Strumal carcinoid of the ovary – report of two cases and review of literature


Strumálny karcinoid vaječníka – opis dvoch prípadov a prehľad literatúry

Cieľ štúdie:

Strumálny karcinoid (SC) je zriedkavý nádor vaječníka zo zárodočných buniek, ktorý je tvorený tkanivom štítnej žľazy v spojení s karcinoidom. SC býva prezentovaný ako monodermálny teratóm alebo ako súčasť zrelého cystického teratómu (dermoidnej cysty).

Typ štúdie:

Kazuistika.

Názov a sídlo pracoviska:

Ústav patológie Onkologického ústavu sv. Alžbety, Bratislava.

Metodika a výsledky:

Autori opisujú dva prípady tohto nádoru u asymptomatických žien vo veku 46 a 52 rokov, ktorým bol tento nádor zistený v rámci preventívnych gynekologických prehliadok. Išlo o solídne cystické tumory veľkosti 65×45×40 mm a 75×45×40 mm, v ktorých bol SC tvorený žltavým tuhším tkanivom s ložiskami želatinózneho charakteru. V oboch prípadoch bol SC súčasťou zrelého cystického teratómu (dermoidnej cysty), v ktorom predstavoval dominantnú časť. SC mali charakteristickú histologickú kompozíciu spojitosti zrelého štítno-žľazového tkaniva s karcinoidom. Imunohistochemicky bolo štítno-žľazové tkanivo pozitívne pri dôkaze cytokeratínu 7, tyreoglobulínu a TTF1, karcinoidný komponent vykazoval expresiu synaptofyzínu a v prvom prípade aj chromogranínu A. Nádorové bunky oboch komponentov boli negatívne pri dôkaze kalcitonínu a CEA. Oba nádory sa prezentovali nízkou proliferačnou aktivitou na úrovni Ki-67 do 2 %. V oboch prípadoch išlo o nádory v štádiu IA. Pacientky sú tri roky a šesť mesiacov bez akýchkoľvek problémov spojených s nádormi.

Záver:

SC predstavuje zaujímavú formu primárneho ovariálneho karcinoidu, ktorá je zvyčajne asymptomatická. V prípade, že je SC obmedzený na ovarium, je takmer vždy benígny a postačujúca je jednostranná alebo obojstranná adnexotómia.

klíčová slova

ovarium, germinálny nádor, strumálny karcinoid, imunohistochémia


Authors: K. Macháleková 1;  G. Kolníková 2;  M. Redecha 3;  P. Žúbor 4,5;  K. Kajo 1,6
Published in: Ceska Gynekol 2018; 83(6): 452-457
Category:

Overview

Objective:

Strumal carcinoid (SC) is a rare ovarian germ-cell tumour, which is characterized by a mixture of thyroid tissue and carcinoid. It can be presented as a monodermal teratoma or as a part of mature cystic teratoma (dermoid cyst).

Design:

Case report.

Setting:

Department of pathology, St. Elisabeth Cancer Institute, Bratislava.

Methods and results:

Hereby the authors describe two cases of this rare tumour in clinically asymptomatic women, 46- and 52-year-old, whom tumours were diagnosed at preventive gynaecological examination. The tumours considered of solid – cystic features, measured 65×45×40 mm and 75×45×40 mm and both contained parts of SC represented by tougher yellowish gelatinous areas. In both cases, SC was a part of the mature cystic teratoma (dermoid cyst), with predominated content. Histologically, both SC had a characteristic composition of intimate mixture of mature thyroid tissue and carcinoid. Immunohistochemically, the thyroid tissue stained positively with cytokeratin7, thyroglobulin and thyroid transcription factor-1, and the carcinoid component exhibited expression of synaptophysin and chromogranin A (only in one case). Tumour cells of both components of SC were negative for calcitonin and carcinoembryonic antigen. Both tumours showed low proliferation activity expressed by Ki-67 (up to 2%). Tumours were diagnosed in stage IA, and up to now are patients without any complications associated with tumours, free of relapse for 3 years and 6 months, respectively.

Conclusion:

SC represents an interesting form of primary ovarian carcinoid, which is usually asymptomatic and when confined to ovary, mostly has benign behaviour and can be treated by simple one-sided or bilateral adnexectomy.

Keywords

ovary, germ cell tumours, strumal carcinoid, immunohistochemistry

INTRODUCTION

Ovarian teratomas are germ cell tumours which are able to produce a wide range of tissues recapitulating the deficient development of various organs [19]. They are mostly of mature type (also called dermoid cysts) and account for up to 20% of all ovarian tumours [6, 18]. On the other hand, strumal carcinoid (SC) is a rare teratomatous tumour containing thyroid tissues intimately associated with carcinoid [18], so that it represents double-line differentiation towards to thyroid gland and neuroendocrine cells. While the thyroid differentiation in SC is a mature part of teratoma, the carcinoid reflects a form of neoplastic transformation inside teratoma.

According to our knowledge, up to now less than 100 cases of SC have been reported in the literature. We present two other cases of this interesting teratomatous tumour.

CASE 1

A 46-year-old woman, para two, no abortions or no artificial interruption of pregnancy (API),without any health problems was referred to our department due to the finding of enlarged both ovaries which were of solid – cystic appearance on ultrasonography (USG), detected on regular preventive gynaecological examination. A surgical intervention was recommended. Preoperative serum tumour markers profile showed normal level of Ca125 (11 IU/mL) and HE4 (15.7 pmol/L), giving a low risk ROMA index for malignancy. Preoperative computed tomography (CT) examination of chest, abdomen and small pelvis did not indicate the tumour spread outside ovaries. Patient underwent bilateral adnexotomy with hysterectomy due to the dysfunctional uterine bleedings.

Macroscopically, nearly whole left ovary, which was 65×45×40 mm in size, was composed of firm yellowish tissue in nodular configuration containing gelatinous areas and peripheral small cysts (up to 6 mm), filled with gelatinous content andsome calcifications. Further structures resembling dermoid cyst (grease, hair, etc.) were also present. The right ovary measured 45×35×20 mm and contained multiple simple cysts (up to 20 mm) with smooth lining and clear fluid inside. Tubes and uterus were of normal appearance.

Microscopic examination of the ovarian tumour revealed a mature cystic tridermal teratoma with a predominant component composed of the strumal carcinoid, the latter accounting up to 95% of the tumour volume. The coexisting thyroid tissue and carcinoid were either abruptly separated (fig. A1) or diffusely mixed (fig. A2). The tumour did not invade through the ovarian capsule. The carcinoid component shows typical trabecular growth pattern (fig. A3). Immunohistochemically, the thyroid follicles expressed CK7, thyroid transcription factor-1 (TTF-1) and thyroglobulin; and carcinoid cells were positive for chromogranin A and synaptophysin (fig. B1). In both components, stains for carcinoembryonic antigen (CEA), calcitonin and alpha-inhibin were negative. Focal immunoreactivity for alpha-inhibin has been observed only in reactive proliferated stromal cells. Proliferation activity evaluated by the Ki-67 index was less than 1%. From additional findings, endometrium was in the proliferation phase of the menstrual cycle and some foci of adenomyosis occurred inside myometrium.

Figure
A1 Strumal carcinoid with a relative abrupt border between
both components; H&E; 200×
Figure A1 Strumal carcinoid with a relative abrupt border between both components; H&E; 200×

Figure A2 Indistinct margin between strumal and carcinoid
component; H&E; 100×
Figure A2 Indistinct margin between strumal and carcinoid component; H&E; 100×

Figure A3 Characteristic view of trabecular carcinoid; H&E, 200×
Figure A3 Characteristic view of trabecular carcinoid; H&E, 200×

Figure B1 Positive immunohistochemical staining of carcinoid cells
with synaptophysin, thyroid follicles are negative; 200×
Figure B1 Positive immunohistochemical staining of carcinoid cells with synaptophysin, thyroid follicles are negative; 200×

According the diagnosis of SC, shortly after surgery the patient was examined by endocrinologist and oncologist. USG examination of the thyroid gland and neck structures disclosed only small non-significant hyperplastic nodules, two inside the right lobe and one inside the left lobe, all of them up to 10 mm in diameter. No enlarged lymph nodes were detected on the neck. The levels of tumour markers (CEA, Ca 19-9, alpha-fetoprotein – AFP, chromogranin A, calcitonin, thyroid stimulating hormone – TSH, and thyroglobulin) and serum calcium were normal 6 months after the surgery. The control postoperative gynaecological and oncologic examinations did not prove any signs of residual disease and oncologist proposed only observation.

Actually, the patient is three years from surgery without any signs of the disease.

CASE 2

The second patient was a 52-year-old woman with one living birth, without any abortions or API; and with long term history of using birth-control pills. From the anamnesis, she underwent laparoscopic surgery of the ovaries for non-specific cysts, and surgery of the breast for benign fibroepithelial lesion fifteen and four years ago, respectively. Twenty years ago the patient underwent two surgeries of thyroid gland for nontoxic nodules; therefore she was annually controlled by the endocrinologist. After subtotal thyroidectomy, only small residual thyroid tissue remained on the neck as a homogenous structure with some calcifications. The patient was without cervical lymphadenopathy.

Recent preventive gynaecological USG examination disclosed enlarged right ovary measuring 7×6 cm. The tumour was of solid appearance with unilocular cyst, 4 cm in diameter, with small distinct nodule protruding into the lumen. Preoperatively, slight elevation of tumour marker Ca125 was detected (45 IU/ml), so that giving low risk malignancy index (RMI < 200). Laparoscopic removal of the right ovary was performed.

Gross appearance of removed tumour showed solid heterogeneous neoplasm of grey-white to tan yellow colour with solitary cyst filled with typical dermoid structures and with intact surface capsule.

The histological examination demonstrated SC arising inside mature cystic tridermal teratoma. The predominant component was carcinoid of trabecular type; the minority was represented by mucinous component (fig. A4).

Figure A4 Strumal carcinoid with a focal mucinous differentiation;
H&E; 200×
Figure A4 Strumal carcinoid with a focal mucinous differentiation; H&E; 200×

Immunohistochemically, carcinoid structures expressed synaptophysin, and chromogranin A and were negative for CD56, proliferative activity was up to 2% positive cells. The thyroid follicular cells stained with CK7, thyroglobulin, TTF-1 (fig. B2) and CD56.

Figure B2 Immunohistochemical nuclear positivity of TTF1 in the
strumal component, carcinoid cells are negative; 400×
Figure B2 Immunohistochemical nuclear positivity of TTF1 in the strumal component, carcinoid cells are negative; 400×

Two month after surgery, the levels of neuron-specific enolase (9.7ng/ml) and chromogranin A (46.1ng/ml) were normal and CT/PET examination did not find any signs of elevated glucose metabolism. Based on these findings, the oncologist recommended only observation.

DISCUSSION

The strumal carcinoid is a distinctive form of ovarian teratoma characterized by mixture of thyroid tissue and carcinoid. Indeed, SC is one of the histological types of primary ovarian carcinoid, which is defined as well differentiated neuroendocrine tumour resembling carcinoid of gastrointestinal tract [18]. The primary ovarian carcinoids represent only 0.1% of all malignant ovarian tumours and approximately 0.5–1.7% of all carcinoid tumours [2, 8, 23]. Histologically, ovarian carcinoids can be divided into insular, trabecular, mucinous and mixed type and SC [3, 27].

SC can be presented as monodermal teratomas, but in more than 80% of cases they are part of mature cystic teratomas [8, 19] or may be associated with other ovarian neoplasm, e.g. with cystic mucinous tumour [18]. Although WHO classification regards SC as a form of carcinoid [18], this entity can be considered as an occurrence of ovarian struma inside secondary somatic malignancy (carcinoid). SC is almost always unilateral, in 15% of cases the mature cystic teratoma or mucinous tumour of the contra lateral ovary can occur [13].

Based to the gross appearance we can recognize three forms of SC: 1. a tan yellow nodule inside the wall of the dermoid cyst; 2. a grey-white to yellow nodule inside either solid mature teratoma or another neoplasm (e.g. cystadenoma); 3. a yellow hard homogeneous nodule representing pure or nearly pure form of SC (sometimes called monodermal teratoma) [19]. SC was described in women aging from18 to 78 years; however, the majority of them were presented as peri- and postmenopausal women [3, 19].

SC are usually clinically silent, mostly are presented as a slowly growing mass in pelvis or are incidentally detected during preventive examinations [13], as it was in our both cases. Imaging modalities (USG, CT, and MRI) usually depict these neoplasms as non-specific ovarian masses with solid and cystic parts [4, 26, 27, 28].

The majority of the cases are non-functional, only 8% of SC from the largest presented cohort yet produced steroids, e.g. androgens causing virilism or oestrogens producing endometrial hyperplasia [19]. In other cases, prominent hirsutism, androgenic type of alopecia, sexual pilosity and clitoromegaly were described [5, 21]. All of these functional effects are probably results of ovarian stroma activation [3]. Another 8% of SC can exhibit functioning thyroid tissue resulting to hyperthyroidism, but up to now none of the patients had symptoms typical for carcinoid syndrome, which can occur in pure ovarian carcinoids as typical facial flushing and diarrhoea [3, 12, 19]. Interestingly, there have been reported several cases of SC with the dominant clinical presentation of severe progressive constipation lasting for several years. As a reason of this constipation has been proved an overproduction of the peptide YY (PYY), which is commonly produced in the gastrointestinal tract and in the pancreas, and its physiological function is the inhibition of gastric and pancreatic secretion, delay of gastric emptying, and slowing of intestinal motility [8, 14, 21, 22, 28]. Symptoms of constipation usually disappeared after surgical removal of SC [8]. Therefore, serum levels of PYY may serve as a tumour marker in cases presenting with constipation, because after removal of the tumour its level decreases. In the literature, rare cases of SC associated with multiple endocrine neoplasia type 2A were described [25]. Ours presented cases were without any clinical presentation as a majority of published cases.

Histologically, SC is composed of thyroid tissue and carcinoid, which is almost always of trabecular or mixed trabecular - insular type [19]. Approximately 46% tumours contain also a small amount of mucinous cells located either at interface between the strumal and carcinoid component or directly in SC [19], as it was presented in our second case. We suppose that this admixture of mucinous cells could be a part of pure SC, although recently published similar case was diagnosed as primary ovarian mixed strumal and mucinous carcinoid arising in mature cystic teratoma [9]. Moreover, SC can contain also for example „transitional cells“, which resemble Brenner ovarian tumour [19].

Thyroid tissue inside SC may be of normal appearance, but may exhibit hyperplastic changes as colloidal goiter, microfollicular or macrofollicular adenoma, and very rarely also follicular or papillary carcinoma [16, 17, 19]. In the half of the cases, follicles can contain birefringent crystals resembling calcium oxalate monohydrate crystals [19]. In our second case, the patient had a previous surgery of the thyroid gland for goiter, but we did not prove any association between thyroid disease and SC.

Neuroendocrine component of SC consists of columnar cells with prolonged hyperchromatic nuclei and mild mitotic activity. Typically, cells are arranged in trabecules or small islets [24]. Neuroendocrine character of carcinoid cells can be confirmed by staining of argyrophilic and argentafine granules or by immunohistochemical stains of chromogranin A and synaptophysin. In spite of thyroid component, the expression of TTF-1 and thyreoglobulin in the carcinoid part is highly variable. Other markers such as somatostatin, serotonin and prostatic acid phosphatase (PSAP) may be positive in carcinoid cells [20], but CEA and calcitonin are usually negative [10]. Also neurosecretory granules were confirmed inside carcinoid cells, less inside some follicular cells, by ultrastructural examination [10, 20].

Both components of SC can be either clearly separated, or in other parts the thyroid follicles can penetrate between carcinoid cells or even some follicles can be covered by proliferated neuroendocrine neoplastic cells [10, 19, 20].

In SC, differential diagnosis includes lesions from the group of sex cord-stromal tumours (e.g. granulosa cell tumour, Sertoli-Leydig cell tumour), ovarian Brenner tumour or poorly differentiated primary or secondary adenocarcinomas of the ovary [13, 19]. Whereas in the group of sex cord-stromal tumours the immunohistochemical evidence of inhibin and calretinin is crucial, differentiation of primary and secondary ovarian adenocarcinoma requests complex histomorphological and immunohistochemical analysis along with oncologic anamnesis. However, the most important point in SC diagnosis is the differentiation of primary ovarian carcinoid from metastatic carcinoid, which is most often of gastrointestinal origin. In metastatic disease, usually both ovaries are affected and thyroid component is missing, primary origin is usually in the ileum [19]. Incidence of metastases of carcinoid from gastrointestinal tract to ovaries is four times less frequent than primary ovarian carcinoid [13].

Preoperative diagnosis of SC is difficult [24]. This tumour should be taken into consideration in cases of ovarian tumours with the above-mentioned clinical presentations (high levels of androgen or long-lasting constipation). Clinically silent SC can be diagnosed only histologically.

It is supposed, that ovarian carcinoid tumours can arise either from teratomatous endocrine cells that are commonly located in the gastrointestinal or respiratory epithelial cells of teratoma, or from neuroectodermal teratomatous cells or from endodermal cells [24]. Trabecular carcinoids and SC are usually of foregut or hindgut origin, so that they are able to produce PYY [14, 15, 24]. In the past there was a hypothesis, that carcinoid component could be derived from the C-cell population of the thyroid tissue, and thus represents medullary carcinoma of the thyroid origin inside the ovary [19]. Later, the ultrastructural examinations disclosed a possibility of hybrid cells existence, which are able to differentiate into thyroid tissue and neuroendocrine cells resembling hind gut carcinoid cells. These findings were supported also by morphological and immunohistochemical analyses, e.g. evidence of PSAP expression, which is common in hind gut carcinoids [10, 19, 20].

Prognosis of SC is favourable, and while the tumour is limited to ovary; its behaviour is almost always benign [5, 18, 24]. From the largest cohort of 50 cases of SC, only one case was associated with extra-ovarian spread and death, which was caused by intra-peritoneal spread and liver metastases of poorly differentiated papillary carcinoma with carcinoid foci [19]. In another published case of 24-year-old pregnant woman, the thyroid follicular carcinoma developed inside SC and spread itself [1]. There was also described a case of SC in IA stadium, where the neuroendocrine component showed changes very similar to atypical carcinoid of lungs (focal necrosis, atypical nuclei and mitoses). Anticancer chemotherapy was not effective in patient, in whom multifocal metastases developed in bones and breast three and a half year after surgery. This tumour was strongly positive for the alpha 2-topoisomerase and exhibited very high proliferation activity measured by Ki-67 [11].

Treatment of SC in the first stage of the disease is based on surgical resection of ovaries and tubes (unilateral or bilateral; with or without hysterectomy) [26], but in the past also more extensive operations were described (e.g. with appendectomy) along with radiotherapy [19]. If metastatic spread of the thyroid component occurs, total thyroidectomy is necessary together with radio-ablation [1, 7].

CONCLUSION

SC represents very rare ovarian tumour, which should be included into differential diagnosis spectrum of adnexal lesions. It is necessary to publish these unique case reports in order to notice their other possible characteristics and it is necessary to realise long-term follow up of the patients to obtain more relevant information about their biological behaviour.

MUDr. Katarína Macháleková, PhD.

Ústav patológie

Onkologický ústav sv. Alžbety

Heydukova 10

812 50 Bratislava

e-mail: katarina.machalekova@ousa.sk


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Paediatric gynaecology Gynaecology and obstetrics Reproduction medicine
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