Endoscopic Ultrasound-Guided Fine-Needle Aspiration of Right Adrenal Masses Report of 2 Cases

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1 Case Series Endoscopic Ultrasound-Guided Fine-Needle Aspiration of Right Adrenal Masses Report of 2 Cases John M. DeWitt, MD Objective. Although transgastric endoscopic ultrasound (EUS)-guided biopsy is a safe and accurate method for sampling of the left adrenal gland, only 2 reports describing EUS-guided fine-needle aspiration (FNA) of the right adrenal gland have been published to date. The aim of this series was to report 2 additional successful cases of EUS-FNA of right adrenal masses. Methods. In this retrospective single-center case series, prospectively updated cytology and EUS databases between January 1997 and September 2007 were reviewed to identify all patients who underwent attempted EUS-FNA of either adrenal gland. Those who underwent EUS-FNA of the right adrenal gland were identified and reviewed. Results. Of 52 consecutive patients who underwent EUS-FNA of either adrenal gland, 2 had attempted biopsy of the right adrenal gland and constituted the study population. The first patient had a history of colon cancer and was found to have a right adrenal mass during workup of jaundice. The second patient also had a history of colon cancer and was found to have an enlarging right adrenal mass and a subcarinal mass during follow-up computed tomography. Endoscopic ultrasound-guided FNA showed a pheochromocytoma in the first patient and metastatic colon cancer in the second patient. No complications were encountered during either procedure. Conclusions. This series further shows that EUS-FNA of right adrenal masses is feasible and may be an option for sampling of these lesions. Prospective studies comparing EUS with percutaneous FNA of adrenal masses are indicated to help delineate the indications and limitations of each technique. Key words: adrenal gland; endoscopic ultrasound; fine-needle aspiration. Abbreviations CT, computed tomography; EUS, endoscopic ultrasound; FNA, fine-needle aspiration Received October 2, 2007, from the Department of Medicine, Division of Gastroenterology and Hepatology, Indiana University School of Medicine, Indianapolis, Indiana USA. Revision requested October 18, Revised manuscript accepted for publication November 5, Address correspondence to John M. DeWitt, MD, Department of Medicine, Division of Gastroenterology, Indiana University Medical Center, 550 N University Blvd, UH 4100, Indianapolis, IN USA. jodewitt@iupui.edu Management of incidentally discovered adrenal masses (incidentalomas) is difficult and involves assessment of any malignant potential and excessive hormone production. Most incidentalomas are benign, nonfunctioning tumors and usually are well characterized by state-ofthe-art abdominal imaging without tissue sampling. However, 2% of incidentally discovered adrenal masses smaller than 4 cm are malignant, a risk that increases to 25% for those larger than 6 cm. 1 During staging of patients with cancer, however, 75% of adrenal masses found represent metastatic lesions. 2 Nonsurgical diagnosis of adrenal masses may help initially identify or further stage malignancy as well as help guide appropriate nonsurgical or surgical management. Adrenal masses are traditionally sampled by percutaneous biopsy 3 12 ; however, there is increasingly reported experience using endo by the American Institute of Ultrasound in Medicine J Ultrasound Med 2008; 27: /08/$3.50

2 Endoscopic Ultrasound-Guided Aspiration of Right Adrenal Masses scopic ultrasound (EUS)-guided fine-needle aspiration (FNA) or Tru-Cut biopsy 22 for this indication. Transduodenal EUS imaging of the right adrenal gland is considered more difficult than transgastric imaging of the left adrenal gland. In fact, EUS shows a normal or minimally enlarged left adrenal gland in 98% of patients compared with only 69% by transabdominal ultrasound. 23 A normal or minimally enlarged right adrenal gland, however, is seen in only 30% of patients on EUS, whereas transabdominal ultrasound may permit detection in nearly all patients. 23 Therefore, EUS- FNA is attempted more often for left compared with right adrenal glands. To date, there have only been 2 reports of EUS-FNA of the right adrenal gland. 18,20 Here, 2 additional cases of EUS-FNA of the right adrenal gland are reported. Materials and Methods This retrospective single-center case series was approved by the Institutional Review Board at Indiana University Medical Center/Clarian Health Partners. Prospectively updated cytology and EUS databases at our hospital were reviewed to identify all patients who underwent attempted EUS-FNA of either adrenal gland between January 1997 and September Those who underwent EUS-FNA of the right adrenal gland were identified and constituted the study population. Hospital and endoscopy records were reviewed for demographic data, procedural indications, EUS findings, cytologic results, previous imaging results, and any complications. Per the institution protocol, all patients were telephoned within 48 hours after EUS imaging to assess for any other short-term complications. Follow-up data regarding the patient outcome, treatment, surgery, and clinical course were also collected from medical records and referring physicians. Endoscopic ultrasound examinations in all patients were performed after written informed consent was obtained. Conscious sedation was given with various combinations of intravenous midazolam, meperidine, fentanyl, or propofol under appropriate cardiorespiratory monitoring. Transduodenal imaging of the right adrenal gland with EUS was performed with the endoscope in the long position along the greater curve of the stomach. The inferior vena cava or the right kidney was then visualized, and the right adrenal gland was uniformly present between the superior pole of the right kidney and the inferior vena cava. Endoscopic ultrasound-guided FNA was performed with on-site cytology support for rapid interpretation of each specimen. According to our routine endoscopy unit protocol, patients were monitored in the recovery area after EUS imaging for at least 60 minutes before discharge; no additional monitoring was performed after adrenal biopsy. Per the department policy, all patients were telephoned 48 hours after each procedure to assess for short-term complications. Results During the study period, 52 consecutive patients underwent EUS-FNA of either the left (n = 50) or right (n = 2) adrenal gland. The following section describes the 2 procedures for biopsy of the right adrenal gland. Case Descriptions Case 1 A 57-year-old man with a history of mental retardation, schizophrenia, and alcohol abuse had an 18-month history of upper abdominal pain. Six months before referral, the patient had undergone laparoscopic cholecystectomy for biliary colic. No intraoperative cholangiography was done. Postoperatively, hematochezia developed. A colonoscopy showed rectal cancer, for which low anterior resection and colostomy were performed. No preoperative computed tomography (CT) was performed. After a prolonged hospitalization, the patient was eventually discharged. Two months after discharge, painless jaundice developed. Computed tomography showed pancreatic head calcifications, a dilated main pancreatic head, and a 3-cm right adrenal mass (Figure 1A). No pancreatic mass was noted. Endoscopic retrograde cholangiopancreatography showed a smooth distal 15-mm biliary stricture with diffuse dilatation of the upstream bile ducts and intrahepatic bile ducts. The stricture was dilated, and a plastic stent was placed. 262 J Ultrasound Med 2008; 27:

3 DeWitt Results of limited pancreatography in the head were normal, and brush cytologic findings from the biliary stricture were negative for malignancy. The patient was then referred for EUS to exclude a pancreatic mass or chronic pancreatitis and for biopsy of the right adrenal mass. Curvilinear array EUS (GF-UC140P; Olympus America, Inc, Center Valley, PA) showed parenchymal and ductal changes of chronic pancreatitis throughout the pancreas without a focal mass. A well-defined mixed solid and cystic right adrenal mass measuring cm was noted (Figure 1, B and C). Cytologic examination after 3 EUS-FNA passes with an 8-cm 22-gauge needle (EchoTip Ultra; Cook Medical, Winston-Salem, NC) showed aggregates of epithelioid cells with granular eosinophilic cytoplasm, which stained positive for chromogranin and negative for inhibin, melan A, and calretinin. Cytomorphologic and immunostaining findings were consistent with a pheochromocytoma. No complications occurred from EUS imaging or EUS-FNA of the pheochromocytoma. The patient was referred to an endocrinologist. Quantitative plasma metanephrine (1.79 nmol/l; normal, nmol/l) and normetanephrine (3.54 nmol/l; normal, nmol/l) levels were elevated. Laparoscopic adrenalectomy was recommended, but the patient refused surgical resection. The patient had no history of hypertension before EUS, and hypertension did not develop during the 19-month follow-up period. A Figure 1. A, Computed tomogram from case 1 showing a well-defined right adrenal mass measuring 3 cm (arrowhead). B, Linear transduodenal EUS image in case 1 showing a mixed solid and cystic right adrenal mass measuring cm adjacent to the right kidney (R KID). C, Endoscopic ultrasound-guided FNA of the right adrenal mass in case 1. The needle is clearly shown in the lesion. B C J Ultrasound Med 2008; 27:

4 Endoscopic Ultrasound-Guided Aspiration of Right Adrenal Masses Case 2 A 77-year-old male with a history of metastatic colon cancer, prostate cancer, and Hodgkin lymphoma was referred for EUS-FNA of a subcarinal lymph node and a right adrenal mass, both of which had enlarged on sequential imaging tests. Pathologically staged T3N1 sigmoid colon cancer was diagnosed 5 years before EUS imaging and was treated with left hemicolectomy and adjuvant therapy. His Hodgkin disease had been in remission for more than 40 years, and suspected early prostate cancer diagnosed 18 months previously had been treated with radiation alone. Computed tomography of the chest, abdomen, and pelvis done 3 months before EUS imaging (to follow his previously diagnosed colon cancer) showed multiple pulmonary nodules, a right apical pulmonary mass measuring mm, a subcarinal mass measuring mm, and a right adrenal mass measuring mm. No liver metastasis or retroperitoneal or pelvic adenopathy was noted. Findings from CT-guided biopsy of the right apical pulmonary mass and transbronchial biopsy of the subcarinal mass Figure 2. A, Computed tomogram from case 2 showing a right adrenal mass (arrowhead). B, Linear EUS image in case 2 of a right adrenal mass measuring cm adjacent to the inferior vena cava (IVC). C, Endoscopic ultrasound-guided FNA of the right adrenal mass in case 2. D, Photomicrograph from EUS-FNA of the right adrenal gland in case 2 showing metastatic adenocarcinoma consistent with primary colon cancer (Diff-Quik, original magnification 40). A B C D 264 J Ultrasound Med 2008; 27:

5 DeWitt were both nondiagnostic. The CT-guided biopsy was complicated by a pneumothorax, which was successfully treated with tube thoracostomy. Follow-up CT 6 weeks before EUS imaging showed an increased size of the right apical pulmonary mass, a subcarinal mass, and a right adrenal mass, which now measured 21 14, 41 24, and mm, respectively (Figure 2A). The patient was then referred for EUS. Curvilinear array EUS (GF-UC140P) showed a subcarinal lymph node measuring mm and a well-defined hypoechoic solid right adrenal mass measuring mm (Figure 2B). Three EUS-FNA passes with an 8-cm 22-gauge needle (EchoTip Ultra) into both the adrenal gland and lymph node showed metastatic colon adenocarcinoma with extensive necrosis (Figure 2, C and D). No complications were encountered from the procedure. The patient continued to receive chemotherapy for colon cancer. Discussion There is increasing evidence that transgastric EUS-guided biopsy is a safe and accurate method for sampling the left adrenal gland However, only 2 cases describing EUS-FNA of the right adrenal gland have been published to date. 18,20 This lack of published data appears to be due to the perception that the right adrenal gland is not readily visible by EUS because it has been reported that radial EUS permits detection of the normal left adrenal in nearly all patients but shows a normal or minimally enlarged right adrenal in only 30% of patients. 23 It is possible that curvilinear array EUS shows the right adrenal gland better than radial EUS; however, this has not been formally tested to date. Only a curvilinear array EUS examination was performed in the 2 patients reported here. The patients in this report represent 2 of 52 patients who underwent EUS-FNA of adrenal masses over a nearly 11-year period at our institution. The other 50 patients all had attempted biopsy of left adrenal masses. The results from these 2 cases further suggest that EUS-FNA may be an option for sampling right adrenal masses. Technical success at sampling right adrenal masses would add to the appeal of EUS for staging of lung cancer because this technique has already proven its utility at sampling potential metastatic sites such as the posterior mediastinum, liver, upper abdominal lymph nodes, and left adrenal gland. One patient in this series was found to have a unilateral right adrenal pheochromocytoma confirmed by cytomorphologic and immunochemical findings. Because of potential precipitation of a hypertensive crisis and bleeding with sampling of these tumors, 24,25 some authors have recommended that urine studies be performed in all patients before gland biopsy. 2 Because of the suspicion of metastatic colorectal cancer in our patients, these studies were not performed before EUS-FNA. After EUS imaging, the consulting endocrinologist requested plasma metanephrine and normetanephrine studies instead of urine studies because determination of plasma normetanephrine levels by radioimmunoassay is the most sensitive test for the diagnosis of pheochromocytomas in high-risk 26,27 and low-risk 28 patients. Multiple studies have reported safe percutaneous 10,29 or EUS-guided biopsies of pheochromocytomas or paragangliomas. 20,21,30 No complications were encountered after biopsy of the pheochromocytoma in our patient. Nevertheless, physicians performing adrenal biopsies must be aware of the potential complications of intra-abdominal hemorrhage and a catecholamine crisis after biopsy of any adrenal mass, and it is advisable to exclude a pheochromocytoma before biopsy of any adrenal mass in patients without cancer. Furthermore, real-time pathologic interpretation of adrenal biopsy specimens (as was performed in this patient) permits the physician to be aware of the possibility of this diagnosis and to obtain additional passes for a cell block so that the pathologist can do special stains to confirm the suspected diagnosis. In patients with known primary extra-adrenal malignancy and either a newly diagnosed adrenal mass in a previously normal gland or a rapidly enlarged adrenal mass, this testing is probably not necessary because most would be metastatic lesions. 2,21,24 Similar to a previously reported large retrospective study from our institution, 21 no complications were encountered in either patient in this series. To date, no serious complications from J Ultrasound Med 2008; 27:

6 Endoscopic Ultrasound-Guided Aspiration of Right Adrenal Masses EUS-guided adrenal biopsy have been reported In contrast, a review 12 of morbidity from 7 large series 3,11,12,31 34 describing percutaneous image-guided adrenal biopsy in 666 patients reported complications of 0% to 12%, with an overall rate of 5.3%. Complications from percutaneous adrenal biopsy are more common with right- compared with left-sided biopsies 11,12 and reportedly include pneumothoraxes, needle tract metastases, hemorrhages, hematomas, and pancreatitis. 11,12,34 In conclusion, this series shows that EUS-FNA of right adrenal masses is feasible and may be an option for sampling these lesions. Further experience will be necessary to show the safety and efficacy of this technique. If this limited experience can be reproduced, prospective randomized studies comparing EUS-FNA with percutaneous ultrasound- and CT-guided FNA of the adrenal glands would be indicated to delineate the indications and limitations of each technique. References 1. Mantero F, Terzolo M, Arnaldi G, et al. A survey on adrenal incidentaloma in Italy: study group on adrenal tumors of the Italian Society of Endocrinology. J Clin Endocrinol Metab 2000; 85: Grumbach MM, Biller BM, Braunstein GD, et al. Management of the clinically inapparent adrenal mass ( incidentaloma ). Ann Intern Med 2003; 138: Silverman SG, Mueller PR, Pinkney LP, Koenker RM, Seltzer SE. Predictive value of image-guided adrenal biopsy: analysis of results of 101 biopsies. Radiology 1993; 187: Welch TJ, Sheedy PF II, Stephens DH, Johnson CM, Swensen SJ. Percutaneous adrenal biopsy: review of a 10- year experience. Radiology 1994; 193: Paulsen SD, Nghiem HV, Korobkin M, Caoili EM, Higgins EJ. Changing role of imaging-guided percutaneous biopsy of adrenal masses: evaluation of 50 adrenal biopsies. AJR Am J Roentgenol 2004; 182: Harisinghani MG, Maher MM, Hahn PF, et al. Predictive value of benign percutaneous adrenal biopsies in oncology patients. Clin Radiol 2002; 57: Pagani JJ. Non-small cell lung carcinoma adrenal metastases: computed tomography and percutaneous needle biopsy in their diagnosis. Cancer 1984; 53: Ettinghausen SE, Burt ME. Prospective evaluation of unilateral adrenal masses in patients with operable non-small-cell lung cancer. J Clin Oncol 1991; 9: Gillams A, Roberts CM, Shaw P, Spiro SG, Goldstraw P. The value of CT scanning and percutaneous fine needle aspiration of adrenal masses in biopsy-proven lung cancer. Clin Radiol 1992; 46: Lumachi F, Borsato S, Brandes AA, et al. Fine-needle aspiration cytology of adrenal masses in noncancer patients: clinicoradiologic and histologic correlations in functioning and nonfunctioning tumors. Cancer 2001; 93: Bernardino ME, Walther MM, Phillips VM, et al. CT-guided adrenal biopsy: accuracy, safety, and indications. AJR Am J Roentgenol 1985; 144: Mody MK, Kazerooni EA, Korobkin M. Percutaneous CTguided biopsy of adrenal masses: immediate and delayed complications. J Comput Assist Tomogr 1995; 19: Giovannini M, Seitz JF, Monges G, Perrier H, Rabbia I. Fineneedle aspiration cytology guided by endoscopic ultrasonography: results in 141 patients. Endoscopy 1995; 27: Chang KJ, Erickson RA, Nguyen P. Endoscopic ultrasound (EUS) and EUS-guided fine-needle aspiration of the left adrenal gland. Gastrointest Endosc 1996; 44: Wallace MB, Ravenel J, Block MI, et al. Endoscopic ultrasound in lung cancer patients with a normal mediastinum on computed tomography. Ann Thorac Surg 2004; 77: Ringbaek TJ, Krasnik M, Clementsen P, Skov BG, Rasmussen EN, Vilmann P. Transesophageal endoscopic ultrasound/fine-needle aspiration diagnosis of a malignant adrenal gland in a patient with non-small cell lung cancer and a negative CT scan. Lung Cancer 2005; 48: Kramer H, Groen HJ. Diagnosis of mediastinal and left adrenal abnormalities with endoscopic ultrasonography. Respir Med 2005; 99: Jhala NC, Jhala D, Eloubeidi MA, et al. Endoscopic ultrasound-guided fine-needle aspiration biopsy of the adrenal glands: analysis of 24 patients. Cancer 2004; 102: Eloubeidi MA, Seewald S, Tamhane A, et al. EUS-guided FNA of the left adrenal gland in patients with thoracic or GI malignancies. Gastrointest Endosc 2004; 59: Stelow EB, Debol SM, Stanley MW, Mallery S, Lai R, Bardales RH. Sampling of the adrenal glands by endoscopic ultrasound-guided fine-needle aspiration. Diagn Cytopathol 2005; 33: DeWitt J, Alsatie M, LeBlanc J, McHenry L, Sherman S. Endoscopic Ultrasound-guided fine needle aspiration of left adrenal gland masses. Endoscopy 2007; 39: Gerke H, Robinson RA, Luo P. Diagnosis of focal metastasis to the adrenal gland by EUS-guided core biopsy. Gastrointest Endosc 2005; 62: Dietrich CF, Wehrmann T, Hoffmann C, Herrmann G, Caspary WF, Seifert H. Detection of the adrenal glands by endoscopic or transabdominal ultrasound. Endoscopy 1997; 29: J Ultrasound Med 2008; 27:

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