Clinical predictors for buserelin acetate treatment of uterine fibroids: a prospective study of 40 women
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1 FERTILITY AND STERILITY Copyright" 1990 The American Fertility Society Printed on ocid-free paper in U.S.A. Clinical predictors for buserelin acetate treatment of uterine fibroids: a prospective study of 40 women Beverley J. Vollenhoven, M.D.*t:l: Paul Shekleton, M.D.* Jillian McDonald, S.R.N.* DavidL. Healy, Ph.D.*t Monash University and Medical Centre, Clayton, and Medical Research Centre, Prince Henry's Hospital, Melbourne, Victoria, Australia Buserelin acetate, a luteinizing hormone-releasing hormone agonist, is known to be effective in the shrinkage of uterine fibroids. A prospective trial was undertaken (1) to compare the efficacy of intranasal (IN) and subcutaneous (SC) administration of buserelin acetate and (2) to assess if tumor regression correlated with fibroid size and/or patient age. Forty patients were randomly allocated to receive 6 months of either IN buserelin acetate (n = 21) or SC buserelin acetate (n = 19). Four patients did not complete the study and were excluded from statistical analysis. Fibroid regression occurred in all36 patients. Overall regression to 66% or less ofthe initial fibroid volume occurred in 70% of subjects. There was no significant difference in fibroid shrinkage between the two administration routes. A significant positive correlation was found between initial fibroid size and subsequent fibroid regression, with larger tumors being more likely to shrink than smaller fibroids. No correlation was found between the patient's age and the extent of fibroid regression. Fertil Steril54:1032, 1990 Uterine fibroids or leiomyomata are the most common tumors in humans, occurring in 20% to 25% of women over 30 years of age. 1 For such a common condition, surprisingly little is known about its etiology. Estrogen (E) and progesterone (P) are both thought to play a role in the formation of these tumors because increased numbers of both receptors have been found in fibroids compared with normal adjacent myometrium. 2-4 Epidermal growth factor (EGF) binding has also been found in fibroids, 5 as well as the recent finding that women treated with luteinizing hormone-releasing hormone (LH-RH) agonists have reduced EGF binding compared with untreated women. 6 Received April10, 1990; revised and accepted August 6, *Department of Obstetrics and Gynecology, Monash University and Medical Centre. t Medical Research Centre, Prince Henry's Hospital. :1: Reprint requests: Beverley J. Vollenhoven, M.D., Department of Obstetrics and Gynaecology, Monash Medical Centre, Clayton Campus, Clayton Road, Clayton 3168, Victoria, Australia Vollenhoven et al. Buserelin acetate and fibroids It is now well known that LH-RH agonists, derived from peptide substitutions of native LH-RH, when given on a continuous basis cause pituitary down regulation oflh-rh receptors and therefore decreased gonadotropin and sex steroid levels. The rationale behind the usage of LH-RH agonists for the treatment of uterine fibroids has been that the hypoestrogenism caused would decrease fibroid growth if the tumors are estrogen dependent for growth. One mechanism by which this decrease occurs may be because of a reduction in uterine arterial blood flow with a parallel increase in the resistance index, as reported by Shaw. 7 He demonstrated, by the use of ultrasound (US), an increase in the uterine arterial resistance index from 0.52 to 0.92 as uterine volume decreased from 656 to 386 ml. It has been shown, by histologic examination of fibroids obtained at hysterectomy from women treated with LH-RH agonists, that intense hyalinization is observed around blood vessels, further suggesting that decreased blood supply to the tumor may play a role in its shrinkage. 8
2 Most studies have used nasal sprays or subcutaneous (SC) methods of delivery of the LH-RH agonists.9-12 Recently, implants and depot LH-RH agonist preparations given monthly or 3-month intervals have also been used Nasal sprays have undergone testing over 10 years and their efficacy is thought to be lower compared with other forms of administration.15 This has also been suggested by Friedman and associates9 who compared a group of patients receiving SC leuprolide acetate (LA) with those receiving intranasal (IN) LA. No significant fibroid regression occurred in the IN group and castrate levels of estradiol (E2) were not reached. However, Maheux and others10 successfully used IN buserelin acetate to induce fibroid shrinkage in their subjects, despite the lowest levels of serum E not being reached. Perl and associates16 reported three types ofe suppression curves: type 1 with rapidly suppressed levels; type 2 with erratic levels; and type 3 with incompletely suppressed levels. The greatest volume reduction was shown to occur with type 1 and 2 responses. A number of groups have used LH-RH agonists successfully to induce fibroid regression.9-14 Typically, there has been regression of fibroids to 50% of their initial volume. In most cases, complete shrinkage only occurred with the smaller tumors. The greatest fibroid regression occurs usually within the 1st 12 weeks of therapy. Although these treatments potentially have great benefits for women's health by avoiding major surgery, it is unclear as to which patients might benefit from this treatment. The aims of this study were (1) to compare the efficacy of both IN and SC buserelin acetate in shrinking uterine fibroids and (2) to assess the clinical predictors of patient age and fibroid size with tumor regression. This series is the largest group of patients so far reported. Patients MATERIALS AND METHODS Forty women, aged 19 to 53 years (mean 36.6 years) with uterine fibroids were referred by other gynecologists for treatment. All fibroids could be measured morphometrically by abdominal or vaginal ultrasonography. Patients were accepted into the trial if they were nonsmokers, were willing to undertake at least 3 hours of weight-bearing exercise a week, and had an intake of 1,500 mg of calcium per day. All 40 patients were symptomatic: 26 suffered from menorrhagia, 17 were infertile for 3 or more years, 15 had pressure symptoms, 6 were anaemic, 4 had pelvic pain, 3 felt bloated and 1 woman had concurrent endometriosis. Some women suffered more than one symptom. The diagnosis of fibroids was made at operation in 23 (57.5%) women and clinically in 17 ( 42.5%) women. Three patients did not complete the study and are excluded from statistical analysis. Two of these women had pelvic pain on therapy, and 1 woman using IN buserelin acetate suffered rhinorrhea necessitating cessation of treatment. A patient in the SC group was noncompliant and likewise excluded. The study was approved by the Research and Ethics committee of the Monash Medical Centre. Informed consent was obtained from all patients before the commencement of therapy. Buserelin Acetate Delivery System Buserelin acetate ([D- ser(but)6,pro9net]l- 9LHRH; Hoechst Pharmaceuticals, Melbourne, Australia) was administered either intranasally 12 X 100 JLg/d (1 insufflation per nostril6 times a day spread out as evenly as possible during the day) or as a SC pulse every 45 minutes (total dose 200 JLg/d) in a semicontinuous fashion throughout a 24- hour period. Both methods of administration were commenced in the luteal phase of the menstrual cycle. Random allocation to either IN or SC administration was made. Twenty-one women received IN and 19 received SC buserelin acetate. Of the four patients who did not complete the study, two were in the SC group and two were in the IN group. Treatment Protocol A weekly blood sample was taken for measurement of serum E2, P, LH, and follicle-stimulating hormone (FSH) as part of monitoring response to therapy. The patients were reviewed frequently and underwent both clinical and gynecological examination. Ultrasound examinations using a Real Time Sector scanner (Sono Layer-V, model SSA- 90A; Toshiba Corporation, Tochigi-Ken, Japan) were performed by a single investigator (P.S.) for fibroid tumor morphometry at 6-week intervals in most cases. Fibroid volume was calculated by the formula 4/31rr 1 X r2 X r3 where r 1, r2, r3 were the three dimensions of the fibroid. When more than one fibroid was present in the same patient, the individual volumes were summed to give a total volume. Seventeen women had one fibroid, 16 had two, 4 had three, and 3 had more than three fibroids present. There was no significant difference be- Vollenhoven et al. Buserelin acetate and fibroids 1033
3 ~l,' RESULTS Fibroid Response During Buserelin Acetate Therapy oW-~~~~~~~~~~~~~~~~_u o a ~ " u u u ~ a u WilD Figure 1 Mean percentage change in fibroid volume during buserelin acetate therapy (mean± SEM). tween the numbers of fibroids in each treatment group. The IN group had 1.80 ± 0.16 fibroids and the SC group had 1.84 ± 0.23 fibroids (P > 0.05). Side effects of and compliance with drug therapy were recorded at each visit. Hormonal Assays Serum levels of E 2 and P were measured using the Coat-a-Count radioimmunoassay (RIA) kit (Diagnostic Products Corporation, Los Angeles, CA). Luteinizing hormone and FSH were measured by World Health Organization method manual RIA. Sensitivity limits for these assays were 20 pg/ml, 0.1 ng/ml, 0.24 IU/L, and 0.19 IU/L, respectively. Intra-assay and interassay coefficients of variation were 10% and 14.8%, and 5% and 9.1% for E 2 and P, and 5.2% and 4.4%, and 5.8% and 4.9% for FSH and LH. All patients had a decrease in fibroid size during buserelin acetate treatment. Twenty-six of 36 patients (70%) had a decrease in fibroid volume to <66% of its initial size. In the 10 women whose fibroids did not decrease by 66% of its initial estimation, 5 had serum E 2 concentrations consistently above the postmenopausal range. In the 26 patients who responded with a greater reduction in fibroid volume, only 2 had serum E 2 concentrations above the postmenopausal range, and this occurred on only one occasion in each patient. Initial fibroid volume expressed as 100% decreased significantly to 49.6% ± 4% (P < ) overall over the 24 weeks of therapy. Most fibroid shrinkage had occurred by 12 weeks of the commencement of therapy, and no further significant fibroid regression occurred for the trial duration, as assessed by US (P < ) (Fig. 1). The response of women with total fibroid volume exceeding 260 ems (n = 24) were compared with those <260 ems (n = 12). The figure of 260 ems represents a fibroid of 8 em diameter and is equivalent to an abdominally palpable uterus or a 12-week pregnancy. In both groups, significant fibroid shrinkage occurred over the trial duration from an initial volume of 100% to 50.3% ± 5.3% in the first group, and 100% to 46.8% ± 5.6% in the second group (P < ) (Fig. 2). A high correlation was found between initial fibroid size and fibroid regression with a correlation coefficient of (P < 0.05). The larger the fi- Bone Densitometry Bone density in the distal third of the radius was measured at the completion of therapy in 31 patients. This examination was performed by singlephoton densitometry with a Molsgaard bone densitometer (model BDS 1100; Molsgaard Inc., Denmark). Statistical Analysis All data are presented as the mean ± SEM. Statistical analysis was performed by the two sample t test in which a value of P > 0.05 was not considered significant, and Spearman's rank correlation coefficient was employed OW-~~~~~~~~~~~~~~~~_w I II II 20 a 24 WEED Figure 2 Mean percentage change in fibroid volume for tumors < 260 cm 3 (mean ± SEM) and >260 cm 3 (mean ± SEM) during buserelin acetate therapy Vollenhoven et al. Buserelin acetate and fibroids
4 broid the more likely it was to shrink compared with the smaller fibroids in which shrinkage was less likely. Three patients whose initial fibroid volumes were 953 cm 3, 929 cm 3, and 888 cm 3 underwent tumor shrinkage to 39% (373 cm 3 ), 25% (235 cm 3 ), and 39% (350 cm 3 ), respectively, of the initial volume. These three women had the largest fibroids. The age of the patient was assessed as another clinical predictor of fibroid shrinkage over the 24 weeks ofbuserelin acetate therapy. In those women younger.than 35 years of age (n = 14), statistically significant fibroid shrinkage occurred (P < ). The initial volume in these patients was 100%, decreasing to 50.4% ± 8%. The group ofwomen older than 35 years (n = 22) also showed a significant decrease in fibroid volume over the trial period (P < ) from an initial fibroid volume of 100% to a post-treatment volume of 46.3% ± 4.5%. However, a minimal correlation was found between patient age and fibroid shrinkage (correlation coefficient 0.117; P > 0.05). Two patients aged 50 years and 21 years experienced fibroid shrinkage to 80% and 87%, respectively, of initial fibroid volume. Fibroid shrinkage was observed in both the IN and SC groups. In the former group, there was a volume reduction from an initial 100% to 49.4% ± 6.1% (P < ). In the latter group, fibroid shrinkage occurred from an initial volume of 100% to 45.6% ± 5.5% (P < ) over the 24 weeks of therapy. There was no significant difference between the two modes of administration (P > 0.05). Six of 10 patients who did not experience fibroid volume shrinkage to <66% of the original volume were in the IN group. Endocrine Response During Therapy The effect of buserelin acetate on serum E 2 concentrations was an initial stimulation after the onset of treatment to a value of pg/ml ± 16 pg/ml and a subsequent decrease in E 2 levels to the castrate range within 2 weeks of the commencement of therapy-a value of 30 pg/ml ± 6.3 pg/ml (P < ). At the e~d of treatment, the mean E 2 concentration was 28.1 pg/ml ± 3.2 pg/ml. The serum E 2 concentrations remained at <60 pg/ml at all times in 28 of 36 women. Serum FSH concentrations showed no significant differences during treatment. When the serum FSH concentrations were compared in those women at or under the age of 35 years with those older than 35 years, it can be seen that there was a 12rJU~/L ~ <31 Jean + >31Jean 0~-L~~~-L~~~-L~~~-L~~~-L~ WEEKS Figure 3 Mean serum FSH concentrations in women :,;;; 35 years and in women > 35 years receiving buserelin acetate treatment. trend for FSH concentrations to be higher in those women over the age of 35 years (Fig. 3). Despite this trend, these women still achieved significant fibroid shrinkage. Serum LH concentrations decreased within 2 weeks of therapy and remained suppressed for the duration of treatment (P = 0.05). Side Effects. of Treatment Side effects were mild and well tolerated by the majority of women. Most effects were secondary to the hypoestrogenism caused by the treatment and occurred usually after 3 to 4 weeks of therapy. All patients experienced hot flushes, 13 had mood changes, 11 vaginal dryness, 9 small joint arthralgias, and 5 were anorgasmic. Two patients developed severe pelvic pain. The first patient presented with >3 years of infertility and after 6 weeks ofbuserelin acetate treatment developed severe pelvic pain thought to be because of a perforated appendix. Buserelin acetate was stopped and at laparotomy she was found to have a normal appendix and what was described as an "inflamed fibroid uterus." She became pregnant 6 weeks after laparotomy. The second patient passed a 6-cm diameter fibroid polyp per vaginum 7 weeks after commencing buserelin acetate treatment. Nine patients reported vaginal bleeding on buserelin acetate treatment. In seven women, the bleeding was irregular and less than their normal periods and occurred in relation to elevated serum E 2 levels above the castrate range. In the other two women, significant vaginal bleeding occurred within the 1st 4 weeks of therapy and necessitated admission to hospital for blood transfusion. It is noteworthy that both these women suffered from Vollenhoven et al. Buserelin acetate and fibroids 1035
5 menorrhagia, were anaemic before commencing buserelin acetate treatment, and that one had required prior transfusions. Before the onset of therapy, six patients were anemic-mean hemoglobin (Hb) was 7.7 g/dl ± 0.70 g/dl (anemia classified as Hb < 10.5 g/dl). However, at the cessation of therapy, the mean Hb in these six subjects was g/dl ± 0.67 g/dl (P < ). Bone density measured in 31 patients at the completion of therapy gave a mean value of mg/ml ± 8.29 mg/ml (normal range for premenopausal women is 400 to 464 mg/ml ±50 mg/ml). In 6 patients both before and after treatment, bone density levels were measured; there was no statistically significant difference between the 2 levelspretreatment 438 mg/ml ± 13 mg/ml and posttreatment mg/ml ± 13 mg/ml (P > 0.05). One patient suffered from mastalgia, the cause of which could not be ascertained. Severe rhinorrhoea, necessitating cessation of therapy at 21 weeks, was suffered by one woman in the IN group. Follow-up Thirty of 36 patients (83%) have undergone follow-up from 2 weeks to 37 months (mean 9.6 months). Of those who have been followed, 23 have undergone subsequent US. Fifteen women elected, with ethical committee approval, to continue buserelin acetate treatment after the initial trial period of 24 weeks. Ten patients who had a posttreatment US but who did not continue buserelin acetate therapy showed a trend for fibroid regrowth, from a post-treatment volume of 55%± 6% to a follow-up volume of 123.1% ± 31% (P > 0.05), although this was not statistically significant because of individual variability and a wide standard error. Six of the 15 women who continued buserelin acetate therapy beyond 24 weeks underwent myomectomy while on therapy. The other 9 women continued treatment for a period of time ranging from 3 to 24 months (mean 7.4 months). After cessation of therapy, fibroid regrowth was observed from a post-treatment volume of 45.5% ± 7.2% to a follow-up volume of 70.4% ± 23% (P > 0.05), though once again this. was not statistically significant because of wide individual variation. In women who ceased treatment after 24 weeks of the trial, menstrual periods resumed within 8 weeks. Despite the regrowth of fibroids, all patients reported a subjective improvement in their subsequent menstrual symptoms, especially those of menorrhagia and dysmenorrhoea. Nine patients underwent myomectomy, 6 continuing therapy beyond 24 weeks until myomectomy. Three women conceived within 4 months of myomectomy and 6 of 17 infertile women (35%) became pregnant within 6 months of a course of buserelin acetate treatment with or without myomectomy. DISCUSSION In our study of 40 patients, the largest series so far reported, the LH-RH agonist, buserelin acetate, delivered both IN and SC, over a period of 24 weeks, was effective in causing significant fibroid shrinkage. Despite the side effects, the treatment was regarded favorably by most subjects. The side effects were considered minor when compared with the presenting symptoms. One of the more desirable effects of this treatment is the cessation of bleeding that occurs in most patients; this allows those patients who are anemic to restore their hemoglobin to normal. Accordingly, most patients found that their well-being improved once their periods ceased. The larger fibroids showed a more dramatic initial decrease in size. There was also a high correlation between initial fibroid size and subsequent fibroid shrinkage with the larger fibroids being more likely to shrink than the smaller tumors. This appears to be a useful predictor of medical treatment of uterine fibroids. No correlation was found between age and fibroid regression. Age therefore seems a poor predictor of clinical outcome. We found there was no difference between the IN and SC methods of administration as far as fibroid shrinkage was concerned. The efficacy of IN LH-RH agonist administration reported here is in contrast to other reports Both methods, however, are inconvenient for the patient and require patient compliance. The LH-RH agonist implant and depot preparations are much more convenient for women, do not depend on compliance, and will probably replace the other methods of LH-RH agonist administration. These modes of LH-RH agonist treatment have been used successfully by a number of groups Side effects were mild and in the main because of the hypoestrogenic effect ofbuserelin acetate. Of the two patients who suffered from severe pelvic pain, one required laparotomy for diagnosis. Both required cessation of buserelin acetate. We postulate that these two cases represent fibroid infarction secondary to acute estrogen deprivation. Acute pain in women with fibroids has also been 1036 Vollenhoven et al. Buserelin acetate and fibroids
6 noted in association with the use of the oral contraceptive pill. Myles and Hartl 7 reported five similar cases, which they termed "apoplectic leiomyomas," to emphasize the marked areas of hemorrhage seen histologically in these tumors. Red degeneration, classically seen in pregnancy, is also associated with acute pain and signs of peritonism. Histologic changes of this syndrome can be seen in fibroids of women treated with high dose progestins; this was the basis of a study by Goldzieher et al.18 who used progestin therapy to shrink fibroids. The side effects, though well tolerated, are inconvenient for the patient. Two recent studies by Friedman 19 and Maheux et al. 20 used an LH-RH agonist for an initial 3-month period and then added hormone replacement therapy, the estrogen from days 1 to 25 and the progestagen from days 16 to 25 of each month. In both studies, there was initial significant fibroid shrinkage and no regrowth with the combination therapy. The initial hypoestrogenic effects, particularly of hot flushes, resolved with the added hormone replacement therapy. The most worrying sequelae to hypoestrogenism is loss of bone density. Matta et al.21 showed a small but significant bone loss of 6% in trabecular bone of the lumbar vertebrae after 6 months of IN buserelin acetate therapy; the loss was reversible 6 months after cessation of treatment. In the study by Friedman/9 no reduction in bone density measured in the distal radius occurred over the 2 years of the study. Likewise in our study, bone density measured in cortical bone, after 6 months ofbuserelin acetate treatment, was within the normal range. Trabecular bone turns over more rapidly than cortical bone and more significant changes in bone density probably occur there than in the cortical bone as shown by Matta et al.21 We are currently measuring trabecular bone density in women on LH-RH agonist therapy. The protocol of an LH-RH agonist with added hormone replacement therapy once fibroid shrinkage has occurred may be the answer to long-term analog treatment. We also found a trend to fibroid regrowth in the patients who ceased buserelin acetate after the trial period. However, an interesting point to note is that during the follow-up p~riod, there was no subjective recurrence of the original presenting symptoms. The converse was found by Matta and others22 in their long-term follow-up of 10 patients. They also found fibroid regrowth and also recurrence of the original symptoms in 8 of the 10 patients. In a recent series of 19 patients undergoing follow-up over 6 months after histerelin treatment, reported by Letterie and associates, 23 they showed regrowth of fibroids to pretreatment levels in all patients, with a significant increase in volume occurring after 8 weeks of histerelin cessation. Three patients required operative intervention because of symptom recurrence. In a recent study by Benagiano,8 after a 6-month regimen of LH-RH agonist therapy, patients received medroxyprogesterone acetate, 200 and 100 mg/d for the 1st 2 months, then 50 mg/d and 25 mg/d for the final 2 months. No statistically significant regrowth occurred in the progestin-treated groups compared with the controls who were not treated with the progestin regimen, in which fibroid regrowth occurred after cessation oflh-rh agonist therapy. When fibroid shrinkage occurs with the usage of LH-RH agonist therapy, drugs capable of maintaining the effect could be used. Nine patients have undergone myomectomy after buserelin acetate treatment, 6 while still on the medication. The surgeons noted that myomectomy in these patients was easy with minimal blood loss. The pregnancy rate (PR) after myomectomy was 3 of the 9 patients, the overall PR being 6 of 17 subjects. Buttram and Reiter24 noted that the size of the fibroid at myomectomy was the most important prognostic factor for future fertility. If buserelin acetate can be used to shrink fibroids before myomectomy, a better subsequent fertility rate may ensue. New methods of fibroid surgery using myoma resectoscopes, hysteroscopic laser resection with the N d- Y AG (neodymium-yttrium- aluminiumgarnet) laser, or abdominal Nd-YAG laser myomectomy are now being used more widely. Luteinizing hormone-releasing hormone agonists used for a period of time before surgery would ensure less blood loss, less adhesion formation, and a better subsequent fertility rate, by presenting a smaller fibroid for the surgeon to resect. Recently, Donnez and others 25 reported a series of 20 patients pretreated with 6.6 mg buserelin acetate implant and 8 weeks later undergoing either hysteroscopic resection using the resectoscope or hysteroscopic Nd-YAG laser myomectomy or endometrial ablation using the Nd-YAG laser. In all cases, the operation was easily performed and blood loss was minimal. One of our patients has also undergone successful hysteroscopic resection, and this case will be reported elsewhere. In conclusion, our study has shown that initial fibroid size is a predictor of clinical response to LH RH agonist: the greater the initial volume, the more likely significant shrinkage would be ex- Vollenhoven et al. Buserelin acetate and fibroids 1037
7 pected to occur. Age, on the other hand, has been shown to be a poor predictor of clinical response to therapy. Luteinizing hormone-releasing hormone agonists are an effective temporary medical management for fibroid disease as, with cessation of treatment there is usually fibroid regrowth. However, they may hold a place in the management of the perimenopausal woman who is awaiting spontaneous menopause and the regression of her fibroids. They will also be invaluable as a preoperative medication for hysteroscopic or pelviscopic myomectomy. Long-term usage is now becoming a viable option using the combination of initial LH RH agonist treatment with added hormone replacement therapy when fibroid shrinkage has occurred. This may prevent the development of osteoporosis, which is the potential risk of prolonged LH-RH agonist therapy. REFERENCES 1. Dewhurst J: Benign disease of the uterus. In Dewhurst's Textbook of Obstetrics and Gynaecology for Post-Graduates, 4th edition, Edited by CR Whitfield. London, Blackwells Publishers, 1986, p Sadan 0, Vanidelekinge B, Van Gelderen CJ, Savage N, Becker PJ, VanDer Walt LA, Robinson M: Oestrogen and progesterone receptor concentrations in leiomyomas and normal myometrium. Ann Clin Biochem 24:263, Tamaya T, Fujimoto J, Okada H: Comparison of cellular levels of steroid receptors in uterine leiomyomata and myometrium. Acta Obstet Gynecol Scand 64:307, Wilson EA, Yang F, Rees D: Estradiol and progesterone binding in uterine leiomyomata and in normal uterine tissues. Obstet Gynecol 55:20, Hofman GE, Rao V, Barrows GH, Schultz GS, Sanfillippo JS: Binding sites for epidermal growth factors in human uterine tissues and leiomyomas. J Clin Endocrinol Metab 58:880, Lumsden MA, West CP, Bromley J, Rumgay L, Baird DT: The binding of epidermal growth factor to the human uterus and leiomyomata in women rendered hypo-oestrogenic by continuous administration of an LHRH agonist. Br J Obstet Gynaecol95:1299, Shaw RW: Mechanism oflhrh analogue action in uterine fibroids. Horm Res 32(suppl1):150, Benagiano G: Uterine fibroids: literature review and summary of posters. Horm Res 32(suppl1):120, Friedman AJ, Barbieri RL, Benacerraf BR, Schiff I: Treatment of leiomyomata with intranasal or subcutaneous leuprolide, a gonadotropin-releasing hormone agonist. Fertil Steril48:560, Maheux R, Lemay A, Me rat P: Use of intranasal luteinizing hormone releasing hormone agonist in uterine leiomyomas. Fertil Steril47:229, Coddington CC, Collins RL, Shawker TH, Anderson R, Loriaux DL, Winkel CA: Long-acting gonadotropin-hormone 1038 Vollenhoven et al. Buserelin acetate and fibroids releasing hormone analog used to treat uteri. Fertil Steril 45:624, Healy D, Lawson S, Abbott M, Baird DT, Fraser HM: Toward removing uterine fibroids without surgery: subcutaneous infusion of a luteinizing hormone releasing hormone agonist commencing in the luteal phase. J Clin Endocrinol Metab 63:619, West CP, Lumsden MA, Lawson S, Williamson J, Baird DT: Shrinkage of uterine fibroids during therapy with goserelin (zoladex): a luteinizing hormone-releasing hormone agonist administered as a monthly subcutaneous depot. Fertil Steril48:45, Vander Spuy ZM, Fieggan AG, Wood MJA, Pienaar CA: The short-term use of luteinizing hormone-releasing hormone analogues in uterine fibroids. Horm Res 32(suppl1): 137, Fraser HM: LHRH analogues: their clinical physiology and delivery systems. In Balliere's Clinical Obstetrics and Gynaecology-International Practice and Research. Antihormones in Clinical Gynaecology, Vol. 2, Edited by DL Healy. London, Balliere Tindall, Publishers, 1988, p Perl V, Marquez J, Schally AV, Comaru-Schally AM, Leal G, Zacharias S, Gomez-Lira C: Treatment ofleiomyomata uteri with D-Trp 6 -luteinizing hormone-releasing hormone. Fertil Steril48:383, Myles JL, Hart WR: Apoplectic leiomyomas of the uterus. A clinico-pathologic study of five distinctive haemorrhagic leiomyomas associated with oral contraceptive usage. Am J Surg Pathol17:548, Goldzieher JW, Maqueo M, Ricaud L, Aquilar JA, Canales E: Induction of degenerative changes in uterine myomas by high dose progestin therapy. Am J Obstet Gynecol96:1078, Friedman AJ: Treatment of leiomyomata uteri with shortterm leuprolide followed by leuprolide plus estrogen-progestin hormone replacement therapy for 2 years: a pilot study. Fertil Steril51:526, Maheux R, Lemay A, Blanchet P, Fontaine JY, Faure N: An alternative to hysterectomy in premenopausal women harbouring uterine leiomyoma: combined utilization of LHRH agonist and hormonal replacement therapy. Presented at the XII World Congress of Gynaecology and Obstetrics, Rio de Janeiro, Brazil, October 23 to 28, Published by Partheon Publishing, 1988, p Matta WH, Shaw RW, Hesp R, Katz D: Hypogonadism induced by luteinizing hormone releasing hormone analogues: effects on bone density in premenopausal women. Br Med J 294:1523, Matta WHM, Shaw RW, Nye M: Long-term follow-up of patients with uterine fibroids after treatment with the LHRH agonist buserelin. Br J Obstet Gynaecol 96:200, Letterie GS, Coddington CC, Winkel CA, Shawker TH, Loriaux DL, Collins RL: Efficacy of a gonadotropin-releasing hormone agonist in the treatment of uterine leiomyomata: a long-term follow-up. Fertil Steril51:951, Buttram VC, Reiter RC: Uterine leiomyomata: etiology, symptomatology and management. Fertil Steril 36:433, Donnez J, Schrurs B, Gillerot S, Sandow J, Clerckx F: Treatment of uterine fibroids with implants of gonadotropin-releasing hormone agonist: assessment by hysterography. Fertil Steril51:947, 1989
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