Thyroid-type carcinoma of struma ovarii.
|Abstract:||* Struma ovarii is a monodermal variant of ovarian teratoma. Thyroid-type carcinoma arising in struma ovarii is rare. The most common type is papillary carcinoma, followed by typical follicular carcinoma, and the new entity of follicular carcinoma--highly differentiated follicular carcinoma of ovarian origin; other forms occur rarely. Consensus on the surgical and postoperative treatment of patients with thyroid-type carcinoma arising in struma ovarii has not been reached. Surgical treatment ranges from total abdominal hysterectomy, plus bilateral salpingo-oophorectomy with omentectomy, to conservative surgery, involving unilateral oophorectomy or strumectomy (cystectomy) for fertility preservation. Adjuvant therapy includes external radiotherapy, chemotherapy, thyroidectomy, and radioactive iodine ablation. Thyroid-type carcinomas arising in struma ovarii, especially the newly recognized entity--highly differentiated follicular carcinoma of ovarian origin--have a favorable prognosis. (Arch Pathol Lab Med. 2010;134:786-791)|
Carcinoma (Risk factors)
Carcinoma (Care and treatment)
Cancer (Risk factors)
Cancer (Care and treatment)
|Publication:||Name: Archives of Pathology & Laboratory Medicine Publisher: College of American Pathologists Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2010 College of American Pathologists ISSN: 1543-2165|
|Issue:||Date: May, 2010 Source Volume: 134 Source Issue: 5|
|Geographic:||Geographic Scope: United States Geographic Code: 1USA United States|
Struma ovarii is a monodermal variant of ovarian teratoma, which
was initially described by Bottlin in 1888 and, later, by Pick in 1902
and 1903, who recognized that struma ovarii was composed of thyroid
tissue. (1) Malignancy of struma ovarii is rare. The malignant struma
ovarii was first described by Wetteland in 1956. (2) Since its initial
description, struma ovarii, especially malignant struma ovarii, has
elicited considerable interest because of its many unique features. (1)
Upon review of the literature, papillary carcinoma and follicular
carcinoma are the most frequent types of malignancy to occur in struma
ovarii; other forms of thyroid carcinoma occur rarely. Most recently,
Roth and Karseladze (3) described a new entity of follicular carcinoma,
highly differentiated follicular carcinoma of ovarian origin (HDFCO),
characterized by extraovarian dissemination of thyroid elements with an
innocuous appearance that histologically resembles nonneoplastic thyroid
tissue. In the literature, the term malignant struma ovarii has been
used in 2 ways: struma ovarii with thyroid-type carcinoma; and struma
ovarii that has metastasized. Regarding the occurrence of malignancy in
struma ovarii, the literature is confusing because many of the cases
reported as malignant struma ovarii have not been accurately classified,
and no large series has been carefully documented. (1) Several cases
reported as malignant struma ovarii in the older literature were
actually examples of strumal or insular carcinoid. (4) Because of
varying usage and the lack of a precise definition, it is recommended
that the term malignant struma ovarii no longer be used for cases of
malignancy that develop in struma ovarii, except in the generic sense.
The term thyroid-type carcinoma originating (arising) in struma ovarii
(specifying the type) is more appropriate. (1)
The incidence of thyroid-type carcinoma arising in struma ovarii is difficult to assess because of the rare nature of this condition and the lack of standard criteria for diagnosis. In 2 literature reviews of cases of "malignant struma ovarii," the average age of patients was 42.9 years (5) and 44 years. (6) Most recently, Roth et al (4) reviewed the reported cases and divided them into 3 main groups according to the pathology classification. Patients with papillary carcinoma ranged from 21 to 68 years old, those with typical follicular carcinoma were 22 to 70 years old, and those with HDFCO were from 17 to 70 years old at the time of initial excision of the primary ovarian neoplasm. (7) Patients predominantly presented with a pelvic mass (45%) and abdominal pain (40%). Several patients presented with menstrual irregularities (9%), hyperthyroidism (5%-8%), ascites (17%), and deep vein thrombosis (4%). (5,6) Zannoni et al (8) reported the first case of pseudo-Meigs syndrome in malignant struma ovarii, which was associated with ascites, hydrothorax, and elevated CA 125 (cancer antigen 125) levels. The associated symptoms disappeared, and the elevated CA 125 returned to within reference range postoperatively without adjuvant therapy. (8)
Hyperthyroidism is rare; however, the preoperative diagnosis of struma ovarii/malignant struma ovarii may be suggested through thyroglobulin measurement or from scanning of patients affected by hyperthyroidism. Matsuda et al (9) reported on a 48-year-old woman who presented with symptoms of hyperthyroidism and an ovarian mass. Hormonal findings revealed increased thyroid function, but the thyroid gland appeared normal in size and texture. Hormone-producing malignant struma ovarii was diagnosed preoperatively and was confirmed by pathology and immunohistochemistry postoperatively. The findings of hyperthyroidism disappeared over several weeks after surgery. (9) The pathophysiology of hyperthyroidism in malignant struma ovarii is unknown. Hyperthyroidism induced by malignant struma ovarii is likely to be mediated by a mechanism different from classic thyroid hyperthyroidism. It is postulated that struma ovarii is an autonomous hormone-secreting tumor or that the ovarian thyroid tissue is stimulated by thyroid-stimulating hormone receptor antibody. (10)
Metastasis of malignant struma ovarii has been documented. It is seen in approximately 5% to 23% of cases of malignant struma ovarii and is mainly intra-abdominal, although blood-borne metastasis can occur in the liver, lung, brain, bone, vertebra, and the contralateral ovary. (6) Roth et al (7) recently reviewed their own cases and literature and demonstrated that osseous metastases occurred in 26% of patients with typical follicular carcinoma and 17% of patients with HDFCO, but only 4% of patients with papillary carcinoma. Typical follicular carcinoma is more likely to metastasize to the lung, liver, and central nervous system; whereas papillary carcinoma has a propensity to involve the abdominal cavity and lymph nodes and occasionally the liver. (7)
Approximately 94% of the thyroid-type carcinomas arising in struma ovarii are unilateral and appear to involve the left ovary more commonly than the right ovary. Macroscopically, the size of the tumor is 10.5 [+ or -] 4.69 cm. (5) The tumor is typically brown or green-brown, predominantly solid, and gelatinous (Figure, A). Usually, thyroid-type carcinoma arises from a pure form of struma ovarii; less frequently, it is associated with a mature cystic teratoma or is a component of strumal carcinoid. Rarely, no associated lesion can be identified. (11) Although most cases are solid, or solid and cystic, some appear as unilocular or multilocular cysts containing brown to green gelatinous fluid. In cases of intra-abdominal implantation or metastasis, multiple nodules can be seen in the omentum and peritoneum, on the surface of the urinary bladder and uterus, or in the distal organs, such as liver, lung, brain, and bone. These metastatic or implanted nodules may not have the same macroscopic features as the original tumors in the ovary. Frequently, the different-sized nodules are solid, without the primary tumor's typical brown, green-brown, gelatinous, thyroidlike appearance. If the lesion is a component of a teratoma, the metastatic nodules may only contain the thyroid component without other components visible macroscopically. The reported dimension of measurable peritoneal nodules vary from 0.5 to 5 cm; rarely, the peritoneal implants are only observed through microscopic examination. (12)
Mature cystic teratomas account for approximately 20% of all ovarian tumors. Of these, approximately 15% contain thyroid tissue. Struma ovarii is a monodermal variant of ovarian teratoma, composed predominantly of thyroid tissue (>50%), and constitutes about 2.5% to 5% of ovarian teratomas. (13,14) Histopathologically, struma ovarii is composed of various-sized thyroid follicles filled with pink-staining, homogenous, gelatinous colloid, lined with cuboidal or columnar epithelium, and separated with internal septications.
The criteria for a histopathologic diagnosis of malignant struma ovarii have varied over time, and uniformly accepted criteria for diagnosis of a thyroid-type carcinoma arising in struma ovarii have yet to be established. However, the guidelines for diagnosis of primary thyroid carcinoma are mostly used currently for the diagnosis of thyroid-type carcinoma arising in struma ovarii. (13,15) Strict criteria are required for the diagnosis of thyroid-type carcinoma because proliferative changes, including areas of densely packed follicles or pseudopapillary formations in a struma ovarii, may be confused with malignancy. (13) The appearance of colloid in a struma ovarii will help the diagnosis. The loss of colloid material during tissue processing, or inadequate sampling, may lead to misdiagnosis, especially in frozen sections (Figure, B). Several different thyroid-type carcinomas have been described in struma ovarii: papillary carcinoma, including the follicular variant; follicular carcinoma, including HDFCO (3); undifferentiated (anaplastic) carcinoma (16); and medullary carcinoma. (17)
Papillary carcinoma is the most common thyroid-type carcinoma to occur in struma ovarii. (1) Criteria for conventional papillary carcinoma include a true papillary architecture, lined by one, or occasionally several, layers of neoplastic cells, with crowded, round or oval nuclei. The papilla consists of a central fibrovascular stalk with loose connective tissue and variably sized, thin-walled vessels. Nuclei of neoplastic cells are enlarged, clear, "ground glass," empty, and overlapping. Mitoses are rarely present. Intranuclear inclusions of cytoplasm and nuclear grooves are often found. These tumors exhibit nuclear features similar to those of their counterparts in the cervical thyroid gland. The identification of psammoma bodies in the context of a thyroid-type papillary neoplasm is highly supportive in the diagnosis of malignancy. Similar nuclear features are present in the follicular variant of papillary thyroid carcinoma; however, papillary architecture is absent or minimal (Figure, C and D).
Follicular carcinoma is the second most common type of carcinoma arising in struma ovarii and varies in its degree of differentiation. (1) The diagnosis of well-differentiated thyroid-type follicular carcinoma is more difficult to make than that of papillary carcinoma. Capsular invasion is an important criterion of malignancy in follicular carcinoma located in the neck, but there is usually no capsule in the corresponding ovarian lesion. Therefore, the identification of invasion into the surrounding ovarian tissue, vascular invasion, or metastasis is employed as evidence of malignancy. (1) The less-differentiated forms show significant architectural abnormalities, nuclear atypia, and mitotic activity.
Recently, Roth and Karseladze (3) described a new variant of follicular carcinoma--HDFCO. Highly differentiated follicular carcinoma of ovarian origin has an innocuous appearance, resembling that of nonneoplastic thyroid tissue in both the ovary and sites of dissemination. The term peritoneal strumosis or strumosis has been applied to the benign-appearing peritoneal implants in the absence of an identifiable thyroid-type carcinoma. (1,18,19) The terminology of peritoneal strumosis is still controversial. Those who consider this phenomenon benign most often use the term peritoneal strumosis, whereas those who consider it malignant use the term malignant struma ovarii. After reviewing the literature and their own cases, Roth and Karseladze proposed that peritoneal strumosis is a lowgrade, malignant neoplasm, and they categorized it as HDFCO. It is suggested that the confused term peritoneal strumosis no longer be used. (3) Because of the benign histologic appearance of HDFCO, this form of follicular carcinoma characteristically can not be diagnosed until the neoplasm spreads beyond the ovary.
Thyroid-type carcinoma has been reported to occur in strumal carcinoid. (11) Strumal carcinoid is a distinctive form of ovarian teratoma characterized by a mixture of thyroid tissue and carcinoid. (20) Histopathologically, it combines the features of carcinoid and struma ovarii (Figure, E). Immunohistochemistry using TTF-1 (thyroid transcription factor 1), thyroglobulin (Figure, F) , and neuroendocrine markers, such as chromogranin or synaptophysine (Figure, G), may assist in the diagnosis. (1) The cases of strumal carcinoid with a component of thyroid-type carcinoma should be diagnosed as thyroid-type carcinoma to ensure patients receive optimal follow-up and therapy.
The diagnosis of thyroid-type carcinoma arising in struma ovarii largely depends on the recognition of its characteristic microscopic features with hematoxylineosin- stained sections. The nuclear features, such as overlapping, ground-glass nuclei with nuclear grooves and intranuclear inclusions, are important in diagnosing papillary thyroid carcinoma (PTC); however, there are PTCs that do not completely fulfill the nuclear criteria, making the diagnosis difficult. The typical nuclear features in PTC may all be present throughout the lesion, but occasionally, they are only present focally. Furthermore, some PTCs may have very bland, subtle nuclear atypia, or only some of the nuclear features are present. The combinations of morphology and biologic behavior (vascular invasion, metastasis) will help in making the correct diagnosis.
A diagnosis of poorly differentiated follicular carcinoma is easy to make; however, a diagnosis of well-differentiated follicular carcinoma may be difficult. The differential diagnosis of well-differentiated, thyroid-type follicular carcinoma includes benign struma ovarii, the follicular variant of PTC, and HDFCO. Recognition of surrounding ovarian tissue, vascular invasions, and metastasis will establish malignancy rather than benign struma ovarii. The typical nuclear features of PTC with follicle formation and minimal papillary structures may aid in the diagnosis of the follicular variant of PTC other than follicular carcinoma. Because of the benign appearance, resembling that of colloid of nodular goiter, the diagnosis of HDFCO can not be made until extraovarian dissemination is detected. The presence of cytologic atypia in either the ovarian struma or its extraovarian manifestations or vascular invasion is not compatible with a diagnosis of HDFCO and should be diagnosed as conventional follicular carcinoma. (3)
Thyroid-type carcinoma arising in struma ovarii may mimic other primary ovarian tumors, such as granulosa cell tumor, Brenner tumor, papillary serous cystadenoma, or cystadenocarcinoma. Distinction from these primary ovarian tumors, especially papillary serous cystadenocarcinoma, is of great importance because misdiagnosis may lead to suboptimal treatment of the patient. Similar to thyroid-type carcinoma arising in struma ovarii, granulosa tumor or Brenner tumor can be a component of mature cystic teratoma and may have a microfollicular or pseudotubular appearance with grooved nuclei, which may simulate follicular carcinoma or follicular-variant PTC. The papillary appearance and the presence of psammoma bodies in ovarian papillary serous cystadenoma or cystadeno-carcinoma may mimic thyroid-type papillary carcinoma. However, the correct diagnosis can be made by the cytologic features of the neoplastic cells and the presence of typical thyroid follicles in most of the cases. Furthermore, the combination of immunohistochemistry staining with thyroglobulin, TTF-1, inhibin, WT1 (Wilms tumor 1), and CA 125 will help differentiate these ovarian primary tumors from thyroid-type carcinoma. (21)
Metastatic cervical thyroid carcinoma of the ovary is extraordinarily uncommon; it can occur many years after the primary cervical carcinoma and may histologically resemble primary thyroid-type carcinoma arising in struma ovarii. (22) A detailed clinical history and examination can be instrumental in establishing the correct diagnosis.
Molecular analysis has revealed that approximately 70% of all follicular cell-derived thyroid carcinomas present with activating mutations of BRAF (v-raf murine sarcoma viral oncogene homolog B1), RAS, RET (rearranged during transfection), and NTRK1 (neurotrophic tyrosine kinase receptor 1). (23-25) Recently, Kondo et al (24) reviewed the pathogenetic mechanisms of thyroid follicular cell neoplasia and found mutations of BRAF (29%- 69%), RET (13%-43%), and RAS (0%-21%) are most commonly seen in adult papillary thyroid carcinoma; RET rearrangements are more prevalent in adult tumors associated with previous radiation exposure. (23,24) Most recently, Schmidt et al (26) observed BRAF, neuroblastoma RAS (NRAS), Kirsten RAS (KRAS), and RET mutations in 6 cases of malignant struma ovarii with histopathologic features of papillary carcinoma and 9 cases of benign struma ovarii. (26) BRAF mutations were present in 4 of 6 malignant struma ovarii (67%) and none of 9 benign struma ovarii (0%). The BRAF mutations included V600E, K601E, and TV599-600M. These data indicate that the development of malignant struma ovarii with papillary thyroid carcinoma features is associated with BRAF mutations of the type commonly observed in cervical thyroid papillary carcinoma, suggesting a common pathogenesis for all papillary thyroid carcinoma regardless of location. Boutross-Tadross et al (15) examined 10 cases of follicular variant thyroid-type papillary carcinoma of struma ovarii and 3 cases of benign struma ovarii and found 100% of the carcinomas were diffusely positive for CK19 (cytokeratin 19), 80% were positive for HMBE-1 (hector battifora mesothelial cell 1), and 70% exhibited RET/PTC rearrangement. All 3 benign struma ovarii were negative for CK19, HBME-1, and RET/PTC rearrangement. These results are consistent with that of cervical follicular variant PTC, indicating that follicular variant papillary carcinoma of struma ovarii exhibits the same profiles as follicular variant papillary carcinoma in cervical thyroid.
Consensus on the surgical and postoperative treatment of patients with thyroid-type carcinoma arising in struma ovarii has not been definitively reached. Surgical treatment ranges from total abdominal hysterectomy, plus bilateral salpingo-oophorectomy with omentectomy, to conservative surgery, involving unilateral oophorectomy or strumectomy (cystectomy), for preservation of fertility. Adjuvant therapy includes external radiotherapy, chemotherapy, and thyroid suppression. (6) Some authors have suggested that total abdominal hysterectomy with bilateral salpingo-oophorectomy is a reasonable option in postmenopausal women or in premenopausal women who have completed childbearing. In cases where preservation of fertility is desired, conservative surgery, such as unilateral oophorectomy or strumectomy (cystectomy), should be attempted only if there is a unilateral lesion without evidence of capsular invasion or gross metastasis. Any case exhibiting gross metastasis, capsular invasion, or an intraoperative frozen section demonstrating malignant struma ovarii should have complete staging for ovarian cancer with peritoneal washings and lymph node sampling. (6) Some authors recommend thyroidectomy and [I.sup.131] ablation as the first-line treatment in cases with extraovarian dissemination or when preservation of fertility is not required after surgical diagnosis, and they have found [I.sup.131] therapy prevented local and distant recurrence. (5,27) However, the rarity of this tumor makes it difficult for prospective trials to validate the optimal treatment options. A few patients with metastatic malignant struma ovarii have been treated with external beam radiation and chemotherapy; however, on the basis of the similarities between malignancy of struma ovarii and thyroid carcinoma, and adjuvant therapy's own set of risks and complications, radioactive iodine has been suggested as the first-line therapy for treatment of recurrent disease. (14,28)
In a manner analogous to treatment of patients with thyroid carcinoma, monitoring of serum thyroglobulin can be performed with greater sensitivity in patients with or without thyroidectomy. Sequential thyroglobulin levels are key to early detection of possible recurrence of malignancy. An increase in serum thyroglobulin greater than baseline level should prompt further evaluation for recurrent disease. (14) Considering the long period between the initial diagnosis and recurrence (average time to detection of recurrence is 4 years), Makani et al (6) recommended that a minimum period of 10 years is needed for follow-up in cases of malignant struma ovarii.
The exact prognosis of thyroid-type carcinoma arising in struma ovarii is still unclear because of its rarity, inadequate follow-up, and the absence of consensus in diagnosis and treatment. However, limited case reports and a small-series review demonstrated a good prognosis. Robboy et al (29) analyzed 36 malignant struma ovarii cases of their own and those from the literature with follow-up of 20 years or longer and reported the 5-, 10-, and 25-year survivals were 92%, 85%, and 79%, respectively, indicating an optimistic prognosis. They also found that extensive adhesions, large size of a struma ovarii (<5 cm, 0%; 5- 6 cm, 40%; 7-15 cm, 60%; >15 cm, 75%), and solid histologic architecture were associated with an increased incidence of recurrence or metastasis. Most recently, Roth et al (7) reviewed the literature and revealed 53 documented cases of papillary carcinoma (44 cases with follow-up), 31 cases of typical follicular carcinoma (29 cases with follow-up), 18 cases of HDFCO (15 cases with follow-up), and 1 case of undifferentiated (anaplastic) carcinoma (with follow-up). Approximately 3 of the 44 patients (14%) with typical follicular carcinoma, 4 of the 29 patients (7%) with papillary carcinoma, the only patient (100%) with undifferentiated (anaplastic) carcinoma, and none of the 15 patients (0%) with HDFCO died of neoplasm. The patients with typical follicular carcinoma died from 0.4 to 10.5 years after discovery of neoplasm, with both mean and median survivals of 5 years. The patients with papillary carcinoma died from 2 weeks to 21.5 years after treatment of the primary tumor, with a mean survival of 8 years and a median survival of 3.5 years. The only patient in the literature with undifferentiated (anaplastic) carcinoma died of neoplasm 13 months after diagnosis, despite aggressive management with therapeutic doses of radioactive iodine followed by chemotherapy. According to the above observations, Roth et al (7) concluded that undifferentiated (anaplastic) carcinoma is the most aggressive tumor type, and HDFCO is the least aggressive. Of the more common tumor types, typical follicular carcinoma is more aggressive than papillary carcinoma. (7) However, the conclusion that typical follicular carcinoma is more aggressive than papillary carcinoma is still not convincing because of the rarity, the limited case reports, and the variability between median and mean survival data. Further investigation and studies with more cases are needed to reveal the survival difference between follicular and papillary carcinoma.
Thyroid-type carcinoma of struma ovarii is rare. The criteria for diagnosis should follow the diagnostic criteria of cervical thyroid carcinoma. The terms malignant struma ovarii and peritoneal strumosis should no longer be used. The most common type is papillary carcinoma, followed by typical follicular carcinoma, and the new entity of follicular carcinoma--HDFCO; other forms of thyroid carcinoma occur rarely. If preservation of fertility is desired and the carcinoma is limited to the ovary, unilateral salpingo-oophorectomy or strumectomy is suggested; otherwise, total abdominal hysterectomy and bilateral salpingo-oophorectomy are typically performed. Sequential thyroglobulin measurements along with total-body scinti-scanning with I131 follow-up are recommended if recurrence is suspected. Thyroid-type carcinomas arising in struma ovarii, especially the newly recognized entity--HDFCO-- have a favorable prognosis.
We thank Yong-Doo Kim, MD, Department of Pathology, SUNY Downstate Medical Center and Kings County Hospital Center, for reviewing and commenting on the manuscript.
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Xuchen Zhang, MD, PhD; Constantine Axiotis, MD
Accepted for publication May 27, 2010.
From the Department of Pathology, State University of New York, Downstate Medical Center, Brooklyn.
The authors have no relevant financial interest in the products or companies described in this article.
Reprints: Xuchen Zhang, MD, PhD, or Constantine Axiotis, MD, Department of Pathology, State University of New York, Downstate Medical Center, 450 Clarkson Ave, Box 25, Brooklyn, NY 11203 (e-mail: email@example.com or firstname.lastname@example.org).
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