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1 All authors: Department of Radiology, University of Michigan, 1500 E Medical Center Dr., UH B1 D530, Ann Arbor, MI 48109.
Received May 28, 2003;
accepted after revision October 28, 2003.
Presented at the 2003 annual meeting of the American Roentgen Ray Society,
San Diego, CA.
Abstract
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MATERIALS AND METHODS. We reviewed 50 consecutive adrenal mass biopsies performed during a 48-month period. The patient demographics, technique of biopsy, pathology results, and results of any prior dedicated adrenal imaging with MRI or CT protocols were noted.
RESULTS. Only six (12%) of 50 biopsies were adenomas. Five of these six cases were preceded by dedicated adrenal CT or MRI. Thirty-five cases were metastatic disease, four were adrenal cortical carcinoma, three were pheochromocytoma, and two biopsies were nondiagnostic. Overall, 20 of 50 cases were preceded by a dedicated adrenal CT or MRI examination to exclude an adenoma; in 21 of the remaining 30 cases, the imaging characteristics before biopsy were inconsistent with the potential diagnosis of an adenoma and dedicated adrenal CT or MRI was not recommended.
CONCLUSION. The number of adrenal adenomas biopsied has declined markedly with the introduction of dedicated adrenal CT and MRI for adrenal adenomas. Percutaneous imaging-guided biopsy is useful in confirming the presence and nature of suspected metastatic deposits to the adrenal gland and in diagnosing or excluding adrenal adenomas in patients with equivocal imaging characteristics.
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The past decade has seen technical advances in specialized CT and MRI protocols, allowing more accurate and more specific noninvasive characterization of lesions of the adrenal gland, particularly benign adenomas. Application of these techniques has the potential to reduce the number of benign lesions biopsied, yielding a more rapid diagnosis while avoiding the risks of biopsy. This series was undertaken to evaluate the effect of dedicated adrenal CT and chemical shift MRI on the rate of biopsy of adrenal adenomas at a large academic medical center.
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The choice of CT or sonographic guidance was made by the radiologist. Local anesthesia with lidocaine was routinely used. Patients commonly received IV conscious sedation with midazolam and fentanyl, with hemodynamic and oximetric monitoring, at the discretion of the radiologist. In cases of fine-needle aspiration, the cytopathologist reviewed the samples at the time of biopsy. Fine-needle aspiration and core biopsy samples were sent to the pathology department for review. Patients were monitored in a recovery area after the biopsy procedure, typically for 4 hr, before discharge.
Histopathologic results are grouped into five main categories: benign adrenal tissue, which includes adrenal cortical adenomas and samples with benign- or normal-appearing adrenal cortical cells; metastases; adrenal cortical carcinoma; pheochromocytoma; and nondiagnostic, which includes any samples containing only skeletal muscle, nerve tissue, adipocytes, or hepatocytes without normal adrenal or neoplastic tissue.
Current practice at our institution for characterizing an adrenal mass as an adenoma using imaging includes the use of both CT [7] and MRI [8] as described in the following text. Using unenhanced CT, attenuation values of 10 H or less are considered diagnostic for a lipid-rich adenoma. For masses with higher attenuation values on unenhanced CT, contrast-enhanced CT is performed with attenuation values calculated at 60 sec and 15 min after injection. A percentage of washout is calculated according to the formula: (attenuation value at enhanced CT – attenuation value at delayed enhanced CT) / (attenuation value at enhanced CT – attenuation value at unenhanced CT) x 100. A percentage of washout equal to or greater than a threshold value of 60% is considered diagnostic of adenoma.
For evaluation of adrenal masses with MRI, we rely on chemical shift imaging. Opposed phase imaging is performed with a 1.5-T magnet using a T1-weighted gradient-recalled echo sequence. In-phase sequences use a TR range of 68–160 msec (based on the patient's ability to breath-hold) and a TE range of 4.2–4.9; opposed phase images are obtained with a similar TR and a TE of 2.1–2.9 sec. The characterization of a lesion as an adenoma relies on the qualitative visual assessment of a decreased relative signal intensity on opposed phase images, which indicates the presence of lipid.
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Histopathology Results
A diagnostic result, either benign or neoplastic adrenal or metastatic
tumor tissue, was obtained in 48 (96%) of the 50 biopsies
(Table 1).
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Metastatic lesions.—At histopathology review, 35 of 50 biopsy samples were consistent with metastasis from an extraadrenal primary neoplasm. The mean mass size of the metastatic deposits was 4.4 cm (median, 3.5 cm; range, 1.5–12 cm). Twenty-two (63%) of these 35 cases were from primary lung neoplasms. Another nine lesions represented adrenal metastases from a variety of identified primary malignancies, including three esophageal neoplasms, two renal neoplasms, one sarcoma, one melanoma, one lymphoma, and one pancreatic neoplasm. Three more lesions represented metastases from unknown primary tumors. In the remaining case, review of the biopsy sample was consistent with a leiomyosarcoma; however, after surgical resection, this retroperitoneal metastatic deposit did not involve the adjacent normal adrenal gland tissue.
Fourteen of these 35 cases of adrenal metastases were preceded by adrenal-protocol CT or MRI that did not indicate a likely adenoma. Of the remaining 21 cases, only six having a size range of 1.9–6.6 cm were candidates for dedicated adrenal imaging on the basis of predominantly homogeneous enhancement at routine CT. In two of these six cases, adrenal-protocol CT was recommended but not performed. In another two of these six cases, positron emission tomography (PET) before biopsy revealed findings suspicious for probable adrenal metastases, and these patients were referred for adrenal biopsy. The remaining 15 metastatic masses showed heterogeneous enhancement, making an imaging-based diagnosis of an adenoma unlikely.
Overall, five of 35 metastatic adrenal masses were evaluated with PET before biopsy, with increased glycolytic activity consistent with metastasis in each case.
Benign adrenal tissue.—Of the 50 adrenal masses, only six (12%) were consistent with benign adrenal tissue after histopathology review. The mean mass size of these lesions was 3.3 cm (range, 2.2–4.9 cm). All six patients had a known extraadrenal primary malignancy, including three esophageal neoplasms and one each of breast, lung, and renal cell carcinoma.
Five of these six cases were preceded by dedicated adrenal-protocol CT (n = 4) or MRI (n = 1). Three masses were inconclusive for the presence of an adenoma, including two that were evaluated with adrenal-protocol CT, which was not diagnostic for an adenoma in either case. The first mass had an unenhanced attenuation value of 15 H and a percentage of enhancement washout of 52% (Fig. 1A, 1B). The second mass had an unenhanced attenuation value of 54 H; after contrast administration, the mass showed heterogeneous peripheral enhancement, precluding calculation of a percentage of enhancement washout value. The third mass, evaluated by chemical shift MRI, had imaging characteristics of a hemorrhagic mass lacking fat on in- and out-of-phase imaging. A fourth case, involving both left and right adrenal masses with calcifications in a patient with esophageal cancer, was evaluated on CT and showed unenhanced values of 4 and 11 H with percentage of enhancement washout values of 59% and 71%, respectively, which were supportive of the diagnosis of adenoma with areas of dystrophic calcification (Fig. 2A, 2B). PET evaluation of these masses showed subtle glycolytic activity, which was much less than the activity at the primary tumor site. The fifth case was evaluated on CT and reported as inconclusive for the presence of an adenoma on the basis of a percentage of enhancement washout value of 54%. In retrospect, the percentage of enhancement washout value was incorrectly calculated; had the calculation been performed correctly, a diagnosis of adenoma could have been made on the basis of a washout value of 63%. The sixth benign adrenal mass measured 3.5 cm and had a homogeneous appearance; although adrenal-protocol CT was recommended, the case was referred directly to biopsy.
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Three of the benign masses were stable on follow-up CT at 3, 16, and 23 months. One mass was confirmed to be benign after surgical resection. Two of the six patients with benign biopsy findings were lost to follow-up.
Adrenal cortical carcinoma.—Four primary adrenal cortical carcinomas having a mean mass size of 12.9 cm (range, 10–16 cm) were biopsied under sonographic guidance using a core biopsy technique. Two masses were positively identified as adrenal cortical carcinomas during histopathology review of the biopsy samples. Of these two masses, the diagnosis was later confirmed after surgical removal in one case; the second patient was not a surgical candidate. The two remaining masses had nonspecific pathology results, showing a poorly differentiated malignant neoplasm without features of lymphoma in one case and an extensively necrotic neoplasm suggestive of carcinoma in the other. These two masses were presumed to be adrenal cortical carcinomas on the basis of their location, centered in the adrenal bed, hypoattenuating centers, unilaterality, adjacent organ displacement or invasion, negative workup for an extraadrenal primary malignancy, and large size (14.5 and 16 cm). Both masses were deemed inoperable, and these patients were treated with palliative care only.
Pheochromocytoma.—Three of 50 adrenal masses were pheochromocytomas measuring 2.5, 3.5, and 7.0 cm (mean, 4.3 cm). Each of these was a unilateral, heterogeneous mass. The two smaller lesions were biopsied using CT guidance and the largest, using sonographic guidance, all as core biopsies. No immediate complications were associated with any of the biopsies.
All three pheochromocytomas were unsuspected clinically before biopsy because they occurred in patients with suspected extraadrenal sites of malignancy. One patient underwent an evaluation of urine catecholamine levels with normal results before biopsy at the recommendation of the radiologist. Before biopsy, this same patient also underwent adrenal-protocol CT that showed the mass to have an attenuation value of 28 H unenhanced and marked heterogeneity after the administration of contrast material, precluding the calculation of washout values. No further workup or treatment for pheochromocytoma was pursued at our institution in this patient.
The diagnosis of pheochromocytoma was confirmed in the remaining two patients by elevated levels of urine catecholamines drawn after the biopsy results were available and by surgical resection of the tumor in both patients.
Nondiagnostic biopsies.—The remaining two of 50 biopsy samples contained only benign-appearing nonadrenal skeletal muscle, nerve, and adipose tissue. Both biopsies, which were of left and right adrenal masses measuring 3.0 cm and 2.3 cm, respectively, were performed using CT guidance in patients with lung cancer. Neither of these masses underwent repeated biopsy; both patients were treated for presumed metastatic disease. One patient died with cerebral metastases and the other died with enlarging, bilateral adrenal metastases.
Adrenal Imaging
Overall, in 20 (40%) of 50 cases, dedicated adrenal CT (n = 19) or
MRI (n = 1) was performed before biopsy. In only one case was the
interpretation of the adrenal imaging potentially supportive of the diagnosis
of adenoma. These 20 studies included 14 cases of metastatic disease, five
cases of benign adrenal tissue, and one pheochromocytoma.
Thirty cases did not undergo dedicated adrenal imaging before biopsy. In 21 of these 30 cases, the masses showed primarily heterogeneous enhancement on routine CT, a finding inconsistent with a diagnosis of adenoma. In these cases, biopsy was required for further evaluation.
In the remaining nine of 30 cases without dedicated adrenal imaging, the masses showed predominantly homogeneous enhancement on routine CT and a dedicated adrenal study could have been considered before biopsy. These nine masses averaged 3.3 cm in size (range, 1.9–6.6 cm; median, 2.7 cm). A dedicated adrenal study had in fact been recommended in four of these nine masses (one case of adenoma, one nondiagnostic biopsy, and two cases of metastasis). Two of these nine masses were evaluated before biopsy with PET, which showed adrenal uptake consistent with metastases.
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Because of the high prevalence of adrenal adenomas, which are seen in as many as 5% of patients undergoing CT [1] and in 2–8% of autopsies [9], this entity is the primary differential diagnostic consideration for suspected adrenal metastatic disease. In prior published series of percutaneous adrenal biopsies, benign adrenal tissue, including adenomas, accounted for about half of the masses biopsied. In a series of 83 consecutive adrenal masses biopsied at our institution before the application of dedicated adrenal imaging protocols, 47 (57%) were consistent with benign adenomas [5]. In comparison, Silverman et al. [3] reported that 53 (52%) of 101 biopsies performed in known oncology patients and in patients with incidentally discovered adrenal masses were benign. Bernardino et al. [6] analyzed adrenal biopsies in 53 consecutive patients, including 39 known oncology patients, and found 28 benign masses (53%). Welch et al. [4] noted a slightly lower rate of benign biopsy findings of 40% (59/147 patients), although this group included only patients with a known diagnosis of lung cancer.
Previously reported dedicated adrenal CT and chemical shift MRI protocols to evaluate adrenal masses for characteristics specific to adrenal adenomas were in use at our institution during the time of this study. Such protocols have been shown to have a sensitivity and specificity of more than 95% and near 80%, respectively, for MRI [1], and 98% and 92%, respectively, for CT [7]. Application of these protocols before referral for percutaneous adrenal biopsy has significantly reduced the numbers of adrenal adenomas biopsied, thus obviating a needless procedure. Of 50 masses in this series, only six (12%) represented benign adrenal tissue. This rate compares favorably with that in a recently published large series of 225 patients with biopsy-proven extraadrenal malignancies [10] who underwent adrenal biopsy after an indeterminate result on unenhanced CT, dedicated adrenal CT, or in- and out-of-phase MRI. In that series, 41 biopsies (18%) were negative for metastases.
As with prior series, metastases to the adrenal gland were the most frequently identified adrenal mass at biopsy, with most of these from primary lung cancer. Five of 35 cases of proven adrenal metastases were also evaluated with PET before biopsy, with a concordant result. Although the role of PET in evaluating adrenal masses has not yet been established, several investigators suggest it may exhibit high sensitivity for identifying malignant masses [11–14].
Although adrenal adenomas are the most common primary adrenal neoplasm, up to 50% of adrenal cortical carcinomas may be nonfunctioning and present a radiologic and histopathologic appearance that is similar to the appearance of large, degenerated adrenal adenomas, which necessitates surgical resection for differentiation [15, 16]. Biopsy is considered relatively contraindicated in cases of potential adrenal cortical carcinoma because of the risk of seeding of the biopsy tract with tumor and difficulties in histopathologic differentiation between a degenerated adenoma and an adrenal cortical carcinoma [1]. Only one of four presumed adrenal cortical carcinomas in our study was surgically resected; the remaining three tumors were inoperable.
Functioning tumors of the adrenal gland, such as pheochromocytomas, do not require biopsy for diagnosis. In the case of pheochromocytoma, biopsy is actually contraindicated because manipulation of these tumors carries a risk of hemodynamic instability [17] by stimulating catecholamine secretion. Although the incidence of morbidity related to percutaneous biopsy of pheochromocytoma is not known, transient headache [18]; labile blood pressures [19, 20]; and abdominal pain, hemodynamic instability, and uncontrolled hemorrhage, leading to eventual death [21] have all been described. The relationship between the severity of the prebiopsy clinical manifestations of the tumor and the rate or severity of complications during or after biopsy is unknown; however, several case reports suggest that the surgical risk for patients with asymptomatic, incidentally discovered pheochromocytomas may be the same as for patients manifesting more severe symptoms [22, 23]. We are aware of only a single case report of a nonsecreting pheochromocytoma [24]. Each biopsy performed of a pheochromocytoma places the patient at risk for serious complications.
Because pheochromocytoma has no specific imaging features, the diagnosis is based on clinical suspicion with confirmatory testing via a 24-hr urine collection for catecholamines and their break-down products or serum catecholamines. Although pheochromocytoma classically presents with episodic hypertension, headache, and palpitations, 14% of patients with pheochromocytoma may present with atypical features [19]; in some cases the diagnosis may be unsuspected clinically. Although pheochromocytoma is a rare tumor found in fewer than 1% of hypertensive patients and in 0.13% of autopsies [25], a significant but widely varying reported percentage (5.5–80%) of documented pheochromocytomas may be clinically unsuspected before discovery [26]. Pheochromocytomas have also been reported in 3.4% of incidentally discovered adrenal masses [27].
The role of screening for a possible pheochromocytoma before biopsy is unclear. Such testing is costly, requires patient compliance in obtaining a 24-hr urine collection, and leads to a delay in diagnosis while awaiting results of tests that are often performed at infrequent intervals. Although in patients with clinically suspected pheochromocytomas the sensitivity of such testing may approach 100% [28], the yield in screening a population of patients referred for adrenal biopsy is unknown. Casola et al. [19] reported two of four cases of clinically unsuspected pheochromocytoma with normal catecholamine levels before biopsy. Similarly, we report one case of pheochromocytoma in which urine catecholamine levels obtained before biopsy were within the normal range.
Our preference is to screen for pheochromocytoma before adrenal biopsy in all patients with an adrenal mass to avoid possible adverse effects. At a minimum, we require screening in all patients whose clinical history suggests even the remote possibility of pheochromocytoma. Fortunately, all three cases of pheochromocytoma reported in our series remained clinically occult during and after biopsy; no complications were noted during resection in the two patients who proceeded to surgery.
Our rate of nondiagnostic biopsies was 4%. This rate compares favorably to reported rates in the literature, which are 6–17% [3–6]. Patients with a nondiagnostic biopsy result should have the biopsy repeated; in our study, although neither nondiagnostic biopsy was repeated at the referring clinician's discretion, both patients later showed evidence of progressive metastatic disease.
In conclusion, the introduction of dedicated adrenal imaging has markedly reduced the rate of biopsy of benign adrenal adenomas. Percutaneous imaging-guided biopsy of the adrenal gland remains useful in confirming the presence and nature of metastatic deposits to the adrenal gland, as well as diagnosing or excluding potential adrenal adenomas in patients in whom an adrenal imaging study does not suggest an adenoma.
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