Imaging features of synchronous bilateral primary tumors of oncocytic thyroid carcinoma and papillary thyroid carcinoma: A case report

Abstract

BACKGROUND

Oncocytic thyroid carcinoma (OTC), previously known as Hürthle cell carcinoma, is a distinct subtype of differentiated thyroid cancer accounting for approximately 5% of all thyroid malignancies. Synchronous thyroid tumors are extremely rare, accounting < 1% of all thyroid tumors.

CASE SUMMARY

We report a 38-year-old female with synchronous OTC in the left lobe and papillary thyroid carcinoma (PTC) in the right lobe, who had a history of thyroid nodules for 8 years. Ultrasound showed that the OTC was a large, hypoechoic, solid nodule with regular margins and internal vascularity. Contrast-enhanced computed tomography confirmed a heterogeneous, well-circumscribed enhancing mass extruding the thyroid boundary, with no cervical lymph node enlargement in the left lateral compartment. The right-lobe PTC was an ill-circumscribed node with spot calcification and internal nonuniform enhancement. It was smaller than the left-lobe OTC, and enlarged lymph nodes in the right lateral cervical compartment were identified. The patient underwent total thyroidectomy. Histopathology confirmed the diagnosis of synchronous minimally invasive left-lobe OTC right-lobe PTC, with right lateral neck compartment lymph node metastasis.

CONCLUSION

This case highlights the importance of recognizing imaging features of coexisting PTC and OTC for preoperative evaluation and surgical management.

Key Words: Oncocytic thyroid carcinoma; Hürthle cell carcinoma; Papillary thyroid carcinoma; Synchronous tumor; Collision tumor; Ultrasound; Computed tomography imaging; Case report

Core Tip: Acknowledgement of the imaging features of coexisting common papillary thyroid carcinoma and rare oncocytic thyroid carcinoma to guide appropriate preoperative evaluation and surgical management.

INTRODUCTION

Oncocytic thyroid carcinoma (OTC), previously known as Hürthle cell carcinoma, is a follicular cell-derived neoplasm accounting for approximately 5% of all thyroid cancers and categorized as differentiated thyroid cancer or papillary and follicular carcinoma[1,2]. Due to its unique molecular and clinicopathologic characteristics, OTC was recently recategorized as a distinct thyroid malignant neoplasm by the World Health Organization[3]. Molecular alternations of OTC can occur at both the nuclear and mitochondrial DNA levels, leading to a high somatic variant burden[4]. On pathological examination, OTC often harbors capsular and/or vascular invasion, and infiltration of the surrounding thyroid parenchyma[5]. The clinical behavior of OTC is more aggressive, and it has a poorer prognosis, compared with other differentiated thyroid cancers[6]. Distinguishing OTC from other differentiated thyroid cancers is necessary for clinical management because most differentiated thyroid cancers have an indolent course and excellent prognosis, and active surveillance or minimally invasive intervention is safe and recommended[7-10]. Oncocytes (Hürthle cells) can be identified through cytological examination of samples obtained by fine-needle aspiration biopsy, but OTC cannot be diagnosed without capsular and/or vascular invasion[11]. Definitive diagnosis of OTC before treatment decision-making is needed. Cross-section imaging and ultrasonography play important roles in diagnosing and managing thyroid nodules, but imaging characteristics are not well documented. We report a case of synchronous OTC and papillary thyroid carcinoma (PTC). Imaging and pathological examinations were performed and review of literatures was conducted.

CASE PRESENTATION

Chief complaints

A 38-year-old female with a history of bilateral thyroid nodules for 8 years was admitted with a right lobe nodule classified as Chinese Thyroid Imaging Reporting and Data System (C-TIRADS) 4A by thyroid ultrasonography at another hospital (Figure 1A). The left lobe nodule was categorized as C-TIRADS 3 (Figure 1B).

Figure 1 A 38-year-old female with collision tumors comprising oncocytic and papillary thyroid carcinomas. A: Ultrasound showed an irregular nodule with abundant intravascular in the right thyroid lobe [Chinese Thyroid Imaging Reporting and Data System (C-TIRADS) 4A]; B: Ultrasound showed a well-demarcated irregular nodule with some intravascular in the left thyroid lobe (C-TIRADS 3); C: Contrast-enhanced computed tomography (CT) revealed an ill-demarcated node (long arrow) with heterogeneous enhancement, calcification (arrowhead) and suspected minimal extrathyroidal extension (curve arrow) in the right thyroid lobe. A lymph node (short arrow) with avid enhancement was noted in the right lateral compartment; D: Contrast-enhanced coronal CT showed a well-demarcated node with nonuniform enhancement in the left thyroid lobe (arrow); E: Histologic section [hematoxylin and eosin (H&E) staining, × 5 original magnification] of the right lobe node indicated classical papillary thyroid carcinoma with encapsulated invasion and no vascular invasion; F: Histologic section (H&E staining, × 5 original magnification) of the left lobe node indicated tumor cells with avid oncocytic staining, encapsulated invasion (arrow), and vascular invasion (arrowhead in the inset).

History of present illness

The patient reported that she had bilateral thyroid nodules on physical examination 8 years ago, which were not palpable at that time. Since she had no discomfort, no treatment was given.

History of past illness

Ultrasound-guided fine-needle aspiration biopsy of the right-lobe nodule indicated PTC, categorized as Bethesda VI with BRAF V600E mutation.

Personal and family history

The patient reported no abnormal past medical or family history.

Physical examination

Neck examination showed no abnormal sign.

Laboratory examinations

Admission laboratory results showed the patient’s thyroid function, routine blood test, liver function, and renal function results were within the reference range, including the thyroglobulin of 16.2 ng/mL(normal range: 3.5-77.0 ng/mL).

Imaging examinations

Contrast-enhanced computed tomography (CT) confirmed a heterogeneous, well-circumscribed enhancing mass with an exophytic growth pattern and suspected minimal extrathyroidal extension, with no cervical lymph node enlargement in the left lateral compartment (Figure 1C). The right-lobe PTC was an ill-circumscribed node with spot calcification and internal nonuniform enhancement. It was smaller than the left-lobe OTC (Figure 1D). No enlarged lymph nodes in the left lateral cervical compartment were identified.

FINAL DIAGNOSIS

Intraoperative frozen sections revealed right lateral compartment lymph node metastasis and a 25 mm × 15 mm left-lobe nodule. Total thyroidectomy with central and lateral neck compartment dissection was then performed. Surgical histopathological examination of the right lobe neoplasm showed classical features of PTC, while the left lobe neoplasm showed oncocytes growing in sheets or clusters, characterized by abundant eosinophilic granular cytoplasm (Figure 1E and F). Capsular and vascular invasion was also noted. A diagnosis of minimally invasive OTC was made, according to the 2022 World Health Organization classification of thyroid neoplasms[3], due to limited vascular invasion (≤ 4 foci) and capsular invasion without overt anaplastic features or extensive invasion. Capsular invasion was also noted in the right-lobe PTC. The final diagnosis was synchronous OTC and PTC. Lateral neck dissection (levels II-IV and Vb) and central compartment dissection (level VI) were performed. Pathological examination revealed central and right lateral compartment metastatic nodes (2/6 and 6/20 nodes, respectively), consistent with PTC metastasis. There was no lymph node metastasis in the left lateral compartment. The final right-lobe PTC stage was pT1bN1bM0, and the final left-lobe OTC stage was pT1N0M0.

TREATMENT

The patient received radioactive iodine ablation (180 mCi) 3 months after surgery.

OUTCOME AND FOLLOW-UP

At the 12-month follow-up, the patient was clinically well with no evidence of disease on neck ultrasound, and the thyroglobulin was 0.29 ng/mL Levothyroxine replacement therapy was remained and lar surveillance were recommended.

DISCUSSION

Synchronous thyroid tumors are extremely rare, constituting < 1% of all thyroid tumors[12]. There are a few case reports of collision thyroid tumors with the synchronous presence of PTC. Medullary thyroid cancer is the most common type of thyroid collision tumor[13,14]. Synchronous OTC and PTC is extraordinarily rare, perhaps because OTC accounts for only 5% of all thyroid cancers. We reported a minimally invasive OTC combined with a PTC in a woman with a history of thyroid nodules for 8 years.

Genomic profiling revealed that the OTC harbored both nuclear and mitochondrial genomic variants, which might account for the high mutation burden and aggressive behavior. Matsuura et al[6] reported that OTC has a tendency toward more extensive vascular invasion and poorer clinical outcomes than follicular thyroid carcinomas. Capsular and/or vascular invasion, and infiltration of the surrounding thyroid parenchyma, necessitates preoperative diagnosis of OTC. Mitochondrial DNA variations are associated with partial or complete loss of function of the proteins forming the mitochondrial respiratory complex, with altered energy production by the Krebs cycle. Tumor cells attempt to compensate for the reduced or absent activity by increasing the number of mitochondria, as typically observed in OTC, which is responsible for the oncocytic staining avidity[1,15]. On ultrasonography, OTC tends to be larger and more hypoechoic, without specificity. In this case, although the OTC in the left thyroid lobe was larger than the right-lobe PTC, it was categorized as C-TIRADS III, while the right-lobe nodule was categorized as C-TIRADS IV. On contrast-enhanced CT, the right-lobe PTC showed an irregular margin and lymph node enlargement in the right lateral compartment. The left-lobe OTC demonstrated a regular margin but extension beyond the thyroid boundary. There was no lymph node enlargement in the left lateral compartment. The imaging characteristics of OTC are not well documented, and preoperative diagnosis is very challenging. In this case, imaging indicated that the PTC was more aggressive than the OTC, possibly because the OTC is microinvasive and the PTC might be late-stage given the patient’s 8-year history of thyroid nodules.

CONCLUSION

Synchronous OTC and PTC is extraordinarily rare. Preoperative differential diagnosis in the same patient remains challenging given the lack of well-documented imaging characteristics. Recognition of the imaging features of these synchronous tumors may facilitate preoperative treatment decision-making. Studies with more cases are needed to establish the imaging characteristics of synchronous thyroid oncocytic and papillary carcinomas.