Cystic Adrenal Neoplasms
Lori A. Erickson, M.D.1 Ricardo V. Lloyd, M.D., Ph.D.1 Robert Hartman, M.D.2 Geoffrey Thompson, M.D.3
1 Department of Laboratory Medicine and Pathol- ogy Mayo Clinic, Rochester, Minnesota.
2 Department of Radiology, Mayo Clinic, Roches- ter, Minnesota.
3 Department of Surgery, Mayo Clinic, Rochester, Minnesota
BACKGROUND. Cystic lesions of the adrenal gland are uncommon and demonstrate a spectrum of histologic changes and may vary from pseudocysts to malignant cystic neoplasms.
METHODS. The authors analyzed a series of primary cystic lesions of the adrenal gland to evaluate the clinicopathologic features and histologic spectrum and to determine features that are helpful in distinguishing benign from malignant cystic adrenal tumors.
RESULTS. A total of 41 cases of macroscopically cystic lesions among patients who underwent surgery at the Mayo Clinic were identified over a 25-year period. Of these 41 cases, 32 were pseudocysts, 8 were endothelial cysts, and 1 was an epithelial cyst. Of the 32 pseudocysts, 6 were associated with adrenal neoplasms, including 2 adrenal cortical carcinomas, 2 adrenal cortical adenomas, and 2 pheochromocytomas. One pheochromocytoma case was identified in association with an endothelial cyst. Both patients with cystic adrenal cortical carcinomas died of disease.
CONCLUSIONS. Adrenal neoplasms, including adrenal cortical carcinomas, may be associated with benign-appearing cysts. Extensive pathologic sampling of resected tissues is important to rule out malignancy in patients with cystic adrenal lesions. Cancer 2004;101:1537-44. @ 2004 American Cancer Society.
KEYWORDS: adrenal, adrenal cyst, pseudocyst, adrenal cortical carcinoma, pheo- chromocytoma.
C ystic adrenal neoplasms are uncommon and may be discovered incidentally or may be symptomatic. Traditionally, adrenal gland cysts have been classified as pseudocysts, endothelial cysts, epithelial cysts, and parasitic cysts.1-3 Pseudocysts are reported to be the most common clinically recognized adrenal cyst in surgical series.1,3 Endo- thelial cysts are divided into lymphangiomatous and angiomatous.1,3 Epithelial cysts are uncommon, and have been divided into true glandular cysts and embryonal cysts, and some authors include cystic adrenal tumors in this category.1,3 Parasitic cysts usually are discov- ered incidentally at autopsy and have been reported to account for approximately 7% of cases.1,3 Small series of cystic neoplasms of the adrenal gland have been reported previously.4-6 However, to our knowledge, the clinicopathologic features of cystic adrenal lesions from one institution have not been reported previously.
Cystic adrenal neoplasms must be differentiated from adrenal cysts. Adrenal cysts may be observed in association with neoplasms of the adrenal medulla and adrenal cortex, but they should be differen- tiated from adrenal neoplasms demonstrating foci of cystic or degen- erative changes. Radiologic studies can be helpful in the presurgical diagnosis of cystic lesions of the adrenal gland.7,8 Computed tomog- raphy (CT) has been reported to be very effective in recognizing cystic lesions, but may not be able to distinguish benign from malignant adrenal cysts.9 Neoplastic adrenal cysts may present in different ways.
Address for reprints: Lori A. Erickson, M.D., De- partment of Laboratory Medicine and Pathology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905; Fax: (507) 284-1599; E-mail: erickson. lori@mayo.edu
Received May 12, 2004; revision received June 22, 2004; accepted June 30, 2004.
| Diagnosis | No. of cases | Mean age (yrs) (range) | Female/male ratio | Mean size (cm) (range) | Right side | Left side | Discovered incidentally |
|---|---|---|---|---|---|---|---|
| Overall | 41 | 50 (16-81) | 22/19 | 9.3 (1-29) | 19 | 22 | 7 |
| Pseudocystª | 32 | 52 (27-81) | 17/15 | 9.7 (3-29) | 17 | 15 | 6 |
| Endothelialb | 8 | 41 (16-60) | 5/3 | 5.8 (2.5-9) | 2 | 6 | 1 |
| Epithelial | 1 | 53 | 0/1 | 4 | 0 | 1 | 0 |
a Two adrenal cortical carcinomas, two adrenal cortical adenomas, and two pheochromocytomas were identified in association with a pseudocyst.
b One pheochromocytoma was identified in association with an endothelial (angiomatous) cyst.
Marked hemorrhage or degeneration within a pheo- chromocytoma or an adrenal cortical tumor may re- sult in a pseudocyst. Hemorrhage or degeneration within a benign adrenal neoplasm must be differenti- ated from coagulative tumoral necrosis, an ominous finding in neoplasms of the adrenal gland. In addition, adrenal cysts, particularly adrenal pseudocysts, may be very large, measuring > 20 cm in size. In addition to primary cystic lesions, metastatic tumors may present as adrenal cysts.10 Therefore, the evaluation of cystic adrenal lesions is important both in recognizing true adrenal cysts and in differentiating these lesions from malignant neoplasms of the adrenal gland.
The goals of the current study were to review the characteristics of adrenal cysts from a single institution that were surgically removed over a 25-year period and to identify those features of adrenal cysts that are helpful in differentiating them from cystic adrenal malignancies.
MATERIALS AND METHODS
Cases and Tissues
Forty-one cystic lesions of the adrenal gland were identified from the files of the Mayo Clinic Tissue Registry from patients who underwent surgery at the Mayo Clinic (Rochester, MN) between 1973-1998. For- malin-fixed, paraffin-embedded tissue blocks from 41 patients were used. Hematoxylin and eosin-stained sections were reviewed by two pathologists (L.A.E. and R.V.L.) for verification of diagnosis. Macroscopic pathologic features were obtained through review of the pathology reports, macroscopic photographs, and surgical reports. The cysts were documented macro- scopically through photographs, pathology, and sur- gical reports, as well as by microscopic review.
Clinical Information
Clinical history and follow-up information including patient age and gender, tumor location, and present- ing symptoms were obtained by chart review (Table 1). Approval from the Mayo Clinic Institutional Review Board was obtained for the study.
Classification
All the tumors were macroscopically found to be cysts. Tumors demonstrating only areas of cystic change or foci of cystic degeneration were excluded. The adrenal cysts were classified as pseudocysts, endothelial cysts, and epithelial cysts. Pseudocysts were defined as be- ing clearly identifiable cysts with walls that lacked lining epithelium or endothelium. Endothelial cysts had a clearly identifiable endothelial lining that was confirmed by immunoperoxidase studies using anti- bodies to CD31 and factor VIII antigen. Endothelial cysts were subclassified as lymphangiomatous or an- giomatous. Lymphangiomatous cysts are comprised of numerous small locules or cysts varying in size from 1-15 mm and containing a smooth, flat, endothelial lining, and the walls do not contain elastic tissue or nerves.1 Epithelial cysts were defined as having a true epithelial lining confirmed by immunoperoxidase studies with antibodies to keratin (AE1/AE3). In the seven cases of adrenal cysts found to be associated with primary adrenal neoplasms, the cysts were clas- sified according to cyst type.
Primary adrenal neoplasms associated with adre- nal cysts also were classified according to tumor type, including adrenal cortical adenoma, adrenal cortical carcinoma, and pheochromocytoma. In these cases, the tumors were found macroscopically to be cysts with foci of tumor identified in the cyst wall. Tumors showing only areas of cystic change or cystic degen- eration were excluded.
Immunohistochemistry
Formalin-fixed, paraffin-embedded tissue sections were cut at 5 pm and treated with 0.1 mol/L of citrate (pH 6.0) in an 800-watt microwave oven for 15 minutes for anti- gen retrieval before immunostaining. The sections then were incubated with the primary antibodies overnight at room temperature. Antibodies to CD31 (dilution of 1:200; Dako Corporation, Carpinteria, CA), factor VIII (dilution of 1:500; Dako Corporation), and keratin (AE1/
| Diagnosis | No. of cases | Mean age (yrs) | Female/male ratio | Mean size (cm) (range) | Right side | Left side | Clinically functional |
|---|---|---|---|---|---|---|---|
| Pseudocysts, overall | 32 | 52 (27-81) | 17/15 | 9.7 (3-29) | 17 | 15 | 3ª |
| Pseudocysts without associated adrenal neoplasm | 26 | 50 (27-77) | 13/13 | 10 (2.5-29) | 11 | 15 | 0 |
| Pseudocysts with associated adrenal neoplasmb | 6 | 59 (30-81) | 4/2 | 11.5 (5-28.5) | 6 | 0 | 3ª |
a One adrenal cortical carcinoma associated with a pseudocyst was clinically aldosterone producing and both pheochromocytomas associated with a pseudocyst were clinically functioning. b Two adrenal cortical carcinomas, two adrenal cortical adenomas, and two pheochromocytomas were identified in association with a pseudocyst.
| Diagnosis | No. of cases | Mean age (yrs) (range) | Female/male ratio | Mean size (cm) (range) | Right side | Left side | Follow-up |
|---|---|---|---|---|---|---|---|
| Adrenal cortical adenomaª | 2 | 54 (49-58) | 0/2 | 10 (8.5-11.5) | 2 | 0 | Both patients were alive without disease |
| Adrenal cortical carcinomaª | 2 | 54 (30-77) | 2/0 | 9.5 (9-10) | 2 | 0 | Both patient had died of disease |
| Pheochromocytomab | 3 | 67 (60-81) | 2/1 | 11.3 (4-25) | 2 | 1 | All three patients were alive without disease. |
a Both adrenal cortical adenomas and both adrenal cortical carcinomas were associated with pseudocysts.
b Two pheochromocytomas were associated with pseudocysts, and one pheochromocytoma was associated with an endothelial (angiomatous) cyst.
AE3) (dilution of 1:200; Zymed Laboratory Inc., San Francisco, CA) were utilized. Immunostaining was per- formed with the elite avidin-biotin-peroxidase kit (Vec- tor Laboratories, Burlingame, CA) according to the man- ufacturer’s specifications. Slides were counterstained with hematoxylin for 1 second
RESULTS
Cases and Tissues
Of the 41 patients with cystic adrenal lesions, 22 were female and 19 were male (Tables 1-3). The age of the patients at the time of presentation ranged from 16-81 years with a mean age of 50 years. Twenty-one cysts were located on the left side and 20 were on the right side. The adrenal cysts ranged in size from 1-29 cm with a mean size of 9.3 cm. Thirty-one cases (76%) measured ≥ 5 cm, 12 of which measured ≥ 10 cm. The neoplasms were all found macroscopically to be cysts. Adrenal neoplasms demonstrating only foci of cystic change or degeneration were excluded. Of the 117 pheochromocytomas reviewed for the current study, 22 demonstrated cystic change but in only 3 of these cases were the neoplasms found to be predominantly cystic with only foci of pheochromocytoma identified in the cyst wall. Of the 79 adrenal cortical carcinomas and 123 adrenal cortical adenomas reviewed for the current study, only 2 adrenal carcinomas and 2 adre- nal adenomas were found to be almost entirely cystic.
Seven of the 41 cases (17%) were discovered inci- dentally. Five of these seven lesions were found inci-
dentally on radiographic imaging that was performed for other reasons, and two were discovered inciden- tally at the time of surgery for another reason. Thirty- four patients were symptomatic, with pain being the most common presenting symptom. All of the cysts were unilateral.
Classification
The adrenal cysts were classified as pseudocysts, en- dothelial cysts, and epithelial cysts (Table 1; Figs. 1-3).1 Pseudocysts were the most common finding, representing 78% of the cases (32 of 41 cases). Of the 32 pseudocysts, 6 (19%) were associated with an ad- renal neoplasm (Tables 2 and 3). Two adrenal cortical carcinomas, two adrenal cortical adenomas, and two pheochromocytomas were identified in association with a pseudocyst.
The endothelial cysts were subclassified as lym- phangiomatous and angiomatous. Immunohisto- chemical stains for CD31 and factor VIII antigen con- firmed the endothelial lining in these cases (Fig. 3). Of the eight endothelial cysts, six were lymphangioma- tous and two were angiomatous. One angiomatous cyst was identified in association with a pheochromo- cytoma. One epithelial-lined cyst was identified. Im- munohistochemical stains for keratin AE1/AE3 con- firmed the epithelial lining in this case. No parasitic cysts were identified.
Seven cysts were associated with an adrenal gland neoplasm (Tables 2, 3; Fig. 3). Two of these were asso-
ciated with an adrenal cortical carcinoma, two with an adrenal cortical adenoma, and three with a pheochro- mocytoma. Six of the seven cysts associated with an adrenal gland neoplasm were pseudocysts whereas one pheochromocytoma was associated with an endothelial angiomatous cyst. Cystic adrenal cortical carcinomas had areas demonstrating histologic features of malig- nancy including eosinophilic tumor cell cytoplasm, vas- cular invasion (venous invasion, sinusoidal invasion), necrosis, fibrous bands, mitotic figures, atypical mitotic
figures, nuclear pleomorphism, and foci of necrosis. Tu- mor cell necrosis was coagulative and therefore differed from areas of degeneration and hemorrhage. Hemor- rhage was identified in the majority of adrenal cysts, including cases associated with pheochromocytomas and adrenal cortical adenomas, but tended to be less common in adrenal cortical carcinomas. However, cal- cifications were identified in the walls of the adrenal cysts, including adrenal cysts with associated adrenal cortical adenomas and carcinomas. Calcifications were
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not identified in the cysts associated with the pheochro- mocytomas.
Follow-Up
Both patients with pseudocysts associated with adre- nal cortical carcinomas died of their disease. No other patient with a cystic adrenal tumor developed disease recurrences or metastases or died of their disease.
DISCUSSION
Cystic adrenal lesions are uncommon, span a broad spectrum of primary adrenal tumors, and may be as- sociated with adrenal neoplasms. In the current study, 41 cystic adrenal lesions were surgically resected at the Mayo Clinic over a 25-year period. The majority of patients were symptomatic, with pain being the most common presenting symptom. The most common clinical features are reported to be abdominal pain, gastrointestinal symptoms, and a palpable mass.1,11 Seven cases in the current series were discovered in- cidentally. Functioning cysts of the adrenal cortex and medulla also have been reported.5,12 One cyst in the current study was associated with a clinically func- tioning, aldosterone-producing adrenal cortical carci- noma. No adrenal cyst without an associated adrenal neoplasm was found to be clinically functioning.
Adrenal cysts are uncommon. To our knowledge, the 2 largest previous series to date each reported 12 cases of adrenal cysts.2,6 Bellantone et al. reported 8 of the 12 patients in their study were symptomatic.6 The cysts in their series included nine pseudocysts, one epithelial cyst (cystic adenoma), and two endothelial cysts. In another study of 12 adrenal cysts, 5 were found to be organized hematomas, 3 were hemor- rhagic and necrotic pheochromocytomas, and 4 were of undetermined origin.2 In a series of 13,996 autop- sies, 9 unsuspected adrenal cysts were identified, in- cluding 3 pseudocysts, 2 lymph cysts, 2 lymphangiec- tatic cysts, and 2 calcified cystic adenomas.4
Adrenal cysts may be discovered incidentally or may be symptomatic. Seven of the 41 cases (17%) in the current series were discovered incidentally. Five of the seven cysts were found incidentally on radio- graphic imaging performed for other reasons, and two of the seven cysts were discovered at the time of surgery for another reason. The most common clinical features reported are abdominal pain, gastrointestinal symptoms, and a palpable mass.1,11 Thirty-four of the 41 cases in the current study were symptomatic with pain being the most common presenting symptom. All three patients with cystic pheochromocytomas were symptomatic with headache, hypertension, and ele- vated urine metanephrines reported in two of the patients. The third patient presented with pain, weight
loss, and diarrhea, but normal urinary metanephrines. One patient with a cystic adrenal cortical carcinoma presented with hypertension and hypokalemia. A right adrenal mass was identified radiographically that ap- peared to invade into the inferior vena cava. The other patient with a cystic adrenal cortical carcinoma pre- sented with a rash and was found to have hepatomeg- aly. A CT scan showed a large cystic mass with a calcific rim displacing the liver. During surgical mar- supialization of the cyst, malignancy was suspected. The cyst later was resected and found to be a cystic adrenal cortical carcinoma with lymph node metasta- ses. Although the majority of patients were symptom- atic, the increasing utilization of advanced cross-sec- tional imaging may result in more incidental cystic adrenal tumors being discovered in the future.
Adrenal gland cysts have been classified as pseudocysts, endothelial cysts, epithelial cysts, and parasitic cysts.1-3 Of the 41 cases in the current series, 32 (78%) were pseudocysts, 8 (20%) were endothelial cysts, and 1 (2%) was an epithelial cyst. No parasitic cysts were identified.1,13 Pseudocysts are reported to be the most common clinically recognized adrenal cyst in surgical series,1,3 and represent a relatively heterogeneous group of cysts with most believed to be due to organization of a previous traumatic hema- toma or a toxic or infectious process, with fewer con- sidered to result from hemorrhage in an adrenal tu- mor.1,3 Other authors have reported an apparent vascular origin for pseudocysts,14 and staining for en- dothelial cell markers has been noted.15,16 It is inter- esting to note that foci of vascular canalization were identified in some of the pseudocysts associated with marked hemorrhage. This finding may reflect canali- zation in the process of hemorrhage resorption. To our knowledge, the etiology of endothelial cysts is not known, but they are postulated to result from ectasia of lymph channels or a maldevelopment of cystic de- generation in a hamartoma.17 Epithelial cysts are re- ported much less often, reportedly accounting for only approximately 9% of cases.1,3 Epithelial cysts were de- fined in the current study as having a true epithelial lining confirmed by keratin immunoreactivity. Adre- nal cysts associated with primary adrenal neoplasms were classified according to cyst type and were not reflexively placed into the epithelial category, the rea- son being that the majority of cysts associated with adrenal tumors had clearly identifiable cyst walls that lacked epithelial lining and were classified as pseudo- cysts, with the exception of a pheochromocytoma that was found to be associated with an endothelial cyst.
Unusual variants of adrenal pseudocysts have been reported, including those with intracystic fat and myelolipomatous metaplasia,1º features of a dermoid
cyst,18 and those with ectopic thyroid tissue.19 None of these features was identified in the cases studied in the current series. Adrenal gland cysts have been re- ported in association with a variety of diseases includ- ing polycystic renal disease,20 Klippel-Trenaunay- Weber syndrome,21 Beckwith-Wiedemann syndrome,22 an abdominal aortic aneurysm,23 and, rarely, with pregnancy.24 None of these associations were identi- fied in the current surgical series.
Rare cases of metastases from a variety of sites, particularly the breast, have been reported to form cystic masses of the adrenal gland and therefore must be considered in the differential diagnosis of a cystic adrenal mass.1º Rare cases of malignant lymphomas primary to the adrenal gland have been reported,25,26 but to our knowledge malignant lymphoma forming a cystic adrenal mass is an extremely uncommon find- ing. Cystic neuroblastomas and schwannomas of the adrenal gland also have been reported.27,28
Seven of the 41 adrenal cysts in the current series were associated with an adrenal neoplasm. Adrenal cysts have been reported with pheochromocyto- mas6,29,30 and adrenal cortical adenomas.6 We are not aware of previously reported cases of cystic adrenal cortical carcinomas. Marked hemorrhage into an ad- renal neoplasm with cyst formation and subsequent resorption of the blood is a likely explanation for the cystic change. Extensive degeneration within an adre- nal cortical neoplasm or a pheochromocytoma also may result in a pseudocyst.
Adrenal cortical cysts must be differentiated from malignant adrenal neoplasms. Hemorrhage or degen- eration within a pheochromocytoma or an adrenal cortical neoplasm may result in a pseudocyst. Hem- orrhage or degeneration must be distinguished from tumoral necrosis, an ominous finding in patients with adrenal medullary or cortical neoplasms. In addition, adrenal cysts may be very large, measuring > 20 cm. Thus, extensive pathologic sampling of resected tis- sues is needed to evaluate the histologic features and to search for foci of tumor in the cyst wall.
Cystic adrenal lesions are uncommon, span a broad spectrum of primary adrenal tumors, and can be associated with benign and malignant adrenal neoplasms. Although cystic adrenal cortical carcino- mas are extremely uncommon, it is important for the pathologist to make the diagnosis when a ma- lignancy is present. Distinguishing adrenal cysts from neoplasms of the adrenal gland demonstrating cystic changes should be performed with extensive pathologic sampling of any macroscopically suspi- cious lesion.
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