23210583

RADIOLOGY-PICTORIAL ESSAY

Bilateral adrenal lesions

Pankaj Gupta, Ashu Bhalla and Raju Sharma

Department of Radiodiagnosis, All India Institute of Medical Sciences, New Delhi, India

P Gupta MBBS; A Bhalla MD; R Sharma MD.

Correspondence

Dr Ashu Bhalla, Department of Radiodiagnosis, All India Institute of Medical Sciences, Flat no. 714, Sector 29, NOIDA, Gautam Budh Nagar 201303, India. Email: ashubhalla1@yahoo.com

Conflict of interest: None delclared.

Submitted 22 October 2011; accepted 4 January 2012.

10.1111/j.1754-9485.2012.02435.x

Summary

Bilateral adrenal lesions include a spectrum of disorders: neoplastic disorders (metastases, lymphoma, bilateral phaeochromocytoma, adrenocortical carci- noma and myelolipoma); longstanding congenital adrenal hyperplasia and macronodular adrenal hyperplasia; infections such as tuberculosis, histoplas- mosis and blastomycosis; adrenal haemorrhage; adrenals in hypoperfusion complex and paediatric masses. Bilateral distribution in addition to other imaging characteristics can help narrow differential diagnoses in case of adrenal masses. We present a pictorial review highlighting the adrenal lesions that can present bilaterally.

Key words: adrenal masses; adrenal neoplasms; bilateral adrenal lesions.

Introduction

Adrenal masses are common and found in 9% of the population.1 Imaging characteristics that help in differ- ential diagnosis of adrenal lesions include size, attenua- tion, washout values, presence of calcification, fat or haemorrhage and unilateral versus bilateral distribution. Though the imaging differentiation of adrenal masses into benign and malignant rests to a large extent on the attenuation values of the lesion in pre-contrast study, other imaging features that help to narrow the differen- tial diagnosis include dynamics of contrast uptake and washout characteristics and unilateral versus bilateral distribution; unilateral versus bilateral distribution also helps to narrow the differential diagnosis of adrenal masses as there are a few lesions that present bilater- ally. This pictorial review shows a spectrum of bilateral adrenal lesions.

Normal adrenals

The adrenals are small, glandular organs situated in close proximity to the kidneys. Each gland is located medial to the upper pole of the associated kidney. The right adrenal gland has a linear or V shape, whereas the left adrenal gland is V- or Y-shaped. The limbs of each adrenal gland are 2-5 cm long and 6-10 mm thick.2

The normal adult adrenal glands are difficult to visu- alise with ultrasound. However, they are almost always visualised in newborns.3,4 This is attributed to physiolo-

gical hypertrophy at this stage of life. In adults, the right adrenal gland is regularly visible using optimised exami- nation techniques. The left adrenal gland is visualised in about 40-50% of cases only.5

The adrenals are routinely visualised on all computed tomography (CT) and magnetic resonance imaging (MRI) examinations of the abdomen.

Bilateral adrenal masses

The differential diagnosis of bilateral adrenal masses (Table 1) include neoplastic disorders - metastases, lymphoma, bilateral phaeochromocytoma, adrenocorti- cal carcinoma, myelolipoma; longstanding congenital adrenal hyperplasia and macronodular adrenal hyperpla- sia; infections such as tuberculosis, histoplasmosis and blastomycosis; and adrenal haemorrhage.

Adrenal neoplasms

Adrenal metastases

Adrenal glands are a common site of metastases from lung, breast, gastric, renal, pancreatic and colon carcinomas; melanomas and malignant lymphomas, usually non-Hodgkin’s lymphomas. About 90% of adrenal metastases are carcinoma; the rest are sarcoma or melanoma.5 Adrenal metastases occur in 20-45% of cancer patients.6 They occur in less than 10% of lung cancer patients at the time of presentation.7 Overall,

Table 1. Bilateral adrenal lesions

Neoplasms

Malignant

Metastases

Lymphoma Phaechromocytoma

Adrenocortical carcinoma Neuroblastoma

Ganglioblastoma

Benign Adenoma

Congenital adrenal hyperplasia Macronodular adrenal hyperplasia

Infections

Tuberculous Histoplasmosis

Blastomycosis

Parasitic cysts

Trauma

Adrenal haemorrhage

Pseudocyst

Hypoperfusion complex

Autoimmune

Addison disease

Miscellaneous Rosai-Dorfmann disease

adrenal metastases are bilateral in 49% cases, occurring more commonly on the left side.5 However, metastases of lung cancer are mostly solitary, unilateral, small asymptomatic lesions. Bilateral metastases are observed in less than 3% of patients with lung cancer (Fig. 1a,b).

On contrast-enhanced computed tomography (CECT), the peak contrast enhancement is variable. Adrenal metastases show slow washout (absolute and relative percentage washout, absolute percentage washout (APW) and relative percentage washout (RPW) values of less than 60% and 40%, respectively) as compared with adenomas.8 Hypervascular metastases, in particular metastases from renal cell carcinoma and melanoma, enhance similar to phaeochromocytoma. On MRI metas- tases exhibit low signal intensity on T1-weighted images and high-signal intensity on T2-weighted images, with progressive enhancement on administration of contrast. There is lack of signal drop on out-of-phase images in contrast to adenomas.9

Adrenal lymphoma

Primary adrenal lymphoma is rare. More commonly, adrenals are secondarily involved. Non-Hodgkin lym- phoma is the most common type with reported incidence of adrenal involvement of 4%.10 Bilateral involvement occurs in 50% of these cases. CECT shows discrete masses of variable attenuation or infiltrative ill-defined masses (Fig. 2a,b). Lymphoma is characterised by low- signal intensity on T1-weighted images and heterogene- ous high-signal intensity on T2-weighted images, with minimal progressive enhancement.

Phaeochromocytoma

Phaeochromocytomas are typically unilateral; bilateral lesions occur in 10% cases. Bilateral disease is more likely

Fig. 1. (a,b) CECT chest in mediastinal window at the level of aortic arch shows a homogeneous low attenuation mass in the anterior and mediastinum with marked compression of the superior vena cava. A small right pleural effusion is also noted. This patient had small cell bronchogenic carcinoma with bulky mediastinal lymphadenopathy. CECT abdomen of the same patient at the level of adrenals shows bilateral large heterogeneous adrenal masses (arrows). Bilateral adrenal metastases are relatively rare in the setting of lung cancer. CECT, contrast-enhanced computed tomography.

(a)

(b)

Fig. 2. (a,b) CECT chest in mediastinal window shows heterogeneous mass in the anterior mediastinum on both sides of midline displacing the mediastinum vessels posteriorly suggesting a diagnosis of lymphoma that was confirmed by the biopsy of this mass. Axial CECT of the abdomen reveals large relatively symmetric large bilateral adrenal masses (arrows) that suggest a secondary adrenal lymphoma. CECT, contrast-enhanced computed tomography.

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to occur in the setting of various syndromes including multiple endocrine neoplasia type 2, Von Hippel-Lindau disease, neurofibromatosis type 1, tuberous sclerosis and Sturge-Weber syndrome. They are significantly larger than adenomas. These functioning tumours secrete catecholamines and manifest as hypertension

and palpitations. On CECT, they appear as homogenous masses (if small) or heterogeneous lesions (larger lesions) (Figs 3,4). Pre-contrast attenuation may be similar to that of adenomas as they can contain abundant fat and show areas of cystic degeneration.11 Phaeochro- mocytoma is typically described as brightly enhancing but

Fig. 3. (a,b) Sequential coronal reformations of CECT abdomen show asymmetrical bilateral adrenal masses. The larger left adrenal mass has low attenuation centre suggestive of necrosis (arrow). Enlarged lymph nodes are noted at the left renal hilum. In Figure 2a, a note is also made of multiple focal liver lesions. A few of these lesions are calcified. This was a patient of multiple endocrine neoplasia type 2a (MEN 2a) with medullary carcinoma of thyroid, bilateral phaeochromocytomas and liver metastases. CECT, contrast-enhanced computed tomography; MEN, multiple endocrine neoplasia.

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Fig. 4. (a,b) T1- and T2-weighted axial MRI of abdomen of a young male patient with recent onset palpitations and hypertension reveals bilateral suprarenal masses. The masses are hypointense on T1-weighted image (arrows), and there is an area of hyperintensity in the centre of the left adrenal mass. These are hyperintense on T2-weighted image with a focus of hypointensity (arrow) corresponding to the hyperintense focus on T1-weighted image. This suggests haemorrhage within left adrenal mass. MRI, magnetic resonance imaging.

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10

can show a range of CT appearances. Washout characteristics are variable, and in conjunction with marked peak enhancement, phaeochromocytomas may mimic adenoma (APW > 60%, RPW > 40%).12,13 The MRI appearance of a phaeochromocytoma is typically described as T2 hyperintense; however, not all phaeo- chromocytomas have this imaging feature (Fig. 5a,b).

Adrenal carcinoma

Adrenal carcinoma is a rare neoplasm arising from the adrenal cortex and is bilateral in 10% cases.14 Almost half are functioning tumours and usually manifest with Cushing syndrome. Adrenal carcinomas are large at presentation, with size ranging from 4 to 10 cm.

Fig. 5. (a,b) CECT and T2-weighted MRI of a middle-aged male presenting with recent onset hypertension and paroxysmal headache. CECT reveals heterogeneous bilateral adrenal masses (arrows). T2-weighted MRI reveals heterogeneous hyperintense masses with focal areas of fluid signal intensity (arrows) suggestive of cystic degeneration of phaeochromocytoma. CECT, contrast-enhanced computed tomography; MRI, magnetic resonance imaging.

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Heterogeneity with central necrosis is common, and calcification is noted in 30% of cases. On contrast admin- istration, they show heterogeneous enhancement with a peripheral rim enhancement noted in some cases. They show slow washout (APW and RPW of less than 60% and 40%, respectively).

Adrenal myelolipoma

Myelolipomas are rare benign tumours composed of myeloid, erythroid and fatty elements. They are esti- mated to occur in 0.2-0.4% of the population based on autopsy series. The imaging appearance of myelolipo- mas is based on the fat content of the lesion (Fig. 6a,b). They appear echogenic at ultrasound, low attenuation at CT and hyperintense on T1-weighted in-phase MRIs. Myelolipomas may occasionally be associated with endocrine dysfunction - Cushing syndrome, Conn’s syn- drome, Nelson syndrome, 17-hydroxylase deficiency and 21-hydroxylase deficiency. The imaging appearance of isolated myelolipomas and those occurring in conjunc- tion with other pathologic lesion is considerably different. Isolated lesions have an average size of 10 cm, fat content between 50% and 90%, calcification in 24% and a pseudocapsule in 75% lesions. Myelolipomas that occur in conjunction with other pathologic conditions are smaller (mean, 7 cm) with less fat (most frequently <10%), a higher frequency of calcification (52%) and lower prevalence of a pseudocapsule.15

Adrenal cortical hyperplasia

Adrenal cortical hyperplasia is often seen in patients with Cushing syndrome, which is the result of hyper-

production of adrenocorticotropic hormone. It may be diffuse or nodular and is typically bilateral. Diffuse cor- tical hyperplasia is seen in 45% of patients with Cushing syndrome, whereas nodular cortical hyperplasia is seen in only 3% of these patients. The signal intensity of hyperplastic adrenal glands is usually similar to that of the normal adrenal gland.16

Congenital adrenal hyperplasia (CAH)

CAH refers to a group of inherited disorders of adrenal steroidogenesis. The common functional defect is impaired cortisol secretion, resulting in hypersecretion of corticotropin-releasing hormone and adreno- corticotropic hormone and consequent hyperplasia of the adrenal glands. About 90% cases of CAH are caused by a defect in the enzyme 21-hydroxylase. Clinically, patients with CAH can present as classic salt-losing (most severe), classic non-salt-losing (simple-virilising) or non-classic (mild or late-onset) form. In untreated cases, a variety of morphologic changes can occur in adrenals including symmetrical enlargement, macronodules and rarely adenoma and carcinoma (Fig. 7a-c).

Infections

Tuberculosis, histoplasmosis and blastomycosis can affect the adrenals. These infections result in bilateral enlargement of the adrenals (Fig. 8a). With long- standing infection, the glands may atrophy and calcify.17 Extensive involvement of the adrenals by these

Fig. 6. (a,b) Axial CECT images of the abdomen show bilateral well-defined fat attenuating lesions with a larger right adrenal lesion and small left adrenal lesion (arrows). The diagnosis of adrenal myelolipoma is relatively straightforward with the imaging demonstration of fat within the lesion. CECT, contrast-enhanced computed tomography.

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Fig. 7. (a-c) Axial sections of the adrenal CT protocol reveal nodular enlargement of bilateral adrenals (arrows). T1-weighted axial MRI of abdomen of a patient with ambiguous genitals reveals bilateral adrenal hyperplasia (arrows). The shape of adrenal limbs is preserved. T1-weighted axial MRI of the pelvis reveals cliteromegaly (arrow). In untreated cases of CAH, adrenals can show a variety of morphologic changes including symmetrical enlargement, macronodules and rarely adenoma and carcinoma. CAH, congenital adrenal hyperplasia; CT, computed tomography; MRI, magnetic resonance imaging.

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infections may result in adrenal insufficiency (Fig. 8b). In fact, tuberculosis is the most common cause of Addison disease worldwide.18

Adrenal haemorrhage

Trauma accounts for 80% cases of adrenal haemorrhage (Fig. 9a). Other causes include systemic anticoagula- tion therapy, sepsis or stress such as surgery. Bilateral haemorrhage occurs in 20% cases. Adrenal haemor- rhage is an unusual cause of adrenal insufficiency. Acute adrenal haemorrhage is hyperdense at CT. Chronic

adrenal haemorrhage has typical MRI appearance with hyperintensity on T1-weighted images and a dark rim along the periphery on T2-weighted images.

Neonatal adrenal haemorrhage is a relatively uncom- mon clinical problem. It is noted in approximately 3% of infants screened by ultrasonography (Fig. 9b).19 The aetiology of adrenal haemorrhage is unclear. Asso- ciations include traumatic delivery, hypoxia, shock, septicaemia and bleeding diathesis.

Other masses that can present bilaterally include adrenal cysts of varying aetiology, adenomas and Rosai- Dorfmann disease (Fig. 10).

Fig. 8. (a,b) Coronal reformatted CT (Fig. 8a) shows bilateral symmetrical heterogeneous adrenal masses (arrows), which on histopathological examination were confirmed to be bilateral adrenal histoplasmosis. Figure 8b shows bilateral atrophic adrenals with chunky calcification in this patient with features of adrenal insufficiency. In the course of adrenal granulomatous infections, the glands are initially enlarged and with progressive disease undergo atrophy and calcification. CT, computed tomography.

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Paediatric adrenal bilateral neoplasms

Bilateral neuroblastoma

Bilateral lesions are rare in neuroblastoma and occur in less than 10% cases.2º Bilateral adrenal neuroblastoma

have been described in up to 20% of patients with familial neuroblastoma.21 Most of the patients with bilat- eral neuroblastomas are less than 6 months of age. The incidence of Stage 4S is higher in bilateral neuroblas- toma than among unilateral tumours. At ultrasonogra- phy, neuroblastoma appears as a hetero-echoic mass.

Fig. 9. (a,b) Axial CECT abdomen (Fig. 9a) shows bilateral hypodense adrenal masses with subtle hyperdensities within (arrow on left). There are associated liver laceration (arrow on right) and hyperdense collection in the posterior perihepatic space. Trauma is the most common cause of adrenal haemorrhage. Axial ultrasound scan (Fig. 9b) shows heterogeneous masses in the location of bilateral adrenals (arrows), which represented bilateral adrenal haemorrhage in this neonate who presented with septicaemia. CECT, contrast-enhanced computed tomography.

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Fig. 10. Axial CECT of abdomen at the level of adrenals of this patient under follow-up for Rosai-Dorfman disease shows bilateral enlarged adrenal glands (arrows). The mediastinal window of axial CECT chest (not shown here) revealed mediastinal lymphadenopathy, which is the hallmark of this disease. CECT, contrast-enhanced computed tomography.

At CT, neuroblastoma appears as either a homogeneous or heterogeneous soft tissue mass. Heterogeneity is caused by haemorrhage, necrosis and/or calcification. Coarse, finely stippled or curvilinear calcifications are seen in 85% of the abdominal neuroblastomas. 22

Ganglioneuroblastoma

These tumours have a less malignant potential as com- pared with neuroblastoma. Therefore, they tend to be smaller and well defined at presentation. They demon- strate intermediate signal intensity on T1-weighted images and heterogeneously high-signal intensity on T2-weighted images. They enhance heterogeneously following contrast administration.

Bilateral adrenal lesions other than masses

Adrenals in hypoperfusion complex

Although not enlarged, an interesting bilateral appear- ance of adrenals is noted in hypoperfusion states. Adrenals show bilaterally symmetrical intense enhance- ment with attenuation values similar to or greater than those of inferior vena cava (IVC) (Fig. 11a). This along with flat IVC gives a clue to the diagnosis (Fig. 11b). It represents a sympathetic response to shock and preservation of perfusion to adrenals that are vital organs.23

Autoimmune Addison disease

Adrenal insufficiency of autoimmune origin is the most common cause of Addison disease in developed coun- tries. On imaging, both the adrenals are markedly atrophic (Fig. 12a,b).

Fig. 11. (a,b) Sequential axial images of CECT abdomen show the findings in hypovolemic shock. Findings noted are flat IVC (arrow, a), ascites and marked enhancement of both adrenal glands (arrow, b) comparable with that of IVC. CECT, contrast-enhanced computed tomography; IVC, inferior vena cava.

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(b)

Fig. 12. (a,b) Autoimmune Addison disease presents as markedly atrophic bilateral adrenals without calcification. Axial NCCT and CECT images of 45-year-old male show markedly atrophic adrenals (arrows). Lack of calcification helps differentiate from atrophy secondary to chronic granulomatous infection. CECT, contrast- enhanced computed tomography; NCCT, non-contrast computed tomography. Table 2. Approach to bilateral adrenal masses. CAH, congenital adrenal hyperplasia; NCCT H.U., non-contrast computed tomography, Hounsefield Unit Approach to bilateral adrenal masses

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Bilateral adrenal masses

Focal

Diffuse

Solid

Cystic

Fat

Hyperplastic

Atrophic

containing

History, age, hypertension

Epithelial

Hemorrhage

Parasitic

Pseudocyst

Myelolipoma

CAH

Nodular adrenal hyperplasia

Autoimmune Addison disease

NCCT H.U. washout dynamics calcification

Metastases

Lymphoma

Phaechromocytoma

Childhood tumor Neuroblastoma Ganglioneuroblastoma

Granulomatous infection TB/histoplasmosis

Conclusion

Bilateral adrenal lesions when encountered are often explained in the context of clinical picture and primary disorders such as metastases, lymphoma, hyperplasia, haemorrhage and myelolipoma have fairly characteristic imaging appearances.

Some lesions may be difficult to differentiate such as adrenal carcinoma versus neuroblastoma versus lym- phoma in children. Although accompanying liver lesions may be seen in all three, splenic lesions and lymphad- enopathy favour lymphoma over adrenal carcinoma and neuroblastoma (Table 2).

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