Micropapillary Thyroid Carcinoma and ConcomitantEctopic Thyroid Tissue in the Adrenal Gland:

Metastasis or Metaplasia?

Brittany N. Bohinc,1 John C. Parker,2 William W. Hope,3 Cyrus Kotwall,3 John Turner,4

Wanli Cheng,4 and Ricardo V. Lloyd 5

Background: Ectopic thyroid tissue is a rare finding but has been reported in many thoracic and abdominallocations. It is usually an incidental pathologic finding after an unrelated surgical intervention. When thyroidtissue is found outside the thyroid bed, it is important to rule out thyroid cancer metastasis.Patient Findings: We present a case of a 61-year-old African American woman who was incidentally found tohave concomitant ectopic thyroid tissue in the adrenal gland and a papillary thyroid microcarcinoma (PTMC) inthe right lobe of the thyroid.Summary: The concurrent finding of ectopic thyroid tissue and PTMC posed the diagnostic dilemma of whetherthe extrathyroidal tissue was metastasis or metaplasia, with very different treatment implications. Althoughmany of these incidental micropapillary cancers are indolent, some patients do experience local or distantmetastasis. Therefore, it is important to delineate which of these microtumors are likely to metastasize. Sometumor markers and gene mutations have been proposed to help differentiate the more benign tumors from themore aggressive tumors, but there is currently no standard method for determination of metastatic potential.Conclusions: Here we present the seventh known case of ectopic thyroid tissue in the adrenal gland and the firstcase of concomitant incidental PTMC in the setting of this ectopic tissue finding. Using this case, we discuss thediagnostic and therapeutic challenges faced and propose the use of biomarkers to help determine the metastaticpotential of these tumors.

Introduction

Ectopic thyroid tissue, especially outside the thoraciccavity or ovaries, is very rare. When thyroid tissue is

found in ectopic locations it is important to rule out meta-stases from thyroid cancer. Here we report a patient withthyroid tissue in the left adrenal gland and describe the stu-dies performed to determine if it was an ectopic rest of benignthyroid tissue or metastatic thyroid carcinoma.

Patient

A 61-year-old African American woman presented withrefractory hypertension, hypokalemia, and metabolic alkalo-sis consistent with hyperaldosteronism. She underwent al-dosterone and renin screening, a saline suppression test,computed tomography (CT) imaging of the abdomen/pelvis,and bilateral adrenal venous sampling. A sub-centimeter left-sided adrenal adenoma was discovered with a 10:1 lateraliz-

ing ratio, confirming appropriate aldosterone production.Laparoscopic left adrenalectomy was performed as definitivetreatment.

Pathology examination of the lesion revealed a 0.8 cm ad-renocortical nodule consistent with a functioning adenoma.There was also an unexpected finding; an adrenal rest con-sisting of bland thyroid tissue and ossification spanning sev-eral millimeters in diameter was found directly adjacent toand within the capsule of the adenoma (Figure 1A, B, C).Immunohistochemical staining of the thyroid tissue withthyroglobulin (Tg) confirmed a thyroid focus.

Because of this unexpected pathologic finding, a work-upwas performed to evaluate for thyroid cancer. The patienthad no high-risk history, including no history of childhoodhead or neck irradiation and no family history of thyroidcarcinoma. Thyroid function tests were performed and re-vealed a thyroid-stimulating hormone (TSH) of 1.12 mIU/mL(reference range, 0.550–4.780). Thyroid ultrasonography re-vealed a multinodular goiter with the following lesions: a

1Division of Diabetes, Endocrinology, and Metabolism, Duke University Hospital, Durham, North Carolina.2Endocrinology Department, Wilmington Health Associates, Wilmington, North Carolina.Departments of 3Surgery and 4Pathology, New Hanover Regional Medical Center, Wilmington, North Carolina.5Department of Pathology, University of Wisconsin, Madison, Madison, Wisconsin.

THYROIDVolume 21, Number 9, 2011ª Mary Ann Liebert, Inc.DOI: 10.1089/thy.2010.0390

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right-sided 4.5�4.1�4.3 mm hypoechoic nodule with rimcalcification and minimal circumferential vascularity, a larger18.2�14.2�7.8 mm mixed lesion in the isthmus, and twolarger nodules in the left lobe (19.6�14.8�15.0 mm, supe-rior and isoechoic and 19.0�13.2�17.0 mm, inferior andhypoechoic). None of the nodules had ultrasonographycharacteristics that were particularly worrisome for carci-noma. Central and lateral neck lymph node evaluation wasalso done and was negative for abnormal-appearing nodes.In concordance with the American Thyroid Association(ATA) guidelines (1), a fine-needle aspiration (FNA) biopsy ofthe two left-sided lesions was performed. The left superiorthyroid nodule consisted of follicular epithelial cells with focalHurthle cell change, colloid, and rare histiocytes favoringnon-neoplastic goiter. The left inferior thyroid nodule con-sisted of Hurthle cells, rare pigment-laden macrophages, andmultinucleated giants cells and colloid. In both specimens,comment was made of focal Hurthle cell change and rareatypia with possibility of vague intranuclear inclusionsand nuclear grooves, which were thought to be artifactual inorigin. Still, the pathologist could not completely rule out aneoplastic process. Because of the finding of thyroid tissuein the adrenal gland and the inconclusive outcome of the FNAbiopsy, the patient underwent total thyroidectomy withlymph node sampling.

Pathological evaluation of the thyroid gland revealed a5 mm papillary thyroid microcarcinoma (PTMC), follicularvariant, in the right lobe corresponding to the small hy-poechoic nodule with rim calcification seen on presurgicalultrasonography. The PTMC was well encapsulated withoutcapsular or vascular invasion and had no other aggressivefeatures (Fig. 1D). The isthmus nodule and the two left-sidedlesions that were inconclusive on FNA biopsy were charac-terized as nodular hyperplasia without atypia.

Immunostaining of the PTMC for Hector Battifora meso-thelial antigen-1 (HBME-1) was strongly positive in a sig-nificant portion of the nodule. Galectin-3 (GAL3) andcytokeratin-19 (CK19) were negative. Further studies oftumor aggressiveness, including the cyclin D-1 immunostainand the BRAFV600E mutation, were negative.

After thyroidectomy, the patient was placed on levothyr-oxine replacement therapy. She underwent recombinanthuman TSH-stimulated whole-body I-131 uptake scan (I-131WBS) that showed residual thyroid tissue in the thyroidbed but no focus of thyroid tissue elsewhere. StimulatedTg measured 1.8 ng/mL with simultaneous undetectable Tgantibody.

Both the thyroid PTMC and adrenal thyroid rest were re-viewed by consultant pathologists, with unanimous agreementof benign ectopic thyroid tissue located in the adrenal and in-cidental, unrelated PTMC. The patient was found to have StageI micropapillary thyroid cancer and treated with suppressivedoses of levothyroxine to a TSH goal of 0.1–0.5mIU/mL. Shewill be followed with serial ultrasonography and thyroglobulinlevels and will not be given I-131 ablative therapy.

Discussion

PTMC: a growing disease burden

The World Health Organization and the ATA describemicrocarcinoma of the thyroid gland as any tumor measuring

<1 cm in greatest diameter (1,2). This diagnosis is common, as10%–20% of thyroid cancer diagnosed currently fall under theheading of microcarcinoma (3). In addition, there are likelymany more cases that go undiagnosed, with some autopsystudies quoting an incidence of 5%–35% (4–6). Because ofadvances in ultrasonography detection of these tumors andother possible undefined reasons, the incidence of thyroidmicrocarcinoma continues to rise, with most tumors identi-fied as PTMC (7).

Most micropapillary thyroid tumors are not aggressive andcan be surgically cured with total or near-total thyroidectomy.Still, local and distant metastases have been described (8–13),most often to the lymph nodes, lung, and bone. The preva-lence of distant metastasis in PTMC is reported at 0.2%–3%with a mortality rate of 0.2%–1% (8,10). Adrenal metastasesare rare in larger papillary thyroid carcinoma (14,15), andhave never been described in PTMC.

Aggressive characteristics of PTMCs

Several tumor characteristics have been reported to be as-sociated with increased tumor aggressiveness. Unifocal dis-ease has been thought to be less aggressive than multifocaldisease, with multiple reports showing an increased risk oflymph node metastases and distant metastases in multifocaltumors (1,8,12). In addition, tumor size <8 mm has been as-sociated with a very low prevalence of metastases (16,17).Cervical lymph node involvement is also predictive of meta-static potential and recurrence (18). Our patient had only onesmall focus of disease (5 mm) and no evidence of lymph nodeinvolvement by preoperative neck ultrasonography, in-traoperative direct lymph node observation, or by postoper-ative thyrogen-stimulated thyroglobulin and I-131 WBS.Other benign features included a well-defined capsule with-out tumor invasion.

The usefulness of immunohistochemistryin determining metastatic potential of microtumors

There have been multiple reports citing the utility of posi-tive GAL3, fibronectin-1 (FN1), cbp/p300 interacting trans-activators with glutamic acid [E] and aspartic acid [D]–richc-terminal domain, 1 (CITED1), HBME-1, and CK19 immu-nohistochemistry in determining malignant potential in thy-roid nodules (19–22). One report cited a 95% sensitivity forthyroid cancer (whether papillary, follicular, Hurtle, or ana-plastic) if the tumor was positive for co-expression of multipleproteins and a 96% specificity for a benign tumor if all stainswere negative (20). The thyroid tissue found in the adrenalgland stained positive for thyroglobulin, but was negative forHBME-1 and GAL3 and equivocal for CK19, making meta-static disease less likely. The PTMC itself stained stronglypositive for HMBE-1 but was negative for GAL3 and for CK-19, suggesting a difference in immunophenotype between thetwo thyroid foci.

Cyclin D-1 immunostaining was also performed on thePTMC to help determine tumor aggressiveness and likelihoodof metastatic disease. One study showed that cyclin D-1protein overexpression helped to predict metastatic behaviorin thyroid papillary microcarcinoma (23). Multiple otherstudies have shown increased tumor aggressiveness with thismarker in several other forms of cancer (24–26). According totheir study criteria, tumors were considered positive for cyclin

1034 BOHINC ET AL.

D-1 overexpression if there was moderate to intense nuclearstaining (>10% of tumor cells) and if there was diffuse dis-tribution of positive cells within the tumor (23). Our patient’stumor had some faint nuclear staining in <5% of thyroid cellsin a localized distribution and, therefore, was considered anegative expressor of cyclin D-1.

BRAF mutations have been linked to more aggressivetumor behavior in papillary thyroid carcinomas, withincreased metastatic potential compared to tumors withRET/PTC rearrangements, RAS mutations, or other muta-tions of the mitogen activated protein kinase pathway(MAPK) (27). Multiple studies examining BRAF mutations(especially the T1799A point mutation) in thyroid carcinomahave reported a significant association with lymph nodespread, extrathyroidal invasion, and distant metastasis (28–

31). Our patient’s primary PTMC did not have a BRAFmutation.

Current ATA guidelines (1) suggest consideration of thesemolecular markers (i.e., BRAF, RAS, RET/PTC, Pax8-PPARy,and galactin-3) in patients with indeterminate FNA cytology.It may also be worthwhile to consider expanding the use ofthese markers to a select group of patients with PTMC, as itmay be useful in stratifying risk in the growing number ofpatients with thyroid microcarcinoma, some of whom mayhave risk for more aggressive tumors.

Ectopic thyroid tissue: metastasis or metaplasia?

Because of the benign tumor characteristics and negativemetastatic work-up, it is highly unlikely that the PTMC found

FIG. 1. (A) Adrenocortical adenoma. Well-circumscribed and encapsulated 8 mm nodule histologically resembling normaladrenal fasciculata. Dystrophic calcification present in the capsule (top). Thyroid tissue also noted in the capsule (lower left).(B) Ectopic thyroid tissue in the adrenal gland showing normal appearing thyroid tissue and adjacent adrenal cortical tissue.The ectopic thyroid shows focal chronic lymphocytic inflammation. (C) Higher magnification of ectopic thyroid and adjacentadrenal cortex. The thyroid cells have round, small nuclei, and cytological features of papillary thyroid carcinoma are absent.(D) Follicular variant of papillary thyroid microcarcinoma, 5 mm, with cytological features of papillary carcinoma includingenlarged, irregular nuclei with nuclear clearing and a few nuclear grooves.

PAPILLARY THYROID MICROCARCINOMA AND ECTOPIC THYROID IN ADRENAL TISSUE 1035

in the adrenal gland was a metastasis and is more consistentwith ectopic thyroid tissue. Ectopic thyroid tissue in theadrenal has been described six other times in the Japanese lit-erature, but has never been described in other patient popu-lations (32–36) (Table 1). One case reported by Hagiuda et al.(36) described ectopic thyroid tissue found after adrenalectomyfor an aldosterone-producing adenoma, similar to the one wehave presented. Although there may be an association betweenthe two conditions, the apparent association between the twofindings may be coincidental as adrenalectomy is most oftenperformed for functional adrenal adenoma.

Most of the previously reported cases discovered thyroidtissue in a cystic adrenal lesion. Adrenal adenomas with ec-topic thyroid rests were either discovered incidentally onimaging and were removed because of their size (3–4 cm), orthey were surgically resected after a positive hormonal work-up (with hormonally active lesions found to be smaller in size)(Table 1). Despite finding thyroid tissue outside of the thyroidbed, thyroidectomy was not performed in the work-up of anyof the previously reported cases. Instead, the thyroid glandwas imaged with MRI, I-123 scintigraphy, CT scan, or ultra-sonography, none of which revealed intrathyroidal lesionssuggestive of malignancy.

Ectopic thyroid tissue is not unusual in the neck, medias-tinum, or anywhere along the pathway of thyroid decent fromthe base of the tongue to the anterior trachea. Inexplicably,ectopic thyroid foci have also been found below the dia-phragm in the abdomen. Ectopic thyroid has been reported inthe gallbladder (37), ovary (38), small intestinal mesentery(39), pancreas (40), duodenum (41), vagina (42), inguinal re-gion(43), porta hepatis (44), and the perisplenic area (45).Thyroid tissue found in the adrenal gland or in other intra-abdominal locations is hard to understand as far as currentlyavailable embryological information is concerned. For exam-ple, the adrenal gland develops from the ectoderm and themesoderm, whereas the thyroid develops from the endoderm.Past explanations for why thyroid tissue can be found intra-abdominally include metaplasia, choristomatous tissue, over-descent of the hypoglossal duct remnant, or the developmentof teratoma. The etiology is unknown.

Conclusion

The discovery of concomitant PTMC and intra-adrenalectopic thyroid tissue presented an interesting and uniquediagnostic dilemma. Making the diagnosis was not only animportant academic exercise, but was vital in determining thepatient’s need for radioactive iodine ablation. The latest ATAguidelines (1) for differentiated thyroid cancer treatmentclassify any subcentimeter intrathyroidal tumor as stage I,with recommendation against radioactive ablative therapy.In contrast, any distant metastasis, regardless of the initialtumor size, is classified as stage IV-C. For stage IV-C diseaseI-131 ablation is recommended as well as more vigorousand frequent surveillance.

As the prevalence of PTMC increases with improvementsin imaging technology, it is likely that more cases of con-comitant PTMC and ectopic thyroid tissue will emerge.Therefore, it may be prudent to determine the degree ofPTMC aggressiveness with immunohistochemical staining,molecular markers, or other methods to determine whetherextrathyroidal foci are likely metastases or simply benignectopic tissue. Classifying PTMC metastatic potential will alsohelp to guide management and longitudinal follow-up. Fur-ther research is needed to determine which markers are mostuseful in determining the aggressiveness of PTMC.

Disclosure Statement

The authors have no disclosures to declare and no com-peting financial interests exist. All authors attest to the accu-racy and integrity of the article.

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Table 1. Summary of All Reported Cases of Ectopic Thyroid Tissue Found in the Adrenal Gland

Patient Reference Gross Pathology Thyroid cancer evaluation Discovered

61-year-oldwoman

Tsujimura et al. (32) Right cystic adrenallesion: 3.5 cm

Imaging not specified; noevidence of cancer

Incidental CT abdomen

50-year-oldwoman

Shiraishi et al. (33);Patient 1

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CT and ultrasonography;No evidence of cancer

Incidental CT abdomen

50-year-oldman

Shiraishi et al. (33);Patient 2

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Incidental CT abdomen

50-year-oldwoman

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Incidental CT abdomen

67-year-oldwoman

Takao et al. (35) Left cystic adrenallesion: 3 cm

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Incidental CT abdomen

54-year-oldwoman

Hagiuda et al. (36) Left cystic adrenallesion: 8 mm

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61-year-oldwoman

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Thyroid ultrasonography andthyroidectomy; papillarymicrocarcinoma

Primary hyperaldosteronism

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Address correspondence to:Brittany N. Bohinc, M.D.

Department of Endocrinology, Diabetes, and MetabolismDuke University Hospital

2301 Erwin RoadDurham, NC 27710

E-mail: brittany.bohinc@duke.edu

1038 BOHINC ET AL.