Ultrasonography

Gastroenterol Clin N Am 31 (2002) 801–825

Ultrasonography Philip W. Ralls, MDa,b,*, R. Brooke Jeffrey, Jr., MDc, Robert A. Kane, MDd,e, Michelle Robbin, MDf a

Keck School of Medicine, University of Southern California b LACþUSC Medical Center c Stanford University Medical Center d Harvard Medical School e Beth Israel Deaconess Medical Center f University of Alabama, Birmingham Medical Center

Diagnostic sonography, considered by some to be a ‘‘mature’’ technology in the late 1980s, is experiencing a breath-taking period of technological advancement. Current systems make use of sophisticated technology to produce high-resolution pictures incorporating anatomy, pathology, and colorcoded blood flow, all visible in a single moving real-time image. Diagnostic sonography’s ability to image flow and soft tissue in real-time is unique among imaging techniques. Contrast agents, tissue harmonics, and advances in computer hardware and software guarantee decades of clinical progress in diagnostic ultrasound. New, capable handheld instruments, if their use is implemented properly, will revolutionize medical practice by becoming an integral part of initial evaluation by virtually all physicians. When sonography can image the area of clinical interest, it is a near ideal modality. It is safe and tolerated well by patients. Its routine spatial resolution is superior to computed tomography (CT) and magnetic resonance imaging. When needed, ultrasound can be performed quickly and at the bedside. Unfortunately, patient factors and physical limitations reduce the usefulness of sonography. It is difficult to scan extremely obese patients and those with limited cutaneous access (eg, burns, incisions, enterostomies). Sonography’s most serious disadvantage is its inability to see beyond gas and bone/soft tissue interfaces. This often makes comprehensive survey scanning impossible. Computed tomography especially, and MRI are much better survey modalities. Lastly, sonography is technically challenging; scanning to obtain optimally diagnostic images is more of an art than a science. Producing acceptable diagnostic images sonographically is usually harder * Corresponding author. 0889-8553/02/$ – see front matter Ó 2002, Elsevier Science (USA). All rights reserved. PII: S 0 8 8 9 - 8 5 5 3 ( 0 2 ) 0 0 0 3 0 - 4

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than obtaining acceptable CT or MRI images. Sonography is, however, often superior to CT and MRI in uncooperative patients who are unable to hold their breath, or unable to remain still during examination. Sonography is often superior in patients with little body fat; this makes sonography very useful in pediatric imaging, for example. Who should perform ultrasound? Diagnostic sonography is complex and technically challenging. True expertise requires knowledge of physics, instrumentation, ultrasound anatomy, pathology and, most important, scanning technique. In the United States, radiologists perform most high quality ultrasound examinations; cardiologists, obstetricians, and a few vascular surgeons and ophthalmologists working in their area of expertise also utilize it. In Asia and Europe, many nonradiologists, including gastroenterologists and surgeons, use sonography effectively, but those individuals complete extensive training, generally as a substantial and integral part of their specialty training. Small handheld scanners make the concept of sonography as an extension of the physical examination a real possibility, one that has the promise of significantly enhancing routine clinical diagnosis. Unfortunately, because of the complexity of diagnostic ultrasound, this goal will not be as easy to achieve as some believe. Those wishing to use sonography as a stand-alone diagnostic tool (‘‘high quality’’ sonography) have a responsibility to learn the technique comprehensively; this is a process that takes years of training and experience. Otherwise, erroneous, even catastrophic, results are inevitable. Alternatively, using sonography as a screening tool to enhance clinical diagnosis during initial evaluation has the potential to revolutionize medicine. Screening sonography has the potential to optimize efficient referral for further imaging and evaluation. After screening, referral might be to other imaging (eg, high quality diagnostic ultrasound, CT, or MRI). Appropriate training for screening ultrasound should be an integral part of medical student education. Optimal use of screening ultrasound requires that there be no separate reimbursement for screening ultrasound, analogous to the use of a stethoscope. Doppler sonography Doppler adds dynamic, real-time flow information to the morphologic images provided by grayscale imaging. Color Doppler sonography (CDS) simultaneously displays flow and anatomical information on a real-time ‘‘motion picture.’’ Spectral Doppler acquires detailed flow information from a small area (the sample volume). In many situations, color Doppler sonography is first used to survey a vessel to facilitate fast and accurate spectral Doppler sample volume placement, when quantitative information is needed.

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Ultrasound contrast agents Most ultrasound contrast agents are intravenously injected microbubbles. Although not used widely in the United States because of lack of FDA approval, significant contrast research and daily clinical use are occurring worldwide. Ultrasound contrast agents improve the information content of ultrasound, just like contrast use in CT and MRI. Clearly, no body would consider performing hepatic CT or MRI without contrast enhancement. Ultrasound contrast examination of the liver may, likewise, increase diagnostic confidence and decrease the need for further diagnostic or correlative imaging. Use of ultrasound contrast agents has the potential to expand ultrasound’s current role into diagnosis of conditions where CT, MRI, and nuclear medicine are currently dominant.

Liver Hepatic sonography’s main strengths are its ability to characterize common benign lesions (cysts, hemangiomas) and guide percutaneous procedures. Primary indications for liver sonography include diffuse liver disease, liver abscess, liver tumor, vascular abnormalities, and transplantation. Sonography can also be used to characterize abnormalities found on CT or MRI. Ultrasound contrast agents may improve both lesion detection and characterization. Sonography’s ability to image in any oblique plane often makes it superior to CT and MRI in localizing lesions to an anatomical hepatic segment when evaluating resectability of a liver tumor. Diffuse liver disease Diffuse liver disease does not always cause distortion of liver anatomy or architecture. Liver surface nodularity or atrophy of the right lobe, when present, can be symptoms of cirrhosis. Parenchymal echogenicity may be increased in fatty infiltration, but no quantitative method to assess echogenicity exists. Liver echogenicity is judged by comparison with adjacent organs such as the kidney or pancreas. Hepatomegaly can be difficult to diagnose objectively with sonography. If the sagittal dimension from the dome to the tip of the right lobe (measured at the midclavicular line) exceeds 15.5 cm, the liver is probably enlarged [1]. Hepatomegaly can be confidently diagnosed when the liver extends caudal to the right kidney and the left lobe is of normal size or larger. The liver is generally normal in patients with acute viral hepatitis. Although increased periportal echoes coupled with decreased parenchymal echogenicity have been described [2], in another series, only 19 of 791 patients had this pattern [3]. In the same study, there was no difference in ultrasound findings between a normal control group and patients with acute viral hepatitis. Striking irregular gallbladder wall thickening, sometimes

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reaching 20 mm (normal wall <3 mm), may be present in patients with acute hepatitis, especially hepatitis A [4]. Hepatomegaly and inhomogeneous patchy or diffuse increased echogenicity are common in patients with chronic active hepatitis and are related to the amount of fatty infiltration and fibrosis present. The liver surface is smooth, unless cirrhosis is also present. Severe fatty infiltration may cause hepatomegaly with diffuse increased echogenicity decreased acoustic penetration, and indistinctness of the diaphragm and vessels (Fig. 1). Most diffusely fatty livers, however, have a higher echogenicity without the other findings. The liver surface is smooth. Fatty infiltration is often patchy or focal. ‘‘Geographic’’ fatty infiltration typically has well-defined margins separating lobes or segments with greater and lesser involvement. Focal fat appears as an area of increased echogenicity. A less affected region (‘‘spared’’ area) may appear as a conspicuous hypoechoic area. While both can simulate neoplasm [5], an appreciation of the usual appearance and location generally suffices to avoid confusion. Common locations for focal fat and sparing include anterior to the porta hepatis, near the falciform ligament, and the dorsal lateral segment of the left lobe. In cirrhosis, sonography detects changes in the shape of the liver, parenchymal inhomogeneity, and nodularity of the liver surface. Intrahepatic vessels may be indistinct. Unequivocal surface nodularity or a small right lobe with left and caudate lobe hypertrophy [6] are quite predictive of cirrhosis, but are not always present [7]. Surface nodularity may be the only sonographic sign of cirrhosis [8,9]. The specificity for macronodular cirrhosis is good (Fig. 2), but micronodular cirrhosis is often missed (poor sensitivity).

Fig. 1. Heavily steatotic livers can significantly attenuate sound, as in this instance. Note that the liver parenchyma at depth [adjacent to the right kidney (K)] is poorly seen. Vessels in the deeper portion of the liver are not identified. Most fatty livers do not attenuate sound to the point that it is noticeable on images.

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Fig. 2. Finding a nodular liver surface is quite specific for the diagnosis of hepatic cirrhosis. Sensitivity is less good because micronodular cirrhosis (with nodules less than 1 mm in size) is generally not identified. Here, nodularity is noted with a modern curved linear transducer. Ascites (A) facilitates visualization of the surface nodularity. Diffuse parenchymal nodularity is present.

The other significant cause of surface nodularity is multiple subcapsular tumor nodules, usually from metastasis. Color Doppler sonography may detect portal vein flow reversal or portal collaterals, prompting the diagnosis of portal hypertension. Enlarged tortuous arteries (‘‘corkscrew’’ arteries) are sometimes imaged by color Doppler sonography in cirrhotic livers [10], probably related to the increased arterial flow that occurs when portal venous flow decreases. Diagnosis of portal hypertension includes evaluation of the portal venous system and a search for portosystemic collaterals. Although absolute portal vein diameter (normally about 1 cm) is not useful in diagnosing portal hypertension, lack of respiratory variation in portal vein (PV) size may be useful in diagnosing portal hypertension [11]. Other portal flow abnormalities include bi-directional flow and, rarely, nearly static blood flow. Detection of portal collaterals may prompt diagnosis of unsuspected portal hypertension, or reinforce it when suspected. Portal collaterals should be sought with color Doppler sonography, as they are often invisible on grayscale images. The most commonly visualized collaterals are left gastric (coronary) and paraumbilical veins. Other types of portal collaterals occur, including retroperitoneal, splenorenal, splenoretroperitoneal, short gastric, and omental. A liver mass in a patient with cirrhosis should suggest the possibility of hepatocellular carcinoma (HCC). Focal fatty infiltration, regenerating nodules (adenomatous hyperplastic nodule), and other focal lesions may occur in a cirrhotic liver.

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Therapeutic portosystemic shunts Color Doppler sonography often displays surgical shunts [12], even when they are inapparent on preliminary grayscale images. Transjugular intrahepatic portosystemic shunt stents can be evaluated by spectral and color flow Doppler before, after, and sometimes during the procedure. Venous thrombosis Intraluminal echoes in veins suggest the presence of clot, but color Doppler is necessary to confirm the diagnosis. When hypoechoic or anechoic, the clot may be virtually invisible without color Doppler. Anechoic thrombus is rare in neoplastic invasion but is fairly common with bland clot. Color Doppler sonography highlights the clot by displaying flow around the clot and in adjacent patent vessels [10]. Color Doppler sonography is unrivaled in diagnosing partially occluded vessels. Small residual flow channels are automatically displayed in color. Contrast agents may be useful in difficult cases. Portal venous thrombosis can result from neoplastic invasion, septic portal thrombosis (pylephlebitis), and pancreatitis. We believe that thrombosis in portal hypertensive patients is considerably more common than the 1% previously reported [13]. Cavernous transformation of the portal vein, resulting from main portal vein clot, consists of prominent hepatopedal portal collaterals. In acute portal vein thrombosis, color Doppler sonography may reveal small, acute hepatopedal portal collaterals, invisible on gray-scale sonography. Budd-Chiari syndrome The Budd-Chiari syndrome is characterized by obstruction or severe stenosis of the hepatic vein (HV), and sometimes stenosis or obstruction of the IVC. Obstruction may be primary, caused by webs or membranous obstruction of the inferior vena cava (IVC) [14], or secondary, caused by hypercoaguable conditions, trauma, neoplasm, medications, pregnancy, and other conditions. Sonography, especially with color Doppler imaging, is the preferred screening technique [15]. Gray-scale findings include HV abnormalities such as absence, stenosis, dilation, irregularity, and abnormal or absent junction with the IVC. The IVC may itself be occluded or stenosed. Less specific changes include caudate hypertrophy and atrophy/enlargement of the other lobes and segments, and parenchymal inhomogeneity. Absent or reversed hepatic venous flow and intrahepatic HV to HV ‘‘spider web’’ collaterals are diagnostic of Budd-Chiari syndrome. A flat HV waveform, lacking the normal phasic fluctuation, indicates HV compression, a finding that, while nonspecific, supports the diagnosis of Budd-Chiari syndrome. Other collaterals seen in Budd-Chiari syndrome include HV to portal vein collaterals with portosystemic shunting (eg, via enlarged paraumbilical veins, esophageal varices) and HV to systemic veins.

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Focal liver disease No standard, noninvasive imaging modality is truly sensitive in detecting focal hepatic disease. Focal hepatic lesions are frequently missed with one modality, then detected with another. While less sensitive than CT and MRI, modern sonography can perform well in detecting focal liver disease [16,17]. Evidence suggests that ultrasound contrast agents can increase detection and improve characterization of focal liver lesions . Sonography’s main advantages are its abilities to guide biopsy and characterize common benign lesions (cysts, hemangiomas), its safety, and its low cost. Its disadvantages include its inability to image the entire liver in some patients and its inferiority to CT in detecting extrahepatic disease. Sonography may be used to evaluate resectability of primary or metastatic liver tumors. Color Doppler sonography improves detection of focal lesions, especially anechoic or hypoechoic lesions. Some tumors are more conspicuous because of increased flow compared with normal liver including: focal nodular hyperplasia (FNH), most HCCs, some metastases, and occasionally other masses [18,19]. Color and spectral Doppler can be used to help discriminate among benign and various types of malignant liver tumors [18,20]. Cystic disease of the liver Sonography is usually superior to CT or MRI for evaluating cysts. Simple cysts are usually well-defined, echo-free, round or oval lesions with imperceptible walls and good through transmission. Thin septations are frequent, and should not suggest a different diagnosis. Thicker septations are generally a sign of a complicated cyst or of a cystic neoplasm. Biliary cystadenoma is a rare neoplasm arising from bile duct epithelium. These lesions have thick septae and varying amounts of solid tissue [21]. Multiple liver cysts, varying in number and size characterize hepatic polycystic disease. About one-half of patients have renal cysts. Sonographic findings include multiple, often contiguous simple cysts. Irregular shape and septae are common. Hemorrhage or infection may cause debris-like echoes within one or more cysts. Von Meyenburg complex is a rare, clinically insignificant disorder characterized by multiple small cystic hamartomas of the bile ducts that may be detected with CT or sonography. Acquired cysts may occur as a result of trauma or infection [22,23]. Neoplasms that simulate simple cysts are unusual; metastases from squamous cell carcinoma and gastrointestinal stromal tumors occasionally appear purely cystic. The liver is the most frequently involved organ in hydatid (echinococcal) disease. A spectrum of sonographic findings from purely cystic to solid-appearing pseudotumors occurs. Internally, wavy bands of delaminated endocyst (the ‘‘water lily’’ sign) may be noted [24]. Daughter cysts, sometimes surrounded by echogenic debris (‘‘matrix’’) are frequent. Calcifications, varying from tiny to massive, are often present.

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Liver abscess When liver abscess is suspected clinically, sonography is the preferred screening modality. Sonographically, pyogenic liver abscesses have a variable appearance (Fig. 3). Typical features include irregular margins and a primarily hypoechoic mass. Irregular areas of increased echogenicity are frequent. On occasion, a diffusely hyperechoic appearance may be noted, owing to microbubbles from gas-forming organisms. Diffuse microabscesses, often associated with biliary obstruction, may cause a confusing sonographic pattern of increased, irregular hepatic echogenicity. Septic portal venous thrombosis (pylephlebitis) may lead to liver abscess [25]. Amebic liver abscesses tend to have a round or oval shape and hypoechoic appearance with fine, homogeneous, low-level echoes throughout. Image findings alone are rarely sufficient to distinguish amebic from pyogenic liver abscesses [26]. When it is unclear if an abscess is amebic or pyogenic, percutaneous diagnostic aspiration should be performed. In contrast to pyogenic liver abscesses, percutaneous drainage or therapeutic aspiration of amebic liver abscess is rarely indicated [27,28]. Benign neoplasms Cavernous hemangioma, the most common benign hepatic neoplasm (prevalence 1%–4%), rarely causes clinical symptoms. Small hemangiomas are usually well-defined, echogenic lesions with enhanced through transmission (Fig. 4) [29]. Larger hemangiomas frequently diverge from this pattern,

Fig. 3. This is a typical pyogenic liver abscess, poorly defined margins with mixed, predominantly hypoechoic echogenicity. Note the small brighter areas (arrows) that represent small gas bubbles within the abscess. The organism was Klebsiella species.

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Fig. 4. This well-defined 2.0 by 3.0 cm lesion fulfills the classic sonographic criteria for hepatic hemangioma, diffuse increased echogenicity and well-defined margins separating the lesion from the normal liver. Fairly subtle through transmission (arrows) is noted, another feature of classic pattern hemangiomas.

with mixed echogenicity or even hypoechoic lesions. A thin, echogenic rim surrounded by normal liver should suggest that the lesion is an hemangioma. Small echogenic hemangiomas need no further evaluation, even in patients with malignancy. If confirmation of hemangioma is needed, CT, MRI, or blood pool scanning may be used. Preliminary results suggest that ultrasound contrast agents may allow confident diagnosis of hemangiomas with ultrasound. Focal nodular hyperplasia is a clinically insignificant lesion, while liver cell adenoma (LCA) can cause morbidity and mortality because of hemorrhage and, occasionally malignant degeneration. The sonographic features of FNH and LCA are variable. There is a tendency for FNH to be more homogeneous than LCA. Focal nodular hyperplasia often has mildly increased echogenicity compared with normal parenchyma, whereas LCAs are usually hypoechoic and more inhomogeneous [30,31]. On color flow imaging, FNH usually has markedly increased flow, sometimes with vessels radiating peripherally from a central feeding artery. Malignant neoplasms Hepatocellular carcinoma (HCC) is the most common primary liver cancer. Most HCCs occur in patients with cirrhosis or precirrhotic conditions. Advanced HCC is almost always multifocal, making it difficult to distinguish from metastatic disease. Small HCCs (<5 cm) are often (75%)

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hypoechoic. Hepatic or portal venous invasion should suggest the diagnosis of HCC (Fig. 5), although other liver tumors may invade veins. About 90% of HCCs have identifiable internal color flow (versus one third of metastases). Metastatic disease is multifocal in 90% of patients. Virtually any sonographic appearance may occur. Metastatic lesions, whether diffuse or focal, are usually heterogeneous and predominantly hypoechoic. Hypoechoic halos, target or bull’s eye patterns with rings of varying echogenicity are common. Ill-defined infiltration with focal nodularity is another frequent pattern (Fig. 6). Metastases that simulate simple cysts or ‘‘classic’’ hemangiomas are uncommon. Predominantly fluid-filled, presumably necrotic metastases occur most frequently with squamous cell carcinoma and gastrointestinal stromal tumor (GIST). Calcified lesions, especially mucinous adenocarcinoma, may occur. Hepatic lymphoma and leukemia are usually diffuse and microscopic. Only 5% of patients with hepatic lymphoma have focal lesions detected with sonography. The lesions are usually anechoic or hypoechoic, although other patterns occur [32]. Chloromas of the liver, associated with myelogenous leukemia, can be hypoechoic or echogenic. HIV-related lymphomas cause more frequent and conspicuous focal lesions than other lymphomas. Hepatic sarcomas are rare. Angiosarcomas and undifferentiated embryonal sarcoma are usually large, internally inhomogeneous masses [33]. Adenomatous hyperplastic nodules in cirrhotic livers (regenerating nodules) are premalignant lesions that, when visualized, are usually hypoechoic and may have a thin echogenic rim [34].

Fig. 5. This mixed pattern multifocal hepatocellular carcinoma is invading the hepatic vein (arrow). Venous invasion, while not unique to hepatocellular carcinoma, should suggest the diagnosis.

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Fig. 6. Hepatic metastasis has many patterns, ranging from multifocal mixed pattern disease (as seen here) to diffuse abnormality. Note that two of the nodules have anechoic areas suggestive of necrosis (arrows). These relatively well-defined metastatic nodules have areas of increased and decreased echogenicity.

Tumor ablation Sonography is useful in guiding tumor ablation. Ultrasound contrast enhancement may be useful in delineating residual liver tumor after tumor ablation. Intratumoral enhancement after percutaneous ethanol injection has been seen in 92% of patients with residual viable HCC on spiral CT. Viable tumor can be identified and targeted for retreatment with ultrasound contrast during or after ethanol or radio-frequency ablation.

Liver transplantation Before liver transplant, color Doppler sonography can be useful in delineating portal and hepatic venous anatomy, defining portal hypertension related collaterals, detecting portal vein clot, and detecting HCC in the native liver. After transplantation, sonography can screen for hepatic arterial occlusion [35]. Absent flow on color Doppler or decreased peripheral resistance, measured by resistive index [36] are signs of arterial compromise. The use of ultrasound contrast agents may improve the accuracy and speed of examination in transplant patients. When abnormalities are noted, arteriographic evaluation and intervention are often indicated. Because sonography misses 50% or more of bile duct complications [37], cholangiography is necessary to detect bile duct injuries. Posttransplant fluid collections include abscess, biloma, seroma, lymphocele, and hematoma.

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Gallbladder Sonography is the imaging method of choice for the initial evaluation of all suspected diseases of the gallbladder. It is particularly valuable in patients with acute, right upper quadrant pain and possible acute cholecystitis [38,39]. Sonography is highly reliably in detecting tiny gallstones and is useful for evaluating focal or diffuse abnormalities of the gallbladder wall [40]. Gallstone disease The characteristic sonographic appearance of gallstones is an intraluminal echogenic focus casting a distal acoustic shadow (Fig. 7). If it is difficult to document acoustic shadowing, small stones can be differentiated from polyps because stones move when the patient changes position. Gallbladder polyps are immobile, echogenic, mucosal lesions that do not shadow. Sludge within the gallbladder generally indicates lack of gallbladder emptying. At times, aggregated ‘‘tumefactive’’ sludge may mimic a mucosal mass. Gas within the gallbladder may be caused by surgically created biliary-enteric anastomoses, endoscopic biliary procedures, or gas-forming infection from emphysematous cholecystitis. Acute cholecystitis A reliable diagnosis of acute cholecystitis can be made in patients with fever, right upper quadrant (RUQ) pain, and leukocytosis when ultrasound reveals gallstones, plus either gallbladder wall thickening (3þ mm), or a positive sonographic Murphy sign [39,40]. Cholecystectomy cures 99% of patients with these findings. The sonographic Murphy sign is focal, reproducible tenderness directly when the transducer applies pressure over the

Fig. 7. This longitudinal image of the gallbladder shows a gallstone with characteristic acoustic shadowing (block arrow) in the neck of the gallbladder. In the correct clinical setting, gallbladder wall thickening with striations [anechoic areas within the wall (arrows)] suggests the diagnosis of gangrenous acute cholecystitis.

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gallbladder. Biliary scintigraphy should be performed in the 20% of patients who do not have these findings. Acalculous cholecystitis, which usually occurs in patients with trauma, major surgical procedures, hyperalimentation, burns, sepsis, and other severe illnesses, comprises 5% to10% of patients with acute cholecystitis [41]. Diagnosis is difficult. In the appropriate clinical setting, gallbladder wall thickening with a positive sonographic Murphy sign is suggestive of acute acalculous cholecystitis. Sonographic features that suggest gangrenous cholecystitis include abnormalities of the gallbladder wall and perforation. Mural abnormalities include gallbladder wall striations (hypoechoic bands of edema) (Fig. 7), intraluminal membranes (sloughed mucosa), and mural microabscesses. Perforation of the gallbladder with pericholecystic abscess is a major cause of sepsis and morbidity. Pericholecystic abscesses are complex fluid collections contiguous to the gallbladder; often the echogenic submucosa is interrupted. Echogenic, inflamed fat may be noted adjacent to the abscess. Gallbladder tumors Small gallbladder polyps [42] are often incidental findings that, when less than 5 mm in diameter, are of no cause for clinical concern. Enlarging polyps on serial sonograms or polyps greater than 1 cm in diameter are usually an indication for cholecystectomy because of the increased risk for carcinoma. The sonographic findings of gallbladder carcinoma are variable, ranging from polyps to focal or irregular thickening of the gallbladder wall, with an extracholecystic mass. Typically advanced at presentation, direct hepatic invasion, nodal metastases, and biliary obstruction are common. Adenomyomatosis and cholesterolosis are benign ‘‘hyperplastic cholecystoses’’ [42]. Cholesterolosis typically results in either single or multiple small mucosal nonadenomatous polyps. Adenomyomatosis causes either focal or diffuse hypertrophy of the normal Rokitansky-Aschoff sinuses and smooth muscle within the gallbladder wall. Crystals trapped within the hypertrophied sinuses may produce echogenic foci with echogenic ‘‘comettail’’ artifacts. Adenomyomatosis can cause masses and bizarre, irregular wall thickening.

Bile ducts Sonography’s ability to detect dilated bile ducts and the level of biliary obstruction makes it the technique of choice for evaluating jaundiced patients. Sonography can also detect the cause of obstruction, albeit with less sensitivity. Infectious cholangitis and conditions such as HIV cholangiopathy are indications for sonography. Color Doppler sonography can detect and assess resectability of cholangiocarcinoma and other tumors affecting the bile ducts.

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Bile duct obstruction Stones and tumors are the most common causes of bile duct obstruction. Benign strictures from pancreatitis and other causes are less frequent. Stones are the most common cause of distal bile duct obstruction. Tumors are a more frequent cause of proximal bile duct obstruction. Sonographically, dilated intrahepatic bile ducts are tubular, anechoic structures that demonstrate posterior acoustic enhancement. Centrally, in the porta hepatis, dilated ducts are usually ventral to the portal veins. The ‘‘too many tubes’’ sign is the classic pattern indicative of intrahepatic biliary dilation. Color Doppler is useful to distinguish veins and enlarged arteries from dilated bile ducts, simplifying detection of abnormal ducts and preventing misidentification of vessels as bile ducts. Surprisingly, ‘‘normal’’ bile duct size is controversial. Obstruction is rarely present when the extrahepatic bile duct is 5 mm or less in maximal internal diameter. Nondilated obstruction may be seen in cholangiocarcinoma or sclerosing cholangitis. Bile ducts with maximal internal diameters of 10 mm or more are almost always obstructed. In most patients, 6- to 9-mm ducts (‘‘gray zone’’ size ducts) are not obstructed, but are that size because of breakdown of the elastic fibers within the duct wall. Choledocholithiasis Choledocholithiasis occurs in at least 15% of patients with cholelithiasis; conversely, 95% of patients with common duct stones also have gallstones. A shadowing echogenic focus in the bile duct is virtually diagnostic of choledocholithiasis (Fig. 8). Potential pitfalls include the Mirizzi syndrome, air in the bile duct, extrabiliary calcifications, or surgical clips. Bile duct stones are harder to detect than gallstones, with optimal reported sensitivity of 75% to 80% [43]. Stones in normal sized ducts can be identified, but are harder to detect than stones in dilated ducts. Cholangitis In infectious cholangitis, diffuse bile duct wall thickening is often present [44], but normal studies may occur. Peribiliary ‘‘cholangitic abscesses’’ may occur. Recurrent pyogenic cholangitis (also known as Oriental cholangiohepatitis), is characterized by recurrent bacterial cholangitis promoted by strictures and primary bile duct stones that may occur in any part of the biliary tree. Massively dilated ducts (2þ cm) with sludge and large stones are common. Gallstones and liver abscesses are frequent. Sonography is the preferred initial imaging technique in patients with recurrent pyogenic cholangitis [45]. HIV-related cholangiopathy is a diffuse biliary tract disease, affecting the gallbladder and bile ducts. More than 80% of patients have alkaline phosphatase levels that are two times as high as normal, but bilirubin is often minimally elevated or even normal [46]. Sonography,

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Fig. 8. An echogenic shadowing focus within the extrahepatic bile duct is diagnostic of choledocholithiasis. Several stones (arrows) are seen within this dilated duct.

although less sensitive than endoscopic retrograde cholangiopancreatography (ERCP), is useful in evaluating patients suspected of having HIVrelated cholangiopathy [47]. Smooth or irregular thickening of the bile duct wall (45%) and biliary dilation (about 70%) are frequent abnormalities [47]. Striking thickening of the gallbladder wall with prominent wall striations suggestive of acute acalculous cholecystitis occasionally occur. Cholangiocarcinoma Primary bile duct tumor, cholangiocarcinoma, has two forms, peripheral cholangiocarcinoma and hilar cholangiocarcinoma (Klatskin tumor). Peripheral cholangiocarcinoma is usually a large tumor, whereas hilar cholangiocarcinoma presents earlier with ductal obstruction and jaundice. Cholangiocarcinoma often has subtle findings. It is usually hypoechoic (Fig. 9), but isoechoic and hyperechoic tumors may occur [48]. Color and spectral Doppler sonography are useful in determining if cholangiocarcinoma is resectable [49]. Biliary cystadenoma Biliary cystic neoplasms (formerly called biliary cystadenoma and cystadenocarcinoma) are rare. Lesion morphology ranges from completely cystic with a few, thin sepatations to cystic with thick septations and large amounts of internal soft tissue. Thick, sometimes papillary septations, and larger amounts of internal soft tissue characterize the mesenchymal variant, which has a greater potential for malignant behavior.

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Fig. 9. Most cholangiocarcinomas are hypoechoic, as seen here (MASS). This cholangiocarcinoma narrows and encases the portal vein (arrows), a sign of unresectability.

Other conditions Choledochal cysts Of the four main types of choledochal cysts, about 90% of cases involve dilation of the extrahepatic bile duct (Type I). Sonographically, there is obvious dilation of the extrahepatic duct, often associated with varying degrees of intrahepatic dilation. Dilation may be cystic (IA), focal (IB), or fusiform (IC). Other types include choledochal diverticula (Type II), choledochocele (Type III), and multiple intra- or extrahepatic cysts (Type IV). Caroli disease Caroli disease is cystic dilation of the intrahepatic bile ducts. Some cases are associated with a choledochal cyst (Todani Type 4A). Sonographically, multiple small cystic areas that may or may not appear to communicate with the unaffected bile ducts characterize Caroli disease. A central vessel identified with Doppler sonography supports the diagnosis.

Pancreas Although CT remains the most sensitive means of evaluating pancreatic disease, modern ultrasound technology and new scanning techniques (oral contrast, compression scanning) are reestablishing sonography as a useful and clinically relevant pancreatic imaging technique. Sonography is indicated in all patients with acute pancreatitis, not to evaluate the pancreas itself, but rather to detect gallstones and biliary dilation. Computed tomogra-

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phy is superior to sonography in the evaluation of potential complications of pancreatitis, but sonography may be used to follow pancreatitis-associated fluid collections and can guide biopsy, drainage, or aspiration of selected pancreatic lesions. Sonography is the primary imaging method to screen patients with jaundice or abdominal pain. Thus, sonography may detect acute or chronic pancreatitis or reveal pancreatic masses. Sonography may be more effective than CT in determining whether a lesion is pancreatic or contiguous to the pancreas. Sonography is occasionally useful to characterize abnormalities noted on CT, determining, for example, whether a lesion is cystic or solid. Acute pancreatitis Evaluation with sonography is mandatory for all patients, even alcoholics, during their first attack of acute pancreatitis. Sonography in patients with acute pancreatitis focuses on the gallbladder and bile ducts; the gallbladder for stones (as a cause of pancreatitis) and the bile duct for choledocholithiasis and obstruction. In our experience, more than 90% of patients with acute pancreatitis have sonographic abnormalities. Peripancreatic inflammation and parenchymal heterogeneity are more common than a hypoechoic pancreas (Fig. 10). Extrapancreatic abnormalities may allow sonographic diagnosis when acute pancreatitis is unsuspected clinically [50]. Acute fluid collections, pseudocysts, and abscesses may be imaged. Color and spectral

Fig. 10. Extra pancreatic abnormalities are more common than the classic finding of decreased echogenicity of the pancreas. This patient has extensive peripancreatic inflammation (small arrows) and glandular inhomogeneity manifested as areas of increased and decreased (block arrow) echogenicity.

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Doppler sonography may be useful in detecting pancreatitis-associated vascular complications, such as pseudoaneurysms and portal thrombosis. Chronic pancreatitis Image findings are poor predictors of the clinical severity of chronic pancreatitis, although patients with severe exocrine insufficiency are more likely to have abnormal pancreatic size and contour irregularity [51]. Multiple calcified stones located within the main or branch pancreatic ducts are the hallmark of chronic pancreatitis, usually alcohol related. Focal masses that can simulate neoplasm occur in about one-third of patients with chronic pancreatitis. Calcification within the mass is strongly suggestive, but not definitive, for chronic pancreatitis. Uncalcified isoechoic or hypoechoic masses may require ERCP or biopsy to exclude malignancy. The ‘‘double-duct sign’’ (dilation of pancreatic and bile ducts) may occur not only in pancreatic carcinoma but also in chronic pancreatitis [52]. Chronic asymptomatic pseudocysts may be found in patients with chronic pancreatitis. Neoplasms As sonography is used to screen patients with jaundice, it often detects pancreatic tumors. Sonography can characterize the internal architecture of masses, facilitating classification of neoplasms. Sonography occasionally detects pancreatic tumors when CT is normal [53]. Ductal adenocarcinoma Sonographically, pancreatic carcinoma is typically a hypoechoic mass that deforms the gland’s morphology (Fig. 11). Occasionally, pancreatic carcinoma is heterogeneous or echogenic. In about 5% of patients, scattered calcifications or cystic areas may [54]. Secondary findings of carcinoma include ductal dilation (biliary and pancreatic), vascular and extraglandular invasion, and metastatic disease. Pseudocysts, related to obstruction of a pancreatic duct, have been reported in as many as 11% of patients, although in our experience carcinoma-related pseudocysts are less frequent. It has been shown that color Doppler sonography can effectively assess resectability, specifically vascular involvement by tumor, with accuracy comparable to that of CT [55–57]. Cystic pancreatic lesions The most common cystic pancreatic neoplasms are the benign serous cystic neoplasm (microcystic adenoma), and the malignant mucinous cystic neoplasms [58]. Morphologically, microcystic adenomas comprise many

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Fig. 11. Typically, ductal adenocarcinoma deforms the shape of the gland and is a hypoechoic mass (M). Color Doppler sonography can be used to assess resectability. In this patient, the common hepatic artery (arrow, CHA) is encased by the hypoechoic mass. This is a sign of unresectability.

tiny cysts, although cysts as large as 2 cm may be seen. The most distinctive feature, present in about one-half of tumors, is a central radial fibrotic scar that frequently calcifies. Sonographically, microcystic adenomas are echogenic in regions where there are many tiny cysts. Through transmission is usual. Mucinous cystic neoplasms contain large cysts (Fig. 12), usually easily

Fig. 12. Mucinous cystic neoplasms are usually multilocular lesions, such as this. Note the thick internal septations, debris, and complex cystic and solid areas.

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imaged with CT or sonography. Unilocular lesions may occur. Septations may be few or many, quite thin or thick, and polypoid. Calcifications occur in approximately 20% of these neoplasms. Endocrine tumors It is difficult to image functional islet cell tumors; they are usually small when the patient presents with hormonal abnormalities. Insulinomas and gastrinomas are frequently less than 2 cm in diameter. In contrast, ‘‘nonfunctional’’ islet cell tumors can be large at the time of presentation. Sonographic detection rates of 25% to 60% for insulinomas have been reported. Sonographically, islet cell tumors are usually hypoechoic, well-defined, and round or oval in shape. Intraoperative sonography is useful in localizing occult neoplasms.

Gastrointestinal tract The most common indication for gastrointestinal tract sonography is evaluation of the patient with right lower quadrant pain and possible appendicitis. Sonography may also be useful in the diagnosis of diverticuli tis, small bowel obstruction, and bulky mesenteric or gastrointestinal neoplasms. Standard transducers cannot routinely visualize five discrete layers of the bowel shown by intraluminal probes [59], but standard transducers can resolve the echogenic submucosal layer. The submucosa serves to identify an intra-abdominal structure as a bowel loop. Pathologic processes that cause ulceration and necrosis of the bowel lead to either focal or global loss of visualization of the echogenic submucosa [60]. Primary neoplasms involving the bowel wall may result in focal bowel wall thickening referred to as the target sign or ‘‘pseudokidney’’ sign. Color Doppler sonography may be useful in evaluating patients with focal bowel wall thickening [61,62]. Increased arterial flow suggests inflammation or infection; diminished or absence flow suggests intramural hemorrhage, ischemia, or infarction. The vascularity of gastrointestinal tract tumors is variable, but in general, adenocarcinomas are typically hypovascular. Acute appendicitis In patients with an uncertain clinical diagnosis of appendicitis, sonography is preferred to CT in women of childbearing age, pediatric patients, and in thin patients. Computed tomography is preferred in patients who are obese or if appendiceal perforation is suspected. Sonographically, a noncompressible appendix measuring 7 mm or more in diameter is diagnostic of acute appendicitis (Fig. 13) [63]. An appendicolith generally indicates acute appendicitis regardless of the size of the appendix. In some patients,

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Fig. 13. This high-resolution graded compression ultrasound shows an appendicolith (labeled) in a noncompressible appendix that is 11 millimeters in external diameter. Both the diameter and the appendicolith are independently sufficient to diagnose acute appendicitis. The small abscess (labeled) was confirmed at surgery.

early acute appendicitis is confined to the distal tip of the appendix [64]. Enlarged mesenteric lymph nodes and a normal appendix are highly suggestive of mesenteric adenitis, which may also be associated thickening of the terminal ileum [65]. Diverticulitis In most patients, CT is the imaging method of choice to evaluate patients with possible sigmoid diverticulitis. Nevertheless, sonography may detect diverticulitis by showing focal mural thickening, echogenic mesenteric fat, and associated hyperemia on color Doppler imaging [66]. In some patients, peridiverticular abscesses maybe detected. Other conditions The sonographic findings of enteritis or colitis are often nonspecific, with CT being a preferred way to evaluate these patients. Typical findings include focal areas of mural thickening of the bowel, often with associated adjacent adenopathy. The affected segment is typically uncompressible. Occasionally, a fistula or sinus tract involving the mesentery may be identified, favoring the diagnosis of Crohn’s disease. In intestinal ischemia, thickening of the small bowel wall as a result of intramural hemorrhage or edema may be visualized as a noncompressible area of mural thickening [62,63]. Absence of vascular flow on power Doppler suggests the diagnosis of ischemia. In patients with palpable gastrointestinal tumors, sonography is often valuable in identifying the organ of origin. The pseudokidney sign may be present. On occasion, focal inflammatory or ischemic masses are

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indistinguishable from neoplasms on sonography. Endoscopy, barium studies, or CT are often required to establish a more precise diagnosis. Intraoperative sonography Intraoperative ultrasonography is an increasingly important and rapidly developing diagnostic imaging technique. It provides indispensable information that influences clinical management and choice of surgical procedure at the time of surgery [67]. Intraoperative ultrasonography is most often used in evaluating patients who are candidates for surgical resection of primary or metastatic hepatic malignancies [68]. Intraoperative ultrasonography is far superior to all preoperative imaging, including MRI and CT portography. It is even better than surgical inspection and palpation [69,70]. Intraoperative ultrasonography is also important in intraoperative pancreatic imaging, searching for small occult tumors, assessing tumor extension (Fig. 14), and detecting metastatic disease in draining lymph nodes and the liver. Laparoscopic ultrasonography is important in gallbladder surgery, replacing intraoperative cholangiography in some centers. Laparoscopic ultrasonography has also been used to stage patients with bowel malignancies, particularly gastric tumors. Intraoperative ultrasonography guidance facilitates more accurate and safer biopsy of deep-seated nonpalpable lesions and small lesions adjacent to critical vascular structures. Intraoperative ultrasonography can effectively guide drainage of cysts, pseudocysts, and other fluid collections encountered intraoperatively. Intraoperative ultrasonography guidance is very useful for tumor ablation with cryosurgery, alcohol injec-

Fig. 14. Intraoperative ultrasound clearly demonstrates the extent of disease in this patient with invasion of the middle hepatic vein by this colorectal metastasis (arrow). Intraoperative ultrasound is unexcelled in both detecting liver lesions and determining the extent of disease within the liver.

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tion, or hyperthermic ablation with radio frequency, laser, or microwave energy sources.

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