Symposium on Radiology in Internal Medicine
Radiologic Approach to Obstructive Jaundice and Pancreatic Disease Irvin F. Hawkins, M.D.,* Alexander M. MacGregor, M.D.,** and Atis Freimanis, M.D. ***
The diagnostic evaluation of the jaundiced patient occasionally can pose a formidable problem to the clinician. Evaluation of pancreatic disease without jaundice can be still more frustrating since even laparotomy may be inconclusive. 21 Obstructive jaundice can usually be diagnosed accurately by clinical and laboratory tests. However, with long-standing disease, and intrinsic hepatic disease with biliary stasis, the laboratory data frequently are misleading. In these cases radiologic evaluation is invaluable. Since surgery may be deleterious in patients with hepatocellular disease, accurate diagnosis is imperative. This paper will review the radiologic procedures which may be employed to evaluate patients with jaundice and those suspected of having pancreatic disease. Space does not permit discussion of history, physical or laboratory findings. Each radiologic procedure will be discussed separately emphasizing its applicability and accuracy. Plain film findings, barium studies, cholecystography, cholangiography, endoscopic pancreatocholangiography, radioisotopic examinations, ultrasound, direct cholangiography (percutaneous and transvenous), angiography and operative cholangiography will be discussed in separate sections. Inevitably, there will be some overlapping with the radiologic approach for investigation of hepatomegaly. A disproportionate amount of space will be devoted to ultrasound since it is a relatively new noninvasive procedure which is becoming readily available and is proving to be valuable for abdominal masses and particularly pancreatic pseudocyst. Only one of the authors (A.K.F.) has extensive experience in the field. Finally an outline of our radiologic approach to jaundice and pancreatic disease will be discussed. "Associate Professor, Department of Radiology, University of Florida College of Medicine, Gainesville ''''Associate Professor, Department of Surgery, University of Florida College of Medicine, Gainesville *""Professor and Chairman, Department of Radiology, Medical College of Ohio, Toledo Supported by NIH Grant No. HL-05856-06S1
Medical Clinics of North America- Vo!. 59, No. 1, January 1975
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PLAIN ABDOMINAL RADIOGRAPHS Plain abdominal radiographs occasionally provide diagnostic information in the jaundiced patient. They may demonstrate enlargement of the liver or spleen, and occasionally show an enlarged gallbladder as a soft tissue mass in the right upper quadrant. The latter must be differentiated from the right kidney. Gallbladder enlargement in a jaundiced patient usually indicates malignant extrahepatic obstruction as Convoissier pointed out, and is much less common in choledocholithiasis. 34 The chief value of the plain film, however, is to demonstrate cholelithiasis, gallstones in the biliary tree, and calcification in the liver and pancreas (Fig. 1). Some 10 to 30 per cent of gallstones are radiopaque, but only 5 per cent of common bile duct calculi are seen on plain films.90 The presence of radiopaque calculi does not necessarily mean that they are the etiology of the jaundice, since 30 per cent of women and 15 per cent
Figure 1. Anteroposterior radiograph demonstrating calcification in the tail of the pancreas typical of that seen in pancreatitis. Since calcification was confined to the pancreatic tail, carcinoma of the body was suspected. Angiography and later surgery confirmed chronic pancreatitis of the entire organ without evidence of tumor. A normal-sized gallbladder is also present.
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of men over the age of 55 years who come to autopsy are found to have stones. 59 However, carcinoma of the gallbladder is associated with gallstones in 75 to 90 per cent of cases,S2 and the incidence of gallstones is increased in cirrhotics. Only rarely will numerous calculi outline the common bile duct; more frequently stones are recognized in the area of the gallbladder with another in a position compatible with the common bile duct. When a gallstone obstructs the cystic duct, calcium may be deposited in the bile ("limey bile" or "milk of calcium bile") or in the gallbladder wall ("porcelain gallbladder"), 26 cases of which have been reported associated with carcinoma of the gallbladder. 2 The presence of pancreatic calcification (Fig. 1) is significant since it establishes the diagnosis of chronic pancreatitis,15 a condition which can produce inflammatory obstruction of the intrapancreatic portion of the common bile duct.s5 Since most pancreatic calcification occurring in the Western Hemisphere is associated with alcoholic pancreatitis, there is a high incidence of coexistent hepatic cirrhosis. However, this does not rule out coexisting pancreatic carcinoma. Other causes include familial pancreatitis associated with kwashiorkor and hyperparathyroidism. Calcification may occur in the liver associated with hepatoma, metastatic carcinoma, hydatid cysts, angiomas, tuberculomas or gummas. 90 Air in the biliary tree signifies a communication between the extrahepatic biliary tree and the lumen of the gut. This is commonly the result of erosion of a large gallstone through the gallbladder into the small intestine or colon or secondary to malignant ulceration from a gastric or primary colonic lesion.
BARIUM UPPER GASTROINTESTINAL STUDIES Evaluation of the esophagus for the presence of varices and the stomach and the duodenum to exclude neoplasm or peptic ulceration is mandatory in the radiologic investigation of the jaundiced patient. Eaton et alY emphasized the important anatomic relationships of duodenum and biliary structures. The biliary structures form an incomplete ring around the duodenum and when distended create characteristic indentations. The duodenal papilla is situated on the posterior aspect of the descending duodenum while the common bile duct descends behind the apical portion of the duodenal bulb. The cystic duct passes over the apical portion of the bulb to the gallbladder lying adjacent to the anterolateral aspect of the upper descending duodenum. Not uncommonly a pancreatic neoplasm will cause a pressure deformity on the outer aspect of the second part of the duodenum or may encircle and compress it from side to side. However, the duodenum may also be distorted by pancreatitis or pancreatic pseudocysts. Gallstones in the common bile duct tend to lodge in its distal end where the lumen narrows abruptly passing through the duodenal wall. The resultant inflammatory edema commonly involves the duodenal papilla which appears as a smoothly rounded mass on the wall of the second part of the duodenum. Carcinomas of the ampulla produce an irregu-
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lar mass in the same location. Occasionally, both may have similar appearances. Dilatation of the common bile duct due to distal obstruction can be detected on barium examination of the duodenum in 50 per cent of cases62 as an extrinsic·well-defined tubular indentation on the apical part of the duodenal bulb (Fig. 2). However, a similar appearance occurs in 12 per cent of normal nonjaundiced patients 12 due to angulation at the superior duodenal flexure, peristalsis activity, incomplete filling, the cystogastrocolic ligament73 and a nondistended nonpathologic gallbladder. Also, several pathologic processes unrelated to bile duct obstructive disease may simulate an enlarged common bile duct, such as duodenal varices, a dilated hepatic artery, an enlarged quadrant lobe of the liver, masses in the porta hepatis, duodenal ulcer disease and hydrops of the gallbladder. Smooth extrinsic indentation of the outer aspect of the descending duodenum is suggestive of gallbladder enlargement. This sign is particularly reliable in the presence of jaundice. This has to be differentiated from masses arising from the right kidney and liver, hydrops of the gallbladder, duodenocolic apposition, carcinoma of the hepatic flexure,
Figure 2. Barium examination of the duodenum demonstrating a mass lesion along the lesser curvature of the duodenal C loop. This proved to be a primary duodenal adenocarcinoma which obstructed the distal duct. Arrows depict impression on duodenal bulb by the distended common bile duct.
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duodenal hematoma or varices. However, since these are infrequently associated with jaundice, they are seldom the cause of diagnostic confusion. Hypotonic duodenography has a place in the evaluation of ampulla lesions and will often help to define subtle mucosal changes in the second part of the duodenum, serving to eliminate many false positive studies on routine upper GI series. At best this study carries a 75 per cent accuracy in defining duodenal pathology, since differentiation between carcinoma, pancreatitis and normal variants may at times be impossible. l1
CHOLECYSTOGRAPHY AND CHOLANGIOGRAPHY Unfortunately there is no oral or intravenous contrast medium available which will reliably visualize the biliary tree in the face of hepatocellular or sustained jaundice. The value of intravenous cholangiography is usually related to the degree of jaundice and this study is only occasionally effective when the bilirubin level is over 4 mg per 100 ml and often fails in the 2 to 4 mg per 100 ml range, especially if the jaundice has been prolonged or is increasing. Visualization may occur more frequently if the jaundice is intermittent or if the bilirubin is decreasing. Recent reports suggest that slow intravenous infusion of methyl glucamine iodipamide (Cholografin) increases the density of opacification of the biliary tree61 as well as reduces the incidence of associated nausea and vomiting. 9 The average diameter of the normal common bile duct is 8 mm and the maximum normal diameter is 10 to 12 mm.BB In those in whom cholecystectomy has been performed or in whom the cystic duct is obstructed, partial obstruction can be inferred from an abnormal time-density relationship.sB Normally the concentration of contrast in such patients should be maximal between 30 and 60 minutes post injection and diminished at 2 hours. If the density is greater at 2 hours than at 1, partial obstruction can be inferred. Presumably the time-density relationship also forms the basis for the occasional success of slow infusion cholangiography. Increasing the dose above an optimum range is without benefit since this only decreases hepatic excretory efficiency and increases the amount excreted by the kidneys.2o When conventional oral and intravenous cholangiography fail to demonstrate the ducts, the technique described by Salzman et al. in 1959,72 may be considered. Iopanoic acid (Telepaque) is administered on four successive days and calculi coated with bile pigment may absorb sufficient opaque medium onto the pigment to render them radiopaque. This has been successful with bilirubin levels of up to 5 mg per 100 ml and more often with common duct calculi than gallbladder stones. 72
ENDOSCOPIC PANCREATOCHOLANGIOGRAPHY A retrograde approach to the bile and pancreatic ducts has become possible with the development of the side viewing fiber duodenoscope, through which the ampulla of Vater can be visualized and cannulated.
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The overall success rate for cannulation ranges from 61.5 to 77 per cent. Kasugai et al. 40 report successful cannulation in 93 of their last 96 attempts. The improved success rates being reported indicate the importance of skill and experience with the technique. Blumgart et al4 were able to define the cause of jaundice in 109 of 145 patients studied. Although this procedure may demonstrate obstructive etiology in traumatic stricture and bile duct neoplasm, the retrograde cholangiogram may fail to provide the surgeon with the next most critical piece of information, namely, the proximal extent of the lesion. Kasugai et al. 39 • 40 have defined the normal and pathological appearance of the pancreatic duct system as seen by pancreatocholangiography, and Weiss et al. 86 describe its use in 258 patients with suspected pancreatic disease without complications. The ability to visualize the pancreatic duct system without operation is a considerable advance, and the method offers a simultaneous opportunity to evaluate the stomach and duodenum and the whole biliary tree, obtain pancreatic secretions and bile for cytology, as well as obtain biopsy specimens of suspect areas at the duodenal papilla. Also the peristalsis and emptying of the pancreatic duct can be directly observed. The procedure is contraindicated in patients whose tests for hepatitis B antigen are positive, since the duodenoscope cannot be sterilized. The major disadvantage of the procedure in pancreatic neoplasm is the inability to detect small tumors that do not involve the major pancreatic ducts. Usually neither small duct not acinar filling occurs, and if one increases the injection pressure to opacify these structures, the risk of producing pancreatitis is also increased. Also the extent of the lesion cannot be determined. The size and location of the lesion can more readily be determined by ultrasound and angiography.
RADIOISOTOPIC EXAMINATIONS Liver Radioiodinated rose bengal is cleared from the blood by the hepatic parenchymal cells and excreted through the biliary tree into the intestinal tract and therefore images the biliary tree. Normal patients have maximal hepatic uptake at 20 to 30 minutes and begin to show intestinal radioactivity at 30 to 60 minutes. No intestinal radioactivity by 90 minutes suggests obstruction, and if follow-up images over the next 24 hours confirm this finding, the diagnosis of extrahepatic biliary obstruction is established, provided hepatocellular disease is excluded by undertaking simultaneous blood clearance de termination s. U sing the head as a nonhepatic pool, the 20 minute count rate should be no greater than 55 per cent of the 5 minute count rate. Marked reduction in clearance indicates hepatocellular disease. A blood retention of 90 per cent or more at 20 minutes and the passage of radioactivity into the intestine indicate "medical" jaundice in 95 per cent of cases. Failure of intestinal activity to appear at 24 hours plus a blood retention of 70 per cent or less indicate extrahepatic obstruction. Extension of the radioac-
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tivity from the inferior margin of the liver indicates extrahepatic obstruction regardless of the blood clearance rate,17 Recent clinical studies suggest a diagnostic accuracy rate using the rose bengal technique of approximately 95 per cent.22. 27. 87 The use of colloidal radiopharmaceuticals (such as 99mTc sulfur colloid) which are phagocytosed by the Kupffer cells of the liver's reticuloendothelial system demonstrate the hepatic substance with negative shadows cast by dilated ducts and metastatic lesions. lo • 32 In hepatocellular diseases this technique demonstrates a diffuse decrease in hepatic radioactivity plus an increased uptake by the bone marrow and spleen. Pancreas Blau and Manske3 introduced the use of selenium tagged methionine for pancreatic scanning. The gamma emitter selenium-75 was substituted for the sulfur atom in methionine. Fifteen minutes after intravenous injection, 80 to 90 per cent is removed from the plasma, and by 60 minutes labeled proteins are predominantly in the zymogen granules. Radioactivity appears in the pancreatic juice at 45 minutes, reaches a maximum at 90 to 180 minutes, and gradually diminishes over the next several hours. The avidity of the pancreas for amino acids is such that its peak radioactivity level occurs about 30 minutes after injection. Accordingly, this technique reflects primarily the labeling of digestive enzymes. 29 Overall results indicate a general agreement over figures of 10 to 30 per cent false negatives and 30 per cent false positive rates. 68 Riccobon069 has noted a false positive rate of 30 per cent and false negative of 30 per cent in a recent review of 1300 patients. The major difficulty appears to stem from generalized dysfunction which can occur in the normal and in acute and chronic pancreatitis, pancreatic pseudocysts and neoplasm. On the other hand scanning seldom fails to demonstrate major abnormality, when present, but of itself it is incapable of defining the etiologic factor or factors involved. For example, in investigating an abdominal mass a normal scan would rule out a pancreatic abnormality with a relatively high degree of accuracy. Figure 3 illustrates absence of radioactivity in the body and tail of the pancreas secondary to pancreatic carcinoma.
ULTRASOUND As early as 1949, George Ludwig50 proposed the use of echography (reflected ultrasound imaging) as a method for detection of gallstones. The application of ultrasound for this purpose failed to achieve prominence for about two decades. With the recent improvement of ultrasound imaging systems, evaluation of the biliary tree and diseases related to it is again becoming more promising. The main applications of ultrasound in the diagnosis of jaundice are evaluation of the gallbladder and, to a lesser extent, the bile ducts; diagnosis of neoplasms and other masses in the pancreas and vicinity, causing obstruction of the common or other bile ducts; and evaluation of the liver, especially for intrahepatic masses.
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Figure 3. Rectilinear "Se selenomethionine scan of a patient with pancreatic carcinoma of the body and tail. Normal uptake by the liver (L) is noted in the patient's right upper quadrant. Normal isotopic uptake noted only in the head of the pancreas (PH). No activity is noted in the body and tail.
Examination of the Gallbladder and the Bile Ducts The normal gallbladder is somewhat difficult to demonstrate echographically, mostly because in the normal person in the average state it is rather a small organ. The technique for demonstration consists of systematic examination of the approximate area of the location of the gallbladder with rather high gain settings on the instrument so that most solid structures are filled with echoes. 26 ,35 Under those circumstances only liquid-containing structures will remain transonic (meaning that they transmit sound but do not return many echoes from the inside), and thus the gallbladder can be identified as a structure of typical shape and free of internal echoes. DILATATION. The major value of ultrasound in the diagnosis of lesions of the gallbladder is determination of dilatation as a result of obstruction. It is to be no'ted that in some cases, especially if there is biliary stasis, the gallbladder may be surprisingly large and yet not obstructed. There is no absolute upper limit of normal, but a cross-sectional diameter of over 3 to 4 cm is unusual. STONES. As originally proposed by Ludwig,50 stones should return fairly strong and readily detectable echoes and they do. Just as our experience in general roentgenology suggests, stones may be found in a dependent portion of the gallbladder, floating in the bile at some intermediate level, in which case a horizontal plane of echoes may be produced if there is more than one or just a few stones, and lastly, rarely, the stones
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may float to the top. Fairly meticulous technique is necessary to make sure that echoes caused by reverberation are not misinterpreted as gallstones. Demonstration of mobility of these stone echoes is a further confirming piece of evidence in favor of this diagnosis. OTHER LESIONS. Cholesterol polyps or carcinoma of the gallbladder will produce stronger echoes than bile, but weaker echoes than surrounding connective tissue or gallstones. BILE DUCTS. Normal bile ducts are difficult to identify because of their small diameter. If the ducts become dilated, they often can be identified on echo graphic examinations of the upper abdomen. This is facilitated by multiple, fairly closely spaced sections; investigators working in this area now recommend that sections be obtained 0.5 cm apart when looking specifically for bile ducts, the gallbladder and gallstones. Both cross and longitudinal, sections need to be obtained. The visualized contrast roentgen cholecystogram is a far superior means of diagnosis. Ultrasonic cholecystography becomes valuable if the gallbladder cannot be visualized by x-ray, in patients with allergy to contrast, and in pregnancy.
The Pancreas Echographic diagnosis of pancreatic lesions is a major subject in itself. Space does not permit complete discussion here. Suffice it to say that pseudocysts 19 , 45, 47 are ideally suited for echo graphic detection and will appear as transonic structures almost anywhere in the usual location of the pancreas, Pseudocysts, however, are not a common cause of jaundice, Pancreatic tumors, of course, are a common cause of jaundice and are frequently identifiable. Pancreatic carcinoma on echograms ordinarily will appear as a lumpy structure in the area of the pancreas. In terms of its echo graphic internal characteristics, a carcinoma may be more transonic than surrounding structures, or it may be a lesion with a relatively clear peripheral zone and internal echoes (Fig. 4), or occasionally it may appear as a
Figure 4. Echographic cross section of the upper abdomen 6 cm. above the level of the iliac crest in a patient with fairly advanced carcinoma of the pancreas. A mass is apparently connected to the portal structures of the liver, but is too far posterior to be the liver (arrows). It is irregular in outline and has heavy internal echoes with a somewhat clearer peripheral zone. L, liver; St, stomach; A, abdominal aorta; Sp, spine; K, partially visualized right kidney.
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structure producing better echoes than the surrounding structures and organs. The transonic variety seems to be the most common with today's ultrasonic equipment. On unusual occasions, a tumor of the pancreas may be echographically of exactly the same characteristics as the pancreas itself, and it will be difficult to detect unless it has a well defined outline, which is not usual in pancreatic carcinoma. The head and the body of the pancreas can normally be examined reasonably easily by echography; the tail is relatively difficult because of overlapping by the stomach which produces acoustic shadows. Occasionally, the tail can be approached by echo graphic scanning from the back. Carcinoma in the tail of the pancreas ordinarily will not cause jaundice unless liver metastases or subhepatic masses are present. 15 , 19, 79 Acute pancreatitis is usually not the cause of jaundice. Chronic pancreatitis with in duration around the distal part of the common bile duct may obstruct it and thus cause jaundice. The demonstration of pancreatitis is the subject of interesting echo graphic studies at the present. The normal pancreas produces more echoes than the liver, spleen and kidneys, bu t fewer echoes than the surrounding connective tissue structures. Thus, it is more difficult to demonstrate than the liver, spleen and kidneys and often cannot be identified or only partially so. With effort and with the newer scanning apparatus it may be shown. Edema, as in pancreatitis, enlarges the pancreas and makes it more transonic. Chronic pancreatitis at times, especially during exacerbations, appears similar to the acute variety. In many cases, however, the gland will not be as much enlarged and, if calcifications are present, internal echoes will be identified. Pancreatic echography at present is not suitable as a tool for detection of carcinoma in asymptomatic patients. There is excellent reason to apply echography as one of the first diagnostic examinations in patients with suspected pancreatic or peripancreatic disease (even before barium gastrointestinal studies), since it is noninvasive and the best pictures will be obtained prior to the administration of barium46 or other intestinal distention-producing measures. The echo graphic information will help direct the type and sequence of subsequent studies.
The Liver The liver with present equipment appears transonic and relatively homogeneous. Intrahepatic masses such as abscesses, primary tumors and metastases may produce a number of different patterns, mostly related to the interface between the mass and the surrounding liver or internal echo patterns in the lesion. Studies of the relative value of echographic scanning in comparison to radioisotope scintiscanning suggest that at the present time scintiscanning has a slight advantage over echography.49 Scintiscanning produces a few more false positives than echographic studies, which in turn produce a few more false negative examinations. Returning specifically to the subject of this paper, in evaluation of jaundice, echo graphic examination of the liver would be recommended mostly if the liver scan or a rose bengal radioactive study do not
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yield satisfactory information and a further search for intrahepatic or subhepatic masses needs to be made. In such cases ultrasonic B-scanning may be a major contribution and sometimes is the sole diagnostic test of help.23, 44, 53, 55, 58, 65, 67, 81 Scattered intrahepatic disease other than metastases - especially irregular areas of hepatitis and dilated bile ducts-in themselves can cause echo returns suggesting ~ntrahepatic lesions. A Short Look at the Future Present day ultrasonic equipment provides a high contrast (essentially black and white) picture mostly because of the use of storage oscilloscopes. Equipment permitting the display of gray-scale images is now under development and will soon become widely available. This display capability is expected to raise the diagnostic accuracy and ease of use in the area of both the liver and the pancreas by at least a full range of magnitude. It will then be quite readily possible to demonstrate the relative echo graphic characteristics of the liver, the pancreas and other organs as well as their normal internal components and abnormal masses.
DIRECT CHOLANGIOGRAPHY In spite of the extensive battery of tests available, there remain cases of jaundice in which efforts fail to differentiate hepatocellular from obstructive jaundice. The prognosis and treatment is very different in these two indications, and a further attempt should be made to define the problem by injecting contrast medium directly into the intrahepatic bile ducts. Direct cholangiography is also useful in known obstructive disease where the cause and site of the obstruction is not known. Since the proximal extent of the obstruction is best defined from the hepatic side, this approach has great value to the surgeon planning to palliate a bile duct carcinoma or reconstruct a bile duct stricture.
PERCUTANEOUS TRANSHEP ATIC CHOLANGIOGRAPHY Insertion of a needle through the liver parenchyma percutaneously either from anterior or lateral directions with injection of contrast into a bile duct has been used for many years36 , 77 and is successful in most cases in which the bile ducts are dilated. Overall success rates in cases in which the ducts are not dilated range between 20 and 50 per cent. 16 , 90 The overall frequency of complications is about 5 per cent in published series. Biliary peritonitis occurs in 3 per cent and bile leakage adds another 1.7 per cent. 91 The overall mortality rate is 0.5 per cent. 16 Recent cases have been documented of septicemia and shock due to the formation of iatrogenic bile-venous fistulas in the presence of pre-existing cholangitis.57 For this reason the procedure is contraindicated in patients with a history of cholangitis unless appropriate antibiotic cover is instituted or sequential surgical exploration performed.
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JUGULAR TRANSVENOUS CHOLANGIOGRAPHY Hanafee and Weiner 8 developed an approach through the jugular venous tree and have subsequently reported their results. 28 ,37 Successful cholangiograms were obtained in 85 per cent of those with proven bile duct obstruction and 22 per cent of those with nonobstructed ducts. By entering the ducts from within the liver it was hoped to avoid the complications of capsular perforation with bleeding and bile peritonitis. This would eliminate the need for routine sequential surgical exploration recommended by some with the percutaneous transhepatic approach.56 Complications have been related mainly to leakage of bile into the venous system with febrile reactions and septic shock; one fatality has been reported to date. Approximately half of the patients had a previous history of cholangitis. The authors now consider this procedure contraindicated in patients with a prior history of cholangitis. 37 Others consider cholangitis much less of a problem. 71
FEMORAL AND ANTECUBITAL TRANSVENOUS CHOLANGIOGRAPHY To radiologists familiar with the femoral and antecubital approach to arteriography and venography, introduction of a catheter via the femoral or antecubital vein is probably more easily performed. We have been using this approach to direct cholangiography over the past 2 years30 (Figs. 5 and 6). We have done 15 transvenous procedures successfully, with the only complication being transient septicemia in a patient in whom prophylactic antibiotics were inadvertently withheld. This technique has the same potential benefits and disadvantages as the jugular route. The transvenous approach also permits biopsy to be performed under fiuoroscopic control. It eliminates the complication of bleeding and may be the more appropriate technique where coagulation parameters are not normal. 28 . 30. 71
ANGIOGRAPHY Considerable experience has been accumulated in recent years with angiographic evaluation of hepatic, biliary and pancreatic pathology. Hepatic angiography can be helpful in the jaundiced patient by demonstrating the shrunken liver of end-stage liver disease (Fig. 7), the presence of hepatoma or cholangiocarcinoma, and avascular metastatic lesions as small as 0.5 cm in diameterY' 63. 64 Angiographic diagnosis of carcinoma of the gallbladder has been described!' 70 and its usefulness in evaluating the extent of hepatic and regional spread has been recently reported. 78 Angiographic diagnosis of bile duct carcinoma is more difficult because of the absence of vascular change, particularly in the sclerosing type of lesion. Pancreatic angiography has become established as a safe, accurate
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Figure 5. Femoral transvenous cholangiogram in a 45 year old jaundiced patient with previous right hepatectomy secondary to an auto accident. A No. 8 French polyethylene catheter is positioned in the left hepa tic vein. A coaxial No. 4 French Tefion catheter (white arrow) is shown in the dilated left biliary radical. Arrows denote severe stricture of the distal bile duct.
method for evaluation of the presence and extent of pancreatic disease. 5. 42. 51.52 The angiographic diagnosis of pancreatic carcinoma initially had limited success, but with the advent of superselective, magnification and pharmacodynamic techniques accurate diagnosis can be made in approximately 95 per cent of patients, providing satisfactory detail of the intrapancreatic vasculature is obtained. H • 31. 52 Tumors as small as 1.5 cm in diameter have been detected by this method,52 permitting surgical resection at an early and potentially curable stage (Figs. 8 and 9). An additional advantage of angiography from the surgeon's viewpoint is demonstration of the vascular anatomy, revealing an anomalous arterial supply and thus giving a road map for the performance of surgical resection. Similarly invasion of larger arteries and portal venous involvement indicates that the lesion is not resectable. It is our experience that in the diagnosis of small lesions the evaluation of arterial and capillary phases for evidence of encasement and small vessel cutoff is more important than the venous changes emphasized by others,6 since we have found portal venous involvement only in association with fairly advanced lesions for which surgical extirpation offers little. We have also found angiography to be helpful in differentiating pancreatic carcinoma from chronic pancreatitis (Fig. 10).
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Figure 6. Transvenous cholangiogram of a 30 year old jaundiced woman demonstrating a meniscus (arrows) characteristic of an intraluminal mass (gallstone). Exploratory surgery two weeks previously demonstrated a porta hepatis mass which was felt to represent a rhab· domyosarcoma. Reexploration post angiogra phy verified the gallstone.
OPERATIVE AND POSTOPERATIVE CHOLANGIOGRAPHY Intraoperative cholangiography as a routine procedure during cholecystectomy is being utilized by many surgeons in preference to limiting it to cases with chemical indications, since several authors have shown that unsuspected common duct calculi are found in 3 to 10 per cent of patients undergoing cholecystectomy. IS. 25 The procedure should add only a few minutes to the operative time and reduce the number of negative duct explorations. The procedure carries a false positive rate of 2 to 7 per cent and a false negative rate of 1 to 4 per cent. 13 • 33. 76 In icteric patients in whom preoperative cholangiography has not been obtained, intraoperative cholangiography is mandatory to identify or exclude biliary tree obstruction. It is important to define the whole biliary tree during this procedure to exclude sclerosing cholangitis, intrahepatic biliary calculi and tumors, or unrecognized distal obstructive lesions, whether or not the extrahepatic bile duct is dilated. 4 3 The techniques and sources of potential error are well recognized. s (Text continued on page 139.)
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Figure 7. A, Arterial phase, and B, capillary phase, of a celiac arteriogram done in a 65 year old woman with a history and laboratory findings typical of obstructive jaundice secondary to pancreatic carcinoma. After the intraarterial infusion of a vasodilator (tolazoline [Priscoline]), a normal pancreas (arrows) and a small end stage liver (L) were demonstrated.
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Figure 8. Selective hepatic artery injection after infusion of a vasodilator (tolazoline [Priscoline]) in a 52 year old jaundiced patient demonstrates an amputated branch of the anterior arcade (arrow) and tumor encasement of multiple small intrapancreatic arteries (superior and right of arrow). A 1.5 cm adenocarcinoma was later excised. H, hepatic artery; CD, gastroduodenal artery.
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Figure 9. Selective gastroduodenal artery (CD ) injection in a 55 year old woman demonstrates amputation of the posterior arcade, a small pseudoaneurysm (large arrow) and encasement of small arteries (small arrows). A Whipple procedure was performed and a 1.5 cm adenocarcinoma was discovered. The patient is alive 3'1. years post surgery.
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Figure 10. A, Arterial phase, and B, capillary and venous phase, of selective high-pressure high-volume gastroduodenal artery (CD) injection after intraarterial infusion of tolazoline (Priscoline), demonstrating filling of the entire pancreas (P H, head; P B, body; PT, tail). An avascular area below the pancreas plus the curvilinear displacement of the omental arteries and veins (arrows) suggest a pancreatic pseudocyst. The increased capillary and venous phase and irregular small intrapancreatic arteries are frequently seen with pancreatitis.
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Burhenne7 has recently described a technique of removal of retained common bile duct calculi using a modified ureteral stone basket passed through the T-tube sinus tract under fiuoroscopic control. The T-tube must be left in site for 4 weeks in order to permit the tract to mature. Mazzariell054 has reported 90 per cent success in a large series of retained common duct calculi with this method. Renewed interest in nonoperative removal of retained stones by dissolution has been stimulated by reports of the installation of cholic acid, which increases the solubility of cholestero183 and heparin utilizing the zeta potential principle. 24
GENERAL RADIOLOGIC APPROACH The course of the work-up for jaundice and suspected pancreatic carcinoma can be quite varied depending on the patient's history and on the physical and laboratory findings. The selection may be dependent on the expertise and experience of the radiology department with the various diagnostic tools. From the above discussion of the many modalities, one can readily see that the accuracy varies considerably with various investigators. At our institution pancreatic isotopic scanning is not available and ultrasound and endoscopic pancreatocholangiography have only recently been introduced. All three, as stated previously, are relatively nonspecific, although they can be quite helpful. Pancreatic isotopic scanning is important since if the scan is normal there is a high probability that no large pancreatic tumor is present. Ultrasound may detect and delineate the extent of larger pancreatic tumors and is particularly accurate for pancreatic pseudocysts. Endoscopic pancreatocholangiography may demonstrate stones or strictures in the ductal systems. In jaundiced patients plain films are obtained. If the patient is jaundiced, the oral cholecystogram is omitted since the gallbladder will not usually be visualized. If the bilirubin is less than 3 mg per 100 ml, an intravenous cholangiogram is performed. If the bilirubin is higher than 3 mg per 100 ml or if the intravenous cholangiogram does not result in visualization, a slow infusion cholangiogram is performed. Recently ultrasound has been requested prior to the gastrointestinal series. If equivocal findings are noted on the GI series, hypotonic duo denography is done immediately. A 99mtechnetium sulfur colloid scan is performed to evaluate the liver for primary metastatic lesions as well as for dilated bile ducts. If the scan suggests hepatic disease or if a pancreatic lesion is suspected, angiography is performed. Conventional celiac and SMA arteriography usually permits diagnosis of only larger lesions, but it may be very helpful in detecting liver and gallbladder disease. High pressure superselective angiography or pharmacoangiography usually is extremely valuable. This type of angiography has detected tumors as small as 1.5 cm, delineated the extent of the lesion and been helpful in differentiating pancreatitis from pancreatic carcinoma. Usually before surgery either percutaneous or transvenous cholangiography is done. In the case of cholelithiasis intraoperative cholangiography should be routinely performed. Figures ·11 and 12 illustrate the usual order of examinations.
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Plain films
--------------s-e-ru-mlJr;l-iru-b-'u------------- Elevated serum Serum bilirubin
< 3 mg per 100 rnl
>3 mg per 100 ml
bilirubin with H x suggesting stone
Tra-nsvenous or percutaneous cholangiography Transvenous or percutaneous char angiography
x - Non-visualization ? - Equivocal findings
Dotted boxes - Studies not available routinely
Figure 11. Work-up of patients with suspected obstructive jaundice.
Plain film
Hypotonic duodenography
Angiography
Figure 12. Work-up for suspected pancreatic lesions in patients without jaundice.
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REFERENCES 1. Abrams, R. M., Meng, C. H., Firooznia, H., Beranbaum, E. R., and Epstein, H. Y.: Angiographic demonstration of carcinoma of the gallbladder. Radiology, 94:277,1970. 2. Berk, R. N., Armbuster, R., and Salztein, S.: Carcinoma of the gallbladder associated with the porcelain gallbladder. Radiology, 106 :29, 1973. 3. Blav, M., and Manske, R. F.: The pancreas specificity of Se" selenomethionine. J. Nucl. Med., 2:102,1961. 4. Blumgart, L. H., Salmon, P. R., and Cotton, P. B.: Endoscopy and retrograde choledochopancreatography in the diagnosis of the patient with jaundice. Surg. Gynec. Obstet., 138:565, 1974. 5. Boijsen, E., and Tylen, U.: Vascular changes in chronic pancreatitis. Acta Radiol., 12:34, 1972. 6. Buranasiri, S., and Baum, S.: The significance of the venous phase of celiac and superior mesenteric arteriography in evaluating pancreatic carcinoma. Radiology, 102: 11, 1972. 7. Burhenne, J. H.: Non-operative obtained biliary stone extraction. A new roentgenologic technique. Am. J. Roent., 117:388, 1973. 8. Custer, D. C., and Clore, J. N.: Source of error in operative cholangiography. Arch. Surg., 100:664, 1970.
9. Darnborovgit, A., and Geffen, N.: Drip infusion cholangiography. Brit. J. Rad., 39:827, 1966. 10. DeLand, F. H. and Wagner, H. N., in Atlas of Nuclear Medicine, Vol. Ill: Reticuloendothelial System, Liver, Spleen and Thyroid. Philadelphia, W. B. Saunders Co., 1972. 11. Eaton, S. 0., and Ferrucci, J. T.: Radiology of the Pancreas and Duodenum. Philadelphia, W. B. Saunders Co., 1973. 12. Eaton, S. 0., Ferrucci, J. T., Margulis, A. F., and Weens, H. S.: Unfamiliar roentgen signs in pancreatic disease. Amer. J. Roentgenol., 116:396, 1972. 13. Edmunds, R., and Hughes, J. H.: Re-exploration of the common bile duct. Arch. Surg., 90:876, 1965.
14. Eisenberger, H., Personal communication, 1973. 15. Engelhart, G., and Blauenstein, U.: Ultrasound in the diagnosis of malignant pancreatic tumors. Gut, 11 :443, 1970. 16. Evans, J. A., Glen, F., Thorbjarnarson, B., and MUjahed, Z.: Percutaneous transhepatic cholangiography. Radiology, 78:362, 1962. 17. Eyler, W. R., Schuman, B. M., DuSault, L. A. and Hinson, R. E.: The radioiodinated rose bengal liver scan as an aid to the differential diagnosis of jaundice. Amer. J. Roentgenol., 94:469, 1965. 18. Ferris, D. 0., and Sterling, W. A.: Surgery of the biliary tract. Surg. Clin. N. Amer., 47:861, 1967. 19. Filly, R., and Freimanis, A.: Echographic diagnosis of pancreatic lesions. Radiology, 96:575, 1970. 20. Fischer, H. W.: Excretion of iodipamide-relation of bile and urine output to dose. Radiology, 84:483, 1965. 21. Forsgren, L., Hansson, K., Lundh, C., and Nordenstam, H.: Pancreatic biopsy. Acta Chir., 134:457, 1968. 22. Freeman, L. M., Kay, C. J., and Derman, A.: Renal excretion of rose bengal: A pitfall in the interpretation of rose bengal abdominal scans. J. Nucl. Med., 9:227, 1968. 23. Freimanis, A.: Echographic exploration of abdominal structures. Crit. Rev. in Radiol. Sci., 1 :207, 1970. 24. Gardner, B.: Experiences with the use of intracholedochal heparinized saline for the treatment of retained common bile duct stones. Ann. Surg., 177:240, 1973. 25. Glass, T. J.: Cholecystectomy and cholangiography. Surgery, 43:452, 1968. 26. Gravelle, I. H., Jones, M., and Roberts, E. S.: The investigation of gallbladder disease. Brit. J. Radiol., 46:568, 1973. 27. Greene, A. G., and Sadowsky, N. L.: A radiologic approach to the differential diagnoses of surgical and non-surgical jaundice. Amer. J. Roentgenol., 116:368, 1972. 28. Hanafee, W., and Weiner, M.: Transjugular percutaneous cholangiography. Radiology, 88:35,1967. 29. Hansson, E.: The formation of pancreatic juice proteins studied with labeled amino acids. Acta Physiol. Scand., 46, Suppl. 161, 1959. 30. Hawkins, I. F.: Intravenous punch biopsy for the liver and kidney capable of cholangiography, renal cyst puncture and bronchial biopsy. Radiology, 105:445, 1972. 31. Hawkins, I. F., Kaude, J. V., and MacGregor, A. M. C.: Priscoline and epinephrine in selective pancreatic angiography: A comparison study using high pressure injection, valsalva maneuver and magnification technique. Radiology, in press. 32. Heck, L. L., and Gottschalk, A.: The appearance of intrahepatic biliary duct dilatation on the liver scan. Radiology, 99:135,1971. 33. Herman, R. E., and Hoerr, S. 0.: The value of routine use of operative cholangiography. Surg. Gynec. Obstet., 121 :1015,1967.
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34. Hess, W.: Surgery of the biliary passages and the pancreas. Princeton, Van Nostrand Co., 1965. 35. Hublitz, U., Kahn, P., and Sell, L: Cholecystosonography: An approach to the nonvisual· ized gallbladder. Radiology, 103 :645, 1972. 36. Hueard, E., and Do-Xuan-Hop: La ponction transhepatique des canaux biliaires. Bull. Soc. Med. Chir. Indochina, 15:1090, 1937. 37. Kadell, B. M., and Weiner, M: Current status of the transjugular approach for direct cholangiography. Surg. Clin. N. Amer., 53:1019,1973. 38. Kakos, G. S., Tompkins, R K., Turnipseed, W., and Zollinger, R M.: Operative cholangiography during routine cholecystectomy. Arch. Surg., 104:484,1972. 39. Kasugai, T., Kuno, N., Kobayashi, S., and Hattori, K.: Endoscopic pancreatocholangiography. I. The normal endoscopic pancreatocholangiogram. Gastroenterology, 63:217, 1972. 40. Kasugai, T., Kuno, N., J(izu,_M., Kobayashi, S.~ and_Hattori, K.: Endoscopic pancreatocholangiography. 11. The pathologic endoscopic pancreatocholangiogram. Gastroenterology, 63:227, 1972. 41. Kaude, J. V., Jensen, R, and Wirtanen, G. W.: Slow injection hepatic angiography. Acta Rad., 14:699, 1973. 42. Khademi, M., Lazaro, E. J., and Rickert, R R: Selective arteriography in the diagnosis of chronic inflammatory pancreatic disease. Amer. J. Roentgenol., 119:141,1973. 43. Legge, D. A., and Carlson, H. C.: Cholangiographic appearance of primary carcinoma of the bile ducts. Radiology, 102:259, 1972. 44. Lehman, J. S.: Ultrasound in the diagnosis of hepatobiliary disease. Rad. Clin. No. Amer., 4:605, 1966. 45. Leopold, G.: Pancreatic echography: A new dimension in the diagnosis of pseudocyst. Radiology, 104:365, 1972. 46. Leopold, G. R, and Asher, W. M.: Deleterious effects of gastrointestinal contrast material on abdominal echography. Radiology, 98:637,1971. 47. Leopold, G., Berk, R, and Reinke, R: Echographic-radiological documentation of spontaneous rupture of a pancreatic pseudocyst into the duodenum. Radiology, 102 :699, 1972. 48. Leopold, G. R, and Sololoff, J.: Ultrasonic scanning in the diagnosis of biliary disease. Surg. Clin. N. Amer., 53:1043,1973. 49. Leyton, B., Halpern, S., Leopold, G., and Hagen, S.: Correlation of ultrasound and colloid scintiscan studies of the normal and diseased liver. J. Nucl. Med., 14:27, 1973. 50. Ludwig, G. D., and Struthers, F. W.: Considerations underlying the use of ultrasound to detect gallstones and foreign bodies in tissue. Naval Medical Research Institute, National Naval Medical Center. Project NM 004001, Report 4, 16 June 1949. 51. Lunderquist, A.: Angiography in carcinoma of the pancreas. Acta. Radiol., Suppl. 235, 1965. 52. MacGregor, A. M. C., and Hawkins, I. F., Jr.: Selective pharmacodynamic angiography in the diagnosis of carcinoma of the pancreas. Surg. Gynec. Obstet., 137:917, 1973. 53. McCarthy, C. F., Davies, E. R, Wells, P. N. T., Ross, F. G., Follett, D. H., Muir, K. M., and Read, A. E.: A comparison of ultrasonic and isotope scanning in the diagnosis of liver disease. Brit. J. Radiol., 43:100,1970. 54. Mazzariello, R: Review of 220 cases of residual biliary tract calculi treated without reoperation. Surgery, 73:299,1973. 55. Melki, G.: Ultrasonic piiltterns of tumors of the liver. J. Clin. Ultrasound, 1 :306, 1973. 56. Misherry, C. K., and Glenn, F.: Surgical aspects of biliary tract disease. Amer. J. Med., 51 :651, 1971. 57. Morettin, L. B., and Dodd, G. D.: Percutaneous transhepatic cholangiography. Amer. J. Dig. Dis., 17:831, 1972. 58. Mountford, R. A., Halliwell, M. and Atkinson, P.: Ultrasonic liver scanning: Automated Ascan analysis. Phy. of Med. and BioI., 18:559,1973. 59. Newman, H. F., and Northrup, J. D.: Collective review: The autopsy incidence of gallstone. Int. Abstracts Surg., 109:1,1959. 60. Oi, I., Kobayashi, S., and Kondo, T.: Endoscopic pancreatocholangiography. Endoscopy, 2:103,1970. 61. Payne, R F.: Drip infusion cholangiography. Clin. Rad., 19:281,1968. 62. Perez, C. A., Powers, W. E., Holtz, S., and Spjut, H. J.: Roentgenologic-pathologic correlation of resectable carcinoma of the pancreatoduodenal region. Amer. J. Roentgenol., 94:438,1965. 63. Pollard, J. J., Fleishli, D. J., and Nebesar, RA.: Angiography of hepatic neoplasms. Radiol. Clin. North. Amer., 8:31, 1970. 64. Pollard, J. J., Nebesar, R A., and Mattoso, L. F.: Angiographic diagnosis of benign diseases of the liver. Radiology, 86:276, 1966. 65. Rasmussen, S.: Liver volume determination by ultrasonic scanning. Brit. J. Radiol., 45:579,1972. 66. Rasmussen, S., Holm, H. H., Kristensen, J., and Barlebo, H.: Ultrasonically-guided liver biopsy. Brit. Med. J., 2:500,1972.
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67. Rasmussen, S. N., Holm, H. H., Kristensen, J. D., Pedersen, J. F., and Hancke, S.: Ultrasound in the diagnosis of liver disease. J. Clin. Ultrasound, 1 :220, 1973. 68. Riccobono, X. J.: Pancreatic scanning. Seminars Roentgenol., 3:310,1968. 69. Riccobono, X. J., personal communication, 1974. 70. Rosch, J., Grollman, J. H., Jr., and Steckel, R J.: Arteriography in the diagnosis of gallbladder disease. Radiology, 92:1485,1969. 71. Rosch, J., Larin, P. C., Antonoric, R., and Dotter, C. T.: Transjugular approach to liver biopsy and transhepatic cholangiography. N. Engl. J. Med., 289:227, 1973. 72. Salzman, E., Spurck, RP., Kier, C., and Watkins, D.: Opacifying gallstones. JAMA, 169:334,1959. 73. Samuel, E.: The cystogastro-celiac band: Radiologic considerations. Brit. J. Radiol., 25:119,1952. 74. Sarles, H.: Chronic calcifying pancreatitis-chronic alcoholic pancreatitis. Gastroenterology, 66:604, 1974. 75. Sarles, H., Sarles, J. C., Carmatte, R, Muratore, R, Gaini, M., Guien, C., Pastor, J., and Leroy, F.: Observations on 205 confirmed cases of acute pancreatitis, recurring pancreatitis and chronic pancreatitis. Gut, 6:545, 1965. 76. Schulenburg, C. A. P.: Operative cholangiography. London, Butterworth and Co., 1966. 77. Shaldon, S., Barber, K. M., and Young, W. B.: Transhepatic percutaneous cholangiography-a new technique. Gastroroentgenology, 42:371, 1962. 78. Sprayregen, S., and Messinger, N. H.: Carcinoma of the gallbladder: Diagnosis and evaluation of regional spread by angiography. Amer. J. Roentgenol., 116:382, 1972. 79. Stuber, J., Templeton, A., and Bishop, K.: Sono graphic diagnosis of pancreatic lesions. Amer. J. Roentgenol., 116:406,1972. 80. Takagi, K., Ikeda, S., Nakagawa, Y., Sakaguchi, N., Takahashi, T., Kumakura, K., Maruyama, M., Someya, M., Nakano, H., Takada, T., Takekoshi, T., and Kin, T.: Retrograde pancreatography and cholangiography by fiber-duodenoscope. Gastroenterology, 59:445, 1970. 81. Taylor, K. J. W., Carpenter, B. E., and McCready, V. R: Grey scale echography in the diagnosis of intrahepatic disease. J. Clin. Ultrasound, 1 :284, 1973. 82. Vaittinen, E.: Carcinoma of the gallbladder. A study of 390 cases diagnosed in Finland 1953-1967. Ann. Chir. Gynaecol. Fenn., 59, Suppl. 168, 1970. 83. Way, L., Admirand, W. H., and Dunphy, J. E.: Management of choledocholithiasis. Ann. Surg., 176:347, 1972. 84. Weiner, M., and Hanafee, W. N.: A review of transjugular cholangiography. Radiol. Clin. N. Amer., 8:53, 1970. 85. Weinstein, B. R, Korn, R J., and Zimmerman, H. J.: Obstructive jaundice as a complication of pancreatitis. Ann. Intern. Med., 58 :245, 1963. 86. Weiss, H. D., Anacker, H., Wiesner, W., and Rupp, N.: Duodenoscopic pancreatography. Radiology, 106:333, 1973. 87. Whiting, E. G., and Nusynowitz, M. L.: Radioactive rose bengal testing on the differential diagnosis of jaundice. Surg. Gynec. Obstet., 127:729, 1968. 88. Wise, RE.: Intravenous Cholangiography. Springfield, Ill., Charles C Thomas, 1962. 89. Wise, R E., Johnston, D. 0., and Salzman, F. A.: The intravenous cholangiography diagnosis of partial destruction of the common duct. Radiology, 68 :507, 1957. 90. Young, W. R: Obstructive jaundice. Amer. J. Roentgenol., 119:4,1973. 91. Zinberg, S. S., Berk, J. E., and Plasencia, H.: Percutaneous transhepatic cholangiography, its use and limitations. Amer. J. Digest Dis., 10:154,1965. Department of Radiology University of Florida College of Medicine Gainesville, Florida 32610
Radiologic Approach to Obstructive Jaundice and Pancreatic Disease Irvin F. Hawkins, M.D.,* Alexander M. MacGregor, M.D.,** and Atis Freimanis, M.D. ***
The diagnostic evaluation of the jaundiced patient occasionally can pose a formidable problem to the clinician. Evaluation of pancreatic disease without jaundice can be still more frustrating since even laparotomy may be inconclusive. 21 Obstructive jaundice can usually be diagnosed accurately by clinical and laboratory tests. However, with long-standing disease, and intrinsic hepatic disease with biliary stasis, the laboratory data frequently are misleading. In these cases radiologic evaluation is invaluable. Since surgery may be deleterious in patients with hepatocellular disease, accurate diagnosis is imperative. This paper will review the radiologic procedures which may be employed to evaluate patients with jaundice and those suspected of having pancreatic disease. Space does not permit discussion of history, physical or laboratory findings. Each radiologic procedure will be discussed separately emphasizing its applicability and accuracy. Plain film findings, barium studies, cholecystography, cholangiography, endoscopic pancreatocholangiography, radioisotopic examinations, ultrasound, direct cholangiography (percutaneous and transvenous), angiography and operative cholangiography will be discussed in separate sections. Inevitably, there will be some overlapping with the radiologic approach for investigation of hepatomegaly. A disproportionate amount of space will be devoted to ultrasound since it is a relatively new noninvasive procedure which is becoming readily available and is proving to be valuable for abdominal masses and particularly pancreatic pseudocyst. Only one of the authors (A.K.F.) has extensive experience in the field. Finally an outline of our radiologic approach to jaundice and pancreatic disease will be discussed. "Associate Professor, Department of Radiology, University of Florida College of Medicine, Gainesville ''''Associate Professor, Department of Surgery, University of Florida College of Medicine, Gainesville *""Professor and Chairman, Department of Radiology, Medical College of Ohio, Toledo Supported by NIH Grant No. HL-05856-06S1
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PLAIN ABDOMINAL RADIOGRAPHS Plain abdominal radiographs occasionally provide diagnostic information in the jaundiced patient. They may demonstrate enlargement of the liver or spleen, and occasionally show an enlarged gallbladder as a soft tissue mass in the right upper quadrant. The latter must be differentiated from the right kidney. Gallbladder enlargement in a jaundiced patient usually indicates malignant extrahepatic obstruction as Convoissier pointed out, and is much less common in choledocholithiasis. 34 The chief value of the plain film, however, is to demonstrate cholelithiasis, gallstones in the biliary tree, and calcification in the liver and pancreas (Fig. 1). Some 10 to 30 per cent of gallstones are radiopaque, but only 5 per cent of common bile duct calculi are seen on plain films.90 The presence of radiopaque calculi does not necessarily mean that they are the etiology of the jaundice, since 30 per cent of women and 15 per cent
Figure 1. Anteroposterior radiograph demonstrating calcification in the tail of the pancreas typical of that seen in pancreatitis. Since calcification was confined to the pancreatic tail, carcinoma of the body was suspected. Angiography and later surgery confirmed chronic pancreatitis of the entire organ without evidence of tumor. A normal-sized gallbladder is also present.
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of men over the age of 55 years who come to autopsy are found to have stones. 59 However, carcinoma of the gallbladder is associated with gallstones in 75 to 90 per cent of cases,S2 and the incidence of gallstones is increased in cirrhotics. Only rarely will numerous calculi outline the common bile duct; more frequently stones are recognized in the area of the gallbladder with another in a position compatible with the common bile duct. When a gallstone obstructs the cystic duct, calcium may be deposited in the bile ("limey bile" or "milk of calcium bile") or in the gallbladder wall ("porcelain gallbladder"), 26 cases of which have been reported associated with carcinoma of the gallbladder. 2 The presence of pancreatic calcification (Fig. 1) is significant since it establishes the diagnosis of chronic pancreatitis,15 a condition which can produce inflammatory obstruction of the intrapancreatic portion of the common bile duct.s5 Since most pancreatic calcification occurring in the Western Hemisphere is associated with alcoholic pancreatitis, there is a high incidence of coexistent hepatic cirrhosis. However, this does not rule out coexisting pancreatic carcinoma. Other causes include familial pancreatitis associated with kwashiorkor and hyperparathyroidism. Calcification may occur in the liver associated with hepatoma, metastatic carcinoma, hydatid cysts, angiomas, tuberculomas or gummas. 90 Air in the biliary tree signifies a communication between the extrahepatic biliary tree and the lumen of the gut. This is commonly the result of erosion of a large gallstone through the gallbladder into the small intestine or colon or secondary to malignant ulceration from a gastric or primary colonic lesion.
BARIUM UPPER GASTROINTESTINAL STUDIES Evaluation of the esophagus for the presence of varices and the stomach and the duodenum to exclude neoplasm or peptic ulceration is mandatory in the radiologic investigation of the jaundiced patient. Eaton et alY emphasized the important anatomic relationships of duodenum and biliary structures. The biliary structures form an incomplete ring around the duodenum and when distended create characteristic indentations. The duodenal papilla is situated on the posterior aspect of the descending duodenum while the common bile duct descends behind the apical portion of the duodenal bulb. The cystic duct passes over the apical portion of the bulb to the gallbladder lying adjacent to the anterolateral aspect of the upper descending duodenum. Not uncommonly a pancreatic neoplasm will cause a pressure deformity on the outer aspect of the second part of the duodenum or may encircle and compress it from side to side. However, the duodenum may also be distorted by pancreatitis or pancreatic pseudocysts. Gallstones in the common bile duct tend to lodge in its distal end where the lumen narrows abruptly passing through the duodenal wall. The resultant inflammatory edema commonly involves the duodenal papilla which appears as a smoothly rounded mass on the wall of the second part of the duodenum. Carcinomas of the ampulla produce an irregu-
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lar mass in the same location. Occasionally, both may have similar appearances. Dilatation of the common bile duct due to distal obstruction can be detected on barium examination of the duodenum in 50 per cent of cases62 as an extrinsic·well-defined tubular indentation on the apical part of the duodenal bulb (Fig. 2). However, a similar appearance occurs in 12 per cent of normal nonjaundiced patients 12 due to angulation at the superior duodenal flexure, peristalsis activity, incomplete filling, the cystogastrocolic ligament73 and a nondistended nonpathologic gallbladder. Also, several pathologic processes unrelated to bile duct obstructive disease may simulate an enlarged common bile duct, such as duodenal varices, a dilated hepatic artery, an enlarged quadrant lobe of the liver, masses in the porta hepatis, duodenal ulcer disease and hydrops of the gallbladder. Smooth extrinsic indentation of the outer aspect of the descending duodenum is suggestive of gallbladder enlargement. This sign is particularly reliable in the presence of jaundice. This has to be differentiated from masses arising from the right kidney and liver, hydrops of the gallbladder, duodenocolic apposition, carcinoma of the hepatic flexure,
Figure 2. Barium examination of the duodenum demonstrating a mass lesion along the lesser curvature of the duodenal C loop. This proved to be a primary duodenal adenocarcinoma which obstructed the distal duct. Arrows depict impression on duodenal bulb by the distended common bile duct.
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duodenal hematoma or varices. However, since these are infrequently associated with jaundice, they are seldom the cause of diagnostic confusion. Hypotonic duodenography has a place in the evaluation of ampulla lesions and will often help to define subtle mucosal changes in the second part of the duodenum, serving to eliminate many false positive studies on routine upper GI series. At best this study carries a 75 per cent accuracy in defining duodenal pathology, since differentiation between carcinoma, pancreatitis and normal variants may at times be impossible. l1
CHOLECYSTOGRAPHY AND CHOLANGIOGRAPHY Unfortunately there is no oral or intravenous contrast medium available which will reliably visualize the biliary tree in the face of hepatocellular or sustained jaundice. The value of intravenous cholangiography is usually related to the degree of jaundice and this study is only occasionally effective when the bilirubin level is over 4 mg per 100 ml and often fails in the 2 to 4 mg per 100 ml range, especially if the jaundice has been prolonged or is increasing. Visualization may occur more frequently if the jaundice is intermittent or if the bilirubin is decreasing. Recent reports suggest that slow intravenous infusion of methyl glucamine iodipamide (Cholografin) increases the density of opacification of the biliary tree61 as well as reduces the incidence of associated nausea and vomiting. 9 The average diameter of the normal common bile duct is 8 mm and the maximum normal diameter is 10 to 12 mm.BB In those in whom cholecystectomy has been performed or in whom the cystic duct is obstructed, partial obstruction can be inferred from an abnormal time-density relationship.sB Normally the concentration of contrast in such patients should be maximal between 30 and 60 minutes post injection and diminished at 2 hours. If the density is greater at 2 hours than at 1, partial obstruction can be inferred. Presumably the time-density relationship also forms the basis for the occasional success of slow infusion cholangiography. Increasing the dose above an optimum range is without benefit since this only decreases hepatic excretory efficiency and increases the amount excreted by the kidneys.2o When conventional oral and intravenous cholangiography fail to demonstrate the ducts, the technique described by Salzman et al. in 1959,72 may be considered. Iopanoic acid (Telepaque) is administered on four successive days and calculi coated with bile pigment may absorb sufficient opaque medium onto the pigment to render them radiopaque. This has been successful with bilirubin levels of up to 5 mg per 100 ml and more often with common duct calculi than gallbladder stones. 72
ENDOSCOPIC PANCREATOCHOLANGIOGRAPHY A retrograde approach to the bile and pancreatic ducts has become possible with the development of the side viewing fiber duodenoscope, through which the ampulla of Vater can be visualized and cannulated.
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The overall success rate for cannulation ranges from 61.5 to 77 per cent. Kasugai et al. 40 report successful cannulation in 93 of their last 96 attempts. The improved success rates being reported indicate the importance of skill and experience with the technique. Blumgart et al4 were able to define the cause of jaundice in 109 of 145 patients studied. Although this procedure may demonstrate obstructive etiology in traumatic stricture and bile duct neoplasm, the retrograde cholangiogram may fail to provide the surgeon with the next most critical piece of information, namely, the proximal extent of the lesion. Kasugai et al. 39 • 40 have defined the normal and pathological appearance of the pancreatic duct system as seen by pancreatocholangiography, and Weiss et al. 86 describe its use in 258 patients with suspected pancreatic disease without complications. The ability to visualize the pancreatic duct system without operation is a considerable advance, and the method offers a simultaneous opportunity to evaluate the stomach and duodenum and the whole biliary tree, obtain pancreatic secretions and bile for cytology, as well as obtain biopsy specimens of suspect areas at the duodenal papilla. Also the peristalsis and emptying of the pancreatic duct can be directly observed. The procedure is contraindicated in patients whose tests for hepatitis B antigen are positive, since the duodenoscope cannot be sterilized. The major disadvantage of the procedure in pancreatic neoplasm is the inability to detect small tumors that do not involve the major pancreatic ducts. Usually neither small duct not acinar filling occurs, and if one increases the injection pressure to opacify these structures, the risk of producing pancreatitis is also increased. Also the extent of the lesion cannot be determined. The size and location of the lesion can more readily be determined by ultrasound and angiography.
RADIOISOTOPIC EXAMINATIONS Liver Radioiodinated rose bengal is cleared from the blood by the hepatic parenchymal cells and excreted through the biliary tree into the intestinal tract and therefore images the biliary tree. Normal patients have maximal hepatic uptake at 20 to 30 minutes and begin to show intestinal radioactivity at 30 to 60 minutes. No intestinal radioactivity by 90 minutes suggests obstruction, and if follow-up images over the next 24 hours confirm this finding, the diagnosis of extrahepatic biliary obstruction is established, provided hepatocellular disease is excluded by undertaking simultaneous blood clearance de termination s. U sing the head as a nonhepatic pool, the 20 minute count rate should be no greater than 55 per cent of the 5 minute count rate. Marked reduction in clearance indicates hepatocellular disease. A blood retention of 90 per cent or more at 20 minutes and the passage of radioactivity into the intestine indicate "medical" jaundice in 95 per cent of cases. Failure of intestinal activity to appear at 24 hours plus a blood retention of 70 per cent or less indicate extrahepatic obstruction. Extension of the radioac-
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tivity from the inferior margin of the liver indicates extrahepatic obstruction regardless of the blood clearance rate,17 Recent clinical studies suggest a diagnostic accuracy rate using the rose bengal technique of approximately 95 per cent.22. 27. 87 The use of colloidal radiopharmaceuticals (such as 99mTc sulfur colloid) which are phagocytosed by the Kupffer cells of the liver's reticuloendothelial system demonstrate the hepatic substance with negative shadows cast by dilated ducts and metastatic lesions. lo • 32 In hepatocellular diseases this technique demonstrates a diffuse decrease in hepatic radioactivity plus an increased uptake by the bone marrow and spleen. Pancreas Blau and Manske3 introduced the use of selenium tagged methionine for pancreatic scanning. The gamma emitter selenium-75 was substituted for the sulfur atom in methionine. Fifteen minutes after intravenous injection, 80 to 90 per cent is removed from the plasma, and by 60 minutes labeled proteins are predominantly in the zymogen granules. Radioactivity appears in the pancreatic juice at 45 minutes, reaches a maximum at 90 to 180 minutes, and gradually diminishes over the next several hours. The avidity of the pancreas for amino acids is such that its peak radioactivity level occurs about 30 minutes after injection. Accordingly, this technique reflects primarily the labeling of digestive enzymes. 29 Overall results indicate a general agreement over figures of 10 to 30 per cent false negatives and 30 per cent false positive rates. 68 Riccobon069 has noted a false positive rate of 30 per cent and false negative of 30 per cent in a recent review of 1300 patients. The major difficulty appears to stem from generalized dysfunction which can occur in the normal and in acute and chronic pancreatitis, pancreatic pseudocysts and neoplasm. On the other hand scanning seldom fails to demonstrate major abnormality, when present, but of itself it is incapable of defining the etiologic factor or factors involved. For example, in investigating an abdominal mass a normal scan would rule out a pancreatic abnormality with a relatively high degree of accuracy. Figure 3 illustrates absence of radioactivity in the body and tail of the pancreas secondary to pancreatic carcinoma.
ULTRASOUND As early as 1949, George Ludwig50 proposed the use of echography (reflected ultrasound imaging) as a method for detection of gallstones. The application of ultrasound for this purpose failed to achieve prominence for about two decades. With the recent improvement of ultrasound imaging systems, evaluation of the biliary tree and diseases related to it is again becoming more promising. The main applications of ultrasound in the diagnosis of jaundice are evaluation of the gallbladder and, to a lesser extent, the bile ducts; diagnosis of neoplasms and other masses in the pancreas and vicinity, causing obstruction of the common or other bile ducts; and evaluation of the liver, especially for intrahepatic masses.
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Figure 3. Rectilinear "Se selenomethionine scan of a patient with pancreatic carcinoma of the body and tail. Normal uptake by the liver (L) is noted in the patient's right upper quadrant. Normal isotopic uptake noted only in the head of the pancreas (PH). No activity is noted in the body and tail.
Examination of the Gallbladder and the Bile Ducts The normal gallbladder is somewhat difficult to demonstrate echographically, mostly because in the normal person in the average state it is rather a small organ. The technique for demonstration consists of systematic examination of the approximate area of the location of the gallbladder with rather high gain settings on the instrument so that most solid structures are filled with echoes. 26 ,35 Under those circumstances only liquid-containing structures will remain transonic (meaning that they transmit sound but do not return many echoes from the inside), and thus the gallbladder can be identified as a structure of typical shape and free of internal echoes. DILATATION. The major value of ultrasound in the diagnosis of lesions of the gallbladder is determination of dilatation as a result of obstruction. It is to be no'ted that in some cases, especially if there is biliary stasis, the gallbladder may be surprisingly large and yet not obstructed. There is no absolute upper limit of normal, but a cross-sectional diameter of over 3 to 4 cm is unusual. STONES. As originally proposed by Ludwig,50 stones should return fairly strong and readily detectable echoes and they do. Just as our experience in general roentgenology suggests, stones may be found in a dependent portion of the gallbladder, floating in the bile at some intermediate level, in which case a horizontal plane of echoes may be produced if there is more than one or just a few stones, and lastly, rarely, the stones
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may float to the top. Fairly meticulous technique is necessary to make sure that echoes caused by reverberation are not misinterpreted as gallstones. Demonstration of mobility of these stone echoes is a further confirming piece of evidence in favor of this diagnosis. OTHER LESIONS. Cholesterol polyps or carcinoma of the gallbladder will produce stronger echoes than bile, but weaker echoes than surrounding connective tissue or gallstones. BILE DUCTS. Normal bile ducts are difficult to identify because of their small diameter. If the ducts become dilated, they often can be identified on echo graphic examinations of the upper abdomen. This is facilitated by multiple, fairly closely spaced sections; investigators working in this area now recommend that sections be obtained 0.5 cm apart when looking specifically for bile ducts, the gallbladder and gallstones. Both cross and longitudinal, sections need to be obtained. The visualized contrast roentgen cholecystogram is a far superior means of diagnosis. Ultrasonic cholecystography becomes valuable if the gallbladder cannot be visualized by x-ray, in patients with allergy to contrast, and in pregnancy.
The Pancreas Echographic diagnosis of pancreatic lesions is a major subject in itself. Space does not permit complete discussion here. Suffice it to say that pseudocysts 19 , 45, 47 are ideally suited for echo graphic detection and will appear as transonic structures almost anywhere in the usual location of the pancreas, Pseudocysts, however, are not a common cause of jaundice, Pancreatic tumors, of course, are a common cause of jaundice and are frequently identifiable. Pancreatic carcinoma on echograms ordinarily will appear as a lumpy structure in the area of the pancreas. In terms of its echo graphic internal characteristics, a carcinoma may be more transonic than surrounding structures, or it may be a lesion with a relatively clear peripheral zone and internal echoes (Fig. 4), or occasionally it may appear as a
Figure 4. Echographic cross section of the upper abdomen 6 cm. above the level of the iliac crest in a patient with fairly advanced carcinoma of the pancreas. A mass is apparently connected to the portal structures of the liver, but is too far posterior to be the liver (arrows). It is irregular in outline and has heavy internal echoes with a somewhat clearer peripheral zone. L, liver; St, stomach; A, abdominal aorta; Sp, spine; K, partially visualized right kidney.
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structure producing better echoes than the surrounding structures and organs. The transonic variety seems to be the most common with today's ultrasonic equipment. On unusual occasions, a tumor of the pancreas may be echographically of exactly the same characteristics as the pancreas itself, and it will be difficult to detect unless it has a well defined outline, which is not usual in pancreatic carcinoma. The head and the body of the pancreas can normally be examined reasonably easily by echography; the tail is relatively difficult because of overlapping by the stomach which produces acoustic shadows. Occasionally, the tail can be approached by echo graphic scanning from the back. Carcinoma in the tail of the pancreas ordinarily will not cause jaundice unless liver metastases or subhepatic masses are present. 15 , 19, 79 Acute pancreatitis is usually not the cause of jaundice. Chronic pancreatitis with in duration around the distal part of the common bile duct may obstruct it and thus cause jaundice. The demonstration of pancreatitis is the subject of interesting echo graphic studies at the present. The normal pancreas produces more echoes than the liver, spleen and kidneys, bu t fewer echoes than the surrounding connective tissue structures. Thus, it is more difficult to demonstrate than the liver, spleen and kidneys and often cannot be identified or only partially so. With effort and with the newer scanning apparatus it may be shown. Edema, as in pancreatitis, enlarges the pancreas and makes it more transonic. Chronic pancreatitis at times, especially during exacerbations, appears similar to the acute variety. In many cases, however, the gland will not be as much enlarged and, if calcifications are present, internal echoes will be identified. Pancreatic echography at present is not suitable as a tool for detection of carcinoma in asymptomatic patients. There is excellent reason to apply echography as one of the first diagnostic examinations in patients with suspected pancreatic or peripancreatic disease (even before barium gastrointestinal studies), since it is noninvasive and the best pictures will be obtained prior to the administration of barium46 or other intestinal distention-producing measures. The echo graphic information will help direct the type and sequence of subsequent studies.
The Liver The liver with present equipment appears transonic and relatively homogeneous. Intrahepatic masses such as abscesses, primary tumors and metastases may produce a number of different patterns, mostly related to the interface between the mass and the surrounding liver or internal echo patterns in the lesion. Studies of the relative value of echographic scanning in comparison to radioisotope scintiscanning suggest that at the present time scintiscanning has a slight advantage over echography.49 Scintiscanning produces a few more false positives than echographic studies, which in turn produce a few more false negative examinations. Returning specifically to the subject of this paper, in evaluation of jaundice, echo graphic examination of the liver would be recommended mostly if the liver scan or a rose bengal radioactive study do not
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yield satisfactory information and a further search for intrahepatic or subhepatic masses needs to be made. In such cases ultrasonic B-scanning may be a major contribution and sometimes is the sole diagnostic test of help.23, 44, 53, 55, 58, 65, 67, 81 Scattered intrahepatic disease other than metastases - especially irregular areas of hepatitis and dilated bile ducts-in themselves can cause echo returns suggesting ~ntrahepatic lesions. A Short Look at the Future Present day ultrasonic equipment provides a high contrast (essentially black and white) picture mostly because of the use of storage oscilloscopes. Equipment permitting the display of gray-scale images is now under development and will soon become widely available. This display capability is expected to raise the diagnostic accuracy and ease of use in the area of both the liver and the pancreas by at least a full range of magnitude. It will then be quite readily possible to demonstrate the relative echo graphic characteristics of the liver, the pancreas and other organs as well as their normal internal components and abnormal masses.
DIRECT CHOLANGIOGRAPHY In spite of the extensive battery of tests available, there remain cases of jaundice in which efforts fail to differentiate hepatocellular from obstructive jaundice. The prognosis and treatment is very different in these two indications, and a further attempt should be made to define the problem by injecting contrast medium directly into the intrahepatic bile ducts. Direct cholangiography is also useful in known obstructive disease where the cause and site of the obstruction is not known. Since the proximal extent of the obstruction is best defined from the hepatic side, this approach has great value to the surgeon planning to palliate a bile duct carcinoma or reconstruct a bile duct stricture.
PERCUTANEOUS TRANSHEP ATIC CHOLANGIOGRAPHY Insertion of a needle through the liver parenchyma percutaneously either from anterior or lateral directions with injection of contrast into a bile duct has been used for many years36 , 77 and is successful in most cases in which the bile ducts are dilated. Overall success rates in cases in which the ducts are not dilated range between 20 and 50 per cent. 16 , 90 The overall frequency of complications is about 5 per cent in published series. Biliary peritonitis occurs in 3 per cent and bile leakage adds another 1.7 per cent. 91 The overall mortality rate is 0.5 per cent. 16 Recent cases have been documented of septicemia and shock due to the formation of iatrogenic bile-venous fistulas in the presence of pre-existing cholangitis.57 For this reason the procedure is contraindicated in patients with a history of cholangitis unless appropriate antibiotic cover is instituted or sequential surgical exploration performed.
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JUGULAR TRANSVENOUS CHOLANGIOGRAPHY Hanafee and Weiner 8 developed an approach through the jugular venous tree and have subsequently reported their results. 28 ,37 Successful cholangiograms were obtained in 85 per cent of those with proven bile duct obstruction and 22 per cent of those with nonobstructed ducts. By entering the ducts from within the liver it was hoped to avoid the complications of capsular perforation with bleeding and bile peritonitis. This would eliminate the need for routine sequential surgical exploration recommended by some with the percutaneous transhepatic approach.56 Complications have been related mainly to leakage of bile into the venous system with febrile reactions and septic shock; one fatality has been reported to date. Approximately half of the patients had a previous history of cholangitis. The authors now consider this procedure contraindicated in patients with a prior history of cholangitis. 37 Others consider cholangitis much less of a problem. 71
FEMORAL AND ANTECUBITAL TRANSVENOUS CHOLANGIOGRAPHY To radiologists familiar with the femoral and antecubital approach to arteriography and venography, introduction of a catheter via the femoral or antecubital vein is probably more easily performed. We have been using this approach to direct cholangiography over the past 2 years30 (Figs. 5 and 6). We have done 15 transvenous procedures successfully, with the only complication being transient septicemia in a patient in whom prophylactic antibiotics were inadvertently withheld. This technique has the same potential benefits and disadvantages as the jugular route. The transvenous approach also permits biopsy to be performed under fiuoroscopic control. It eliminates the complication of bleeding and may be the more appropriate technique where coagulation parameters are not normal. 28 . 30. 71
ANGIOGRAPHY Considerable experience has been accumulated in recent years with angiographic evaluation of hepatic, biliary and pancreatic pathology. Hepatic angiography can be helpful in the jaundiced patient by demonstrating the shrunken liver of end-stage liver disease (Fig. 7), the presence of hepatoma or cholangiocarcinoma, and avascular metastatic lesions as small as 0.5 cm in diameterY' 63. 64 Angiographic diagnosis of carcinoma of the gallbladder has been described!' 70 and its usefulness in evaluating the extent of hepatic and regional spread has been recently reported. 78 Angiographic diagnosis of bile duct carcinoma is more difficult because of the absence of vascular change, particularly in the sclerosing type of lesion. Pancreatic angiography has become established as a safe, accurate
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Figure 5. Femoral transvenous cholangiogram in a 45 year old jaundiced patient with previous right hepatectomy secondary to an auto accident. A No. 8 French polyethylene catheter is positioned in the left hepa tic vein. A coaxial No. 4 French Tefion catheter (white arrow) is shown in the dilated left biliary radical. Arrows denote severe stricture of the distal bile duct.
method for evaluation of the presence and extent of pancreatic disease. 5. 42. 51.52 The angiographic diagnosis of pancreatic carcinoma initially had limited success, but with the advent of superselective, magnification and pharmacodynamic techniques accurate diagnosis can be made in approximately 95 per cent of patients, providing satisfactory detail of the intrapancreatic vasculature is obtained. H • 31. 52 Tumors as small as 1.5 cm in diameter have been detected by this method,52 permitting surgical resection at an early and potentially curable stage (Figs. 8 and 9). An additional advantage of angiography from the surgeon's viewpoint is demonstration of the vascular anatomy, revealing an anomalous arterial supply and thus giving a road map for the performance of surgical resection. Similarly invasion of larger arteries and portal venous involvement indicates that the lesion is not resectable. It is our experience that in the diagnosis of small lesions the evaluation of arterial and capillary phases for evidence of encasement and small vessel cutoff is more important than the venous changes emphasized by others,6 since we have found portal venous involvement only in association with fairly advanced lesions for which surgical extirpation offers little. We have also found angiography to be helpful in differentiating pancreatic carcinoma from chronic pancreatitis (Fig. 10).
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Figure 6. Transvenous cholangiogram of a 30 year old jaundiced woman demonstrating a meniscus (arrows) characteristic of an intraluminal mass (gallstone). Exploratory surgery two weeks previously demonstrated a porta hepatis mass which was felt to represent a rhab· domyosarcoma. Reexploration post angiogra phy verified the gallstone.
OPERATIVE AND POSTOPERATIVE CHOLANGIOGRAPHY Intraoperative cholangiography as a routine procedure during cholecystectomy is being utilized by many surgeons in preference to limiting it to cases with chemical indications, since several authors have shown that unsuspected common duct calculi are found in 3 to 10 per cent of patients undergoing cholecystectomy. IS. 25 The procedure should add only a few minutes to the operative time and reduce the number of negative duct explorations. The procedure carries a false positive rate of 2 to 7 per cent and a false negative rate of 1 to 4 per cent. 13 • 33. 76 In icteric patients in whom preoperative cholangiography has not been obtained, intraoperative cholangiography is mandatory to identify or exclude biliary tree obstruction. It is important to define the whole biliary tree during this procedure to exclude sclerosing cholangitis, intrahepatic biliary calculi and tumors, or unrecognized distal obstructive lesions, whether or not the extrahepatic bile duct is dilated. 4 3 The techniques and sources of potential error are well recognized. s (Text continued on page 139.)
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Figure 7. A, Arterial phase, and B, capillary phase, of a celiac arteriogram done in a 65 year old woman with a history and laboratory findings typical of obstructive jaundice secondary to pancreatic carcinoma. After the intraarterial infusion of a vasodilator (tolazoline [Priscoline]), a normal pancreas (arrows) and a small end stage liver (L) were demonstrated.
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Figure 8. Selective hepatic artery injection after infusion of a vasodilator (tolazoline [Priscoline]) in a 52 year old jaundiced patient demonstrates an amputated branch of the anterior arcade (arrow) and tumor encasement of multiple small intrapancreatic arteries (superior and right of arrow). A 1.5 cm adenocarcinoma was later excised. H, hepatic artery; CD, gastroduodenal artery.
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Figure 9. Selective gastroduodenal artery (CD ) injection in a 55 year old woman demonstrates amputation of the posterior arcade, a small pseudoaneurysm (large arrow) and encasement of small arteries (small arrows). A Whipple procedure was performed and a 1.5 cm adenocarcinoma was discovered. The patient is alive 3'1. years post surgery.
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Figure 10. A, Arterial phase, and B, capillary and venous phase, of selective high-pressure high-volume gastroduodenal artery (CD) injection after intraarterial infusion of tolazoline (Priscoline), demonstrating filling of the entire pancreas (P H, head; P B, body; PT, tail). An avascular area below the pancreas plus the curvilinear displacement of the omental arteries and veins (arrows) suggest a pancreatic pseudocyst. The increased capillary and venous phase and irregular small intrapancreatic arteries are frequently seen with pancreatitis.
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Burhenne7 has recently described a technique of removal of retained common bile duct calculi using a modified ureteral stone basket passed through the T-tube sinus tract under fiuoroscopic control. The T-tube must be left in site for 4 weeks in order to permit the tract to mature. Mazzariell054 has reported 90 per cent success in a large series of retained common duct calculi with this method. Renewed interest in nonoperative removal of retained stones by dissolution has been stimulated by reports of the installation of cholic acid, which increases the solubility of cholestero183 and heparin utilizing the zeta potential principle. 24
GENERAL RADIOLOGIC APPROACH The course of the work-up for jaundice and suspected pancreatic carcinoma can be quite varied depending on the patient's history and on the physical and laboratory findings. The selection may be dependent on the expertise and experience of the radiology department with the various diagnostic tools. From the above discussion of the many modalities, one can readily see that the accuracy varies considerably with various investigators. At our institution pancreatic isotopic scanning is not available and ultrasound and endoscopic pancreatocholangiography have only recently been introduced. All three, as stated previously, are relatively nonspecific, although they can be quite helpful. Pancreatic isotopic scanning is important since if the scan is normal there is a high probability that no large pancreatic tumor is present. Ultrasound may detect and delineate the extent of larger pancreatic tumors and is particularly accurate for pancreatic pseudocysts. Endoscopic pancreatocholangiography may demonstrate stones or strictures in the ductal systems. In jaundiced patients plain films are obtained. If the patient is jaundiced, the oral cholecystogram is omitted since the gallbladder will not usually be visualized. If the bilirubin is less than 3 mg per 100 ml, an intravenous cholangiogram is performed. If the bilirubin is higher than 3 mg per 100 ml or if the intravenous cholangiogram does not result in visualization, a slow infusion cholangiogram is performed. Recently ultrasound has been requested prior to the gastrointestinal series. If equivocal findings are noted on the GI series, hypotonic duo denography is done immediately. A 99mtechnetium sulfur colloid scan is performed to evaluate the liver for primary metastatic lesions as well as for dilated bile ducts. If the scan suggests hepatic disease or if a pancreatic lesion is suspected, angiography is performed. Conventional celiac and SMA arteriography usually permits diagnosis of only larger lesions, but it may be very helpful in detecting liver and gallbladder disease. High pressure superselective angiography or pharmacoangiography usually is extremely valuable. This type of angiography has detected tumors as small as 1.5 cm, delineated the extent of the lesion and been helpful in differentiating pancreatitis from pancreatic carcinoma. Usually before surgery either percutaneous or transvenous cholangiography is done. In the case of cholelithiasis intraoperative cholangiography should be routinely performed. Figures ·11 and 12 illustrate the usual order of examinations.
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Plain films
--------------s-e-ru-mlJr;l-iru-b-'u------------- Elevated serum Serum bilirubin
< 3 mg per 100 rnl
>3 mg per 100 ml
bilirubin with H x suggesting stone
Tra-nsvenous or percutaneous cholangiography Transvenous or percutaneous char angiography
x - Non-visualization ? - Equivocal findings
Dotted boxes - Studies not available routinely
Figure 11. Work-up of patients with suspected obstructive jaundice.
Plain film
Hypotonic duodenography
Angiography
Figure 12. Work-up for suspected pancreatic lesions in patients without jaundice.
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REFERENCES 1. Abrams, R. M., Meng, C. H., Firooznia, H., Beranbaum, E. R., and Epstein, H. Y.: Angiographic demonstration of carcinoma of the gallbladder. Radiology, 94:277,1970. 2. Berk, R. N., Armbuster, R., and Salztein, S.: Carcinoma of the gallbladder associated with the porcelain gallbladder. Radiology, 106 :29, 1973. 3. Blav, M., and Manske, R. F.: The pancreas specificity of Se" selenomethionine. J. Nucl. Med., 2:102,1961. 4. Blumgart, L. H., Salmon, P. R., and Cotton, P. B.: Endoscopy and retrograde choledochopancreatography in the diagnosis of the patient with jaundice. Surg. Gynec. Obstet., 138:565, 1974. 5. Boijsen, E., and Tylen, U.: Vascular changes in chronic pancreatitis. Acta Radiol., 12:34, 1972. 6. Buranasiri, S., and Baum, S.: The significance of the venous phase of celiac and superior mesenteric arteriography in evaluating pancreatic carcinoma. Radiology, 102: 11, 1972. 7. Burhenne, J. H.: Non-operative obtained biliary stone extraction. A new roentgenologic technique. Am. J. Roent., 117:388, 1973. 8. Custer, D. C., and Clore, J. N.: Source of error in operative cholangiography. Arch. Surg., 100:664, 1970.
9. Darnborovgit, A., and Geffen, N.: Drip infusion cholangiography. Brit. J. Rad., 39:827, 1966. 10. DeLand, F. H. and Wagner, H. N., in Atlas of Nuclear Medicine, Vol. Ill: Reticuloendothelial System, Liver, Spleen and Thyroid. Philadelphia, W. B. Saunders Co., 1972. 11. Eaton, S. 0., and Ferrucci, J. T.: Radiology of the Pancreas and Duodenum. Philadelphia, W. B. Saunders Co., 1973. 12. Eaton, S. 0., Ferrucci, J. T., Margulis, A. F., and Weens, H. S.: Unfamiliar roentgen signs in pancreatic disease. Amer. J. Roentgenol., 116:396, 1972. 13. Edmunds, R., and Hughes, J. H.: Re-exploration of the common bile duct. Arch. Surg., 90:876, 1965.
14. Eisenberger, H., Personal communication, 1973. 15. Engelhart, G., and Blauenstein, U.: Ultrasound in the diagnosis of malignant pancreatic tumors. Gut, 11 :443, 1970. 16. Evans, J. A., Glen, F., Thorbjarnarson, B., and MUjahed, Z.: Percutaneous transhepatic cholangiography. Radiology, 78:362, 1962. 17. Eyler, W. R., Schuman, B. M., DuSault, L. A. and Hinson, R. E.: The radioiodinated rose bengal liver scan as an aid to the differential diagnosis of jaundice. Amer. J. Roentgenol., 94:469, 1965. 18. Ferris, D. 0., and Sterling, W. A.: Surgery of the biliary tract. Surg. Clin. N. Amer., 47:861, 1967. 19. Filly, R., and Freimanis, A.: Echographic diagnosis of pancreatic lesions. Radiology, 96:575, 1970. 20. Fischer, H. W.: Excretion of iodipamide-relation of bile and urine output to dose. Radiology, 84:483, 1965. 21. Forsgren, L., Hansson, K., Lundh, C., and Nordenstam, H.: Pancreatic biopsy. Acta Chir., 134:457, 1968. 22. Freeman, L. M., Kay, C. J., and Derman, A.: Renal excretion of rose bengal: A pitfall in the interpretation of rose bengal abdominal scans. J. Nucl. Med., 9:227, 1968. 23. Freimanis, A.: Echographic exploration of abdominal structures. Crit. Rev. in Radiol. Sci., 1 :207, 1970. 24. Gardner, B.: Experiences with the use of intracholedochal heparinized saline for the treatment of retained common bile duct stones. Ann. Surg., 177:240, 1973. 25. Glass, T. J.: Cholecystectomy and cholangiography. Surgery, 43:452, 1968. 26. Gravelle, I. H., Jones, M., and Roberts, E. S.: The investigation of gallbladder disease. Brit. J. Radiol., 46:568, 1973. 27. Greene, A. G., and Sadowsky, N. L.: A radiologic approach to the differential diagnoses of surgical and non-surgical jaundice. Amer. J. Roentgenol., 116:368, 1972. 28. Hanafee, W., and Weiner, M.: Transjugular percutaneous cholangiography. Radiology, 88:35,1967. 29. Hansson, E.: The formation of pancreatic juice proteins studied with labeled amino acids. Acta Physiol. Scand., 46, Suppl. 161, 1959. 30. Hawkins, I. F.: Intravenous punch biopsy for the liver and kidney capable of cholangiography, renal cyst puncture and bronchial biopsy. Radiology, 105:445, 1972. 31. Hawkins, I. F., Kaude, J. V., and MacGregor, A. M. C.: Priscoline and epinephrine in selective pancreatic angiography: A comparison study using high pressure injection, valsalva maneuver and magnification technique. Radiology, in press. 32. Heck, L. L., and Gottschalk, A.: The appearance of intrahepatic biliary duct dilatation on the liver scan. Radiology, 99:135,1971. 33. Herman, R. E., and Hoerr, S. 0.: The value of routine use of operative cholangiography. Surg. Gynec. Obstet., 121 :1015,1967.
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34. Hess, W.: Surgery of the biliary passages and the pancreas. Princeton, Van Nostrand Co., 1965. 35. Hublitz, U., Kahn, P., and Sell, L: Cholecystosonography: An approach to the nonvisual· ized gallbladder. Radiology, 103 :645, 1972. 36. Hueard, E., and Do-Xuan-Hop: La ponction transhepatique des canaux biliaires. Bull. Soc. Med. Chir. Indochina, 15:1090, 1937. 37. Kadell, B. M., and Weiner, M: Current status of the transjugular approach for direct cholangiography. Surg. Clin. N. Amer., 53:1019,1973. 38. Kakos, G. S., Tompkins, R K., Turnipseed, W., and Zollinger, R M.: Operative cholangiography during routine cholecystectomy. Arch. Surg., 104:484,1972. 39. Kasugai, T., Kuno, N., Kobayashi, S., and Hattori, K.: Endoscopic pancreatocholangiography. I. The normal endoscopic pancreatocholangiogram. Gastroenterology, 63:217, 1972. 40. Kasugai, T., Kuno, N., J(izu,_M., Kobayashi, S.~ and_Hattori, K.: Endoscopic pancreatocholangiography. 11. The pathologic endoscopic pancreatocholangiogram. Gastroenterology, 63:227, 1972. 41. Kaude, J. V., Jensen, R, and Wirtanen, G. W.: Slow injection hepatic angiography. Acta Rad., 14:699, 1973. 42. Khademi, M., Lazaro, E. J., and Rickert, R R: Selective arteriography in the diagnosis of chronic inflammatory pancreatic disease. Amer. J. Roentgenol., 119:141,1973. 43. Legge, D. A., and Carlson, H. C.: Cholangiographic appearance of primary carcinoma of the bile ducts. Radiology, 102:259, 1972. 44. Lehman, J. S.: Ultrasound in the diagnosis of hepatobiliary disease. Rad. Clin. No. Amer., 4:605, 1966. 45. Leopold, G.: Pancreatic echography: A new dimension in the diagnosis of pseudocyst. Radiology, 104:365, 1972. 46. Leopold, G. R, and Asher, W. M.: Deleterious effects of gastrointestinal contrast material on abdominal echography. Radiology, 98:637,1971. 47. Leopold, G., Berk, R, and Reinke, R: Echographic-radiological documentation of spontaneous rupture of a pancreatic pseudocyst into the duodenum. Radiology, 102 :699, 1972. 48. Leopold, G. R, and Sololoff, J.: Ultrasonic scanning in the diagnosis of biliary disease. Surg. Clin. N. Amer., 53:1043,1973. 49. Leyton, B., Halpern, S., Leopold, G., and Hagen, S.: Correlation of ultrasound and colloid scintiscan studies of the normal and diseased liver. J. Nucl. Med., 14:27, 1973. 50. Ludwig, G. D., and Struthers, F. W.: Considerations underlying the use of ultrasound to detect gallstones and foreign bodies in tissue. Naval Medical Research Institute, National Naval Medical Center. Project NM 004001, Report 4, 16 June 1949. 51. Lunderquist, A.: Angiography in carcinoma of the pancreas. Acta. Radiol., Suppl. 235, 1965. 52. MacGregor, A. M. C., and Hawkins, I. F., Jr.: Selective pharmacodynamic angiography in the diagnosis of carcinoma of the pancreas. Surg. Gynec. Obstet., 137:917, 1973. 53. McCarthy, C. F., Davies, E. R, Wells, P. N. T., Ross, F. G., Follett, D. H., Muir, K. M., and Read, A. E.: A comparison of ultrasonic and isotope scanning in the diagnosis of liver disease. Brit. J. Radiol., 43:100,1970. 54. Mazzariello, R: Review of 220 cases of residual biliary tract calculi treated without reoperation. Surgery, 73:299,1973. 55. Melki, G.: Ultrasonic piiltterns of tumors of the liver. J. Clin. Ultrasound, 1 :306, 1973. 56. Misherry, C. K., and Glenn, F.: Surgical aspects of biliary tract disease. Amer. J. Med., 51 :651, 1971. 57. Morettin, L. B., and Dodd, G. D.: Percutaneous transhepatic cholangiography. Amer. J. Dig. Dis., 17:831, 1972. 58. Mountford, R. A., Halliwell, M. and Atkinson, P.: Ultrasonic liver scanning: Automated Ascan analysis. Phy. of Med. and BioI., 18:559,1973. 59. Newman, H. F., and Northrup, J. D.: Collective review: The autopsy incidence of gallstone. Int. Abstracts Surg., 109:1,1959. 60. Oi, I., Kobayashi, S., and Kondo, T.: Endoscopic pancreatocholangiography. Endoscopy, 2:103,1970. 61. Payne, R F.: Drip infusion cholangiography. Clin. Rad., 19:281,1968. 62. Perez, C. A., Powers, W. E., Holtz, S., and Spjut, H. J.: Roentgenologic-pathologic correlation of resectable carcinoma of the pancreatoduodenal region. Amer. J. Roentgenol., 94:438,1965. 63. Pollard, J. J., Fleishli, D. J., and Nebesar, RA.: Angiography of hepatic neoplasms. Radiol. Clin. North. Amer., 8:31, 1970. 64. Pollard, J. J., Nebesar, R A., and Mattoso, L. F.: Angiographic diagnosis of benign diseases of the liver. Radiology, 86:276, 1966. 65. Rasmussen, S.: Liver volume determination by ultrasonic scanning. Brit. J. Radiol., 45:579,1972. 66. Rasmussen, S., Holm, H. H., Kristensen, J., and Barlebo, H.: Ultrasonically-guided liver biopsy. Brit. Med. J., 2:500,1972.
OBSTRUCTIVE JAUNDICE AND PANCREATIC DISEASE
143
67. Rasmussen, S. N., Holm, H. H., Kristensen, J. D., Pedersen, J. F., and Hancke, S.: Ultrasound in the diagnosis of liver disease. J. Clin. Ultrasound, 1 :220, 1973. 68. Riccobono, X. J.: Pancreatic scanning. Seminars Roentgenol., 3:310,1968. 69. Riccobono, X. J., personal communication, 1974. 70. Rosch, J., Grollman, J. H., Jr., and Steckel, R J.: Arteriography in the diagnosis of gallbladder disease. Radiology, 92:1485,1969. 71. Rosch, J., Larin, P. C., Antonoric, R., and Dotter, C. T.: Transjugular approach to liver biopsy and transhepatic cholangiography. N. Engl. J. Med., 289:227, 1973. 72. Salzman, E., Spurck, RP., Kier, C., and Watkins, D.: Opacifying gallstones. JAMA, 169:334,1959. 73. Samuel, E.: The cystogastro-celiac band: Radiologic considerations. Brit. J. Radiol., 25:119,1952. 74. Sarles, H.: Chronic calcifying pancreatitis-chronic alcoholic pancreatitis. Gastroenterology, 66:604, 1974. 75. Sarles, H., Sarles, J. C., Carmatte, R, Muratore, R, Gaini, M., Guien, C., Pastor, J., and Leroy, F.: Observations on 205 confirmed cases of acute pancreatitis, recurring pancreatitis and chronic pancreatitis. Gut, 6:545, 1965. 76. Schulenburg, C. A. P.: Operative cholangiography. London, Butterworth and Co., 1966. 77. Shaldon, S., Barber, K. M., and Young, W. B.: Transhepatic percutaneous cholangiography-a new technique. Gastroroentgenology, 42:371, 1962. 78. Sprayregen, S., and Messinger, N. H.: Carcinoma of the gallbladder: Diagnosis and evaluation of regional spread by angiography. Amer. J. Roentgenol., 116:382, 1972. 79. Stuber, J., Templeton, A., and Bishop, K.: Sono graphic diagnosis of pancreatic lesions. Amer. J. Roentgenol., 116:406,1972. 80. Takagi, K., Ikeda, S., Nakagawa, Y., Sakaguchi, N., Takahashi, T., Kumakura, K., Maruyama, M., Someya, M., Nakano, H., Takada, T., Takekoshi, T., and Kin, T.: Retrograde pancreatography and cholangiography by fiber-duodenoscope. Gastroenterology, 59:445, 1970. 81. Taylor, K. J. W., Carpenter, B. E., and McCready, V. R: Grey scale echography in the diagnosis of intrahepatic disease. J. Clin. Ultrasound, 1 :284, 1973. 82. Vaittinen, E.: Carcinoma of the gallbladder. A study of 390 cases diagnosed in Finland 1953-1967. Ann. Chir. Gynaecol. Fenn., 59, Suppl. 168, 1970. 83. Way, L., Admirand, W. H., and Dunphy, J. E.: Management of choledocholithiasis. Ann. Surg., 176:347, 1972. 84. Weiner, M., and Hanafee, W. N.: A review of transjugular cholangiography. Radiol. Clin. N. Amer., 8:53, 1970. 85. Weinstein, B. R, Korn, R J., and Zimmerman, H. J.: Obstructive jaundice as a complication of pancreatitis. Ann. Intern. Med., 58 :245, 1963. 86. Weiss, H. D., Anacker, H., Wiesner, W., and Rupp, N.: Duodenoscopic pancreatography. Radiology, 106:333, 1973. 87. Whiting, E. G., and Nusynowitz, M. L.: Radioactive rose bengal testing on the differential diagnosis of jaundice. Surg. Gynec. Obstet., 127:729, 1968. 88. Wise, RE.: Intravenous Cholangiography. Springfield, Ill., Charles C Thomas, 1962. 89. Wise, R E., Johnston, D. 0., and Salzman, F. A.: The intravenous cholangiography diagnosis of partial destruction of the common duct. Radiology, 68 :507, 1957. 90. Young, W. R: Obstructive jaundice. Amer. J. Roentgenol., 119:4,1973. 91. Zinberg, S. S., Berk, J. E., and Plasencia, H.: Percutaneous transhepatic cholangiography, its use and limitations. Amer. J. Digest Dis., 10:154,1965. Department of Radiology University of Florida College of Medicine Gainesville, Florida 32610
