PROLIFERATIVE HIGHLY DIFFERENTIATED FOLLICULAR CARCINOMA OF OVARIAN ORIGIN (HDFCO) PRESENTING LONG AFTER BILATERAL OOPHORECTOMY
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1 Case Report PROLIFERATIVE HIGHLY DIFFERENTIATED FOLLICULAR CARCINOMA OF OVARIAN ORIGIN (HDFCO) PRESENTING LONG AFTER BILATERAL OOPHORECTOMY Natalie M. Liu, BS 1 ; Neda Moatamed, MD 1 ; Racquel S. Bueno, MD 2 ; Wendy L. Sacks, MD 3 ABSTRACT Objective: The malignant spread of histologically benign struma ovarii was historically referred to as peritoneal strumosis. Recently, highly differentiated follicular carcinoma of ovarian origin (HDFCO) was proposed as a more accurate diagnostic term for this rare disease. We report the unusual case presentation of a woman with HDFCO and the subsequent management of her cancer. Methods: Her interventions included abdominal surgery, postoperative laboratory tests, imaging, thyroidectomy, radioactive iodine-123 (RAI-123) diagnostic screening, and thyroid function studies. Results: A 72-year-old Chinese female was diagnosed with metastatic HDFCO approximately 30 years after hysterectomy and bilateral oophorectomy. While undergoing evaluation for an upper gastrointestinal bleed, a computed tomography scan revealed a 10 cm pelvic mass and multiple other peritoneal tumors. She underwent tumor debulking surgery, and the pathology was interpreted at two institutions; both made the diagnosis of a very welldifferentiated follicular carcinoma arising in struma ovarii. Lab tests revealed hyperthyroidism and RAI-123 uptake Submitted for publication August 27, 2016 Accepted for publication November 1, 2016 From the 1 Department of Pathology and Laboratory Medicine, University of California, Los Angeles, California, 2 Department of Surgery, Ekahi Central Medical Center, Honolulu, Hawaii, and 3 Department of Medicine, Cedars- Sinai Medical Center, Los Angeles, California. Address correspondence to Dr. Wendy L. Sacks, Department of Medicine, Cedars-Sinai Medical Center, Los Angeles, CA wendy.sacks@cshs.org DOI: /EP CR To purchase reprints of this article, please visit: confirmed tumor production of thyroid hormone. A total thyroidectomy was performed in anticipation of treatment with radioactive iodine-131 (RAI-131). However, the patient remained clinically asymptomatic and, therefore, neither additional tumor debulking nor RAI-131 treatment were performed. No disease progression has been noted for over 3 years. Conclusion: This case highlights the potentially slowgrowing nature of HDFCO which, in such cases, may be suited to less aggressive disease management. (AACE Clinical Case Rep. 2017;3:e264-e268) Abbreviations: CT = computed tomography; Hb = hemoglobin; HDFCO = highly differentiated follicular carcinoma of ovarian origin; RAI-123 = radioactive iodine-123; RAI-131 = radioactive iodine-131; T3 = triiodothyronine; T4 = thyroxine; TSH = thyroid-stimulating hormone INTRODUCTION Struma ovarii is a rare monodermal teratoma that predominantly contains thyroid tissue (50 to 100%) (1). Most struma ovarii are benign, but malignancy occurs in 5% of cases (2,3). The diagnosis of malignant struma ovarii can be complex, with most cases identified postoperatively through the extra-ovarian spread of tissue. The peritoneal or systemic spread of struma ovarii can exhibit a histologically normal appearance, despite its metastatic behavior. This entity was previously described as peritoneal strumosis. Recent literature argues that this terminology fails to encapsulate the malignant nature of the disease, and therefore a new entity, highly differentiated follicular carcinoma of ovarian origin (HDFCO), has been proposed (4,5). e264 AACE CLINICAL CASE REPORTS Vol 3 No. 3 Summer 2017
2 HDFCO Case Report, AACE Clinical Case Rep. 2017;3(No. 3) e265 Whereas most HDFCO patients have at least 1 ovary, we report a 72-year-old female that was diagnosed with HDFCO approximately 30 years post bilateral oophorectomy. The slower growth of her HDFCO coupled with lack of symptoms stemming from systemic invasion could be markers of disease quiescence. Hypothetically, cancer dormancy may contribute to the underlying mechanism of our patient s asymptomatic status (6). CASE REPORT A 72-year-old Chinese woman was admitted to the emergency room with chest discomfort, shortness of breath, black stool, and anemia (hemoglobin [Hb] = 5.8 g/dl). She received 2 units of blood that initially raised her Hb to 8.0 g/dl; however, this level fell again within 24 hours. On exam, the patient had decreased skin turgor, no abdominal tenderness, no palpable spleen/liver, and no lower extremity edema. She had a past medical history of hypertension and diet-controlled glucose intolerance. Past surgeries included: bilateral oophorectomy (left 1968, right 1984), hysterectomy (1984), and cholecystectomy (1990). The hysterectomy and oophorectomies were performed in Vietnam due to palpable ovaries on exam and the pathology is unknown. She had a father with diabetes mellitus, mother with a 15 cm thyroid goiter, and grandmother with reportedly benign ovarian cysts that were removed. To assess the presumed gastrointestinal bleeding as the source of her severe anemia, the patient underwent esophagogastroduodenoscopy (EGD). The EGD revealed superficial duodenal ulcers and the suspicion of an abdominal mass obstructing blood flow, as evidenced by vascular congestion and ampulla blushing. A computed tomography (CT) scan discovered a 10 cm mass near the right colon, a 2.4 cm mass on the left adrenal gland, and 4 additional masses throughout the peritoneum ranging from 1.7 to 4.2 cm. The patient continued to have persistent bleeding despite blood transfusion. Therefore, a right hemicolectomy was performed with resection of the 10 cm abdominal mass and a few peritoneal nodules. Attempts to remove the additional masses were unsuccessful due to prior surgical adhesion and risk of bowel perforation. After surgery, the patient s Hb stabilized. Surgical pathology initially identified the 10 cm abdominal mass as benign thyroid tissue. Due to the rarity of normal thyroid tissue in the abdomen, multiple endocrine and gynecological pathologists were consulted. The pathology was confirmed to be consistent with malignant struma ovarii, a rare entity called HDFCO (Fig. 1), despite her history of bilateral oophorectomy. Following surgery, the patient underwent various staging imaging studies. A thyroid ultrasound revealed bilateral nodules with the largest at the right lower pole measuring 1.6 cm. A chest CT scan showed a 5 mm mass near the left lung base. A pelvic CT scan also revealed multiple Fig. 1. Tissue histology. (A) Hematoxylin and eosin (H&E) stain shows the benign thyroid follicles of the tumor. (B) H&E stain shows the malignant part of the tumor with atypical follicular cells having irregular nuclear membrane, pale chromatin, and intranuclear grooves. (C) HBME immunostain shows positive staining of the malignant follicular cells.
3 e266 HDFCO Case Report, AACE Clinical Case Rep. 2017;3(No. 3) masses throughout the pelvis: 2.5 cm and 1.9 cm adjacent masses near the right pelvis, a 1.5 cm mass near the left colon, a 1.7 cm mass near the right psoas muscle, a 2.2 cm mass on the left adrenal gland, and several subcentimeter nodules throughout the abdomen. In addition, there was a 5 mm hypodensity in the bilateral common femoral vein which was later confirmed by ultrasound to be a deep vein thrombosis. Subsequently, a temporary inferior vena cava filter was placed and the patient was started on lovenox for anticoagulation after her gastrointestinal bleed resolved. The patient s postoperative labs included: Hb = 10.9 g/dl, thyroglobulin = ng/ml, antithyroglobulin antibody = 1.0 IU/mL, thyroid-stimulating hormone (TSH) <0.07 µiu/ml, and thyroxine (T4) = 1.5 ng/dl. The suppressed TSH was thought to be due to tumor production of T4, which was confirmed on a diagnostic radioactive iodine-123 (RAI-123) whole-body scan (Fig. 2). The patient later underwent a total thyroidectomy in preparation for radioactive iodine-131 (RAI-131) treatment. Thyroid pathology showed. Thyroid function studies revealed negative thyroid antibody status and persistent hyperthyroidism 6 months after total thyroidectomy without T4 replacement: total T4 = 8.6 ng/dl, adjusted T4 = 10.4 µg/dl, free triiodothyronine (T3) = 4.9 pg/ml, total T3 = 149 ng/dl, TSH <0.02 µiu/ml, thyroid hormone uptake = 36.30%, thyroid peroxidase antibodies <63 IU/mL, and thyroid-stimulating immunoglobulin <89%. The patient is clinically asymptomatic from the residual abdominal masses while the hyperthyroidism is managed with beta blockade. She continues to be monitored through regular labs with imaging studies and has not yet received RAI-131. DISCUSSION Fig. 2. Radioactive iodine-123 (RAI-123) scans. The patient s (A) anterior and (B) posterior RAI-123 imaging displays uptake by thyroid and abdominal masses. Relative RAI-123 uptake was calculated to be 10-fold higher in the abdominal nodules (44%) compared to the thyroid gland (4%). This was an interesting case of HDFCO diagnosed over 30 years after bilateral oophorectomy in a 72-year-old woman. Also notable about this case was the tumor s ability to produce thyroid hormone, which was confirmed on the RAI-123 whole-body scan that showed iodine uptake in the abdominal masses was 10 times higher than that in the thyroid (Fig. 2). The patient had excellent performance status with no complications until her gastrointestinal bleeding from the 10 cm tumor. Her previous lack of symptoms, rapid postoperative recovery, and continued excellent health suggest that an underlying level of quiescence was associated with the patient s HDFCO, much like that of well-differentiated thyroid carcinomas which tend to progress slowly (6). HDFCO treatment is generally managed similarly to thyroid malignancy, with thyroidectomy and RAI-131 (4). Because of the size and location of the patient s distant metastatic disease, further debulking may be required to optimize RAI-131 efficacy. However, her prior abdominal operations and the metastases adjacent to the bowel present an increased risk for any additional surgical intervention. Considering the indolent nature of HDFCO, physicians and patient must weigh the risks and benefits of the various treatment options. Because chronic thyrotoxicosis can lead to cardiac arrhythmias and other significant negative outcomes, it is important to address this aspect of the patient s disease. Using RAI-131 to ablate the thyroid tissue, which predominantly produces T3, can thereby treat both the hyperthyroidism and potentially shrink the size of the tumors. However, future monitoring will indicate the necessity of surgical intervention or additional RAI-131. HDFCO is an uncommon diagnosis and only a few cases have recorded a comparable presentation to our patient. Despite the benign appearance of HDFCO tissue, the peritoneal spread of our patient s disease also showcases the inherent malignancy of this rare entity. Other cases (Table 1) similarly demonstrate the metastatic potential of HDFCO, regardless of its well-differentiated histology. While the extent of treatment varied for each patient (as summarized in Table 1), most were successfully controlled through surgery, thyroidectomy, and RAI-131 ablation. All of the compiled cases either had no evidence of disease or were living with disease at the time of follow-up. Like our patient, those with persistent disease will require continued monitoring. The level of T4/T3 production from residual HDFCO tissue in these patients will dictate the need and degree of thyroid hormone replacement or suppression (2). A unique aspect of our patient was the timing of her extra-ovarian disease, which was diagnosed 30 years after her ovaries had been removed. This unusual presentation is shared by 2 of the cases in Table 1 that were diagnosed 31
4 HDFCO Case Report, AACE Clinical Case Rep. 2017;3(No. 3) e267 Table 1 Previous Cases of HDFCO with Abdominal Spread of Disease Case reference Age (years) Prior oophorectomy or hysterectomy Abdominal spread of HDFCO Thyroid pathology Extent of treatment Abdominal surgery Thyroidectomy RAI-131 Post-treatment thyroid hormone profile Follow-up Case 1 58 Hysterectomy, LSO (26 years prior), and RSO (20 years prior) 5 cm para-aortic lymph node, multiple peritoneal nodules Colloid nodule, Cholecystectomy, appendectomy, Yes Yes (2nd course 2.5 years later for recurrence) Elevated T3 (6 years) (8 years) Case 2 49 RSO (15 years prior) Multiple nodules throughout omentum No malignancy Total hysterectomy, LSO, No (patient declined thyroidectomy) No (received 3 courses of combination chemotherapy) n/a (16 years) Case 3 50 No 15 cm right lower quadrant, multiple cm nodules (omentum, urinary bladder, rectouterine pouch) Colloid nodules, Subtotal hysterectomy, RSO, omentectomy, Yes Yes WNL (6 years) Carey et al (7) 70 Total hysterectomy and BSO (31 years prior) Epicardial and peritoneal nodules (largest measuring cm) 0.5 cm welldifferentiated papillary carcinoma (no lymphovascular invasion, stage PT1) Partial omentectomy Yes Yes (30.5 mci) Elevated thyroglobulin (91 ng/ml) Ranade et al (2) 55 Unknown extent of surgery for previous struma ovarii (18 years prior) 7 6 cm iliac fossa mass, multiple peritoneal nodules (recurrence of past struma ovarii) No malignancy Resection of iliac fossa mass and other nodules Yes Yes (200 mci) WNL (without thyroid hormone replacement) Wei et al (9) Case No Multiple nodules (right fallopian tube, urinary bladder, pelvic wall) n/a Extent unknown No No WNL (17 years) Park et al (10) Case 1 35 Surgery of left ovary, extent unknown Nodules in peritoneum and omentum Chronic lymphocytic thyroiditis, Resection of nodules Yes Yes (200 mci) n/a (2 years) Abbreviations: BSO = bilateral salpingo-oophorectomy; HDFCO = highly differentiated follicular carcinoma of ovarian origin; LSO = left salpingo-oophorectomy; = living with disease; mci = millicuries; n/a = not available; = no evidence of disease; RAI-131 = radioactive iodine-131; RSO = right salpingo-oophorectomy; T3 = triiodothyronine; WNL = within normal limits.
5 e268 HDFCO Case Report, AACE Clinical Case Rep. 2017;3(No. 3) and 20 years after total hysterectomy and bilateral oophorectomy (4,7). The delayed nature of disease in these 3 women raises the question of how a rare ovarian cancer like HDFCO can arise without any ovaries present to undergo cancer transformation. Future research is needed to distinguish the true source of HDFCO in this clinical scenario. If our patient s disease originated from the removed ovaries, then cells with oncogenic potential may have persisted in the body in a quiescent state for several years prior to abdominal dissemination (6,8). CONCLUSION For HDFCO patients such as the one in the current case that remain asymptomatic for long periods, possibly due to a level of cancer dormancy, the timing of intervention may be unclear. While treatment can be tailored based on age and preference, RAI-131 remains the most effective and targeted option for patients with HDFCO. ACKNOWLEDGMENT We thank Dr. Virginia LiVolsi (Department of Pathology and Laboratory Medicine, University of Pennsylvania), Dr. Murli Krishna (Department of Pathology, Mayo Clinic), and Dr. Patricia Kim (Department of Pathology, Kuakini Medical Center) for aiding in pathology review. We thank Dr. Joseph Accurso (Department of Radiology, Mayo Clinic) for his important insight and discussion of considerations for RAI-131 treatment. We thank Dr. Michael Yeh and Dr. Masha Livhits (Department of Surgery, University of California Los Angeles) for helpful discussion of this case during UCLA s Endocrine Tumor Board. Finally, we thank Dr. Nu Lu (Department of Hematology and Oncology, Department of Pathology and Laboratory Medicine, University of California Los Angeles) for her strong support and continued guidance. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Willemse PH, Oosterhuis JW, Aalders JG, et al. Malignant struma ovarii treated by ovariectomy, thyroidectomy, and 131I administration. Cancer. 1987;60: Ranade R, Rachh S, Basu S. Late manifestation of struma peritonei and widespread functioning lesions in the setting of struma ovarii simulating highly differentiated follicular carcinoma. J Nucl Med Technol. 2015;43: Dujardin MI, Sekhri P, Turnbull LW. Struma ovarii: role of imaging? Insights Imaging. 2014;5: Roth LM, Karseladze AI. Highly differentiated follicular carcinoma arising from struma ovarii: a report of 3 cases, a review of the literature, and a reassessment of so-called peritoneal strumosis. Int J Gynecol Pathol. 2008;27: Roth LM, Miller AW 3rd, Talerman A. Typical thyroidtype carcinoma arising in struma ovarii: a report of 4 cases and review of the literature. Int J Gynecol Pathol. 2008;27: Sosa MS, Bragado P, Aguirre-Ghiso JA. Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat Rev Cancer. 2014;14: Carey K, Jain M, Krishna M, Accurso J. Peritoneal and mediastinal highly differentiated follicular carcinoma of ovarian origin. Indian J Nucl Med. 2014;29: Páez D, Labonte MJ, Bohanes P, et al. Cancer dormancy: a model of early dissemination and late cancer recurrence. Clin Cancer Res. 2012;18: Wei S, Baloch ZW, LiVolsi VA. Pathology of struma ovarii: a report of 96 cases. Endocr Pathol. 2015;26: Park MJ, Kim MA, Shin MK, Min HS. Follicular proliferative lesion arising in struma ovarii. J Pathol Transl Med. 2015;49:
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