MALIGNANT PRIMARY PARAGANGLIOMA OF THE THYROID GLAND: THE FIRST REPORTED CASE
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1 Case Report MALIGNANT PRIMARY PARAGANGLIOMA OF THE THYROID GLAND: THE FIRST REPORTED CASE David Reznick, MD 1 ; Joe Scharpf, MD 2 ; Krupa Doshi, MD 3 ; Allan Siperstein, MD 4 ; Eren Berber, MD 4 ; Deborah Chute, MD 5 ; Jamie Mitchell, MD 4 ABSTRACT Submitted for publication January 28, 2014 Accepted for publication September 24, 2014 From 1 Department of Surgery, 2 Head and Neck Surgery, 3 Endocrinology & Metabolism Institute, 4 Department of Endocrine Surgery, and 5 Department of Pathology, Cleveland Clinic, Cleveland, OH Address correspondence to Dr. David Reznick, Department of Surgery, Cleveland Clinic, Mail Code F20, 9500 Euclid Avenue, Cleveland, OH 44195, reznicd@ccf.org. DOI: /EP14041.CR To purchase reprints of this article, please visit: Copyright 2016 AACE. Objective: Primary paragangliomas of the thyroid gland are rare tumors with just 45 previously reported cases in the literature. While locally aggressive tumor behavior has been documented, there are no reported cases of a malignant thyroid paraganglioma. Methods: This report presents the case of a 73-yearold female who presented with a rapidly enlarging right thyroid mass. Results: At the time of initial resection, the mass had grossly invaded the trachea and esophagus and encased the recurrent laryngeal nerve. Central neck lymph node metastases were present. A right thyroid lobectomy with central neck dissection was performed, with a final histologic diagnosis of primary paraganglioma of the thyroid gland. Within 1 year, the patient showed local tumor recurrence that required a laryngeopharyngectomy with reconstruction. New cervical lymph node metastases had also developed, and within 1 year a solitary liver metastasis was identified and excised, confirming the malignant nature of the tumor. Conclusion: Thyroid paragangliomas are an extremely rare subset of thyroid tumors that have gained increasing recognition as a clinical entity in recent years. Recent case reports and a review of the literature emphasize that despite a tendency to display aggressive local behavior; distant metastatic spread was not reported for any of the 45 previously reported cases. This is the first case to show clearly malignant behavior in a thyroid primary paraganglioma with local recurrence as well as regional lymph node and distant tumor metastases. This case has important implications pertaining to patient postoperative management and emphasizes the importance of perioperative and postoperative surveillance for possible local recurrence or metastasis. (AACE Clinical Case Rep. 2016;2:e70-e75) INTRODUCTION Paragangliomas are tumors that arise from the chromaffin tissue of the autonomic nervous system (1). They can occur wherever the cells of the paraganglionic system are located. These complexes of chromaffin tissue, an accessory tissue of the autonomic nervous system, are distributed along the paravertebral and para-aortic axes extending from the cervical region inferiorly to the urinary bladder. Paragangliomas of the head and neck are typically parasympathetic in origin, and include carotid body tumors and chemodectomas of the glomus jugulotympanicum. Primary paragangliomas of the thyroid gland have also been described; however, these are exceedingly rare, with only 45 reported cases (1-10). While aggressive local behavior has been described in a number of case reports, none have reported actual metastases. We present the first case of a malignant primary thyroid paraganglioma with regional and distant metastases. CASE REPORT A 73-year-old Caucasian female with a past medical history significant for longstanding hypothyroidism, hypertension, and hyperparathyroidism underwent subtotal parathyroidectomy in At that time, an initial fine needle aspiration biopsy of a right thyroid nodule cytologically e70 AACE CLINICAL CASE REPORTS Vol 2 No. 1 Winter 2016 Copyright 2016 AACE
2 Malignant Thyroid Paraganglioma, AACE Clinical Case Rep. 2016;2(No. 1) e71 showed an abundance of stripped, naked nuclei which at the time of the original review were interpreted as lymphocytes consistent with Hashimoto s thyroiditis. In 2010, the patient presented initially with an increasing ionized calcium concentration of 1.33 mg/dl (upper limit, 1.30 mg/dl) and a parathyroid hormone concentration of 31 pg/ml. An ultrasound performed at that time revealed a rapidly enlarging right thyroid mass (Fig. 1). The mass measured 3.56 C 4.03 C 7.91 cm and had a heterogeneous sonographic echotexture and hypervascularity on color flow Doppler exam. Imaging revealed no abnormal lymph nodes in the central compartments or along the jugular chains. The results of a repeat fine needle aspiration biopsy were inconclusive, with some evidence of a lymphoproliferative process or a follicular neoplasm apparent. Concern over the rapid tumor growth and the conflicting biopsy reports prompted a recommendation for total thyroidectomy. Intra-operatively, a large mass with an unusual appearance had replaced the right thyroid lobe, with locally aggressive behavior evident, including invasion of the tracheal and esophageal surfaces and complete encasement of the right recurrent laryngeal nerve. These char- A B Fig. 1. Ultrasound images demonstrating a large, hypoechoic mass replacing the right thyroid lobe.
3 e72 Malignant Thyroid Paraganglioma, AACE Clinical Case Rep. 2016;2(No. 1) acteristics prompted an incisional biopsy, which was read as highly suspicious for lymphoma. Since management of this condition is nonsurgical, the procedure was aborted. However, the final pathology was interpreted as showing an epithelioid neoplasm with neuroendocrine differentiation. Tumor cell staining at this time was negative for AE1/ AE3, Cam5.2, and CK7. These results prompted reoperation for right thyroid lobectomy with limited superficial resection of the tracheal cartilage and esophageal muscle and an ipsilateral central neck dissection. Within the initial resection specimen, the majority of the right lobe of the thyroid had been replaced by a large mass containing extensive fibrosis and cell degeneration. Where viable, tumor cells were arranged in small nests and trabeculae surrounded by delicate vessels and fibrous bands. The tumor cells contained moderate amphiphilic to eosinophilic cytoplasm and uniform, central round nuclei lacking pinpoint nucleoli. No nuclear pleomorphism was identified. Mitotic activity was low, with up to 1 mitotic figure per 10 high power fields. Tumor nests had infiltrated the surrounding thyroid parenchyma and adjacent skeletal muscle (Fig. 2). No lymphovascular space or perineural invasion was identified within the initial resection specimen. The minimal residual normal thyroid tissue present did not show a thyroiditis, but there was extensive infiltration and destruction of the thyroid parenchyma by tumor cells and fibrosis tissue originating from a prior parathyroid exploration. However, there was a significant amount of peritumoral inflammatory reactive material composed of reactive fibroblasts, lymphocytes, and neutrophils. A second review of the stored aspirate from 2009 was performed and the stripped, naked nuclei present in the sample most likely originated from the paraganglioma. Histologically, the mass and central neck lymph nodes both showed tumor cells that were positive for synaptophysin and neuron-specific enolase, and negative for chromogranin, calcitonin, CEA, CAM 5.2, and TTF-1. Additionally, S100 staining was negative within the tumor cells but present in the sustentacular cells rimming the tumor nests. This immunohistochemical profile was consistent with a paraganglioma arising within the thyroid gland (Fig. 3). Because there was no pre-operative suspicion of paraganglioma, serum metanephrines were not assessed prior to resection and they were normal postoperatively. Genetic testing was recommended to determine the presence of hereditary syndromes, but it was declined by the patient. Within 6 months, a surveillance ultrasound exam showed a suspicious mass in the right central neck. Flexible laryngoscopy revealed a tumor that had invaded through the laryngeal complex. Subsequently, re-excision of recurrent paraganglioma was required that also necessitated laryngopharyngectomy with upper aerodigestive tract reconstruction, including central and modified radical neck dissection. There was extensive invasion of the larynx and esophagus (Fig. 4) and additional lymph node metastases were also identified. An initial computed tomography scan at a 3 month follow-up appointment showed no evidence of distant metastases. Within 12 months, repeat imaging was obtained for unexplained weight loss and revealed a large lesion in the left lateral segment of the liver (Fig. 5). Percutaneous biopsy confirmed metastatic paraganglioma. Due to the absence Fig. 2. Paraganglioma invading the surrounding thyroid tissue (hematoxylin and eosin, 40C).
4 Malignant Thyroid Paraganglioma, AACE Clinical Case Rep. 2016;2(No. 1) e73 Fig. 3. Paraganglioma characterized by nests of small, uniform cells on a background of fibrosis (A, hematoxylin and eosin, 200C) diffusely positive for synaptophysin (B, 200C) and surrounded by sustentacular cells highlighted by positive S100 staining (C, 200C). Fig. 4. Laryngectomy specimen showing the primary tumor (white arrow) with clear invasion through the laryngeal cartilage (black arrows).
5 e74 Malignant Thyroid Paraganglioma, AACE Clinical Case Rep. 2016;2(No. 1) Fig. 5. Axial computed tomography image showing a large mass in the left lateral segment of the liver (arrow). of additional metastatic disease, left lateral segmentectomy was performed. Eight months later, the patient developed diffuse metastases throughout the liver and peritoneal cavity and ultimately succumbed to her disease 13 months after her last surgery. DISCUSSION Paragangliomas arising from the thyroid represent a rare subset of head and neck paragangliomas. Laryngeal paraganglia consist of 2 paired paraganglia called the superior and inferior laryngeal paranglia (3). The inferior laryngeal paraganglia is normally located at the superior edge of the thyroid cartilage and the first tracheal ring (4). It has been hypothesized that this tissue may rarely migrate into the thyroid during development or allow thyroid tissue growth around the paraganglia, causing the intrathyroidal paraganglia tissue from which these tumors can arise (3). This development explains how some of the paragangliomas appear completely intrathyroidal while others are located laterally (3). Only 45 thyroid paragangliomas have been previously reported (1-10). These tumors were much more common in women at approximately a 9:1 ratio compared with men (5). The reported mean age at presentation was 48 (3), with a wide range from 9 to 73 years of age (5). The tumors typically presented as a palpable, often rapidly enlarging thyroid mass. Several of the reported cases also initially presented as a tender thyroid mass, which is distinct from the more common benign and malignant thyroid nodules and may serve as a distinguishing feature of these difficult to diagnose tumors. While fine needle aspiration biopsy rarely definitively confirms the diagnosis (only 1 of 45 cases), it usually shows suspicious features prompting surgical resection (3). Histologically, these tumors are comprised of 2 different cell types: chief cells and the sustentacular supporting cells that surround vascular sinusoids (3). Immunohistochemical analyses show staining of the chief cells for synaptophysin and usually chromogranin, with the sustentacular cells staining positive for S100 (3). Negative staining for calcitonin, CEA, and TTF1 helps exclude medullary thyroid cancers and other follicular cell-derived thyroid cancers, respectively (3). At the time of surgery, these lesions are often found to be locally aggressive, with invasion of surrounding structures, such as the trachea and neurovascular structures found in 30% of cases according to previous reports (5). They have also been found to be fairly vascular tumors, with increased operative blood loss compared to other thyroid surgeries in some cases (3). Previous thyroid paragangliomas have demonstrated local aggressiveness with vascular, esophageal, and tracheal invasion; however, they were successfully resected without evidence of metastatic recurrence (5). Despite their tendency to be locally aggressive, they have previously been felt to have a benign biologic behavior with no previously reported cases describing local recurrence, regional lymph node metastasis, or distant metastases. In
6 Malignant Thyroid Paraganglioma, AACE Clinical Case Rep. 2016;2(No. 1) e75 addition to the commonly seen aggressive local behavior, the tumor in our patient is the first reported instance of a primary paraganglioma of the thyroid to demonstrate clearly malignant behavior with local recurrence, regional lymph node metastases, and extensive distant metastases. This case has important implications for the initial evaluation and postoperative monitoring of these patients, arguing for an initial metastatic survey at the time of diagnosis as well as developing a program for ongoing monitoring for recurrence. As these tumors do not typically demonstrate catecholamine hypersecretion and they are not derived from follicular cells, serum studies are not helpful in this regard. Periodic neck ultrasonography and cross sectional imaging of the chest, abdomen, and pelvis are likely most prudent for long-term surveillance. Recurrences and metastatic lesions should be treated with aggressive surgical resection when possible, with adjuvant therapy showing little benefit in most patients with paragangliomas of the head and neck (4). CONCLUSION Primary paragangliomas of the thyroid gland are extremely rare tumors that pose a diagnostic and therapeutic challenge. Previously reported cases have shown that while these tumors can be locally aggressive, aggressive surgical resection typically leads to long-term disease-free survival, with no previous reports of local recurrences, or locoregional or distant metastatic disease. Our case demonstrates that these tumors can in fact display malignant biologic behavior, with the potential to recur locally as well as metastasize to both regional lymph nodes and distant sites. It is therefore important to perform a thorough metastatic survey at initial diagnosis and to perform periodic postoperative surveillance with neck ultrasound and axial imaging of the chest, abdomen, and pelvis when monitoring patients with these unusual tumors. DISCLOSURE The authors have no multiplicity of interest to disclose. REFERENCES 1. Pellitteri PK, Rinaldo A, Myssiorek D, et al. Paragangliomas of the head and neck. Oral Oncol. 2004;40: Basu S, Viswanathan S. Primary paraganglioma of thyroid presenting as solitary thyroid mass. J Cancer Res Ther. 2011;7: Phitayakorn R, Faquin W, Wei N, Barbesino G, Stephen AE. Thyroid-associated paragangliomas. Thyroid. 2011;21: Myssiorek D, Rinaldo A, Barnes L, Ferlito A. Laryngeal paraganglioma: An updated critical review. Acta Otolaryngol. 2004;124: Armstrong MJ, Chiosea SI, Carty SE, Hodak SP, Yip L. Thyroid paragangliomas are locally aggressive. Thyroid. 2012;22: Yu B, Sheng W, Wang J. Primary paraganglioma of thyroid gland: a clinicopathologic and immunohistochemical analysis of three cases with a review of the literature. Head Neck Pathol. 2013;7: Akhtar K, Sen Ray P, Ahmad S, Sherwani R. Paraganglioma of the thyroid gland: cytologists enigma. BMJ Case Rep. May 22, Costinean S, Balatti V, Bottoni A, Old M, Croce C, Wakely PJ Jr. Primary intrathyroidal paraganglioma: histopathology and novel molecular alterations. Hum Pathol. 2012;43: D Angelo F, Antolino L, Magistri P, et al. Primary thyroid paraganglioma: a rare entity affecting middle-aged women. Am Surg. 2013;79:E351-E Evankovich J, Dedhia R, Bastaki J, Tublin M, Johnson J. Primary sclerosing paraganglioma of the thyroid gland: a case report. Ann Otol Rhinol Laryngol. 2012;121:
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