CASE REPORT
The coexistence of stromomyoma and uterine tumor resembling ovarian sex-cord tumors Report of a case and immunohistochemical study YlLDlZ
ERHAN,MINEBAYGUN AND NECMETTIN OZDEMIR
From the Department of Pathology, Ege University School of Medicine, Izmir, Turkey
Acta Obstet Gynecol Scand 1992; 71: 39&393 The case of a 40-year-old female with a uterine tumor resembling an ovarian sex-cord tumor, located within another neoplastic nodule having the histopathological features of a stromomyoma is reported. Light microscopic examination of the uterine sex-cord-like tumor revealed a highly cellular tumor tissue with no specific differentiation, consisting of solid nests and anastomosing cords and a few pseudo-tubular structures. The vacuoleted cytoplasm of the lipid-rich cells proved vimentin-positive, but desmin- and keratin-negative. The coexistence of the two variants of endometrial stromal tumor was interpreted as arising from endometrial stroma or multipotential uterine mesenchyme that showed a diverse differentiation toward ovarian sex-cord stroma and uterine smooth muscle with interspersed stromal cell clusters.
Key words: endometrial stromal tumor; uterine tumor; ovarian sex-cord-like tumor; stromomyoma Submitted October 2, I991 Accepted December 12, 1991
Uterine neoplasm resembling an ovarian sex-cord tumor and combined muscle-stromal tumor o f the uterus designated as stromomyoma are two extremely rare variants of endometrial stromal tumors. Morehead & Bowman (1) described a case in 1945 and Langley et al. (2) reported a similar case in 1953. Both were interpreted as extraovarian granulosa cell tumors. Uterine neoplasms resembling ovarian sexcord tumors were described by Clement & Scully (3) in 1976 in a report of 14 cases, which they divided into two groups on the basis of clinical and histological features. We have examined a uterine tumor that vaguely resembled an ovarian sex-cord tumor, which was located within a stromomyoma. Since there was no distinguishable pattern, the case was not categorized
Actu Obstet Gynecol Scand 71 (1992)
into either of the two groups described by Clement & Scully.
Report of a case A 40-year-old female who complained of abdominal pain and a delay in her menstrual period of lY2 months was found at physical examination to have a pelvic mass. A fractional curettage was performed. Examination of the specimens by our pathology laboratory led to a diagnosis of non-specific chronic cervicitis and secretory endometrium. A week later, the patient underwent total abdominal hysterectomy and bilateral salpingo-oophorectomy under the preoperative diagnosis of leiomyoma of the uterus.
Stromomyoma and sex-cord-like tumor
391
Light microscopic appearance
Fig. 1. An area of smooth muscle differentiation with anastomosing and whorled fascicles of fusiform cells and focal hyalinization in a starburst pattern, merged in between endometrial stromal cells (hematoxylin-eosin, original magnification x 110).
Gross pathologic findings The uterus measured 14 X 9 X 8 cm. The fundus was distorted by a well-circumscribed intramural nodule, 9 cm in diameter. The nodule was rubbery, firm, bulging above the surrounding myometrium. It had a solid and white cut surface, and a whorled trabecular pattern, often alternating with white to tan granular areas. Dark red discoloration representing hemorrhage was noted. There was another well-circumscribed spherical mass with a diameter of 5 cm located within this nodule, characterized by a softer consistency, yellowish orange color, and a smooth glistening cut surface, helping to distinguish it macroscopically from the enveloping mass.
The sections were stained with hematoxylin-eosin, reticulin, Masson’s trichrome, and Van Gieson stains. Frozen sections were cut with a cryostat and stained for lipids with Oil Red 0. The histological examination performed on the sections prepared from the predominant nodule revealed a highly cellular tumor tissue, rich in blood vessels. The cells resembling normal endometrial stroma were arranged in a whorling pattern around fine blood vessels which displayed an apparently endothelial cell proliferation. In other areas, they formed large irregular sheets. There was no nuclear atypia and the cells were uniform in shape, dimensions and staining quality. The nuclei were oval or spindly and the cytoplasm was acidophilic with indistinct borders. There was very little mitotic activity (less than one per ten high-power fields) and a heavy mast cell infiltration of the stroma. A definite and diffuse smooth muscle differentiation with anastomosing and whorled fascicles of fusiform cells and focal hyalinization in a starburst pattern was merged in between these cells, as seen in Fig. 1. This nodular mass, designated as stromomyoma, showed expanding and non-infiltrative margins with compression of the neighboring myometrium. Examination of the yellowish orange nodule identified grossly within the aforementioned lesion revealed an apparently more cellular tumor tissue with prominent intracytoplasmic Oil Red 0-positive lipid droplets (Fig. 2A). In many areas the tumor cells formed solid clumps and anastomosing cords with occasional pseudo-tubule formations (Fig. 2B). A fibromatous component displayed a radiating pattern separating islands of cells in some areas. These
Fig. 2. (A) Intracytoplasmic lipid droplets were verified in the uterine tumor resembling ovarian sex-cord tumors (Oil Red 0 , original magnification ~ 2 2 0 ) . (B) The tumor cells forming solid nests and anastomosing cords with occasional pseudo-tubule formations (hematoxylin-eosin, original magnification x 110). 21
Acfa Obsrer Gynecol Scand 71 (lYY2)
392
Y . Erhan et al.
cells were small and had a vacuolated or clear cytoplasm, round and vesicular nuclei with inconspicuous nucleoli. Mitoses were not found. In the reticulin-stained material, the individual cells were surrounded by a thin reticulin network. In some areas, clusters of polygonal cells, resembling luteinized ovarian stromal cells or endometrial foam cells with abundant clear or foamy cytoplasm, were identified. No Reinke crystalloids or Call-Exner bodies were noted anywhere in the lesion. This tumor was distinguished from the main mass of stromomyoma and was diagnosed as a uterine tumor resembling an ovarian sex-cord tumor composed of lipid-laden cells.
Irnmunohistochemical findings A panel of monoclonal antibodies consisting of keratin, vimentin and desmin (obtained from Dakopatts A/S) were performed on paraffin sections of both nodules by the peroxidase-antiperoxidase method. Examination of the multiple sections of stromomyoma revealed focal desmin positivity, while the sections of the uterine tumor resembling an ovarian sex-cord tumor were desmin- and keratin-negative, but vimentin-positive. The intracytoplasmic vimentin staining was light and diffuse.
Discussion Some uterine tumors may bear a close resemblance to gonadal stroma, as the ovary and uterus are both derived from coelomic epithelium and mesenchyme. Uterine tumors resembling ovarian sex-cord tumors have been described both with and without associated endometrial stromal tumors, but not with leiomyomata (4). The case reported was deemed to be a stromomyoma containing a uterine tumor resembling an ovarian sex-cord tumor, both of which are classified as variants of endometrial stromal tumors (5). Although of uncertain histogenesis, stromomyomas and uterine tumors resembling ovarian sex-cord tumors, especially those with associated endometrial stromal tumors, are both believed to have originated from the endometrial stromal cell possibly located in foci of adenomyosis or stromal myosis within the myometrium, or from the multipotential uterine mesenchyme (4, 6, 7). There is another view that regards these tumors as originating from misplaced ovarian tissue within the myometrium, which is logical in view of reports of extra-ovarian sex-cord tumors in the adrenal gland, broad ligament and retroperitoneum (8, 9, 10). Simultaneous occurrence of stromomyoma and Acta Ohstet Gynecol Scand 71 (1992)
uterine tumor resembling ovarian sex-cord tumors has not been reported previously, although one electron-microscopic study has raised the possibility of uterine tumors resembling ovarian sex-cord tumors being actually stromomyomas (7). According to Clement & Scully ( 3 ) , sex-cord-like uterine tumors are divided into two groups. Group I tumors are endometrial stromal tumors showing focal epitheliallike differentiation resembling sex-cord tumors and recurred frequently. Group I1 tumors demonstrate a diffuse or predominant tubular pattern more closely resembling that of ovarian sex-cord tumors and behaving in a benign fashion. The diagnosis of a granulosa cell tumor as to specify the sex-cord elements is debatable in our case because of the absence of Call-Exner bodies and the characteristic nuclear grooves. There was a prominent reticulin network surrounding each cell. The cells contained intracytoplasmic lipid droplets, but there was n o true lumen formation and no distinctive differentiation toward a Sertoli-Leydig cell tumor. There are two possibilities for the sex-cord-like elements of this case, first being a thecoma, and the second a poorly differentiated Sertoli-Leydig cell tumor, which can be classified as Group I tumors of Clement & Scully. In conclusion we should stress the fact that there was no transition between stromomyoma and uterine tumor resembling ovarian sex-cord tumors in the case presented and the tumors had distinct margins which may represent diverse differentiation of the same multipotential cell line forming two nodular neoplasms.
References 1. Morehead RP, Bowman MC. Heterologous mesenchyma1 tumors of the uterus. Report of a neoplasm resembling a granulosa cell tumor. Am J Pathol 1945; 21: 5341. 2. Langley FA, Smith JP, Woodcock AS. Debatable uterine tumors. Acta Obstet Gynecol Scand 1953; 32: 143-69. 3. Clement PB, Scully RF. Uterine tumors resembling ovarian sex-cord tumors. A clinicopathologic analysis of fourteen cases. Am J Clin Pathol 1976; 66: 512-25. 4. Hirschfield L, Kahn LB, Chen S , Winkler B, Rosenberg S. Mhllerian adenosarcorna with ovarian sex cordlike differentiation: A light- and electron-microscopic study. Cancer 1986; 57: 1197-200. 5 . Norris HJ, Zaloudek CJ. Mescnchymal tumors of the uterus. In: Blaustein A , ed. Pathology of the Female Genital Tract. New York: Springer-Verlag, 1982; 352-92. 6. Kantelip B , Cloup N, Dechelotte P. Uterine tumor resembling ovarian sex cord tumors: Report of a casc with ultrastructural study. Hum Pathol 1986; 17: 9 1 4 .
Stromomyoma and sex-cord-like tumor 7. Tang C-K, Toker C, Ances IG. Stromomyoma of the uterus. Cancer 1979; 43: 308-16. 8. Orselli RC, Bussler TJ. Thcca granulosa cell tumor arising in adrenal gland. Cancer 1973; 31: 474-7. 9. Ragins AB, Frankel L. lntraligamentous granulosa cell tumor. Am J Obstet Gynecol 1940; 40: 302-6. 10. Voight WW. Primary giant granulosa cell tumor of retroperitoneal origin with development into the mesosigmoideurn Am J Obstet Gynecol 1948; 36: 6 8 W 3 .
393
Address for correspondence:
Prof. Dr. Yildiz Erhan Ege Tip Fakirltesi
oniversitesi
Patoloji Anabilim Dali Bornova Izmir 35100 Turkey
Acta Obstet Gynecol %and 71 (lYY2)
The coexistence of stromomyoma and uterine tumor resembling ovarian sex-cord tumors Report of a case and immunohistochemical study YlLDlZ
ERHAN,MINEBAYGUN AND NECMETTIN OZDEMIR
From the Department of Pathology, Ege University School of Medicine, Izmir, Turkey
Acta Obstet Gynecol Scand 1992; 71: 39&393 The case of a 40-year-old female with a uterine tumor resembling an ovarian sex-cord tumor, located within another neoplastic nodule having the histopathological features of a stromomyoma is reported. Light microscopic examination of the uterine sex-cord-like tumor revealed a highly cellular tumor tissue with no specific differentiation, consisting of solid nests and anastomosing cords and a few pseudo-tubular structures. The vacuoleted cytoplasm of the lipid-rich cells proved vimentin-positive, but desmin- and keratin-negative. The coexistence of the two variants of endometrial stromal tumor was interpreted as arising from endometrial stroma or multipotential uterine mesenchyme that showed a diverse differentiation toward ovarian sex-cord stroma and uterine smooth muscle with interspersed stromal cell clusters.
Key words: endometrial stromal tumor; uterine tumor; ovarian sex-cord-like tumor; stromomyoma Submitted October 2, I991 Accepted December 12, 1991
Uterine neoplasm resembling an ovarian sex-cord tumor and combined muscle-stromal tumor o f the uterus designated as stromomyoma are two extremely rare variants of endometrial stromal tumors. Morehead & Bowman (1) described a case in 1945 and Langley et al. (2) reported a similar case in 1953. Both were interpreted as extraovarian granulosa cell tumors. Uterine neoplasms resembling ovarian sexcord tumors were described by Clement & Scully (3) in 1976 in a report of 14 cases, which they divided into two groups on the basis of clinical and histological features. We have examined a uterine tumor that vaguely resembled an ovarian sex-cord tumor, which was located within a stromomyoma. Since there was no distinguishable pattern, the case was not categorized
Actu Obstet Gynecol Scand 71 (1992)
into either of the two groups described by Clement & Scully.
Report of a case A 40-year-old female who complained of abdominal pain and a delay in her menstrual period of lY2 months was found at physical examination to have a pelvic mass. A fractional curettage was performed. Examination of the specimens by our pathology laboratory led to a diagnosis of non-specific chronic cervicitis and secretory endometrium. A week later, the patient underwent total abdominal hysterectomy and bilateral salpingo-oophorectomy under the preoperative diagnosis of leiomyoma of the uterus.
Stromomyoma and sex-cord-like tumor
391
Light microscopic appearance
Fig. 1. An area of smooth muscle differentiation with anastomosing and whorled fascicles of fusiform cells and focal hyalinization in a starburst pattern, merged in between endometrial stromal cells (hematoxylin-eosin, original magnification x 110).
Gross pathologic findings The uterus measured 14 X 9 X 8 cm. The fundus was distorted by a well-circumscribed intramural nodule, 9 cm in diameter. The nodule was rubbery, firm, bulging above the surrounding myometrium. It had a solid and white cut surface, and a whorled trabecular pattern, often alternating with white to tan granular areas. Dark red discoloration representing hemorrhage was noted. There was another well-circumscribed spherical mass with a diameter of 5 cm located within this nodule, characterized by a softer consistency, yellowish orange color, and a smooth glistening cut surface, helping to distinguish it macroscopically from the enveloping mass.
The sections were stained with hematoxylin-eosin, reticulin, Masson’s trichrome, and Van Gieson stains. Frozen sections were cut with a cryostat and stained for lipids with Oil Red 0. The histological examination performed on the sections prepared from the predominant nodule revealed a highly cellular tumor tissue, rich in blood vessels. The cells resembling normal endometrial stroma were arranged in a whorling pattern around fine blood vessels which displayed an apparently endothelial cell proliferation. In other areas, they formed large irregular sheets. There was no nuclear atypia and the cells were uniform in shape, dimensions and staining quality. The nuclei were oval or spindly and the cytoplasm was acidophilic with indistinct borders. There was very little mitotic activity (less than one per ten high-power fields) and a heavy mast cell infiltration of the stroma. A definite and diffuse smooth muscle differentiation with anastomosing and whorled fascicles of fusiform cells and focal hyalinization in a starburst pattern was merged in between these cells, as seen in Fig. 1. This nodular mass, designated as stromomyoma, showed expanding and non-infiltrative margins with compression of the neighboring myometrium. Examination of the yellowish orange nodule identified grossly within the aforementioned lesion revealed an apparently more cellular tumor tissue with prominent intracytoplasmic Oil Red 0-positive lipid droplets (Fig. 2A). In many areas the tumor cells formed solid clumps and anastomosing cords with occasional pseudo-tubule formations (Fig. 2B). A fibromatous component displayed a radiating pattern separating islands of cells in some areas. These
Fig. 2. (A) Intracytoplasmic lipid droplets were verified in the uterine tumor resembling ovarian sex-cord tumors (Oil Red 0 , original magnification ~ 2 2 0 ) . (B) The tumor cells forming solid nests and anastomosing cords with occasional pseudo-tubule formations (hematoxylin-eosin, original magnification x 110). 21
Acfa Obsrer Gynecol Scand 71 (lYY2)
392
Y . Erhan et al.
cells were small and had a vacuolated or clear cytoplasm, round and vesicular nuclei with inconspicuous nucleoli. Mitoses were not found. In the reticulin-stained material, the individual cells were surrounded by a thin reticulin network. In some areas, clusters of polygonal cells, resembling luteinized ovarian stromal cells or endometrial foam cells with abundant clear or foamy cytoplasm, were identified. No Reinke crystalloids or Call-Exner bodies were noted anywhere in the lesion. This tumor was distinguished from the main mass of stromomyoma and was diagnosed as a uterine tumor resembling an ovarian sex-cord tumor composed of lipid-laden cells.
Irnmunohistochemical findings A panel of monoclonal antibodies consisting of keratin, vimentin and desmin (obtained from Dakopatts A/S) were performed on paraffin sections of both nodules by the peroxidase-antiperoxidase method. Examination of the multiple sections of stromomyoma revealed focal desmin positivity, while the sections of the uterine tumor resembling an ovarian sex-cord tumor were desmin- and keratin-negative, but vimentin-positive. The intracytoplasmic vimentin staining was light and diffuse.
Discussion Some uterine tumors may bear a close resemblance to gonadal stroma, as the ovary and uterus are both derived from coelomic epithelium and mesenchyme. Uterine tumors resembling ovarian sex-cord tumors have been described both with and without associated endometrial stromal tumors, but not with leiomyomata (4). The case reported was deemed to be a stromomyoma containing a uterine tumor resembling an ovarian sex-cord tumor, both of which are classified as variants of endometrial stromal tumors (5). Although of uncertain histogenesis, stromomyomas and uterine tumors resembling ovarian sex-cord tumors, especially those with associated endometrial stromal tumors, are both believed to have originated from the endometrial stromal cell possibly located in foci of adenomyosis or stromal myosis within the myometrium, or from the multipotential uterine mesenchyme (4, 6, 7). There is another view that regards these tumors as originating from misplaced ovarian tissue within the myometrium, which is logical in view of reports of extra-ovarian sex-cord tumors in the adrenal gland, broad ligament and retroperitoneum (8, 9, 10). Simultaneous occurrence of stromomyoma and Acta Ohstet Gynecol Scand 71 (1992)
uterine tumor resembling ovarian sex-cord tumors has not been reported previously, although one electron-microscopic study has raised the possibility of uterine tumors resembling ovarian sex-cord tumors being actually stromomyomas (7). According to Clement & Scully ( 3 ) , sex-cord-like uterine tumors are divided into two groups. Group I tumors are endometrial stromal tumors showing focal epitheliallike differentiation resembling sex-cord tumors and recurred frequently. Group I1 tumors demonstrate a diffuse or predominant tubular pattern more closely resembling that of ovarian sex-cord tumors and behaving in a benign fashion. The diagnosis of a granulosa cell tumor as to specify the sex-cord elements is debatable in our case because of the absence of Call-Exner bodies and the characteristic nuclear grooves. There was a prominent reticulin network surrounding each cell. The cells contained intracytoplasmic lipid droplets, but there was n o true lumen formation and no distinctive differentiation toward a Sertoli-Leydig cell tumor. There are two possibilities for the sex-cord-like elements of this case, first being a thecoma, and the second a poorly differentiated Sertoli-Leydig cell tumor, which can be classified as Group I tumors of Clement & Scully. In conclusion we should stress the fact that there was no transition between stromomyoma and uterine tumor resembling ovarian sex-cord tumors in the case presented and the tumors had distinct margins which may represent diverse differentiation of the same multipotential cell line forming two nodular neoplasms.
References 1. Morehead RP, Bowman MC. Heterologous mesenchyma1 tumors of the uterus. Report of a neoplasm resembling a granulosa cell tumor. Am J Pathol 1945; 21: 5341. 2. Langley FA, Smith JP, Woodcock AS. Debatable uterine tumors. Acta Obstet Gynecol Scand 1953; 32: 143-69. 3. Clement PB, Scully RF. Uterine tumors resembling ovarian sex-cord tumors. A clinicopathologic analysis of fourteen cases. Am J Clin Pathol 1976; 66: 512-25. 4. Hirschfield L, Kahn LB, Chen S , Winkler B, Rosenberg S. Mhllerian adenosarcorna with ovarian sex cordlike differentiation: A light- and electron-microscopic study. Cancer 1986; 57: 1197-200. 5 . Norris HJ, Zaloudek CJ. Mescnchymal tumors of the uterus. In: Blaustein A , ed. Pathology of the Female Genital Tract. New York: Springer-Verlag, 1982; 352-92. 6. Kantelip B , Cloup N, Dechelotte P. Uterine tumor resembling ovarian sex cord tumors: Report of a casc with ultrastructural study. Hum Pathol 1986; 17: 9 1 4 .
Stromomyoma and sex-cord-like tumor 7. Tang C-K, Toker C, Ances IG. Stromomyoma of the uterus. Cancer 1979; 43: 308-16. 8. Orselli RC, Bussler TJ. Thcca granulosa cell tumor arising in adrenal gland. Cancer 1973; 31: 474-7. 9. Ragins AB, Frankel L. lntraligamentous granulosa cell tumor. Am J Obstet Gynecol 1940; 40: 302-6. 10. Voight WW. Primary giant granulosa cell tumor of retroperitoneal origin with development into the mesosigmoideurn Am J Obstet Gynecol 1948; 36: 6 8 W 3 .
393
Address for correspondence:
Prof. Dr. Yildiz Erhan Ege Tip Fakirltesi
oniversitesi
Patoloji Anabilim Dali Bornova Izmir 35100 Turkey
Acta Obstet Gynecol %and 71 (lYY2)
