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Note: This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights. EDUCATION EXHIBIT 135 MR Imaging of the Gallbladder: A Pictorial Essay1 CME FEATURE See accompanying test at http:// www.rsna.org /education /rg_cme.html LEARNING OBJECTIVES FOR TEST 3 After reading this article and taking the test, the reader will be able to: Discuss the state䡲 of-the-art MR and MR cholangiographic imaging techniques for the diagnosis of gallbladder disease. 䡲 Describe the normal MR imaging features of the gallbladder. 䡲 Identify the MR imaging appearances of gallbladder disease. TEACHING POINTS See last page Onofrio A. Catalano, MD2 ● Dushyant V. Sahani, MD ● Sanjeeva P. Kalva, MD ● Matthew S. Cushing, MD ● Peter F. Hahn, MD, PhD Jeffrey J. Brown, MD ● Robert R. Edelman, MD The gallbladder serves as the repository for bile produced in the liver. However, bile within the gallbladder may become supersaturated with cholesterol, leading to crystal precipitation and subsequent gallstone formation. The most common disorders of the gallbladder are related to gallstones and include symptomatic cholelithiasis, acute and chronic cholecystitis, and carcinoma of the gallbladder. Other conditions that can affect the gallbladder include biliary dyskinesia (functional), adenomyomatosis (hyperplastic), and postoperative changes or complications (iatrogenic). Ultrasonography (US) has been the traditional modality for evaluating gallbladder disease, primarily owing to its high sensitivity and specificity for both stone disease and gallbladder inflammation. US performed before and after ingestion of a fatty meal may also be useful for functional evaluation of the gallbladder. However, US is limited by patient body habitus, with degradation of image quality and anatomic detail in obese individuals. With the advent of faster and more efficient imaging techniques, magnetic resonance (MR) imaging has assumed an increasing role as an adjunct modality for gallbladder imaging, primarily in patients who are incompletely assessed with US. MR imaging allows simultaneous anatomic and physiologic assessment of the gallbladder and biliary tract in both initial evaluation of disease and examination of the postoperative patient. This assessment is accomplished chiefly through the use of MR imaging contrast agents excreted preferentially via the biliary system. © RSNA, 2008 Abbreviations: BOPTA ⫽ benzyloxypropionictetraacetate, CHD ⫽ common hepatic duct, HIDA ⫽ hydroxyiminodiacetic acid, MnDPDP ⫽ mangafodipir trisodium, SE ⫽ spin-echo, XGC ⫽ xanthogranulomatous cholecystitis, 3D ⫽ three-dimensional RadioGraphics 2008; 28:135–155 ● Published online 10.1148/rg.281065183 ● Content Codes: 1From the Department of Radiology, Division of Gastrointestinal Radiology, Massachusetts General Hospital, WHT 270, 55 Fruit St, Boston, MA 02114 (O.A.C., D.V.S., S.P.K., M.S.C., P.F.H.); Mallinckrodt Institute of Radiology, Washington University School of Medicine, St Louis, Mo (J.J.B.); and the Department of Radiology, Northwestern University School of Medicine, Evanston, Ill (R.R.E.). Presented as an education exhibit at the 2004 RSNA Annual Meeting. Received October 23, 2006; revision requested January 23, 2007; final revision received June 7; accepted June 11. The authors discuss an investigational or unlabeled use of a commercial product, device, or pharmaceutical that has not been approved for such purpose by the FDA. D.V.S. is a researcher for GE Healthcare and a consultant with Bracco Diagnostics; S.P.K. received research grants from Johnson & Johnson (Cordis) and Cook and is with the speakers’ bureau of Johnson & Johnson; J.J.B. is a consultant with Tyco Healthcare (Mallinckrodt), Bayer Healthcare, and GE Healthcare and is with the speakers’ bureau of Bracco Diagnostics; and R.R.E. received research support from GE Healthcare and Schering (Berlex); all remaining authors have no financial relationships to disclose. Address correspondence to D.V.S. (e-mail: [email protected]). 2Current © address: Department of Radiology, AO G Rummo, Benevento, Italy. RSNA, 2008 136 January-February 2008 RG f Volume 28 ● Number 1 Figure 1. Two-dimensional versus three-dimensional (3D) MR cholangiopancreatography. (a) During two-dimensional acquisition, a thick slab is imaged in an oblique plane. Two-dimensional heavily T2-weighted MR cholangiopancreatogram shows fluid-filled structures, which may overlap because the imaging is performed in only one plane. The biliary and pancreatic ducts are well visualized. (b) Three-dimensional thinsection maximum-intensity-projection reformatted heavily T2-weighted MR cholangiopancreatogram shows how it is possible to rotate and separate the structures with a 3D sequence. Introduction The gallbladder is a pear-shaped hollow viscus located in the right upper quadrant, lodged on the visceral surface of the liver between segments IV and V, and connected to the hepatic duct through the cystic duct to form the common bile duct. The gallbladder is composed of the fundus, which usually projects beyond the inferior border of the liver; the body; and the neck. It is usually 7–10 cm long and 2.5 cm wide, and the wall measures less than 3 mm in thickness (1). The gallbladder serves as the repository for bile produced in the liver, with an average volume of 30 –50 mL (2). Bile within the gallbladder may become supersaturated with cholesterol, leading to crystal precipitation and subsequent gallstone formation. Imaging of the gallbladder is typically requested for evaluation of right upper quadrant pain in patients with or without fever and jaundice. Ultrasonography (US) is typically the initial imaging modality. However, technologic advances in magnetic resonance (MR) imaging software, hardware, and contrast media (eg, phasedarray surface coils, breath-hold imaging, singleshot imaging techniques, hepatobiliary contrast agents) allow MR imaging to be used as the initial imaging modality for the evaluation of pain, jaundice, or masses or as a problem-solving tool for gallbladder disease. Moreover, MR imaging Figure 2. Three-dimensional MR cholangiopancreatogram shows the normal gallbladder. The cystic duct appears as a curvilinear bright line connecting the gallbladder with the common hepatic duct (CHD). Pancreas divisum is incidentally noted. allows functional assessment of the gallbladder through the use of contrast agents excreted preferentially via the biliary system. In this article, we review MR imaging techniques for the evaluation of the gallbladder and the normal MR imaging appearance of this structure. In addition, we discuss and illustrate congenital abnormalities of the gallbladder and a variety of pathologic conditions affecting the gallbladder (cholelithiasis, acute and chronic RG f Volume 28 ● Number 1 Catalano et al 137 Table 1 MR Imaging Protocol Step Description Evaluation of gallbladder anatomy MR cholecystography Contrast-enhanced MR cholecystography Dynamic contrastenhanced study Axial in-phase and opposed-phase breath-hold gradient-echo T1-weighted imaging (TR msec/first TE msec/second TE msec ⫽ 150–200/4.2/1.8, flip angle ⫽ 80°, section thickness ⫽ 6–9 mm); axial and coronal breath-hold steady state fast SE T2weighted imaging (TR/TE ⫽ minimum/180, section thickness ⫽ 5 mm); axial respiratory-triggered fat-saturated T2-weighted imaging (TR/TE ⫽ 5000/80, echo train length ⫽ 12, section thickness ⫽ 3 mm) Oblique radial steady state fast SE T2-weighted imaging (14 sections) (TR/TE ⫽ minimum/500, section thickness ⫽ 40 mm); oblique right anterior steady state fast SE T2-weighted imaging (TR/TE ⫽ minimum/160, section thickness ⫽ 5 mm); oblique left anterior steady state fast SE T2-weighted imaging (TR/TE ⫽ minimum/160, section thickness ⫽ 5 mm); 3D fat-saturated MR cholangiopancreatography (TR/TE ⫽ 4000/500–600, section thickness ⫽ 1.4 mm) 0.05–0.1 mL/kg (up to 20 mL) of gadolinium benzyloxyproprionictetraacetate (BOPTA) (Multihance; Bracco, Milano, Italy) at 2 mL/sec or 0.5 mol/kg of mangafodipir trisodium (MnDPDP) (Teslascan; Amersham Health, Princeton, NJ) slowly administered over 1–2 min; axial and coronal 3D breath-hold interpolated fat-suppressed spoiled gradient-echo T1-weighted imaging (TR/TE ⫽ 6.5/2.1, flip angle ⫽ 15°, section thickness ⫽ 2.4 mm) 30–90 minutes after contrast material injection 0.1 mmol/kg (up to 40 mL) of gadolinium-based contrast material injected at 2 mL/sec or 0.05–0.1 mL/kg (up to 20 mL) of gadolinium BOPTA injected at 2 mL/sec; axial 3D fat-suppressed spoiled gradient-echo imaging (TR/TE ⫽ 4.5/1.9, flip angle ⫽ 12°, section thickness ⫽ 4–5 mm) to cover the entire liver (run prior to and 25 sec, 60–70 sec, and 120 sec after bolus administration) TE ⫽ echo time, TR ⫽ repetition time. cholecystitis, Mirizzi syndrome, xanthogranulomatous cholecystitis [XGC], adenomyomatosis, carcinoma, lymphoma, endometrial implants). We also discuss functional evaluation of the gallbladder in the acute setting, postoperative functional evaluation of the gallbladder and biliary tree, and the assessment of angiogenesis as a possible future application. Imaging Techniques MR imaging sequences should be tailored to the clinical question. T2-weighted sequences (usually fast spin-echo [SE] sequences with respiratory gating) are optimal for evaluating soft-tissue abnormalities involving the wall of the gallbladder, the biliary system, and adjacent soft-tissue structures. The section thickness should be less than 5 mm, with a 1–2-mm gap between sections. Useful additional T2-weighted sequences are similar to those used to evaluate the biliary tree (MR cholangiopancreatography) (Figs 1, 2): acquisition techniques such as half-Fourier rapid acquisition with relaxation enhancement and singleshot fast SE imaging. Although T1-weighted MR imaging of the gallbladder can be performed with either SE or breath-hold spoiled gradient-echo techniques, the latter are superior because they decrease respiratory artifacts. Dynamic contrast material– enhanced fat-suppressed T1-weighted MR imaging sequences improve the delineation of the gallbladder wall, bile ducts, and associated entities such as inflammation and neoplasms and allow assessment of the liver parenchyma for tumor invasion and metastatic disease (Table 1). Two agents, MnDPDP and gadolinium BOPTA—the latter not yet having been approved in the United States for evaluation of the gallbladder and biliary tree—are excreted into the bile. After being injected intravenously, these agents are specifically taken up by the hepatocytes and subsequently excreted into the bile, resulting in significant T1 shortening of the bile, which appears hyperintense on T1-weighted MR images. This phenomenon permits evaluation of the physiologic characteristics of the gallbladder and biliary tree. This branch of MR cholangiography is known as functional MR cholangiography (2– 4). 138 January-February 2008 RG f Volume 28 ● Number 1 Figure 3. Gallbladder sludge in a 63-year-old man who underwent MR imaging for a left adrenal mass. Coronal T2-weighted (a) and axial in-phase T1-weighted (b) MR images show an incidental finding of dependent material within the gallbladder lumen (arrow). The material is hypointense on the T2weighted image and hyperintense on the T1-weighted image. Normal Appearance of the Gallbladder The gallbladder should be imaged after the patient has fasted for 8 –12 hours, which promotes physiologic distention of the gallbladder. On T2weighted images, the gallbladder wall has low signal intensity and stands out against the bright visceral fat. The wall adjacent to the liver cannot be identified as a separate structure. On T1weighted images, the gallbladder wall has intermediate signal intensity and enhances uniformly after the administration of gadolinium-based contrast material. The portion of the gallbladder wall adjacent to the liver may not be well appreciated owing to similar enhancement of the wall and the liver parenchyma. The insertion of the cystic duct into the hepatic duct can be demonstrated with routine T2weighted imaging and MR cholangiography. Normal bile appears uniformly bright with T2weighted sequences. On T1-weighted images, bile varies greatly in signal intensity depending on its concentration. During fasting, bile undergoes a process of concentration. Water is reabsorbed and the concentration of cholesterol and bile salts increases, leading to a shortened T1 relaxation time and, consequently, to bright bile on T1-weighted images. A layering effect is sometimes observed, with concentrated and denser bile in the dependent position. Gallbladder sludge may have similar signal intensity characteristics, namely, iso- to mild hyperintensity on T2-weighted images and hyperintensity on T1-weighted images (Fig 3) (2– 4). Congenital Abnormalities of the Gallbladder There are many uncommon anomalies of the gallbladder and biliary tree that are delineated with MR cholangiography. MR cholangiography is useful in defining (a) the biliary anatomy for preoperative planning, and (b) anatomic variants that may predispose to conditions such as Mirizzi syndrome (discussed later). Bilobed or duplicated gallbladder is a congenital abnormality that is well defined at MR imaging and MR cholangiography. This entity is rare, having been seen in one of every 4000 adults in an autopsy series (5), and may be associated with right upper quadrant pain (Fig 4). Classifications vary, with distinctions sometimes being made between bilobed gallbladder and true gallbladder duplication. Bilobed or duplicated gallbladder has been found to predispose to complications such RG f Volume 28 ● Number 1 Catalano et al 139 Figure 4. Duplicated gallbladder in a 24-year-old woman with right upper quadrant discomfort and dyspepsia. (a) Axial single-shot fast SE T2-weighted MR image shows two pear-shaped high-signal-intensity structures in the gallbladder fossa (arrows). (b) On an axial in-phase gradient-echo T1-weighted MR image, the anterior structure (arrow) has higher signal intensity than the posterior structure (arrowheads), probably due to increased bile concentration. (c) Coronal 3D maximum-intensity-projection reformatted T1-weighted MR cholecystogram acquired 60 minutes after MnDPDP administration demonstrates enhancement of the pear-shaped structures (arrows) and two separate cystic ducts (arrowheads), findings that allowed the diagnosis of a double gallbladder. as cholelithiasis and cholecystitis. Delineation of the anatomy is important for preoperative planning and avoidance of biliary injury. Techniques have recently been described for defining the anatomy of the intra- and extrahepatic biliary tree more precisely using MnDPDP-enhanced MR cholangiography (6). Pathologic Conditions Affecting the Gallbladder Cholelithiasis Cholecystectomy is the most common elective abdominal surgery in the United States and is usually prompted by gallstones. Gallstones are found in about 10% of the general population, are twice as common in women as in men, and become more prevalent with increasing age. Obesity, rapid weight loss, pregnancy, and estrogens are known risk factors. Gallbladder stones are usually classified as cholesterol stones when they are composed of at least 50% cholesterol and as pigment stones when they contain lesser amounts of cholesterol and higher percentages of other constituents such as calcium bilirubinate and glycoproteins. Cholesterol stones are by far the more common, accounting for more than 80% of all gallstones in the United States. Although most gallstones remain asymptomatic throughout life, some are responsible for clinical symptoms, the most common being biliary colic. The risk of complications is 1% per year. US is the most commonly used modality in the evaluation of gallstone disease, with a high specificity (⬎95%) and sensitivity (95%) for stones larger than 2 mm (7,8). It is important to be familiar with the MR imaging appearance of gallstones, since they are often detected incidentally. Gallstones are best appreciated at T2-weighted MR imaging and MR cholangiopancreatography and appear as signal 140 RG f Volume 28 January-February 2008 ● Number 1 Figure 5. Cholelithiasis in a 45-year-old man with right upper quadrant pain. (a) Coronal T2weighted MR image reveals stones (arrows) appearing as hypointense material within the hyperintense bile. (b) On a two-dimensional MR cholangiopancreatogram, the stones are not visible. Table 2 Gallstone Composition and Signal Intensity Type of Gallstone Cholesterol Pigment T1 Signal Intensity Percentage of Stones Detected Signal-Intensity Ratio (Stone to Bile) Hypointense Hyperintense 100 (4/4) 90 (18/20) 0.24 ⫾ 0.10 3.36 ⫾ 1.88 voids on both T1- and T2-weighted images (Fig 5) (9). The presence of protein macromolecules (which have shorter T1 relaxation times) within gallstones may sometimes be responsible for the central hyperintensity with a peripheral rim of hypointensity seen on T1- or T2-weighted images, or for the predominant hyperintensity seen on T1-weighted images (10,11). MR imaging can also help distinguish between different types of gallstones. Like cholesterol stones, pigment stones typically appear hypointense with T2weighted sequences; unlike cholesterol stones, they usually have increased signal intensity on T1-weighted images. Pigment stones also show a greater range of signal intensity, which in vitro studies have shown to be related to the degree of hydration. The composition of the stones may affect management: Pigment stones may easily be removed with endoscopic lithotripsy, whereas cholesterol stones are much harder in consistency and more difficult to treat endoscopically (Table 2) (12). Acute Cholecystitis Acute cholecystitis is by far the most common acute complication of gallstone disease. The clinical presentation is characterized by right upper quadrant tenderness, abdominal pain, fever, and leukocytosis. In 90% of cases, the eliciting factor is an impacted gallstone obstructing the cystic duct. In the remaining cases, the condition occurs in the absence of gallstones and is known as acute acalculous cholecystitis, which is usually seen in critically ill patients and carries higher morbidity and mortality rates. In the first few days after clinical onset, the gallbladder appears distended at pathologic analysis, with the lumen filled with exudate and sometimes with pus. Bacteria may be cultured from gallbladder bile. Bile salts are subsequently ab- RG f Volume 28 ● Number 1 Catalano et al 141 Figures 6 – 8. (6) Gallbladder wall thickening in an 81-year-old man with hepatitis C virus–related cirrhosis and hypoproteinemia but no intrinsic gallbladder disease. Axial single-shot fast SE T2-weighted MR image shows thickening and hyperintensity of the gallbladder wall (arrow) due to the patient’s hypoproteinemic state. Note the enlargement of the spleen. (7) Acute cholecystitis in a 77-year-old woman with a history of gallstones who presented with fever, leukocytosis, and right upper quadrant pain. Fat-saturated respiratory-triggered fast SE T2-weighted MR image shows thickening, sloughing, irregularity, and edema of the gallbladder wall and surrounding liver tissue (arrow). (8) Acute cholecystitis in a 58-year-old woman who presented with right upper quadrant pain radiating to the right shoulder, along with fever, vomiting, and leukocytosis. Axial single-shot fast SE T2-weighted MR image shows gallstones (black arrow). The gallbladder wall is thickened and has increased signal intensity. Minimal pericholecystic fluid is also present (white arrow). sorbed, and clear mucoid fluid accumulates. The gallbladder wall is edematous and thickened (⬎3 mm). Necrosis and perforations may ensue (8,13). US is the usual modality of choice for the diagnosis of acute cholecystitis but may be significantly limited by large body habitus, with obesity representing an increasingly serious issue in both Europe and the United States. When US findings are equivocal, MR imaging may be helpful in detecting stones in the gallbladder neck and cystic duct and associated gallbladder wall abnormalities. On T2-weighted images, the gallbladder wall may show increased signal intensity and thickening (⬎3 mm). This finding must be differentiated from gallbladder wall thickening related to other causes (eg, hypoproteinemic states) (Fig 6) (2– 4). Pericholecystic fluid collections and edema of the surrounding liver tissue may be found (Figs 7, 8). Viral cholecystitis can have a similar appearance. Periportal hyperintensity, although a nonspecific finding, may be observed on T2-weighted images. Although an inflammation-related increase in bile protein content may result in variable signal intensity of the bile on T1-weighted images, the bile usually appears markedly hypointense with T1-weighted sequences due to the impairment of gallbladder concentrating capability, which is typical of the acute inflammatory state. Teaching Point 142 January-February 2008 RG f Volume 28 ● Number 1 Figure 9. Acute cholecystitis with cholangitis in a 61-year-old woman who presented with right upper quadrant pain, vomiting, nausea, fever, and leukocytosis. (a) Axial T1-weighted MR image shows diffuse gallbladder wall thickening (arrows). (b) Coronal gadolinium-enhanced fat-suppressed T1-weighted MR image shows marked enhancement of the gallbladder walls, intra- and extrahepatic bile ducts, and surrounding liver tissue (arrows). Contrast-enhanced fat-suppressed images demonstrate increased enhancement of the gallbladder wall, adjacent fat, and surrounding liver parenchyma (Fig 9). The “interrupted rim sign,” which is characterized by patchy enhancement of the gallbladder mucosa, represents areas of necrosis and is useful in identifying the gangrenous form of acute cholecystitis at MR imaging (14 – 16). Gangrenous cholecystitis may be suggested by asymmetric gallbladder wall thickening due to intramural microabscesses, intramural hemorrhage, and complex pericholecystic fluid collections containing debris. Emphysematous cholecystitis is caused by gasforming bacteria that infect the gallbladder wall and produce intramural and intraluminal gas. It is easily diagnosed with computed tomography (CT), is usually acalculous, and can occur in diabetic patients or in cases of atherosclerosis of the cystic artery with resulting ischemia. Pericholecystic abscesses result from perforation of the gallbladder and appear on contrastenhanced images as localized fluid collections with rim enhancement. Transient enhancement of pericholecystic hepatic parenchyma on dynamic images obtained immediately after the administration of gadolinium-based contrast material is a highly specific sign found in 70% of patients with acute cholecystitis (7,8,17). This finding is due to a hyperemic response in the liver adjacent to the inflamed gallbladder. Functional evaluation of the gallbladder in cases of suspected cystic duct obstruction has long been the province of nuclear medicine and is used in problem solving in patients with acute cholecystitis. Functional MR cholangiography serves as a combination of anatomic and physiologic assessment. Kim et al (18) compared conventional T2-weighted MR cholangiography with MnDPDP-enhanced functional MR cholangiography in the evaluation of 12 patients with suspected acute cholecystitis. Hydroxyiminodiacetic acid (HIDA) scans were also obtained to assess for common bile duct obstruction. The authors found excellent correlation between findings on HIDA scans, findings on functional MR cholangiograms, and surgical findings. Furthermore, in a study by Fayad et al (19), positive predictive values of up to 100% for the diagnosis of acute cholecystitis were described in patients examined with functional MR cholangiography. Chronic Cholecystitis Chronic cholecystitis is the most common form of clinically symptomatic gallbladder disease and is almost invariably associated with gallstones (7). The gallbladder appears small and contracted, with irregular and thickened walls. Signs and symptoms are vague and include abdominal distention, epigastric discomfort, and nausea (7). After the administration of gadolinium-based contrast material, the gallbladder wall enhances less intensely than in acute cholecystitis. The enTeaching hancement is usually smooth, slow, and proPoint longed (Fig 10), unlike in gallbladder carcinoma, in which it is usually irregular, early, and prolonged (3,4). However, the utility of conventional MR cholangiography, functional MR cholangiography, and a combination of the two in the evalu- RG f Volume 28 ● Number 1 Catalano et al 143 Figure 10. Chronic cholecystitis in a 47-year-old woman with right upper quadrant pain. On axial T1-weighted (a), fat-saturated T2-weighted (b), and gadolinium-enhanced fat-saturated arterial phase (c) and portal venous phase (d) MR images, the gallbladder wall is thickened and stratified without interruption or irregularity. The tunica muscularis appears hypointense on the T1-weighted image (arrow in a) and hyperintense on the T2-weighted image (arrow in b) due to edema. The gallbladder wall enhances homogeneously and progressively from the arterial phase to the portal venous phase. The tunica muscularis remains relatively poorly enhanced on the contrast-enhanced images (arrow in c and d). ation of chronic cholecystitis has not been clearly established; in the study mentioned earlier, Fayad et al (19) found a 50% positive predictive value for the detection of chronic cholecystitis for both conventional and functional MR cholangiography. Mirizzi Syndrome Mirizzi syndrome is a rare complication of gallstone disease that is caused by an impacted stone in the neck of the gallbladder or the cystic duct, leading to extrinsic compression and subsequent obstruction of the CHD (20). On rare occasions, it occurs after cholecystectomy due to an impacted stone in the cystic duct remnant. Mirizzi syndrome is usually classified as either type 1 (simple obstruction of the CHD) or type 2 (erosion of the wall of the CHD resulting in cholecystocholedochal fistula). The syndrome is associated with an increased prevalence of bile duct injury when standard cholecystectomy is performed; therefore, preoperative recognition is of paramount importance (21). Visualization of a gallstone at the junction of the CHD and cystic duct with associated biliary ductal dilatation or gallbladder inflammation is diagnostic (22). MR cholangiopancreatography typically reveals an impacted gallstone in the cystic duct or gallbladder neck associated with dilatation of the biliary tree, with the level of obstruction at the junction of the cystic duct and CHD. 144 January-February 2008 RG f Volume 28 ● Number 1 Figure 11. Mirizzi syndrome in a 42-year-old man who presented with right upper quadrant pain, fever, vomiting, leukocytosis, and hyperbilirubinemia. US revealed gallstones and dilated intrahepatic biliary ducts. (a) Thick-slab MR cholangiopancreatogram shows the dilated intrahepatic biliary ducts and the level of obstruction at the CHD due to extrinsic compression (top arrow). Bottom arrow indicates the point at which the cystic duct joins the CHD. (b) Axial single-shot fast SE T2-weighted MR image reveals stones within the gallbladder lumen and an impacted stone in the cystic duct (arrow). (c) Axial contrast-enhanced fat-suppressed T1-weighted MR image shows diffuse enhancement of the gallbladder and cystic duct due to associated inflammation (arrow). The gallbladder wall is usually thickened. It has a smooth contour and enhances after contrast material administration (Fig 11). Whereas US and CT can usually demonstrate only the presence and level of biliary obstruction, MR cholangiopancreatography can further characterize the nature of the obstruction, define the burden of gallstones in the biliary tree, and help evaluate the cystic duct obstruction. Moreover, MR cholangiopancreatography can help detect some anatomic variants that predispose to the development of the syndrome, such as a low insertion of the cystic duct or a long parallel cystic duct. Contrast-enhanced MR imaging can demonstrate the inflammation of the gallbladder associated with Mirizzi syndrome (23,24). Xanthogranulomatous Cholecystitis XGC is an uncommon inflammatory disease of the gallbladder that is characterized histologically by a focal or diffuse destructive inflammatory process with xanthomalike foam cells, scarring, and ceroid nodules. At macroscopic analysis, the gallbladder appears nodular, with thickened and poorly defined walls; gallstones are present in most cases. The surrounding fat and liver may be infiltrated. The process may extend to involve other nearby organs such as the colon and duodenum and may be complicated by fistulous or abscess formation. Lymphadenopathy and biliary obstruction may be associated findings, and gallbladder cancer may coexist. XGC is thought to be induced by intramural extravasation of bile from the Rokitansky-Aschoff sinuses or from superficial mucosal ulcerations, leading to an inflammatory response in which histiocytes predominate as they ingest the chemically irritating cholesterol crystals (7,25,26). The disease usually manifests as an acute episode of cholecystitis in women 60 –70 years of age and tends to persist even for years (7). At CT, XGC closely resembles gallbladder carcinoma, with diffuse or focal gallbladder wall thickening, heterogeneous wall enhancement, and hypoattenuating intramural nodules. Statistically significant CT findings that help discriminate between gallbladder malignancy and RG f Volume 28 ● Number 1 Catalano et al 145 Figure 12. XGC in a 63-year-old woman with right upper quadrant pain and abnormal liver function test results. (a) US image shows echogenic stones and debris (arrowhead), diffuse gallbladder wall thickening, and masslike hypoechogenicity in the liver (arrow). (b) Contrast-enhanced abdominal CT scan demonstrates gallbladder wall thickening with heterogeneous enhancement. Note the continuous enhancement of the gallbladder mucosa (arrows) and the diffuse character of the wall thickening. (c) Axial fat-saturated respiratory-triggered fast SE T2-weighted MR image shows diffuse thickening with a fundal mass and unbroken mucosal hyperintensity. There is focal high T2 signal intensity within the wall of the gallbladder (arrow), a finding that is consistent with an intramural collection. (d) Gadolinium-enhanced T1-weighted MR image shows diffuse wall thickening with a mass at the fundus (arrow) and continuous enhancement of the gallbladder mucosa. (e) Photograph of the gross pathologic specimen of the gallbladder obtained at cholecystectomy shows diffuse thickening of the wall, intramural xanthogranulomas, and intraluminal stones. XGC include (a) low-attenuation intramural nodules occupying more than 60% of the thickened wall area and corresponding to the xanthogranulomas, and (b) continuous linear en- hancement of the mucosa. In one series, although diffuse gallbladder wall thickening was observed in 91% of cases of XGC, it was also seen in 41% of cases of gallbladder carcinoma (27); thus, wall thickening alone is a sign with only limited utility (27,28). MR imaging demonstrates intramural lesions with markedly elevated T2 signal intensity that correspond to the low-attenuation intramural nodules seen at CT. Preservation of linear mucosal enhancement at MR imaging is suggestive of XGC rather than carcinoma (Fig 12) (29). 146 January-February 2008 RG f Volume 28 ● Number 1 Figures 13, 14. (13) Adenomyomatosis in a 51-year-old man. (a) Contrast-enhanced CT scan demonstrates focal fundal gallbladder wall thickening (arrow) with only minimal enhancement. (b) T2-weighted MR image shows wall thickening (arrow) and increased mural signal intensity. (c) Contrast-enhanced T1-weighted MR image also shows only minimal enhancement (arrow). (14) Adenomyomatosis in a 53-year-old man. MR imaging of the liver was performed to evaluate thickening of the gallbladder fundus that was seen at US performed at another institution. (a, b) Axial (a) and coronal (b) T2-weighted MR images show focal thickening of the gallbladder wall in the fundus (arrow in a), with small hyperintense foci (string of beads sign) representing dilated Rokitansky-Aschoff sinuses (arrow in b). (c) Axial gadolinium-enhanced portal venous phase T1-weighted MR image shows enhancement of the gallbladder wall (arrow). RG f Volume 28 ● Number 1 Adenomyomatosis of the Gallbladder Adenomyomatosis of the gallbladder is a common, distinct, noninflammatory benign condition that has been reported in up to 8.7% of cholecystectomy specimens. It is more frequently seen in women than in men, usually manifests with persistent right upper quadrant pain, and is usually associated with gallstones (90% of cases). Adenomyomatosis is characterized by excessive proliferation of surface epithelium with deep and branching invaginations (Rokitansky-Aschoff sinuses) into the thickened tunica muscularis or beyond (26,30,31). The Rokitansky-Aschoff sinuses can be found in about 90% of gallbladder specimens; if they are deep, branching, and accompanied by hyperplasia of the muscular layer, adenomyomatosis can be diagnosed (30). At gross examination, adenomyomatosis of the gallbladder may manifest as diffuse, segmental, or focal disease. Diffuse adenomyomatosis manifests as diffuse mural thickening and luminal narrowing. In the segmental form, there is focal circumferential thickening in the midportion (“waist”) of the gallbladder, producing an “hourglass” appearance (32). The localized form of adenomyomatosis manifests as a focal, frequently semilunar or crescentic solid mass, usually in the fundus of the gallbladder (Figs 13, 14) (26). Dysplastic changes and even carcinoma may arise from adenomyomatous epithelium, especially in patients with segmental type adenomyomatosis, but this phenomenon seems to be related to the presence of gallstones and chronic inflammation (26,33). MR imaging demonstrates the mural thickening and multiple intramural cystic components (Rokitansky-Aschoff sinuses) (34). Adenomyomatosis can appear almost identical to a mass and may be difficult to distinguish from gallbladder malignancy. On contrast-enhanced images, the diffuse type shows early mucosal and subsequent serosal enhancement. The “string of beads sign,” the hallmark of adenomyomatosis at MR imaging, refers to highTeaching signal-intensity foci in the gallbladder wall on T2Point weighted images, findings that correspond to bilefilled Rokitansky-Aschoff sinuses. This sign is highly specific (92%) in diagnosing gallbladder adenomyomatosis versus gallbladder cancer. Catalano et al 147 The sign may be absent in cases of small (⬍3-mm) sinuses or sinuses filled with inspissated proteinaceous bile or small calculi; therefore, its sensitivity is only 62%. In approximately 70% of patients, the contrast enhancement pattern of adenomyomatosis is indistinguishable from that of gallbladder cancer (31,33). Gallbladder Carcinoma Gallbladder cancer is the fifth most common gastrointestinal carcinoma and the most common carcinoma of the biliary tree, with an incidence of 2.5 new cases per 100,000 population per year. It is usually advanced at presentation, having spread to the lymph nodes and invaded the surrounding structures, mainly the liver; furthermore, it has a poor outcome, with a median patient survival time of 3 months and a 5-year survival rate of 5% (35). Gallbladder cancer most often occurs in the elderly and in women and is usually associated with gallstones (90% of cases). Other risk factors include a chronic typhoid carrier state, a long common pancreatic-biliary channel, and porcelain gallbladder. About 20% of patients with porcelain gallbladder develop gallbladder cancer (36). It has been postulated that the most important risk factor is the presence of chronic gallbladder inflammation, usually related to stones (35). The initial presenting signs and symptoms are vague and nonspecific; they include abdominal pain (mainly in the right upper quadrant), weight loss, and fever. Jaundice develops when the carcinoma involves and obstructs the common bile duct, right hepatic duct, or CHD (36,37). Carcinoembryogenic antigen values higher than 4 ng/mL in the appropriate clinical setting are 93% specific but only 50% sensitive for the diagnosis of gallbladder cancer (35). At histologic analysis, about 90% of gallbladder carcinomas are adenocarcinomas; other causes, such as small cell carcinomas and squamous cell carcinomas, are rare (36,37). Gallbladder cancer usually arises in the fundus or neck, but its rapid spread may obscure the site of origin (38). It progresses from epithelial dysplasia to carcinoma in situ to invasive carcinoma (35). Because of the thinness of the muscular 148 January-February 2008 RG f Volume 28 ● Number 1 Figure 15. Gallbladder cancer in a 73-year-old woman who presented with abdominal pain, hyperbilirubinemia, and weight loss. On an axial fat-saturated T2-weighted MR image (a) and axial (b) and coronal (c) gadolinium-enhanced T1-weighted MR images, the gallbladder wall is heterogeneously thickened (thick arrow in a, arrow in b and c). The mucosa and submucosa cannot be clearly distinguished along the entire gallbladder wall. Stones are present within the gallbladder lumen (thin arrows in a). In contrast, chronic cholecystitis manifests as smooth, well-defined enhancement of the gallbladder wall with preservation of the submucosa (cf Fig 10). layer and the continuity of the connective tissue of the gallbladder wall with the interlobular connective tissue of the liver, gallbladder carcinoma can easily invade the liver and gain access to the lymphatic and vascular channels. Once it has penetrated the serosa, it can also spread to the peritoneal cavity. According to the American Joint Committee on Cancer (AJCC)–Union Internationale Contre le Cancer (UICC) TNM classification system, gall bladder carcinoma is considered to be T1 when confined within the muscular layer, T2 when it extends beyond the muscular layer into the perimuscular connective tissue, T3 when liver invasion of less than 2 cm has occurred, and T4 when the extent of liver involvement exceeds 2 cm. Although lymphatic drainage may not follow a predictable pattern, it usually involves the cystic and pericholedochal nodes initially (N1) but subsequently extends into the posterior pancreaticoduodenal, retroportal, and celiac nodes (N2). Involvement of intercaval nodes occurs later and is classified as M1 (35). At macroscopic examination, gallbladder cancer typically manifests as either (a) focal or diffuse mural thickening; (b) an intraluminal polypoid mass; or (c) a soft-tissue mass replacing the gallbladder, with invasion of the liver. Gallbladder carcinomas most often manifest as diffusely infiltrating lesions extending into the liver (⬃68% of cases) and less often manifest as intraluminal polypoid masses or mural thickening (37). New and potentially curative surgical therapies have been introduced that allow a 5-year survival rate of more than 50%. These therapies include resection of the gallbladder, resection of segments IVb and V of the liver, and even extended right hepatectomy and regional lymphadenectomy. They necessitate an accurate preoperative radiologic assessment of tumor extension and a preoperative vascular “road map” (35,39,40). Focal or diffuse mural thickening of more than 1 cm as well as asymmetric thickening are highly suggestive of the diagnosis (41,42). On T2- Teaching Point RG f Volume 28 ● Number 1 Catalano et al 149 Figure 16. Sludge mimicking neoplasm. (a, b) On axial fat-saturated T2-weighted (a) and gadolinium-enhanced T1-weighted baseline (b) MR images, the gallbladder lumen appears to be filled by a mass that is hypointense on the T2-weighted image (arrow in a) and hyperintense on the T1-weighted image (arrow in b). The gallbladder wall is of normal thickness on the baseline image. (c, d) On axial fat-saturated T2-weighted (c) and gadolinium-enhanced T1weighted (d) MR images obtained 2 months later, the “mass” has disappeared, indicating that the finding in a and b represented sludge. Irregular thickening of the gallbladder wall due to inflammation is also seen (arrow). weighted images, the tumor is usually heterogeneously hyperintense relative to the liver, whereas on T1-weighted images it is relatively iso- or hypointense. All gallbladder cancers show enhancement after the administration of gadoliniumbased contrast material. In the early phase of dynamic contrast-enhanced imaging, the outer margin of enhancement is irregular, whereas it appears smooth in chronic cholecystitis. The late phases of enhancement are less useful because of the spread of enhancement toward the outer wall in both chronic cholecystitis and gallbladder car- cinoma (39,43). However, these characteristics may overlap, and it may be difficult to differentiate benign mural thickening from gallbladder carcinoma (Figs 15, 16). In 25% of patients, gallbladder carcinoma manifests as an intraluminal polypoid mass, usually well differentiated and confined to the muscular layer with a better prognosis (9,44). On T1weighted images, the polypoid form is seen as an intermediate-signal-intensity mass protruding 150 January-February 2008 RG f Volume 28 ● Number 1 Figure 17. Gallbladder carcinoma in a 73-year-old woman who presented with right upper quadrant pain, weight loss, and hyperbilirubinemia. (a) Axial fat-suppressed T1-weighted MR image shows irregular gallbladder wall thickening with a focal mass at the fundus (arrows). The mass exhibits the intermediate signal intensity typically seen on T1-weighted images. (b) On an axial fat-suppressed T2-weighted MR image, the mass is heterogeneously hyperintense (arrows). (c) Contrastenhanced T1-weighted MR image shows the mass with variable enhancement. The tumor-liver interface is ill defined (arrow), a finding that suggests tumor infiltration of the liver. into the lumen and arising from the wall of the gallbladder, which may be thickened. On T2weighted images, the mass exhibits increased signal intensity. Necrosis and calcification are rare in this type of tumor (9,45,46). Polypoid lesions enhance moderately and homogeneously on gadolinium-enhanced images. Malignant polypoid lesions are usually larger than 1 cm and demonTeaching strate early and prolonged enhancement; in conPoint trast, benign lesions demonstrate early enhancement with subsequent washout (9,47). Gallbladder carcinoma most commonly manifests as a large solid mass in the gallbladder fossa obscuring the gallbladder, with extension into the liver or adjacent organs (Figs 17, 18). Nonvisualization of the gallbladder and the presence of gallstones within the mass are helpful in making the diagnosis. The mass demonstrates intermediate signal intensity on T1-weighted images and heterogeneously hyperintense signal intensity on T2weighted images. Enhancement is early and prolonged after gadolinium-based contrast material administration (Fig 17) (47). Gadolinium-en- hanced fat-suppressed T1-weighted images are useful in diagnosing tumor extent, direct invasion of surrounding organs, liver metastases, and involvement of critical vascular structures such as the portal vein and hepatic artery (9,39,48). MR imaging has a high sensitivity for the detection of direct hepatic invasion (100%), although it may lead to underestimation of the depth of invasion in 11% of patients. Its sensitivity for the detection of lymphadenopathy is also high (nearly 92%). MR cholangiopancreatography facilitates identification of the site of biliary obstruction, which may be caused by duct compression by the tumor or by lymphadenopathy or induced by duct invasion. MR imaging has a sensitivity of 92% in detecting biliary dilatation but is less efficient (sensitivity of 69%) in detecting bile duct invasion. Microscopic invasion should be suspected in cases of tumor contiguity with a duct, even if a biliary obstruction cannot be visualized. Small peritoneal implants may be better appreciated on delayed gadolinium-enhanced fat-suppressed T1-weighted images (9,39). RG f Volume 28 ● Number 1 Catalano et al 151 Figure 18. Lymphoma of the gallbladder in a 37-year-old man who presented with weight loss and vague abdominal pain. (a, b) Contrast-enhanced fat-suppressed arterial phase (a) and portal venous phase (b) T1-weighted MR images demonstrate irregular thickening of the gallbladder wall in the fundus, with an associated soft-tissue mass (arrows in a, black arrows in b) infiltrating the liver. A focal lesion in the liver, one of several deposits of lymphoma, is also seen (white arrow in b). A single retroperitoneal lymph node is evident (arrowhead in b). (c) MR image obtained at a higher level demonstrates biliary ductal dilatation (black arrows) and additional parenchymal lesions (white arrows). (d) MR cholangiopancreatogram demonstrates an irregularly contoured gallbladder with biliary ductal dilatation. Arrow indicates an obstruction; arrowheads indicate a biliary stent. Lymphoma of the Gallbladder Lymphoma of the gallbladder is rare and may represent primary non-Hodgkin lymphoma from mucosa-associated lymphoid tissue or may be secondary to systemic disease (49,50). Primary lymphoma is extremely rare, having been reported in only about 20 cases. At MR imaging, it is difficult to differentiate between primary gallbladder cancer and gallbladder lymphoma. MR imaging findings include thickening of the gallbladder wall; a mass in the gallbladder fossa with extension into the liver, with the mass being hypointense on T1-weighted images and hyperintense on T2-weighted images relative to the liver; biliary obstruction; and lymph nodes in the porta hepatis (Fig 18). Tumor extension into the liver may mimic adenomyomatosis at US, but MR cholangiopancreatograms will not show the string of beads sign, a sign that is typical of adenomyomatosis and allows its identification (51). Endometrial Implants on the Gallbladder Rarely, endometrial implants may occur on the surface of the gallbladder. Contrast-enhanced T1- and T2-weighted MR images will demonstrate the presence of blood products with variable enhancement (Fig 19). 152 January-February 2008 RG f Volume 28 ● Number 1 Figure 19. Endometrial implant on the surface of the gallbladder in a 35-year-old woman with right upper quadrant pain. Liver function tests showed no abnormalities. US disclosed a mass in hepatic segment IV. (a) Axial fatsuppressed T1-weighted MR image shows a hyperintense mass (arrow) on the medial surface of the gallbladder. (b) On an axial T2-weighted MR image, the mass is hypointense (arrow), a finding that suggests the presence of subacute blood. Functional Evaluation of the Gallbladder in Patients with Acute Symptoms MR cholangiography can be used to evaluate gallbladder function in terms of volume and ejection fraction following ingestion of a fatty meal or the infusion of cholecystokinin. The gallbladder ejection fraction following the infusion of cholecystokinin has been found to correlate with that measured at hepatobiliary scintigraphy performed with HIDA. It is possible to assess the patency and range of contractions of that portion of the bile duct covered by the sphincter of Oddi with pharmacodynamic MR cholangiopancreatography after the ingestion of a fatty meal or the infusion of secretin (52). Contrast-enhanced MR cholangiography with MnDPDP or gadolinium BOPTA can be used to assess gallbladder function as well as biliary obstruction (Fig 20) (53). For MnDPDP-enhanced MR cholangiography, 0.5 mL/kg of MnDPDP up to a maximum of 35–50 mL is slowly injected intravenously for 1–2 minutes, followed by a 10-mL saline flush. The patient is scanned 15–30 minutes after injection to obtain MnDPDP-enhanced T1-weighted MR cholangiopancreatograms. For MR cholangiography with gadolinium BOPTA, 0.05 mmol (0.1 mL)/kg of gadolinium BOPTA up to a maximum of 15 mL is administered intravenously with a power injector at a rate of 2 mL/sec, followed by a 20-mL saline flush. During intravenous administration, dynamic vascular images are acquired with the same scanning delay and parameters that are used with any nonhepatospecific extracellular gadolinium chelate. At 30 – 60 minutes after injection, the patient is rescanned to take advantage of the biliary excretion and to obtain gadolinium-enhanced T1weighted MR cholangiopancreatograms. Normally, contrast-enhanced bile will appear bright in both the gallbladder lumen and the bile ducts on delayed T1-weighted images. In our experience, contrast-enhanced bile will not accumulate in the gallbladder lumen in cases of compromised gallbladder function or cystic duct obstruction. Postoperative Functional Evaluation of the Gallbladder and Biliary Tree The presence of air in the biliary system is common following endoscopic retrograde cholangiopancreatography, endoscopic papillotomy, and the creation of biliary-enteric anastomoses. Because the air is nondependent within both the gallbladder and the biliary tree, it is seen as a nondependent signal void–fluid level on T2-weighted images. MR imaging may be useful in identifying noncalcified dropped gallstones, since CT may fail to depict them. With T2-weighted sequences, these stones appear as focal well-defined signal voids, whereas with T1-weighted sequences their signal intensity is variable. The surrounding inflammatory tissue is hyperintense on T2-weighted images and shows variable enhancement after the administration of gadolinium-based contrast material. If an abscess has developed, it appears as a relatively well-defined fluid collection with rim enhancement. RG f Volume 28 ● Number 1 Catalano et al 153 Figure 20. Preoperative MnDPDP-enhanced MR cholangiographic evaluation for living donor liver transplantation. (a) Axial fat-suppressed T1-weighted MR image shows the gallbladder and cystic duct containing bright bile (arrow), a finding caused by the excretion of contrast material into the bile. The heterogeneous signal intensity within the gallbladder is due to incomplete mixing of the contrast material and bile. (b) Maximum-intensity-projection image of the gallbladder and liver demonstrates the normal intra- and extrahepatic bile ducts and gallbladder. MR cholangiopancreatography, especially with MnDPDP, is useful in identifying postoperative biliary leaks, biliary strictures, and cystic duct leaks (54). Contrast-enhanced T1-weighted MR cholangiography with intravenous hepatobiliary contrast agents, either in combination with conventional MR cholangiography or as a single delayed contrast-enhanced study, can help differentiate biliary-enteric anastomotic strictures from functional obstruction and help identify postoperative leaks (55–57). In a series of 13 patients with hepaticojejunostomies, Hottat et al (58) compared the accuracy of MnDPDP-enhanced functional MR cholangiography with that of conventional T2-weighted MR cholangiography in assessing anastomotic stricture. Although seven patients had dilated intrahepatic bile ducts at T2-weighted MR cholangiography, only two were found to have delayed excretion of MnDPDP at T1-weighted imaging. These two patients were also the only ones in whom percutaneous transhepatic cholangiography showed strictures requiring dilation (58). The tendency of conventional T2-weighted MR cholangiography to lead to overestimation of strictures in cases of biliary ductal dilatation has been documented previously (59). Although these findings are preliminary, they dovetail with current imaging concepts, and functional MR cholangiography would appear to afford an opportunity to streamline imaging protocols. Future Applications: Assessment of Angiogenesis Unresectable gallbladder cancer has traditionally had an extremely poor prognosis due to the lack of success with traditional chemotherapeutic treatment. Novel treatment methods with the socalled angiogenesis inhibitors are being devised that target the vascular supply of the tumor. These agents may be used alone or in combination with conventional therapies. 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Radiology 2004;231: 101–108. 60. Morgan B, Utting JF, Higginson A, Thomas AL, Steward WP, Horsfield MA. A simple, reproducible method for monitoring the treatment of tumours using dynamic contrast-enhanced MR imaging. Br J Cancer 2006;94:1420 –1427. 61. Muruganandham M, Lupu M, Dyke JP, et al. Preclinical evaluation of tumor microvascular response to a novel antiangiogenic/antitumor agent RO0281501 by dynamic contrast-enhanced MRI at 1.5 T. Mol Cancer Ther 2006;5:1950 –1957. This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician’s Recognition Award. To obtain credit, see accompanying test at http://www.rsna.org/education/rg_cme.html. RG Volume 28 • Volume 1 • January-February 2008 Catalano et al MR Imaging of the Gallbladder: A Pictorial Essay Onofrio A. Catalano, MD, et al RadioGraphics 2008; 28:135–155 ● Published online 10.1148/rg.281065183 ● Content Codes: Page 141 On T2-weighted images, the gallbladder wall may show increased signal intensity and thickening (more than 3 mm). This finding must be differentiated from gallbladder wall thickening related to other causes (eg, hypoproteinemic states) (Fig 6) (2–4). Page 142 The enhancement is usually smooth, slow, and prolonged (Fig 10), unlike in gallbladder carcinoma, in which it is usually irregular, early, and prolonged (3,4). Page 147 The "string of beads sign," the hallmark of adenomyomatosis at MR imaging, refers to high-signalintensity foci in the gallbladder wall on T2-weighted images, findings that correspond to bile-filled Rokitansky-Aschoff sinuses. This sign is highly specific (92%) in diagnosing gallbladder adenomyomatosis versus gallbladder cancer. Page 148 Gallbladder carcinomas most often manifest as diffusely infiltrating lesions extending into the liver (~68% of cases) and less often manifest as intraluminal polypoid masses or mural thickening (37). Page 150 Malignant polypoid lesions are usually larger than 1 cm and demonstrate early and prolonged enhancement; in contrast, benign lesions demonstrate early enhancement with subsequent washout (9,47).