ENDOMETRIOSIS: ROLE OF OVARIAN STEROIDS IN INITIATION, MAINTENANCE, AND SUPPRESSION

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1 FERTILITY AND STERILITY Copyright e 1980 The American Fertility Society Vol. 33, No.6, June 1980 Printed in U.SA. ENDOMETRIOSIS: ROLE OF OVARIAN STEROIDS IN INITIATION, MAINTENANCE, AND SUPPRESSION GERE S. DIZEREGA, M.D.* DONALD L. BARBER GARY D. HODGEN, PH.D. Pregnancy Research Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland Although endometriosis is commonly associated with infertility, the hormonal requirements for its spontaneous initiation and maintenance remain unknown. Since endometriosis occurs in the monkey, these primates are useful for examining the hormonal dependencies of endometrial plaques. Sequential estradiol and progesterone in Silastic capsules were placed subcutaneously into long-term castrated monkeys (N = 26). Blood samples obtained biweekly were assayed for progesterone and estradiol by radioimmunoassay. Three weeks later, endometi-iectomies were performed and the minced endometrium was "seeded" into the peritoneal cavity. Thereafter, monkeys were divided into four groups: (1) control, received no therapy; (2) received only estradiol capsules; (3) received only progesterone capsules; and (4) received both estradiol and progesterone capsules. All monkeys underwent laparotomy 4,12, and 16 weeks after endometrial transplantation to determine whether viable endometrial plaques were present. After 4 weeks, endometriosis was found in all groups, including the controls. At 12 and 16 weeks, monkeys treated with both estradiol and/or progesterone contained viable endometrial plaques, whereas monkeys without steroid supplementation contained only "burnt out" plaques, that is, nonviable endometrial tissue. In conclusion, endometrial tissue transplanted into the peritoneum required no steroid supplementation for initiation. However, once implanted, either estradiol or progesterone, alone or in combination, was required for maintenance. These findings suggest that successful treatment of endometriosis may require both the eradication of existing endometrial plaques and the prevention of reseeding over the peritoneum resulting from retrograde menstruation. Fertil Steril33:649, 1980 Although endometriosis is commonly associated with infertility, the endogenous hormonal support of its initiation and maintenance remain unknown. 1 -a Operative statistics from predominantly private practice hospitals suggest that endometriosis may account for 14% to 21% of all gynecologic surgical procedures for the treatment of infertility. 2 Furthermore, existing therapeutic modalities are commonly associated with significant side effects, including androgenization and surgical trauma. I, a Received January 25, 1980; accepted February 21, *Recipient of National Fellowship in Reproductive Medicine. To whom reprint requests should be addressed. Since endometriosis occurs spontaneously in monkeys,4-10 these surrogate primates are useful for examining the steroidal dependencies of ectopic endometrial tissue. In this study the effects of estradiol, progesterone, and a combination of the two hormones on the survival of endometrial tissue transplanted outside the uterine cavity of the cynomolgus monkey were assessed. This report demonstrates that extrauterine endometrial tissue does not require ovarian secretions for successful transplantation and initiation of growth in the peritoneal cavity; however, once initiated, a supplemental steroid, either estrogen or progesterone, is required for prolonged survival. 649

2 650 DIZEREGA ET AL. June 1980 TABLE 1. Number of Monkeys in Which at Least One Viable Plaque of Ectopic Endometrial Tissue Was Found at Different Times following Transplantation of Endometrium Weeks of treatment No. of monkeys with ectopic endometrial tissue/no. in groups Group 1: control Group 2: estradiol Group 3: progesterone Group 4: Estradiol + progesterone 4/6 0/6 0/6 2a 3/3 5/6 5/6 2b a 3a 0/2 2/2 asteroid implants were removed from monkeys in groups 2b, 3b, and 4b at 12 weeks. 4/6 5/6 4/6 5/6 3b a 4a 4b a 0/2 3/3 0/2 MATERIALS AND METHODS The care and general husbandry practices of the monkey colony have been described previously.u As determined at laparotomy, none of the monkeys had spontaneous pelvic disease prior to the study; all had had cyclic vaginal bleeding consistent with normal ovulatory menstrual cycles prior to castration. In order to manipulate ovarian steroid levels in circulation, long-term (4 to 12 months) castrated female cynomolgus monkeys (Macaca fascicularis) were treated with subcutaneous Silastic implants containing estradiol or progesterone, or both. 12 We applied steroid therapy in these castrated monkeys to simulate the natural pattern of ovarian steroids during the proliferative and secretory phases of the menstrual cycle. 13 Thus, estradiol alone was given the first 2 weeks (days 1 to 14), with the addition of a progesterone implant the 3rd week (days 15 to 21). Thereafter, endometriectomies were performed by excision of the endometrium at hysterotomy (day 22). The endometrial tissue was minced in 0.9% saline, 10 to 12 endometrial fragments (-10 mg of tissue) were inserted into the peritoneal layer at random throughout the cul-de-sac and pelvic sidewall. After the monkeys had received the endometrial transplants, they were divided randomly into four groups containing six monkeys each: (1) controls, not receiving steroid implants; (2) those receiving only estradiol; (3) those receiving only progesterone; and (4) those receiving both progesterone and estradiol implants. The subsequent levels of these steroids in circulation were in the normal physiologic ranges observed during ovulatory menstrual cycles. 13 All 24 monkeys underwent laparotomies at 4,12, and 16 weeks after tissue transplantation to assess the presence of endometrial plaques and attendant adhesion formation. At the time of direct observation the extrauterine endometrial tissue was considered viable if it was a soft, blue-green cyst or, alternatively, atrophic ("burnt out") if it was a firm, white nodule. During the laparotomy at 12 weeks, the steroid implants were removed from two of the monkeys in all groups except the controls, hereafter referred to as groups 2b, 3b, and 4b. Representative biopsy specimens were obtained from all groups during the laparotomy at week 16. These tissues were fixed in Bouin's solut:'on, cut into 7-J..Lm sections, and stained with hematoxylin and eosin for evaluation by light microscopy. Throughout the course of steroid administration, daily femoral blood samples were obtained and the sera were stored frozed ( -10 C) until estradiol and progesterone levels were determined. Radioimmunoassays of estradiol and progesterone were performed as described elsewhere. 13 Statistical analysis was performed by the X 2 test. RESULTS The results of the serial visual inspections are summarized by treatment groups in Table 1. At 4 weeks after tissue transplantation,thriving, soft, blue-green cysts were found within the pelvic peritoneum of most monkeys from all groups (two to six per monkey, 3 to 8 mm in diameter), including the control group (group 1). In several instances, adhesions had formed between the endometrial implants and adjacent omentum, uterus, adenexa, or large bowel. Monkeys were removed from the study if we were unable to detect surviving or degenerating endometrial plaques (N = 3) or if a Silastic implant had been dislodged {N = 3) prematurely. After 12 weeks, all endometrial plaques in the control group were firm, white nodules. These transplants were regarded as atrophic, or burnt out. In contrast, numerous endometrial plaques found in the pelvic cavities of monkeys receiving steroid hormones (groups 2, 3, and 4) were unchanged from observations made at 4 weeks, that is, these plaques remained as viable cystic structures which had maintained, but not extended, dissemination of the lesions. At 16 weeks, endometrial transplants found at

3 651 OVARIAN STEROIDS IN ENDOMETRIOSIS Vol. 33, No.6 FIG. 2. A representative biopsy section taken from the bluegreen cyst growing beneath the pelvic peritoneum 16 weeks after transplantation of endometrium. Note the presence of glands and stroma characteristic of viable intrauterine endometrium (hematoxylin and eosin, x 130). plants had been removed at 12 weeks (groups 2b, 3b, and 4b) were atrophic (1 to 3 mm in diameter) and appeared as firm, white nodules. That the differences in the survival of endometrial plaques were directly related to steroid hormone support is evident in Figure 1, which illustrates peripheral serum levels of progesterone and estradiol that were achieved by inserting or removing, as appropriate, the steroid-filled Silastic implants. Histologic evaluation of representative biopsies taken from blue-green, cystic lesions demonstrated characteristic endometrial glands and stroma (Fig. 2), so that the transplanted tissue appeared indistinguishable from that in spontaneous endometriosis. In contrast, microscopic evaluation of atrophic (burnt out) lesions demonstrated a fibrotic stroma surrounding degenerated endometrial glands (Fig. 3). DISCUSSION Weeks After Transplantation Serum estradiol and progesterone levels obtained from monkeys 4, 12, and 16 weeks after transplantation of endometrium into the pelvic peritoneum. Group 1 received no treatment (controll, group 2 received estradiol implants, group 3 received progesterone implants, and group 4 received both estradiol and progesterone implants. The steroid implants were removed from two of the monkeys in each treatment group during week 12 (groups 2b, 3b, and 4b). FIG weeks remained viable in association with all combinations of continued steroid therapy (groups 2a, 3b, and 4a). In contrast, all ectopic endometrial tissues in monkeys from which the steroid im- That ectopic endometrial tissue in women is dependent upon ovarian steroid secretions for its survival is evident from the regression of spontaneous endometriosis following menopause or castration. 1-3 This interplay of sex steroids, principally estrogens and gestagens, provides the current mainstay of medical therapy for this disease. 3, However, the therapeutic efficacy of estrogen and progesterone is paradoxical, since prolonged survival of established ectopic endometrial tissue is promoted by these ovarian steroids. In our surrogate primates, the transplanted en-

4 652 June 1980 DIZEREGA ET AL. FIG. 3. A representative biopsy taken from a white, firm nodule located beneath the pelvic peritoneum. Note the preseitce of atrophic glands surrounded by degenerated, fibrous stroma <hematoxylin and eosin, x 130). dometrium frequently formed masses characterized by multiple bluish-green cysts. That these plaques persisted for at least 4 weeks, even in castrated monkeys which did not receive steroid implants after tissue transplantation, suggests that the continuing presence of ovarian steroids may not be required to accommodate initiation of endometriosis. Indeed, the surprising resilience of ectopic endometrial tissue among untreated castrated monkeys is consistent with the naturally occurring rhythmicity of ovarian steroids in the menstrual cycle,13 as well as the lengthy regimens of medical therapy commonly required to induce clinical remission of endometriosis. 1-3 Since ectopic endometrial tissue was sustained in the pelvic peritoneum for 16 weeks with concurrent progesterone and/or estrogen administration, either of these ovarian steroids provided sufficient support to extrauterine endometrial plaques for survival in the castrated monkeys. On this point, possible peripheral conversion'to other steroid hormones must be considered. Similarly, Scott and Whatron 9 maintained viable ectopic endometrium for up to 37 months in castrated monkeys receiving estrone alone. However, by treating cycling monkeys with norethindrone or pharmacologic doses of 17 -hydroxyprogesterone, they were unable to identify a suppressive effect of gestagens upon viable ectopic endometrium even after 212 days of continuous therapy.10 The present study confirms and extends those observations, since both estradiol and progesterone alone successfully supported prolonged survival of extrauterine endometrial tissue. Thus, the apparent paradox continues; how can these ovarian steroids be necessary to support the survival of endometrial plaques and yet have therapeutic value in the treatment of spontaneous endometriosis? Although oral contraceptives consisting of various combinations of estrogens and progestins are among the recommended modes of standard therapy for endometriosis, their efficacy has never been evaluated conclusively in a prospective study. Yet the purported efficacy of birth control pills in the treatment of endometriosis may be well founded, not because of a direct suppression of ongoing disease but rather because of inhibition of retgrograde menstruation (believed to account for most cases of spontaneous endometriosis1), which might prevent initiation of new lesions. Indeed, the combination of estrogens and progestins known to suppress uterine contractility17 may prevent reseeding of the peritoneum with new lesions. Collectively, these results suggest that, although an antiestrogen or an antigestagen alone may provide some therapeutic benefit, regimens designed to suppress both ovarian steroid secretion and retrograde menstruation simultaneously may provide maximal opportunities for clinical remission. Reports describing the successful response of patients with endometriosis during danazol therapy, an agent which accomplishes both therapeutic objectives, support this hypothesis In conclusion, hyperplastic-decidualized endometrial tissue transplanted into the peritoneum retains viability beyond 4 weeks in castrated monkeys, even without exogenous hormonal support. However, administration of supplemental estrogen or progesterone is required to sustain these endometrial plaques for up to 16 weeks. Thus, the initiation of endometriosis is either independent of sex steroids or can be established transiently in the steroidal milieu of castration; conversely, long-term maintenance of endometrial plaques is highly dependent on ovarian steroids. Our findings suggest that successful treatment of persistent endometriosis may require both the eradication of existing endometrial plaques and the simultaneous prevention of reseeding over the peritoneum from retrograde menstruation in patients manifesting a recurrent predisposition to this disease. REFERENCES 1. Kistner RW: Endometriosis and infertility. In Progress in Infertility, Second Edition, Edited by RW Kistner, SJ Behrman. Boston, Little, Brown and Co, 1975, p 345

5 Vol. 33, No.6 OVARIAN STEROIDS IN ENDOMETRIOSIS Israel RB: Endometriosis. In Reproductive Endocrinology, Infertility and Contraception, Edited by DR Mishell, V Davajan. Philadelphia, FA Davis; 1979, p Hammond CB, Haney AF: Conservative treatment of endometriosis: Fertil Steril 30:497, Fraser AD: Ectopic endometrium in a macacus rhesus. J Obstet Gynaecol Br Emp 36:590, Kluver H, Bartelmez GW: Endometriosis in a rhesus monkey. Surg Gynecol Obstet 92:650, McCann TO, Meyers RE: Endometriosis in rhesus monkeys. Am J Obstet Gynecol 106:516, MacKenzie WF, Casey HW: Animal model of human disease: endometriosis in rhesus monkeys. Am J Pathol 80:341, McClure HM: Endometriosis. In Spontaneous Animal Models of Human Disease, Edited by Andrews EJ, Ward BC, Altman NH. New York, Academic Press, 1979, p Scott RB, Whatron LR: The effects of estrone and progesterone on the growth of experimental endometriosis in rhesus monkeys. Am J Obstet Gynecol 74:852, Scott RB, Whatron LR: Effects of progesterone and norethindrone on experimental endometriosis in monkeys. Am J Obstet Gynecol 84:867, Goodman AL, Nixon WE, Johnson DK, Hodgen GD: Regulation of folliculogenesis in the cycling rhesus monkey: selection of the dominant follicle. Endocrinology 100: 155, Legan SJ, Coon GA, Karsch FJ: Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 96:50, Goodman AL, Descalzi CD, Johnson DK, Hodgen GD: Composite pattern of circulating LH, FSH, estradiol and progesterone during the menstrual cycle of the cynomolgus monkey. Proc Soc Exp Med Bioi 155:479, Andrews WC, Larson D: Endometriosis: treatment with hormonal pseudopregnancy and/or operation. Am J Obstet Gynecol 118:643, Kistner RW: The treatment of endometriosis by inducing pseudopregnancy with ovarian hormones: a report of fiftyeight cases. Fertil Steril 10:539, Andrews MC, Andrews WC, Strauss AF: Effects ofprogestin-induced pseudopregnancy on endometriosis: clinical and microscopic studies. Am J Obstet Gynecol 78:776, Anderson NC: Physiologic basis of myometrial function. Semin Perinatol 2:211, 19' Greenblatt RB, Dmowski WP, Mahesh VB, Scholer HFL: Clinical studies with an antigonadotropin-danazol. Fertil Steril 22:102, Dmowski WP, Cohen MR: Treatment of endometriosis with an antigonadotropin, danazol: a laparoscopic and histologic evaluation. Obstet GynecoI46:147, Ansbacher R: Treatment of endometriosis with danazol. Am J Obstet Gynecol 121:283, 1975

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