Use of Transvaginal Ultrasonography to Monitor the Effects of Tamoxifen on Uterine Leiomyoma Size and Ovarian Cyst Formation

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1 Use of Transvaginal Ultrasonography to Monitor the Effects of Tamoxifen on Uterine Leiomyoma Size and Ovarian Cyst Formation Lisa Barrie Schwartz, MD, Nicole Rutkowski, BS, Camille Horan, RDMS, Lila E. Nachtigall, MD, Jon Snyder, MD, Steven R. Goldstein, MD To evaluate the effects of tamoxifen on leiomyomas and ovarian cysts in postmenopausal breast cancer patients, uterine and leiomyoma volumes were monitored sonographically in 17 postmenopausal women receiving postoperative tamoxifen for breast cancer; patients were examined twice with a mean of 1.18 ± 0.17 years between examinations. The mean increase in leiomyoma volume was 1.26 ± 0.73 cm 3. The mean myoma volume was significantly larger at follow-up evaluation than at initial ultrasonography (5.75 ± 1.09 cm 3 versus 4.36 ± cm 3, respectively; Wilcoxon signed rank test, P = ). Six women developed new leiomyomas. Of the 21 leiomyomas initially detected, 13 increased, six decreased, and two were unchanged in volume. T ABBREVIATIONS TVUS, Transvaginal ultrasonography; SEM, Standard error of the mean; NS, Not significant; S, Significant Received November 25, 1997, from the Department of Obstetrics and Gynecology, New York University School of Medicine, New York, New York. Revised manuscript accepted for publication August 2, Address correspondence and reprint requests to Lisa Barrie Schwartz, MD, Assistant Professor, Department of Obstetrics and Gynecology, New York University Medical Center, 550 First Avenue, New York, NY The mean increase in uterine volume was ± 8.49 cm 3. Three patients had simple ovarian cysts at initial ultrasonographic examination, two of which remained unchanged in size, and the third resolved. Two patients had newly developed simple ovarian cysts. The increase in uterine and leiomyoma volumes with the development of new leiomyomas and the persistence or development of ovarian cysts in some patients support the existence of agonistic tamoxifen effects. Serial measurements of uterine and leiomyoma volumes and surveillance for ovarian cysts is recommended for tamoxifen users. KEY WORDS: Tamoxifen; Leiomyoma; Fibroid; Transvaginal ultrasonography; Ovary, cysts; Uterus, leiomyoma. he triphenylethylene tamoxifen, a partial estrogen agonist-antagonist, has been widely used as a competitive blocker of tumor estrogen receptors for the postoperative adjuvant treatment of early breast cancer. 1 The actions of tamoxifen appears to be tissue specific, with estrogenic effects on the skeletal and cardiovascular systems, liver, and uterus. 2,3 Tamoxifen s stimulatory effects within these target tissues may reduce the risk of osteoporosis and arteriosclerosis while increasing the prevalence of endometrial proliferation, polyps, hyperplasia, and cancer. 2 9 Few studies have focused on the effect of tamoxifen on uterine leiomyomas, and most of these consist of case reports and small series of patients In light of the substantial rate of breast cancer as well as the high prevalence of leiomyomas in women, the effects of tamoxifen on uterine and myoma size merits further investigation. In addition, whether the action of tamoxifen on the uterus is a direct effect or instead is mediated via a stimulatory intraovarian effect needs to be investigated further. The stimulatory effect of tamoxifen on 1998 by the American Institute of Ultrasound in Medicine J Ultrasound Med 17: , /98/$3.50

2 700 EFFECTS OF TAMOXIFEN J Ultrasound Med 17: , 1998 the ovaries was applied clinically in the past when tamoxifen was used for ovulation induction before clomiphene citrate was available. Since TVUS has proved to be a highly valuable modality for monitoring normal and pathologic uterine and ovarian changes, its use for monitoring uterine leiomyomas and ovarian cysts in tamoxifen-treated breast cancer patients should be investigated in greater depth. MATERIALS AND METHODS Seventeen postmenopausal women with surgically treated breast cancer receiving adjuvant tamoxifen (20 mg/day) were monitored with pelvic ultrasonography (Siemens Quantum 2000 vaginal probe, 5 MHz transabdominal probe) twice during therapy with a mean of 1.18 ± 0.17 years between examinations by a single sonographer (C.H.) in our Gynecologic Ultrasound Unit. The mean patient age was ± 1.84 years (range, 51 to 73 years) at the time of the initial ultrasonography. At each pelvic sonographic examination, the size (in three dimensions) of the uterus and the size (in three dimensions) and location of every leiomyoma within the uterus were documented. Uterine and leiomyoma volumes were calculated with the formula for a prolate ellipse (4/3 π length/2 anteroposterior diameter/2 transverse diameter/2). The uterine volume and the location and volume of each of the leiomyomas within the uterus were compared between the two sonographic examinations. The precise determination of the leiomyoma locations enabled the initial and follow-up measurements to be compared reliably. Data were expressed as the mean ± SEM, and statistical comparisons were performed with the Wilcoxon signed rank test. The endometrial thickness was measured at both the initial and the follow-up examinations in the midsagittal plane and were compared statistically with the Mann-Whitney rank sum test. Statistical significance was established at P < RESULTS At the time of the first ultrasonogram, 13 women had at least one leiomyoma, six women had a single leiomyoma, six women had two leiomyomas, and one woman had three leiomyomas. The locations of the tumors within the uterus were as follows: 16 intramural, three submucosal, and two intramural with subserosal components. The overall mean increase in leiomyoma volume between the initial and follow-up sonograms was 1.26 ± 0.73 cm 3. The mean myoma volume was significantly larger at the follow-up study than at the initial examination (5.75 ± 1.09 cm 3 versus 4.36 ± 0.82 cm 3, respectively; Wilcoxon signed rank test, P = , S). Six women developed new leiomyomas (Figs. 1D, 2). Of the 21 leiomyomas that were initially detected on the first ultrasonogram, 13 increased (Fig. 1A, C), six decreased, and two remained unchanged in volume. The overall mean percentage change in leiomyoma volume was 68.3 ± 23.0% (with a maximum value of 508% and minimum value of 60.0%). The overall mean increase in uterine volume was ± 8.49 cm 3. However, the uterine sizes at the initial versus follow-up sonographic examinations were not significantly different (82.24 ± cm 3 versus ± cm 3, respectively; Wilcoxon signed rank test, P = 0.058, NS). Of the 11 patients who developed a new leiomyoma or who demonstrated leiomyoma growth between the first and second sonograms, eight had a concomitant increase in overall uterine volume, two had a decrease, and one patient had no discernible change in uterine volume. The two patients whose leiomyomas decreased in size also had decreases in overall uterine volume. The three patients who each had multiple leiomyomas that both increased and decreased within the same uterus did not display any overall pattern of uterine volume change; two had an increase and one had a decreased in overall uterine volume. The mean endometrial thickness was 8.19 ± 2.22 mm at the time of the first sonogram versus ± 2.56 mm at the time of the second sonogram (Mann- Whitney rank sum test, P = , NS) (Fig. 1B). All 17 patients also were monitored for ovarian cysts during both sonographic examinations. Three patients had simple ovarian cysts at the initial study, two of which remained unchanged in size at the follow-up sonogram; the third was no longer detectable. Two additional patients had newly developed simple ovarian cysts on follow-up sonographic study. All patients remained asymptomatic during the short duration of tamoxifen therapy, and tamoxifen did not need to be discontinued in any patient during the course of this study. None of the patients required myomectomies or hysterectomies during the course of this investigation.

3 J Ultrasound Med 17: , 1998 SCHWARTZ ET AL 701 DISCUSSION Uterine leiomyomas are benign myometrial tumors that develop in approximately 25% of women of reproductive age. They may increase in size during pregnancy and usually regress after menopause, although the use of postmenopausal hormone replacement therapy may interfere with this natural regression. 16 These clinical observations, along with the increased number of estrogen receptors on myomas compared with adjacent myometrium, 17 have linked leiomyoma growth with the presence of estrogen. Progesterone also may mediate leiomyoma growth by opposing estrogenic actions. 18 The effects of tamoxifen on leiomyoma growth has not been well studied. Five studies (including our own) consisting of 22 patients have demonstrated an overall increase in leiomyoma growth (Table 1) These studies did not measure leiomyoma size and changes in size rigorously. Only Lumsden and coworkers study of six patients was unable to detect any change in leiomyoma size after the initiation of tamoxifen therapy. 11 A dramatic increase in size of a myomatous uterus in a woman treated with tamoxifen and megestrol acetate was described in a case report, which was reversed when the progestin was withdrawn. 14 Even given the shortcomings of our study, including the small sample size and the over- Figure 1 TVUS of a 55 year old woman with breast cancer treated with postoperative adjuvant tamoxifen (20 mg daily). A, Initial sonogram shows a sole mm leiomyoma on the left side. B, Sagittal section of the thin endometrial echo at the time of the first sonogram. C, D, Follow-up sonography 15 months later. C, The leiomyoma on the left side is larger (23 23 mm). D, A new 18.6 mm right posterior leiomyoma is seen. A B C D

4 702 EFFECTS OF TAMOXIFEN J Ultrasound Med 17: , 1998 A B Figure 2 TVUS of a 75 year old woman on postoperative tamoxifen therapy for breast cancer for 3 years. A, Follow-up sonogram shows a 20.8 mm leiomyoma on the right side that was not seen on the initial sonographic study. B, This leiomyoma is distinct from the quiescent right ovary. all short amount of time between the two sonographic examinations, a significant increase in leiomyoma size and the growth of new leiomyomas during tamoxifen therapy were still able to be detected. Future studies should recruit a larger pool of patients to permit a more accurate account of volume changes. In addition, such studies should also obtain a baseline ultrasonogram before tamoxifen therapy is initiated. Given the results of our study, a comparison of leiomyoma growth between women receiving tamoxifen and women who are not undergoing this therapy also is worthy of future investigation. Owing to the demonstration of tamoxifen-induced changes in leiomyoma volumes on a short-term basis, a longer study (i.e., 5 years) is warranted, especially to see if such patients eventually become symptomatic. Despite these shortcomings, the overall increase in uterine and leiomyoma volumes noted in our tamoxifen-treated patients is evidence of an agonistic estrogenic effect of tamoxifen on the uterine myometrium. The finding of no significant changes in endometrial thickness at the time of the second versus the first sonographic study further suggests that the overall increase in uterine volume is attributed to myometrial and myoma changes independent of endometrial effects. The sonographic finding of the development or persistence of simple ovarian cysts in patients treated with tamoxifen suggests the possibility that its agonistic effect on the uterus may, at least in part, be an indirect effect mediated by a direct ovarian action. Other studies also have detected simple ovarian cysts sonographically in tamoxifen users. 19,20 The clinical and biochemical significance of this effect needs to be investigated in greater depth. TVUS, which has proved to be a highly valuable modality for monitoring normal and pathologic uterine and ovarian changes, also is useful for monitoring uterine leiomyomas and ovarian cysts in tamoxifen-treated breast cancer patients. Although the majority of women in our study demonstrated simultaneous increases in both leiomyoma and uterine volumes, this was not the case for all study patients. Three patients had decreases in uterine volumes with increases in leiomyoma volumes or newly Table 1: Summary of Studies on Tamoxifen and Uterine Myoma Size Study No. of Patients Tamoxifen (mg/day) Duration* Overall Change in Uterine Size Overall Change in Myoma Size Current study Increase Increase Leo et al Increase Increase Lumsden et al Not recorded No change Dilts et al Not recorded Increase Ugwumadu et al Increase Increase *Mean number of years on tamoxifen therapy at first sonographic examination.

5 J Ultrasound Med 17: , 1998 SCHWARTZ ET AL 703 developed leiomyomas, or both. Thus, the less timeconsuming measurement of the overall uterine volume may not be an adequate indication of potential leiomyomatous changes. The overall uterine volume and an individual leiomyoma volume both should be measured sonographically for each patient receiving tamoxifen therapy. Simultaneously, the ovaries also should also be investigated sonographically to detect possible ovarian stimulation. In conclusion, the overall increase in uterine and leiomyoma volumes with the development of new leiomyomas in some patients and the persistence or formation of ovarian cysts in some patients support the existence of agonistic effects of tamoxifen. Using TVUS for serial measurements of uterine and leiomyoma volumes and surveillance for ovarian cyst formation or persistence is recommended for tamoxifen-treated patients. REFERENCES 1. Early Breast Cancer Trials Collaborative Group: Effects of tamoxifen and of cytotoxic therapy on mortality in early breast cancer: An overview of 61 randomized trials among 28,896 women. N Engl J Med 319:1681, Davidson NE: Tamoxifen panacea or Pandora s box? N Engl J Med 326:885, Thangaraju M, Kumar K, Gandhirajan R, et al: Effect of tamoxifen on plasma lipids and lipoproteins in postmenopausal women with breast cancer. Cancer 73:659, Forlander T, Cedermark B, Mattsson A, et al: Adjuvant tamoxifen in early breast cancer: Occurrence of new primary cancers. Lancet 1:117, Magriples U, Naftolin F, Schwartz PE, et al: High-grade endometrial carcinoma in tamoxifen-treated breast cancer patients. J Clin Oncol 11:485, Barakat RR, Wong G, Curtin JP, et al: Tamoxifen use in breast cancer patients who subsequently develop corpus cancer is not associated with a higher incidence of adverse histologic features. Gynecol Oncol 55:164, Rutqvist LE, Cedermark B, Glas U: The Stockholm trial on adjuvant tamoxifen in early breast cancer. Breast Cancer Res Treat 10:255, Anzai Y, Holinka CF, Kuramoto H, et al: Stimulatory effects of 4-hydroxytamoxifen on proliferation of human endometrial adenocarcinoma cells (Ishikawa line). Cancer Res 49:2362, Gottardia MM, Robinson SP, Satyaswaroop PG, et al: Contrasting actions of tamoxifen on endometrial and breast tumor growth in the athymic mouse. Cancer Res 48:812, Leo L, Lanza A, Re A, et al: Leiomyomas in patients receiving tamoxifen. Clin Exp Obstet Gynecol 21:94, Lumsden MA, West CP, Baird DT: Tamoxifen prolongs luteal phase in premenopausal women but has no effect on the size of uterine fibroids. Clin Endocrinol 31:335, Dilts PV Jr, Hopkins MP, Chang AE, et al: Rapid growth of leiomyoma in patient receiving tamoxifen. Am J Obstet Gynecol 166:167, Ugwumadu AH, Harding K: Uterine leiomyomata and endometrial proliferation in postmenopausal women treated with the anti-oestrogen tamoxifen. Eur J Obstet Gynecol Reprod Biol 54:153, Harrison-Woolrych M, Robinson R: Fibroid growth in response to high-dose progestogen. Fertil Steril 64:191, Kang J, Baxi L, Heller D: Tamoxifen-induced growth of leiomyomas: A case report. J Reprod Med 41:119, Schwartz LB, Lazer S, Mark M, et al: Does the use of postmenopausal hormone replacement therapy influence the size of uterine leiomyomata? A preliminary report. Menopause: J North Am Menopause Soc, 3:38, Brandon DD, Erickson TE, Keenan EJ, et al: Estrogen receptor gene expression in human uterine leiomyomata. J Clin Endocrinol Metab 80:1876, Rein MS, Barbieri RL, Friedman AJ: Progesterone: A critical role in the pathogenesis of uterine myomas. Am J Obstet Gynecol 172:14, Re A, Wierdis T, Tessarolo M, et al: Two cases of ovarian cysts in postmenopausal patients under antiestrogen treatment. Clin Exp Obstet Gynecol 21:221, Shushan A, Peretz T, Uziely B, et al: Ovarian cysts in promenopausal and postmenopausal tamoxifen-treated women with breast cancer. Am J Obstet Gynecol 175:752, 1996

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