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(Radiology. 1999;210:385-391.)
© RSNA, 1999

Genitourinary Imaging

Large Degenerated Adrenal Adenomas: Radiologic-Pathologic Correlation

Jeffrey H. Newhouse, MD1, Clara S. Heffess, MD2, Brent J. Wagner, MD2,1, Thomas J. Imray, MD3,1, Carol F. Adair, MD2 and Alan J. Davidson, MD1

1 Departments of Radiology (J.H.N., B.J.W., T.J.I., A.J.D.)
2 Endocrine Pathology (C.S.H., C.F.A.), Armed Forces Institute of Pathology, Department of Radiologic Pathology, Washington, DC.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To correlate the radiologic and pathologic findings and differential diagnosis of large, degenerated adrenal adenomas.

MATERIALS AND METHODS: The authors reviewed the radiologic and pathologic characteristics of 30 large adenomas with cystic regions or areas of heterogeneity that were either intrinsic or demonstrated at contrast material–enhanced computed tomography (CT) or magnetic resonance (MR) imaging. Images of 24 adrenocortical carcinomas were also reviewed to determine whether differentiating characteristics existed.

RESULTS: Most of the adrenocortical adenomas were in asymptomatic women. Ten adenomas contained calcification. Pathologic examination revealed good correlation between heterogeneity and liquefied regions. Histologic examination confirmed regions of adenomatous tissue with areas of hemorrhage, amorphous degenerated material, calcification, and fibrosis. Some tumors contained myelolipomatous foci. Although some clinical and imaging findings differed between the groups, no features could be found that enabled the radiologic differentiation of adenomas from carcinomas.

CONCLUSION: A subgroup of adrenal adenomas are larger, more heterogeneous, and more frequently calcified than those with the usual imaging findings. Central necrosis, hemorrhage, or both are responsible for many of the imaging features. Differentiation of these lesions from other large adrenal masses, including adrenal carcinoma, cannot be made by means of imaging alone; resection is required for the definitive diagnosis.

Index terms: Adrenal gland, CT, 86.12111, 86.12112 • Adrenal gland, MR, 86.121411, 86.12143 • Adrenal gland, neoplasms, 86.317, 86.324


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Most adrenal adenomas have a limited range of radiologic findings (1–16): They are almost always smaller than 5 cm, are relatively homogeneous, and display rapid and relatively uniform enhancement with rapid washout of iodinated or gadolinium-based contrast material. They often reveal computed tomographic (CT) and magnetic resonance (MR) imaging findings associated with intracellular lipid and almost never liquefy; calcification is very rare. These lesions, however, may occasionally undergo intratumoral hemorrhagic degeneration with development of avascular and cystic internal regions and subsequent fibrosis. They then become much larger and display focal liquefaction, central or peripheral calcification and fibrosis, internal soft-tissue nodules, and patchy heterogeneous contrast enhancement, features that are commonly associated with adrenocortical carcinomas and other lesions. We performed this study to correlate the radiologic and pathologic findings in a series of such lesions, demonstrate the difficulty of distinguishing them from primary adrenal carcinomas, and discuss the implications of these features for their management.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The cases were drawn from the files of the Department of Radiologic Pathology at the Armed Forces Institute of Pathology (AFIP), Washington, DC. Lesions were included in this study if they were (a) definitively diagnosed as adenomas with degenerative changes after independent review by two staff pathologists; (b) examined with CT, MR imaging, or both; and (c) larger than 5 cm in diameter with coarse heterogeneity (ie, irregularly shaped regions of variable attenuation or signal intensity that were at least half a centimeter in size) or cystic change at imaging examinations. All cases meeting these criteria were included. Images were reviewed by four genitourinary radiologists (J.H.N., B.J.W., T.J.I., A.J.D.) together. The size, degree of heterogeneity and cystic change; presence of solid tissue nodules within cystic regions; presence and characteristics of calcification; and evidence of invasion of adjacent structures and veins were assessed. Twenty-four patients were found in the AFIP archives to have histologically confirmed adrenocortical carcinoma; their images were studied in identical ways to determine whether features enabling the differentiation of the two groups of lesions could be found.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Adenoma Group
Patients.—Thirty patients with adrenocortical adenomas with atypical radiologic features were found. There were 20 women and 10 men. The average patient age was 63 years (range, 21–87 years); all but three patients were older than 53 years. Four patients had clinical or biochemical evidence of Cushing disease, two of whom also had elevated catecholamine levels. The remainder of the patients had no endocrine dysfunction.

Radiologic findings.—Twenty-five of the 30 patients underwent only CT, one patient underwent only MR imaging, and four patients underwent both examinations. CT was performed without intravenous contrast material in 19 patients, with contrast material in seven, and both with and without contrast material in three. The dose of contrast material and timing of contrast material administration were not available. In most patients, measurement of the exact CT attenuation was not performed. All contrast material–enhanced CT examinations were performed at a time at which contrast material was visible in the renal collecting systems. MR imaging was performed with spin-echo or fast spin-echo sequences; each patient underwent T1-weighted (repetition time, 34–600 msec; echo time, 11–21 msec [34–600/11–21]) and T2-weighted (2,500–6,000/104–134) imaging; no contrast agents were used, nor was fat-saturation or gradient-echo imaging performed. None of the lesions was preoperatively sampled for biopsy.

The adenomas (Figs 1–4) ranged in diameter from 5 to 20 cm (average, 11.1 cm; SD, 3.1 cm). Ten adenomas had calcification visible at CT. In one adenoma, the calcification was confined to the rim. Calcification was visible as irregularly shaped regions of various sizes scattered throughout the tumors in the remainder of adenomas. Two adenomas appeared completely cystic, 12 appeared to be almost entirely cystic, and three had focal cystic regions. The walls of the cystic lesions were irregular, and six cases had soft-tissue nodules that appeared to protrude into the cystic regions. "Cystic" regions were assumed to contain fluid on the basis of CT findings of homogeneous low attenuation (the attenuation of the cystic region was lower than that of muscle and blood) and by having very low signal intensity on T1-weighted MR images and very high signal intensity on T2-weighted MR images; these regions showed good correlation between MR and CT images in those cases in which both were available. The noncystic lesions and the solid portions of the partially cystic lesions were heterogeneous on all images and enhanced heterogeneously in those cases in which pre- and postcontrast CT images had been obtained.



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  		Figure 1a. Adrenal adenoma in a 73-year-old woman with a palpable mass. (a) Contrast-enhanced CT scan shows a large, heterogeneous mass with a large, central region of low attenuation (*), calcifications (arrowheads), and irregular peripheral enhancement (arrows). (b) Cut section of gross specimen shows regions of hemorrhagic necrosis (*); only the small yellow regions are viable adenoma.

 


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  		Figure 1b. Adrenal adenoma in a 73-year-old woman with a palpable mass. (a) Contrast-enhanced CT scan shows a large, heterogeneous mass with a large, central region of low attenuation (*), calcifications (arrowheads), and irregular peripheral enhancement (arrows). (b) Cut section of gross specimen shows regions of hemorrhagic necrosis (*); only the small yellow regions are viable adenoma.

 


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  		Figure 4a. Adrenal adenoma discovered incidentally in a 59-year-woman many years after the patient underwent right nephrectomy for multicystic dysplastic kidney. (a) Contrast-enhanced CT scan shows a low-attenuation mass (*) with focal calcifications (curved arrow) and enhancement (straight arrow). (b) Coronal T1-weighted MR image shows a low-signal-intensity mass (*) with minimal heterogeneity. (c) T2-weighted transverse MR image shows that the mass (*) has marked heterogeneity. (d) Cut section of gross specimen reveals regions of acute and chronic hemorrhage and necrosis (*); the yellow regions represent viable adenoma.

 


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  		Figure 4b. Adrenal adenoma discovered incidentally in a 59-year-woman many years after the patient underwent right nephrectomy for multicystic dysplastic kidney. (a) Contrast-enhanced CT scan shows a low-attenuation mass (*) with focal calcifications (curved arrow) and enhancement (straight arrow). (b) Coronal T1-weighted MR image shows a low-signal-intensity mass (*) with minimal heterogeneity. (c) T2-weighted transverse MR image shows that the mass (*) has marked heterogeneity. (d) Cut section of gross specimen reveals regions of acute and chronic hemorrhage and necrosis (*); the yellow regions represent viable adenoma.

 


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  		Figure 4c. Adrenal adenoma discovered incidentally in a 59-year-woman many years after the patient underwent right nephrectomy for multicystic dysplastic kidney. (a) Contrast-enhanced CT scan shows a low-attenuation mass (*) with focal calcifications (curved arrow) and enhancement (straight arrow). (b) Coronal T1-weighted MR image shows a low-signal-intensity mass (*) with minimal heterogeneity. (c) T2-weighted transverse MR image shows that the mass (*) has marked heterogeneity. (d) Cut section of gross specimen reveals regions of acute and chronic hemorrhage and necrosis (*); the yellow regions represent viable adenoma.

 


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  		Figure 4d. Adrenal adenoma discovered incidentally in a 59-year-woman many years after the patient underwent right nephrectomy for multicystic dysplastic kidney. (a) Contrast-enhanced CT scan shows a low-attenuation mass (*) with focal calcifications (curved arrow) and enhancement (straight arrow). (b) Coronal T1-weighted MR image shows a low-signal-intensity mass (*) with minimal heterogeneity. (c) T2-weighted transverse MR image shows that the mass (*) has marked heterogeneity. (d) Cut section of gross specimen reveals regions of acute and chronic hemorrhage and necrosis (*); the yellow regions represent viable adenoma.

 
Pathologic examination.—The diameter of the excised lesion (Figs 1–4) varied from the diameter measured on the images by 10% or less. All lesions that appeared to be primarily cystic at CT or MR imaging had central regions that were filled with fluid, old thrombus, or gelatinous material. The walls varied in thickness from 3 to 20 mm and tended to be irregular. In most cases, a portion of the wall consisted of the limbs of the adrenal gland splayed over the surface of the mass. The lesions that appeared to be heterogeneous, rather than cystic, contained focal regions of hemorrhage, necrosis, or both; in one case, regions of fibrosis were found in the center of the lesion.

At histologic examination, the neoplasms were well circumscribed and partially surrounded by connective tissue capsules. Occasionally, a thick capsule separated the adenoma from the remaining noninvolved cortex. Each had large, well-differentiated adrenocortical cells resembling those seen in the adrenal cortex. The abnormal cortical cell proliferation was of variable thickness; the irregular inner surface was contiguous to the degenerative areas (Fig 5). Some of the cyst walls contained adipocytes and myeloid elements, which comprised small lipomatous and myelolipomatous foci. Some also contained small calcifications. The amount of connective tissue was also variable; occasional bands of dense connective tissue delimited the adenomatous tissue from the cystic or degenerated areas. The degenerative changes consisted mainly of hemorrhage, amorphous material, calcification, fibrosis, small and large cavernous blood vessels ("neovascularization"), and viable and nonviable islands of cortical cells (Fig 5). No mitoses or tumor necrosis of the kind seen in cortical carcinomas were found, nor were any of the histologic patterns that are seen in carcinomas found.



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  		Figure 5a. (a) Low-power view of adrenocortical adenoma demonstrates the junction (curved arrows) between a rim of well-preserved neoplasm (straight thin arrow) and a large central area of hemorrhage and degenerative changes (straight thick arrow). (Masson trichrome stain.) (b) A closer view of the degenerated area of the adenoma seen in a shows an admixture of pale neoplastic cortical cells arranged in nests (curved arrows) with large areas of eosinophilic fibrin-containing brown hemosiderin pigment, which indicates remote hemorrhage with organization. A few clusters of degenerative tumor cell "ghosts" (straight arrow) are seen. (Masson trichrome stain.) (c) The central area of degeneration in another adrenocortical adenoma contains both foamy macrophages and neoplastic adrenocortical cells, which may look very similar at histologic examination. Cohesive trabecular groups in this field represent tumor cells (arrow). (Hematoxylin-eosin stain.)

 


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  		Figure 5b. (a) Low-power view of adrenocortical adenoma demonstrates the junction (curved arrows) between a rim of well-preserved neoplasm (straight thin arrow) and a large central area of hemorrhage and degenerative changes (straight thick arrow). (Masson trichrome stain.) (b) A closer view of the degenerated area of the adenoma seen in a shows an admixture of pale neoplastic cortical cells arranged in nests (curved arrows) with large areas of eosinophilic fibrin-containing brown hemosiderin pigment, which indicates remote hemorrhage with organization. A few clusters of degenerative tumor cell "ghosts" (straight arrow) are seen. (Masson trichrome stain.) (c) The central area of degeneration in another adrenocortical adenoma contains both foamy macrophages and neoplastic adrenocortical cells, which may look very similar at histologic examination. Cohesive trabecular groups in this field represent tumor cells (arrow). (Hematoxylin-eosin stain.)

 


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  		Figure 5c. (a) Low-power view of adrenocortical adenoma demonstrates the junction (curved arrows) between a rim of well-preserved neoplasm (straight thin arrow) and a large central area of hemorrhage and degenerative changes (straight thick arrow). (Masson trichrome stain.) (b) A closer view of the degenerated area of the adenoma seen in a shows an admixture of pale neoplastic cortical cells arranged in nests (curved arrows) with large areas of eosinophilic fibrin-containing brown hemosiderin pigment, which indicates remote hemorrhage with organization. A few clusters of degenerative tumor cell "ghosts" (straight arrow) are seen. (Masson trichrome stain.) (c) The central area of degeneration in another adrenocortical adenoma contains both foamy macrophages and neoplastic adrenocortical cells, which may look very similar at histologic examination. Cohesive trabecular groups in this field represent tumor cells (arrow). (Hematoxylin-eosin stain.)

 
Carcinoma Group
Patients.—Adrenocortical carcinomas were found in 11 male and 13 female patients ranging in age from 13 to 61 years (mean, 43 years). Twelve patients had endocrine dysfunction, including Cushing syndrome, virilization, feminization, hyperaldosteronism, and elevated metanephrine and normetanephrine levels.

Twenty patients underwent only CT, one patient underwent only MR imaging, and three patients underwent both examinations. CT was performed without intravenous contrast material in 17 patients, with contrast material in four, and with and without contrast material in two. Attenuation measurements were usually not available. MR imaging was performed with spin-echo or fast spin-echo sequences; each patient underwent T1-weighted (120–600/11–30) and T2-weighted (2,400–5,400/84–120) imaging. Gadolinium enhancement was used in one patient; gradient-echo techniques were not used.

Radiologic findings.—Carcinomas were on the left in 11 patients and on the right in 13. The carcinomas were slightly larger than the adenomas, ranging in diameter from 5 to 50 cm (average, 15 cm). Eight carcinomas (33%) contained calcification; one had rim calcification and seven had irregular calcific deposits of varying sizes. None of the carcinomas had a unilocular cystic configuration; one had focal cystic degeneration. Two carcinomas were homogeneous; in the remainder, the attenuation, signal intensity, or both had irregular heterogeneity. None of the carcinomas had nodules in cystic regions. Four patients had evidence of metastatic or invasive disease: One patient had multiple lung metastases and three patients had tumor thrombus that extended from the primary neoplasm into the inferior vena cava.

Radiologic features that permitted confident differentiation between carcinomas and adenomas were found in only a minority of cases. Metastases and tumor thrombi were present only in patients with carcinomas; however, 20 (83%) of the patients with carcinomas did not have these findings. Completely cystic lesions and lesions containing soft-tissue nodules were found only in patients with adenomas; however, 22 (73%) of the patients with adenomas did not have these findings.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Adrenal adenomas are relatively common in adults. They appear in autopsy series with reported prevalences of 2%–9% (17,18) and are frequently encountered incidentally at CT; literally hundreds of them have been described in the literature (1–16). The features of the adenomas in this series (large size, heterogeneity, cystic change, and calcification), however, appear to be very rare among the reported lesions (1,19–22). The fact that 30 such adenomas could be found in the AFIP archives is almost certainly a reflection of the requirement that accession into the radiologic pathology archives generally requires resection and examination of the entire lesion, which very rarely occur with lesions that have typical radiologic appearances. Selection bias notwithstanding, the number of cases in this series suggests that radiologists should be aware that adenomas may have this atypical appearance.

Our tumors were considerably larger than most that have been previously described. The growth rate of adrenal adenomas is not known, but is probably slow—indeed, a characteristic frequently invoked to indicate that an adrenal mass is an adenoma is its failure to increase in size during a lengthy observation. The increasing prevalence of adrenal adenomas with increasing age, however, suggests that adrenocortical adenomas must grow, so it is not surprising that a few ultimately become large.

Our tumors were heterogeneous, in contrast to most of those described previously. Heterogeneity may be linked with size: Larger tumors are more likely to become ischemic centrally, and ischemic regions may become fibrotic or liquefy, either of which may produce the heterogeneity seen at CT and MR imaging. Whether the small amount of fatty tissue found in the tumors was in part responsible for the heterogeneity is not clear. Similar findings have been reported in other adrenal adenomas (3,23–25); the reason for the association of tissue types is not known.

A large lesion may also experience internal hemorrhage (15,26–28) and ultimately evolve to become a "pseudocyst." The cystic region may be so much more voluminous than the solid tumor that the adenoma might be overlooked in radiologic examinations, during surgical inspection, and even at pathologic examination. Several of the lesions in our series were originally diagnosed as cysts, pseudocysts, or hemangiomas and were subsequently found to be adenomas only after careful microscopic examination revealed residual neoplastic cortical tissue (29–31). Neoplastic regions, which contain cells that have more cytoplasm and are larger than normal cells, must be distinguished from islands of normal cortical tissue, which have been described in hemorrhagic pseudocysts arising in adrenal glands without tumors (29).

The appearances of our lesions pose problems for making the differential diagnosis. As we have shown, these adenomas share many radiologic features with adrenocortical carcinomas, which are usually large and heterogeneous and frequently contain necrotic regions. About one-third of adenomas calcify (32,33). Although adrenocortical carcinomas may display specific features of malignancy, including invasion of adjacent structures, metastases, and venous tumor thrombi, the absence of these features by no means is proof of benignity. The functional status of a tumor usually does not permit differentiation between carcinoma and adenoma. Many of the tumors in our series were resected because their size and heterogeneity led to a preoperative diagnosis of carcinoma. These lesions can be misdiagnosed histologically if the criteria for malignancy (34), which include mitoses, a trabecular growth pattern, and an increased nuclear-cytoplasmic ratio, are not applied correctly, so the mistake may be perpetuated after pathologic examination (35,36). It is also easy to miss the neoplasm completely at histologic examination and to call the lesion a pseudocyst (37) or hemangioma (38) due to the marked cystic degeneration and vascular proliferation.

Metastases to the adrenal glands have a wide range of sizes; large ones may be heterogeneous. Unlike the tumors in this series, metastases are unlikely to calcify and may be bilateral. They are usually discovered in patients already known to have primary malignancies elsewhere; occasionally, they may be the primary manifestation of the disease (39). None of the tumors in this series was believed preoperatively to represent a metastasis.

Pheochromocytomas may share features with tumors in this series (40,41), including large size, cystic regions, and occasional calcification. Most pheochromocytomas, however, produce endocrine abnormalities and characteristic symptoms that permit a specific diagnosis, as do the features they sometimes display on T2-weighted MR images and scintigrams obtained with metaiodobenzylguanidine. None of our tumors was believed preoperatively to be a pheochromocytoma.

Calcified cystic lesions may also be produced by hydatid disease (15,42,43), and epithelial cysts without neoplasm have also been described (44,45).

The tumors in our series were selected so that none demonstrated the homogeneous low-attenuation appearance that permits specific diagnosis at CT (9), but other techniques for diagnosing adenomas, such as needle biopsy and out-of-phase gradient-echo MR imaging, were not applied to any of our tumors. We suspect these techniques would not have been effective. Loss of signal has not been shown to be diagnostic of adenoma if it occurs in only a small portion of a large, heterogeneous lesion imaged with gradient-echo techniques with fat and water out of phase (5). Biopsy of the adenomas in this series would frequently have recovered necrotic and hemorrhagic tissue and, even if a small sample were to contain viable adenoma, it would be difficult to be confident that no other part of a heterogeneous tumor contained malignant tissue. We conclude, therefore, that these radiologically atypical adenomas will continue to require resection.



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  		Figure 2a. Adrenal adenoma with infarction discovered incidentally at CT in a 64-year-old woman. (a) Contrast-enhanced CT scan shows a low-attenuation mass with an enhancing wall (arrows) and peripheral nodules (arrowheads). (b) Cut section of gross specimen shows hemorrhagic necrosis (*); only the small yellow regions at the periphery of the mass are adenoma tissue.

 



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  		Figure 2b. Adrenal adenoma with infarction discovered incidentally at CT in a 64-year-old woman. (a) Contrast-enhanced CT scan shows a low-attenuation mass with an enhancing wall (arrows) and peripheral nodules (arrowheads). (b) Cut section of gross specimen shows hemorrhagic necrosis (*); only the small yellow regions at the periphery of the mass are adenoma tissue.

 



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  		Figure 3a. Adrenal adenoma discovered incidentally at ultrasonography in an 81-year-old man. (a) Contrast-enhanced CT scan shows peripheral enhancement (arrow) and a central region of irregular low attenuation (*). The tiny area of high attenuation in the anterior of the mass is an artifact. (b) Cut section of gross specimen shows hemorrhagic necrosis (*); the only viable adenoma is represented by the irregular yellow regions.

 



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  		Figure 3b. Adrenal adenoma discovered incidentally at ultrasonography in an 81-year-old man. (a) Contrast-enhanced CT scan shows peripheral enhancement (arrow) and a central region of irregular low attenuation (*). The tiny area of high attenuation in the anterior of the mass is an artifact. (b) Cut section of gross specimen shows hemorrhagic necrosis (*); the only viable adenoma is represented by the irregular yellow regions.

 


   Acknowledgments
 
The illustrations contained herein come from the cases in the archives of the department of radiologic pathology. The authors are indebted to all of the radiologists and pathologists whose contributions of outstanding cases to the AFIP have made this publication possible.


   Footnotes
 
Current address: West Reading Radiology Associates, West Reading, Pa. Back

Current address: West Reading Radiology Associates, West Reading, Pa. Back

Current address: Department of Radiology, University of Nebraska Medical Center, Omaha. Back

Address reprint requests to J.H.N., Department of Radiology, Columbia-Presbyterian Medical Center, 177 Ft Washington Ave, New York, NY 10032.

The opinions expressed herein are not to be construed as those of the Departments of Defense, Army, or Navy.

Abbreviation: AFIP = Armed Forces Institute of Pathology

Author contributions: Guarantor of integrity of entire study, J.H.N.; study design, J.H.N., B.J.W., A.J.D., T.J.I.; definition of intellectual content, J.H.N., C.S.H., B.J.W., T.J.I., C.F.A., A.J.D.; literature research, J.H.N.; data acquisition and analysis, J.H.N., C.S.H., B.J.W., T.J.I., C.F.A., A.J.D.; manuscript preparation, J.H.N. manuscript editing and review, J.H.N., B.J.W., T.J.I., A.J.D., C.S.H.

Received January 7, 1998; revision requested March 17, 1998; revision received June 8, 1998; accepted September 28, 1998.
   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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