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Ultrasonography of the adrenals
Ultrasonography of the Adrenals By Hsu-Chong Yeh
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E LIN E ATIO N of the normal adrenal glands and small adrenal lesions used to be one of the most difficult techniques in ultrasonography. These organs are high in location and deep within the rib cage near the vertebrae, so they are easily obscured by the ribs and transverse processes of the spine and by the stomach and bowel gas. With the advent of the highresolution real-time scanner, especially the sector scanner, which can be easily applied to the intercostal space, adrenal lesions have become easier to examine. Successful scanning requires a thorough understanding of the anatomy of the adrenal area as well as of the proper scanning technique. A large adrenal mass is usually easy to delineate by any approach, but when the mass is huge, its origin may be difficult to determine. THE NORMAL ADRENAL GLAND
The normal adrenal glands are a pair of flat organs located anteromedial to the upper pole of the kidneys, only partly extending above the kidney. The right gland is triangular, whereas the left gland is semilunar in shape.' The left gland extends down to the renal hilum in about 10% of normal individuals." Although the glands are 4 to 6 em in length and 2 to 3 em in width, they are only 3 to 6 mm in thickness. I Because of their thinness and the frequent high level nature of their echoes, similar to that of surrounding fat, the adrenals frequently are not easily recognized by ultrasonography. With careful scanning, however, the normal right and left glands are visualized by manual scanning in 78% and 44% of cases, respectively," and by real-time scanning in 92% and 71 %, respectively." In newborn infants, with the high-frequency real-time scanner, the figures were 97% and 83%, respectively.l Each adrenal gland consists of three parts: the From the Department of Radiology, Mount Sinai Hospital and Mount Sinai School of Medicine of City University ofNew York. Hsu-Chong Yeh: Professor of Radiology. Address reprint requests to Hsu-Chong Yeh, MD, Department of Radiology, Box 1234, Mount Sinai Hospital, 1 Gustave L. Levy PI, New York, NY 10029-6574. © 1988 by GTUne & Stratton, Inc. 0037-198X/88/2304-0004$5.00/0 250
anteromedial ridge and the lateral and medial wings. The two wings open posterolaterally to straddle the anteromedial aspect of the upper pole of the kidney.Y Due to their thinness, each wing appears as an elongated or linear structure on cross-sectional CT or ultrasound imaging. They have been inappropriately called medial and lateral "limbs."3,7 The medial wing is larger superiorly and smaller or absent inferiorly (vice versa for the lateral wing). This results in a characteristic pattern on a series of transverse sections from the top downward." The apical section shows a vertical linear or curvilinear structure, consisting of only the anteromedial ridge and the medial wing. In the middle sections, both wings are seen and the gland has an inverted "Y" or "V" shape. On sections through the base of the gland, the medial wing may be very small or absent, and only the anteromedial ridge and a long lateral wing may be seen. The gland becomes L-shaped (left adrenal) or reverse L-shaped (right adrenal), or appears as a horizontal line when only the lateral wing is shown. Based on this cross-sectional anatomy, one can understand the following facts. First, the crosssectional images of the normal adrenal gland vary in different planes but in a characteristic sequence of patterns. Therefore, one can tell the level of section simply by the configuration of the image (Fig 1).8 Second, all these variations in contour can be seen in a single normal adrenal gland, depending on the level of the section. Therefore it is not appropriate to classify the CT or ultrasonographic features of normal adrenal glands into groups based on shape," Third, diffusely enlarged adrenal glands may show similar variations in shape on the sectional images, the sequence being the same as in normal glands. Therefore, they are not simply round or oval in shape, as some authors have reported. Understanding the relations of the adrenal glands to adjacent structures is important in ultrasound scanning. The right adrenal gland is located immediately posterior to the inferior vena cava, to which the anteromedial ridge of the gland usually attaches. It lies between the crus of the diaphragm and the posteromedial margin of
Seminars in Roentgenology, Vol XXIII. No 4 (October), 1988: pp 250-258
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Fig 1. Ultrasonographic and CT features of normal right adrenal gland. (A) Transverse sector scan from right upper flank shows the superior section of the right adrenal gland (arrow) to be a thick linear structure posterior to the inferior vena cava (V). and lateral to the crus of diaphragm (arrowhead). H - liver; K - kidney. (B) Scanned slightly inferiorly. the middle section of the right adrenal gland becomes an inverted V-shaped structure. (C) Scanned further inferiorly. the base of the adrenal gland appears as a reversed L-shaped structure. (0 through F) Corresponding CT scans in a different individual show similar features of the right adrenal gland (arrows) at different levels. All labels are the same as on the ultrasonographs except S spleen; black arrowhead = splenic artery. (A through C reprinted with permission. 3 )
the right lobe of the liver laterally. It is anteromedial to the upper pole of the right kidney. The left adrenal gland is located lateral or slightly posterior to the aorta and lateral to the crus of the diaphragm. It is posterior to the lesser sac superiorly and posterior to the pancreas inferiorly. Because the lesser sac is usually collapsed, the gland may appear to lie posterior to the stomach. It is anteromedial to the upper pole of the left kidney. The adrenal medulla is frequently seen as a highly echogenic linear structure in the gland (Fig 2). It is especially prominent in the newborn and fetus (Fig 3). Scanning Technique A high-resolution real-time sector scanner is the equipment of choice for scanning the adrenal glands. The best scanning approach is the transverse scan (Fig 4).4 For the right adrenal, the transducer is placed in the intercostal space in the right upper quadrant at the mid- or anterior axillary line. The liver usually serves as a good
Fig 2. Normal right adrenal gland. High-power zoom transverse scan shows the inferior portion of the right adrenal gland (arrow) posterior to the inferior vena cava IV). Note that the medulla of the gland is clearly seen as an echogenic linear structure.
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Fig 3. Fetal adrenal gland. Transverse scan of the upper abdomen of a 29-week fetus shows a relatively large right adrenal gland (white arrowhead) posterior to the inferior vena cava IV). A highly echogenic medulla is clearly seen. A - aorta.
acoustic window. By scanning slowly from the renal hilum upward to a few em above the kidney, concentrating on the area posterior to the inferior vena cava and lateral to the crus of the diaphragm, the adrenal area will be completely covered. Because the beam will be more or less perpendicular to the wings of the adrenal gland and crus of the diaphragm, these structures can be seen clearly. Scanned from an anterior or posterior direction, these structures become parallel to the sound beam and are not well seen. The left adrenal gland is best examined on transverse scan from the intercostal space in the left upper quadrant in mid- or posterior axillary line through the kidney or spleen. Because stomach or bowel gas may obscure the left adrenal area,
Fig 4. Scanning approaches for edrenal glands. Drawing shows transverse section of upper abdomen. With a sector real-time transducer placed, at the right lateral flank region and scanning through the intercostal space. the right adrenal area can be examined. For the left adrenal gland. one may have to place the transducer more posteriorly (eg. at the posterior axillary line) in the left lateral flank region. to avoid gas in the stomach or bowel. L = liver; 5 ~ spleen; K = kidney; V - inferior vena cava; A = aorta: arrows = adrenel glands.
scanning for the left gland is better accomplished by a more posterior approach. One should sweep slowly up and down the adrenal area so that every small detail in the area will be clearly visualized. The gain setting should be optimally adjusted since echoes in the adrenal glands may be only slightly less than that of surrounding fat tissue. Scanning with high-power zoom may also help in visualizing fine details. Longitudinal oblique scans" may be done through the same intercostal spaces as transverse scans. The craniocaudal dimension of a lesion can be measured by this scan. THE ABNORMAL ADRENAL GLAND
Adrenal Neoplasms
Focal Tumor A neoplasm may focally or diffusely involve the adrenal gland. The former is much more common, and its ultrasonographic features are usually different from the latter, except that when the mass is large and irregular both may be similar. The focal tumor is usually round or oval, may be located in any part of the gland, and ranges from 0.6 to 20 em in diameter. The diagnosis of an adrenal mass is usually certain when the uninvolved portion of the adrenal gland is also visible. Occasionally the mass may he located at the tip of one of the wings and extend outward. The mass may then appear to arise outside the gland, and its exact connection to the adrenal gland may be difficult to determine. Small adrenal masses. A small adrenal mass, less than 3 em in diameter, used to be difficult to delineate by ultrasonography. 10·14 With proper technique, however, the rate of detection is now high (97%),3 and a mass as small as 0.6 em in diameter may be seen (Fig 5).15 Although the overall rate of detection is slightly less by ultrasonography than by CT scan, a small right adrenal mass is not uncommonly better visualized by ultrasonography than by CT,3 especially in patients with scanty perirenal fat (eg, children or thin adults). In obese patients or those with Cushing syndrome, abundant perirenal fat forms a good natural contrast for visualizing the adrenal mass on CT, but the fat degrades the ultrasonographic image. The CT attenuation number of some adrenal neoplasms
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Fig 5. A small adrenal edenoma. Coronal scan from left upper flank shows a small nodule (arrowhead) 0.6 cm in diameter in the tip of the lateral wing of the left adrenal gland, which is horizontally V-shaped (arrow). S - spleen; K = kidney; A - aorta. (Reprinted with permission.'")
may be quite low, especially aldosteronoma or adenoma in Cushing syndrome, and may be poorly shown because of poor contrast with the surrounding fat." Ultrasonography may clearly visualize such masses." An adrenal mass with a relatively low attenuation number, similar to that of water, may simulate a cyst on CT scan, but ultrasonography will clearly show it as a solid mass. A small adrenal mass is usually easier to delineate than a normal adrenal gland because its diameter usually exceeds the thickness of the normal gland and because it is usually hypoechoic compared to the surrounding fat. The weak echoes are usually homogeneous. Even when a normal adrenal gland is not visualized, if the adrenal area is thoroughly scanned and no mass is seen, an adrenal neoplasm can be practically excluded.' When uninvolved normal parts of adrenal gland are visualized along with the adrenal mass, the exact location of the mass in the gland can be determined (Figs 5 and 6). The adrenal mass is frequently small in nonfunctioning adenoma and in functioning aldosteronoma. The adenoma of Cushing syndrome may also be small. Contrary to the common belief that the pheochromocytoma is large," a small mass is found in 20% in my experience." In malignant variety, metastatic tumor is the most common among the small adrenal masses. Differentiation between the benign and malignant tumors is usually impossible by ultrasonography. With
Fig 6. Small left adrenal adenome (0.7 cm in diameter). (A) High-power transverse scan of left adrenal gland through the left upper flank. A small mass (arrow) is seen in the medial aspect of the antaromedial ridge of the gland. The uninvolved portion of the gland (arrowheads) can be seen. Inset: drawing of the adrenal gland and mass. (B) CT scan through the superior aspect of the mass. The mass (arrow) is of low density because of partial volume effect with surrounding fat. However, the uninvolved portion of the adrenal gland (arrowheads) is clearly seen. (C) CT scan through the center of the mass (arrow). A - aorta.
clinical evidence of cortical hyperfunction, a nodule of less than 1 em diameter may represent an adenoma or a hyperplastic nodule. The latter mayor may not be associated with bilaterally enlarged (thickened) adrenal glands. Multiple small nodules usually favor bilateral hyperplasia. Differentiation between the two is very impor-
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tant since the adenoma requires surgical removal, whereas hyperplastic nodule needs only conservative treatment. When differentiation is impossible with ultrasound, CT, or MRI, adrenal venography, venous blood sampling, or adrenal scintigraphy may be performed. Larger adrenal masses. A moderate-sized (3.5 em to 5 cm diameter) adrenal mass is usually easy to delineate by ultrasonography and may be seen on anterior, lateral, or posterior scanning. It is usually round or oval and characteristically is located anterolateral to the upper pole of a kidney. A transverse scan through the intercostal spaces from the upper flank region will clearly demonstrate this relationship. Occasionally, the mass may be located immediately superior to the upper pole of the kidney rather than anterornedial to it and blend with it. A longitudinal scan from the upper flank region (ie, coronal or oblique coronal scan) may be useful in localizing such a mass. A large adrenal tumor usually displaces the upper pole of the kidney laterally, or the entire kidney inferiorly, or both. Occasionally, the tumor may extend downward anterior to the kidney without displacing it." The mass may indent the liver or the kidney. When a right adrenal mass is huge, it may markedly indent the right lobe of the liver (Fig 7). A notch at the demarcation of the liver with the mass and a relatively thick echogenic demarcating zone usually indicates that the mass is extrahepatic in origin (Fig 8). The inferior vena cava may be displaced anteriorly by a right adrenal mass; the tail of the pancreas may be displaced anteriorly by a left adrenal mass. Focal areas of necrosis or hemorrhage are more likely to occur in a large adrenal mass. This may cause inhomogeneity of the echo pattern, with areas of increased echoes and echo-free areas when liquefaction occurs. Nonliquefied necrosis may sometimes be echo-free due to marked edema; a completely clotted hematoma may also be echo-free." A large adrenal neoplasm is frequently malignant, whether functioning or nonfunctioning. However, a benign pheochromocytoma may become huge." Necrosis and hemorrhage are more frequent in the large malignant tumors. This does not apply to pheochromocytoma, in which they occur frequently, even in small tumors.P-"
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Large adrenel carcinoma with liver metasFig 7. tases. (A) Longitudinal scan of right upper abdomen shows a large adrenal mass (M) superior to the right kidney (K). The mass markedly indents the liver ILl. HV ~ hepatic vein. IB) LongitUdinal scan more medially shows the medial portion of the mass (M) displacing the inferior vena cava (V) anteriorly. Two metastatic masses 1m) are seen within the liver. Ie) Transverae scan of epigastrium shows the inferior portion of the mass (M) indenting the right kidney IK) and compressing the inferior vena cava (V) from behind. The head of the pancreas (P) and the inferior vena cava are displaced anteriorly. A = aorta; S = spine.
Multiple adrenal masses. Multiple masses may occur in the adrenal gland unilaterally or bilaterally. They are not uncommon and may be seen in: (1) metastatic disease (Fig 9) (especially bronchogenic carcinoma, renal cell carcinoma,
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Fig 8. Large adrenal carcinoma simulating a liver mass. This 73-year-old woman had been previously admitted to another hospital where the diagnosis of liver tumor was made on the basis of ultrasonography. CT. and celiac arteriography. Needle biopsy showed cancer cells probably of hepatic origin. Ultresonography was repeated after admission to Mount Sinai Hospital. and an adrenal tumor was diagnosed. Adrenal venography confirmed the diagnosis. and the adrenal carcinoma was surgically proven. There was no tumor in the liver. (A) Transverse scan of upper abdomen shows a large mass (arrows) that appears to involve a large mass in the entire right lobe of liver. l = normal left lobe of the liver; A - aorta. (S) Longitudinal scan 5 em to the right of the midline. The liver (L). high in the rib cage. was scanned through multiple intercostal spaces. The mass (arrows) is located inferior to the liver and above the kidney (K). A thick echogenic demarcation (broken arrow) is seen between the liver and the mass. and a notch (white arrowheadl is present at the posterior end of the demarcation. Ie) CT scan corresponding to A. The tumor location is easily mistaken for liver.
and melanoma); (2) pheochromocytoma; (3) lymphoma primarily in the adrenal or widespread; and (4) bilateral adrenal hyperplasia with multiple nodules usually less than 1 em in diameter. In macronodular hyperplasia, the nodules may be larger. When multiple masses are small or separated, they can be seen individually. When larger and closer together, they may appear as a single mass on CT scan unless sagittal reconstruction is performed. Longitudinal or coronal ultrasonography will often clearly demonstrate the multiple lesions (Fig 10). Ultrasonography will more clearly show multiple masses than CT. Diffuse adrenal enlargement. Diffuse adrenal enlargement may occur in (1) diffuse bilateral hyperplasia. In most patients, the adrenal glands are only slightly enlarged, and it
is difficult to detect this by ultrasonography. When the glands are substantially enlarged, it is important to identify the echogenic medulla (Fig 10)\5 so that hyperplasia can be differentiated from a diffuse infiltrative process, in which case the medulla will not be seen (Fig 11); (2) neoplastic disease, most commonly lymphoma but sometimes bronchogenic or renal cell carcinoma (Fig 11); or (3) inflammatory disease, such as tuberculosis" or histoplasmosis.f When the adrenal glands are moderately enlarged, they become thickened but maintain their original shape. With markedly enlarged glands, the superior section will show an elongated oval shape, and the middle section becomes round or a rounded-off triangle; sometimes the two wings may still be visible as a fat inverted Y or V. The lower section will show a triangular
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Fig 9. Two metastatic masses to the right adrenal gland from endometrial cancer. High-power zoom transverse scan of right adrenal gland. The smaller mass (rn] is at the postarior tip of the medial wing (arrow) of the gland. and the larger mass (MI is at the posterior tip of tha lateral wing (broken arrow) of the gland. V = inferior vena cava.
shape. Therefore, with a series of sections, diffuse enlargement can be recognized. This is contrary to previous reports in which diffusely enlarged adrenal glands on CT were said to be oval in shape and not distinguishable from a focal mass.P It is only when the glands are huge that they become irregular in shape and may be difficult to differentiate from a huge focal mass. Following chemotherapy or radiation, the dif-
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Fig 11. Diffusely enlarged right adrenal gland due to metastasis from renal cancer. High-power zoom transverse scan from right upper flank shows a thickened inverted V-shaped right adrenal gland (arrowhead) posterior to the inferior vena cava [VI.
fusedly enlarged gland will regain its normal shape even though it may remain enlarged. Adrenal Cysts and Hemorrhage
Both adrenal cysts and hemorrhage may appear as a round echo-free lesion. The most common adrenal cyst (45%) is the endothelial type." They are mostly lymphangiomatous in origin but some are of angiomatous variety. The other cysts are sequelae of hemorrhage, epithelial glandular cysts, or cchinococcal cyst. About 15% of adrenal cysts are calcified. This causes a thick, highly echogenic wall that casts an acoustic shadow." Although adrenal hemorrhage is usually echofree,2s-27 (Fig 12), echoes may be seen if there is clot. After lysis of the clot, the echoes may disappear. As the hematoma decreases in size, echoes may reappear due to organization of hematoma. The hematoma may eventually disappear or calcify in 4 to 9 months." Miscellaneous Adrenal Lesions
Fig 10. Adrenal hyperplasia. Oblique longitudinal scan of the right upper abdomen shows a "fat" horizontal V-shaped adranal gland [arrowl. The thickness of the lataral wing is 1.2 em. more than twice normal. Note the echogenic medulla within the gland. indicating hyperplastic gland rather than an infiltrating procass. (Raprinted with permission.'")
Myelolipoma is a relatively uncommon tumor that contains fat and bone marrow cells. It is usually seen in the fourth to sixth decades. Ultrasonography demonstrates a highly echogenic mass due to the fat content"; CT will show low density in the mass due to the fat.
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Fig 13. Accessory spleen. Transverse sector scan from the left upper flank shows a small mass (arrowhead) anteromedial to the kidney (Kl similar to an adrenal mass. An artery (arrow) arises from the mass and courses toward the splenic hilum. Therefore this is an accessory spleen rather than an adrenal mass. S = spleen; A - aorta.
Fig 12. Bilateral adrenal hemorrhage in a newborn. (A and B) Longitudinal oblique scans show an echo-free lesion (arrowhead) above each kidney, representing the hematomas.
In portal hypertension, varicosities of the adrenal vein may occasionally be seen. Large tortuous vessels may be seen in the adrenal areas on ultrasonography." Tuberculosis" or histoplasmosis" may affect the adrenal gland, forming a masslike lesion or diffuse enlargement of the gland. A fibrofatty mass in the adrenal gland caused by old inflammatory disease may appear as an ill-defined echogenic mass.P Differential Diagnosis
An accessory spleen is a smooth round nodule located near the splenic hilum, usually lateral to the adrenal gland. However, when it is located medially, it may be confused with an adrenal mass. Demonstration of vessels connecting the nodule to the splenic artery or the splenic hilum indicate accessory spleen (Fig 13).30 A protrusion of the medial inferior aspect of the spleen may also simulate an adrenal mass." With real time, it is usually easy to find the connection between the protrusion and the spleen. The echo pattern is the same for both. An enlarged retrocrural node may be located in the adrenal area and be mistaken for an
adrenal mass. Demonstration of a crus of the diaphragm and a normal adrenal gland will solve the problem. A mass that is partly in and partly outside the liver may be difficult to localize and to differentiate from one of adrenal origin. A thick echogenic demarcation between the mass and the liver due to fat and a notch at the end of the demarcation suggest that the mass is of extrahepatic origin, ie, an adrenal mass. When these signs are absent, if the larger portion of the mass is located outside the expected contour of the liver, the mass is probably extrahepatic in -origin." The same applies to a marginal renal mass. Tortuous high renal veins may pass by the adrenal area and simulate an adrenal lesion. Careful examination with real-time scanning will show the lesion to be tubular in nature and to connect to the inferior vena cava superiorly and renal hilum inferiorly. Enlarged para-aortic, paracaval, or retropancreatic nodes may also simulate an adrenal mass. Differentiation depends on the demonstration of a normal adrenal gland clearly separate from the mass. ACKNOWLEDGMENT I thank Louisa Haigler and Gilbert Zakow for preparation of the manuscript.
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REFERENCES 1. Netter NH: The ClBA Collection of Medical Illustrations, vol 4. Endocrine System and Selected Metabolic Disease. Summit, NJ: CIBA, 1965:78-79 2. Brownlie K, Kreel L: Computer assisted tomography of normal suprarenal glands. J Comput Assist Tomogr 1978;2:1-10 3. Yeh HC: Ultrasonography of normal adrenal gland and small adrenal masses. AJR 1980;135:1167-1177 4. Marchal G, Olin J, Verbeken E, et al: High resolution real-time sonography of adrenal glands: A routine examination? J Ultrasound Med 1986;5:65-68 5. Oppenheimer DA, Carroll BA, Yousem S: Sonography of the normal neonatal adrenal gland. Radiology 1983; 146:157-160 6. Yeh HC, Mitty HA, Rose J, et al: Ultrasonography of adrenal masses: Usual features. Radiology 1978;127:467474 7. Karstaedt H, Sagel SS, Stanley RJ, et al: Computed tomography of adrenal gland. Radiology 1978;129:723-730 8. Yeh HC: Ultrasonography of the adrenal gland. In: Resnick MI, Sanders RC (eds): Ultrasound in Urology. Baltimore: Williams & Wilkins, 1984:285-306 9. Sample WF: A new technique for the evaluation of the adrenal gland with gray scale ultrasonography. Radiology 1977; 124:463-469 10. Birnholz JC: Ultrasound imaging of adrenal mass lesions. Radiology 1973;109:163-166 11. Davidson JK, Morley P, Hurley OD, et al: Adrenal venography and ultrasonography in the investigation of the adrenal gland: An analysis of 53 cases. Dr J Radiol 1975;48:435-450 12. Forsythe JR, Gosink BB, Leopold OR: Ultrasound in the evaluation of adrenal metastases. J CUn Ultrasound 1977;5:31-34 13. Ghorashi B, Holmes JH: Gray scale sonographic appearance of an adrenal mass: A case report. J CUn Ultrasound 1976;4:121-123 14. Holm HH, Kristensen JK, Rasmussen SN, et al: Ultrasonic diagnosis of juxtarenal masses. Soand J Urol NephroI1972;6(suppI15):83-88 15. Yeh HC: Adrenal gland and nonrenal retroperitoneum. Urol RadioI1987;9:127-140 16. Schaner EO, Dunnick NR, Doppman JL, et al:
Adrenal cortical tumors with low attenuation coefficients: A pitfall in computed tomography diagnosis. J Comput Assist Tomogr 1978;2:11 17. Mitty HA, Yeh HC: Radiology of the Adrenals with Sonography and CT. Philadelphia: Saunders, 1981:116-135, 178 18. Bowerman RA, Silver TM, Jaffe MH, et al: Sonography of adrenal pheochromocytomas. AJR 1981;137:12271231 19. Yeh HC, Pertsemlidis D, Mitty HA: Pheochromocytoma: Role of ultrasonography and CT. Presented at the 70th Annual Meeting of the Radiologic Society of North America, Washington, November 1984 20. Yeh HC, Mitty HA, Rose JS, et al: Ultrasonography of adrenal masses-Unusual manifestations. Radiology 1978;127:475-483 21. Wilms OE, Baert AL, Kint EJ, et al: Computed tomographic findings in bilateral adrenal tuberculosis. Radiology 1983;146:729-730 22. Wilson DA, Muchmore HO, Tisdal RO, et al: Histoplasmosis of the adrenal glands studied by CT. Radiology 1984;150:779-783 23. Paling MR, Williamson BRJ: Adrenal involvement in non-Hodgkin's lymphoma. AJR 1983;141:303-305 24. Foster DO: Adrenal cysts: Review of literature and report of case. Arch Surg 1986;92:131-143 25. Pery M, Kaltori JK, Bar-Maor JA: Sonography for diagnosis and follow-up of neonatal adrenal hemorrhage. J CUn Ultrasound 1981;9:397-401 26. Mittlestaedt CA, Volberg FM, Merten DR, et al: The sonographic diagnosis of neonatal adrenal hemorrhage. Radiology 1979; 131:453-457 27. Mineau DE, Koehler PR: Ultrasound diagnosis of neonatal adrenal hemorrhage. AJR 1979;132:443-444 28. Behan M, Martin EC, Muecke EC, et al: Myelolipoma of the adrenal: Two cases with ultrasound and CT findings. AJR 1977;129:993-996 29. Yeh HC: Adrenal sonography. In: Leopold OR (ed): Ultrasound in breast and endocrine disease. Clin Diagn Ultrasound 1984;12:101-130 30. Subramanyam BR, Balthazar EJ, Horii SC: Sonography of accessory spleen. AJR 1984;143:47-49
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E LIN E ATIO N of the normal adrenal glands and small adrenal lesions used to be one of the most difficult techniques in ultrasonography. These organs are high in location and deep within the rib cage near the vertebrae, so they are easily obscured by the ribs and transverse processes of the spine and by the stomach and bowel gas. With the advent of the highresolution real-time scanner, especially the sector scanner, which can be easily applied to the intercostal space, adrenal lesions have become easier to examine. Successful scanning requires a thorough understanding of the anatomy of the adrenal area as well as of the proper scanning technique. A large adrenal mass is usually easy to delineate by any approach, but when the mass is huge, its origin may be difficult to determine. THE NORMAL ADRENAL GLAND
The normal adrenal glands are a pair of flat organs located anteromedial to the upper pole of the kidneys, only partly extending above the kidney. The right gland is triangular, whereas the left gland is semilunar in shape.' The left gland extends down to the renal hilum in about 10% of normal individuals." Although the glands are 4 to 6 em in length and 2 to 3 em in width, they are only 3 to 6 mm in thickness. I Because of their thinness and the frequent high level nature of their echoes, similar to that of surrounding fat, the adrenals frequently are not easily recognized by ultrasonography. With careful scanning, however, the normal right and left glands are visualized by manual scanning in 78% and 44% of cases, respectively," and by real-time scanning in 92% and 71 %, respectively." In newborn infants, with the high-frequency real-time scanner, the figures were 97% and 83%, respectively.l Each adrenal gland consists of three parts: the From the Department of Radiology, Mount Sinai Hospital and Mount Sinai School of Medicine of City University ofNew York. Hsu-Chong Yeh: Professor of Radiology. Address reprint requests to Hsu-Chong Yeh, MD, Department of Radiology, Box 1234, Mount Sinai Hospital, 1 Gustave L. Levy PI, New York, NY 10029-6574. © 1988 by GTUne & Stratton, Inc. 0037-198X/88/2304-0004$5.00/0 250
anteromedial ridge and the lateral and medial wings. The two wings open posterolaterally to straddle the anteromedial aspect of the upper pole of the kidney.Y Due to their thinness, each wing appears as an elongated or linear structure on cross-sectional CT or ultrasound imaging. They have been inappropriately called medial and lateral "limbs."3,7 The medial wing is larger superiorly and smaller or absent inferiorly (vice versa for the lateral wing). This results in a characteristic pattern on a series of transverse sections from the top downward." The apical section shows a vertical linear or curvilinear structure, consisting of only the anteromedial ridge and the medial wing. In the middle sections, both wings are seen and the gland has an inverted "Y" or "V" shape. On sections through the base of the gland, the medial wing may be very small or absent, and only the anteromedial ridge and a long lateral wing may be seen. The gland becomes L-shaped (left adrenal) or reverse L-shaped (right adrenal), or appears as a horizontal line when only the lateral wing is shown. Based on this cross-sectional anatomy, one can understand the following facts. First, the crosssectional images of the normal adrenal gland vary in different planes but in a characteristic sequence of patterns. Therefore, one can tell the level of section simply by the configuration of the image (Fig 1).8 Second, all these variations in contour can be seen in a single normal adrenal gland, depending on the level of the section. Therefore it is not appropriate to classify the CT or ultrasonographic features of normal adrenal glands into groups based on shape," Third, diffusely enlarged adrenal glands may show similar variations in shape on the sectional images, the sequence being the same as in normal glands. Therefore, they are not simply round or oval in shape, as some authors have reported. Understanding the relations of the adrenal glands to adjacent structures is important in ultrasound scanning. The right adrenal gland is located immediately posterior to the inferior vena cava, to which the anteromedial ridge of the gland usually attaches. It lies between the crus of the diaphragm and the posteromedial margin of
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Fig 1. Ultrasonographic and CT features of normal right adrenal gland. (A) Transverse sector scan from right upper flank shows the superior section of the right adrenal gland (arrow) to be a thick linear structure posterior to the inferior vena cava (V). and lateral to the crus of diaphragm (arrowhead). H - liver; K - kidney. (B) Scanned slightly inferiorly. the middle section of the right adrenal gland becomes an inverted V-shaped structure. (C) Scanned further inferiorly. the base of the adrenal gland appears as a reversed L-shaped structure. (0 through F) Corresponding CT scans in a different individual show similar features of the right adrenal gland (arrows) at different levels. All labels are the same as on the ultrasonographs except S spleen; black arrowhead = splenic artery. (A through C reprinted with permission. 3 )
the right lobe of the liver laterally. It is anteromedial to the upper pole of the right kidney. The left adrenal gland is located lateral or slightly posterior to the aorta and lateral to the crus of the diaphragm. It is posterior to the lesser sac superiorly and posterior to the pancreas inferiorly. Because the lesser sac is usually collapsed, the gland may appear to lie posterior to the stomach. It is anteromedial to the upper pole of the left kidney. The adrenal medulla is frequently seen as a highly echogenic linear structure in the gland (Fig 2). It is especially prominent in the newborn and fetus (Fig 3). Scanning Technique A high-resolution real-time sector scanner is the equipment of choice for scanning the adrenal glands. The best scanning approach is the transverse scan (Fig 4).4 For the right adrenal, the transducer is placed in the intercostal space in the right upper quadrant at the mid- or anterior axillary line. The liver usually serves as a good
Fig 2. Normal right adrenal gland. High-power zoom transverse scan shows the inferior portion of the right adrenal gland (arrow) posterior to the inferior vena cava IV). Note that the medulla of the gland is clearly seen as an echogenic linear structure.
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Fig 3. Fetal adrenal gland. Transverse scan of the upper abdomen of a 29-week fetus shows a relatively large right adrenal gland (white arrowhead) posterior to the inferior vena cava IV). A highly echogenic medulla is clearly seen. A - aorta.
acoustic window. By scanning slowly from the renal hilum upward to a few em above the kidney, concentrating on the area posterior to the inferior vena cava and lateral to the crus of the diaphragm, the adrenal area will be completely covered. Because the beam will be more or less perpendicular to the wings of the adrenal gland and crus of the diaphragm, these structures can be seen clearly. Scanned from an anterior or posterior direction, these structures become parallel to the sound beam and are not well seen. The left adrenal gland is best examined on transverse scan from the intercostal space in the left upper quadrant in mid- or posterior axillary line through the kidney or spleen. Because stomach or bowel gas may obscure the left adrenal area,
Fig 4. Scanning approaches for edrenal glands. Drawing shows transverse section of upper abdomen. With a sector real-time transducer placed, at the right lateral flank region and scanning through the intercostal space. the right adrenal area can be examined. For the left adrenal gland. one may have to place the transducer more posteriorly (eg. at the posterior axillary line) in the left lateral flank region. to avoid gas in the stomach or bowel. L = liver; 5 ~ spleen; K = kidney; V - inferior vena cava; A = aorta: arrows = adrenel glands.
scanning for the left gland is better accomplished by a more posterior approach. One should sweep slowly up and down the adrenal area so that every small detail in the area will be clearly visualized. The gain setting should be optimally adjusted since echoes in the adrenal glands may be only slightly less than that of surrounding fat tissue. Scanning with high-power zoom may also help in visualizing fine details. Longitudinal oblique scans" may be done through the same intercostal spaces as transverse scans. The craniocaudal dimension of a lesion can be measured by this scan. THE ABNORMAL ADRENAL GLAND
Adrenal Neoplasms
Focal Tumor A neoplasm may focally or diffusely involve the adrenal gland. The former is much more common, and its ultrasonographic features are usually different from the latter, except that when the mass is large and irregular both may be similar. The focal tumor is usually round or oval, may be located in any part of the gland, and ranges from 0.6 to 20 em in diameter. The diagnosis of an adrenal mass is usually certain when the uninvolved portion of the adrenal gland is also visible. Occasionally the mass may he located at the tip of one of the wings and extend outward. The mass may then appear to arise outside the gland, and its exact connection to the adrenal gland may be difficult to determine. Small adrenal masses. A small adrenal mass, less than 3 em in diameter, used to be difficult to delineate by ultrasonography. 10·14 With proper technique, however, the rate of detection is now high (97%),3 and a mass as small as 0.6 em in diameter may be seen (Fig 5).15 Although the overall rate of detection is slightly less by ultrasonography than by CT scan, a small right adrenal mass is not uncommonly better visualized by ultrasonography than by CT,3 especially in patients with scanty perirenal fat (eg, children or thin adults). In obese patients or those with Cushing syndrome, abundant perirenal fat forms a good natural contrast for visualizing the adrenal mass on CT, but the fat degrades the ultrasonographic image. The CT attenuation number of some adrenal neoplasms
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Fig 5. A small adrenal edenoma. Coronal scan from left upper flank shows a small nodule (arrowhead) 0.6 cm in diameter in the tip of the lateral wing of the left adrenal gland, which is horizontally V-shaped (arrow). S - spleen; K = kidney; A - aorta. (Reprinted with permission.'")
may be quite low, especially aldosteronoma or adenoma in Cushing syndrome, and may be poorly shown because of poor contrast with the surrounding fat." Ultrasonography may clearly visualize such masses." An adrenal mass with a relatively low attenuation number, similar to that of water, may simulate a cyst on CT scan, but ultrasonography will clearly show it as a solid mass. A small adrenal mass is usually easier to delineate than a normal adrenal gland because its diameter usually exceeds the thickness of the normal gland and because it is usually hypoechoic compared to the surrounding fat. The weak echoes are usually homogeneous. Even when a normal adrenal gland is not visualized, if the adrenal area is thoroughly scanned and no mass is seen, an adrenal neoplasm can be practically excluded.' When uninvolved normal parts of adrenal gland are visualized along with the adrenal mass, the exact location of the mass in the gland can be determined (Figs 5 and 6). The adrenal mass is frequently small in nonfunctioning adenoma and in functioning aldosteronoma. The adenoma of Cushing syndrome may also be small. Contrary to the common belief that the pheochromocytoma is large," a small mass is found in 20% in my experience." In malignant variety, metastatic tumor is the most common among the small adrenal masses. Differentiation between the benign and malignant tumors is usually impossible by ultrasonography. With
Fig 6. Small left adrenal adenome (0.7 cm in diameter). (A) High-power transverse scan of left adrenal gland through the left upper flank. A small mass (arrow) is seen in the medial aspect of the antaromedial ridge of the gland. The uninvolved portion of the gland (arrowheads) can be seen. Inset: drawing of the adrenal gland and mass. (B) CT scan through the superior aspect of the mass. The mass (arrow) is of low density because of partial volume effect with surrounding fat. However, the uninvolved portion of the adrenal gland (arrowheads) is clearly seen. (C) CT scan through the center of the mass (arrow). A - aorta.
clinical evidence of cortical hyperfunction, a nodule of less than 1 em diameter may represent an adenoma or a hyperplastic nodule. The latter mayor may not be associated with bilaterally enlarged (thickened) adrenal glands. Multiple small nodules usually favor bilateral hyperplasia. Differentiation between the two is very impor-
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tant since the adenoma requires surgical removal, whereas hyperplastic nodule needs only conservative treatment. When differentiation is impossible with ultrasound, CT, or MRI, adrenal venography, venous blood sampling, or adrenal scintigraphy may be performed. Larger adrenal masses. A moderate-sized (3.5 em to 5 cm diameter) adrenal mass is usually easy to delineate by ultrasonography and may be seen on anterior, lateral, or posterior scanning. It is usually round or oval and characteristically is located anterolateral to the upper pole of a kidney. A transverse scan through the intercostal spaces from the upper flank region will clearly demonstrate this relationship. Occasionally, the mass may be located immediately superior to the upper pole of the kidney rather than anterornedial to it and blend with it. A longitudinal scan from the upper flank region (ie, coronal or oblique coronal scan) may be useful in localizing such a mass. A large adrenal tumor usually displaces the upper pole of the kidney laterally, or the entire kidney inferiorly, or both. Occasionally, the tumor may extend downward anterior to the kidney without displacing it." The mass may indent the liver or the kidney. When a right adrenal mass is huge, it may markedly indent the right lobe of the liver (Fig 7). A notch at the demarcation of the liver with the mass and a relatively thick echogenic demarcating zone usually indicates that the mass is extrahepatic in origin (Fig 8). The inferior vena cava may be displaced anteriorly by a right adrenal mass; the tail of the pancreas may be displaced anteriorly by a left adrenal mass. Focal areas of necrosis or hemorrhage are more likely to occur in a large adrenal mass. This may cause inhomogeneity of the echo pattern, with areas of increased echoes and echo-free areas when liquefaction occurs. Nonliquefied necrosis may sometimes be echo-free due to marked edema; a completely clotted hematoma may also be echo-free." A large adrenal neoplasm is frequently malignant, whether functioning or nonfunctioning. However, a benign pheochromocytoma may become huge." Necrosis and hemorrhage are more frequent in the large malignant tumors. This does not apply to pheochromocytoma, in which they occur frequently, even in small tumors.P-"
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Large adrenel carcinoma with liver metasFig 7. tases. (A) Longitudinal scan of right upper abdomen shows a large adrenal mass (M) superior to the right kidney (K). The mass markedly indents the liver ILl. HV ~ hepatic vein. IB) LongitUdinal scan more medially shows the medial portion of the mass (M) displacing the inferior vena cava (V) anteriorly. Two metastatic masses 1m) are seen within the liver. Ie) Transverae scan of epigastrium shows the inferior portion of the mass (M) indenting the right kidney IK) and compressing the inferior vena cava (V) from behind. The head of the pancreas (P) and the inferior vena cava are displaced anteriorly. A = aorta; S = spine.
Multiple adrenal masses. Multiple masses may occur in the adrenal gland unilaterally or bilaterally. They are not uncommon and may be seen in: (1) metastatic disease (Fig 9) (especially bronchogenic carcinoma, renal cell carcinoma,
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Fig 8. Large adrenal carcinoma simulating a liver mass. This 73-year-old woman had been previously admitted to another hospital where the diagnosis of liver tumor was made on the basis of ultrasonography. CT. and celiac arteriography. Needle biopsy showed cancer cells probably of hepatic origin. Ultresonography was repeated after admission to Mount Sinai Hospital. and an adrenal tumor was diagnosed. Adrenal venography confirmed the diagnosis. and the adrenal carcinoma was surgically proven. There was no tumor in the liver. (A) Transverse scan of upper abdomen shows a large mass (arrows) that appears to involve a large mass in the entire right lobe of liver. l = normal left lobe of the liver; A - aorta. (S) Longitudinal scan 5 em to the right of the midline. The liver (L). high in the rib cage. was scanned through multiple intercostal spaces. The mass (arrows) is located inferior to the liver and above the kidney (K). A thick echogenic demarcation (broken arrow) is seen between the liver and the mass. and a notch (white arrowheadl is present at the posterior end of the demarcation. Ie) CT scan corresponding to A. The tumor location is easily mistaken for liver.
and melanoma); (2) pheochromocytoma; (3) lymphoma primarily in the adrenal or widespread; and (4) bilateral adrenal hyperplasia with multiple nodules usually less than 1 em in diameter. In macronodular hyperplasia, the nodules may be larger. When multiple masses are small or separated, they can be seen individually. When larger and closer together, they may appear as a single mass on CT scan unless sagittal reconstruction is performed. Longitudinal or coronal ultrasonography will often clearly demonstrate the multiple lesions (Fig 10). Ultrasonography will more clearly show multiple masses than CT. Diffuse adrenal enlargement. Diffuse adrenal enlargement may occur in (1) diffuse bilateral hyperplasia. In most patients, the adrenal glands are only slightly enlarged, and it
is difficult to detect this by ultrasonography. When the glands are substantially enlarged, it is important to identify the echogenic medulla (Fig 10)\5 so that hyperplasia can be differentiated from a diffuse infiltrative process, in which case the medulla will not be seen (Fig 11); (2) neoplastic disease, most commonly lymphoma but sometimes bronchogenic or renal cell carcinoma (Fig 11); or (3) inflammatory disease, such as tuberculosis" or histoplasmosis.f When the adrenal glands are moderately enlarged, they become thickened but maintain their original shape. With markedly enlarged glands, the superior section will show an elongated oval shape, and the middle section becomes round or a rounded-off triangle; sometimes the two wings may still be visible as a fat inverted Y or V. The lower section will show a triangular
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Fig 9. Two metastatic masses to the right adrenal gland from endometrial cancer. High-power zoom transverse scan of right adrenal gland. The smaller mass (rn] is at the postarior tip of the medial wing (arrow) of the gland. and the larger mass (MI is at the posterior tip of tha lateral wing (broken arrow) of the gland. V = inferior vena cava.
shape. Therefore, with a series of sections, diffuse enlargement can be recognized. This is contrary to previous reports in which diffusely enlarged adrenal glands on CT were said to be oval in shape and not distinguishable from a focal mass.P It is only when the glands are huge that they become irregular in shape and may be difficult to differentiate from a huge focal mass. Following chemotherapy or radiation, the dif-
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Fig 11. Diffusely enlarged right adrenal gland due to metastasis from renal cancer. High-power zoom transverse scan from right upper flank shows a thickened inverted V-shaped right adrenal gland (arrowhead) posterior to the inferior vena cava [VI.
fusedly enlarged gland will regain its normal shape even though it may remain enlarged. Adrenal Cysts and Hemorrhage
Both adrenal cysts and hemorrhage may appear as a round echo-free lesion. The most common adrenal cyst (45%) is the endothelial type." They are mostly lymphangiomatous in origin but some are of angiomatous variety. The other cysts are sequelae of hemorrhage, epithelial glandular cysts, or cchinococcal cyst. About 15% of adrenal cysts are calcified. This causes a thick, highly echogenic wall that casts an acoustic shadow." Although adrenal hemorrhage is usually echofree,2s-27 (Fig 12), echoes may be seen if there is clot. After lysis of the clot, the echoes may disappear. As the hematoma decreases in size, echoes may reappear due to organization of hematoma. The hematoma may eventually disappear or calcify in 4 to 9 months." Miscellaneous Adrenal Lesions
Fig 10. Adrenal hyperplasia. Oblique longitudinal scan of the right upper abdomen shows a "fat" horizontal V-shaped adranal gland [arrowl. The thickness of the lataral wing is 1.2 em. more than twice normal. Note the echogenic medulla within the gland. indicating hyperplastic gland rather than an infiltrating procass. (Raprinted with permission.'")
Myelolipoma is a relatively uncommon tumor that contains fat and bone marrow cells. It is usually seen in the fourth to sixth decades. Ultrasonography demonstrates a highly echogenic mass due to the fat content"; CT will show low density in the mass due to the fat.
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Fig 13. Accessory spleen. Transverse sector scan from the left upper flank shows a small mass (arrowhead) anteromedial to the kidney (Kl similar to an adrenal mass. An artery (arrow) arises from the mass and courses toward the splenic hilum. Therefore this is an accessory spleen rather than an adrenal mass. S = spleen; A - aorta.
Fig 12. Bilateral adrenal hemorrhage in a newborn. (A and B) Longitudinal oblique scans show an echo-free lesion (arrowhead) above each kidney, representing the hematomas.
In portal hypertension, varicosities of the adrenal vein may occasionally be seen. Large tortuous vessels may be seen in the adrenal areas on ultrasonography." Tuberculosis" or histoplasmosis" may affect the adrenal gland, forming a masslike lesion or diffuse enlargement of the gland. A fibrofatty mass in the adrenal gland caused by old inflammatory disease may appear as an ill-defined echogenic mass.P Differential Diagnosis
An accessory spleen is a smooth round nodule located near the splenic hilum, usually lateral to the adrenal gland. However, when it is located medially, it may be confused with an adrenal mass. Demonstration of vessels connecting the nodule to the splenic artery or the splenic hilum indicate accessory spleen (Fig 13).30 A protrusion of the medial inferior aspect of the spleen may also simulate an adrenal mass." With real time, it is usually easy to find the connection between the protrusion and the spleen. The echo pattern is the same for both. An enlarged retrocrural node may be located in the adrenal area and be mistaken for an
adrenal mass. Demonstration of a crus of the diaphragm and a normal adrenal gland will solve the problem. A mass that is partly in and partly outside the liver may be difficult to localize and to differentiate from one of adrenal origin. A thick echogenic demarcation between the mass and the liver due to fat and a notch at the end of the demarcation suggest that the mass is of extrahepatic origin, ie, an adrenal mass. When these signs are absent, if the larger portion of the mass is located outside the expected contour of the liver, the mass is probably extrahepatic in -origin." The same applies to a marginal renal mass. Tortuous high renal veins may pass by the adrenal area and simulate an adrenal lesion. Careful examination with real-time scanning will show the lesion to be tubular in nature and to connect to the inferior vena cava superiorly and renal hilum inferiorly. Enlarged para-aortic, paracaval, or retropancreatic nodes may also simulate an adrenal mass. Differentiation depends on the demonstration of a normal adrenal gland clearly separate from the mass. ACKNOWLEDGMENT I thank Louisa Haigler and Gilbert Zakow for preparation of the manuscript.
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