Struma ovarii is a neoplasm characterized by thyroid tissue in the ovary as the predominant component in a benign cystic teratoma, or a benign teratoma in.
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Annals of Clinical & Laboratory Science, vol. 34, no. 1, 2004
Case Report: Malignant Struma Ovarii Maria D. Navarro,1 Mary Aldrene L. Tan,1 John L. Lovecchio,2 and Steven I. Hajdu 1 Departments of Pathology1 and Gynecologic Oncology,2 North Shore University Hospital, Manhasset, New York Abstract. Struma ovarii are specialized teratomas consisting of thyroid tissue with various microscopic features, ranging from benign to malignant. We report a rare form of malignant struma ovarii, composed exclusively of a follicular variant of papillary thyroid carcinoma with capsular invasion, which occurred in a 65-yr-old woman. (received 2 July 2003; accepted 3 October 2003) Keywords: malignant struma ovarii, malignant ovarian tumor, follicular variant of papillary thyroid carcinoma Introduction Struma ovarii is a neoplasm characterized by thyroid tissue in the ovary as the predominant component in a benign cystic teratoma, or a benign teratoma in which only thyroid tissue has developed [1]. It has a peak incidence in the fifth decade of life and often involves the left ovary [1,2]. Although 5 - 15 % of benign ovarian teratomas contain some thyroid tissue, only 2% are composed exclusively of struma ovarii [3]. Malignant transformation of struma ovarii is uncommon, with reported rates ranging from 537% [2]. The rarity of the tumor, lack of universally accepted histologic criteria for malignancy, and protracted clinical course contribute to discrepancies in the reported cases. Presented here is a case in which an unusual malignant transformation with capsular invasion occurred in a pure struma ovarii. Case Report A 65-yr-old woman was found to have a pelvic mass that was discovered during an evaluation of postmenopausal bleeding. She was admitted to the hospital for an exploratory laparotomy, total abdominal hysterectomy, bilateral salpingoAddress correspondence to Maria D. Navarro, M.D., Department of Pathology, North Shore University Hospital, Manhasset, New York, 11030, USA; te1 516 562 4184; fax 516 562 4591.
oophorectomy, and possible staging. Her medical history included essential hypertension for 10 yr, diverticulosis, repair of recto-vaginal fistula postdelivery, cholelithiasis, tonsillectomy, and adenoidectomy as a child. There was no history of smoking or alcohol consumption. Pre-operative studies included an abdominal computed tomographic scan, performed 2 weeks before admission, which showed a complex left adnexal mass, 7 cm in diameter. A pelvic sonogram showed an enlarged left ovary, 7 x 6 x 5 cm, with cystic components, septations, and no calcification or free fluid. The uterus and right ovary appeared to be normal. Laboratory studies included a normal complete blood count. The serum potassium was slightly low, 3.0 mmoI/L, and for this she received supplemental potassium. The electrocardiogram showed a sinus rhythm with a nonspecific ST and T wave abnormality. She underwent an exploratory laparotomy, and a total abdominal hysterectomy with bilateral salpingooophorectomy. The intraoperative pathologic diagnosis was “favor struma ovarii,” based on frozen section examination of the left ovary . Grossly, the left ovary weighed 106 g and measured 7 x 6 x 4 cm; cut sections of the ovary showed multiple cysts, which contained clear brown fluid, with a multilobated, soft, brown, solid, inner lining. The fallopian tube measured 6 x 0.5 cm; cut surfaces of the fallopian tube were unremarkable.
0091-7370/04/0100-0107, $1.50. © 2004 by the Association of Clinical Scientists, Inc.
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Fig. 1. Malignant struma ovarii showing follicular variant of papillary thyroid carcinoma with solid backto-back arrangement of follicles mostly devoid of colloid and varying in size, with macrofollicular areas (H&E, x200).
Fig. 2. Follicular variant of papillary thyroid carcinoma, exhibiting clear nuclei, prominent nucleoli, occasional nuclear grooves, and follicles with scalloping (H&E, x400).
Malignant struma ovarii 109
Fig. 3. Follicular neoplasm showing infiltration of the capsule (H&E, x400).
The histologic sections showed a partly encapsulated neoplasm composed of small to mostly medium or rarely larger follicles, filled with homogenous, pale to strongly eosinophilic colloid with focally scalloped configuration. Follicular lining cells of approximately 50-70% of the tumor had characteristic vesicular nuclei with occasional grooves. A follicular variant of papillary carcinoma of thyroid with capsular invasion was favored. The whole tumor was embedded for microscopic examination. Practically the entire tumor was composed of carcinoma without identifiable benign thyroid tissue (struma ovarii) or other teratoid elements (Figs. 1-3). Vascular invasion was not evident. The diagnosis was subsequently confirmed by examination at Memorial Sloan Kettering Cancer Center (Reuter, V, personal communication). The right ovary measured 2.0 x 1.5 cm and showed simple cysts and corpora albicantia; the right fallopian tube was unremarkable. The uterus weighed 43 g and showed an inactive endometrium, but was otherwise unremarkable. The post-operative course was uneventful and the patient was discharged from the hospital 4 days after surgery. Shortly after discharge, she had a complete clinical, radiologic, and laboratory
evaluation. The results of all examinations and laboratory studies, including thyroid tests, were within the normal ranges. Since surgery 6 months ago, the patient has been closely followed by her oncologist without additional treatment. Discussion The presence of thyroid tissue in the ovary was first described by Böttlin in 1889 and the term “struma ovarii colloides” was coined by Meyer in 1903 [4]. Since then the entire spectrum of thyroid pathology, including nontoxic nodular goiter, toxic goiter, Hashimoto’s thyroiditis, nonspecific thyroiditis, adenomas, and carcinomas has been described [1]. Struma ovarii, as in our case, is more often found to involve the left ovary. Malignant transformation of struma ovarii is very rare. Malignancy arises more often in a nest of benign thyroid tissue within a benign cystic teratoma than in struma ovarii [5]. As listed in Table 1, our review of the literature has identified reports of 16 papillary carcinomas [1,59], 10 follicular carcinomas [8,10-14], 5 combined papillary and follicular carcinomas [11,13,15-17], and 4 follicular variants of papillary carcinoma [2,18,19].
110 Annals of Clinical & Laboratory Science Table 1. Tabulation of reported cases of malignant struma ovarii. Age (yr) Size (cm)
Type of carcinoma
Teratomatous elements
Authors and references
33
6
papillary
yes
Gould et al [1]
28 39
11 -
follicular variant of papillary follicular variant of papillary
yes yes
Dardik et al [2]
42
12
malignant struma ovarii
yes
Checrallah et al [3]
30
15
papillary
yes
Yannopoulos et al [5]
37
11
papillary
yes
Rosenblum et al [6]
32
5.5
papillary
yes
Berghella et al [7]
3-77
5-18
11 papillary 2 follicular
69% yes
Devaney et al [8]
80
7
papillary
yes
Hemli et al [9]
72
18
follicular
yes
de Graaff et al [10]
52 30
20 13
follicular mixed follicular and papillary
yes yes
Zakhem et al [11]
47
7
follicular
no
Bhansali et al [12]
44 52 36 38 62
29 60 9 14 16
follicular follicular follicular follicular mixed follicular and papillary
yes -
Woodruff et al [13]
35
9 (right)
-
O’Connell et al [14]
35
15
adenocarcinoma with follicular and papillary elements follicular
no
57
“grapefruit”
mixed follicular and papillary
-
Zbranca et al [15]
60
17 (right) 6 (left)
mixed follicular and papillary
-
Pardp-Mindan et al [16]
42
8
mixed papillary and follicular
yes
Rose et al [17]
38
9
follicular variant of papillary
yes
Kostoglou-Athanassiou et al [18]
67
10
follicular variant of papillary
-
Ribeiro-Silva et al [19]
48
16
pure stroma ovarii without malignant features & pelvic follicular variant of papillary ca
no
Vadmal et al [20]
47 72 53
8 8 12
malignant stroma ovarii malignant stroma ovarii suspect malignant stroma ovarii
yes yes
Nieminen et al [22]
28
5
suggestive malignant stroma ovarii yes
Tokuda et al [23]
Malignant struma ovarii
Our case is an extremely rare form of ovarian tumor. It is the fifth reported case of follicular variant of papillary thyroid carcinoma and is the first instance in which close to 100% of the struma ovarii exhibits cytologic features of carcinoma. In addition, the neoplasm in out case shows capsular invasion, which has been reported in only 5 cases of papillary and follicular carcinoma and 1 case of pure struma ovarii; capsular invasion has not previously been described in the follicular variant of papillary carcinoma [2,5,8,12,14,18,19-22]. There is disagreement about the criteria for the diagnosis of malignant transformation within a struma ovarii. Pardo-Mindan et al [16] noted that nuclear alterations alone are insufficient diagnostic criteria, since atypical cells are frequent in noncancerous lesions. In addition, for the diagnosis of malignancy, Pardo-Mindan et al required the presence of invasion of the capsule or a peritoneal implant. The presence or absence of capsular or vascular invasion is difficult to evaluate in the ovary, since the thyroid tissue microscopically often does not form a discrete nodule, is not encapsulated in the usual fashion, and is sometimes associated with thick connective tissue septa into which the struma is embedded. These features make the evaluation of capsular invasion in struma ovarii difficult and capsular invasion cannot be used as a criterion for separating benign from malignant lesions. Many authors believe that the diagnosis of malignancy can be made on the basis of cellularity, cellular atypia, and mitotic activity, although blood vessel invasion has been mentioned as the most reliable criterion [1]. As quoted by deGraaf et al [10], Fox and Langley opined that a sufficient degree of cellular pleomorphism, cytologic atypia, and mitotic activity are acceptable as signs of malignancy. From our institution, Vadmal et al [20] reported a case of benign struma ovarii without evidence of malignant features at oophorectomy. Six years after the oophorectomy, there were pelvic recurrences and metastases to the liver and retroperitoneum. Microscopically, the neoplastic nodules in the tumor ranged from benign appearing thyroid tissue to lowgrade complex papillary and follicular carcinoma. Recurrences reported in the literature have occurred in the omentum, peritoneum, contralateral ovary,
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liver, spleen, lungs, pleura, inguinal lymph nodes, skin, and, in one instance, the cranial vault [23]. It is notable that, even with recurrences and metastases, only 1 patient is reported to have died; the death 3 yr post-diagnosis and was attributed to pneumonia and cardiovascular insufficiency [16]. Follow-up in reported cases has ranged from a few mo to 27 yr. The prognosis of malignant struma ovarii is difficult to predict, because of the scarcity of cases and the long intervals before recurrences and metastases occur [5]. Thus, patients with malignant struma ovarii should be managed with caution; they require long-term follow-up with a “wait and see” attitude. References 1.
Gould SF, Lopez RL, Speers WC. Malignant struma ovarii. A case report and literature review. J Reprod Med 1983;28:415-419. 2. Dardik RB, Dardik M, Westra W, Montz FJ. Malignant struma ovarii. Two case reports and a review of the literature. Gyn Onc 1999;73:447-451. 3. Checrallah A, Medlej R, Saade C, Khayat G, Halaby G. Malignant struma ovarii, an unusual presentation. Thyroid 2001;11:889-892. 4. Soto Moreno A, Venegas EM, Rodriguez JR, Sanchez F, Robles MJ, Martinez MA, Gonzalez D, Navarro E, Astorga R. Thyroid carcinoma on an ovarian teratoma: a case report and review of the literature. Gynecol Endocrinol 2002; 16:207-211. 5. Yannopoulos D, Yannopoulos K, Ossowski R. Malignant struma ovarii. Pathol Annual 1976;11:403-413. 6. Rosenblum NG, LiVolsi VA, Edmonds PR, Mikuta J. Malignant struma ovarii. Gyn Onc 1989;32:224-227. 7. Berghella V, Ngadiman S, Rosenberg H, Hoda S, Zuna RE. Malignant struma ovarii. A case report and review of the literature. Gynecol Obstet Invest 1997;43:68-72. 8. Devaney K, Snyder R, Norris HJ, Tavassoli FA. Proliferative and histologically malignant stuma ovarii. a clinicopathologic study of 54 cases. Int J Gynecol Pathol 1993; 12:333-343. 9. Hemli JM, Barakate MS, Appleberg M, Delbridge LW. Papillary carcinoma of the thyroid arising in struma ovariireport of a case and review of management guidelines. Gynecol Endocrinol 2001;15:243-247. 10. de Graaff J, van Vliet MA, Miseree J. Malignant struma ovarii. Eur J Ostet Gynecol Reprod Biol 1983;16:31-35. 11. Zakhem A, Aftimos G, Kreidy R, Salem P. Malignant struma ovarii: a report of two cases and selected review of the literature. J Surg Oncol 1990;43:61-65. 12. Bhansali A, Jain V, Rajwanshi A, Lohda S, Dash RJ. Follicular carcinoma in a functioning struma ovarii. Postgrad Med J 1999;75:617-618.
112 Annals of Clinical & Laboratory Science 13. Woodruff JD, Rauh T, Markley RL. Ovarian struma. Obstet Gynecol 1966;27:194-201. 14. O’Connell MEA, Fisher C, Harmer CL. Malignant struma ovarii presentation and management. Br J Radiol 1990;63:360-363. 15. Zbranca E, Ciubotaru CC, Cotrutz C, Rusu M, Damaschin V, Dbrescu G. Malignant struma ovarii, diagnosed post menopause. Rev Med Chir Soc Med Nat Iasi 1984; 88:733-736. 16. Pardo-Mindan FJ, Vazquez JJ. Malignant struma ovarii. Light and electron microscopic study. Cancer 1983;51: 337-343. 17. Rose PG, Arafah B, Abdul-Karim FW. Case report. Malignant struma ovarii: Recurrence and response to treatment monitored by thyroglobulin levels. Gyn Onc 1998;70:425-427. 18. Kostoglou-Athanassiou I, Lekka-Katsouli, Gogou L, Papagrigoriou L, Chatonides I, Kaldrymides P. Malignant
19.
20.
21.
22. 23.
struma ovarii: report of a case and review of the literature. Horm Res 2002;58:34-38. Ribeiro-Silva A, Bezerra AMPS, Serafini LN. Case report. Malignant struma ovarii. An autopsy report of a clinically unsuspected tumor. Gyn Onc 2002;87:213-215. Vadmal MS, Smilari TF, Lovecchio JL, Klein IL, Hajdu SI. Diagnosis and treatment of disseminated struma ovarii with malignant transformation. Gyn Onc 1997;64:541546. Marcus CC, Marcus SL. Struma ovarii. A report of 7 cases and a reivew of the subject. Am J Obstet Gynecol 1961; 81:752-762. Nieminen U, Von Numers C, Widholm O. Struma ovarii. Acta Obstet Gynecol Scand 1963;42:399-424. Tokuda Y, Hatayama T, Sakoda K. Metastasis of malignant struma ovarii to the cranial vault during pregnancy. Neurosurgery 1993;33:515-518.
