Oncocytic Neoplasms of the Adrenal Gland
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1 Genitourinary Imaging linical Perspective Tirkes et al. drenal Oncocytic Neoplasms Genitourinary Imaging linical Perspective Downloaded from by on 12/20/17 from IP address opyright RRS. For personal use only; all rights reserved Temel Tirkes 1 Tunc Gokaslan 2 Jonathan Mcrea 1 Kumaresan Sandrasegaran 1 Margaret. Hollar 1 Fatih kisik 1 handana Lall 1 Tirkes T, Gokaslan T, Mcrea J, Hollar M, Sandrasegaran K, kisik F, Lall Keywords: adrenal gland, T, MRI, neoplasm, oncocytic DOI: /JR Received June 23, 2010; accepted after revision July 15, Department of Radiology and Imaging Sciences, Indiana University School of Medicine, 550 N University lvd., UH 0279, Indianapolis, IN ddress correspondence to T. Tirkes (atirkes@iupui.edu). 2 Department of Pathology, University of Texas Southwestern Medical enter, Dallas, TX. JR 2011; 196: X/11/ merican Roentgen Ray Society Oncocytic Neoplasms of the drenal Gland OJETIVE. Our study was aimed at review of the radiologic findings on oncocytic neoplasms to identify the features that differentiate these tumors from other adrenal neoplasms. ONLUSION. enign and malignant oncocytic neoplasms could not be differentiated on the basis of the T and MRI criteria used for differentiating adrenal cortical adenoma from carcinoma. Oncocytic neoplasms should be considered in the differential diagnosis of indeterminate adrenal tumors. T he sole term oncocytoma previously has been used in the literature to describe adrenal oncocytic neoplasms. However, because using this term suggests that these tumors have purely benign characteristics, we prefer to classify the lesions as either benign or malignant oncocytic neoplasms. This terminology allows correlation with the benign or malignant features typically found at pathologic review [1]. Oncocytic neoplasms originating in the kidney, adrenal glands, thyroid, and salivary glands have been described [2]. The adrenal gland is a rare site for an oncocytic neoplasm; only 57 cases have been described in the English and non-english medical literature [3]. The radiologic literature contains the most information on oncocytic neoplasms of the kidneys, but very little discussion appears concerning oncocytic neoplasms originating from the adrenal glands. However, as with the more common adrenal adenoma, the increasing use of cross-sectional imaging has led to an increase in detection and the incidence of these tumors; 38 of the 57 reported cases have been described within the last 5 years. ecause most of these tumors are nonfunctioning and usually found incidentally, it is only logical that before the modern imaging era, their prevalence was underestimated. ontinued advances in cross-sectional abdominal imaging will make understanding the characteristics of these tumors more relevant. t pathologic review, these rare adrenal neoplasms are composed exclusively of oncocytic cells that, like those in the other organs, are characterized by abundant granular eosinophilic cytoplasm [4]. The pathogenesis of these adrenal tumors is not fully understood. Materials and Methods The archives in the pathology department were searched for oncocytic adrenocortical neoplasms documented in the past 10 years. This search yielded the cases of 11 patients, two of whom did not have imaging studies available. The other nine patients (eight women, one man; age range, years; mean, 46.5 years) were included in this study. The clinical charts and imaging reports were reviewed, and a record was made of each patient s age, sex, size of mass, and imaging features. Findings from three previous radiology case reports also are included in this discussion. Twenty-eight additional patients described in the nonradiologic literature are included in the discussion of age, sex, and side of presentation. ll of our patients underwent T of the abdomen. Five of the nine patients received IV contrast material; one patient underwent both unenhanced and contrast-enhanced imaging. The T parameters ranged from 4-mm collimation reconstructed at 3-mm intervals to 8-mm collimation with 5-mm reconstruction. The T criterion used for the diagnosis of benign lipid-rich adenoma was unenhanced attenuation of 10 HU or less [5]. Four of the nine patients underwent additional MRI, and MRI was considered unnecessary in cases in which the T examination was satisfactory to the radiologist. MRI was performed with a 1.5- or 3-T system, and all examinations included in-phase and opposed-phase T1-weighted sequences. IV contrast material was not routinely used for MRI. 592 JR:196, March 2011
2 drenal Oncocytic Neoplasms Downloaded from by on 12/20/17 from IP address opyright RRS. For personal use only; all rights reserved entimeters In all cases, the final diagnosis was obtained by examination of the excised surgical specimen. The senior surgical pathologists who confirmed the oncocytic nature of the neoplasms reviewed the pathologic slides. Malignancy was determined by application of the Weiss criteria [1] for adrenal cortical neoplasms (ppendix 1). Results The average size of all of the oncocytic neoplasms (n = 40), including those described in the nonradiologic literature [2 4, 6 11], was 9.3 cm (range, 3 22 cm). Malignant oncocytic neoplasms were observed to be larger than benign oncocytic neoplasms at presentation. The average diameter of the malignant tumors was 12.2 cm (range, 5 22 cm), and that of the benign tumors was 7.6 cm (range, 3 15 cm) (Fig. 1). Seventy-seven percent (31/40) of the patients with these neoplasms were women, and 63% (25/40) of the tumors were in the left adrenal gland. The average age of patients found to have a benign tumor was 48 years (range, years) and of those found to have malignant tumors was 47 years (range, years) (Fig. 1). ll patients were adults except for enign Malignant Years enign Malignant Fig. 1 Size and age distribution of benign and malignant oncocytic neoplasms at presentation. Patients reported in nonradiologic literature (n = 40) are included in analysis., Graph shows average size of benign tumors is 7.6 cm (range, 3 15 cm) and average size of malignant tumors is 12.2 cm (range, 5 22 cm). Overall average tumor size is 9.3 cm (range, 3 22 cm)., Graph shows average age of patients found to have benign tumors is 48 years (range, years) and of those with malignant tumors is 47 years (range, years). one who was found to have benign oncocytoma at the age of 12 years [11]. Seven of the 12 oncocytic neoplasms were inhomogeneous regardless of benign or malignant origin (Table 1). Inhomogeneous adrenal lesions are considered indeterminate because T attenuation and MRI signal intensity are not considered reliable diagnostic criteria [5]. The homogeneous oncocytic adrenocortical neoplasms had attenuation greater than 10 HU on unenhanced T scans (average attenuation, 14 HU for benign lesions, 35 HU for malignant lesions) (Figs. 2 and 3). fter contrast administration, all benign tumors tended to exhibit low-grade homogeneous enhancement similar to that of paraspinal muscle (Fig. 2). t MRI examination, neither benign (Fig. 3) nor malignant (Fig. 4) oncocytic neoplasms exhibited loss of signal intensity on opposed-phase images. tendency toward areas of increased T1 signal intensity secondary to hemorrhage (Fig. 5) and increased T2 signal intensity secondary to necrosis (Fig. 4D) were found at MRI of malignant lesions. oth benign and malignant tumors had T1 and T2 signal intensity similar to that of spleen (Figs. 3 and 4D). TLE 1: Imaging haracteristics of drenocortical Oncocytic Neoplasms pathologic feature useful in identifying adrenal oncocytic tumors is a fibrous capsule (Fig. 6). We identified the capsule in the large tumors (Figs. 4 and 5). Large malignant oncocytic neoplasms applied mass effect on the liver, kidney, and inferior vena cava, although no instances of local invasion or metastatic disease were identified in our review. There was no extension of tumor into the adrenal vein or inferior vena cava. Preservation of the capsule and lack of local invasion even in large tumors can be considered features that differentiate adrenal oncocytic tumor from adrenal cortical carcinoma. In all patients found to have benign disease, radiologists correctly identified the adrenal gland as the source of the tumor. However, this was not the case in most of the patients (three of four) with malignant lesions, likely because of the large tumor size and distorted anatomy. None of the reviewed cases involved multiple or bilateral masses, and none of the cases in the radiologic literature had distant metastatic involvement. Gross examination of surgically resected specimens revealed tumors of varying size, the largest of which measured 22 cm in greatest Loss of Signal Intensity During hemical Shift MRI Study Histologic Finding No. of Patients Inhomogeneous verage ttenuation at Unenhanced T (HU) Enhancement Pattern T1 and T2 Signal Intensity urrent study enign 5 2/5 14 Low grade (2/2) Equal to spleen No No Malignant 4 3/4 35 Low grade (3/3) Equal to spleen; foci of increased intensity Gandras et al. [6] enign 1 0/1 Low grade Intermediate No Poretti et al. [4] enign 1 1/1 Low grade Equal to spleen Shah et al. [7] enign 1 1/1 Low grade JR:196, March
3 Tirkes et al. Fig year-old woman with benign oncocytic neoplasm of left adrenal gland., Unenhanced T scan shows 5.6-cm left adrenal mass with smooth and sharply defined borders (arrow)., ontrast-enhanced T scan shows benign tumor (arrow) has typical heterogeneous low-grade enhancement similar to that of paraspinal muscle. Downloaded from by on 12/20/17 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with known history of colon carcinoma found to have new right adrenal mass at follow-up T., Unenhanced T scan shows 3-cm heterogeneous mass (arrow) with central low attenuation (11 HU)., xial T1-weighted opposed-phase MR image (1.5 T; TR/TE, 25/6.9) shows mass (arrow) of intermediate signal intensity without loss of signal intensity compared with in-phase image (not shown). enign oncocytic neoplasm was diagnosed after adrenalectomy., xial T2-weighted MR image (2,500/120; no fat suppression) shows mass (arrow) is isointense in relation to spleen. D Fig year-old woman with 22-cm malignant adrenal oncocytic neoplasm., ontrast-enhanced T scan shows large encapsulated tumor with inhomogeneous enhancement secondary to central necrosis (asterisk). alcification (arrow) also is evident., xial in-phase T1-weighted MR image shows areas of both increased and decreased T1 signal intensity (white arrows) within mass, representing hemorrhage and necrosis, respectively. lack arrows outline capsule of mass., xial T1-weighted opposed-phase MR image shows no loss of signal intensity. rrows outline capsule of mass. D, oronal T2-weighted MR image (3 T; TR, 185 milliseconds; in-phase TE, 2.4 milliseconds; opposed-phase TE, 5.8 milliseconds) shows area of increased signal intensity representing extensive necrosis (arrow). Stomach (St) and spleen (Sp) are displaced superiorly. ccordingly, patient had presented with left upper quadrant pain and early satiety. 594 JR:196, March 2011
4 drenal Oncocytic Neoplasms Downloaded from by on 12/20/17 from IP address opyright RRS. For personal use only; all rights reserved diameter. ll of the tumors were distinct from the renal parenchyma, and gross inspection revealed a thin rim of adrenal cortex, which was compressed at the periphery in some cases. Large areas of necrosis and infiltration into the adjacent parenchyma were observed in large tumors. The color of the tumors ranged from dark brown to tan with interspersed yellow areas of necrosis. t microscopic examination, the adrenal parenchyma was consistently completely replaced by the tumor and in some instances contained fragments of remaining capsule embedded in the tumor. Histologic examination showed the neoplastic oncocytic cells were arranged predominantly in a diffuse pattern separated by large areas of geographic necrosis. The neoplastic cells were typically large and took on a round to polygonal shape. Round nuclei and prominent nucleoli were consistently noted, as was abundant granular and eosinophilic cytoplasm (Fig. 6). Occasional tumor giant cells were seen. Mitotic counts were low with rare atypical mitoses. Fig year-old woman with 17-cm malignant oncocytic neoplasm., ontrast-enhanced T scan shows large tumor (asterisk) with internal vasculature and inhomogeneous enhancement (arrow)., oronal T2-weighted MR (1.5 T; TR/TE, 1,859/91; no fat suppression) image shows area of fluid signal intensity (arrow) corresponding to area of low attenuation in ; findings are consistent with necrosis. Substantial mass effect on liver and right kidney is evident. Despite large size of tumor, intact interface (arrowheads) is present between mass and liver. Signal intensity of tumor is similar to that of spleen., Unenhanced axial T1-weighted MR image (1.5 T; TR/TE, 150/4.2; no fat suppression) shows marked mass effect of tumor on liver and duodenum (black arrow). T1 signal intensity is similar to that of spleen. reas of decreased T1 signal intensity (white arrows) correspond to necrosis. Foci of increased T1 signal intensity represent tumor vessels, findings more clearly depicted in. Discussion efore our study, most of the literature on oncocytic adrenal neoplasms focused on the clinical and pathologic aspects, only three case reports being found in the radiology literature [4, 6, 7], all involving benign lesions only. To our knowledge, our study group is the largest described in the radiology literature, the cases including four malignant and five benign oncocytic tumors. In the imaging of oncocytic neoplasms, as of any mass of the adrenal gland, it is important to differentiate the lesion from adrenal adenoma. In our series, none of the oncocytic neoplasms could be classified as lipid-rich adenoma. The inhomogeneous appearance, increased attenuation on T images, and absence of loss of signal intensity on opposedphase MR images excluded the diagnosis of adenoma. This result is consistent with the histologic findings on oncocytic neoplasms, which have a close arrangement of neoplastic cells and mitochondria-packed cytoplasm with no lipid deposition (Fig. 6). Fig year-old woman found to have incidental adrenal mass with indeterminant imaging findings. Subsequent biopsy revealed oncocytic neoplasm., Photomicrograph shows neoplastic oncocytic cells have abundant granular and eosinophilic cytoplasm arranged in predominantly diffuse pattern of large polygonal cells with round prominent nucleoli. (H and E, 200), Photomicrograph of same specimen at low magnification shows oncocytic neoplasm with fibrous capsule (). (H and E, 40) In our study, we could not differentiate benign from malignant lesions on the basis of contrast enhancement. The low-grade enhancement seen in our patients is consistent with that described in previous case reports, in which benign oncocytic neoplasms did not have increased vascularity at pathologic examination [6, 8]. Marked enhancement was seen only in large malignant tumors and tended to be inhomogeneous owing to necrosis. The lack of marked enhancement of benign oncocytic tumors is helpful in differentiating them from pheochromocytoma. Pheochromocytoma can have a granular cytoplasm similar to that of oncocytic tumors at histologic examination, and rare oncocytic tumors may result in catecholamine production [8]. However, pheochromocytoma is avidly enhancing, and the results of immunohistochemical staining confirm the diagnosis [4]. n imaging feature that differentiates benign from malignant adrenal neoplasms is tumor size. diameter less than 5 cm usually suggests a benign origin [5]. Our review of the JR:196, March
5 Tirkes et al. Downloaded from by on 12/20/17 from IP address opyright RRS. For personal use only; all rights reserved literature showed that the average size of benign oncocytic tumors was 7.6 cm; therefore, the size criteria used for adenoma would not be reliable for benign oncocytic neoplasms. There is a slight left-sided predominance of oncocytic neoplasms, as there is for adrenocortical carcinoma [5]. Review of the literature showed that 78% of patients (31/40) with oncocytic neoplasms were women; adrenocortical carcinoma tends to have a slight male predominance [12]. t presentation, adrenocortical carcinoma often exhibits evidence of being metastatic to the liver, lung, or lymph nodes, especially in cases of large tumors [5]; however, we did not find any metastatic disease in our study group. T and MRI are accurate in identification of the adrenal gland as the source of benign oncocytic neoplasms. However, owing to the large size of these masses, which have a notable mass effect on the surrounding structures, the value of T and MRI is low in the assessment of the origin of malignant tumors. In addition, these malignant tumors efface the remaining adrenal gland, making it difficult to appreciate directly during imaging that the adrenal gland is the origin of the tumor. Our study was somewhat limited by the number of patients evaluated; however, because of the rarity of the disease assessed, the number can be considered acceptable. In addition, because the analysis was retrospective, imaging studies were not standardized. Oncocytic neoplasms (oncocytomas) of the adrenal gland are rare tumors that originate from the adrenal cortex and are histologically composed of oncocytic cells that lack lipid. These neoplasms are more common in women. T and MRI findings cannot be used to differentiate benign and malignant oncocytic neoplasms on the basis of the criteria used for differentiating adrenal cortical adenoma from carcinoma. Oncocytic neoplasms should be considered in the differential diagnosis of indeterminate adrenal tumors. PPENDIX 1: Weiss Histopathologic riteria 1. High nuclear grade 2. Mitotic rate greater than five per 50 high power fields 3. typical mitotic figures 4. Eosinophilic tumor cell cytoplasm (greater than 75% tumor cells) 5. Diffuse architecture (greater than 33% of tumor) 6. Necrosis 7. Venous invasion 8. Sinusoidal invasion 9. apsular invasion This histopathologic system is the most widely used for differentiating benign from malignant adrenocortical tumors. Each Weiss criterion is scored 0 when absent and 1 when present. Thus each tumor is graded from 0 to 9 for determination of a total Weiss score. tumor is labeled malignant when it meets four or more of these histologic criteria. References 1. Weiss LM, Medeiros LJ, Vickery L. Pathologic features of prognostic significance in adrenocortical carcinoma. m J Surg Pathol 1989; 13: Lin T, onsib SM, Mierau GW, Weiss LM, Medeiros LJ. Oncocytic adrenocortical neoplasms: a report of seven cases and review of the literature. m J Surg Pathol 1998; 22: isceglia M, Ludovico O, Di Mattia, et al. drenocortical oncocytic tumors: report of 10 cases and review of the literature. Int J Surg Pathol 2004; 12: Poretti D, Mazzarol G, onomo G, asadio, ellomi M. drenocortical oncocytoma: case report. lin Imaging 2003; 27: Dunnick NR, Korobkin M, Francis I. drenal radiology: distinguishing benign from malignant adrenal masses. JR 1996; 167: Gandras EJ, Schwartz LH, Panicek DM, Levi G. ase report: adrenocortical oncocytoma T and MRI findings. J omput ssist Tomogr 1996; 20: Shah RK, Oto, Ozkan OS. drenal oncocytoma: US and T findings. JR-TR 2004; 87: Goel T, Thomas J, Garg S, Rao, Reddy S. drenal oncocytoma masquerading as a functional tumor. Indian J Urol 2007; 23: Song SY, Park S, Kim SR, Suh YL. Oncocytic adrenocortical carcinomas: a pathological and immunohistochemical study of four cases in comparison with conventional adrenocortical carcinomas. Pathol Int 2004; 54: Kitching P, Patel V, Harach HR. drenocortical oncocytoma. J lin Pathol 1999; 52: Gumy-Pause F, ongiovanni M, Wildhaber, Jenkins JJ, hardot, Ozsahin H. drenocortical oncocytoma in a child. Pediatr lood ancer 2008; 50: The International gency for Research on ancer. Tumors of the adrenal gland. In: DeLellis R, Lloyd R, Heitz P, Eng, eds. Pathology and genetics of tumours of endocrine organs (IR WHO lassification of Tumours). Lyon, France: IR Press, JR:196, March 2011
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