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(Radiographics. 1999;19:949-963.)
© RSNA, 1999

SCIENTIFIC EXHIBIT

Imaging of Nontraumatic Hemorrhage of the Adrenal Gland1

Akira Kawashima, MD , Carl M. Sandler, MD , Randy D. Ernst, MD , Naoki Takahashi, MD , Marilyn A. Roubidoux, MD , Stanford M. Goldman, MD, Elliot K. Fishman, MD and N. Reed Dunnick, MD

1 From the Departments of Radiology (A.K., C.M.S., R.D.E., N.T., S.M.G.) and Urology (C.M.S., S.M.G.), University of Texas–Houston Medical School; the Department of Radiology, Lyndon B. Johnson General Hospital, 5656 Kelley St, Houston, TX 77026 (A.K., C.M.S., R.D.E.); the Department of Radiology, University of Michigan Medical Center, Ann Arbor (M.A.R., N.R.D.); and the Department of Radiology, Johns Hopkins Medical Institutions, Baltimore, Md (E.K.F.). Recipient of a Certificate of Merit award for a scientific exhibit at the 1997 RSNA scientific assembly. Received December 8, 1998; revision requested February 2, 1999, and received March 8; accepted March 11. Address reprint requests to A.K.


   Abstract
Top
 Abstract
INTRODUCTION
 IMAGING FEATURES OF NONTRAUMATIC...
 CAUSES OF NONTRAUMATIC ADRENAL...
 CONCLUSIONS
 References
 
Nontraumatic hemorrhage of the adrenal gland is uncommon. The causes of such hemorrhage can be classified into five categories: (a) stress, (b) hemorrhagic diathesis or coagulopathy, (c) neonatal stress, (d) underlying adrenal tumors, and (e) idiopathic disease. Computed tomography (CT), ultrasonography (US), and magnetic resonance (MR) imaging play an important role in diagnosis and management. CT is the modality of choice for evaluation of adrenal hemorrhage in a patient with a history of stress or a hemorrhagic diathesis or coagulopathy (anticoagulant therapy). CT may yield the first clue to the diagnosis of adrenal insufficiency secondary to bilateral massive adrenal hemorrhage; such insufficiency is rare but life threatening. US is the modality of choice for evaluation of neonatal hematoma, and MR imaging is helpful for further characterization. MR imaging is also useful in the diagnosis of coexistent renal vein thrombosis. When an adrenal abscess is suspected, percutaneous aspiration and drainage under imaging guidance should be performed. Hemorrhage into an adrenal cyst or tumor can cause acute onset of symptoms and signs in a patient without discernible risk factors for adrenal hemorrhage. A hemorrhagic adrenal tumor should be suspected when CT or MR imaging reveals a hemorrhagic adrenal mass of heterogeneous attenuation or signal intensity that demonstrates enhancement.

Index Terms: Adrenal gland, abnormalities, 86.18 • Adrenal gland, abscess, 86.211 • Adrenal gland, CT, 86.1211 • Adrenal gland, hemorrhage, 86.546 • Adrenal gland, insufficiency, 86.549 • Adrenal gland, MR, 86.1214 • Adrenal gland, neoplasms, 86.30 • Adrenal gland, US, 86.1298


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
IMAGING FEATURES OF NONTRAUMATIC...
 CAUSES OF NONTRAUMATIC ADRENAL...
 CONCLUSIONS
 References
 
Hemorrhage of the adrenal gland occurs secondary to both traumatic conditions and nontraumatic conditions (1,2). Nontraumatic adrenal hemorrhage is uncommon and may be associated with a variety of conditions (3). The clinical manifestations of nontraumatic adrenal hemorrhage are varied and probably depend on the amount of hemorrhage, its effect on hemodynamics, the rate of onset of the hemorrhage (sudden or gradual), the ability of the surrounding structures to contain the bleeding, the presence or absence of rupture of the hemorrhage into the perinephric space, and the functional status of the patient's hemostatic system. Patients may have sudden or gradual onset of upper abdominal, flank, or back pain and signs of massive blood loss.

The large majority of patients with adrenal hemorrhage do not have clinically obvious signs of adrenal insufficiency, and the diagnosis is usually made incidentally at imaging performed for another reason. Acute primary adrenal insufficiency associated with massive bilateral adrenal hemorrhage is rare but life threatening. In the critical care setting, the clinical manifestations of adrenal insufficiency are often nonspecific; coexistent disease and ongoing supportive therapy may mask its presence. Hemorrhage into an adrenal cyst or neoplasm may cause acute onset of symptoms and signs in a patient without discernible risk factors and necessitate radiologic evaluation.

Most articles on nontraumatic adrenal hemorrhage consist of a single case report or a small series of cases. In this article, we review the imaging features of nontraumatic adrenal hemorrhage and present a systematic review of its causes. These causes are classified into five categories: (a) stress, (b) hemorrhagic diathesis or coagulopathy, (c) neonatal stress, (d) underlying adrenal tumors, and (e) idiopathic disease (Table). The computed tomographic (CT), ultrasonographic (US), and magnetic resonance (MR) imaging features are shown on representative images.


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  		Causes of Nontraumatic Adrenal Hemorrhage
 

   IMAGING FEATURES OF NONTRAUMATIC ADRENAL HEMORRHAGE
Top
 Abstract
 INTRODUCTION
 IMAGING FEATURES OF NONTRAUMATIC...
CAUSES OF NONTRAUMATIC ADRENAL...
 CONCLUSIONS
 References
 
The appearance of an adrenal hematoma in a patient without an underlying adrenal condition depends on the age of the patient and the age of the hematoma (1).

Computed Tomography
Unilateral or bilateral adrenal hematomas can be demonstrated with CT. Nontraumatic hematomas characteristically appear round or oval, an appearance similar to that of traumatic hematomas. Stranding of the periadrenal fat is evident as well. Periadrenal hemorrhage with extension to the perinephric space may be seen.

The attenuation value of such a lesion depends on its age. Acute to subacute hematomas contain areas of high attenuation that usually range from 50 to 90 HU (1) and can be readily seen on nonenhanced CT scans obtained with narrow window settings. Adrenal hematomas decrease in size and attenuation over time, and most resolve completely. An adrenal hematoma may calcify after 1 year. An organized chronic hematoma appears as a mass with a hypoattenuating center with or without calcifications. Such masses are termed adrenal pseudocysts. The absence of enhancement allows confirmation of the cystic nature of the mass.

Ultrasonography
US is the modality of choice for initial and follow-up evaluation of a flank mass in a neonate for the following reasons: (a) the small patient size, (b) the relatively large size of the normal adrenal gland in this age group, and (c) the lack of ionizing radiation. In older children and adults, it is frequently a challenge to image a small suprarenal mass with US, particularly on the left side. In neonates, the normal adrenal glands are clearly visualized at US and consist of a hypoechoic cortex and a thin, echogenic medulla (4).

The pattern of echogenicity of an adrenal hematoma depends on its age (4,5). An early-stage hematoma appears solid with diffuse or inhomogeneous echogenicity. As liquefaction occurs, the mass demonstrates mixed echogenicity with a central hypoechoic region and eventually becomes completely anechoic and cystlike. Calcifications may be seen in the walls of the hematoma as early as 1–2 weeks after onset and gradually compact as the blood is absorbed. Color Doppler and power Doppler imaging allow confirmation of the avascular nature of the mass.

MR Imaging
An adrenal hematoma can be imaged and its age can be determined with MR imaging (6,7). In the acute stage (less than 7 days after onset), the hematoma typically appears isointense or slightly hypointense on T1-weighted images and markedly hypointense on T2-weighted images due to a high concentration of intracellular deoxyhemoglobin, which leads to preferential T2 proton relaxation enhancement.

In the subacute stage (7 days to 7 weeks after onset), the hematoma appears hyperintense on T1- and T2-weighted images. The T1 shortening is due to the paramagnetic effects of free methemoglobin (Fe3+), which is produced by the oxidation of hemoglobin (Fe2+) as the hematoma ages. The marked high signal intensity on T2-weighted images is due to the T1 shortening and the presence of serum. The high signal intensity appears at the periphery of the hematoma on T1-weighted images approximately 7 days after onset and fills in over several weeks. The hematoma may be multilocular, and each locule may have different signal intensity characteristics due to different degrees of oxidation. A fluid-fluid level may be present.

In the chronic stage (which typically begins 7 weeks after onset), a hypointense rim is present on T1- and T2-weighted images due to preferential T2 proton relaxation enhancement, which is attributed to hemosiderin deposition and the presence of a fibrous capsule. Calcifications are not evident on MR images. Gradient-echo imaging is helpful in demonstrating the "blooming" effect (magnetic susceptibility effect) that results from hemosiderin deposition. Larger hematomas usually exhibit slower clot evolution.

MR imaging is often used to determine whether blood is the sole component of the hematoma, a finding that most likely indicates a benign cause. Such evaluation is performed with a combination of T1-weighted, T2-weighted, and gadolinium chelate–enhanced images. The blooming effect has proved useful in identifying blood and in monitoring hemorrhage as it progresses from liquid methemoglobin to hemosiderin.

Other Imaging Studies
Radiography.—Suprarenal masses are rarely appreciable on plain radiographs unless curvilinear or eggshell calcifications are present. Ipsilateral atelectasis and small pleural effusions may be seen at the lung bases.

Excretory Urography.—A large adrenal hematoma appears as a relatively lucent suprarenal mass on nephrotomograms obtained during excretory urography. Urography is helpful in distinguishing an adrenal mass from the adjacent kidney, which may be displaced inferiorly.

Angiography.—Angiography is rarely used to evaluate an adrenal hematoma. Angiography can demonstrate the vascular supply of an adrenal mass and occasionally shows the contour of an adrenal cyst and hematoma or neovascularity in a tumor associated with a hematoma, but the findings are not diagnostic.

Nuclear Medicine.—An adrenal hematoma typically appears as a photopenic suprarenal mass with inferior displacement of the associated kidney on technetium-99m mercaptoacetyltriglycine, Tc-99m diethylenetriaminepentaacetic acid, and Tc-99m dimercaptosuccinic acid studies.

Percutaneous Needle Aspiration, Biopsy, and Drainage.—In most cases, the presence of the typical imaging features of hemorrhage obviates fine-needle aspiration. CT- or US-guided percutaneous aspiration and drainage are usually indicated when an adrenal abscess is suspected. When a hemorrhagic adrenal tumor is suspected at imaging, percutaneous needle biopsy may be performed. In cases of cystic pheochromocytoma, intracystic catecholamine values are elevated. However, needle biopsy should not be performed when a pheochromocytoma is clinically suspected because a hypertensive crisis may occur.

Does the Hemorrhage Truly Arise from the Adrenal Gland?
In some cases, it may be difficult to determine whether a hemorrhagic mass arises from the adrenal gland or from an adjacent organ such as the kidney, liver, or spleen. Periadrenal hemorrhage may be caused by extension of perinephric hemorrhage because the adrenal gland and kidney are both located within the renal fascia. Traditionally, excretory urography and selective angiography have been used for localization. The axial plane is the most familiar to radiologists and is often used in initial identification of an adrenal mass. When a right adrenal mass is large, the inferior vena cava is typically displaced anteriorly; the kidney is displaced inferiorly and deviates vertically. The use of multiple reformatted imaging planes generated from axial CT data is valuable in demonstrating the relationship of a hemorrhagic mass of adrenal origin to adjacent organs, particularly when contrast material–enhanced helical volumetric acquisition techniques are used. The direct multiplanar imaging capability of MR imaging and US is also useful for this purpose. Review of multiplanar images almost invariably improves our confidence in locating the organ of origin of a periadrenal hemorrhage.


   CAUSES OF NONTRAUMATIC ADRENAL HEMORRHAGE
Top
 Abstract
 INTRODUCTION
 IMAGING FEATURES OF NONTRAUMATIC...
 CAUSES OF NONTRAUMATIC ADRENAL...
CONCLUSIONS
 References
 
Stress
Adrenal hemorrhage is associated with stress caused by surgery, overwhelming sepsis, burns, or hypotension (3,8). Bilateral massive adrenal hemorrhage is particularly associated with a stressful critical illness. The risk of adrenal hemorrhage secondary to surgical stress is increased in patients who have received anticoagulant therapy (3). Adrenal hemorrhage is associated with fulminant meningococcemia (Waterhouse-Friderichsen syndrome), Pseudomonas infection, or infection with other gram-negative bacteria. A number of other stress-related predisposing factors have been associated with adrenal hemorrhage including pregnancy, cardiovascular disease, and administration of adrenocorticotropic hormone (9) or steroids (10).

The adrenal gland has a unique blood supply and is very vulnerable to hemorrhage. Fifty to sixty small adrenal branches from the three main adrenal arteries form a subcapsular plexus that drains into the medullary sinusoids. The gland is drained by relatively few venules. This pattern of blood supply has been described as a "vascular dam" (3). Stress increases endogenous secretion of adrenocorticotropic hormone severalfold; the result is a marked increase in adrenal vascularity (3). Increased vascularity in an intrinsically vulnerable network, together with elevation of the adrenal venous pressure from venoconstriction during shock, probably leads to intraglandular hemorrhage. Fulminant meningococcal or other septicemia and stress from an overwhelming infection or disseminated intravascular coagulopathy are additional causes of adrenal hemorrhage. In a pathologic study, adrenal vein thrombosis was found in 33 of 78 cases of adrenal hemorrhage and necrosis (11). It was suggested that the factors responsible for the initiation of thrombosis in the adrenal veins are catecholamines, thrombin, fibrin, and endotoxin (11).

Pain of varying severity localized to the abdomen, flank, lower chest, or back is often present. Pain in postoperative patients with adrenal hemorrhage may be incorrectly attributed to the surgery.

CT plays an important role in the evaluation of acute to subacute adrenal hemorrhage in critically ill patients (3,8). CT is a readily available and accurate method of evaluating the morphologic status of the adrenal glands. Typically, CT shows massive adrenal enlargement with areas of increased attenuation.

Hemorrhagic Diathesis or Coagulopathy
Nontraumatic adrenal hemorrhage is often associated with hemorrhagic diathesis or coagulopathy (Fig 1) (3,8,12–14). Adrenal hemorrhage and thrombosis can interact primarily or secondarily. The strong correlation of adrenal hemorrhage with anticoagulant therapy or other hemorrhagic diatheses suggests that hemorrhage may be a primary event and is not initiated by thrombosis. In a patient with thrombotic disease, adrenal vein thrombosis may occur first and subsequent anticoagulant therapy may precipitate hemorrhage. The central adrenal vein has a unique arrangement in that its musculature is eccentric and is composed of thick, longitudinal muscle bundles. Turbulence and local stasis may occur in this vein when the bundles contract; the result is venous thrombosis and hemorrhagic infarction (3). For instance, in a patient with a hypercoagulable state secondary to antiphospholipid syndrome, adrenal vein thrombosis is believed to be the cause of hemorrhagic infarction (14).



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  		Figure 1.  Adrenal hematoma in a 44-year-old man receiving coumarin for pulmonary emboli from deep venous thrombosis. Nonenhanced helical CT scan shows a large, hyperattenuating left adrenal mass, a finding consistent with acute hemorrhage.

 
Most cases of anticoagulant-associated adrenal hemorrhage occur during the first 3 weeks of treatment. Pain, fever, and hypotension in a patient with recurrent thromboembolic disease may be incorrectly attributed to another embolus (15).

As in stress-related adrenal hemorrhage, CT is usually indicated for evaluation and can demonstrate unilateral or bilateral hemorrhage.

Acute Primary Adrenal Insufficiency Secondary to Bilateral Adrenal Hemorrhage
Primary adrenal insufficiency manifests clinically when 90% or more of each gland is destroyed (16). Acute primary adrenal insufficiency (addisonian crisis) is most likely to result from bilateral adrenal hemorrhage. In the United States, bilateral adrenal hemorrhage is most frequently caused by stress secondary to surgery, sepsis, hypotension, or hemorrhagic diathesis (3). It is important to prevent such an acute adrenal crisis. Early treatment with replacement therapy should be instituted to prevent death from adrenal insufficiency.

The clinical findings are often nonspecific. Abdominal or back pain is common. Fever occurs in 70% of cases. Other signs and symptoms include hyperpyrexia, lethargy, nausea, and vomiting. Hypotension is not often seen before the onset of catastrophic hypotension and shock. The laboratory findings are also nonspecific. The most common laboratory abnormalities are hyponatremia, hyperkalemia, azotemia, and hypercalcemia, which are typically present in the chronic stage of adrenal insufficiency. Measurement of the serum cortisol level and an adrenal stimulation test are useful in assessing adrenal function; however, the usefulness of these tests in the critical care setting is often limited because they are not readily available.

CT is the modality of choice for evaluation of patients with acute onset of adrenal insufficiency because most such patients are critically ill or in hemodynamically unstable condition. Demonstration of bilateral adrenal enlargement with areas of increased attenuation at CT strongly suggests bilateral adrenal hemorrhage and may be the first clue to the diagnosis of acute adrenal insufficiency in an appropriate clinical setting.

Neonatal Stress
Adrenal hemorrhage is more common in neonates than in older children or adults and is the most common adrenal mass in neonates. Such hemorrhage sometimes occurs prenatally and may be the result of a difficult labor or delivery, particularly in infants of diabetic mothers or infants who are large for their gestational age. Adrenal hemorrhage may also result from asphyxia, hypoxia, septicemia, or hemorrhagic disorders (eg, disseminated intravascular coagulopathy, hypoprothrombinemia) (4,17). Neonatal adrenal hemorrhage may be discovered incidentally during US performed for other reasons. The disorder is more frequent on the right side (70% of cases), a phenomenon that has been attributed to compression of the adrenal gland between the liver and kidney. Adrenal hemorrhage has been reported in 4% of infants with severe respiratory failure who are undergoing extracorporeal membrane oxygenation (18). Such hemorrhage has also occurred during the routine performance of third-trimester obstetric US (19,20). The cause of fetal adrenal bleeding is not clear.

At birth, the adrenal gland is quite large and weighs 5–10 g because of fetal embryogenesis and homeostasis (the normal adult adrenal gland weighs about 5 g) (21). The adrenal gland is susceptible to hemorrhage at birth as the result of regression of the fetal cortex, which occurs rapidly during the first 6 weeks of life (22). The vascular channels in the primitive cortex become markedly engorged and more susceptible to hemorrhage. In addition to the superior, middle, and inferior adrenal arteries, an adrenal arterial supply arising from the gonadal arteries has been reported in 60% of fetal adrenal vascular dissections (23). Hemorrhagic necrosis within the hyperemic fetal cortex after birth is considered to result in the development of gross hemorrhage (4).

If the hemorrhage is significant, a palpable flank mass, anemia, prolonged jaundice, and hypovolemic shock due to blood loss may occur. A scrotal hematoma is an unusual clinical manifestation (24). Adrenal insufficiency is rare in neonates.

US is the examination of choice in neonates with suspected adrenal hematoma. Initial US typically reveals a complex, echogenic mass (Fig 2) (4,5). If the mass is large, the kidney may be displaced inferiorly. Regression of the mass over a period of weeks is shown on serial US scans (25). MR imaging reveals a mass with the signal intensity characteristics of hemorrhage (Fig 3). Other characteristic radiologic findings include rimlike calcification, whereas stippled calcifications are typical of neuroblastoma. Adrenal hemorrhage may be localized with visualization of the normal gland adjacent to the focal hemorrhage or may primarily involve the medulla (5).



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  		Figure 2.  Adrenal hematoma in a 3-day-old boy. Transverse US scan shows a complex right suprarenal mass. The differential diagnosis of the US findings includes cystic neuroblastoma. MR images (not shown) demonstrated the signal intensity characteristics of a subacute hematoma.

 


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  		Figure 3a.  Adrenal hematoma in a 3-day-old girl with an abdominal mass. (a, b) Coronal T1-weighted spin-echo MR image (repetition time msec/echo time msec = 500/11) (a) and axial T2-weighted fast spin-echo MR image (3,000/108, echo train length of eight) (b) show a 3 x 4-cm suprarenal mass. The mass is isointense on the T1-weighted image (a) and hypointense on the T2-weighted image (b) with a hyperintense rim, findings consistent with acute to subacute hemorrhage. (c) Coronal T1-weighted spin-echo MR image (550/26) obtained 19 days later shows a decrease in the size of the mass, which is now hyperintense. The mass was also hyperintense on the T2-weighted image (not shown), findings consistent with the evolution of hemorrhage.

 


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  		Figure 3b.  Adrenal hematoma in a 3-day-old girl with an abdominal mass. (a, b) Coronal T1-weighted spin-echo MR image (repetition time msec/echo time msec = 500/11) (a) and axial T2-weighted fast spin-echo MR image (3,000/108, echo train length of eight) (b) show a 3 x 4-cm suprarenal mass. The mass is isointense on the T1-weighted image (a) and hypointense on the T2-weighted image (b) with a hyperintense rim, findings consistent with acute to subacute hemorrhage. (c) Coronal T1-weighted spin-echo MR image (550/26) obtained 19 days later shows a decrease in the size of the mass, which is now hyperintense. The mass was also hyperintense on the T2-weighted image (not shown), findings consistent with the evolution of hemorrhage.

 


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  		Figure 3c.  Adrenal hematoma in a 3-day-old girl with an abdominal mass. (a, b) Coronal T1-weighted spin-echo MR image (repetition time msec/echo time msec = 500/11) (a) and axial T2-weighted fast spin-echo MR image (3,000/108, echo train length of eight) (b) show a 3 x 4-cm suprarenal mass. The mass is isointense on the T1-weighted image (a) and hypointense on the T2-weighted image (b) with a hyperintense rim, findings consistent with acute to subacute hemorrhage. (c) Coronal T1-weighted spin-echo MR image (550/26) obtained 19 days later shows a decrease in the size of the mass, which is now hyperintense. The mass was also hyperintense on the T2-weighted image (not shown), findings consistent with the evolution of hemorrhage.

 
A case of cystic neuroblastoma in a neonate has been reported (26). In most cases, hemorrhage can be distinguished from neuroblastoma on the basis of clinical, laboratory, and radiologic findings and surgery can be avoided (17). Follow-up at intervals of several weeks for 2–3 months can be performed to document the evolution of the clot. Measurement of the 24-hour urinary excretion of vanillylmandelic acid is also relevant because an increased level of vanillylmandelic acid is virtually diagnostic of neuroblastoma (27).

Simultaneous Adrenal Hemorrhage and Renal Vein Thrombosis.—Renal vein thrombosis in neonates is associated with adrenal hemorrhage. The presence of hematuria and azotemia suggests a diagnosis of coexistent renal vein thrombosis. The renal vein thrombosis often leads to progressive renal atrophy.

The excretory urographic findings in renal vein thrombosis range from nonvisualization of the affected kidney to a completely normal appearance. Nephromegaly is generally demonstrated. Tc-99m mercaptoacetyltriglycine or Tc-99m diethylenetriaminepentaacetic acid scans may reveal absent or diminished blood flow to the involved kidney with decreased function (Fig 4). US may show renal enlargement with loss of corticomedullary differentiation and accompanying focal or generalized areas of increased echogenicity and hyperechoic radial streaks (28). Extension of the thrombus into the inferior vena cava may be present. MR imaging shows high signal intensity with both T1- and T2-weighted pulse sequences (Fig 4) (29).



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  		Figure 4a.  Simultaneous adrenal hemorrhage and renal vein thrombosis in a 6-day-old girl with hyperbilirubinemia and hypertension whose mother had diabetes mellitus (class B). Bedside US scans (not shown) demonstrated a complex right suprarenal mass, a finding consistent with adrenal hemorrhage. (a) Tc-99m mercaptoacetyltriglycine scan (posterior view) shows a suprarenal area of decreased activity (arrow), a finding consistent with adrenal hemorrhage. There is only faint uptake in the right kidney. The left kidney (LK) is normal. (b) Coronal T2-weighted fast spin-echo MR image (2,200/112, echo train length of eight) shows a hyperintense mass of the right adrenal gland, a finding consistent with subacute hemorrhage. Note the high signal intensity of the right kidney, a finding consistent with acute and subacute hemorrhage. The right adrenal mass was hyperintense and the right kidney was isointense on a T1-weighted spin-echo MR image (500/14) (not shown).

 


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  		Figure 4b.  Simultaneous adrenal hemorrhage and renal vein thrombosis in a 6-day-old girl with hyperbilirubinemia and hypertension whose mother had diabetes mellitus (class B). Bedside US scans (not shown) demonstrated a complex right suprarenal mass, a finding consistent with adrenal hemorrhage. (a) Tc-99m mercaptoacetyltriglycine scan (posterior view) shows a suprarenal area of decreased activity (arrow), a finding consistent with adrenal hemorrhage. There is only faint uptake in the right kidney. The left kidney (LK) is normal. (b) Coronal T2-weighted fast spin-echo MR image (2,200/112, echo train length of eight) shows a hyperintense mass of the right adrenal gland, a finding consistent with subacute hemorrhage. Note the high signal intensity of the right kidney, a finding consistent with acute and subacute hemorrhage. The right adrenal mass was hyperintense and the right kidney was isointense on a T1-weighted spin-echo MR image (500/14) (not shown).

 
Neonatal Adrenal Abscess.—Microscopic abscesses of the adrenal glands are not uncommon; however, an adrenal abscess that produces a focal mass is rare in the neonate. Most such abscesses have been found in neonates with preexisting adrenal hemorrhage, in which case hematogenous bacterial seeding results in abscess formation (30). In some cases, adrenal abscesses may also be caused by seeding of a normal adrenal gland. The seeding may be secondary to neonatal septicemia or maternal infection. Infecting organisms include Neisseria meningitidis, Escherichia coli, and group B hemolytic streptococci.

US is useful in defining the morphology of the complex cystic suprarenal mass. A central fluid-debris level that changes with position may be present. CT typically shows a thick-walled cystic mass in the gland that is better defined after intravenous administration of contrast material. MR imaging reveals a complex cystic mass of the adrenal gland. The expected signal intensity characteristics of hemorrhage may not be present in an infected hematoma. In the clinical setting of persistent fever, septicemia, and failure to respond to antibiotic therapy, as well as failure of an adrenal hematoma to resolve at serial imaging, imaging-guided percutaneous needle aspiration and drainage of the cystic adrenal mass is necessary for diagnosis and treatment.

Underlying Adrenal Tumors
In a patient without discernible risk factors who has nontraumatic unilateral or bilateral adrenal hematoma, careful imaging analysis is necessary to identify an underlying adrenal cyst or neoplasm as the cause of the hemorrhage. A primary adrenal cyst or tumor was reported to be the fourth most common cause of spontaneous retroperitoneal hemorrhage after renal cell carcinoma, angiomyolipoma, and renal artery aneurysm by Swift et al (31). Patients with a large adrenal mass such as a cyst (32,33) or myelolipoma (34) are susceptible to intracystic or intratumoral hemorrhage after blunt or deceleration injuries.

In patients without discernible risk factors, it is necessary to determine whether the lesion is a bland nontraumatic adrenal hemorrhage rather than a neoplastic process complicated by hemorrhage. CT performed with and without intravenous contrast material is of value in distinguishing an uncomplicated hematoma from an underlying neoplastic process of the adrenal gland. MR imaging is also useful in determining whether blood is the sole component (a finding that indicates a benign cause) by means of T1- and T2-weighted pulse sequences and in assessing the presence or absence of enhancement after administration of gadolinium contrast material. Serial imaging can document the evolution of the clot. Percutaneous biopsy or surgery may still be required for definitive diagnosis.

Pseudocysts.—The cause of adrenal pseudocysts is not clear, but they are considered to result from prior hemorrhage and subsequent clot organization within a normal adrenal gland. Pseudocysts represent the common variety of adrenal cysts that are discovered clinically (35–38). Pseudocysts may be found incidentally during a nonurinary imaging work-up but may also cause acute symptoms with intracystic bleeding. US reveals a complex cystic suprarenal mass (Fig 5) (39,40). A fluid-fluid level may be present; the dependent layer is echogenic and changes with position (40). The typical CT findings in acute to subacute hemorrhagic adrenal cysts include a well-defined suprarenal cyst containing an area of high attenuation (Fig 5). Clot in a hemorrhagic cyst may also appear as a solid component in the cystic mass, thus mimicking cystic pheochromocytoma, cystic degeneration of a metastasis, or adrenocortical carcinoma (Fig 5) (41). Interval change in the size and appearance of a solid component at serial imaging suggests the presence of a clot. Thickening of the cyst wall may be reactive. In time, pseudocysts may appear as homogeneous, thin-walled fluid collections. In one study, a calcified wall was present in 56% of pseudocysts (42). Intravenous contrast material may be required to exclude a solid component at CT and MR imaging. Distinction of a hemorrhagic cyst from a hemorrhagic tumor may still be difficult, particularly when stippled central or thick peripheral calcification or a thick (>5 mm) or irregular wall is present.



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  		Figure 5a.  Proved hemorrhagic pseudocyst in a 21-year-old woman who experienced blunt trauma 6 months earlier. (a) Excretory urogram shows inferior displacement of the right kidney. (b) Longitudinal US scan of the right kidney shows a complex, echogenic suprarenal mass. (c) Nonenhanced CT scan shows a right suprarenal mass containing a rounded area of increased attenuation (curved arrow). The intracystic clot mimics a mural nodule in a cystic tumor. A fluid-fluid level in the mass (straight arrow) is indicative of hemorrhage in the lesion.

 


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  		Figure 5b.  Proved hemorrhagic pseudocyst in a 21-year-old woman who experienced blunt trauma 6 months earlier. (a) Excretory urogram shows inferior displacement of the right kidney. (b) Longitudinal US scan of the right kidney shows a complex, echogenic suprarenal mass. (c) Nonenhanced CT scan shows a right suprarenal mass containing a rounded area of increased attenuation (curved arrow). The intracystic clot mimics a mural nodule in a cystic tumor. A fluid-fluid level in the mass (straight arrow) is indicative of hemorrhage in the lesion.

 


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  		Figure 5c.  Proved hemorrhagic pseudocyst in a 21-year-old woman who experienced blunt trauma 6 months earlier. (a) Excretory urogram shows inferior displacement of the right kidney. (b) Longitudinal US scan of the right kidney shows a complex, echogenic suprarenal mass. (c) Nonenhanced CT scan shows a right suprarenal mass containing a rounded area of increased attenuation (curved arrow). The intracystic clot mimics a mural nodule in a cystic tumor. A fluid-fluid level in the mass (straight arrow) is indicative of hemorrhage in the lesion.

 
Benign Neoplasms.—Myelolipomas are usually unilateral masses composed of benign mature fat and bone marrow (43,44). When the tumor has bled, CT reveals nonenhancing areas with high to low attenuation, depending on the age of the blood (Fig 6). Demonstration of a fatty component (-30 to -115 HU) in a hemorrhagic adrenal mass at CT is virtually diagnostic of underlying myelolipoma (45). Histologic analysis demonstrates calcifications from previous hemorrhage in up to 20% of cases. The fatty component of the myelolipoma can be accurately identified with MR imaging. In equivocal cases, a definitive diagnosis can be made with CT-guided needle biopsy to confirm the presence of mature adipose tissue and normal hematopoietic tissue.



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  		Figure 6.  Nontraumatic bleeding from a myelolipoma in a 65-year-old man. Enhanced CT scan shows a large mass (M) that contains areas of fat. Acute hemorrhage is present in and around the mass.

 
Adrenal hemangiomas are rare, benign, stromal tumors of the adrenal gland and are usually larger than 10 cm in diameter (46,47). When these tumors bleed, CT reveals nonenhancing areas with high to low attenuation, depending on the age of the blood. A hemangioma is typically markedly hyperintense on T2-weighted MR images but often appears as a complex mass due to variable degrees of hemorrhage, thrombosis, necrosis, and fibrosis (Fig 7). After bolus administration of intravenous contrast material, CT and MR imaging may show multiple peripheral nodular areas of marked enhancement. However, a complete filling-in phenomenon, which is frequently described in cavernous hemangioma of the liver, rarely occurs in adrenal hemangioma (Fig 7). Calcifications from previous hemorrhage are present at CT in 28%–87% of cases (48).



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  		Figure 7a.  Proved cavernous hemangioma in a 69-year-old man. (a) Enhanced helical CT scan obtained during the corticomedullary junction phase shows a left adrenal mass with peripheral nodular enhancement. (b) Delayed CT scan shows heterogeneous enhancement. (c) Axial T1-weighted spin-echo MR image (500/20) shows a right adrenal mass with a small, rounded area of high signal intensity (arrow), a finding consistent with subacute hemorrhage. (d) Axial T2-weighted spin-echo MR image (1,820/70) shows a heterogeneously hyperintense mass with a smaller focal area of low signal intensity (arrow). Note the large area of mixed low and high signal intensity within the mass laterally, a finding consistent with chronic hemorrhage. (Figs 7a-7d courtesy of Kotaro Yasumori, MD, and Toru Muranaka, MD, National Kyushu Medical Center Hospital, Fukuoka, Japan.)

 


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  		Figure 7b.  Proved cavernous hemangioma in a 69-year-old man. (a) Enhanced helical CT scan obtained during the corticomedullary junction phase shows a left adrenal mass with peripheral nodular enhancement. (b) Delayed CT scan shows heterogeneous enhancement. (c) Axial T1-weighted spin-echo MR image (500/20) shows a right adrenal mass with a small, rounded area of high signal intensity (arrow), a finding consistent with subacute hemorrhage. (d) Axial T2-weighted spin-echo MR image (1,820/70) shows a heterogeneously hyperintense mass with a smaller focal area of low signal intensity (arrow). Note the large area of mixed low and high signal intensity within the mass laterally, a finding consistent with chronic hemorrhage. (Figs 7a-7d courtesy of Kotaro Yasumori, MD, and Toru Muranaka, MD, National Kyushu Medical Center Hospital, Fukuoka, Japan.)

 


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  		Figure 7c.  Proved cavernous hemangioma in a 69-year-old man. (a) Enhanced helical CT scan obtained during the corticomedullary junction phase shows a left adrenal mass with peripheral nodular enhancement. (b) Delayed CT scan shows heterogeneous enhancement. (c) Axial T1-weighted spin-echo MR image (500/20) shows a right adrenal mass with a small, rounded area of high signal intensity (arrow), a finding consistent with subacute hemorrhage. (d) Axial T2-weighted spin-echo MR image (1,820/70) shows a heterogeneously hyperintense mass with a smaller focal area of low signal intensity (arrow). Note the large area of mixed low and high signal intensity within the mass laterally, a finding consistent with chronic hemorrhage. (Figs 7a-7d courtesy of Kotaro Yasumori, MD, and Toru Muranaka, MD, National Kyushu Medical Center Hospital, Fukuoka, Japan.)

 


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  		Figure 7d.  Proved cavernous hemangioma in a 69-year-old man. (a) Enhanced helical CT scan obtained during the corticomedullary junction phase shows a left adrenal mass with peripheral nodular enhancement. (b) Delayed CT scan shows heterogeneous enhancement. (c) Axial T1-weighted spin-echo MR image (500/20) shows a right adrenal mass with a small, rounded area of high signal intensity (arrow), a finding consistent with subacute hemorrhage. (d) Axial T2-weighted spin-echo MR image (1,820/70) shows a heterogeneously hyperintense mass with a smaller focal area of low signal intensity (arrow). Note the large area of mixed low and high signal intensity within the mass laterally, a finding consistent with chronic hemorrhage. (Figs 7a-7d courtesy of Kotaro Yasumori, MD, and Toru Muranaka, MD, National Kyushu Medical Center Hospital, Fukuoka, Japan.)

 
Pheochromocytoma is the most common cause of massive bleeding from a primary adrenal tumor. In the past, massive adrenal hemorrhage secondary to a previously undiagnosed pheochromocytoma was lethal in 50% of cases (49,50). CT frequently reveals areas of decreased attenuation due to hemorrhage, necrosis, liquefaction, cyst formation, and fibrous encapsulation (Fig 8). Cystic pheochromocytomas are thought to result from intratumoral hemorrhage with subsequent liquefaction and fibrous capsule formation (51,52). Pheochromocytomas characteristically appear markedly hyperintense on T2-weighted MR images but often contain areas of hemorrhage and cystic components (Fig 8). In a recent study, six of 17 pheochromocytomas (35%) contained areas of decreased signal intensity on T2-weighted MR images (53). Dynamic enhanced CT and MR imaging typically reveal marked enhancement.



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  		Figure 8a.  Proved pheochromocytoma in a 37-year-old man with von Hippel-Lindau disease. (a) Enhanced CT scan shows a right adrenal mass. Note the area of low attenuation (arrow). (b) Axial T2-weighted spin-echo MR image (3,000/80) shows a hyperintense mass with an area of low signal intensity (arrow). This finding and demonstration of the blooming effect on a gradient-echo MR image (not shown) were consistent with hemosiderin.

 


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  		Figure 8b.  Proved pheochromocytoma in a 37-year-old man with von Hippel-Lindau disease. (a) Enhanced CT scan shows a right adrenal mass. Note the area of low attenuation (arrow). (b) Axial T2-weighted spin-echo MR image (3,000/80) shows a hyperintense mass with an area of low signal intensity (arrow). This finding and demonstration of the blooming effect on a gradient-echo MR image (not shown) were consistent with hemosiderin.

 
Although a cortical adenoma is the most common neoplasm of the adrenal gland, massive hemorrhage from an adenoma is extremely rare (Fig 9) (54–57). Unlike in primary carcinoma, foci of hemorrhage and necrosis are rare in adenoma, probably due to its hypovascular nature.



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  		Figure 9.  Proved adrenal adenoma with intratumoral hemorrhage in a 48-year-old woman. CT scan obtained after excretory urography shows a large cystic mass with a fluid-fluid level within it. Note the flecks of calcification in the wall (arrow).

 
Malignant Neoplasms.—Adrenocortical carcinomas are usually large (>6 cm in diameter) and highly aggressive with local invasion and distant metastasis. They contain areas of hemorrhage and necrosis in variable degrees at histologic analysis (58–60). Calcification may be present. Intratumoral hemorrhage is typically central. CT reveals a hemorrhagic adrenal mass of heterogeneous attenuation with or without retroperitoneal hemorrhage. In a review of eight cases of adrenocortical carcinoma studied with MR imaging, intratumoral hemorrhage was evident in seven (60). Peripheral nodular enhancement was also present in seven of these eight cases (60).

Hemorrhagic adrenal metastasis is rare, although adrenal metastases are common (61–63). Patients with hemorrhagic adrenal metastases are usually symptomatic and typically experience acute onset of pain. Massive adrenal hemorrhage can be the initial clinical manifestation of a metastatic tumor. Bronchogenic carcinoma is the most common cause of hemorrhagic adrenal metastases. CT and MR imaging typically reveal unilateral or bilateral suprarenal masses of inhomogeneous attenuation and signal intensity, respectively (Fig 10). Solid components will enhance after administration of intravenous contrast material. Extensive periadrenal and perinephric changes may obliterate the contour of the involved adrenal gland (Fig 10). Intratumoral hemorrhage may occur in a patient with metastatic melanoma. CT-guided biopsy of the adrenal mass may be necessary to establish the diagnosis.



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  		Figure 10a.  Hemorrhagic adrenal metastasis in a 60-year-old woman with acute onset of right flank pain and hemoptysis. (a) Nonenhanced helical CT scan through the right suprarenal region shows a large mass of mixed increased and decreased attenuation with high-attenuation stranding around the mass, findings consistent with hemorrhage. (b) Sagittally reformatted image generated from enhanced helical CT data shows the relationship of the right adrenal mass (M) to the right kidney and liver. Note the extension of the hemorrhage to the perinephric space around the upper pole of the right kidney. Chest radiographs and CT scans (not shown) revealed a lobulated mass in the right upper lobe of the lung. Percutaneous needle biopsy of the right adrenal mass yielded undifferentiated adenocarcinoma.

 


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  		Figure 10b.  Hemorrhagic adrenal metastasis in a 60-year-old woman with acute onset of right flank pain and hemoptysis. (a) Nonenhanced helical CT scan through the right suprarenal region shows a large mass of mixed increased and decreased attenuation with high-attenuation stranding around the mass, findings consistent with hemorrhage. (b) Sagittally reformatted image generated from enhanced helical CT data shows the relationship of the right adrenal mass (M) to the right kidney and liver. Note the extension of the hemorrhage to the perinephric space around the upper pole of the right kidney. Chest radiographs and CT scans (not shown) revealed a lobulated mass in the right upper lobe of the lung. Percutaneous needle biopsy of the right adrenal mass yielded undifferentiated adenocarcinoma.

 
Differential Diagnosis.—The differential diagnosis of juxtaadrenal masses that cause hemorrhage includes renal or renal capsular neoplasms (eg, angiomyolipoma, renal cell carcinoma, Wilms tumor, lymphoma, sarcoma, metastases) and juxtaadrenal retroperitoneal neoplasms (eg, neurogenic tumor, sarcoma, metastases). Use of multiple imaging planes can help identify a mass of adrenal or juxtaadrenal origin. The differential diagnosis of suprarenal fat-containing masses includes angiomyolipoma and liposarcoma. Angiomyolipomas of the kidney are usually larger than 4 cm in diameter when they bleed. A small liposarcoma in the suprarenal region could mimic an adrenal myelolipoma.

Idiopathic Disease
Hemorrhage of the adrenal gland without any apparent predisposing factors is termed idiopathic hemorrhage. Such cases are usually discovered at surgery or autopsy (57).


   CONCLUSIONS
Top
 Abstract
 INTRODUCTION
 IMAGING FEATURES OF NONTRAUMATIC...
 CAUSES OF NONTRAUMATIC ADRENAL...
 CONCLUSIONS
References
 
Causes of nontraumatic adrenal hemorrhage can be classified into five categories: (a) stress, (b) hemorrhagic diathesis or coagulopathy, (c) neonatal stress, (d) underlying adrenal tumors, and (e) idiopathic disease. CT, US, and MR imaging play an important role in diagnosis and management. The imaging appearance of an adrenal hematoma depends on the age of the patient, the patient's clinical condition, the presence of underlying adrenal lesions, and the age of the hematoma. Understanding the clinical and imaging features of nontraumatic adrenal hemorrhage is important for correct diagnosis and appropriate management.


   Footnotes
 
CME FEATURE This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician's Recognition Award. To obtain credit, see the questionnaire on pp 1029–1036.

LEARNING OBJECTIVES After reading this article and taking the test, the reader will: • Be familiar with the causes of nontraumatic adrenal hemorrhage. • Be able to identify the CT, US, and MR imaging features of nontraumatic adrenal hemorrhage. • Be able to integrate the imaging features of nontraumatic adrenal hemorrhage.


   References
Top
 Abstract
 INTRODUCTION
 IMAGING FEATURES OF NONTRAUMATIC...
 CAUSES OF NONTRAUMATIC ADRENAL...
 CONCLUSIONS
 References
 

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