The Computed Tomography-Guided Adrenal Biopsy

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1 The Computed Tomography-Guided Adrenal Biopsy An Alternative to Surgery in Adrenal Mass Diagnosis WILLIAM A. BERKMAN, MD,'$ MICHAEL E. BERNARDINO, MD,' CHARLES W. SEWELL, MD,t R. BARTON PRICE, MD,' AND PETER J. SONES JR, MD' A series of 16 patients with adrenal masses were biopsied percutaneously under computed tomography (CT) guidance with 18- to 22-gauge modified Chiba needles. Adrenal adenomas, cysts, metastases, melanoma, and adrenal hemorrhage were identified. Of nine oncologic patients, four had adrenal metastases, while five had other nonmalignant adrenal masses. Thus, an adrenal mass in an oncologic patient is not always metastases. No complications occurred. The diagnostic evaluation of an adrenal mass in selected cases should include CT-guided percutaneous aspiration as a safe and reliable alternative to open surgical biopsy. CT-guided biopsy can be performed as an outpatient procedure, avoiding the cost of hospitalization and the morbidity of surgery. Cuncer 53: , w ITH THE INCREASING USE of computed tomography (CT) in oncologic and nononcologic patients many adrenal masses are now being detected. If these newly diagnosed lesions are malignant, they can change the patient's prognosis and therapy. In the past, surgery has been advocated to determine the etiology of these masses. This approach requires hospitalization and significant patient cost. This report describes our experience and approach to adrenal masses. This approach uses the CT-guided needle biopsy which is safe, accurate, and may be an outpatient procedure. Patients and Methods CT-guided percutaneous adrenal biopsies were performed on 16 patients. The age range was from 3 1 to 70 years. There were 9 males and 7 females. Three of 16 patients had a suspected primary malignancy as the reason for the initial CT examination. Six of 16 patients had eight primary malignancies. The etiology of the primary malignancies were bladder ( l), prostate (2), adenocarci- From the Department of Radiology and?the Department of Pathology, Emory University School of Medicine, I364 Clifton Road, N.E., Atlanta, Georgia $ Current address: Good Samaritan Hospital, Baltimore, MD. Address reprints to M. E. Bernardino, Department of Radiology, Emory University School ofmedicine, 1364 Clifton Road, N.E., Atlanta GA Accepted for publication March 4, noma of the lung (3), and melanoma (2). In 6 of the 16 patients the finding of an adrenal mass was an incidental finding. These patients were being scanned for abdominal pain, diarrhea, relapsing pancreatitis, cirrhosis, hypertension, diabetes, and fatigue. In the remaining case, specific evaluation of the adrenal glands was for a possible functioning mass. This patient had Cushing's syndrome and the study yielded bilateral adrenal enlargement (consistent with hyperplasia). The etiology of the Cushing's syndrome was found to be a pituitary tumor. Prior to adrenal biopsy (when indicated), appropriate adrenal function tests were performed in order to exclude a pheochromocytoma. The procedure is started by obtaining reference CT scans of the mass for localization in either the prone or supine position. The reference scans are obtained with an opaque catheter placed over the mid portion of the patient's back or abdomen (Figs. IA-1F). This catheter acts as a landmark. Left adrenal glands are biopsied in the prone position since it provides the most accessible route. Right adrenal masses are biopsied using a transhepatic approach in the supine position (Figs. 2A and 2B). The transhepatic approach reduces the chance of pneumothorax. Through CT computer manipulation, the distance from the catheter to an area directly over the adrenal mass is measured. Additionally, a measurement is taken from this point to the center point of the adrenal gland so that the depth of the biopsy needle can be predeter- 2098

2 No. 10 CT-GUIDED ADRENAL BIOPSY - Berkman et al FIGS. IA-ID. (A, top left) Supine CT scan demonstrates a left adrenal mass. The mass has different densities within it. (B, bottom left) Prone CT scan of the same patient demonstrates the mass. At this time, a catheter has been placed over the spine as a measurement reference point. (C, top right) A measurement is made from the catheter to an area directly over the adrenal lesion. (D, bottom right) The curser is now dropped to the adrenal lesion and the measurement is made from the patient s back to the mass. This measurement is cm. This is the distance the needle will travel when it is placed into the patient. mined. Under CT guidance, the needle is then advanced into the adrenal gland after only minimal local anesthesia. Then a repeat scan is obtained until the needle tip is located within, or preferably at, the edge of the adrenal mass. Two of the biopsies in the study were performed with 22-gauge needles, and 14 biopsies were obtained using 18- to 20-gauge Chiba needles. These larger needles yield histologic as well as cytologic specimens. Two to three needle passes are made in each patient from different sites within the mass to minimize the change of sampling error. The patient is then watched in the radiology department for a period of 1 hour after the procedure. Results Eighteen masses in 16 patients were detected by CT. The 18 masses ranged in size from 1.7 to 5 cm. Single masses were seen in 14 patients, and 2 patients had bi-

3 2 100 CANCER May IS 1984 Vol. 53 evidence of adrenal hyperfunction was present. One patient had an adrenal cyst (diagnosed by CT criteria and cyst puncture fluid characteristics), three patients had adrenal cortical adenomas, and one patient had an enlarged adrenal gland due to recent hemorrhage. One patient was evaluated for suspected adrenal hyperfunction, and tissue obtained revealed adrenal hyperplasia (normal structure but increased cellular size and lipid content). Diagnostic tissue was obtained in 15 of 16 cases (94%). FIGS. IE AND IF. (E, top) A scout view is obtained to localize the needle tip. This digital radiograph allows us to take our slice at the needle top and not the needle hub. Note the needle hub is inferior to the plane of the needle tip. (F, bottom) A repeat CT scan is then obtained at the site of the needle tip. Note that the needle is at the edge of the adrenal mass. lateral adrenal enlargement. Biopsy of one mass in each of the 16 cases was attempted. The smallest mass biopsied was 1.7 cm and largest was 6 cm. Fifteen of 16 cases revealed diagnostic tissue (94%). One case was unsuccessful due to technical difficulties (severe obesity and inability of the patient to duplicate breathing for each CT slice). Of the nine patients with known or suspected primary malignancies, only four (44%) had metastatic involvement of the adrenals. In one of these four cases, the adrenal biopsy was diagnostic of malignant melanoma (Figs. 3A- C), a diagnosis which had not been previously considered in a patient with a lung mass. Four had findings consistent with benign cortical adenomas (Figs. 4A and 4B). One patient had hemorrhage in an adrenal adenoma. In the six patients in whom the finding of an adrenal incidental, one had insufficient tissue for eva]- uation* This was the patient* He was followed by CT with no change in the adrenal size, and no FIGS. 2A AND 29. (A, top) Supine CT Scan demonstrates the transhepatic biopsy approach to the right adrenal mass (arrows). The needle tip is optimally identified within the mass. (B, bottom) Millipore filter preparation of hemorrhagic adrenal aspirate showing a cluster of carcinoma cells. Nuclear membrane alterations and abnormal chromatin pattern aid in the diagnosis (~200).

4 No. 10 CT-GUIDED ADRENAL BIOPSY - Berkman ef al FIGS. 3A AND 3B. (A, top) CT scan in a patient with a left lower lobe lung mass which was felt to be a primary lung carcinoma demonstrates a right adrenal lesion. (B, bottom) Using a right hepatic approach the needle is noted adjacent to the adrenal mass. There were no false-positive or false-negative examinations. Therefore, our diagnostic accuracy was 100%. There were no complications. Discussion The adrenal glands are, per unit weight, the most frequent site for metastatic deposits. Metastases to the adrenal glands are common from breast, melanoma, gastric, renal, pancreatic, colon, and lung carcinoma. I The adrenal glands are the most common site of extranodal spread from primary lung carcinoma. Lung tumor metastases may involve adrenal glands when other metastases are absent. Twenty to 40% of the patients with lung carcinoma have adrenal metastases. Dunnick el al6 reported 4 of 45 patients with small cell pulmonary carcinoma who had adrenal masses detected by CT. These were presumed to be metastases. Although no histologic proof was obtained in these cases, chemotherapy was instituted, and two of the four patients had a decrease in size of the adrenal masses on therapy. Since there was no histologic confirmation of their data, and considering our data, it could be questioned whether the other two patients in the series by Dunnick and associates really had adrenal metastases or nonfunctioning adenomas. Nonfunctioning adrenal adenomas are present in as many as 2% to 9% of adults at autopsy.'-1 It is probably more important in the non-small cell carcinoma patient to determine whether the CT detected adrenal mass is a metastasis or nonfunctioning adenoma. Curative therapy (surgery or radiation therapy) might be attempted if there is a small localized pulmonary lesion with no distant metastases. However, if distant metastases are found, chemotherapy is indicated. In 84 patients with non-small cell bronchogenic carcinoma, CT of the upper abdomen revealed 18 abnormal adrenal glands in 15 patients." Four of these patients were biopsied, and these masses were positive for metastases. Again, the remaining adrenal masses were considered to be malignant, but no biopsy specimens were obtained, and it could be questioned whether these patients were accurately staged. The incidental detection of adrenal masses must be considered in light of the patient population examined. Pagani and Bernardino," in evaluating the CT studies of 62 1 oncologic patients, found that 37 (6%) had an adrenal mass. In ten patients these findings were thought to be clinically significant. This meant that the pressure of an adrenal mass in these patients either altered the type of chemotherapy, extent of the radiation therapy treatment field, or caused adrenalectomy. In two other series, 25 adrenal masses were incidentally discovered on computed tom~graphy.'~*'~ Ten of these had benign lesions. Three benign masses were found in patients with known neoplastic disease. Glazer ef al. I3 recommended an adrenal biopsy or surgical excision in those patients with suspected metastatic disease or with an adrenal mass larger than 3 to 4 cm. They recommended repeat CT scans at 2- to 3- month intervals in patients with adrenal masses less than 3 cm in size.13 Three previous reports have demonstrated the accuracy of adrenal biop~ies.''.'~.~~ Zornosa ef al. l 5 biopsied 2 1 patients demonstrating an accuracy of 8 1 %, and Heaston et in evaluating 14 patients with 16 adrenal masses obtained diagnostic material in 93% with no complications. Our results compare quite favorably to the previous reports. Although we originally used 22-gauge needles in two cases, our smallest gauge routinely used is a 20-gauge needle. The smallest lesion biopsied was less than 2 cm. It is possible to obtain a core of tissue with this needle which we believe has significantly increased our accuracy and reliability. The one case in which we were unable to

5 2102 CANCER May VOl. 53 FIG. 3C. Histologic specimens from this biopsy demonstrates metastatic melanoma. This lesion was the first clue to the fact that the lesion of the lung was not primary lung carcinoma. CT scan during the adrenal biopsy demonstrates that the needle is within a left adrenal mass. This mass was a serendipitous finding. obtain tissue was not due to needle size, but due to technical factors in the performing of the procedure. In all of the remaining cases a diagnostic tissue sample was obtained. Our experience suggests that larger needles (>22 gauge and 5 18 gauge) may be used with reliability and safety. There were no complications in our series, and when added to the biopsy numbers from previous reports, the incidence of complications is less than We believe that CT-guided adrenal biopsies should be performed as a preferable alternative to an open surgical biopsy because of their safety and accuracy. They should be performed in those oncologic patients in whom there is a need to determine the etiology of an adrenal mass for staging. In nononcologic patients, a proper endocrine evaluation should be performed prior to biopsy to eliminate the possibility of performing a biopsy on a functioning adelloma Or ~heochromocfloma~ a biopsy should be performed in any patient with a mass greater FIG. 4A. CT scan demonstrates the biopsy needle in a left adrenal mass.

6 No. 10 CT-GUIDED ADRENAL BIOPSY * Berkman et al FIG. 4B. Histologic specimen obtained with a 20 gauge needle shows normal adrenal tissue consistent with an adrenal adenoma. than 5 cm in size (if the information would be clinically significant for the patient s care). In the remaining cases, it is possible to follow incidentally found adrenal masses by CT without doing a biopsy. REFERENCES I. Thomas JL, Barnes PA, Bernardino ME, Lewis E. Diagnostic approach to adrenal and renal metastasis. RadClin Norih Am 1982; 20: Shields TW. Bronchial Carcinoma. Springfield, Illinois: Charles C Thomas, Mathews MJ, Kanhouwa S, Pickren J, Robinette D. Frequency of residual and metastatic tumor in patients undergoing curative surgical resection for lung cancer. Cancer Treat Rep (Purr 111) 1973; 4: Winstanley DP, Smith RA. Selection of patients for the surgical treatment of bronchial carcinoma Thorax 1978; 23: Abrams HL, Spiro R, Goldstein N. Metastasis in carcinoma. Cancer 1950; 3: Dunnick NR, lhde DC, Johnston EA. Abdominal Computerized tomography in the evaluation of small cell carcinoma of the lung. AJR 1979; 133: Robins SL. Pathologic Basis of Disease. Philadelphia: W. B. Saunders, 1979: Sommer SC. Adrenal glands. In: Anderson WAD, Kissane JM, eds. Pathology. St. Louis: C. V. Mosby, 1977; Commons RR, Callaway CP. Adenomas of the adrenal cortex. Arch Int Med 1948; 81: Hedeland H, Ostberg G, Hokfelt B. On the prevalence of adrenal cortical adenomas in an autopsy material in relation to hypertension and diabetes. ACTA Med Scand 1968; 184: Neilsen ME, Heaston DK, Dunnick NR, Korobkin M. Pre-operative CT evaluation of adrenal glands in non-small cell bronchogenic carcinoma. AJR 1982; 139: Pagani JJ, Bernardino ME. Incidence and significance of serendipitous CI findings in the oncologic patient. J Computer Assisted Tomogr 1982; 6(2): Glazer HS, Weyman PJ, Sagel SS, Levitt RG. Nonfunctioning adrenal masses: Incidental discovery on computed tomography. AJR 1982; 139: Prinz R, Brooks MH, Churchill R et al. Incidental asymptomatic adrenal masses detected by computerized tomographic scanning: Is operation required? JAMA 1982; 248: Zomoza J, Ordonez N, Bemardino ME, Cohen MD. Percutaneous biopsy of adrenal tumors. Urology 1981; 18: Heaston DK, Handel DB, Ashton PR, Korobkin M. Narrow gauge needle aspiration of solid adrenal masses. AJR 1982; 138: Fermcci JT, Wittenberg J, Mueller PR et al. Diagnosis of abdominal malignancy by radiologic fine needle biopsy AJR