Malignant transformation in benign cystic teratomas, dermoids of the ovary
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1 European JournalofObstetrics& Gynecology andreproductivebiology, 29 (1988) Elsevier EJO Malignant transformation in benign cystic teratomas, dermoids of the ovary S. Chadha 1 and A. Schaberg 2 1 Department of Pathology, Erasmus University Rotterdam and 2 Ovarian Tumor Committee, Rotterdam, The Netherlands Summary Twenty-four cases with a malignant change involving one of the elements of a benign ovarian dermoid cyst are reported. Squamous cell carcinoma was most frequent. Eighteen patients (75%) were over 50 years of age. The prognosis is rather good if the tumor has not extergled beyond the capsule, 85% surviving without detectable disease after 4 months to 9 years. The prognosis is very poor if the tumor has extended beyond the capsule, over 80% dying within 2 years. Hysterectomy with bilateral salpingo-oophorectomy is the treatment of choice, certainly in older patients. Additional treatment with cytostatics or radiation seems to have little influence on the prognosis. Malignant teratoma; Dermoid of the ovary Introduction Gynecologists are familiar with benign mature cystic teratomas of the ovary, usually called dermoids. The diagnosis is easy to make: an ovoid cyst with a grey external surface containing yellow to brown sebaceous material and hair. Bone, cartilage, brain and adipose tissue may be detectable at first examination. Microscopic examination confirms the diagnosis already made at operation. The cysts appear to be lined by keratinized epidermis with sebaceous glands, sweat glands and hair follicles. Other structures, derived from mesoderm and endoderm may also be present. Over 80% of these tumors, which account for 20% of all ovarian tumors and 30% of those in the benign category occur mainly during the reproductive years. The Correspondence: Dr. S. Chadha, Department of Pathology, Erasmus University, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands /88/$ Elsevier Science Publishers B.V. (Biomedical Division)
2 198 tumor is bilateral in approximately 12% of the cases [1]. Malignant transformation in one of the components is, according to the literature, rare, varying from 1 to 2%. Within recent years the 'Dutch Ovarian Tumor Committee' was confronted with several ovarian dermoids in which one of the components showed malignant transformation. This gave us the opportunity to study the histology of these tumors and especially the relation between the clinical stage and prognosis in this group of patients. Material Among the 1458 registered ovarian tumors there were 24 dermoids with malignant transformation in one of the components. These tumors were staged (FIGO) based on the findings during operations and the results of histological examination. All sections were revised and, if necessary and possible, new sections were made. Examples of solid malignant teratomata and synchronous benign dermoids with separate malignant tumors were not included. Follow-up of these patients varied from 1 ~ month to 9 years. Results The results are given in Table I. All 24 tumors were cystic containing sebaceous material with matted hair and lined by squamous epithelium. In ten cases the tumor had extended beyond the capsule. Histological examination revealed that all cysts had the basic features of a benign cystic teratoma with skin, hair, sebaceous material, fat and connective tissue. In addition, there was a malignant tumor arising from one of the elements. Squamous cell carcinoma was most frequent, occurring in 16 patients. Macroscopically, this presented mostly as a solid area in the wall of the dermoid cyst (Fig. 1). In 13 cases, this solid area varied from 1 to 11 cm. In one case grossly, no localised tumor was visible and in the remaining two the diameter of the solid focus was unknown. Microscopically, the cyst wall was lined by squamous epithelium which showed transition to squamous epithelium with carcinoma in situ (Fig. 2) and to a moderate to poorly differentiated squamous cell carcinoma (Fig. 3). In three cases the dermoid cyst macroscopically showed a yellow-brown solid area (Fig. 4). The diameter of the solid area was 5 cm in one case while this was unknown in the remaining two cases. Microscopically, these were carcinoids with an insular pattern (Fig. 5). Grimelius stain was positive in all the three tumors (Fig. 6). Out of the five cases with adenocarcinoma, one was a dermoid cyst measuring 18 cm with a solid area measuring 7 cm. Microscopically, this was a follicular carcinoma composed of thyroid tissue with foci of compact arrangement of small follicles lined by cuboidal epithelium showing nuclear polymorphism and sporadic mitosis (Fig. 7). Capsular or blood and lymphatic vessel invasion was not present. Thyroid gland and thyroid function tests were normal. The remaining four dermoid cysts revealed adenocarcinoma arising from sldn appendages. In one of these, a solid nodule of 6 cm diameter projected into the lumen of the dermoid cyst. Microscopically this was a well-differentiated adenocar-
3 199 TABLE I Malignancy arising in cystic ovarian teratomas (Dermoid cysts) Patient Age Operative findings Malignant Treatment Stage Follow-up (yrs) elements 1 56 dermoid cyst L 25 cm SCC L BSO, hyst. Ial A & W 4 yrs dermoid cyst R 2 55 dermoid cyst R 13 cm SCC BSO, hyst. IIb A & W 2 yrs in dimeter partial bladder resection, XRT 3 65 dermoid cyst R 35 cm SCC BSO, hyst. III D few months omentectomie 4 45 dermoid cyst L 15 cm SCC BSO, hyst. Ial A with tumor XRT 1 year 5 57 dermoid cyst L 15 cm SCC BSO, hyst. Ial A & W 2 yrs 6 54 dermoid cyst L 3.5 cm SCC BSO, hyst. Ial A & W 9 yrs 7 60 dermoid cyst L 13 cm SCC inoperable III D 2 months 8 71 dermoid cyst L 40 cm SCC BSO, hyst. XRT lal D 1½ yrs 9 56 dermoid cyst R 15 cm SCC BSO, hyst. IV D 2 yrs dermoid cyst L 13 cm SCC excision of III D 1½ yrs tumour, chemotherapy dermoid cyst L 9 cm SCC L BSO, hyst. III D 2 months dermoid cyst R epidermis cyst L 11 cm SCC BSO, hyst, XRT, IV D 4 months chemotherapy dermoid cyst R 30 cm SCC excision of Ial A & W 5 months tumour dermoid cyst L 18 cm SCC BSO, hyst. Ial A & W 5 months dermoid cyst L 25 cm SCC excision of III A & W 4 months tumour, sigmoid resection dermoid cyst L 35 cm SCC L BSO, hyst. Ial A & W 4 months dermoid cyst L 16 cm carcinoid excision of Ial A & W 1 yr tumour dermoid cyst R 28 cm sebaceous BSO Ial no follow-up gland car- available dermoid cyst L 10 cm cinoma adenocar- BSO, hyst. Ia2 A & W 8 yrs cinoma dermoid cyst L 10 cm carcinoid BSO, hyst. Ial A & W 6 months dermoid cyst R adenocar- excision of Ial A & W 6 yrs cinoma tumour dermoid cyst R 14 cm carcinoid BSO Ial A & W 7 yrs
4 200 TABLE I (continued) Patient Age Operative findings Malignant Treatment Stage Follow-up (yrs) elements dermoid cyst R 18 cm follicular BSO, hyst. Ial A & W 5 yrs thyroid carcinoma dermoid cyst L 20 cm adenocar- BSO, hyst. Ia2 D 1 month cinoma A & W, afive and well; BSO, bilateral salpingo-oophorectomy; D, dead; L, left; R, right; XRT, X-ray therapy; hyst., hysterectomy; SCC, squamous cell carcinoma. cinoma composed of sebaceous cells with foamy cytoplasm and undifferentiated cells (Fig. 8). The other three showed poorly differentiated adenocarcinomas also arising from skin appendages. There seems to be a slight preference as to the side, eight were located in the right ovary, 16 in the left ovary, three were bilateral with a malignant component in one ovary. The average age of the patients was 55 years (range years); six were under 50 years of age, 18 were over 50. If we take the patients with a squamous cell carcinoma separately, the average age was 58 years (range years) of whom three were under 50 and 13 were over 50. Fig. 1. Dermoid cyst with solid area in the wall.
5 201 Fig. 2. Same dermoid cyst showing squamous cell carcinoma in situ. Hematoxylin azofloxin, 150. Fig. 3. Moderately differentiated invasive squamous cell carcinoma. Hematoxylin azofloxin, 150.
6 202 Fig. 4. Dermoid cyst with a yellow brown sofid area in the wall. Fig. 5. Same dermoid cyst showing carcinoid tumor with insular pattern. Hematoxylin azofloxin, x 150.
7 203 Fig. 6. Carcinoid tumor showing Grimelius positive granules, 350. Fig. 7. Compact follicular arrangement with moderate nuclear polymorphism. Hematoxylin azofloxin, x 150.
8 204 Fig. 8. Adenocarcinoma composed of sebaceous cells and undifferentiated cells. Hematoxylin azofloxin, 150. Irrespective of the tumor type and the size of the cyst the prognosis was good if the tumor was limited to one ovary, with an intact capsule and without any tumor on the external surface (FIGO stage Ial). From the 14 patients in this stage, 11 are alive without signs of disease after 4 months to 9 years, one died and one is still alive with metastases. In one patient we have no follow-up. If the tumor has extended outside the capsule the prognosis is poor, from the ten patients in this stage only three are alive without disease. From eight patients who died, six received additional radiotherapy and/or chemotherapy. Discussion Malignancy developing in a dermoid cyst has been reported by several authors [2-8]. In the different publications, the frequency of this complication varies from 1 to 2% [1,9] based on all dermoids irrespective of the age of the patient. As our material is highly selective, we can neither deny nor support these figures. However, in this material of the 'Dutch Ovarian Tumor Committee' it is such a frequent observation that we doubt this low percentage. The pathologist has to be aware of the possibility of malignant transformation developing in a benign dermoid cyst. To avoid missing the diagnosis, any thick area in the wall of the dermoid cyst has to be selected and sectioned for histology. Dermoid cysts with malignant transformation is rarely found in young women, over three-fourths of the patients are older than 40, the average age being 50 years
9 [3,7]. The peak incidence of those with a squamous cell carcinoma is even at a higher age [1]. These findings are in accordance with the age of our patients. The average age of our patients is 55 years, 81% is over 50 years. Our series confirms previous reports [3,5,7] that the malignant transformation usually involves one of the epithelial elements, squamous cell carcinoma being the most common (75%) followed by adenocarcinoma; carcinoids come in the third place, while other malignancies are rare. In most cases the histological diagnosis of malignancy is relatively simple after adequate sampling. The presence of benign squamous epithelium in parts of the cyst wall strongly indicates the diagnosis of a dermoid cyst. This study shows that the combination of a dermoid cyst with an epithelial tumor is a real possibility. The prognosis of dermoid cysts complicated by concurring malignancy seems mainly to depend on the stage of the tumor [3,8]. From our stage Ial tumors, 85% is still alive without symptoms after 4 months to 9 years. More advanced stages have a poor prognosis. In our series, only three patients (30%) in stage Ia2, IIb and III were alive after 8 years, 2 years, and 4 months, respectively. Our figures, though small, suggest that chemotherapy and radiation have not much to offer in improving the survival of the patients, as six of the eight patients who died received additional radiotherapy or chemotherapy without effect. From the above facts it may be concluded that malignant transformation in a dermoid has to be taken seriously into account in older women. The pathologist should be aware of this real possibility, should examine an ovarian dermoid cyst carefully macroscopically, and section especially any thickened or solid areas of the tumor. Considering the experience that over 10% of benign dermoids is bilateral, hysterectomy and removal of both ovaries appears to be the treatment of choice, certainly in the older age group. 205 Acknowledgements We wish to thank M. Hanegraaff for typing the manuscript and P. Delfos for technical assistance. References 1 Scully RE. Tumors of the ovary and maldeveloped gonads. Armed Forces Inst Pathol 1979, Washington. 2 Peterson WF. Malignant degeneration of benign cystic teratomas of the ovary. Obstet Gynecol Surv 1957;12: Climie ARW, Heath LP. Malignant degeneration of benign cystic teratomas of the ovary. Cancer 1968;22: Pantoja E, Noy MA, Axtmayer RW, et al. Ovarian dermoids and their complications. Obstet Gynecol Surv 1975;30: Krumerman MS, Chung A. Squarnous carcinoma arising in benign cystic teratoma of the ovary. Cancer 1977;39: Amerigo J, Nogales FF Jr, Fernandez-Sanz J, et al. Squamous cell neoplasms arising from ovarian benign cystic teratoma. Gynecol Oncol 1979;8:
10 206 7 Stamp GWH, McConnell EM. Malignancy arising in cystic teratomas. A report of 24 cases. Br J Obstet Gynaecol 1983;90: Selim MA, Razi A, Lankerani M. Squamous cell carcinoma arising from ovarian benign cystic teratoma. Am J Obstet Gynecol 1984;150: Kelley RR, Scully RE. Cancer developing in dermoid cysts of the ovary. A report of 8 cases including a carcinoid and a leiomyosarcorna. Cancer 1961;14:
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