MULTILOCULAR PURE LEYDIG CELL TUMOR OF OVARY, FALLOPIAN TUBE, AND EXTRAOVARIAN SOFT TISSUE
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1 Case Report MULTILOCULAR PURE LEYDIG CELL TUMOR OF OVARY, FALLOPIAN TUBE, AND EXTRAOVARIAN SOFT TISSUE Marie Boehnisch, MD* 1 ; Uwe Lindner, MD* 2 ; Touhama Salameh, MD 1 ; Anja Gebbert, MD 3 ; Lutz Kaltofen, MD 3 ; Mike Krah, MD 4 ; Olaf Dirsch, MD 1 ABSTRACT Submitted for publication July 19, 2018 Accepted for publication July 24, 2018 *These authors contributed equally. From the 1 Centre of Histopathology, 2 Department of Internal Medicine II, Gastroenterology, Hepatology, Endocrinology, Metabolic Disorders, Oncology, 3 Department of Gynecology, and 4 Institute of Radiology and Neuroradiology, Klinikum Chemnitz ggmbh, Chemnitz, Germany. Address correspondence to Dr. Uwe Lindner, Department of Internal Medicine II, Klinikum Chemnitz ggmbh, Chemnitz, Flemmingstraße 2 Germany. u.lindner@skc.de. DOI: /ACCR To purchase reprints of this article, please visit: Objective: Leydig cell tumors (LCTs) of the ovary may produce androgens and cause virilization. Although they are generally benign, these tumors are typically very small, making them hard to detect by imaging processes. Methods: We report a case of a multilocular LCT involving the ovarian stroma, fallopian tube, and extraovarian soft tissue. It was diagnosed by catheter blood sampling of ovarian and adrenal venous blood. Results: A 63-year-old female presented to the endocrinology department with progressive hirsutism and male pattern alopecia occurring within 1 year. Laboratory tests revealed high serum testosterone. Diagnosis of an androgen-producing tumor was considered, however computed tomography and magnetic resonance imaging scans did not show any conspicuous results. Gynecological examination showed slightly enlarged ovaries. Ovarian and adrenal venous blood sampling was performed via catheter for further diagnostics. The testosterone concentration from the right ovarian vein was highly elevated. The patient was admitted for surgery to the gynecological department and bilateral adnexectomy was performed. Microscopic examination showed a multilocular LCT of the right ovary which was located in the ovarian stroma, the fallopian tube, and the extraovarian soft tissue. Following the surgery, her hirsutism disappeared and serum testosterone decreased to normal levels. Conclusion: LCTs typically present with postmenopausal virilization. Catheter blood sampling is a reliable method for diagnosis. Furthermore, follow up is essential as ovarian LCTs often have multilocular presentation. (AACE Clinical Case Rep. 2019;5:e16-e21) Abbreviations: GnRH = gonadotropin-releasing hormone; LCT = Leydig cell tumor INTRODUCTION We present the case of a postmenopausal woman showing rapid progress of hyperandrogenism and demonstrate the investigative pathway leading to the diagnosis in this case. CASE REPORT A 63-year-old female presented with progressive hirsutism and a 1-year history of alopecia. Physical examination showed an obese patient with a body mass index of 30.5 kg/m². The Ferriman-Gallwey score for hirsutism was 15 points out of 36. The patient had experienced menopause 10 years previously. While premenopausal, the patient was diagnosed with polycystic ovarian syndrome. Surgical history was significant for cholecystectomy and palatine tonsillectomy. Current medical conditions included uterus myomatosis, metabolic syndrome, type 2 diabetes mellitus, diffuse and nodulous goiter, vitamin D deficiency, and a cyst on the left kidney. e16 AACE CLINICAL CASE REPORTS Vol 5 No. 1 January/February 2019
2 Multilocular Leydig Cell Tumor, AACE Clinical Case Rep. 2019;5(No. 1) e17 Laboratory tests revealed a highly elevated serum testosterone concentration (over 6 times the normal upper limit) with a high androgen index (13.8%, maximum range is 3.6%). Additionally, low serum levels of antimüllerian-hormone (<0.01 μg/l, minimal range is 1 μg/l) and inhibin B were identified. Dehydroepiandrosterone sulfate and androstenedione serum levels were normal and 24-hour urinary cortisol excretion was also within the normal range. Serum estrogen concentration was found at premenopausal levels and was associated with elevated luteinizing hormone and follicle-stimulating hormone serum concentrations. A tumor of the pituitary gland was excluded by magnetic resonance imaging scan of the head. In search of an androgen-producing tumor, an abdominal and pelvic computed tomography scan revealed no obvious results, only a slight increase in the size of both ovaries. Gynecological examination showed no abnormalities other than mild enlargement of the ovaries. A positron emission tomography scan did not show any increased glucose metabolism. A small androgen-producing tumor was regarded as the most likely diagnosis, so catheter sampling of ovarian and adrenal venous blood was performed as depicted in Figure 1 (1). The hormonal results of the sampling are presented in Table 1, and there was a reliable catheterization of both adrenal veins as evidenced by the cortisol concentration being more than twofold higher than in the inferior vena cava. Table 1 also reveals a very high testosterone concentration in the right ovarian vein, indicating the excessive production was from that area. Surgery was identified as the best course of treatment and bilateral adnexectomy was performed (Fig. 2). Both ovaries underwent pathology investigation, and the left side was found to be healthy. On the other hand, macroscopic examination of the right ovary revealed a single, brown tumor measuring cm located in the ovarian medulla. Histology showed a well-circumscribed tumor consisting of medium-sized cells with monomorphic nuclei (Fig. 3). Some tumor cells showed a single prominent nucleolus. However, no atypical cells were found. The tumor cells showed abundant, eosinophilic cytoplasm and also some lipid vacuoles. No Reinke crystals were identified. Histologically similar cell nests were found in the hilar area of the right ovary, the extraovarian soft tissue, and the fallopian tube. Immunhistochemical staining showed a strong positive reaction of the tumor cells with calretinin, melan-a, and inhibin. A faint positive reaction was shown with androgen receptor. Estrogen receptor was negative and progesterone receptor only showed faint positivity. Less than 1% of the tumor cells showed positivity with the cell proliferation marker MIB-1. A rapid normalization of testosterone serum level was observed postoperatively. A follow-up examination of the patient 4 months after surgery revealed a steady normal testosterone serum level and virilization had subsided. DISCUSSION Signs of hyperandrogenism often cause severe stress for women. After menopause, estrogen production declines rapidly but the ovaries remain hormonally active. Androgen production in women persists depending on luteinizing hormone levels. This postmenopausal imbalance between estrogens and androgens may lead to mild signs of hyperandrogenism such as decreased scalp hair or the appearance of a few terminal hairs in the face (2). However, a search for preexisting or undiagnosed causes of postmenopausal hyperandrogenism should be undertaken if signs such as hirsutism (Ferriman-Gallwey score for hirsutism >8), alopecia, or acne exist. When hyperandrogenism is severe, with rapid progression or with signs of virilization (such as deepening of the voice or clitoromegaly), an androgen-secreting tumor should be excluded. Such tumors can originate from the adrenal glands, ovaries, or be ectopic and they may also be malignant. However, markedly elevated androgen concen- Fig. 1. Sites of venous sampling locations. Abbreviations: RD = ren dexter; RS = ren sinister; V. OV DX = vena ovarica dextra; V. OV SN = vena ovarica sinistra; VRS = vena renalis superior. Fig. 2. Intraoperative view of the right ovary.
3 e18 Multilocular Leydig Cell Tumor, AACE Clinical Case Rep. 2019;5(No. 1) trations can also be due to non-tumorous causes like hyperthecosis. The specific diagnosis is important for prognosis and therapy (2,3). Workup of patients with postmenopausal hyperandrogenism follows a specific investigative pathway (Fig. 4) (2). This approach allows for a streamlined diagnostic process, but it is also important to recognize potential pitfalls in the diagnostic pathway. Adrenal tumors may be benign, hormonally inactive adenomas. These tumors are relatively common and do not cause hyperandrogenism (4). Conversely, tumors of ovarian origin can be less than 1 cm and invisible by imaging techniques. Therefore, Table 1 Serum Hormone Levels at the Venous Sampling Locations Site Testosterone (nmol/l) Cortisol (nmol/l) Testosterone / cortisol ratio , A B C D Fig. 3. Right ovary with medullary tumor. (A) arrow points to the tumor, hematoxylin and eosin staining, magnification (B) detail from panel A showing typical histology of Leydig cells, hematoxylin and eosin staining, magnification 20. (C) Leydig tumor cell nests in extraovarian tissue of the fallopian tube, hematoxylin and eosin staining, magnification 5. (D) positive inhibin staining of the right ovary, magnification 1.09.
4 Multilocular Leydig Cell Tumor, AACE Clinical Case Rep. 2019;5(No. 1) e19 combined ovarian and adrenal venous blood sampling is a useful method to determine the site of androgen secretion. This procedure requires experience, because success rates of complete catheterization of all adrenal and ovarian veins are <50%. Additionally, androgen-suppression tests such as the 1-mg dexamethasone suppression test and the gonadotropin-releasing hormone (GnRH) analogue test can assist with identifying hyperandrogenism of adrenal and ovarian origin (2,3,5). In our case, diagnostic workup led to the identification of a multifocal Leydig cell tumor (LCT). In postmenopausal women with high serum testosterone levels, an androgen-producing tumor of the ovary must be considered (3,6). Ovarian LCTs are a possible cause and are the most frequent neoplastic source of virilization in postmenopausal women (7,8). The mean age of disease occurrence is 58 years (9). Initial presentation of LCTs often is due to testosterone production. In some cases, LCTs can produce estrogen and progesterone (10). LCTs can be derived from ovarian hilus cells; these are the ovarian counterpart to testicular Leydig cells (11). Alternatively, the tumor may also develop initially from ovarian stroma Fig. 4. Diagnostic pathway for postmenopausal hyperandrogenism adopted with modification from Markopoulos et al (2). Abbreviations: AGS = adrenogenital syndrome; CT = computed tomography; DHEA-S = dehydroepiandrosterone-sulfate; MRI = magnetic resonance imaging; PCOS = polycystic ovarian syndrome; US = ultrasound.
5 e20 Multilocular Leydig Cell Tumor, AACE Clinical Case Rep. 2019;5(No. 1) (8). Therefore, ovarian LCTs are subclassified into hilar and non-hilar types (12). LCTs are a rare subgroup of steroid cell tumors which represent about 0.1% of all ovarian tumors (13). Within these steroid cell tumors, LCTs represent about 20% (14). They are usually well circumscribed and have a solid, white-yellow cut surface. Mostly the tumor is composed of polyhedral to rounded cells with generally abundant eosinophilic cytoplasm. Lipid vacuoles within the cytoplasm may be present with or without lipofuscin pigment, and the tumor cells may contain crystals of Reinke. Most tumors show positive immunostaining for inhibin, calretinin, CD99, and less frequently, melan-a (15). However, positive immunostaining for androgen receptor is uncommon (15). Ovarian LCTs are often very small and are therefore very difficult to detect using imaging processes (8). It is helpful to use invasive techniques such as extracting blood via a catheter to determine exact serum hormone levels and locate the tumor (6). Surgical adnexectomy is both diagnostic and typically curative. An alternative therapeutic approach to bilateral adnexectomy is the use of GnRH analogues. Some LCTs respond to GnRH analogues with decreasing testosterone secretion (16). A study conducted by Pascale et al (17) showed suppression of serum testosterone levels by GnRH analogues in virilized women with various ovarian androgen-secreting tumors. They suggested that these tumors are not autonomous, but depend upon continuous gonadotropin stimulation. This would also help explain the tendency for LCTs to emerge after menopause. Unlike in males, it is unknown precisely where Leydig cells derive from in females. Two main possibilities are discussed in the literature (18). One theory identifies them as vestiges of male structures (18,19). Another model attributes their origin to undifferentiated mesenchyme (18,20). In women, Leydig cells can be distributed in the hilus, mesovarium, and in the cortex of the ovary (18,20,21). Both of these theories help explain why LCTs arise in different locations and therefore may be multilocular. Paraskevas and Scully (7) performed a study where the clinical and pathological features of 12 Reinke crystalpositive and 9 (probable) crystal-negative hilus cell ovarian tumors were reviewed. It is highly likely there were LCTs within these 21 samples as 62% of the cases had androgenic manifestations with elevated serum testosterone levels. The results showed that none of the 10 patients for whom follow-up data ranging from 1 to 17 years were available died because of their tumors, which emphasizes the benign behavior of these tumors. However, the results also showed that the virilizing signs did not completely disappear in 5 of the 10 patients after removal of the tumor, which shows multifocality might not be rare. So, it is essential to perform follow-up examination of the patient with postoperative testosterone serum level controls. CONCLUSION In postmenopausal women exhibiting signs of hyperandrogenism, LCTs of the ovary must be considered. These tumors typically present with markedly elevated serum testosterone levels and therefore cause hirsutism, alopecia, and virilization. Due to the neoplasm s small size, preoperative location using imaging techniques is very challenging as demonstrated by this case. However, if serum testosterone levels are significantly elevated and imaging identifies no adrenal or ovarian tumor mass, venous blood extraction via catheter can determine the tumor s origin. Bilateral adnexectomy is performed for diagnosis and is typically curative, although a subsection of ovarian LCTs respond to GnRH analogues. As demonstrated by this case, it is possible that LCTs of the ovary may be multilocular despite their benign nature. Therefore, it is essential to measure serum testosterone postoperatively to exclude residual tissue. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Stephens JW, Katz JR, McDermott N, MacLean AB, Bouloux PM. An unusual steroid-producing ovarian tumour: case report. Hum Reprod. 2002;17: Markopoulos MC, Kassi E, Alexandraki KI, Mastorakos G, Kaltsas G. Hyperandrogenism after menopause. Eur J Endocrinol. 2015;172.2:R79-R Alpañes M, González-Casbas JM, Sánchez J, Pián H, Escobar- Morreale HF. Management of postmenopausal virilization. J Clin Endocrinol Metab. 2012;97: Fassnacht M, Arlt W, Bancos I, et al. Management of adrenal incidentalomas: European Society of Endocrinology Clinical Practice Guideline in collaboration with the European Network for the Study of Adrenal Tumors. Eur J Endocrinol. 2016;175: G1-G Mendoza-Mathison LC, Rabasa MF, González C, Pérez A. Postmenopausal hyperandrogenism in a patient with an adrenal adenoma: how should we approach it? AACE Clin Case Rep. 2016;2:e138-e Matuszczyk A, Petersenn S, Lahner H, et al. Leydig cell tumor as a cause of hirsutism in a postmenopausal woman [in German]. Med Klin (Munich). 2007;102: Paraskevas M, Scully RE. Hilus cell tumor of the ovary. A clinicopathological analysis of 12 Reinke crystal-positive and nine crystal-negative cases. Int J Gynecol Pathol. 1989;8: Roth LM, Sternberg WH. Ovarian stromal tumors containing Leydig cells. II. Pure Leydig cell tumor, non-hilar type. Cancer. 1973;32: Nucci MR, Oliva E. Diagnostic Pathology: Gynecological. 2nd ed. Milton, Canada: Elsevier, Inc.; Mikuz G. 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6 Multilocular Leydig Cell Tumor, AACE Clinical Case Rep. 2019;5(No. 1) e Staebler A, Tübingen, Kommoss F, Friedrichshafen. Lehrserie Nummer 195 Ovarialtumoren IV [in German]. Available at: Accessed December 11, Roux-Guinot S, Gorin I, Vadrot D, Djid R, Bethoux JP, Escande JP. Androgenic alopecia revealing an androgen secreting ovarian tumor [in French]. Ann Dermatol Venereol. 2001;128: Jones MW, Harri R, Dabbs DJ, Carter GJ. Immunohistochemical profile of steroid cell tumor of the ovary: a study of 14 cases and a review of the literature. Int J Gynecol Pathol. 2010;29: Klotz RK, Müller-Holzner E, Fessler S, et al. Leydig-cell-tumor of the ovary that responded to GnRH-analogue administration - case report and review of the literature. Exp Clin Endocrinol Diabetes. 2010;118: Pascale MM, Pugeat M, Roberts M, et al. Androgen suppressive effect of GnRH agonist in ovarian hyperthecosis and virilizing tumours. Clin Endocrinol (Oxf). 1994;41: Anderson MC. Hilar cell tumour of the ovary. J Clin Pathol. 1972;25: Teter J, Nadworny J, Zachwiej E, Bartoszewicz W. Interstitial cell tumour of ovary with virilism detected preoperatively with the help of endocrinological methods. J Obstet Gynaecol Br Commonw. 1961;68: Merrill JA. Ovarian hilus cells. Am J Obstet Gynecol. 1959;78: Sternberg WH, Roth LM. Ovarian stromal tumors containing Leydig cells. I. Stromal-Leydig cell tumor and non-neoplastic transformation of ovarian stroma to Leydig cells. Cancer. 1973;32:
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