This patient did not undergo second-look laparoscopy. Endometriosis Response The pretreatment median AFS-R score was 28.0 (range, 6 117) in the GnRH agonist plus placebo group and 29.0 (range, 8 78) in the GnRH agonist plus HRT group. The posttreatment median AFS-R score was 6.0 (range, 0 63) in the GnRH agonist plus placebo group and 9.0 (range, 4 40) in the GnRH agonist plus HRT group. The difference between groups at both time points was not statistically significant. In both groups, the median AFS-R score was significantly reduced (P.05) (Fig. 1). The decrease was 78.6% in the GnRH agonist plus placebo group and 69% in the GnRH agonist plus HRT group; the difference between the two groups was not statistically significant (P.64). Indications for laparoscopy were pelvic pain and infertility. Seventeen patients (73.9%) in the GnRH agonist plus placebo group and 8 (44.4%) in the GnRH agonist plus HRT group had pelvic pain. Infertility was the reason for laparoscopy in 6 (26.1%) patients in the GnRH agonist plus placebo group and 10 (55.6%) patients in the GnRH agonist plus HRT group. The distribution of both indications in the different groups almost reached statistical significance (P.0549). Bone Mineral Density Pretreatment median ( SD) bone mineral density of the lumbar spine was g/cm 2 in the GnRH agonist plus placebo group and g/cm 2 in the GnRH agonist plus HRT group. The difference between groups was not statistically significant. 536 Franke et al. Endometriosis and GnRH agonist therapy Vol. 74, No. 3, September 2000

4 FIGURE 2 Bone mineral density of the lumbar spine (L2 to L4) in patients receiving GnRH agonist plus placebo (black square) or GnRH agonist plus HRT with 17 -E 2 norethisterone acetate (white circles). After 24 weeks of treatment, bone mineral density decreased 5.02% in the GnRH agonist plus placebo group and increased 0.18% in the GnRH agonist plus HRT group. (difference between groups, P.001). Posttreatment median bone mineral density of the lumbar spine was g/cm 2 in the GnRH agonist plus placebo group and g/cm 2 in the GnRH agonist plus HRT group. The difference between groups was not statistically significant. After 24 weeks of treatment, the mean bone mineral density of the lumbar spine (L2 to L4) had decreased significantly (by 5.02%) in the GnRH agonist plus placebo group, whereas it increased by 0.18% the GnRH agonist plus HRT group (Figure 2). The difference between groups was statistically significant (P.001). Transvaginal Ultrasonography At the initiation of treatment and after 24 weeks of therapy the double-layered endometrial thickness was measured and the mean area of both ovaries was calculated (Table 2). After 24 weeks of therapy, both groups experienced a statistically significant reduction in median endometrial thickness. Endometrial thickness was reduced by 43.1% P.002 in the GnRH agonist plus placebo group and 49.2% (P.009) in the GnRH agonist plus HRT group. The difference between groups was not statistically significant (P.77). The observed decrease in the median area of the ovaries was similar in both groups. After 24 weeks of treatment, the median area decreased by 31.6% in the GnRH agonist plus placebo group and 46.7% in the GnRH agonist plus HRT group. This difference was not statistically significant (P.63). Endocrinologic Effects After 24 weeks of treatment, the median serum FSH level decreased by 55.9% (P.01) in the GnRH agonist plus HRT group but by only 16.7% in the GnRH agonist plus placebo group (P.62) (Table 3). The difference in decreases between the groups was significant (P.05). The median serum E 2 level increased in both the GnRH agonist plus placebo group (P.83) and the GnRH agonist plus HRT group (P.55). However, the increase of 6.8% in TABLE 2 Transvaginal ultrasonographic findings before treatment and after 24 weeks of treatment. Group Double-layer endometrial thickness (mm) Mean area right and left ovary (mm 2 ) a Pretreatment Posttreatment Pretreatment Posttreatment endometrial thickness b endometrial thickness c area of ovary b area of ovary c GnRH agonist placebo 5.1 ( ) 2.9 ( ) 544 (155 1,266) 372 ( ) (n 23) (n 18) (n 16) (n 17) GnRH agonist HRT 6.5 ( ) 3.3 ( ) 603 (305 3,117) 321 (192 1,319) (n 17) (n 16) (n 16) (n 16) d Note: Values are given as median (range). The GnRH agonist was goserelin acetate; HRT consisted of 17 E 2 plus norethisterone acetate. a See text for formula used to calculate mean area. b Wilcoxon matched-pairs signed-rank test. c Mann-Whitney U test or Student t-test. d Mann-Whitney U test for between groups differences. FERTILITY & STERILITY 537

5 TABLE 3 Serum concentrations of FSH and E 2 before treatment and after 24 weeks of treatment. Group Pretreatment Posttreatment FSH (IU/L) E 2 (pmol/l) FSH (IU/L) E 2 (pmol/l) FSH a FSH b E 2 a E 2 c GnRH agonist placebo 6.0 (0.4 15) 117 (40 550) 5.0 (2.1 25) 125 (41 1,129) (n 23) (n 22) (n 19) (n 18).052 b.72 GnRH agonist HRT 5.9 (0.4 23) 116 (30 1,300) 2.6 (0.6 9) 280 (70 608) (n 18) (n 18) (n 18) (n 18) d Note: Values are given as median (range). The GnRH agonist was goserelin acetate; HRT consisted of 17 E 2 plus norethisterone acetate. a Wilcoxon matched-pairs signed-rank test. b Student t-test. c Mann-Whitney U test. d Mann-Whitney U test for between-groups. the GnRH agonist plus placebo was not statistically significantly different compared with the increase of 141.1% in the GnRH agonist plus HRT group (P.72). Subjective Side Effects The total Kupperman index score was calculated just before treatment was begun and at 4, 12, and 24 weeks after initiation of therapy (Fig. 3). The reduction in Kupperman index score in the GnRH agonist plus placebo group was FIGURE 3 Total Kupperman index score before treatment and at 4, 12, and 24 weeks after initiation of therapy in patients receiving GnRH agonist plus placebo (black squares) or GnRH agonist plus HRT with 17 -E 2 norethisterone acetate (white circles). In the GnRH agonist plus placebo group, the Kupperman index score decreased by 75% at 4 weeks, 129% at 12 weeks, and 113% at 24 weeks (P.0004). The difference between groups at 24 weeks was statistically significant (P.003). 75%, at 4 weeks, 129% at 12 weeks, and 113% at 24 weeks (P.004). The difference between the GnRH agonist plus placebo group and the GnRH agonist plus HRT group at 24 weeks was statistically significant (P.003). DISCUSSION Few prospective randomized trials of follow-up laparoscopy in patients with endometriosis treated with GnRH agonist plus placebo or GnRH agonist plus HRT have been published (5 9). The results of these investigations made it clear that the addition of different HRT regimens to GnRH agonist treatment for endometriosis did not influence the healing of the endometriotic implants but ameliorated subjective side effects of therapy and did not reduce bone mineral density. In the placebo group of two studies (5, 6), bone mineral densities decreased; one of these study noted reversibility (5). The type of add-back HRT is not particularly important; rather, what is important is that some type of add-back therapy is given. Compston et al. (12) demonstrated a deleterious effect to the bone microstructure induced by GnRH agonists without add-back therapy. Adverse effects on the cancellous microstructure will follow, which are unlikely to be reversed after cessation of therapy and may lead to increased risk for fracture in later life. Paoletti et al. (13) observed a complete reversal of lumbar bone mineral density loss 2 years after completion of 6 months of GnRH agonist therapy without add-back in patients with endometriosis. However, bone mineral density does not measure the microstructure of cancellous bone; increased risk for fracture may therefore be present despite demonstrable restoration of bone mineral density. Bone mineral density measurements are relevant because 538 Franke et al. Endometriosis and GnRH agonist therapy Vol. 74, No. 3, September 2000

6 relatively small decreases can produce an increase in actual risk for fracture. Because of their antiresorptive capacity, estrogens are widely accepted as having a central role in protecting the female skeleton. Estrogenic action is not uniform throughout the skeleton; the vertebrae of the lumbar spine are especially susceptible to hypoestrogenism because they are composed of more than 70% trabecular bone, whereas the appendicular skeleton of the limbs are less sensitive. Most patients achieve relief of subjective side effects within 1 month of commencing therapy. This relief may continue for 6 months after cessation of treatment, but some women, usually those with higher disease scores before treatment, experience rapid recurrence of symptoms. These women may benefit from prolonged GnRH agonist administration, preferably with add-back therapy. The demonstration of recurrent endometriotic lesions after 24 weeks of GnRH agonist treatment with or without add-back therapy emphasizes the fact that extension of treatment would benefit patients with endometriosis. Because addition of HRT to GnRH agonist treatment in these patients will neither influence the microstructure of cancellous bone nor interfere with healing of endometriotic implants (according to laparoscopy) and will decrease subjective side effects, we recommend a standard combination of GnRH agonist treatment with a continuous combined estrogen-progestin preparation. Long-term studies are needed to determine whether treatment for more than 24 weeks without unwanted side effects is possible. Acknowledgments: The authors thank Mrs. E.R.A. Peters-Muller, M.Sc., for data management and statistical analysis; the Dutch HRT-Network Foundation for logistical management of the trial; and the research nurses of the participating hospitals. They also thank H. Sipko Mülder, M.Sc., Ph.D., of AstraZeneca for his continuous support during the trial. Participating investigators in the trial were Henk R. Franke, M.D., Ph.D. (Enschede); Robert- Jan Iding, M.D. (Venray); Hans C.L.V. Kock, M.D., Ph.D. (Tilburg); Ton M.M. Pennings, M.D. (Den Helder); Jacqueliene J.P.M. Pieters, M.D. (Tilburg); and Peter H.M. van de Weijer, M.D., Ph.D. (Apeldoorn). References 1. Sampson JA. Perforating hemorrhagic (chocolate) cysts of the ovary. Arch Surg 1921;3: Dmowski WP, Steele RW, Baker GF. Deficient cellular immunity in endometriosis. Am J Obstet Gynecol 1981;141: Surrey ES. Add-back therapy and gonadotropin-releasing hormone agonists in the treatment of patients with endometriosis: can a consensus be reached? The Add-back Consensus Working Group. Fertil Steril 1999;71: Hornstein MD, Surrey ES, Weisberg GW, Casino LA. Leuprolide acetate depot and hormonal add-back in endometriosis: a 12-month study. Lupron Add-Back Study Group. Obstet Gynecol 1998;91: Surrey ES, Judd H. Reduction of vasomotor symptoms and bone mineral density loss with combined norethindrone and long-acting gonadotropin-releasing hormone agonist therapy of symptomatic endometriosis: a prospective randomized trial. J Clin Endocrinol Metab 1992;75: Howell R, Edmonds DK, Dowsett M, Crook D, Lees B, Stevenson JS. Gonadotropin-releasing hormone analogue (goserelin) plus hormone replacement therapy for the treatment of endometriosis: a randomized controlled trial. Fertil Steril 1995;3: Kiiholma P, Korhonen M, Tuimala R, Korhonen M, Hagman E. Comparison of the gonadotropin-releasing hormone agonist goserelin acetate alone versus goserelin combined with estrogen-progestagen addback therapy in the treatment of endometriosis. Fertil Steril 1995;64: Makarainen L, Ronneberg L, Kauppila A. Medroxyprogesterone acetate supplementation diminishes the hypoestrogenic side-effects of gonadotropin-releasing hormone agonists without changing its efficacy in endometriosis. Fertil Steril 1996;65: Taskin O, Yalcinoglu AI, Kucuk S, Uryan I, Buhur A, Burak F. Effectiveness of tibolone on hypoestrogenic symptoms induced by goserelin treatment in patients with endometriosis. Fertil Steril 1997; 67: Pickersgill A. GnRH agonists and add-back therapy: is there a perfect combination? Br J Obstet Gynaecol 1998;105: Leather AT, Studd JWW, Watson NR, Holland EFN. The prevention of bone loss in young women treated with GnRH analogues with addback estrogen therapy. Obstet Gynecol 1993;83: Compston JE, Yamaguchi K, Croucher PI, Garrahan NJ, Lindsay PC, Shaw RW. The effects of gonadotropin-releasing hormone agonists on iliac crest cancellous bone structure in women with endometriosis. Bone 1995;16: Paoletti AM, Serra GG, Cagnacci A, Vacca AMB, Guerriero S, Solla S, et al. Spontaneous reversibility of bone loss induced by gonadotropinreleasing hormone analog treatment. Fertil Steril 1996;65: Barbieri R. Hormone treatment of endometriosis: the estrogen threshold hypothesis. Am J Obstet Gynecol 1992;166: American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: Fertil Steril 1997;67: FERTILITY & STERILITY 539

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