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Keywords:

  • adrenal;
  • adrenal cyst;
  • pseudocyst;
  • adrenal cortical carcinoma;
  • pheochromocytoma

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

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. © 2004 American Cancer Society.

Cystic 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 Endothelial 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 discovered 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 differentiated from adrenal neoplasms demonstrating foci of cystic or degenerative changes. Radiologic studies can be helpful in the presurgical diagnosis of cystic lesions of the adrenal gland.7, 8 Computed tomography (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. Marked hemorrhage or degeneration within a pheochromocytoma or an adrenal cortical tumor may result in a pseudocyst. Hemorrhage or degeneration within a benign adrenal neoplasm must be differentiated 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

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

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. Formalin-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 macroscopically through photographs, pathology, and surgical reports, as well as by microscopic review.

Clinical Information

Clinical history and follow-up information including patient age and gender, tumor location, and presenting symptoms were obtained by chart review (Table 1). Approval from the Mayo Clinic Institutional Review Board was obtained for the study.

Table 1. Clinicopathologic Features of Patients with Adrenal Cysts
DiagnosisNo. of casesMean age (yrs) (range)Female/male ratioMean size (cm) (range)Right sideLeft sideDiscovered incidentally
  • 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.

Overall4150 (16–81)22/199.3 (1–29)19227
Pseudocysta3252 (27–81)17/159.7 (3–29)17156
Endothelialb841 (16–60)5/35.8 (2.5–9)261
Epithelial1530/14010

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 being 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 antibodies to CD31 and factor VIII antigen. Endothelial cysts were subclassified as lymphangiomatous or angiomatous. 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 classified according to cyst type.

Primary adrenal neoplasms associated with adrenal 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 degeneration were excluded.

Immunohistochemistry

Formalin-fixed, paraffin-embedded tissue sections were cut at 5 μm and treated with 0.1 mol/L of citrate (pH 6.0) in an 800-watt microwave oven for 15 minutes for antigen 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/AE3) (dilution of 1:200; Zymed Laboratory Inc., San Francisco, CA) were utilized. Immunostaining was performed with the elite avidin-biotin-peroxidase kit (Vector Laboratories, Burlingame, CA) according to the manufacturer's specifications. Slides were counterstained with hematoxylin for 1 second

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

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 adrenal adenomas were found to be almost entirely cystic.

Table 2. Clinicopathologic Features of Patients with Adrenal Pseudocysts
DiagnosisNo. of casesMean age (yrs)Female/male ratioMean size (cm) (range)Right sideLeft sideClinically functional
  • 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.

Pseudocysts, overall3252 (27–81)17/159.7 (3–29)17153a
Pseudocysts without associated adrenal neoplasm2650 (27–77)13/1310 (2.5–29)11150
Pseudocysts with associated adrenal neoplasmb659 (30–81)4/211.5 (5–28.5)603a
Table 3. Adrenal Neoplasms Associated with Adrenal Cysts
DiagnosisNo. of casesMean age (yrs) (range)Female/male ratioMean size (cm) (range)Right sideLeft sideFollow-up
  • 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.

Adrenal cortical adenomaa254 (49–58)0/210 (8.5–11.5)20Both patients were alive without disease
Adrenal cortical carcinomaa254 (30–77)2/09.5 (9–10)20Both patient had died of disease
Pheochromocytomab367 (60–81)2/111.3 (4–25)21All three patients were alive without disease.

Seven of the 41 cases (17%) were discovered incidentally. Five of these seven lesions were found incidentally on radiographic imaging that was performed for other reasons, and two were discovered incidentally 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, endothelial 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 adrenal neoplasm (Tables 2 and 3). Two adrenal cortical carcinomas, two adrenal cortical adenomas, and two pheochromocytomas were identified in association with a pseudocyst.

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Figure 1. Adrenal pseudocyst. Ultrasound (longitudinal section) of the upper abdomen demonstrating a rounded soft tissue mass (long arrow) relative to the spleen (short arrow) and the upper pole of the kidney (curved arrow). The lesion was anechoic without mural nodules present.

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Figure 2. Adrenal pseudocyst. Contrast-enhanced computed tomography axial image showing the adrenal cyst (arrow) lying entirely within the left adrenal gland.

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Figure 3. Macroscopic and microscopic features of cystic tumors of the adrenal gland. (A) Adrenal pseudocyst with fibrinous exudate. (B) Adrenal endothelial cyst with trabeculated inner surface. (C) Pheochromocytoma associated with a hemorrhagic pseudocyst. (D) Pheochromocytoma associated with a smooth-walled pseudocyst. (E) Adrenal endothelial cyst with a delicate lining of endothelial cells (H & E, medium power). (F) Adrenal endothelial cyst lining staining positive for the vascular marker CD31 (CD31 immunostain, medium power). (G) Adrenal pseudocyst wall with rim of normal adrenal parenchyma identified within the wall and hemorrhage found on the internal surface of the cyst wall (H & E, medium power). (H) Adrenal cortical carcinoma associated with a pseudocyst. Nests of malignant adrenal cortical cells in the wall of the pseudocyst in a patient who died of metastatic adrenal cortical carcinoma (H & E, low power). (I) Foci of pheochromocytoma in the wall of an adrenal pseudocyst (H & E, high power). (J) Pheochromocytoma associated with a pseudocyst showing nests of tumor cells with rounded to ovoid nuclei (H & E, medium power).

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The endothelial cysts were subclassified as lymphangiomatous and angiomatous. Immunohistochemical stains for CD31 and factor VIII antigen confirmed the endothelial lining in these cases (Fig. 3). Of the eight endothelial cysts, six were lymphangiomatous and two were angiomatous. One angiomatous cyst was identified in association with a pheochromocytoma. One epithelial-lined cyst was identified. Immunohistochemical stains for keratin AE1/AE3 confirmed 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 associated with an adrenal cortical carcinoma, two with an adrenal cortical adenoma, and three with a pheochromocytoma. 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 malignancy including eosinophilic tumor cell cytoplasm, vascular invasion (venous invasion, sinusoidal invasion), necrosis, fibrous bands, mitotic figures, atypical mitotic figures, nuclear pleomorphism, and foci of necrosis. Tumor cell necrosis was coagulative and therefore differed from areas of degeneration and hemorrhage. Hemorrhage 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, calcifications were identified in the walls of the adrenal cysts, including adrenal cysts with associated adrenal cortical adenomas and carcinomas. Calcifications were not identified in the cysts associated with the pheochromocytomas.

Follow-Up

Both patients with pseudocysts associated with adrenal 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

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES

Cystic adrenal lesions are uncommon, span a broad spectrum of primary adrenal tumors, and may be associated 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 incidentally. 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 functioning, aldosterone-producing adrenal cortical carcinoma. 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 hemorrhagic and necrotic pheochromocytomas, and 4 were of undetermined origin.2 In a series of 13,996 autopsies, 9 unsuspected adrenal cysts were identified, including 3 pseudocysts, 2 lymph cysts, 2 lymphangiectatic 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 radiographic 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 elevated 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 appeared to invade into the inferior vena cava. The other patient with a cystic adrenal cortical carcinoma presented with a rash and was found to have hepatomegaly. A CT scan showed a large cystic mass with a calcific rim displacing the liver. During surgical marsupialization of the cyst, malignancy was suspected. The cyst later was resected and found to be a cystic adrenal cortical carcinoma with lymph node metastases. Although the majority of patients were symptomatic, the increasing utilization of advanced cross-sectional 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 hematoma or a toxic or infectious process, with fewer considered to result from hemorrhage in an adrenal tumor.1, 3 Other authors have reported an apparent vascular origin for pseudocysts,14 and staining for endothelial cell markers has been noted.15, 16 It is interesting to note that foci of vascular canalization were identified in some of the pseudocysts associated with marked hemorrhage. This finding may reflect canalization 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 degeneration in a hamartoma.17 Epithelial cysts are reported much less often, reportedly accounting for only approximately 9% of cases.1, 3 Epithelial cysts were defined in the current study as having a true epithelial lining confirmed by keratin immunoreactivity. Adrenal cysts associated with primary adrenal neoplasms were classified according to cyst type and were not reflexively placed into the epithelial category, the reason being that the majority of cysts associated with adrenal tumors had clearly identifiable cyst walls that lacked epithelial lining and were classified as pseudocysts, 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,10 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 reported in association with a variety of diseases including 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 identified 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.10 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 finding. 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 pheochromocytomas6, 29, 30 and adrenal cortical adenomas.6 We are not aware of previously reported cases of cystic adrenal cortical carcinomas. Marked hemorrhage into an adrenal neoplasm with cyst formation and subsequent resorption of the blood is a likely explanation for the cystic change. Extensive degeneration within an adrenal cortical neoplasm or a pheochromocytoma also may result in a pseudocyst.

Adrenal cortical cysts must be differentiated from malignant adrenal neoplasms. Hemorrhage or degeneration within a pheochromocytoma or an adrenal cortical neoplasm may result in a pseudocyst. Hemorrhage 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 tissues 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 carcinomas are extremely uncommon, it is important for the pathologist to make the diagnosis when a malignancy is present. Distinguishing adrenal cysts from neoplasms of the adrenal gland demonstrating cystic changes should be performed with extensive pathologic sampling of any macroscopically suspicious lesion.

REFERENCES

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. REFERENCES
  • 1
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  • 27
    Petit T, de Lagausie P, El Ghoneimi A, Garel C, Aigrain Y. Postnatal management of cystic neuroblastoma. Eur J Pediatr Surg. 2001; 11: 411414.
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