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Adenoid Cystic Carcinoma of the Ovary.

Eichhorn and Scully[1] first described adenoid cystic carcinoma (ACC) of the ovary in 1995. Although these extremely rare tumors resembled those of salivary ACC, some differences were recorded. They were therefore labeled "adenoid-cystic" or adenoid cysticlike carcinomas. We describe an additional case of ovarian ACC that, in contrast to the cases described in the original study,[1] showed features of myoepithelial differentiation similar to those in the salivary gland ACC.[2]

MATERIALS AND METHODS

The tissue from adnexectomy was fixed in 10% buffered formalin routinely processed, and embedded in paraffin. Sections were stained with hematoxylin-eosin, Alcian blue, Masson's trichrome, van Gieson, and periodic acid-Schiff (PAS) stains. Immunohistochemical studies were performed on paraffin sections using the avidin-biotin complex (ABC) technique. The antibodies used included S100 protein (polyclonal), desmin (D33), carcinoembryonic antigen (polyclonal), chromogranin A, [Alpha]-1-fetoprotein (polyclonal), glial fibrillary acidic protein (GFAP, 6F2), and placental alkaline phosphatase (polyclonal; all from Dakopatts, Glostrup, Denmark); CD34 (QBend 10, Serotec, Washington, DC); pancytokeratin (AE1/AE3, Boehringer, Mannheim, Germany); [Alpha]-smooth muscle actin (1A4, Sigma, St Louis, Mo); muscle-specific actin (HHF-35, Enzo Diagnostic, New York, NY); CD99 (O13, Signet, Dedham, Mass), [Alpha]-inhibin (RI, Serotec, Oxford, England); estrogen receptor (ER1D5, Dakopatts), and progesterone receptor (PR10A9, Immunotech, Marseille, France). Appropriate tissues that stained with the primary antibodies were used as positive controls. Clinical information was obtained from the submitting gynecologist.

REPORT OF A CASE

A 23-year-old nonobese woman (para 0, gravida 0) presented with abdominal pain of 2 weeks' duration. A sonogram showed a left ovarian mass. A salpingo-oophorectomy was performed. At laparotomy, the contralateral ovary and peritoneum were normal. Tumor markers were not determined prior to surgery. Neither chemotherapy nor radiation therapy was administered. The patient is free of recurrence 11 months postoperatively. The 6 x 5 x 4-cm tumor was encapsulated and had a solid cut surface with several 2-mm to 5-mm cystic spaces containing clear fluid.

Histologically, the tumor was composed of nests and sheets of small, uniform cells surrounding multiple round hyaline stromal cylinders or lumens containing mucoid material (Figures 1 and 2). A few lumens had an appearance of true ducts (Figure 2). In some areas, the tumor cells were ovoid to spindle-shaped suggesting possible myoepithelial differentiation (Figure 3). Some lumens were cystic. Focally, small nests and thin cords of tumor cells infiltrated the ovarian stroma without a desmoplastic response. The nuclei were small, round, and hyperchromatic, and lacked nucleoli. Nuclear atypia was mild to moderate. The cytoplasm was scanty and eosinophilic or clear, with clearly visible cell membranes. The average mitotic count was 10 per 10 high-power fields (range, 5 to 16 mitoses per 10 HPF). The PAS and Alcian blue stains produced faint staining of the mucin between the tumor cells, but there was no convincing evidence of epithelial mucin. Immunohistochemically, all tumor cells expressed pancytokeratin AE1/AE3. Approximately one fourth of the tumor cells were positive for S100 protein (Figure 4). Scattered cells expressed GFAP (Figure 5) and CEA. All other antibodies gave negative results.

[Figures 1-5 ILLUSTRATION OMITTED]

COMMENT

Adenoid cystic carcinoma of the ovary was described in 1995 by Eichhorn and Scully.[1] In their series, the tumors differed from the typical salivary gland ACC, containing a component of surface epithelium carcinoma and lacking the myoepithelial differentiation characteristic in salivary gland-type ACC. The authors labeled these neoplasms "adenoid cystic" or adenoid cysticlike carcinomas, and suggested they arose from a surface epithelial origin. Similar ACC-like tumors have been described in the uterine cervix by Ferry and Scully[3]; these tumors also had features that distinguished them from salivary gland ACC (lack of myoepithelial differentiation and, in some cases, neuroendocrine differentiation).[4] Thus, the tumors in both series appear to be variations of common carcinomas that only resemble ACC. However, an ACC of the ovary typical of salivary ACC was subsequently described by Feczko et al.[5] This tumor lacked a surface epithelial carcinoma component and showed myoepithelial differentiation, which was demonstrable ultrastructurally and immunohistochemically. Similarly, our tumor is a pure ACC. It contained myoepithelial cells, which were ovoid to spindle-shaped and showed characteristic immunohistochemical coexpression of cytokeratin, S100 protein, and GFAP.[6,7] Actin, an additional marker of myoepithelial differentiation, was not detected, but may be absent in a substantial subset of salivary gland ACC as well.[8] As in the case we describe, the salivary gland-type ovarian tumor described by Russell et al[9] lacked actin expression, even though myoepithelial differentiation was found by ultrastructural study. These authors explained the discrepancy between their ultrastructural and immunohistochemical results by postulating incomplete myoepithelial differentiation. It is possible that actin negativity along with a high mitotic rate, which is rarely seen in salivary ACCs,[2] may also reflect immaturity of the tumor cells in the case we describe. We cannot determine whether these findings have prognostic significance. Our patient had no recurrence during a limited follow-up period of 11 months, but study of additional similar cases is needed to determine the prognosis.

Although the evidence that ACC-like carcinomas of the ovary are of surface epithelial origin is convincing, the histogenesis of pure ovarian ACC is difficult to explain. The normal ovary lacks epi-myoepithelial structures, which might be considered to be the origin of ACC. There was no evidence in our case of an origin by metaplasia of surface epithelium. An alternative explanation could be a teratomatous origin of these tumors. The young age of our patient supports such a hypothesis. Furthermore, several ovarian neoplasms resembling salivary basal-cell tumors have also been described in young women.[1,9] However, a germ-cell tumor component, which could point to the teratomatous origin of such lesions, was not found in the described cases or in our patient. A third histogenetic possibility for pure ovarian ACC is a sex cord-stromal origin. At the light microscopic level, the cords and cribriform nests of ACC superficially resemble patterns of granulosa cell or other sex cord-stromal-cell tumors. However, the gonadal stromal origin of ACC is improbable, because staining with immunohistochemical markers of sex cord-stromal differentiation, such as inhibin and CD99,[10-13] gave negative results. The epithelial immunophenotype and the absence of hormone receptors are also inconsistent with this origin. Thus, the histogenesis of the present ACC as well as other pure ACCs of the ovary remains unknown.

The differential diagnosis of our case includes metastasis of ACC from another site,[14] primary or metastatic ACC-like carcinoma,[1,3] and a reticular variant of a yolk-sac tumor.[15] Metastasis of ACC from another site could be excluded only after careful clinical examination, which revealed no tumor elsewhere. The so-called ACC-like carcinomas contained surface epithelial-type components and occured in older patients, similar to the patterns of uterine and ovarian carcinomas. The cribriform pattern of the ACC resembles the microcystic-reticular pattern of a yolk-sac tumor and, particularly in a young patient, may cause inclusion of this tumor in the differential diagnosis. In contrast to ACC, the yolk-sac tumor usually contains hyaline globules and immature nuclei, expresses [Alpha]-1-fetoprotein and placental alkaline phosphatase, and lacks myoepithelial differentiation. In summary, we have described an ovarian ACC showing typical features of salivary gland ACC. The lower level of atypia, absence of any Mullerian or surface epithelial carcinoma component, and the presence of myoepithelial differentiation indicate that this tumor differs from the so-called ACC-like carcinoma of the ovary and uterine cervix.

References

[1.] Eichhorn JH, Scully RE. "Adenoid cystic" and basaloid carcinomas of the ovary: evidence for a surface epithelial lineage. A report of 12 cases. Mod Pathol. 1995;8:731-740.

[2.] Ellis GL, Auclair PL. Tumors of the Salivary Glands. Washington, DC: Armed Forces Institute of Pathology; 1996:203-216. Atlas of Tumor Pathology; 3rd series.

[3.] Ferry JA, Scully RE. "Adenoid cystic" carcinoma and adenoid basal carcinoma of the uterine cervix. Am J Surg Pathol. 1998;2:134-144.

[4.] Zamecnik M, Patrikova P, Mirejovsky I, Jakubovsky I. Combined small cell and "adenoid cystic" carcinoma of uterine cervix. Ceskoslovenska Patol. 1992; 28:230-237.

[5.] Feczko JD, Jentz DL, Roth LM. Adenoid cystic ovarian carcinoma compared with other adenoid cystic carcinomas of the female genital tract. Mod Pathol. 1996;9:413-417.

[6.] Dardick I, Stratis M, Parks WR, DeNardi FG, Kahn HJ. S-100 protein antibodies do not label normal salivary gland myoepithelium. Histogenetic implications for salivary gland tumors. Am J Surg Pathol. 1991;138:619-628.

[7.] Gustafsson H, Virtanen I, Thornell LE. Glial fibrillary acidic protein and desmin in salivary neoplasms. Expression of four different types of intermediate filament proteins within the same cell type. Virchows Arch. 1989;57:303-313.

[8.] Morrice WM, Ferreiro JA. Distinction of basaloid squamous cell carcinoma from adenoid cystic and small cell undifferentiated carcinoma by immunohistochemistry. Hum Pathol. 1998;29:609-612.

[9.] Russel P, Wills EJ, Watson G. Monomorphic (basal cell) salivary adenoma of ovary: report of a case. Ultrastruct Pathol. 1995;19:431-438.

[10.] Merchenthaler I, Culler MD, Petrusz P, Negro-Vilar A. Immunocytochemical localization of inhibin in rat and human reproductive tissues. Mol Cell Endocrinol. 1987;54:239-243.

[11.] Zheng W, Sung J, Hanna I, et al. Alpha and beta subunits of inhibin/activin as sex cord-stromal differentiation markers. Int J Gynecol Pathol. 1997;16:263-271.

[12.] Loo KT, Leung AKF, Chan JKC. Immunohistochemical staining of ovarian granulosa cell tumours with MIC2 antibody. Histopathology. 1995;27:388-390.

[13.] Stevenson AJ, Chatten J, Bertoni F, Miettinen M. CD99 ([p30/32.sup.MIC2]) neuroectodermal/Ewing's sarcoma antigen as an immunohistochemical marker: review of more than 600 tumours and the literature experience. Appl Immunohistochem. 1994;2:231-240.

[14.] Longacre TA, O'Hanlan K, Hendrickson MR. Adenoid cystic carcinoma of the submandibular gland with symptomatic ovarian metastases. Int J Gynecol Pathol. 1996;15:349-355.

[15.] Talerman A. Germ cell tumors of the ovary. In: Kurman RJ, ed. Blaustein's Pathology of the Female Genital Tract. 4th ed. New York: Springer-Verlag Inc; 1994:860-870.

Accepted for publication March 1, 2000.

From the Department of Pathology, Slovak Postgraduate Academy of Medicine, Bratislava, Slovak Republic (Dr Zamecnik); the Sikl's Department of Pathology, Faculty Hospital, Pilsen, Czech Republic (Dr Michal); and the Department of Pathology, Ostrava Faculty Hospital, Ostrava, Czech Republic (Dr Curik).

Reprints: Michal Zamecnik, MD, General Hospital, 911 71 Trencin, Slovak Republic (e-mail: zamecnikmichal@hotmail.com).
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Author:Zamecnik, Michal; Michal, Michal; Curik, Romek
Publication:Archives of Pathology & Laboratory Medicine
Date:Oct 1, 2000
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