OSAMI KUnO, M.D., NAOMI YAMASAKI, M.D., YASUO KAMIJO, M.D., KEIICHI AMANO, M.D., KOICHI KITAMURA, M.D., AND REIKO DEMURA, M.D.
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1 J Neurosurg 47: , 1977 Human chorionic gonadotropin produced by ectopic pinealoma in a girl with precocious puberty Case report OSAMI KUnO, M.D., NAOMI YAMASAKI, M.D., YASUO KAMIJO, M.D., KEIICHI AMANO, M.D., KOICHI KITAMURA, M.D., AND REIKO DEMURA, M.D. Departments of Neurosurgery and Internal Medicine, Tokyo Women's Medical College, Tokyo, Japan A case is reported in which a human chorionic gonadotropin (HCG)-producing ectopic pinealoma was found in a 5-year-old girl with precocious puberty. Physical examination revealed abnormal breast enlargement. Endocrinological study disclosed a high plasma HCG concentration of 1192 ng/ml with a normal follicular stimulating hormone (FSH) level. The HCG content of the tumor was as high as 400 ng/mg of acetone dried tissue, but no FSH was detectable. This is the first reported case of precocious puberty associated with pineal tumor in a female. KEY WORDS 9 ectopic pinealoma 9 precocious puberty 9 human chorionic gonadotropin T HE causative mechanism of precocious puberty in patients with pineal-parasellar tumor is unknown. The pineal body, and dysfunction of the hypothalamus have been implicated, and recently, the ectopic secretion of human chorionic gonadotropin (HCG) from the tumor itself. Precocious puberty associated with pinealoma in the pineal-parasellar region has until now been seen exclusively in males. We are reporting the first such case in a young girl. We believe that precocious puberty in this patient was caused by an HCG-producing ectopic pinealoma of the anterior third ventricle, verified at surgery. The clinicopathological and endocrinological aspects of this rare case are briefly discussed. Case Report This 5-year-old girl was admitted to our neurosurgical department on August 5, 1975, with complaints of headache, nausea, and vomiting. She had had a generalized convulsion 8 months before admission, and had begun to complain of progressive headache. She was found to have choked discs and was referred to our clinic. Family history and past history were noncontributory. Examination. She was a somewhat drowsy girl with normal physical development except for bilateral breast enlargement as shown in Fig. 1. Bone age was 5 years. The mammary gland was palpable and slightly tender but there was no nipple discharge. No axillary or J. Neurosurg. / Volume 47 / July, 1977 ]0]
2 O. Kubo, et al. FIG. 1. Early development of the breasts. pubic hair was seen. She had not experienced menarche and no clitoral enlargement was evident. A vaginal smear was not performed. Neurological examination showed bilateral choked discs but no focal neurological deficits. The visual acuity and fields were normal. Laboratory data revealed normal urinalysis, complete blood count, and serum electrolytes. A ventricular puncture performed soon after admission revealed an opening pressure of 400 mm H20, and grossly normal appearance of the cerebrospinal fluid (CSF). The CSF analysis showed protein 142 mg/dl, glucose 70 mg/dl, HCG 2000 ng/ml, and HCB-/3 146 ng/ml. Skull x-ray films showed diastasis of the sutures and erosion of the sella turcica. Right brachial angiogram showed straightening of the anterior cerebral artery, and stretching of the anterior choroidal, lenticulostriate, and thalamoperforating arteries. Dimer-X ventriculogram revealed a filling defect in the anterior floor of the third ventricle outlining the tumor but no abnormalities in the pineal and suprapineal recesses (Fig. 2). A ventriculoperitoneal shunt was performed on the fourth hospital day to relieve progressively increasing intracranial pressure. Operation. A right frontal craniotomy was performed 14 days after admission. A reddish-brown tumor was seen to fill most of the anterior third ventricle. Partial resection of the tumor was carried out by the transventricular approach. Postoperatively the patient was given a course of irradiation, with a total dose of 4350 rads. Breast enlargement had disappeared by the completion of radiotherapy. Histological Study. The surgical tissue was fixed in 10% formalin. The sections were stained with hematoxylin-eosin (H & E), PAS, and Azan. In the routine H & E preparation, the tumor tissue was seen to be composed of two types of cells, epithelioid cells and small cells like lymphocytes (Fig. 3). In the PAS preparation, fine granules were demonstrated in the epithelioid cells. Ectopic pinealoma of the two-cell pattern was diagnosed. Electron Microscopic Study. The specimens were immediately fixed in 2% glutaraldehyde, then fixed in 1% osmium tetroxide solution with phosphate buffer for 2 hours, dehydrated with a graded concentration of ethanol, and finally embedded in Epon 812. The ultrathin sections were stained with uranyl acetate followed by lead citrate. The specimen was examined with a Hitachi lid electron microscope.* The electron micrograph of the tumor cells revealed both clear and dark cells. The most prominent finding was the presence of multiple electron-dense granules in the dark tumor FIG. 2. Dimer-X ventriculogram revealed a filling defect of the anterior third ventricle and no abnormalities of the pineal and suprapineal recesses. *Hitachi I 1D electron microscope manufactured by Niseisangiyo Ltd., 2-Sakuragawa-cho, Shibanishikubo Minato-ku, Tokyo 105, Japan. ]02 J. Neurosurg. / Volume 47 / July, 1977
3 - Centro Pinealoma and precocious puberty cells. They were round, uniform in shape, and measured approximately 500 m# (Fig. 4). Endocrinological Studies. We measured plasma luteinizing hormone (LH) and follicular stimulating hormone (FSH) by radioimmunoassay (RIA) using RIA kitst with a reference standard of 2nd IRP-HMG (International Reference Preparation-Human Menopausal Gonadotropin) (mlu/ml). The plasma HCG was measured by RIA with the RIA kit for HCG,~ expressed as ng/ml (1 mg is equivalent to 6600 IU of the 2nd IS- HCG (International Standard-Human Chorionic Gonadotropin)). The LH and HCG cross reacted nonspecifically with each other and the LH kit measured HCG at about a half of LH and the HCG kit measured LH at about one-third of HCG. We measured the HCG-# subunit by RIA using an antibody against HCG-# subunit, which permits the selective measurement of HCG in the presence of physiologic amounts of LH. The plasma prolactin was measured by RIA with a Friesen No. 2 kit.w We measured plasma estradiol and testosterone by RIA using antisera raised in our laboratory. The tumor contents of gonadotropins were determined by RIA after the extraction of acetonedried tumor tissue with a modification of Hartree's method? The luteinizing hormonereleasing hormone (LH-RH) and thyrotropin releasing hormone (TRH) test was performed by the intravenous administration of 100 ug of LH-RH mixed with 10 izg/kg of TRH. During the test the patient was not allowed any food intake. Blood samples were drawn before and 30, 60, 90, and 120 minutes after the injection. Basal plasma levels of various hormones before and after surgical excision and radiotherapy of the tumor are shown in Table 1. The HCG and HCG-# values were markedly high and LH was also measured to be high FIG. 3. A light microscopic finding of the resected tumor shows a typical two-cell pattern pinealoma. H & E, X 50. before treatment but all of them decreased rapidly immediately after treatment. The basal level of FSH was at the upper limit of normal for age both before and 4 months after treatment. Estradiol was not detectable either before or after treatment. Plasma concentration of cortisol and thyroid hormones were normal. Figure 5 shows the response of HCG, LH, FSH, prolactin, and TSH to the LH-RH and TRH test. The HCG, LH, and FSH response to LH-RH was negative both #Radioimmunoassay kits for FSH manufactured by Daiichi Radioisotope Labs, Ltd., 10-5 Nihonbashi 3-chome, Chuo-ku, Tokyo 103, Japan. :~Radioimmunoassay kit for HCG manufactured by CEA-IRE-SORIN: CEA -- D6partement des Radio616ments, Gif-sur-Yvette, France; IRE- Institut National des Radio616ments, 2400 Mol; SORIN - Ricerche Nucleari, Saluggia (Vercelli), Italy. w No. 2 kit was a gift of the National Institutes of Health, Bethesda, Maryland. FIG. 4. Electron micrograph showing dark and clear cells. In the dark cell, secretory granules (G) with a diameter of about 500 mu were seen. X J. Neurosurg. / Volume 47 / July, 1977 I03
4 O. Kubo, et al. TABLE 1 Basal levels of various hormones before and after treatment* Hormone Normal Before 2 Months after 4 Months after Range Treatment Treatment Treatment HCG (ng/ml) ND LH (miu/ml) FSH (mlu/ml) prolactin (ng/ml) TSH (uu/ml) HGH (ng/ml) estradiol (pg/ml) <20 ND ND -- testosterone (ng/dl) < HCG-/3 (ng/ml) ND *HCG = human chorionic gonadotropin; LH = luteinizing hormone; FSH = follicular stimulating hormone; TSH = thyroid stimulating hormone; HGH = human growth hormone; ND = not detectable. before and after treatment. Prolactin showed a somewhat atypical response with a slightly elevated basal level before treatment, but responded normally with a decreased basal level after treatment. Tumor content of HCG was 400 ng/mg of acetone-dried tissue and FSH was not detectable. Discussion A study of the research on hormoneproducing ectopic tumor in the various organs supports the hypothesis that the precocity was caused by active secreting tumor tissue. 2,4 In 1973, Takakura, et al., 8 J, 60 Ii,'~ "" "~''*'' 4o,b>---'-.. I0 "" ", O ~u/ml ~ "0 min 1 ng/ml min ng/m 0 { ]20 min I00 I0 mlu/ml 6 p 5 ""*"- ~"" mlu/ml. 7 al. o ~ 1 7 6,.m.. ~,,m. I000~ 500 ~ : = ~ 15 ~..., min min FIG. 5. Responses of (left to right) plasma TSH, HGH, and prolactin (top row), and LH, FSH, and HCG (bottom row) to LH-RH and TRH test before and after treatment. Unbroken curve = before treatment; broken curve = after treatment. ]04 J. Neurosurg. / Volume 47 / July, 1977
5 Pinealoma and precocious puberty were the first to demonstrate the occurrence of a gonadotropin-producing ectopic pinealoma by means of tissue culture. Diagnostic criteria of the ectopic hormoneproducing tumor in our case were satisfied by the following points: 1) the demonstration of elevated plasma HCG and the presence of precocious puberty, which was probably due to the increased HCG production; 2) the demonstration of high HCG content in the tumor tissue; 3) disappearance of breast enlargement in accordance with markedly decreased plasma HCG level after the treatment; and 4) demonstration of the secretory granules in the tumor tissue by an electron microscope. It is of academic interest that intracranial HCG-producing tumor is associated with precocious puberty in males but not in females. Mori, et al., 5 speculated that both LH and FSH would not be necessary for precocious sexual development in females, but not in males. Decreased or undetectable levels of plasma FSH have been noted in most of the reports of HCG-producing tumors. It is interesting that, in the present case, the FSH level was compatible with that in normal girls her age. Although Albert 1 demonstrated a considerable FSH action of HCG, the necessity for the coexistence of FSH with HCG for precocious sexual development in female is not now known. According to Wilkins, et al., 7 breast tissue has a lower threshold of response to estrogens than other female sex organs and premature thelarche occurs easily with low levels of estrogens. Plasma estrogens were not detectable in our case. This may reflect the limit of assay sensitivity, therefore a slight and temporary increase in estrogen secretion could not be denied. A main contributing factor for the very rare occurrence of precocious puberty in females may be the very low incidence of two-cell pattern pinealoma in females. Summary An ectopic pinealoma of two-cell pattern producing HCG was demonstrated in a 5- year-old girl who presented precocious puberty and bilateral choked discs. The tumor was localized at the anterior third ventricle and suprasellar region. Plasma basal LH was markedly elevated to 306 miu/ml and HCG was elevated to 1192 ng/ml; HCG-/3 was 75 ng/ml. Provocative test of hypophyseal function revealed low response. Plasma estrogen was not detectable. The HCG content of resected tumor tissue was elevated to 400 ng/mg; however, FSH was not detectable. Histological findings of this tumor showed atypical teratoma, so-called two-cell pattern pinealoma. Electron microscopy revealed two types of cells, dark and clear ceils. Many secretory granules were found in the dark cell. In this case, HCG in plasma, CSF, and tumor tissue was remarkably elevated. In addition, plasma FSH was also elevated to 8.9 mlu/ml. This was the first female case in which HCG-producing ectopic pinealoma was demonstrated in precocious puberty. References 1. Albert A: Follicle-stimulating activity of human chorionic gonadotropin. J Clin Endocrinol 29: , 1969 (Letter) 2. Askanazy M: Teratom und Chorioepitheliom der Zirbel. Verb Dtseh Ges Pathnl 10:58-76, Hartree AS: Separation and partial purification of the protein hormones from human pituitary glands. Biochem J 100: , Kageyama N: Pubertas praecox. Jap J Clin Med 20: , Mori K, Iwayama K, Fujita Y: [Malignant suprasellar teratoma in a girl with elevated serum gonadotropin. Case report and some considerations for development and precocious puberty.] Neurol Surg 2: , 1974 (Jap) 6. Takakura K, Miki Y, Kubo O, et al: [Gonadotropin producing pinealoma.] Saishin Agaku 28: , 1973 (Jap) 7. Wilkins L, Blizzard RM, Migeon C J: The Diagnosis and Treatment of Endocrine Disorders in Childhood and Adolescence, ed. 3. Springfield, I11: Charles C Thomas, 1965, pp This study was supported in part by the 1975 Cancer Research Fund of the Welfare Ministry of Japan. Address reprint requests to: Osami Kubo, M.D., Department of Neurosurgery, Neurological Institute, Tokyo Women's Medical College, 10 Kawada-cho, Shinjuku-ku, Tokyo, Japan. J. Neurosurg. / Volume 47 / July,
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