Internal Medicine The Japanese Society of Internal Medicine
Adrenocortical Carcinoma Diagnosed by Endoscopic Ultrasound-guided Fine-needle Aspiration
Hiromune Katsuda’, Shomei Ryozawa1, Yuki Tanisaka’, Akashi Fujita’, Tomoya Ogawa’, Masahiro Suzuki’, Yoichi Saito’, Mei Hamada2, Masanori Yasuda2, Koshiro Nishimoto3 and Masafumi Mizuide 1
Abstract:
Adrenocortical carcinoma (ACC) is a rare malignancy with a very poor prognosis. A 77-year-old man un- derwent imaging studies due to poorly controlled hypertension, which revealed a mass measuring 43 mm in diameter near the left adrenal gland. There were no findings indicative of pheochromocytoma. Endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) was performed for the preoperative pathological evalu- ation, and the findings indicated a possibility of ACC. Based on these results, curative surgery was per- formed. If the diagnosis of pheochromocytoma is excluded, then EUS-FNA for adrenal lesions is relatively safe. It can also be used for the preoperative diagnosis of ACC.
Key words: adrenocortical carcinoma, EUS-FNA
(Intern Med 60: 3889-3896, 2021) (DOI: 10.2169/internalmedicine.7555-21)
Introduction
Adrenocortical carcinoma (ACC) is a rare malignant tu- mor with a reported frequency of 0.5-2 cases per 1 million individuals annually (1). It usually occurs in adults in the fourth to fifth decade of life (2). Additionally, a smaller peak is observed in children aged <5 years (3). It occurs more frequently in women than in men; the female to male ratio is between 2.5 and 3 to 1 (4). Approximately 55% of the affected patients present with symptoms indicative of hy- persecretion of adrenocortical hormones; 30-40% have symptoms related to the tumor volume, and 10% are asymp- tomatic (5). The mortality rate associated with ACC is >70% (6). Stages I, II, III and IV accounted for 3%, 29%, 19%, and 50% of the cases, respectively (7). Approximately 40% of the cases have distant metastases (8). The median duration of survival is 101 months for stages I and II, whereas it is 15 months for stages III and IV (2). Advanced cases have a poor prognosis.
ACC is a rare tumor that is sometimes difficult to differ- entiate when only imaging findings are used. Moreover, ow- ing to its rapid progression, few cases are diagnosed at an operable stage. In this report, we present a case of ACC di- agnosed by endoscopic ultrasound-guided fine-needle aspira- tion (EUS-FNA), which was surgically resectable.
Case Report
The patient was a 77-year-old man who had been treated by another doctor for hypertension for the past 3 years. His hypertension was poorly controlled by oral therapy; there- fore, he was referred to a hospital to rule out secondary hy- pertension. Abdominal computed tomography (CT) revealed a heterogeneous mass, measuring 43 mm in diameter, and abutting the left adrenal gland. The margins of the mass were enhanced on contrast imaging; however, the central part was not enhanced, thus indicating either degeneration or necrosis of the cyst (Fig. 1). T1-weighted magnetic reso- nance imaging (MRI) showed that the mass had low signal
Department of Gastroenterology, Saitama Medical University International Medical Center, Japan, 2Department of Pathology, Saitama Medical University International Medical Center, Japan and 3Department of Uro-Oncology, Saitama Medical University International Medical Center, Ja- pan
Correspondence to Dr. Shomei Ryozawa, ryozawa@saitama-med.ac.jp
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intensity. It also showed a faint high-signal area within the mass. T2-weighted MRI showed that the mass had a rela- tively high signal intensity. There was a high-signal region with liquid surface formation inside the mass. Fat- suppressed T2-weighted MRI showed no change in the in- ternal properties of the tumor compared with the normal T2- weighted MRI. These results indicated that the lesion was an adrenal mass with cystic degeneration containing blood components (Fig. 2). The results of endocrinological exami- nations are shown in Table 1. Specifically, under the admini- stration of candesartan cilexeil 12 mg/day, the plasma al- dosterone level was 126 pg/mL, the serum potassium level was 3.6 mEq/L, and the plasma renin activity was 0.4 ng/ mL/h. The aldosterone-renin ratio (ARR) was relatively high. However, iodine-131 adsterol scintigraphy showed a normal uptake in both adrenal glands (right, 2.1%; left, 1.4%) (Fig. 3). This suggested that it could be an aldosterone-secreting tumor. The level of serum adrenocorti-
cotropic hormone (ACTH) was 10.7 pg/mL and that of se- rum cortisol was 12.0 µg/dL. A low-dose dexamethasone suppression test revealed subclinical Cushing’s syndrome based on the serum ACTH level of 9.8 pg/mL and the un- suppressed serum cortisol level of 7.7 ug/dL. By contrast, the serum dehydroepiandrosterone sulfate (DHEA-S) level was 72 ug/dL, which was within the normal range.
He was referred to our hospital for further diagnosis and treatment. The levels of plasma adrenaline, noradrenaline, and dopamine were 136 pg/mL, 1,100 pg/mL, and 27 pg/ mL, respectively. The level of plasma noradrenaline was relatively high. However, the 24-hour urinary metanephrine was 0.15 mg/day, and normetanephrine was 0.23 mg/day, both of which were not elevated. Iodine-123 adrenal meta- iodobenzylguanidine (MIBG) scintigraphy showed no in- crease in the uptake of this tumor (Fig. 4). The possibility of pheochromocytoma was considered to be low. The lesion was relatively large with hormone secretion, and there was a
| Pre-operation | Post-operation | Normal range | |
|---|---|---|---|
| Hormonal profile | |||
| Serum ACTH (pg/mL) | 10.7 | 16.2 | 7.2-63.3 |
| Serum cortisol (ug/dL) | 12.0 | 11.9 | 3.7-19.4 |
| Plasma renin activity (ng/mL/h) | 0.4 | 0.8 | 0.3-2.9 |
| Plasma aldosterone concentration (pg/mL) | 126 | 77.0 | 35.7-240 |
| Serum DHEA-S (µg/dL) | 72 | 54 | 5-253 |
| Plasma adrenaline (pg/mL) | 136 | N/A | 0-100 |
| Plasma noradrenaline (pg/mL) | 1,100 | N/A | 100-450 |
| Plasma dopamine (pg/mL) | 27 | N/A | 0-20 |
| 24-hour urinary metanephrine (mg/day) | 0.15 | 0.22 | 0.05-0.20 |
| 24-hour urinary normetanephrine (mg/day) | 0.23 | 0.44 | 0.10-0.28 |
| Low dose dexamethasone suppression test | |||
| Serum ACTH (pg/mL) | 9.8 | ||
| Serum cortisol (ug/dL) | 7.7 |
ACTH: adrenocorticotropic hormone, DHEA-S: dehydroepiandrosterone sulfate
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possibility of malignancy; therefore, surgery was considered, and a biopsy was performed for the preoperative evaluation.
EUS (GF-UCT260; Olympus Optical Tokyo, Japan) de- tected a 38-mm diameter mass adjacent to the left adrenal gland via a gastric approach. It was not continuous with the tail of the pancreas or the left kidney. The surface was smooth, with cystic degeneration inside; however, there was no obvious calcification. EUS-FNA was performed via the gastric approach, and two passes were made with a 22- gauge needle (Acquire; Boston Scientific, Marlborough, USA). Solid lesions of the tumor edges were punctured (Fig. 5). No fluctuations in blood pressure occurred either during or after the procedure. The histopathological findings were as follows: Atypical cells with round nuclei and mostly eosinophilic cytoplasm were seen in alveolar-like patterns. There were some swollen nuclei; however, the overall nu- clear atypia was mild to moderate, and the mitotic image was unclear. Immunohistologically, the tumor cells were positive for steroidogenic factor-1 (SF-1) and negative for S 100 protein, cytokeratin AE1/AE3, and chromogranin A, and
the Ki-67 index was approximately 30% (Fig. 6). Based on the above, the possibility of a primary adrenal tumor, espe- cially ACC, was suspected.
Left adrenal resection was performed, and the left adrenal gland and adrenal tumor were excised as a single mass. The excised material was a 9.5-6.5 cm mass containing a cyst with internal hemorrhaging and normal adrenal glands. Histopathologically, there was a diffuse proliferation of atypical cells with eosinophilic cytoplasm in most regions of the tumor. Partially, there were myxoid areas of mucus deposition in the stroma. Overall, the tumor cells had nu- clear atypia, and some mitotic images were observed [>5/50 high power field (HPF)], but no atypical mitotic images were observed. Coagulation necrosis was observed in the tu- mor. The tumor invaded the capsule; however, extracapsular invasion was unclear. Elastica van Gieson (EVG) staining showed venous and sinusoidal capillary invasion; however, no lymphatic invasion was observed. Immunohistologically, SF-1 was positive, and the Ki-67 index was approximately 15% (Fig. 7). Seven of the Weiss criteria (9, 10) (Table 1)
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were met: nuclear atypia, an increased mitotic rate, the per- centage of clear cytoplasm, coagulation necrosis, invasion of venous and sinusoidal structures, and capsular invasion. Considering the presence of mucus in the tumor stroma, it was diagnosed as an ACC of myxoid variant type. The final pathological stage was T2N0M0 stage II. After the surgery, his hormone levels, including aldosterone and renin, normal- ized (Table 1), and the antihypertensive medication could also be reduced. We recommended adjuvant therapy with mitotane, but he declined, so he has thereafter been carefully monitored on an outpatient basis.
Discussion
ACC most commonly presents with features of excessive hormonal secretion or symptoms of compression due to the
enlarging mass. An increasing percentage of patients with ACC are diagnosed with incidentaloma during abdominal imaging (12). In the case of adrenal incidentalomas, it is es- pecially important to differentiate primary benign lesions from malignant lesions and to rule out metastasis for the proper management and staging of each case. Most adrenal incidentalomas are benign, and the determination of the ma- lignant potential of an adrenal mass depends on the size of the lesion, imaging features, and hormonal status (13). Tu- mors measuring greater than 40 mm and heterogeneous en- hancement on CT are important discriminators of malig- nancy in adrenal incidentalomas (14). In this case, the tumor diameter was 43 mm, which was large, and the contrast en- hancement on CT was heterogeneous, thus leading to a sus- pected malignancy. ACC often shows a low-attenuation cen- tral region on CT that represents tumor necrosis, irregular
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contrast enhancement, calcification, and a thin capsule-like margin surrounding the tumor (15). On ultrasound imaging, ACC usually appears as a rounded or oval well-defined hy- poechoic mass, with a few displaying a thick partial or com-
plete echogenic rim (16). Although conventional imaging modalities, as mentioned above, are used to rule out adrenal involvement in different malignancies, false-positive and negative-results have been observed in approximately 10%
| Location | US | CT | MRI | Endocrinology | Histology | |
|---|---|---|---|---|---|---|
| Adrenocortical carcinoma | Cortex | Large (>6 cm), oval, hypoechoic, heterogeneous, hypervascular, hemorrhage, necrosis, echogenic rim, calcifications | High attenuation (>10 HU), heterogeneous contrast enhancement, invasions, metastases | Hetero-intensity on both T1WI and T2WI, small signal loss on out-of-phase images (<30%) | Cushing syndrome or virilization, less commonly Conn's syndrome or feminization (if functional) | SF-1 (+), high Ki-67 index |
| Pheochromocytoma | Cortex | Large (>5 cm), well-defined, hypoechoic, hypervascular, cystic necrosis, calcifications | High attenuation (>10 HU), homogenous contrast enhancement | Hyperintensity on T2WI referred to as "light bulb sign" | Secreting catecholamine, sometimes Cushing syndrome, high uptake on MIBG scintigraphy | Chromogranin A (+) |
| Adrenal adenoma | Medulla | Small (<3 cm), oval, well-defined, hypoechoic, homogenous, hypovascular | Low attenuation (<10 HU), homogeneous, mild contrast enhancement | Signal loss on out-of-phase images (>20%) | Cushing syndrome or Conn's syndrome (if functional) | SF-1 (+), low Ki-67 index |
| Adrenal metastasis | Cortex and medulla | Usually bilateral, <3 cm, solid homogeneous; large, heterogeneous by necrosis or hemorrhage | Other metastases lesions, high attenuation (>10 HU), less contrast washout | Hypointensity on T1WI, hyperintensity on T2WI, lack of signal loss on out-of-phase images | - | Depending on a primary |
| Adrenal lymphoma | Interstitial | Large (average 8 cm), well-defined, hypoechoic, homogeneous, mimicking cysts, no calcifications | Low attenuation, homogeneous, mild to moderate contrast enhancement | Hypointensity on T1WI, hetero- hyperintensity on T2WI | - | Atypical lymphocyte |
| Ganglioneuroma | Medulla | Large (>5 cm), irregular, hyperechoic, homogeneous, calcifications | Low attenuation, homogeneous, mild and progressive contrast enhancement | Low homointensity on T1WI, hetero- hyperintensity on T2WI | - | Mature ganglion cells, Schwann cells, mucous matrix and nerve fibers |
| Adrenal hemorrhage | Cortex and medulla | Oval, mild echoic in the center of adrenal glands | High attenuation (50-90 HU), surrounded by fat stranding | Depending on the age of the hematoma | - | No solid components |
| Adrenal pseudocyst | Cortex and medulla | Well-defined, cystic fluid, wall calcifications | Cystic structure with thin wall | Depending on the age of the hematoma | - | No solid components |
| Adrenal hemangioma | Interstitial | Large (2.5-25 cm), oval, well-defined, heterogeneous, hemorrhage, calcifications | Peripheral patchy enhancement with central filling | Hyperintensity on T2WI and focal hyperintensity on T1WI | - | Angioblastic cells |
US: ultrasound, CT: computed tomography, MRI: magnetic resonance imaging, HU: Hounsfield unit, T1WI: T1-weighted image, T2WI: T2-weighted image, SF-1: steroidogenic factor 1, MIBG: metaiodobenzylguanidine
of the cases (17). In addition, ACC has imaging findings similar to those of pheochromocytoma, adrenal adenoma, adrenal metastasis, adrenal lymphoma, ganglioneuroma, ad- renal hemorrhaging, adrenal pseudocyst, and adrenal heman- gioma (Table 2) (18-23). Although malignancy was sus- pected in this case, it was difficult to differentiate ACC from other diseases such as pheochromocytoma, adrenal lym- phoma, and adrenal metastasis based on the imaging find- ings alone. Therefore, endocrinological examinations were necessary. When evaluating some primary adrenal neo- plasms, the differential diagnoses can be refined by labora-
tory biochemical testing, including serum cortisol, aldoster- one, and metanephrine measurements (24). ACC secretes various hormones, including androgens, cortisol, estrogen, and aldosterone (25). Among adult patients with ACC, 30% present with Cushing’s syndrome and 20% with virilization. Feminization and hyperaldosteronism are much rarer, ac- counting for approximately 2% of the cases (26). In the pre- sent case, subclinical Cushing’s syndrome was revealed by the low-dose dexamethasone suppression test. Although the accumulation of lesions was not clear on iodine-131 adsterol scintigraphy, the plasma aldosterone level and plasma renin
Table 3. Weiss System for Differentiating Benign from Malignant Adre- nocortical Neoplasms (9, 10).
Criteria
1. High nuclear grade [grade 3 or 4 according to the criteria of Fuhrman et al. (11)]
2. Mitotic rate greater than 5 per 50 high-power fields
3. Atypical mitoses
4. Clear cells comprising ≤25% of the tumor
5. Diffuse architecture (greater than one-third of the tumor)
6. Necrosis
7. Invasion of venous structures
8. Invasion of sinusoidal structures
9. Invasion of capsule of tumor
* The presence of three or more criteria correlates with subsequent malignant behavior.
activity revealed the aldosterone production capacity of the tumor. However, the DHEA-S level was within the normal limits. Endocrinological examinations were somewhat atypi- cal, but ACC was suspected first, considering the imaging findings. Resection was considered, and a pathological ex- amination was performed to confirm the diagnosis before surgery.
Adrenal FNA for the diagnosis of predominantly solid masses gained attention in the 1970s and has been increas- ingly used in clinical practice following improvements in imaging technologies and deep-seated FNA techniques (27). For decades, adrenal FNA has been primarily performed by interventional radiologists using percutaneous approaches guided by CT. In recent years, EUS-FNA advancements have provided an alternative approach for the biopsy of ad- renal mass lesions. EUS-FNA sampling of the adrenal gland started in the 1990s and has become more common with im- provements in technology and equipment (28). EUS is use- ful as a diagnostic imaging modality because of its superior resolution, and it also provides direct access to the left and sometimes to the right adrenal glands. Complications of FNA in the adrenal glands, such as adrenal hematoma, ab- dominal pain, adrenal abscess formation, and tumor recur- rence along the needle track, have been reported but are in- frequent (29). In a review of 416 patients who underwent EUS-FNA of the adrenal glands, no major complications were reported, except for one case of adrenal hemorrhag- ing (30). EUS-FNA of the adrenal gland can be performed safely. However, if the targets of the puncture are pheochro- mocytomas, extreme caution is required because it might cause hemorrhaging and hypertensive crisis (31). When per- forming EUS-FNA for adrenal tumors, it is important to rule out pheochromocytoma. In addition, we always have phento- lamine, an alpha-blocker, on standby, to deal with a hyper- tensive crisis if it occurs. In this case, the iodine-123 adrenal MIBG scintigraphy showed no accumulation in the lesion, and 24-hour urine metanephrine and normetanephrine levels were within the normal limits, suggesting a low probability of pheochromocytoma. However, we took all possible prepa- rations for the examination and were able to perform the
procedure safely.
Pathologically, ACC is one of the most difficult tumors to differentiate benign disease from malignancy, and it is often impossible to distinguish a benign tumor from amalignant tumor using only commonly used indices such as nuclear atypia and vascular invasion. A scoring system that com- bines multiple indices is recommended for the diagnosis of ACC, and the Weiss criteria are the most commonly used (9, 10) (Table 3). It is useful in that it is simple and can diagnose ACC based on the pathological findings alone. ACC can be diagnosed using EUS-FNA; however, it is im- portant to understand that there are certain limitations to this diagnosis. To diagnose ACC accurately, an evaluation of the entire lesion after surgery is necessary. However, EUS is a useful tool to confirm the location of the tumor and adjacent organs, and EUS-FNA allows for pathological evaluations including immunostaining. ACC is often difficult to differen- tiate from other diseases based on imaging, as it sometimes shows endocrinologically atypical characteristics. Preopera- tive pathological evaluations are important because it can identify benign and malignant tumors and exclude other ma- lignant tumors such as pheochromocytoma, adrenal metasta- sis, and adrenal lymphoma. Therefore, it is worthwhile to consider tissue sampling by EUS-FNA before performing surgical resection. ACC is a rare tumor, and there are few reports of cases diagnosed by EUS-FNA. To the best of our knowledge, only three cases of ACC diagnosed using EUS- FNA have so far been reported (32-34). This case is valu- able because the ACC was diagnosed using EUS-FNA and then surgically resected.
We encountered a rare case of ACC diagnosed using EUS-FNA. When performing EUS-FNA for adrenal tumors, it is important to rule out pheochromocytoma in advance. There were no major complications at the time of examina- tion, and complete resection was possible based on the diag- nosis. An early diagnosis of ACC and surgery is important for improving the prognosis. In conclusion, EUS-FNA is therefore considered to be useful for the preoperative diag- nosis of ACC.
The authors state that they have no Conflict of Interest (COI).
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