Clinical Practice
The Incidentally Discovered Adrenal Mass
N Engl J Med 2007; 356:601-610February 8, 2007
- Article
This Journal feature begins with a case vignette highlighting a common clinical problem. Evidence supporting various strategies is then presented, followed by a review of formal guidelines, when they exist. The article ends with the author's clinical recommendations.
A 68-year-old woman is incidentally found to have a left adrenal mass, 2.8 cm in diameter, on abdominal computed tomography that was ordered to evaluate right lower abdominal discomfort (which has since resolved). Her medical history is notable only for hypertension that has been well controlled with hydrochlorothiazide, at a dose of 25 mg daily. She reports no sweating, palpitations, headache, weight gain, or proximal muscle weakness. Her physical examination is unremarkable. How should she be evaluated?
The Clinical Problem
An adrenal “incidentaloma” is an adrenal mass, generally 1 cm or more in diameter, that is discovered serendipitously during a radiologic examination performed for indications other than an evaluation for adrenal disease.1 This definition excludes cases in which a symptomatic adrenal-dependent syndrome is “missed” because of a superficial interview or physical examination.1 The widespread use of abdominal ultrasonography, computed tomography (CT), and magnetic resonance imaging (MRI) has resulted in the clinical dilemma of the adrenal incidentaloma.
Numerous autopsy studies have examined the frequency of incidental adrenal nodules.2 In a report on 25 studies, the overall frequency of adrenal adenomas in 87,065 autopsies was 6% (range, 1 to 32).1,2 Abdominal CT yields similar findings; a recent study reported a prevalence of adrenal incidentaloma of 4%.3 The prevalence of adrenal adenomas increases with increasing age1,2: the probability of finding an unsuspected adrenal adenoma on abdominal CT in a patient between 20 and 29 years of age would be approximately 0.2%, as compared with approximately 7% in a patient over 70 years of age.1,2
The majority of adrenal incidentalomas are clinically nonhypersecreting, benign adrenocortical adenomas.4 Other frequently reported diagnoses include cortisol-secreting adrenocortical adenoma, pheochromocytoma, adrenocortical carcinoma, and metastatic carcinoma.1
Strategies and Evidence
The optimal diagnostic approach to a patient who has an adrenal incidentaloma has not been established.1,4-6 However, it is reasonable to start by taking a careful history and performing a physical examination, focusing on the signs and symptoms suggestive of adrenal hyperfunction or malignant disease (Table 1Table 1
Symptoms and Signs Suggestive of Adrenal Hyperfunction or Malignant Disease.) and hormonal testing7,8 (Table 2Table 2
Laboratory Evaluation of the Patient with Adrenal Incidentaloma.). Although no specific diagnostic approach has been prospectively validated, an algorithm based on clinical experience and data regarding laboratory and imaging studies is shown in Figure 1Figure 1
Algorithm for the Evaluation of Patients with an Adrenal Incidentaloma..Hormonal Evaluation
Subclinical Cushing's Syndrome
The term “subclinical” Cushing's syndrome is used to refer to autonomous cortisol secretion in patients who do not have the typical signs and symptoms of hypercortisolism. Although the obvious stigmata of Cushing's syndrome are absent, these patients may have the adverse effects of continuous, endogenous cortisol secretion, including hypertension, obesity, diabetes mellitus, and osteoporosis.9-13
In a report summarizing the results of 13 studies including 2005 patients with adrenal incidentalomas, autonomous cortisol secretion (independent of normal hypothalamic–pituitary control) was found in 5.3% of the patients.1 Since such patients do not have clinical Cushing's syndrome and may have normal 24-hour urinary cortisol excretion, a measure of autonomous adrenocortical secretion is the best strategy for testing. Because there is no reliable way to distinguish between low-normal values and suppressed values with most commercially available corticotropin assays, adrenal autonomy is best assessed by an overnight dexamethasone (1 mg) suppression test (Table 2).1,14 Although the optimal cutoff value is debated, the use of a cortisol level greater than 5 μg per deciliter (138 nmol per liter) is standard to define abnormal values according to this test,15,16 because this level is considered to be a reasonable criterion for clinically significant glucocorticoid secretory autonomy.15 The specificity of the 1-mg overnight dexamethasone suppression test is 91%17,18; if the result is abnormal, confirmatory testing should be performed to rule out a false positive result (Table 2).
Data from randomized trials are lacking to guide the optimal management of subclinical Cushing's syndrome. A reasonable strategy is to consider adrenalectomy for younger patients (below the age of 40 years) and those with disorders that are potentially attributable to autonomous glucocorticoid secretion (e.g., the recent onset or worsening of underlying hypertension, diabetes mellitus, obesity, or osteoporosis). A patient with subclinical Cushing's syndrome should receive glucocorticoid therapy perioperatively because of the risks of adrenal insufficiency, hemodynamic crisis, and death.19 The need for longer-term replacement and slow tapering of exogenous glucocorticoids should be assessed postoperatively. In limited case series, weight loss, improvement in hypertension or glycemic control or both, and the normalization of markers of bone turnover were reported after unilateral adrenalectomy in patients with subclinical Cushing's syndrome.9,11,14 Long-term prospective studies are needed to provide a better understanding of the natural history of subclinical Cushing's syndrome and better guidance for decisions regarding surgical intervention.
At least two reports have suggested that cortisol secretion may be normal when the adrenal incidentaloma is discovered but may become autonomous during a subsequent period of 4 years or longer.20,21 Until data are available from large prospective studies, these observations suggest that it is reasonable to repeat the hormonal screening annually for 4 years, as suggested by the National Institutes of Health (NIH) state-of-the-science statement.5
Clinically Silent Pheochromocytoma
Approximately 5% of adrenal incidentalomas have proved to be pheochromocytomas.1 In one study, 19 of 33 adrenal pheochromocytomas (58%) were detected initially as incidental adrenal masses, and only 10 of the 19 patients had hypertension.22 However, even clinically silent pheochromocytomas can be lethal.23
The characteristics of an adrenal mass on imaging — the imaging phenotype — can be helpful in determining whether it is a pheochromocytoma1 (Table 3Table 3
Characteristics of Adrenal Incidentalomas on Imaging (Imaging Phenotype).). Findings consistent with (although not diagnostic of) pheochromocytoma include increased attenuation on unenhanced CT, prominent vascularity of the mass (Figure 2AFigure 2
Pheochromocytoma (Panel A), Benign Cortical Adenoma (Panel B), and Adrenocortical Carcinoma (Panel C).), delayed washout of contrast medium, and high signal intensity on T2-weighted MRI.22 Because not all pheochromocytomas have this phenotype and because the expertise of radiologists and clinicians in identifying this rare neoplasm can vary, biochemical assessment is warranted for all patients. Studies reporting the characteristics of biochemical tests for pheochromocytoma are based on data from both symptomatic and asymptomatic patients. The measurement of fractionated metanephrines and catecholamines in a 24-hour urine specimen is recommended for all patients with adrenal incidentalomas; the detection of elevated levels of fractionated metanephrines, catecholamines, or both has high sensitivity and specificity for pheochromocytoma (91 to 98% in Mayo Clinic series, for both).8,26,27 The additional measurement of fractionated catecholamines in the 24-hour urinary specimen increases the sensitivity of this approach by 5%8 and is especially helpful in diagnosing patients with dopamine-secreting neoplasms.26 If the suspicion of subclinical pheochromocytoma is high on the basis of the imaging phenotype but the results of 24-hour urinary studies are normal, the measurement of fractionated plasma free metanephrines (available at most reference laboratories) may be useful.28 Although elevated levels of fractionated plasma metanephrines have high sensitivity for pheochromocytoma (96 to 100%),26,28 the test has low specificity (85 to 89% overall26,28,29 and 77% in patients older than 60 years).26 Thus, the measurement of fractionated plasma metanephrines is recommended only when suspicion is high, to minimize the risk of false positive results that might lead to unnecessary surgery.
Primary Aldosteronism
Approximately 1% of adrenal incidentalomas have proved to be aldosterone-producing adenomas.1 Excessive secretion of aldosterone is associated with an increased risk of cardiovascular disease and other disorders,7 and the normalization of circulating aldosterone levels or mineralocorticoid receptor blockade is warranted in patients with excessive secretion of aldosterone.8 Screening for hyperaldosteronism is routinely recommended for hypertensive patients who have an adrenal incidentaloma. Given that patients with aldosterone-producing adenomas may have normal levels of potassium in the blood,30 the measurement of potassium levels is not reliable in screening. A reasonable screening test is the ratio of the ambulatory morning plasma aldosterone concentration to plasma renin activity (Table 2).30,31 If this ratio is high, the diagnosis of primary aldosteronism should be confirmed by an additional measurement of mineralocorticoid secretory autonomy (Table 2).8
Other Hormonally Active Processes
Sex hormone–secreting adrenocortical tumors are rare and typically occur in the presence of clinical manifestations (e.g., hirsutism or virilization).1 Routine screening for excess androgens or estrogens in patients with adrenal incidentalomas is therefore not warranted.
Nonclassic congenital adrenal hyperplasia is another infrequent cause of adrenal incidentalomas (unilateral or bilateral).1 Cosyntropin-stimulation testing with the measurement of cortisol precursors (e.g., 17-hydroxyprogesterone) is not routinely recommended but, rather, should be reserved for patients in whom the diagnosis is suspected on the basis of clinical manifestations (e.g., hyperandrogenism) or the presence of bilateral adrenal masses.
Assessment of Malignant Potential
The possibility of malignant disease is the major concern when an incidental adrenal mass is identified. Among 2005 patients in whom adrenal incidentalomas were detected, adrenocortical carcinoma was found in 4.7% of the patients and metastatic cancer in 2.5%.1 The size of the mass and its appearance on imaging are the two major predictors of malignant disease.
Size of Adrenal Mass
In a report involving 887 patients who had adrenal incidentalomas,32 a diameter greater than 4 cm was shown to have 90% sensitivity for the detection of adrenocortical carcinoma but low specificity; only 24% of lesions greater than 4 cm in diameter were malignant.32 Size is also important because the smaller an adrenocortical carcinoma is at the time of diagnosis, the lower the tumor stage is and the better the overall prognosis will be.33 Although most experts would recommend resection of adrenal masses larger than 6 cm in diameter,5 decisions regarding surgery should also take into account the imaging phenotype of the mass, as well as the patient's age and any coexisting conditions. For example, a nonfunctioning adrenal incidentaloma that is 6.5 cm in diameter and has a benign imaging phenotype may be reasonably followed in an octogenarian. Because the prevalence of benign adrenal cortical adenomas increases with age, the finding of a nonfunctioning adrenal mass that is 3.2 cm in diameter in a younger patient (e.g., below the age of 30 years) should increase the suspicion of an alternative diagnosis. The size of an adrenal incidentaloma does not affect recommendations regarding biochemical testing.
Imaging Phenotype
The CT features used to distinguish adenomas from nonadenomas are the lipid content of the adrenal mass and rapidity of the washout of contrast medium (Table 3).34 The intracytoplasmatic fat in adenomas results in low attenuation on unenhanced CT (Figure 2B); nonadenomas have higher attenuation on unenhanced CT.34 On chemical-shift MRI (a form of lipid-sensitive imaging that is routinely used), benign adrenocortical adenomas lose signal on out-of-phase images, as compared with in-phase images.35 However, up to 30% of adenomas do not contain large amounts of lipid and may be indistinguishable from nonadenomas on both unenhanced CT and chemical-shift MRI.34
On delayed contrast-enhanced CT, adenomas typically exhibit rapid washout of contrast medium, whereas other adrenal nonadenomas have delayed washout of contrast material (Table 3).36 Ten minutes after the administration of the contrast medium, an absolute washout of more than 50% of the contrast medium was reported to be 100% sensitive and specific for adenoma in a comparison between patients with adenomas and those with carcinomas, pheochromocytomas, or metastatic disease.34,36,37 Although the imaging phenotype does not predict hormonal function, it does predict the underlying pathology, and surgical resection should be considered for patients who have adrenal incidentalomas with a suspicious imaging phenotype (Figure 2C).
Metastatic Disease
Metastases are the cause of the adrenal incidentaloma in approximately half of patients who have a history of malignant disease.38 Tumors that commonly metastasize to the adrenals include carcinomas of the lung, kidney, colon, breast, esophagus, pancreas, liver, and stomach (Figure 3A and 3BFigure 3
Serial CT Scans Showing Metastatic Disease to the Adrenal Gland (Panels A and B), a Benign Pheochromocytoma (Panels C through F), and Adrenocortical Carcinoma (Panels G and H).).39 Metastases to the adrenal glands are frequently bilateral. The primary cancer usually has already been recognized when an adrenal incidentaloma is discovered; metastatic cancer to the adrenal without a known primary cancer is extremely rare.40 Positron-emission tomography (PET) with 18F-fluorodeoxyglucose (18F-FDG) can be helpful in selected patients (those with a history of malignant disease) because of its high sensitivity in detecting malignant diseases.41 However, 16% of benign adrenal lesions may have greater FDG-PET uptake than the background uptake.41 The absence of activity on 11C-metomidate (MTO)–PET appears to be specific for tumors of nonadrenocortical origin (e.g., pheochromocytomas and metastatic disease),42 but this type of imaging is not routinely available. Because of their cost and because there are insufficient data to support their routine use, FDG-PET and MTO-PET are not recommended for the evaluation of a patient with an adrenal incidentaloma who does not have a history of malignant disease.
Fine-Needle Aspiration Biopsy
The primary role of fine-needle aspiration biopsy is to differentiate between adrenal tissue and nonadrenal tissues (e.g., metastases or infection).43-45 Image-guided fine-needle aspiration biopsy is relatively safe; the complication rate was 2.8% in one series of 277 biopsies.45 The risks of this procedure include adrenal hematoma, abdominal pain, hematuria, pancreatitis, pneumothorax, formation of an adrenal abscess, and tumor recurrence along the needle track.1,44,45 Also, fine-needle aspiration biopsy of a pheochromocytoma may result in hemorrhage and hypertensive crisis, and the possibility of pheochromocytoma should always be ruled out by biochemical testing before fine-needle aspiration biopsy is undertaken.46,47
Bilateral Adrenal Masses
When adrenal masses occur bilaterally (as they do in up to 15% of patients with adrenal incidentaloma),20,32 the most likely diagnoses are metastatic disease, congenital adrenal hyperplasia, bilateral cortical adenomas, and infiltrative disease of the adrenal glands.1 Adrenocortical hypofunction may occur in patients with bilateral adrenal masses, so screening for adrenocortical hypofunction may be prudent in such patients, although the yield is unknown.
Areas of Uncertainty
The optimal frequency and duration of follow-up for patients who have adrenal incidentalomas are uncertain, and prospective data to guide the clinician are scarce. Repeated imaging is commonly recommended at 6, 12, and 24 months; earlier follow-up (at 3 months) has been suggested when the imaging phenotype is suspicious (Figure 1), with the rationale that many malignant lesions will grow during this 3-month interval (Figure 3A and 3B), resulting in earlier intervention. However, the yield and cost-effectiveness of repeated imaging at these intervals are uncertain. On the basis of our unpublished experience with nine patients who underwent serial imaging, the typical rate of growth of benign adrenal pheochromocytoma is approximately 0.5 to 1.0 cm in diameter per year (Figure 3C through 3F), whereas adrenocortical carcinomas typically have a rapid growth rate (>2 cm per year) (Figure 3G and 3H). However, most adrenal masses that grow are not malignant. In case series of adrenal incidentalomas followed for an average of 4 years, 5 to 20% increased in size, and 1.3 to 5.2% decreased in size.1,21,48 In two of these series, only 1 of 9 patients and none of 11 patients with enlarging adrenal masses who underwent surgery were found to have malignant tumors.21,48 Less frequent imaging during follow-up is reasonable for patients who have no history of malignant disease and who have small (<2 cm), uniform, hypodense cortical nodules.
The observation that abnormal adrenal function (secretion of glucocorticoids and catecholamines) that is not present at baseline may be detected during follow-up testing21,48,49 has led to the recommendation of repeating hormonal evaluation annually for at least 4 years when the initial evaluation is negative.5,48,49 However, the yield and cost-effectiveness of such testing are unknown.
Guidelines
No comprehensive guidelines have been published by professional societies to guide the evaluation of patients with adrenal incidentalomas. The recommendations given here are in general agreement with the NIH state-of-the-science statement on adrenal incidentalomas, which was published in 2003.5
Conclusions and Recommendations
For the patient described in the vignette, a thorough history should be obtained and a physical examination performed to assess the evidence of adrenal hormone excess (Table 1). I would perform a 1-mg overnight dexamethasone suppression test, collect a 24-hour urinary specimen for measurement of fractionated metanephrines and catecholamines, and (because she has hypertension) measure the plasma aldosterone concentration and plasma renin activity. If the results of the initial hormonal testing are consistent with autonomous hormone secretion, and if this finding is confirmed by subsequent studies, unilateral laparoscopic adrenalectomy should be considered. The adrenal imaging should be reviewed with a radiologist. If the imaging phenotype suggests infection or metastatic disease, CT-guided fine-needle aspiration biopsy should be considered (after biochemical testing to rule out pheochromocytoma). If the results of hormonal testing are normal and the imaging features are consistent with benign disease, I would recommend repeating the imaging studies at 6, 12, and 24 months and repeating the hormonal evaluation yearly for 4 years, even though there are no data from large, long-term studies to support these recommendations. Although the data are also scarce to suggest when surgery is necessary, I would recommend consideration of adrenalectomy if the adrenal mass is 4 cm or greater in diameter, if the mass enlarges by 1 cm or more during the period of observation, or if evidence of autonomous hormonal secretion develops.
No potential conflict of interest relevant to this article was reported.
Source Information
From the Division of Endocrinology, Diabetes, Metabolism, Nutrition, and Internal Medicine, Mayo Clinic, Rochester, MN.
Address reprint requests to Dr. Young at the Division of Endocrinology, Diabetes, Metabolism, Nutrition, and Internal Medicine, Mayo Clinic, 200 First St. SW, Rochester, MN 55905, or at young.william@mayo.edu.
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