(Radiographics. 1999;19:989-1008.)
© RSNA, 1999
From the Archives of the AFIP1
Adrenocortical Neoplasms in Children: Radiologic-Pathologic Correlation
Geoffrey A. Agrons, MD,
Gael J. Lonergan, Lt Col, USAF, MC,
Glenn E. Dickey, Lt Col, USAF, MC and
Juan E. Perez-Monte, MD
1 From the Departments of Radiology, Pennsylvania Hospital, 800 Spruce St, Philadelphia, PA, 19107 (G.A.A., J.E.P-M.); Radiologic Pathology (G.J.L.) and Pediatric Pathology (G.E.D.), Armed Forces Institute of Pathology, Washington, DC; Radiology, Children's Hospital of Philadelphia (G.A.A.), Penn; and Radiology and Nuclear Medicine, Uniformed Services University of the Health Sciences, Bethesda, Md (G.J.L.). Received February 4, 1999; revision requested March 3 and received April 14; accepted April 15. Address reprint requests to G.A.A.
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Abstract
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Primary neoplasms of the adrenal cortex are rare in children and differ significantly in epidemiology, clinical characteristics, and biologic features from their counterparts in adults. In children, the inclusive term adrenocortical neoplasm is applied because adrenal adenoma and adrenal carcinoma may be difficult to distinguish histopathologically. Pediatric adrenocortical neoplasms typically occur before 5 years of age, affect young girls more commonly than boys, and are associated with hemihypertrophy and Beckwith-Wiedemann and Li-Fraumeni syndromes. Most children with an adrenocortical neoplasm present with signs and symptoms of endocrine abnormality, including virilization and Cushing syndrome. Cross-sectional imaging studies typically demonstrate a large, circumscribed, predominantly solid suprarenal mass with variable heterogeneity due to hemorrhage and necrosis. Calcification is not uncommon. Local invasion and metastases to the lungs, liver, and regional lymph nodes may be present at diagnosis. When friable tumor thrombus extends into the inferior vena cava, it poses a high risk of pulmonary embolization. The finding of increased retroperitoneal fat due to hypercortisolism on computed tomographic and magnetic resonance images of children with an adrenal mass favors the diagnosis of adrenocortical neoplasm. Surgical resection is the mainstay of therapy, with chemotherapy used for patients with metastases or persistent elevated hormone levels following surgery. Patients younger than 5 years with aggressive adrenocortical neoplasms fare better than older children.
Index Terms: Adrenal gland, neoplasms, 862.30 • Children, genitourinary system, 862.30 • Infants, genitourinary system, 862.30 • Neoplasms, in infants and children, 862.30
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INTRODUCTION
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Neoplasms of the adrenal cortex are rare in childhood. Unlike similar tumors in adults, adrenal adenomas in children have no histopathologic features that allow them to be reliably distinguished from carcinomas. In addition, the biologic behavior of pediatric adrenocortical neoplasms may be difficult to predict on the basis of morphologic criteria. Thus, the term adrenocortical neoplasm is currently used to designate both benign and malignant tumors of the adrenal cortex in children. Adrenocortical neoplasms of childhood, particularly those occurring in infants, merit separate discussion from their counterparts in adults because they have distinctive epidemiologic and clinical features (1).
Each year, an estimated 25 adrenocortical neoplasms occur in patients younger than 20 years of age, representing an annual incidence rate of three per million (2). Of adrenal tumors in children, adrenocortical neoplasms are far less common than neuroblastomas but more common than pheochromocytomas (3). Despite their relative rarity, adrenocortical neoplasms represent the most common tumor of the pediatric adrenal cortex (4,5).
The hormonal activity of childhood adrenal neoplasms has been recognized since 1948, when Wilkins (6) reported an unusual case of an estrogen-secreting adrenal tumor that caused gynecomastia in a 6-month-old-boy. It is now recognized that most children with an adrenocortical neoplasm show clinical evidence of an endocrine abnormality, in contrast to the behavior of adrenocortical tumors in adults (1). Thus, diagnostic imaging of adrenocortical neoplasms in children is typically guided by clinical presentation; similar tumors in asymptomatic adults are discovered incidentally during cross-sectional imaging studies performed for unrelated indications (7).
This article, illustrated with cases contained in the radiologic pathology archives of the Armed Forces Institute of Pathology, examines the clinical, pathologic, and radiologic features of adrenocortical neoplasms in children and discusses differential diagnosis, treatment, and prognosis.
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CLINICAL FEATURES
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Most adrenocortical neoplasms occur in children with no underlying disorder. However, in some cases, these tumors are associated with other syndromes. In 1967, an association between adrenocortical neoplasms and congenital hemihypertrophy was established by Fraumeni and Miller (8), who reviewed the charts of 62 pediatric patients with adrenocortical neoplasms. Of these patients, two (3%) had hemihypertrophy. The adrenal tumors did not always lateralize to the enlarged side of the body. Children with Beckwith-Wiedemann syndrome (sometimes referred to as EMG [exomphalos-macroglossia-gigantism] syndrome) have an increased risk of benign and malignant tumors of multiple organs (8,9), and the most common neoplasm associated with this syndrome is nephroblastoma (Wilms tumor), followed by adrenocortical carcinoma and hepatoblastoma (1). Beckwith-Wiedemann syndrome is also commonly accompanied by nonneoplastic enlargement of the adrenal glands caused by cortical hyperplasia. In addition, fetal adrenocortical cells are characteristically enlarged in patients with Beckwith-Wiedemann syndrome. This condition, called bilateral adrenal cytomegaly, has been associated with congenital metastasizing adrenocortical carcinoma in one case report (10). The Li-Fraumeni syndrome, also known as the SBLA (sarcoma; breast and brain tumors; leukemia, laryngeal carcinoma, and lung cancer; and adrenocortical carcinoma) syndrome, represents a familial aggregation of neoplasms that includes adrenocortical carcinoma (11,12). Patients with this syndrome may have alterations in the p53 tumor suppressor gene located on the short arm of chromosome 17, band 13 (13, 14). Finally, in rare cases, adrenocortical neoplasms have been reported in association with congenital urinary tract abnormalities such as duplication of the collecting system, tumors such as ganglioneuroma and ganglioneuroblastoma, and congenital adrenal hyperplasia (1,15–19).
In a study of 32 pediatric patients with adrenocortical neoplasms, the age at diagnosis ranged from 6 months to 19 years (mean age, 8 years; median age, 5 years), with a predominant number of patients being 5 years of age and younger (20). In another study of 42 patients with adrenocortical neoplasms, two-thirds were younger than 5 years of age (21). In addition, rare examples of congenital adrenocortical neoplasms have been reported (22–26). In an analysis of 40 Brazilian children, in whom adrenocortical tumors are more common than in United States children (27), the median age at diagnosis was 3.9 years and over half were girls (28. A female-to-male ratio of 2.2 to 1 was noted in a recent literature review (29).
The primary tumor may not be apparent at physical examination. In a retrospective review by Teinturier and colleagues (30), a palpable mass was found in only 57% of 45 children with adrenocortical neoplasms. However, unlike adult patients with tumors of the adrenal cortex, most children with an adrenocortical neoplasm present with signs or symptoms of endocrine abnormality. In a review of over 200 tumors in children by Neblett et al (29), only 17 nonfunctioning adrenocortical neoplasms were identified.
Precocious puberty refers to secondary sex characteristics that appear earlier than 8 years of age in girls and before 9 years in boys. Precocious puberty may be gonadotropin-dependent (true precocious puberty) or gonadotropin-independent (pseudoprecocious puberty). Furthermore, precocious puberty may be characterized as isosexual when secondary sex characteristics are appropriate for the patient's gender or heterosexual when they are inappropriate. Heterosexual precocious puberty manifests as virilization in girls and feminization in boys. Because functioning adrenocortical neoplasms represent a gonadotropin-independent source of endogenous androgens and cortisol, they usually produce pseudoprecocious puberty, Cushing syndrome, or a mixture of the two (Fig 1).
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Figure 1a. Mixed endocrine syndrome in a 7-month-old boy with an adrenocortical neoplasm. (a) Photograph of the patient at 4 months shows normal facies. (b) Photograph of the same patient at 7 months demonstrates moon facies, acne, and bitemporal excess hair growth. Penile enlargement and premature pubic hair growth were also present.
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Figure 1b. Mixed endocrine syndrome in a 7-month-old boy with an adrenocortical neoplasm. (a) Photograph of the patient at 4 months shows normal facies. (b) Photograph of the same patient at 7 months demonstrates moon facies, acne, and bitemporal excess hair growth. Penile enlargement and premature pubic hair growth were also present.
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Young girls with an adrenocortical neoplasm most commonly come to clinical attention because of virilization and less frequently present with a mixed endocrine syndrome composed of cushingoid features and virilization. Virilization manifests as abnormal size and strength due to increased muscle mass (herculean habitus), clitoromegaly (Fig 2), facial hair (Fig 3), advanced pubic and axillary hair development, and advanced bone age. Overproduction of androgen by adrenocortical tumor causes isosexual pseudoprecocious puberty in boys, evidenced by the early development of acne, pubic hair, and penile enlargement (Fig 4). Pure Cushing syndrome, feminization in boys caused by secretion of estrogen, or hypertension due to primary hyperaldosteronism (Conn syndrome) are unusual (1,31,32). Infants with Cushing syndrome tend to have generalized obesity, rather than the truncal distribution of increased fat found in adults (33).
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Figures 2, 3. (2) Virilization in a 3-year-old girl with an adrenocortical tumor. Clinical photograph of the external genitalia shows clitoromegaly and early pubic hair growth. (3) Adrenocortical neoplasm in a 16-year-old girl with amenorrhea and hirsutism. (a) Clinical photograph shows facial and chest hair and absence of breast development. (b) Axial contrast material-enhanced computed tomographic (CT) scan of the abdomen demonstrates a heterogeneous left flank mass containing a large focus of low attenuation (arrowhead), consistent with necrosis. Retroperitoneal adenopathy (arrow) partly encases the abdominal aorta.
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Figures 2, 3. (2) Virilization in a 3-year-old girl with an adrenocortical tumor. Clinical photograph of the external genitalia shows clitoromegaly and early pubic hair growth. (3) Adrenocortical neoplasm in a 16-year-old girl with amenorrhea and hirsutism. (a) Clinical photograph shows facial and chest hair and absence of breast development. (b) Axial contrast material-enhanced computed tomographic (CT) scan of the abdomen demonstrates a heterogeneous left flank mass containing a large focus of low attenuation (arrowhead), consistent with necrosis. Retroperitoneal adenopathy (arrow) partly encases the abdominal aorta.
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Figures 2, 3. (2) Virilization in a 3-year-old girl with an adrenocortical tumor. Clinical photograph of the external genitalia shows clitoromegaly and early pubic hair growth. (3) Adrenocortical neoplasm in a 16-year-old girl with amenorrhea and hirsutism. (a) Clinical photograph shows facial and chest hair and absence of breast development. (b) Axial contrast material-enhanced computed tomographic (CT) scan of the abdomen demonstrates a heterogeneous left flank mass containing a large focus of low attenuation (arrowhead), consistent with necrosis. Retroperitoneal adenopathy (arrow) partly encases the abdominal aorta.
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Figure 4a. Adrenocortical neoplasm in a 3-year-old boy with a 2-year history of pubic hair growth, penile enlargement, deepening voice, and acne. (a) Frontal photograph of the patient demonstrates precocious development of secondary sexual characteristics, evidenced by penile enlargement, pubic hair, and increased muscle mass. (b) Photograph of the patient's back shows extensive acne. (c) Frontal radiograph of the left hand demonstrates accelerated skeletal maturation (estimated at 12 years). (d) Transverse abdominal sonogram shows a heterogeneous retrohepatic mass (arrow). (e) Contrast-enhanced CT scan reveals the slightly ill-defined heterogeneous right suprarenal mass.
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Figure 4b. Adrenocortical neoplasm in a 3-year-old boy with a 2-year history of pubic hair growth, penile enlargement, deepening voice, and acne. (a) Frontal photograph of the patient demonstrates precocious development of secondary sexual characteristics, evidenced by penile enlargement, pubic hair, and increased muscle mass. (b) Photograph of the patient's back shows extensive acne. (c) Frontal radiograph of the left hand demonstrates accelerated skeletal maturation (estimated at 12 years). (d) Transverse abdominal sonogram shows a heterogeneous retrohepatic mass (arrow). (e) Contrast-enhanced CT scan reveals the slightly ill-defined heterogeneous right suprarenal mass.
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Figure 4c. Adrenocortical neoplasm in a 3-year-old boy with a 2-year history of pubic hair growth, penile enlargement, deepening voice, and acne. (a) Frontal photograph of the patient demonstrates precocious development of secondary sexual characteristics, evidenced by penile enlargement, pubic hair, and increased muscle mass. (b) Photograph of the patient's back shows extensive acne. (c) Frontal radiograph of the left hand demonstrates accelerated skeletal maturation (estimated at 12 years). (d) Transverse abdominal sonogram shows a heterogeneous retrohepatic mass (arrow). (e) Contrast-enhanced CT scan reveals the slightly ill-defined heterogeneous right suprarenal mass.
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Figure 4d. Adrenocortical neoplasm in a 3-year-old boy with a 2-year history of pubic hair growth, penile enlargement, deepening voice, and acne. (a) Frontal photograph of the patient demonstrates precocious development of secondary sexual characteristics, evidenced by penile enlargement, pubic hair, and increased muscle mass. (b) Photograph of the patient's back shows extensive acne. (c) Frontal radiograph of the left hand demonstrates accelerated skeletal maturation (estimated at 12 years). (d) Transverse abdominal sonogram shows a heterogeneous retrohepatic mass (arrow). (e) Contrast-enhanced CT scan reveals the slightly ill-defined heterogeneous right suprarenal mass.
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Figure 4e. Adrenocortical neoplasm in a 3-year-old boy with a 2-year history of pubic hair growth, penile enlargement, deepening voice, and acne. (a) Frontal photograph of the patient demonstrates precocious development of secondary sexual characteristics, evidenced by penile enlargement, pubic hair, and increased muscle mass. (b) Photograph of the patient's back shows extensive acne. (c) Frontal radiograph of the left hand demonstrates accelerated skeletal maturation (estimated at 12 years). (d) Transverse abdominal sonogram shows a heterogeneous retrohepatic mass (arrow). (e) Contrast-enhanced CT scan reveals the slightly ill-defined heterogeneous right suprarenal mass.
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Laboratory abnormalities in children with functioning adrenocortical neoplasms include an increase in 24-hour urinary ketosteroid excretion and increased levels of serum cortisol, testosterone, androstenedione, and estradiol (5).
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PATHOLOGIC FEATURES
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Microscopic Features
Adrenocortical adenomas comprise a heterogeneous group of benign neoplasms that histologically resemble the appearance of the normal zona fasciculata, the zona glomerulosa, or most often, a combination of both. Cells are typically arranged in nests separated by a delicate fibrovascular stroma. Cytologic features vary from large, pale vacuolated cells with vesicular nuclei characteristic of the zona fasciculata to smaller cells with eosinophilic cytoplasm and condensed chromatin similar to those in the zona glomerulosa and zona reticularis (Fig 5).
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Figure 5a. Pathologic features of adrenocortical neoplasm. (a) Photomicrograph (original magnification, x300; hematoxylin-eosin [H-E] stain) shows large, pale vacuolated cells (arrow) and smaller cells (arrowhead) with eosinophilic cytoplasm, representing benign features. (b) Photomicrograph (original magnification, x300; H-E stain) of a malignant adrenocortical neoplasm shows nuclear atypia, pleomorphism, multinucleated forms (straight arrow), and atypical mitoses (curved arrow). (c) Photograph of sectioned surgical specimen of an adrenocortical carcinoma demonstrates a nodular appearance, extensive hemorrhage, and necrosis. Scale is in inches.
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Figure 5b. Pathologic features of adrenocortical neoplasm. (a) Photomicrograph (original magnification, x300; hematoxylin-eosin [H-E] stain) shows large, pale vacuolated cells (arrow) and smaller cells (arrowhead) with eosinophilic cytoplasm, representing benign features. (b) Photomicrograph (original magnification, x300; H-E stain) of a malignant adrenocortical neoplasm shows nuclear atypia, pleomorphism, multinucleated forms (straight arrow), and atypical mitoses (curved arrow). (c) Photograph of sectioned surgical specimen of an adrenocortical carcinoma demonstrates a nodular appearance, extensive hemorrhage, and necrosis. Scale is in inches.
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Figure 5c. Pathologic features of adrenocortical neoplasm. (a) Photomicrograph (original magnification, x300; hematoxylin-eosin [H-E] stain) shows large, pale vacuolated cells (arrow) and smaller cells (arrowhead) with eosinophilic cytoplasm, representing benign features. (b) Photomicrograph (original magnification, x300; H-E stain) of a malignant adrenocortical neoplasm shows nuclear atypia, pleomorphism, multinucleated forms (straight arrow), and atypical mitoses (curved arrow). (c) Photograph of sectioned surgical specimen of an adrenocortical carcinoma demonstrates a nodular appearance, extensive hemorrhage, and necrosis. Scale is in inches.
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In general, adrenocortical adenomas are bland with low nuclear-to-cytoplasmic ratio, very little necrosis or hemorrhage, and absent or exceptionally rare mitoses or bizarre nuclear forms. In children, however, benign adrenocortical tumors are more likely to display marked nuclear atypia, pleomorphism, necrosis, and mitotic activity than similar tumors in adult patients. Occasionally, central degenerative changes, including necrosis, hemorrhage, cystic alteration, and vascular proliferation, may be seen in adenomas, particularly as a complication of thrombosis following adrenal venography (34). Despite some association of cell types with secretory products, it is not possible to reliably predict endocrine function (eg, hyperaldosteronism, hypercortisolism, virilization) on the basis of histologic characteristics.
Adrenocortical carcinomas show a wide range of differentiation on histologic examination, not only between different tumors but within the same tumor. Morphology ranges from normal-appearing adrenal cells to completely undifferentiated cells. Broad fibrous bands often separate the tumor into multiple nodules. Most cells are lipid-poor and eosinophilic, and they may be arranged in nests, trabeculae, or sheets. Hyperchromatic nuclei, pleomorphism with bizarre giant cells and multinucleated forms, necrosis (especially confluent areas), mitotic activity (including atypical mitoses), and vascular or capsular invasion may be seen (Fig 5). However, none of these histologic features is necessarily diagnostic of malignancy in children (see adenoma vs carcinoma) (2,35).
Gross Features
In a clinicopathologic study of 30 patients with adrenocortical neoplasms by Lack et al (2), 60% of lesions arose in the right adrenal gland, and no patients had bilateral involvement. Ectopic adrenocortical tumors are exceedingly rare (36).
Adenomas are typically spherical, unilateral and solitary, and well-demarcated but often unencapsulated, and they weigh less than 50 g. Adenomas range in color from yellow to reddish-brown and may appear black if the tumor contains a large amount of the piment lipofuscin (34,37–39).
Carcinomas are usually over 100 g (although smaller weights have been reported) with coarse trabeculations, multinodular contour, and yellow to brown color. Areas of hemorrhage and necrosis are frequently seen (Fig 5) (38,40). In adrenocortical neoplasms of childhood, malignant behavior is usually associated with lesions that weigh more than 500 g, whereas most tumors that weigh less than 500 g are benign (35). Cystic change may be seen in both adenomas and carcinomas, but it is more common in carcinomas and larger adenomas.
Adenoma versus Carcinoma
An attempt to clarify the pathologic distinction between adrenocortical adenomas and carcinomas has been made in at least several studies reviewing adrenocortical tumors in the general population. These classification attempts include criteria for malignancy based on tumor weight, clinical findings, and histologic features proposed by Hough and coworkers (41) and two systems based solely on histologic criteria proposed by Weiss and colleagues and van Slooten and colleagues (42–44). Division of carcinomas into low grade and high grade based on mitotic rate has also been proposed (45,46). Adrenocortical tumors in children, however, cannot be reliably distinguished based on these systems (39,46,47).
Lack et al (2) considered mitotic activity, vascular invasion, and extent of tumor necrosis to be the most prognostically useful histologic parameters in pediatric adrenocortical neoplasms. In children, histologic characteristics and tumor size may be suggestive of malignant potential, but no single parameter (except for detection of metastases) allows benign tumors to be discriminated from malignant ones.
Special studies are often of limited value in the pathologic diagnosis of adrenocortical tumors. Immunohistochemistry is not helpful in distinguishing between benign and malignant adrenocortical tumors, but it may be helpful in diagnosing other primary neoplasms that metastasize to the adrenal gland (48). Adrenocortical carcinomas are usually vimentin positive and often negative for cytokeratin, epithelial membrane antigen, and carcinoembryonic antigen. The electron microscopic appearance of adenomas resembles that of cells of the normal adrenal cortex, with steroid-producing cells showing tubulovesicular or tubulolamellar mitochondria, abundant smooth endoplasmic reticulum, and parallel stacks of rough endoplasmic reticulum. In addition, carcinomas may show abnormal numbers and morphology of mitochondria and dissolution of the basement membrane surrounding alveolar groups of cells (2,34). At DNA analysis, the presence of aneuploidy tends to favor malignancy, although this characteristic is also found in benign tumors, especially larger ones (44,49). Cytogenetic studies of carcinomas have shown loss of heterozygosity of several gene loci in some cases (44,50).
The histologic differential diagnosis of adrenocortical neoplasms includes nonneoplastic adrenal nodules, multinodular hyperplasia (which is usually bilateral and associated with hyperplasia of intervening cortical areas), pheochromocytoma, and metastatic carcinoma (particularly renal cell carcinoma, which is rare in children).
Metastases
The lung is the most common site of metastases from adrenocortical carcinoma, followed in frequency by the liver. Other metastatic sites include the peritoneum (29% of cases), pleura or diaphragm (24%), abdominal lymph nodes (24%), and kidney (18%) (2). Direct extension of tumor thrombus from the adrenal veins into the inferior vena cava represents an important mechanism of nonhematogenous malignant spread and may be clinically silent.
Tumor invasion of the inferior vena cava has been reported in six of 17 (35%) patients with clinically malignant adrenocortical neoplasms, sometimes producing lower extremity and truncal edema (2). There has been a case report of spontaneous regression of metastatic skin nodules and brain metastases 4 months after surgical resection of a right-sided adrenocortical carcinoma that manifested at birth (22).
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RADIOLOGIC FEATURES
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The clinical presentation of an infant or child with a functioning adrenocortical tumor may be indistinguishable from that of patients with adrenal hyperplasia or extraadrenal causes of isosexual or heterosexual precocious puberty (5). Moreover, the adrenal mass may be radiologically occult. In a review of 17 children with adrenocortical neoplasms, conventional radiography of the abdomen demonstrated a soft-tissue mass in eight, of whom only three had tumor calcification (5). Thus, before the widespread availability of ultrasound (US) and CT, the final diagnosis of adrenocortical tumor was often delayed (3,4). Cross-sectional imaging studies, including US, CT, and magnetic resonance (MR) imaging, have largely supplanted use of invasive procedures such as arteriography (Fig 6), venography, and venous sampling in the evaluation of adrenal abnormalities in children (51).
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Figure 6. Adrenocortical tumor in a 17-year-old girl with a 4-month history of lassitude. Spot radiograph from a selective right inferior adrenal arteriogram demonstrates neovascularity and puddling of contrast material within a large right suprarenal mass.
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Sonography is an effective screening study for a child with a suspected abdominal mass. When carefully performed, US helps characterize the mass as solid, cystic, or complex and often reveals preserved tissue planes between the tumor and adjacent organs, allowing distinction of a suprarenal mass from one arising in the adjacent kidney or liver. Large adrenal masses may rotate the ipsilateral kidney or displace it inferiorly (52). In addition to its usefulness in the initial detection of the primary tumor, US with color flow imaging facilitates the detection of venous tumor thrombus from adrenocortical carcinoma, which may extend into the right atrium and pose a risk of embolism (53).
Hamper et al (54) described the sonographic features of adrenocortical tumors in 26 patients, including seven children with pathologically proved adrenocortical carcinoma. The size of the adrenal lesions ranged from 3 to 22 cm. All were rounded or ovoid circumscribed masses that commonly displayed a lobulated border and, in seven (27%), a thin echogenic capsule-like rim. Five adrenocortical carcinomas that measured 6 cm or less were homogeneous solid masses nearly isoechoic to renal cortex (Fig 7). The larger lesions were heterogeneous and contained central or diffuse hypoechoic regions that corresponded to necrotic foci in the surgical pathology specimens (Fig 8). In two patients, central tumor necrosis produced a multiseptated cystic appearance at sonography. Tumor calcification was demonstrated in five cases (19%) (Fig 9).
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Figure 7a. Adrenocortical neoplasm in a 2-year-old girl with an abdominal mass and recent development of pubic hair. (a) Longitudinal US image of the abdomen reveals a homogeneous, solid right suprarenal mass. (b) Contrast-enhanced CT scan demonstrates the circumscribed right suprarenal mass (arrow), which enhances slightly more than the adjacent liver. (c) Photograph of the bisected surgical specimen shows a smooth, homogeneous, reddish-brown tumor.
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Figure 7b. Adrenocortical neoplasm in a 2-year-old girl with an abdominal mass and recent development of pubic hair. (a) Longitudinal US image of the abdomen reveals a homogeneous, solid right suprarenal mass. (b) Contrast-enhanced CT scan demonstrates the circumscribed right suprarenal mass (arrow), which enhances slightly more than the adjacent liver. (c) Photograph of the bisected surgical specimen shows a smooth, homogeneous, reddish-brown tumor.
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Figure 7c. Adrenocortical neoplasm in a 2-year-old girl with an abdominal mass and recent development of pubic hair. (a) Longitudinal US image of the abdomen reveals a homogeneous, solid right suprarenal mass. (b) Contrast-enhanced CT scan demonstrates the circumscribed right suprarenal mass (arrow), which enhances slightly more than the adjacent liver. (c) Photograph of the bisected surgical specimen shows a smooth, homogeneous, reddish-brown tumor.
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Figure 8a. Adrenocortical tumor in an 18-month-old boy with precocious puberty. (a) Longitudinal sonogram of the left flank demonstrates a large, heterogeneous mass (straight arrows, M) containing scattered cystic spaces. The left kidney (curved arrow) is compressed and displaced inferiorly. (b) Contrast-enhanced CT scan shows the heterogeneous left flank mass with a faintly enhancing, capsule-like rim (arrow), associated with a contralateral retroperitoneal nodal mass (arrowhead). (c) Photograph of the sectioned surgical specimen demonstrates extensive cystic change due to hemorrhage and necrosis. At surgery, one of seven nodes contained tumor.
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Figure 8b. Adrenocortical tumor in an 18-month-old boy with precocious puberty. (a) Longitudinal sonogram of the left flank demonstrates a large, heterogeneous mass (straight arrows, M) containing scattered cystic spaces. The left kidney (curved arrow) is compressed and displaced inferiorly. (b) Contrast-enhanced CT scan shows the heterogeneous left flank mass with a faintly enhancing, capsule-like rim (arrow), associated with a contralateral retroperitoneal nodal mass (arrowhead). (c) Photograph of the sectioned surgical specimen demonstrates extensive cystic change due to hemorrhage and necrosis. At surgery, one of seven nodes contained tumor.
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Figure 8c. Adrenocortical tumor in an 18-month-old boy with precocious puberty. (a) Longitudinal sonogram of the left flank demonstrates a large, heterogeneous mass (straight arrows, M) containing scattered cystic spaces. The left kidney (curved arrow) is compressed and displaced inferiorly. (b) Contrast-enhanced CT scan shows the heterogeneous left flank mass with a faintly enhancing, capsule-like rim (arrow), associated with a contralateral retroperitoneal nodal mass (arrowhead). (c) Photograph of the sectioned surgical specimen demonstrates extensive cystic change due to hemorrhage and necrosis. At surgery, one of seven nodes contained tumor.
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Figure 9a. Adrenocortical tumor in an 8-month-old girl with pubic hair. (a) Longitudinal sonogram demonstrates a heterogeneous, solid, left flank mass containing a shadowing echogenic focus (arrow), consistent with calcification. (b) Axial unenhanced CT scan of the abdomen shows the large left flank mass with faint calcifications (arrow). (c) Contrast-enhanced CT scan shows heterogeneous enhancement of the mass, low-attenuation regions (curved arrow) consistent with necrosis, and faint enhancement of a capsule-like rim (straight arrows).
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Figure 9b. Adrenocortical tumor in an 8-month-old girl with pubic hair. (a) Longitudinal sonogram demonstrates a heterogeneous, solid, left flank mass containing a shadowing echogenic focus (arrow), consistent with calcification. (b) Axial unenhanced CT scan of the abdomen shows the large left flank mass with faint calcifications (arrow). (c) Contrast-enhanced CT scan shows heterogeneous enhancement of the mass, low-attenuation regions (curved arrow) consistent with necrosis, and faint enhancement of a capsule-like rim (straight arrows).
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Figure 9c. Adrenocortical tumor in an 8-month-old girl with pubic hair. (a) Longitudinal sonogram demonstrates a heterogeneous, solid, left flank mass containing a shadowing echogenic focus (arrow), consistent with calcification. (b) Axial unenhanced CT scan of the abdomen shows the large left flank mass with faint calcifications (arrow). (c) Contrast-enhanced CT scan shows heterogeneous enhancement of the mass, low-attenuation regions (curved arrow) consistent with necrosis, and faint enhancement of a capsule-like rim (straight arrows).
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Fourteen children with adrenocortical carcinoma were evaluated with US in a study by Prando et al (55). The lesions, which ranged from 2.5 to 19 cm in maximum diameter, were all well-circumscribed. Smaller lesions were homogeneous and either uniformly hypoechoic or hyperechoic. A complex, predominantly hyperechoic pattern was demonstrated in the 10 patients with larger tumors, of which eight showed radiating linear echoes. The authors called this nonspecific stellate pattern the "scar sign," and considered it suggestive of cortical carcinoma. To our knowledge, the predictive value of this sign has not been determined. Vascular invasion or retroperitoneal adenopathy was noted in three patients.
CT is considered the most valuable technique for examining the adrenal glands (56). The CT findings of adrenocortical neoplasms in adults and children have been described (5,57–59). On CT scans, adrenocortical tumors are typically circumscribed, appear variably heterogeneous due to hemorrhage and necrosis, and may display a thin capsule-like rim (Fig 9). Larger lesions tend to enhance heterogeneously following intravenous administration of contrast material. In a study of 38 patients with adrenocortical carcinoma by Fishman et al (59), nine (24%) had detectable calcification at CT (Fig 10).
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Figure 10a. Adrenocortical neoplasm in a 13-year-old girl with hirsutism and hypertension. (a) Contrast-enhanced CT scan of the abdomen reveals a bulky, lobulated, heterogeneous left flank mass. Curvilinear foci of high attenuation (arrow), consistent with calcification, delimit tumor lobules. (b) Coronal T1-weighted (repetition time msec/echo time msec = 670/15) MR image shows a left flank mass of heterogeneous and predominantly low signal intensity. A renal origin is suggested by the beak of normal renal parenchyma (arrowhead) about the inferior aspect of the tumor. The kidney is seen below the mass (arrows). (c) Coronal proton density-weighted (2,500/22) MR image demonstrates heterogeneous increased signal intensity within the lesion. (d) Photograph of the surgical specimen sectioned sagittally shows the inferior margin (arrows) of the lobulated and necrotic mass apparently invading the upper pole of the left kidney. However, no invasion of the renal capsule was seen at microscopy.
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Figure 10b. Adrenocortical neoplasm in a 13-year-old girl with hirsutism and hypertension. (a) Contrast-enhanced CT scan of the abdomen reveals a bulky, lobulated, heterogeneous left flank mass. Curvilinear foci of high attenuation (arrow), consistent with calcification, delimit tumor lobules. (b) Coronal T1-weighted (repetition time msec/echo time msec = 670/15) MR image shows a left flank mass of heterogeneous and predominantly low signal intensity. A renal origin is suggested by the beak of normal renal parenchyma (arrowhead) about the inferior aspect of the tumor. The kidney is seen below the mass (arrows). (c) Coronal proton density-weighted (2,500/22) MR image demonstrates heterogeneous increased signal intensity within the lesion. (d) Photograph of the surgical specimen sectioned sagittally shows the inferior margin (arrows) of the lobulated and necrotic mass apparently invading the upper pole of the left kidney. However, no invasion of the renal capsule was seen at microscopy.
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Figure 10c. Adrenocortical neoplasm in a 13-year-old girl with hirsutism and hypertension. (a) Contrast-enhanced CT scan of the abdomen reveals a bulky, lobulated, heterogeneous left flank mass. Curvilinear foci of high attenuation (arrow), consistent with calcification, delimit tumor lobules. (b) Coronal T1-weighted (repetition time msec/echo time msec = 670/15) MR image shows a left flank mass of heterogeneous and predominantly low signal intensity. A renal origin is suggested by the beak of normal renal parenchyma (arrowhead) about the inferior aspect of the tumor. The kidney is seen below the mass (arrows). (c) Coronal proton density-weighted (2,500/22) MR image demonstrates heterogeneous increased signal intensity within the lesion. (d) Photograph of the surgical specimen sectioned sagittally shows the inferior margin (arrows) of the lobulated and necrotic mass apparently invading the upper pole of the left kidney. However, no invasion of the renal capsule was seen at microscopy.
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Figure 10d. Adrenocortical neoplasm in a 13-year-old girl with hirsutism and hypertension. (a) Contrast-enhanced CT scan of the abdomen reveals a bulky, lobulated, heterogeneous left flank mass. Curvilinear foci of high attenuation (arrow), consistent with calcification, delimit tumor lobules. (b) Coronal T1-weighted (repetition time msec/echo time msec = 670/15) MR image shows a left flank mass of heterogeneous and predominantly low signal intensity. A renal origin is suggested by the beak of normal renal parenchyma (arrowhead) about the inferior aspect of the tumor. The kidney is seen below the mass (arrows). (c) Coronal proton density-weighted (2,500/22) MR image demonstrates heterogeneous increased signal intensity within the lesion. (d) Photograph of the surgical specimen sectioned sagittally shows the inferior margin (arrows) of the lobulated and necrotic mass apparently invading the upper pole of the left kidney. However, no invasion of the renal capsule was seen at microscopy.
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The distinction between adrenocortical carcinoma and adenoma in children is difficult to make radiologically unless there is evidence of hematogenous metastases or venous spread. In adult patients, unenhanced CT densitometry allows adrenal adenomas to be accurately differentiated from nonadenomas because of the relatively high lipid content in adenomas (60,61). To our knowledge, this method has not been studied in adrenocortical tumors in children. It has been proposed that tumor size greater than 6 cm in diameter and heterogeneity of the primary mass at imaging studies are useful indicators of malignancy (55,62). However, Fishman and colleagues (59) concluded that adrenocortical carcinoma may manifest as a well-marginated, homogeneous mass 6 cm or less in diameter on CT scans.
There are few descriptions of the MR imaging appearance of hyperfunctioning adrenocortical tumors occurring in childhood (51,53,58,63). In one study of five pediatric patients with pathologically proved adrenocortical tumors (four adenomas, one of indeterminate histologic characteristics) ranging in size from 1.0 to 7.5 cm, all lesions were of intermediate signal intensity on T1-weighted MR images and of high signal intensity relative to liver on T2-weighted images (Figs 10, 11). There was no significant difference in signal intensity characteristics between the larger indeterminate lesion and the four adenomas. Similar MR imaging features in two adenomas and one carcinoma were illustrated in a pictorial review by Westra et al (51). The multiplanar capability of MR imaging facilitates detection of inferior vena cava tumor thrombus (Fig 12) (53). The accuracy of opposed-phase chemical shift MR imaging of adrenal masses, which allows adrenal adenomas to be differentiated from nonadenomas based on their relative fat content, has been established in adult patients (64–69). However, the utility of this technique has not been studied in the pediatric population.
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Figure 11a. Adrenocortical tumor in an 18-month-old boy with pubic hair. (a) Longitudinal right renal sonogram depicts a round, circumscribed, hypoechoic suprarenal mass (arrow). (b) Coronal T1-weighted (530/15) MR image shows the homogeneous mass that is nearly isointense relative to the renal cortex. (c) Axial T2-weighted (3,400/90) MR image reveals a moderate increase in signal intensity within the lesion, which appears distinct from the normal right adrenal gland (arrow). A well-encapsulated mass arising from a posterior limb of the right adrenal gland was found at surgery.
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Figure 11b. Adrenocortical tumor in an 18-month-old boy with pubic hair. (a) Longitudinal right renal sonogram depicts a round, circumscribed, hypoechoic suprarenal mass (arrow). (b) Coronal T1-weighted (530/15) MR image shows the homogeneous mass that is nearly isointense relative to the renal cortex. (c) Axial T2-weighted (3,400/90) MR image reveals a moderate increase in signal intensity within the lesion, which appears distinct from the normal right adrenal gland (arrow). A well-encapsulated mass arising from a posterior limb of the right adrenal gland was found at surgery.
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Figure 11c. Adrenocortical tumor in an 18-month-old boy with pubic hair. (a) Longitudinal right renal sonogram depicts a round, circumscribed, hypoechoic suprarenal mass (arrow). (b) Coronal T1-weighted (530/15) MR image shows the homogeneous mass that is nearly isointense relative to the renal cortex. (c) Axial T2-weighted (3,400/90) MR image reveals a moderate increase in signal intensity within the lesion, which appears distinct from the normal right adrenal gland (arrow). A well-encapsulated mass arising from a posterior limb of the right adrenal gland was found at surgery.
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Figure 12a. Obstruction of the inferior vena cava by tumor thrombus in a 15-year-old girl with a palpable abdominal mass and bilateral lower extremity swelling. (a) Contrast-enhanced chest CT scan (mediastinal window) shows the intrahepatic segment of the inferior vena cava (black arrow) distended by heterogeneously enhancing soft tissue. Dilated azygous (white arrow) and hemiazygous (arrowhead) veins represent collateral pathways of systemic venous return. A right pleural effusion is present. (b) CT scan obtained cephalad to a demonstrates a lobulated, right atrial filling defect (arrow). (c) Coronal T2-weighted (4,000/102) MR image reveals the primary tumor (arrowhead) in continuity with inferior vena cava thrombus (arrow) that extends into the right atrium.
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Figure 12b. Obstruction of the inferior vena cava by tumor thrombus in a 15-year-old girl with a palpable abdominal mass and bilateral lower extremity swelling. (a) Contrast-enhanced chest CT scan (mediastinal window) shows the intrahepatic segment of the inferior vena cava (black arrow) distended by heterogeneously enhancing soft tissue. Dilated azygous (white arrow) and hemiazygous (arrowhead) veins represent collateral pathways of systemic venous return. A right pleural effusion is present. (b) CT scan obtained cephalad to a demonstrates a lobulated, right atrial filling defect (arrow). (c) Coronal T2-weighted (4,000/102) MR image reveals the primary tumor (arrowhead) in continuity with inferior vena cava thrombus (arrow) that extends into the right atrium.
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Figure 12c. Obstruction of the inferior vena cava by tumor thrombus in a 15-year-old girl with a palpable abdominal mass and bilateral lower extremity swelling. (a) Contrast-enhanced chest CT scan (mediastinal window) shows the intrahepatic segment of the inferior vena cava (black arrow) distended by heterogeneously enhancing soft tissue. Dilated azygous (white arrow) and hemiazygous (arrowhead) veins represent collateral pathways of systemic venous return. A right pleural effusion is present. (b) CT scan obtained cephalad to a demonstrates a lobulated, right atrial filling defect (arrow). (c) Coronal T2-weighted (4,000/102) MR image reveals the primary tumor (arrowhead) in continuity with inferior vena cava thrombus (arrow) that extends into the right atrium.
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Excess serum cortisol may produce interesting secondary findings on cross-sectional imaging studies that carry a high specificity for the diagnosis of adrenocortical neoplasm. Of the many causes of medullary nephrocalcinosis, hypercalcemia due to Cushing syndrome is unusual (70). Hyperechoic renal medullary pyramids at sonography or high-attenuation medullary areas on unenhanced CT images of patients with a suprarenal mass support the diagnosis of adrenocortical neoplasm (Fig 13). Similarly, an increase in the amount of retroperitoneal fat in infants or young children, who normally have little, is a useful anatomic clue to the nature of an adrenal mass (Fig 13).
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Figure 13a. Adrenocortical tumor in a 7-week-old girl with acne and hypertension. (a) Axial contrast-enhanced CT scan of the abdomen shows a circumscribed, heterogeneous left suprarenal mass. (b, c) Longitudinal sonograms of the kidneys show the hypoechoic left suprarenal mass associated with hyperechoic renal pyramids (arrow in c), representing medullary nephrocalcinosis. (d) Axial T1-weighted (600/15) MR image of the abdomen obtained inferior to the level of the mass reveals increased retroperitoneal fat (arrows) due to Cushing syndrome.
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Figure 13b. Adrenocortical tumor in a 7-week-old girl with acne and hypertension. (a) Axial contrast-enhanced CT scan of the abdomen shows a circumscribed, heterogeneous left suprarenal mass. (b, c) Longitudinal sonograms of the kidneys show the hypoechoic left suprarenal mass associated with hyperechoic renal pyramids (arrow in c), representing medullary nephrocalcinosis. (d) Axial T1-weighted (600/15) MR image of the abdomen obtained inferior to the level of the mass reveals increased retroperitoneal fat (arrows) due to Cushing syndrome.
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Figure 13c. Adrenocortical tumor in a 7-week-old girl with acne and hypertension. (a) Axial contrast-enhanced CT scan of the abdomen shows a circumscribed, heterogeneous left suprarenal mass. (b, c) Longitudinal sonograms of the kidneys show the hypoechoic left suprarenal mass associated with hyperechoic renal pyramids (arrow in c), representing medullary nephrocalcinosis. (d) Axial T1-weighted (600/15) MR image of the abdomen obtained inferior to the level of the mass reveals increased retroperitoneal fat (arrows) due to Cushing syndrome.
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Figure 13d. Adrenocortical tumor in a 7-week-old girl with acne and hypertension. (a) Axial contrast-enhanced CT scan of the abdomen shows a circumscribed, heterogeneous left suprarenal mass. (b, c) Longitudinal sonograms of the kidneys show the hypoechoic left suprarenal mass associated with hyperechoic renal pyramids (arrow in c), representing medullary nephrocalcinosis. (d) Axial T1-weighted (600/15) MR image of the abdomen obtained inferior to the level of the mass reveals increased retroperitoneal fat (arrows) due to Cushing syndrome.
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DIFFERENTIAL DIAGNOSIS
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The combination of clinical features of hormone overproduction in a child, supportive laboratory findings, and a circumscribed adrenal mass at cross-sectional imaging studies is virtually diagnostic of a functioning adrenocortical neoplasm. Other pediatric adrenal masses include neuroblastoma, pheochromocytoma, adrenal hemorrhage, and, rarely, metastases.
Neuroblastoma, a neoplasm of the adrenal medulla and extraadrenal sympathetic tissue, typically affects young children, and its age of manifestation may overlap with that of childhood adrenocortical neoplasm. However, neuroblastoma often produces an increase in the serum and urinary levels of catecholamines. In addition, neuroblastoma is more commonly metastatic at presentation than adrenocortical carcinoma, and patients with this neoplasm often appear ill. Neuroblastoma may be associated with the paraneoplastic syndrome of myoclonic encephalopathy of infancy, and tumor elaboration of vasoactive intestinal peptide may produce watery diarrhea and hypokalemia. Although the protean manifestations of neuroblastoma are well-recognized (71), cross-sectional imaging studies of patients with neuroblastoma typically demonstrate a large, irregular, retroperitoneal mass that frequently encases vascular structures, often contains characteristic punctate calcifications, and may extend into the extradural spinal canal through neural foramina. Nevertheless, neuroblastoma may also manifest as a circumscribed suprarenal mass that is indistinguishable from an adrenocortical tumor, and adrenocortical tumors may also be associated with calcifications (Fig 14), retroperitoneal adenopathy, and vascular encasement (Figs 3, 8). Unlike adrenocortical neoplasms, neuroblastoma accumulates iodine-labeled metaiodobenzoguanidine (MIBG) at scintigraphy.
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Figure 14a. Metastatic adrenocortical carcinoma in a 17-year-old girl with fatigue, weight gain, and hypertension. (a) Unenhanced axial CT scan of the abdomen shows a large, lobulated, right flank mass containing punctate calcifications (arrow). (b) On a CT scan obtained after intravenous contrast material administration, the mass enhances heterogeneously and displays low-attenuation regions representing hemorrhage and necrosis. The inferior vena cava (arrow) is compressed, displaced, and possibly invaded. (c) Axial contrast-enhanced CT scan through the upper abdomen shows a low-attenuation metastasis (arrow) in the liver dome.
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Figure 14b. Metastatic adrenocortical carcinoma in a 17-year-old girl with fatigue, weight gain, and hypertension. (a) Unenhanced axial CT scan of the abdomen shows a large, lobulated, right flank mass containing punctate calcifications (arrow). (b) On a CT scan obtained after intravenous contrast material administration, the mass enhances heterogeneously and displays low-attenuation regions representing hemorrhage and necrosis. The inferior vena cava (arrow) is compressed, displaced, and possibly invaded. (c) Axial contrast-enhanced CT scan through the upper abdomen shows a low-attenuation metastasis (arrow) in the liver dome.
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Figure 14c. Metastatic adrenocortical carcinoma in a 17-year-old girl with fatigue, weight gain, and hypertension. (a) Unenhanced axial CT scan of the abdomen shows a large, lobulated, right flank mass containing punctate calcifications (arrow). (b) On a CT scan obtained after intravenous contrast material administration, the mass enhances heterogeneously and displays low-attenuation regions representing hemorrhage and necrosis. The inferior vena cava (arrow) is compressed, displaced, and possibly invaded. (c) Axial contrast-enhanced CT scan through the upper abdomen shows a low-attenuation metastasis (arrow) in the liver dome.
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Abstract
INTRODUCTION
