S INCE the first reports of Holmes, #{176} Lehman, 3 and Freimanis et al.,5 the abdominal echographic investigation has been

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1 VoL. 125, No. i HEPATIC ECHOGRAPHY* ABSTRACT: By GUY HEBERT, M.D., and CLAUDE GELINAS, M.D. MONTREAL, QUEBEC, CANADA There are 2 kinds of echographic investigations: those which are only complementary and those which are specific by themselves. To improve this latter category, we would like to emphasize two useful echographic signs. First, the attenuation sign, which indicates the fibrotic nature, therefore practically speaking, the cirrhotic nature of a diffuse echogenic pattern. Secondly, the posterior echo accumulation sign, which indicates the liquid nature, and therefore in general the cystic nature of a localized sonolucent pattern. S INCE the first reports of Holmes, #{176} Lehman, 3 and Freimanis et al.,5 the abdominal echographic investigation has been gradually accepted as a valuable diagnostic method. However, there are relatively few publications pertaining to upper abdominal lesions. We have found that the echographic investigation of the liver is usually a complementary study, but that it may sometimes be very specific and quite diagnostic by itself. METHOD The examinations are performed with a 2 mhz transducer, embedded in a contact scanner. The patient needs no special preparation, and lies in a supine position. His abdomen is covered with an oily material to assure proper sonic transmission. The views are recorded while the patient holds his breath in deep inspiration, to avoid superimposition of ribs, as much as possible. Sometimes, subcostal views with a cephalad angled probe may be necessary. THE NORMAL LIVER The normal liver is an echo-free structure, at low to moderate sensitivity levels, and it becomes echogenic only at high sensitivity levels. In other words, a normal liver is sonolucent at usual sensitivity levels (Fig. i). This anechoic character comes from the fact that the normal liver parenchyma is homogeneous, so it harbors almost no interfaces reflecting echoes. The only exceptions, at usual sensitivity levels, to this anechoic character come from the capsule and the hilus, which structures constitute highly reflecting interfaces. THE PATHOLOGIC LIVER Cirrhosis. The outstanding characteristic of a cirrhotic liver is its great echogenicity, even at low sensitivity levels (Fig. 2). This occurs because such a partially necrotic and partially regenerating liver is no longer homogeneous but contains many interfaces for reflection. A further characteristic of a cirrhotic liver is the miliary phenomenon (Fig. 2), FIG. I. Transverse section of a normal liver, at moderate sensitivity. The liver is seen as an anechoic area. The only exceptions are the capsule at the periphery and the hilus (arrow) centrally, in front of the vertebral column (V). * From the Department of Radiology, Notre-Dame Hospital, Montreai, Quebec, canada. 5

2 52 Guy H#{233}bert and Claude G#{233}linas SEPTEMBER, 1975 FIG. 2. Transverse section of a cirrhotic liver, at low sensitivity. The liver is now seen as an echogenic area, and the echoes are diffusely scattered. where the echoes recorded are fine and diffusely scattered, without any tendency for particular grouping. The explanation of this miliary phenomenon is simply the generalized aspect of the cirrhotic process. The cirrhotic liver may display a third sign, the ascitic sign. This is seen as an absolutely sonolucent area anteroinferior to the liver (Fig. 3), even at high sensitivity, representing fluid which has no interfaces to reflect the ultrasound beam. Such a sonolucent ascitic area must be distinguished from the sonolucent band very often seen coming from the subcutaneous fat. The distinction is easily made by considering these 3 criteria: (i) The ascitic absolutely sonolucent area (A) anteroinferior to the liver tip (arrow) represents the ascites (caudal is left). band is absolutely sonolucent, while the subcutaneous fat band becomes echogenic at high sensitivity (Fig., A and B). (2) In the dorsal recumbent position, the ascitic band widens inferiorly, while the subcutaneous fat band maintains its width (Fig., A and B). (3) The width of an ascitic band will vary according to the patient s position, while the width of a subcutaneous fat band will not change (Fig. 5, 1 and B). Finally, there is another possible sign with cirrhosis, the attenuation sign. This sign, when present, means that the echoes are found mostly in the superficial parts of the liver, while the deepest portions seem to be less echogenic (Fig. 6, A and B). This has a double explanation. First, the great heterogeneity of cirrhotic livers, by creating FIG. 4. Transverse sections of an ascitic abdomen, in dorsal recumbent position, at low (A) and high (B)sensitivity, displaying both the subcutaneous fat hand (1) and an ascitic area (A). In contrast to the subcutaneous fat band, the ascitic area widens infetiorly and resists the gain increase.

3 VOL. 125, No. Hepatic Echography 53 many reflecting interfaces, prevents good transmission of the beam toward the deepest portions. Secondly, the fibrosis of advanced cirrhosis greatly absorbs the beam and also prevents good transmission of the beam toward the deepest portions. Thus, the attenuation sign, being partially due to fibrosis, is a sign of severity, and when present means that we are dealing with an advanced stage of cirrhosis. Myeloid Metaplasia. The echographi c appearance of this infrequent liver disease resembles mild cirrhosis with no fibrosis. Thus, the echographic signs are a great echogenicity and a miliary phenomenon, but a negative attenuation sign (Fig. 7). The great echogenicity again comes from the heterogeneity of the liver, where hematopoietic foci give many reflecting interfaces, seen even at low sensitivity. The FIG.. Transverse sections of an ascitic abdomen in left posterior oblique recumbent ( 1) and right posterior oblique recumbent (B) positions. These sections display that ascites (A), in contrast to the subcutaneous fat band (F), is mobile. I FIG. 6. Transverse sections of a cirrhotic liver in dorsal recumbent (A) and right posterior oblique recumbent (B) positions. The sonolucent band at the periphery represents subcutaneous fat: it does not widen inferiorly and does not shift. The liver itself displays a positive attenuation sign: the deepest portions seem to be less echogenic than the superficial. miliary phenomenon is again due to the generalized aspect of the process. Finally, the negative attenuation sign means that the deepest parts are easily explored by the ultrasound beam, even at low sensitivity. This is mainly explained by the low density of such a nonfibrosing process, therefore less absorbing for the ultrasound energy which easily reaches and discloses the echogenicity of the deepest portions. Liver Carcinomatosis. In liver carcinomatosis, there are two kinds of echographic patterns: the miliary and the nodular. The first consists of many diffusely scattered echoes and corresponds to an extensive involvement (Fig. 8). Unfortunately, this pattern is not specific and resembles the

4 54 Guy H#{233}bertand Claude G#{233}linas SEPTEMBER, 1975 Fi. 7. 1rL... e echo Jc sect.on or a ir myeloid metaplasia. 1 pattern is echogenic and miliary. The attenuation sign is negative: the echoes are found equally in the superficial and in the deep portions of the liver (V: vertebra). one we have seen for cirrhosis and myeloid metaplasia. The second pattern for carcinomatosis is nodular where the echoes are no longer diffusely scattered, but show a tendency for particular groupings. Two kinds of nodule can be seen. The first is echogenic, seen as a localized accumulation of echoes (Fig. 9, 4 and B). This pattern is obtained from heterogeneous metastasis which, being necrotic, contains many interfaces reflecting the ultrasounds. The second kind of metastatic nodule is FIG. 8. Transverse section of a metastatic liver, showing the miliary pattern of carcinomatosis: the pattern is echogenic, and the echoes are diffusely scattered (V: vertebra). sonolucent and appears as a ringlike structure. This ringlike pattern is produced by metastasis, the texture of which is rather homogeneous, so that there are almost no interfaces reflecting the ultrasound in echoes (Fig. ro). Such a ringlike pattern for metastasis must be differentiated from simple cystic disease. This is done by increasing the gain setting. When the gain is increased, the ringlike patterns produced by metastasis gradually fill in with echoes, while fluid-filled cysts, which are homogeneous, resist a gain increase. This is shown in Figure u. Hepatoma. The echographic appearance of this disease is shown in Figure W - T I. + rfh. #{149}2.. FIG. 9. (A) Transverse section of a liver with metastases showing the echogenic nodular pattern of carcinomatosis: the lesions (arrows) are spontaneously seen, at low sensitivity, as localized accumulations of echoes (V: vertebra). (B) Longitudinal section showing the echogenic nodular pattern of carcinomatosis: the lesions (arrows) are spontaneously seen again as localized accumulations of echoes (C: caudal end).

5 VOL. 125, No. Hepatic Echography 55 Hepatoma presents as an echogenic mass with ill-defined contours. The echogenicity is due to its necrotic and hemorrhagic characteristics producing many reflecting interfaces, while the ill-defined contours are a manifestation of the invading aspect of such a pathology. Multicystic Liver. The echographic picture of any cystic process rests on 3 signs. The first is a great sonolucency. Cysts are anechoic structures, even when the gain setting is increased (Fig. 13). This sonolucency comes from the fact that the liquid content gives to cysts a homogeneous, interface-free, internal structure. The second echographic sign is a sharp boundary. Cysts have typical, precise contours which come from the great impedance difference between their walls and the surrounding tissues on the one hand and their fluid content on the other hand (Fig. 13). Finally, cysts classically display a positive posterior echo accumulation sign. The latter is explained by the fact that liquids, as opposed to solids, do not attenuate the ultrasound beam. Thus the beam is strongly reflected by the interfaces beyond the cyst (Fig. 13 and 14). DIFFERENTIAL ECHOGRAPHIC APPROACH FIG. 10. Transverse section of a metastatic liver showing the sonolucent nodular pattern of carcinomatosis: the lesions appear as ringlike areas (arrows) particulatly in the pre-aortic area (A: aorta, V: vertebra). By utilizing all the signs described prej r -%. FIG. II. When the gain is increased (upper section), the ringlike patterns coming from metastasis do not keep their sonolucency, while the ringlike pattern coming from the aorta (a), a fluid filled structure, resists and keeps its sonolucency. viously, it is possible to build a synthetic differential echographic approach to the liver pathology. For this approach, we simply divide the echographic patterns into diffuse or localized, and each of these patterns may be echogenic or sonolucent. This creates 4 categories. Diffuse Echogenic Presentation. In this first category (Table i), the type of distribution is important. If it is nodular, it means that the diffuse heterogeneous involvement we are dealing with is coarse, and in these circumstances, carcinomatosis must be considered. On the other hand, if the diffuse heterogeneous involvement is of the miliary type, we are left with many possibilities including cirrhosis, extensive

6 Guy H#{233}bert and Claude G#{233}linas SEPTEMBER, 1975 heads) with ill-definedcontours (C: caudal end). carcinomatosis, hepatitis, storage diseases, and myeloid metaplasia. But these numerous possibilities can be divided into 2 FIG. 13. Transverse sections of a huge simple biliary cyst. The sonolucency resists the gain increase (upper section). Its contours are sharp. There is a positive posterior echo accumulation sign (A). groups by the useful attenuation sign, which, when positive, indicates fibrosis, and circumscribes the diagnosis strongly in favor of moderate to advanced cirrhosis. Diffuse Initially Sonolucent (ring/ike) Presentation. In this second category (Table we consider whether the ringlike structures we have represent homogeneous or only pseudohomogeneous lesions. This is done by increasing the gain. If the ringlike patterns do not persist, the lesions are only pseudohomogeneous, and carcinomatosis is to be considered. On the other hand, if the ringlike patterns resist a gain increase we have true homogeneous lesions, and a multicystic liver disease is present. Localized Echogenic Presentation. In this third category (Table ii), we are dealing with a single heterogeneous process. Such a presentation is, in most instances, a malignant one, and represents either a hepatoma or a single necrotic metastasis. Localized Initially Sonolucent (ring/ike) Presentation. In this last category (Table ii), we determine if the initial sonolucency resists a gain increase. If it does not, then the localized lesion is a pseudohomogeneous one, and we consider either an abscess with necrotic fragments or a single metastasis. On the other hand, if the initial sonolucency remains despite a gain increase, we can conclude that the lesion is truly homo- FIG. I4. Subcostal oblique section of a multicystic liver, at high sensitivity, illustrating 2 cysts (arrows) appearing as absolutely sonolucent areas, with echoes accumulating posteriorly.

7 VOL. 125, No. i Hepatic Echography 57 TABLE I DIFFUSE PATTERNS Diffuse Pattern Echogenic Initially Sonolucent geneous, and is, for practical purposes, Miliary Nodular liquid. But a further test is available, and we use the posterior echo accumulation sign to discriminate between a liquid lesion and a homogeneous solid lesion. If this last sign is negative, that is, if there is no echo accumulation posteriorly, it means that the very homogeneous lesion we are dealing with is also an absorbing one Filling in with Echoes with Sensitivity Increase - Remaining Sonolucent with Sensitivity Increase - Positive Attenuation Sign Negative Attenuation Sign Advanced Congenital Mild Cirrhosis Carcinomatosis Hepatitis Storage Disease Myeloid Metaplasia -+ Carcinomatosis Carcinomatosis Multicystic Cirrhosis Fibrosis Liver for the beam, and thus a solid one. The diagnosis to propose in this instance is a homogeneous and solid lesion such as an adenoma or a fibroma. On the other hand, if the posterior echo accumulation sign is positive, that is, if there is echo accumulation posteriorly, it means that the homogeneous lesion we are dealing with is also nonabsorbing for the beam, and thus liquid.

8 Guy H#{233}bert and Claude G#{233}linas SEPTEMBER, 1975 LOCALIZED TABLE II PATTERNS Localized Pattern Echogenic Initially Sonolucent Filling in with Echoes with Sensitivity Increase Remaining Sonolucent with Sensitivity Increase The diagnosis is then a fluid filled cystic lesion. Guy H#{233}bert, M.D. Notre-Dame Hospital 1560 Sherbrooke East Montreal H2L 4Mi Quebec, Canada REFERENCES I. BECKER, J. C. Ultrasonic sym7tomatology of liver diseases. 7. de radio/., d #{233}lectro/.ci de med. nuc/caire, 1972, 53, 74I CHARBONNIER, A. Differential diagnosis of solid liquid tumors of liver by ultrasonic B echotomography. Arch. Fr. Mal. App. Dig., 1971, #{243}o, COHEN, W. N. B-scan ultrasonography of abdominal mass lesions. Radiology, 1969, 93, I. 4. DAMASCELLI, B. Two-dimensional ultrasound in liver diseases. 7.A.M.A., 1968, 204, Negative Posterior Echo Accumulation Sign Positive Posterior Echo Accumulation Sign Hepatoma Single Necrotic Metastasis Abscess With Necrotic Fragments Single Rather Homogeneous Metastasis Adenoma Fibroma. FREIMANIS, A. K., and ASHER, W. M. Development of diagnostic criteria in echographic study of abdominal lesions. AM. J. ROENT- GENOL., RAD. THERAPY & NUCLEAR MED., 1970, 108, GOLDBERG, B. B. Evaluation of ascites by ultrasound. Radiology, I970, 96, GOTTLIEB, S. Quantitation of hepatic abscess by A-mode ultrasound: report of case. Ann. Surg., 1972, 38, GRos, C. Echography and liver pathology. 7. de radiol., d #{233}lectrol. ci de med. nucl#{233}aire, 1972,53, HOLM, H. H. Ultrasonic scanning in diagnosis of space-occupying lesions of upper abdomen. Brit. 7. Radiol., 1971, 44, HOLMES, J. H. Ultrasonic diagnosis of liver diseases. Diagnostic Ultrasound, 1965, II. HOWRY, D. H. Brief atlas of diagnostic ultrasonic radiologic results. Radiol. C/in. North America, I965, 3, I2. IGAWA, K. I. Use of scintillation and ultrasonic

9 VOL. 125, No. Hepatic Echography 59 scanning to disclose polycystic kidneys and liver. 7. Urol., 1972, zo8, LEHMAN, J. S. Ultrasound in diagnosis of hepatobiliary disease. Radio/. C/in. North America, 1966, 4, 6o MATHEWS, A. W. Use of combined ultrasonic and isotope scanning in diagnosis of amoebic liver disease. Gut, 1973, 14, MCCARTHY, C. F. Comparison of ultrasonic and isotope scanning in diagnosis of liver disease. Brit. 7. Radio/., 1970, 43, i6. MCCARTHY, C. F. Use of ultrasound in diagnosis of cystic lesions of liver and upper abdomen and in detection of ascites. Gut, 1969, JO, MELKI, G. Hepatic and pancreatic investigation using contact echotomography. Ann. Radio/., 1972, 15, i8. MONROE, L. S. Ultrasonic scan in management of amebic hepatic abscess. Am. 7. Digest. Dis., 1971, i6, MOUNTFORD, R. A. Quantitative analysis of ultrasonic liver scan. Gut, 1971, 12, RASMUSSEN, S. N. Liver volume determination by ultrasonic scanning. Brit. 7. Radiol., 1972, 45, WEILL, F. Tomoechographic exploration of liver. 7. de radio/., d #{233}lectro/. ci de mid. nuc/iaire, 1971, 52, WEILL, F. Tomoechographic hepato-biliary elementary semiology. Ann. Radio/., 1970, 13, , 23. WELLS, P. N. Comparison of A-scan and compound B-scan ultrasonography in diagnosis of liver disease. Brit. 7. Radio/., 1969, 42,

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