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Radiology of the Gallbladder and Bile Ducts
Symposium on Surgery of the Biliary Tree
Radiology of the Gallbladder and Bile
Ducts Robert N. Berk, M.D.*
A thorough understanding of the radiology of the gallbladder and bile ducts is essential for the proper clinical management of patients with biliary tract disease. It is appropriate, therefore, that a review of the radiologic procedures used for the diagnosis of diseases of the gallbladder and bile ducts be included in a symposium on surgery of the biliary system. The x-ray techniques employed are plain abdominal radiographs, barium studies of the gastrointestinal tract, oral cholecystography, intravenous cholangiography, transhepatic cholangiography, celiac angiography, and operative and postoperative cholangiography. Transjugular cholangiography, cholangiography by direct cannulation via the duodenoscope, and abdominal echography are considered by other authors in this symposium.
PLAIN ABDOMINAL RADIOGRAPHS The oldest and simplest radiological method for the detection of disease of the biliary tract is the plain radiograph of the abdomen. Because only 10 to 30 per cent of gallstones are radiopaque, the plain radiograph is of relatively little value in the detection of cholelithiasis compared to cholecystography. Yet it is common to find cholelithiasis incidentally in patients having radiographic studies of the stomach, colon, or urinary tract. Figure 1 shows radiopaque gallstones on the plain abdominal radiograph of a 24 year old man. Thickened trabecular architecture of the skeleton is also visible. This permits a diagnosis of sickle cell anemia which explains the presence of gallstones in this young patient. In patients with acute cholecystitis, the plain abdominal radiograph may reveal a dilated loop of small intestine with air-fluid levels in the right upper quadrant. In these cases the localized paralytic ileus is due to impaired motility in a segment of the intestine adjacent to the inflammatory reaction. When hydrops or empyema of the gallbladder occurs, a mass adjacent to the liver may become visible on the abdominal radio''Associate Professor of Radiology, University of California, San Diego, School of Medicine, La Jolla, California
Surgical Clinics of North America- Vol. 53, No.5, October 1973
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* Figure 1. Plain abdominal radiograph in a 24 year old man with sickle cell disease. There are radiopaque gallstones in the gallbladder (arrows) and skeletal changes characteristic of sickle cell disease.
graph. Occasionally, perforation of the gallbladder can be detected when gallstones are noted free in the peritoneal cavity. Emphysematous cholecystitis is readily diagnosed by the presence of gas in the wall and in the lumen of the gallbladder (Fig. 2). When a gallstone obstructs the cystic duct, calcium may be deposited in the lumen or in the wall of the gallbladder. Calcium within the gallbladder, termed milk of calcium bile, is visible on the plain abdominal radiograph. In these cases the appearance of the gallbladder on the plain radiograph is often identical to a normal cholecystogram (Fig. 3). Calcification in the gallbladder wall is known as porcelain gallbladder. The plain radiograph shows an irregular ring of calcium in the right upper quadrant which often resembles a large single gallstone (Fig. 4). Two patients with carcinoma of the gallbladder in association with porcelain gallbladder have recently been reported, and 24 others have been described in the literature." The association is sufficiently common to warrant prophylactic cholecystectomy for porcelain gallbladder if the patient's general health permits. Erosion of a gallstone into the intestinal tract produces characteristic findings on the plain abdominal radiograph. If the gallstone is large enough to produce intestinal obstruction, gallstone ileus occurs. The ab-
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Figure 2. Upright plain abdominal radiograph of an elderly woman showing gas in the wall and in the lumen of the gallbladder, indicative of emphysematous cholecystitis.
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* Figure 3. Plain abdominal radiograph showing milk of calcium bile in the gallbladder. No contrast material has been given.
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* Figure 4. Plain abdominal radiograph showing calcification in the wall of the gallbladder characteristic of porcelain gallbladder.
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dominal radiograph discloses air in the biliary tree, gas-filled distended loops of small intestine, and a gallstone in an ectopic location (Figs. 5 and 6). Figure 7 shows air in the common duct in an elderly patient who developed a cholecystocolic fistula due to erosion of a gallstone into the colon. Genereux and Tchang reported a case of hydrops of the gallbladder in which the gallbladder wall was visible on tomograms of the right upper quadrant of the abdomen made after the infusion of a large amount of diatrizoate, a urinary contrast material. 19 The gallbladder failed to visualize on routine cholecystography or intravenous cholangiography. Recognizing that the gallbladder was enlarged, they made a correct diagnosis of hydrops. Rabushka et al. studied a group of patients with nonvisualization of the gallbladder by tomography after a large-dose infusion of diatrizoate.35 In their cases, visualization of a thickened, irregular wall was accurate evidence of acute or chronic cholecystitis. The wall of normal gallbladders rarely opacified. When seen, it was thin and sharp. This technique requires further evaluation, for it may prove to be a valuable tool for studying gallbladders which cannot be opacified by conventional techniques (Fig. 8).
* Figure 5. Plain abdominal radiograph showing gallstone ileus. There is distention of the small intestine and air in the common duct (arrow).
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•• Figure 6. Plain abdominal radiograph in a patient a cholecystoduodenal fistula. Figure 6. Plain abdominal radiograph in a patient with with a cholecystoduodenal fistula. is a radiopaque gallstone the terminal (arrow). ThereThere is a radiopaque gallstone in theinterminal ileumileum (anow).
* Figure 7. Right quadrant of a plain abdominal radiograph showing Figure 7. Right upperupper quadrant of a plain abdominal radiograph showing air in air thein the biliary tree (arrows) in a patient a cholecystocolic fistula. (Courtesy Dr. Lawrence biliary tree (armws) in a patient with with a cholecystocolic fistula. (Courtesy of Dr.ofLawrence Sweeney.) Sweeney.)
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* Figure 8. Tomogram of the right upper quadrant of the abdomen taken after the rapid intravenous injection of a large dose of diatrizoate. The gallbladder wall is opacified (arrows). Thickening of the wall and distention of the gallbladder indicate the presence of hydrops, which was confirmed at surgery. The right kidney is well visualized.
BARIUM STUDIES OF THE GASTROINTESTINAL TRACT Before the introduction of cholecystography in 1924, radiologists relied heavily on radiographic abnormalities in the stomach and duodenum for the diagnosis of gallbladder disease. The proximity of the gallbladder to the first part of the duodenum accounts for the spasm and edema which may occur in the duodenum in cases of acute cholecystitis (Fig. 9). Chronic cholecystitis produces adhesions which may distort the .duodenum. When the gallbladder lies against the hepatic flexure of the colon, cholecystitis may produce deformity of the colon which is visible on barium enema studies (Fig. 10). Upper gastrointestinal barium examinations may be useful in studying patients with jaundice due to a stone im~ted at the ampulla of Vater. In such cases, edema of the ampulla ofte'V produces a smooth, sharply defined mass in the wall of the second portion of the duodenum (Fig. 11). Carcinoma of the ampulla produces an irregular mass in the same location (Fig. 12). In both situations and in patients with jaundice due to carcinoma of the pancreas, the dilated common duct may compress the duodenum in a characteristic fashion. The use of hypotonic duodenography (barium studies of the duodenum after the administration of an anticholinergic drug) is a valuable technique for detecting and evaluating such abnormalities.
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Figure 9.9. Supine Supine left left posterior posterior oblique oblique projection projection of of the the stomach stomach and and duodenum duodenum showshowFigure ing deformity deformity of of the the postbulbar postbulbar area area of of the the duodenum duodenum due due to to acute acute cholecystitis cholecystitis (arrow). ( an·ow). ing
Figure 10. 10. Barium Barium enema enema examination examination showing showing deformity deformity of of the the hepatic hepatic flexure Figure flexure due due to acute acute cholecystitis. cholecystitis. (Courtesy (Courtesy of of Dr. Dr. Wendell Wendell Dietz.) Dietz.) to
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Figure 11. Barium study of the duodenum showing a smooth mass at the ampulla of Vater due to edema of the ampulla caused by an impacted gallstone (arrow).
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Figure 12. Barium study of the duodenum showing an irregular mass at the ampulla of Vater caused by carcinoma of the ampulla (arrows).
Barium studies may disclose the presence of a cholecystoduodenal fistula. In these cases barium may enter the biliary tree or outline a gallstone in the intestine (Fig. 13).
ORAL CHOLECYSTOGRAPHY The introduction of cholecystography into diagnostic radiology by Graham and Cole in 1924 was based on two physiologic facts. 16 It had been shown by Abel and Rowntree that certain halogenated dyes are excreted almost entirely into the bile. Rous and McMaster then discovered that the gallbladder concentrates bile 8 to 10 times. Thus the halogen appears in bile and is sufficiently concentrated to permit radiographic visualization of the gallbladder. Since 1952, the most frequently used contrast material in the United States has been iopanoic acid (Telepaque''). This material, which is highly insoluble in water, is absorbed by passive diffusion across the intestinal mucosa, transported in the blood bound to albumin, and taken up by the liver where it is con*Winthrop Laboratories Inc., New York, N.Y.
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Figure 13. Barium study of the duodenum showing a gallstone (arrows) impacted in the third portion. A small amount of barium can be seen entering a cholecystoduodenal fistula at the apex of the duodenal cap. (Courtesy of Dr. William Pogue.)
jugated into the more water-soluble glucuronide. 29 The rate of excretion into the bile is directly related to the volume of bile flow. 11 Once in the gallbladder, the contrast material is concentrated by reabsorption of water from the bile. A concentration of 0.25 to 1.0 per cent iodine is required in the gallbladder for radiographic visualization. 24 Impaired visualization of the gallbladder may result from a variety of extrabiliary as well as biliary causes. The former include failure to take the contrast material, vomiting, gastric obstruction, malabsorption, diarrhea, and poor liver function. Biliary factors include obstruction of the common or cystic duct and inability of the gallbladder to concentrate bile. Poor opacification of the gallbladder without detectable cholelithiasis occurs in 20 per cent of patients on the initial cholecystogram performed with iopanoic acid. 3 Repeat examination in these cases is required because visualization is inadequate for accurate diagnosis. Gallbladder opacification is not always maximum on the first examination even in the normal. Ten per cent of patients with initial non visualization and 65 per cent of those with poor visualization are normal on the second examination.3 Consequently, initial impaired visualization does not definitely indicate the presence of disease and a second examination is required. 4 This waste of time and effort is regrettable, but failure to perform the repeat examination significantly impairs the accuracy of the procedure
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Figure 14. Supine (A) and erect (B) radiographs made during an oral cholecystogram. The gallstones are more easily detected on the erect projection because they form a distinct layer in the bile.
and invites unacceptable diagnostic error. The reasons for this phenomenon are unclear, but may be related to poor intestinal absorption15 or decreased hepatic excretion of the contrast materiaP 1 and to bile stasis in the gallbladder. 45 In performing cholecystography, careful attention must be given to radiographic technique. Properly exposed radiographs are essential. Upright spot films of the gallbladder made under fluoroscopic control or lateral decubitus projections should be made in every case since small gallstones may be overlooked on supine or prone projections. In the upright or decubitus views the stones fall to the dependent portion of the gallbladder where they become visible on the radiograph (Fig. 14). If, after the first examination of the gallbladder with 3.0 gm. of iopanoic acid, visualization is insufficient to exclude cholelithiasis, one of three courses may be followed. The cholecystogram may be repeated on the following day with a second dose of 3.0 gm. of iopanoic acid. The use of a double dose is never justified because it increases the risk of nephrotoxicity without improving radiographic visualization. A second alternative after initial impaired visualization is to perform an intravenous cholangiogram on the same day. This is more hazardous for the patient than the oral study and time consuming for the radiology department, but it provides drect evidence of biliary tract disease. Third, calcium ipodate (Oragraffin':') may be administered on the same day. This will improve gallbladder opacification within a few hours in one third of the patients *E. R. Squibb Inc., Princeton, N.J.
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with impaired visualization. 34 If no visualization is obtained, however, most authors still advise a third study with either ipodate or iopanoic acid on the next day. Burhenne recommends that every patient have a two day iopanoic acid preparation prior to the initial cholecystogram (personal communication, December 1971). This eliminates the need for two radiographic studies, but requires a two day preparation which may increase the patient's hospitalization unnecessarily. Use of the sodium salt of iopanoic acid or sodium tyropanoate (Bilopaque*) may circumvent the irregular absorption of iopanoic acid caused by its marked insolubility in water and reduce the need for a second cholecystogram. 42 In 40 per cent of cases, iopanoic acid produces side effects which are usually mild and without sequelae. 42 Approximately one quarter have diarrhea. Dysuria, nausea, vomiting, and a skin rash may occur. Coronary insufficiency and acute renal failure have been reported, both probably related to hypotension and localized ischemia. Transient retention of sulfobromophthalein and bilirubin may result when iopanoic acid is given because of competition for hepatic excretion. Pseudoalbuminuria for several days and elevation of the protein-bound iodine for several months may occur. Iopanoic acid has a marked urosuric effect, equal to probenecid.ao The use of a fatty meal as a routine part of cholecystography is of doubtful merit. Occasionally, however, cholesterolosis, adenomyomatosis, or small calculi become visible when the gallbladder contracts. When no calculi are identified on oral cholecystography in patients with a strong clinical history of biliary tract disease, cholecystokinin may be given in an attempt to identify chronic cholecystitis or biliary dyskinesia. Cholecystokinin is a hormone produced by the duodenal mucosa which is a potent stimulus to gallbladder contraction. Nathan et al. found acalcareous chronic cholecystitis at surgery in all patients who developed localized contraction of the fundus, body, or neck of the gallbladder following cholecystokinin and in whom cholecystokinin produced right upper quadrant pain (Fig. 15).31 Ninety-four per cent of these patients were either free of symptoms or markedly improved 3 to 48 months after cholecystectomy. Valberg studied 13 women with intermittent attacks of typical biliary-type pain in whom cholecystokinin reproduced the symptomsY In 12 who underwent cholecystectomy, no pathologic abnormality of the gallbladder was identified. These patients were followed for 30 to 44 months after surgery and all were relieved of their pain. The size, shape, and position of the gallbladder vary considerably. Large gallbladders are frequent in diabetics or after a vagotomy. 6 Small, trabeculated, poorly functioning gallbladders occur in many patients with cystic fibrosisP Occasionally, when the gallbladder has a long mesentery, the gallbladder may herniate into the foramen of Winslow. In these cases, cholecystography shows the body and fundus of the gallbladder rotated upward and medially. Such herniation is of doubtful clinical significance. Cholecystography is 97 to 99 per cent accurate in the detection of *Winthrop Laboratories Inc.
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* Figure 15. Oral cholecystogram showing localized contraction of the body of the gallbladder after the intravenous injection of cholecystokinin. Chronic acalcareous cholecystitis was found at surgery. (Courtesy of Dr. M. H. Nathan.)
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Figure , partly Figure16. 16. Oral Oralcholecystograms cholecystogramsinintwo twopatients patientsshowing showinga asingle single, partlycalcified calcifiedgallgallstone . stone(A) (A)and andmultiple multiplesmall smallstones stones(B) (B).
. ~. . .
Figure 17. 17.Upright radiograph made during an an oral cholecystogram showing layering Figure Upright radiograph made during oral cholecystogram showing layering of small gallstones in the bile. of small gallstones in the bile.
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cholelithiasis. 32 Gallstones may be single or multiple, large or sand-like (Fig. 16). Frequently they form a radiolucent layer at their own specific gravity in the bile on the upright projections (Fig. 1 7). Occasionally, the contrast material may precipitate in the gallbladder due to bacterial deconjugation of the glucuronide forming the original water insoluble compound. 40 In these cases, upright projections reveal opaque amorphous debris in the fundus of the gallbladder which must be differentiated from sand-like gallstones. Differentiation is usually possible on repeat cholecystogram. Precipitation does not usually recur, while cholelithiasis persists unchCiilged. Benign tumors of the gallbladder such as adenomatous polyps and a variety of pseudotumors such as pancreatic rests present as a radiolucent defect fixed to the wall of opacified gallbladders. Fixed defects in opacified gallbladders are almost never malignant since gallbladders with carcinoma rarely visualize on cholecystography (Fig. 18). The hyperplastic cholecystoses are a group of noninflammatory diseases of the gallbladder consisting primarily of cholesterolosis and adeno-
I
* Figure 18. Radiograph of the gallbladder showing faint opacification and multiple gallstones in a patient with diffuse carcinoma of the gallbladder wall. Radiographic visualization of the gallbladder in this circumstance is unusual.
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Figure 19. Upright radiograph made during an oral cholecystogram showing multiple radiolucencies in the gallbladder due to cholesterolosis.
myomatosis."n Either disease may be localized or diffuse in the gallbladder. Cholesterolosis produces radiolucencies in the gallbladder of varying size which do not fall to the fundus on upright radiographs (Fig. 19). This is in distinction to gallstones which usually are the same size and are free to collect in the fundus when the patient is upright. Adenomyomatosis produces small out-pouches of the gallbladder lumen which fill with contrast material (Fig. 20). In the localized form, defects in the fundus of the gallbladder are common. All forms of hyperplastic cholecystoses often exhibit hyperconcentration and tend to contract more vigorously after a fatty meal than do normal gallbladders. The clinical significance of these abnormalities is uncertain.
INTRA VENOUS CHOLANGIOGRAPHY The contrast material used for intravenous cholangiography in the United States is methyglucamine iodipamide (Cholograffin':'). After intravenous injection, the compound is carried in the blood bound to al'''E. R. Squibb Inc., Prip.ceton, N.J.
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humin and excreted by the liver by an active transport process without chemical modification. Various attempts by Fischer to increase the biliary excretion with bile salts, renal tubular blockers, and cortisone failed.'7 Raising the dose above an optimum range serves only to decrease hepatic excretory efficiency and to increase the amount of iodipamide eliminated by the kidneys. 18 In recent years several investigators have noted a marked reduction in nausea and vomiting when iodipamide is given by slow intravenous infusion rather than in a single bolus. 10 Some authors claim that the infusion technique also increases the degree of opacification of the biliary tree. 33 Ansell emphasizes that iodipamide is one of the most toxic contrast materials in use in clinical radiology. 2 In the United Kingdom, one death occurred in 5000 examinations with iodipamide compared to one death in 40,000 urographic procedures. With iodipamide, one patient in 160G.o;.ltad a severe reaction and one in 700 had an intermediate reaction compilred to one in 14,000 and one in 2000 respectively for urography patients. Clinical indications for the use of intravenous cholangiography include patients with an acute abdomen in whom it is desirable to diagnose or exclude cholecystitis promptly, patients with right upper quadrant abdominal symptoms after cholecystectomy, and patients with nonvisualization of the gallbladder on oral cholecystography when the nonvisuali-
* Figure 20. Oral cholecystogram showing localized (A) and generalized (B) adenomyomatosis of the gallbladder (arrows).
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Figure 21. Tomogram made during an intravenous cholangiogram showing contrast material in the duodenal cap simulating a gallbladder (arrow).
zation may be due to extrabiliary factors. According to Wise, visualization of the biliary tract is nearly always possible when the serum bilirubin is less than 1.0 mg. per 100 ml.44 It almost never occurs when the bilirubin is greater than 4.0 mg. per 100 ml. When the serum bilirubin is 2.0 mg. per 100 ml. visualization is usually possible, while at 3.0 mg. per 100 ml. opacification usually does not occur. Errors in interpretation may occur in a number of circumstances. Accumulation of contrast material in the duodenal cap may be mistaken for an opacified gallbladder (Fig. 21). Faint calcification in the left costal cartilages may have the appearance of the common duct. Also, incomplete mixing of opaque and nonopaque bile produces radiolucent defects in the gallbladder on the radiograph which may simulate gallstones (Fig. 22). The average diameter of the normal common duct is 8 mm. and the maximum normal diameter is 10 to 12 mm. 4 '3 Dilatation does not normally occur after cholecystectomy. 44 In postoperative patients when the common duct drains properly, maximum opacification of the duct occurs at 60 to 90 minutes followed by diminution of opacification at 2 hours.4 4
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Figure 22. Upright radiograph of the gallbladder made during an intravenous cholangiogram showing poorly defined radiolucencies in the gallbladder due to incomplete mixing of opaque and non-opaque bile.
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Figure 23. Tomogram made during an intravenous cholangiogram showing a single large gallstone in the common duct (arrows).
Reversal of these time-density relationships associated with loss of normal tapering of the duct indicates common duct obstruction at the ampulla. Gallstones in the common duct are visible as radiolucencies in the duct (Fig. 23). When impacted at the ampulla of Vater, only the convex proximal margin of the calculus may be identified. ·Wise claims that 10 per cent of patients with nonvisualization of the gallbladder on consecutive oral cholecystograms have a normal intravenous cholangiogram and probably do not have biliary tract disease. 43 In addition, according to Wise, 30 per cent of this group have visualization of the gallbladder which provides important direct evidence of biliary tract disease. However, most other authors find 97 to 99 per cent accuracy in the diagnosis of cholecystitis and cholelithiasis after nonvisualization of the gallbladder on consecutive oral cholecystograms when extrabiliary causes of nonvisualization have been excluded.a 2 Because of this, and in view of the hazards associated with the use of iodipamide reported by Ansell,2 routine use of intravenous cholangiography to further establish the diagnosis of gallbladder disease in these circumstances is not indicated.
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In cases of an acute abdomen, visualization of the common duct without opacification of the gallbladder after 4 hours is almost conclusive evidence of cholelithiasis. 21 Rarely gallbladder visualization may be delayed until 24 hours in normal patients. Visualization of the gallbladder in this circumstance excludes the diagnosis of acute cholecystitis. However, in Wise's series only 55 per cent of gallstones in the gallbladder were detected on intravenous cholangiography. 43 Hence, to exclude calculi, oral studies should follow the intravenous examination.
TRANSHEPATIC CHOLANGIOGRAPHY Transhepatic cholangiography permits the differentiation between obstructive and nonobstructive jaundice in patients in whom opacification of the biliary tree by oral or intravenous cholangiography is impossible (Fig. 24). By inserting a needle into the liver parenchyma percutaneously under fluoroscopic guidance either from a lateral or an anterior direction, contrast material can be injected into the hepatic bile ducts. Radiographs made in multiple positions including the upright disclose the presence and location of biliary obstruction and may determine its eti-
Figure 24. Transhepatic cholangiogram showing obstruction of the common duct due to carcinoma of the pancreas (arrow).
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Arterial phase of a normal celiac angiogram showing the cholecystic artery
(large arrows) arising from the right hepatic artery. The size of the gallbladder can be determined by the position of the smaller arterial branches (small arrows).
ology. This information can be of great importance to the surgeon who, at operation, may have difficulty identifying the structures at the porta hepatis because of adhesions or tumor. A successful examination is possible in nearly every case in which the biliary tree is dilated, whereas filling of a nondilated system is possible in only one half of the cases. The main complications of the technique are hemorrhage due to puncture of a blood vessel and bile peritonitis caused by leak of bile from the liver. Evans tabulated the world literature, collecting 851 patients in whom transhepatic cholangiography was attempted. 14 Cholangiograms were obtained in 653 with 4 fatalities attributed to the procedure or a mortality incidence of 0.5 per cent. While some insist that surgery be undertaken immediately after the procedure when obstructive jaundice is discovered in order to prevent bleeding and bile leakage, most authorities are confident that this is an unnecessary precaution.
CELIAC ANGIOGRAPHY The gallbladder is often visualized by angiography, especially with the use of superselective methods. In the arterial phase the cystic artery is usually seen arising from the proper hepatic artery close to its bifurca-
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tion (Fig_ 25)_ The two main branches of the cystic artery encircle the gallbladder and, together with secondary branches, outline its position, size, and shape_ The capiliary phase usually distinctly outlines the gallbladder by delineating its wall as a 2 to 3 mm_ thick radiopaque line (Fig_ 26). A large range of pathologic angiographic findings occur in patients with cholecystitis depending on the severity of the inflammatory reaction. With chronic inflammation, the vascularity is diminished. The gallbladder is small and the wall is opacified poorly. In acute cholecystitis, the cystic artery may be enlarged and the gallbladder wall opacifies intensely in the capillary phase. Rosch et al. studied 7 cases of carcinoma of the gallbladder angiographically and found abnormal findings in every case. 37 Tumor neovascularity and arterial encasement were the most constant finding. Extension of tumor into the liver hilus was determined by the presence of abnormal vessels and neovascularity in the porta hepatis. In jaundiced patients the detection of an enlarged gallbladder on the angiogram suggests the presence of obstructive jaundice. 36 When the jaundice is due to carcinoma of the pancreas, the angiogram may also show abnormal arterial branches and venous occlusion in the head of the pancreas. In the absence of jaundice, an enlarged gallbladder may indicate the presence of hydrops or empyema of the gallbladder.
Figure 26. Capillary phase of a normal celiac angiogram showing opacification of the wall of the gallbladder (arrows).
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Angiography is a complementary procedure in clinical diagnosis providing valuable information about the normal and pathological anatomy of the gallbladder. It allows the early diagnosis of malignant tumor, aids in the differentiation between inflammation and tumor, shows the extent of advanced tumor and helps in the evaluation of tumor operability.
OPERATIVE AND POSTOPERATIVE CHOLANGIOGRAPHY The purpose of operative cholangiography is to avoid unnecessary exploration of the common duct, to detect residual common duct calculi after duct exploration, to identify congenital anomalies, strictures and tumors of the biliary tree, and to determine the presence of a cystic duct remnant. In recent years there has been a definite trend toward more frequent use of operative cholangiography. Many surgeons and radiologists now recommend its routine use during cholecystectorny. 7 • 27 A number of papers in the literature confirm its value.' In a review of 3012 patients undergoing cholecystectomy by Kakos et al., the use of operative cholangiography rose progressively from 2.9 per cent in the 1951-1955 period to 93 per cent in the 1966-1970 period. 27 This change was associated with a decrease in the number of patients undergoing choledochotomy from 41 per cent to 25 per cent and by a striking increase in the number of positive explorations from 28 per cent to 62 per cent. Jolly noted a decrease of common duct exploration with the routine use of cholangiography from 70 per cent to 20 per cent. 25 Schulenburg had a decrease from 50 per cent to 10 per cent.3 8 In a series reported by Hicken, 23 the incidence of retained stones fell from 19 per cent when cholangiography was not used to 4 per cent with cholangiography. Several authors found that from 3 to 10 per cent of gallstones noted on cholangiography were clinically unsuspected. 16 • 20 Jolly noted 78 per cent accuracy for operative cholangiography and only 54 per cent for clinical judgment. 25 · Authorities who argue against the routine use of operative cholangiography claim the procedure significantly adds to the length of the operation.20 Some state that the cholangiogram is not reliable in the detection of calculi. However, when cholangiography is done routinely, technical efficiency improves. Most authors report that only 5 to 10 minutes are added to the operative time by the cholangiogram. 16• 38 False positive interpretations have been reported in from 2 to 7 per cent, while false negatives occur in from less than 2 to 4 per cent.'"· 22 • as Success with operative cholangiography depends on careful attention to the technical aspects of the examination. A preliminary radiograph before the injection of contrast material is mandatory. Precise radiographic technique using proper collimation, a short exposure time, and proper kilovoltage is necessary. All surgical instruments must be removed from the field during the x-ray exposure. The contrast material should be properly diluted so that it is neither too radiopaque nor too
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radiolucent. Fifty per cent sodium diatrizoate diluted one half is generally recommended, although when the common duct is markedly dilated, further dilution is usually necessary. An attempt should be made to fill both the right and left hepatic ducts in order to avoid overlooking calculi in the ducts within the liver. Air bubbles must be carefully eliminated from the injection tubing. The patient should be rotated 15° into the right posterior oblique positions so that the common duct is not obscured by the spine. This is best accomplished by putting the patient in the oblique position before surgery. During the operation, the patient is turned supine by rotating the operating table. If the table cannot be turned, the proper obliquity for the radiograph can be obtained by angling the x-ray tube. In this case, the radiographic grid must be turned at right angles to the patient. An appropriate tunnel must be available for easy positioning of the radiographic cassette and the surgeon must assist in properly positioning the cassette under the common duct. A radiologist should be available to ensure that the radiographic technique is satisfactory and to
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Figure 27. (arrows).
Normal operative cholangiogram showing filling of the pancreatic duct
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Figure 28. Operative cholangiogram showing two stones in the common duct which were not palpable at surgery (arrows).
review the radiographs as they are made. Whenever uncertainties arise, the examination should be repeated until the situation is clarified. Sources of error besides improper radiographic technique include confusion of functional for organic obstruction at the ampulla, inclination on the part of the surgeon to disregard evidence before him, and failure to persist until complete delineation of the biliary tree is obtained. 9 The pancreatic duct may fill during the cholangiogram (Fig. 27). It is not unusual to recognize gallstones on the cholangiogram when they are not palpable (Fig. 28). Occasionally the cholangiogram detects filling of the entire biliary system with gallstones or a congenital anomaly such as a choledochal cyst (Figs. 29 and 30). Postoperative cholangiography is valuable for the detection of retained calculi and for the evaluation of duct obstruction and other abnormalities such as tumors and strictures (Fig. 31).
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A number of techniques have been described recently for the nonoperative removal of retained common duct calculi using fluoroscopic guidance.3 9 Burhenne uses a ureteral stone extraction basket inserted through a steerable catheter':' to snare retained calculi.B He waits 4 weeks before removing the T-tube in order to allow a sinus tract to form. Then the T-tube is removed and the catheter is guided into the common duct through the tract. The wire basket is inserted through the catheter and into the common duct beyond the gallstone. The stone falls into the basket as the basket and catheter are withdrawn and the stone is removed.
*Medi-Tech Inc., Watertown, Mass.
Figure 29. Operative cholangiogram showing gallstones throughout the entire biliary tree. (Courtesy Dr. Theodore Hilbish.)
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Figure 30. Operative cholangiogram showing a choledochal cyst. (Courtesy of Dr. Lawrence Sweeney.)
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Figure 31. Postoperative cholangiogram showing irregularity of the distal portion of the common duct due to carcinoma of the pancreas (arrow).
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SUMMARY Radiology of the biliary tree plays a major role in the diagnosis of diseases of the gallbladder and bile ducts. The clinician must be aware of the diagnostic potential of all of the radiologic examinations that are available. A review of the various x-ray studies in use is presented. These include the plain abdominal radiograph, barium studies of the gastrointestinal tract, oral cholecystography, intravenous cholangiography, transhepatic cholangiography, celiac angiography, and operative and postoperative cholangiography.
REFERENCES 1. Acosta, J. M., Fotheringham, W. T., Ruiz, L. 0., and Nardi, G. L.: Operative cholangiography. Arch. Surg., 99:29-32, 1969. 2. Ansell, G.: Adverse reactions to contrast agents. Inves. Rad., 5:374-391, 1970. 3. Berk, R. N.: Consecutive dose phenomenon in oral cholecystography. Am. J. Roent., 110:230-234, 1970. 4. Berk, R.N.: The problem of impaired first-dose visualization of the gallbladder. Am. J. Roent., 113:186-188, 1971. 5. Berk, R.N., Armbuster, R., and Salzstein, S.: Carcinoma of the gallbladder associated with the porcelain gallbladder. Rad., 106:29-33, 1973. 6. Bloom, A. A., and Stachenfeld, R.: Diabetic cholecystomegaly. J.A.M.A., 208:357-359, 1969. 7~ Bordenheier, J. A., Kaminski, D. L., Willman, V. L., and Hanlon, C. R.: Ten year experience with direct cholangiography. Am. J. Surg., 118:900-905, 1969. 8. Burhenne, J. H.: Non-operative retained biliary tract stone extraction: a new roentgenologic technique. Am. J. Roent., 117:388-399, 1973. 9. Custer, D. C., and Clore, J. N.: Source of error in operative cholangiography. Arch. Surg., 100:664-667, 1970. 10. Darnborough, A., and Geffen, N.: Drip infusion cholangiography. Brit. J. Rad., 39:827832, 1966. 11. Dunn, C. R., and Berk, R.N.: The pharmaco-kinetics of Telepaque metabolism: The relation of blood concentration and bile flow to the rate of hepatic excretion. Am. J. Roent., 114:758-766, 1972. 12. Edmunds, R., and Hughes, J. H.: Re-exploration of common bile duct. Arch. Surg., 90:876-878, 1965. 13. Esterly, J. R., and Oppenheimer, E. H.: Observations in cystic fibrosis of the pancreas. I. The gallbladder. Bull. Johns Hopkins Hosp., 110:247-254,1962. 14. Evans, J. A., Glenn, F., Thorbjarna,rson, B., and Mujahed, Z.: Percutaneous transhepatic cholangiography. Rad., 78:362-370, 1962. 15. Evens, R. G., Schroer, C., and Koehler, P.R.: Importance of contrast absorption i:il evaluation of nonvisualized gallbladder. Rad., 98:354-368, 1971. 16. Ferris, D. 0., and Sterling, W. A.: Surgery of the biliary tract. SuRG. GLIN. N. AMER., 47:861-865, 1967. 17. Fischer, H. W.: Attempts to improve iodipamide intravenous cholangiography. Am. J. Roent., 96:477-483, 1966. 18. Fischer, H. W.: Excretion of iodipamide-relation of bile and urine output to dose. Rad., 84:483-491, 1965. 19. Genereux, F. P., and Tchang, S. P.: Hydrops of the gallbladder: Unusual roentgenographic demonstration. J. Can. Assoc. Rad., 21:39-42, 1970. 20. Glass, T. J.: Cholecystectomy and cholangiography. Surg., 43:452-464, 1968. 21. Harrington, 0. B., Beall, A. C., Noon, G., DeBakey, M. E.: Intravenous cholangiography in acute cholecystitis. Arch. Surg., 88:585-589, 1964. 22. Herman, R. E., and Hoerr, S. 0.: The value of routine use of operative cholangiography. Surg. Gynec. Obstet., 121:1015-1020, 1967. 23. Hicken, N. F., and McAllister, A. J.: Operative cholangiography as an aid in reducing the incidence of "overlooked" common duct stones. Surg., 55:753-758, 1964. 24. Joffe, H., and Wachowski, R. J.: Relation of density of cholecystographic shadows of the gallbladder to the iodine content. Rad., 38:43-45, 1942. 25. Jolly, P. C., Baker, J. W., and Schmidt, H. M.: Operative cholangiography. Arch. Surg., 99:29-32, 1969.
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26. Jutras, J. A.: Hyperplastic cholecystoses. Am. J. Roent., 83:795-827, 1960. 27. Kakos, G. S., Tompkins, R. K., Turnipseed, W., and Zollinger, R. M.: Operative cholangiography during routine cholecystectomy. Arch. Surg., 104:484-487, 1972. 28. Knoefel, P. K.: Radiocontrast Agents. New York, Pergamon Press, Inc., 1971. 29. Lasser, E. C.: Pharmacodynamics of biliary contrast media. RAD. CLrN. N. AMER., 4:511516, 1966. 30. Mudge, G. H.: Uricosuric action of cholecystographic agents. N. Eng. J. Med., 294:929933, 1971. 31. Nathan, M. H., Newman, A., Murray, D. J., and Camponovo, R.: Cholecystokinin cholecystography. Am. J. Roent., 110:240-251, 1970. 32. Ochsner, S. F.: Performance and reliability of cholecystography. South. Me d. J ., 63:12681272, 1970. 33. Payne, R. F.: Drip infusion cholangiography. Clin. Rad., 19:281-285, 1968. 34. Pogonowska, M. J ., and Collins, L. C.: Immediate repeat cholecystography with Oragrafincalcium after initial nonvisualization of the gallbladder. Rad., 93:178-181, 1969. 35. Rabushka, J. E., Love, L., and Moncada, R.: Infusion Tomography of the Gallbladder. Exhibit at the neeting of the Radiological Society of North America, Chicago, Illinois, 1972. 36. Redman, H. C., and Reuter, S. R.: Roentgenographic evaluation of patients with suspected obstructive jaundice. Sur g. Gynec. Obstet., 131:1110-1114, 1970. 37. Rosch, J., GroHman, J. H., and Steckel, R. J.: Arteriography in the diagnosis of gallbladder disease. Rad., 92:1485-1491, 1969. 38. Schulenburg, C. A. P.: Operative Cholangiography. London, Butterworth & Co. (Publishers) Ltd., 1966. 39. Short, W., and Howard, P.: Trans-T-tube biliary catheterization: Diagnostic and therapeutic tool. Inves. Rad., 5:274-276, 1970. 40. Theander, G.: Pseudoconcretions in precipitate of contrast medium in the gallbladder. Am. J. Roent., 86:828-830, 1969. 41. Valberg, L. S., Jabbari, M., Kerr, J. W., Curtis, A. C., and Ramchand, S.: Biliary pain in young women in the absence of gallstones. Gastroent., 60:1020-1025, 1971. 42. White, W. W., and Fischer, H. W.: A double blind study of Oragrafin and Telepaque. Am. J. Roent., 87:745-758, 1972. 43. Wise, R. E.: Intravenous Cholangiography. Springfield, Illinois, Charles C Thomas, 1962. 44. Wise, R. E., Johnston, D. 0., and Salzman, F. A.: The intravenous cholangiographic diagnosis of partial obstruction of the common duct. Rad., 68:507-525, 1957. 45. Zboralske, F. F., and Amberg, J. R.: Cholecysto-cholestasis: A cause of cholecystographic error. Am. J. Dig. Dis., 7:339-346, 1962.
Department of Radiology University Hospital 225 West Dickinson Street San Diego, California 92103
Radiology of the Gallbladder and Bile
Ducts Robert N. Berk, M.D.*
A thorough understanding of the radiology of the gallbladder and bile ducts is essential for the proper clinical management of patients with biliary tract disease. It is appropriate, therefore, that a review of the radiologic procedures used for the diagnosis of diseases of the gallbladder and bile ducts be included in a symposium on surgery of the biliary system. The x-ray techniques employed are plain abdominal radiographs, barium studies of the gastrointestinal tract, oral cholecystography, intravenous cholangiography, transhepatic cholangiography, celiac angiography, and operative and postoperative cholangiography. Transjugular cholangiography, cholangiography by direct cannulation via the duodenoscope, and abdominal echography are considered by other authors in this symposium.
PLAIN ABDOMINAL RADIOGRAPHS The oldest and simplest radiological method for the detection of disease of the biliary tract is the plain radiograph of the abdomen. Because only 10 to 30 per cent of gallstones are radiopaque, the plain radiograph is of relatively little value in the detection of cholelithiasis compared to cholecystography. Yet it is common to find cholelithiasis incidentally in patients having radiographic studies of the stomach, colon, or urinary tract. Figure 1 shows radiopaque gallstones on the plain abdominal radiograph of a 24 year old man. Thickened trabecular architecture of the skeleton is also visible. This permits a diagnosis of sickle cell anemia which explains the presence of gallstones in this young patient. In patients with acute cholecystitis, the plain abdominal radiograph may reveal a dilated loop of small intestine with air-fluid levels in the right upper quadrant. In these cases the localized paralytic ileus is due to impaired motility in a segment of the intestine adjacent to the inflammatory reaction. When hydrops or empyema of the gallbladder occurs, a mass adjacent to the liver may become visible on the abdominal radio''Associate Professor of Radiology, University of California, San Diego, School of Medicine, La Jolla, California
Surgical Clinics of North America- Vol. 53, No.5, October 1973
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* Figure 1. Plain abdominal radiograph in a 24 year old man with sickle cell disease. There are radiopaque gallstones in the gallbladder (arrows) and skeletal changes characteristic of sickle cell disease.
graph. Occasionally, perforation of the gallbladder can be detected when gallstones are noted free in the peritoneal cavity. Emphysematous cholecystitis is readily diagnosed by the presence of gas in the wall and in the lumen of the gallbladder (Fig. 2). When a gallstone obstructs the cystic duct, calcium may be deposited in the lumen or in the wall of the gallbladder. Calcium within the gallbladder, termed milk of calcium bile, is visible on the plain abdominal radiograph. In these cases the appearance of the gallbladder on the plain radiograph is often identical to a normal cholecystogram (Fig. 3). Calcification in the gallbladder wall is known as porcelain gallbladder. The plain radiograph shows an irregular ring of calcium in the right upper quadrant which often resembles a large single gallstone (Fig. 4). Two patients with carcinoma of the gallbladder in association with porcelain gallbladder have recently been reported, and 24 others have been described in the literature." The association is sufficiently common to warrant prophylactic cholecystectomy for porcelain gallbladder if the patient's general health permits. Erosion of a gallstone into the intestinal tract produces characteristic findings on the plain abdominal radiograph. If the gallstone is large enough to produce intestinal obstruction, gallstone ileus occurs. The ab-
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Figure 2. Upright plain abdominal radiograph of an elderly woman showing gas in the wall and in the lumen of the gallbladder, indicative of emphysematous cholecystitis.
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* Figure 3. Plain abdominal radiograph showing milk of calcium bile in the gallbladder. No contrast material has been given.
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* Figure 4. Plain abdominal radiograph showing calcification in the wall of the gallbladder characteristic of porcelain gallbladder.
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dominal radiograph discloses air in the biliary tree, gas-filled distended loops of small intestine, and a gallstone in an ectopic location (Figs. 5 and 6). Figure 7 shows air in the common duct in an elderly patient who developed a cholecystocolic fistula due to erosion of a gallstone into the colon. Genereux and Tchang reported a case of hydrops of the gallbladder in which the gallbladder wall was visible on tomograms of the right upper quadrant of the abdomen made after the infusion of a large amount of diatrizoate, a urinary contrast material. 19 The gallbladder failed to visualize on routine cholecystography or intravenous cholangiography. Recognizing that the gallbladder was enlarged, they made a correct diagnosis of hydrops. Rabushka et al. studied a group of patients with nonvisualization of the gallbladder by tomography after a large-dose infusion of diatrizoate.35 In their cases, visualization of a thickened, irregular wall was accurate evidence of acute or chronic cholecystitis. The wall of normal gallbladders rarely opacified. When seen, it was thin and sharp. This technique requires further evaluation, for it may prove to be a valuable tool for studying gallbladders which cannot be opacified by conventional techniques (Fig. 8).
* Figure 5. Plain abdominal radiograph showing gallstone ileus. There is distention of the small intestine and air in the common duct (arrow).
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•• Figure 6. Plain abdominal radiograph in a patient a cholecystoduodenal fistula. Figure 6. Plain abdominal radiograph in a patient with with a cholecystoduodenal fistula. is a radiopaque gallstone the terminal (arrow). ThereThere is a radiopaque gallstone in theinterminal ileumileum (anow).
* Figure 7. Right quadrant of a plain abdominal radiograph showing Figure 7. Right upperupper quadrant of a plain abdominal radiograph showing air in air thein the biliary tree (arrows) in a patient a cholecystocolic fistula. (Courtesy Dr. Lawrence biliary tree (armws) in a patient with with a cholecystocolic fistula. (Courtesy of Dr.ofLawrence Sweeney.) Sweeney.)
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* Figure 8. Tomogram of the right upper quadrant of the abdomen taken after the rapid intravenous injection of a large dose of diatrizoate. The gallbladder wall is opacified (arrows). Thickening of the wall and distention of the gallbladder indicate the presence of hydrops, which was confirmed at surgery. The right kidney is well visualized.
BARIUM STUDIES OF THE GASTROINTESTINAL TRACT Before the introduction of cholecystography in 1924, radiologists relied heavily on radiographic abnormalities in the stomach and duodenum for the diagnosis of gallbladder disease. The proximity of the gallbladder to the first part of the duodenum accounts for the spasm and edema which may occur in the duodenum in cases of acute cholecystitis (Fig. 9). Chronic cholecystitis produces adhesions which may distort the .duodenum. When the gallbladder lies against the hepatic flexure of the colon, cholecystitis may produce deformity of the colon which is visible on barium enema studies (Fig. 10). Upper gastrointestinal barium examinations may be useful in studying patients with jaundice due to a stone im~ted at the ampulla of Vater. In such cases, edema of the ampulla ofte'V produces a smooth, sharply defined mass in the wall of the second portion of the duodenum (Fig. 11). Carcinoma of the ampulla produces an irregular mass in the same location (Fig. 12). In both situations and in patients with jaundice due to carcinoma of the pancreas, the dilated common duct may compress the duodenum in a characteristic fashion. The use of hypotonic duodenography (barium studies of the duodenum after the administration of an anticholinergic drug) is a valuable technique for detecting and evaluating such abnormalities.
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Figure 9.9. Supine Supine left left posterior posterior oblique oblique projection projection of of the the stomach stomach and and duodenum duodenum showshowFigure ing deformity deformity of of the the postbulbar postbulbar area area of of the the duodenum duodenum due due to to acute acute cholecystitis cholecystitis (arrow). ( an·ow). ing
Figure 10. 10. Barium Barium enema enema examination examination showing showing deformity deformity of of the the hepatic hepatic flexure Figure flexure due due to acute acute cholecystitis. cholecystitis. (Courtesy (Courtesy of of Dr. Dr. Wendell Wendell Dietz.) Dietz.) to
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Figure 11. Barium study of the duodenum showing a smooth mass at the ampulla of Vater due to edema of the ampulla caused by an impacted gallstone (arrow).
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Figure 12. Barium study of the duodenum showing an irregular mass at the ampulla of Vater caused by carcinoma of the ampulla (arrows).
Barium studies may disclose the presence of a cholecystoduodenal fistula. In these cases barium may enter the biliary tree or outline a gallstone in the intestine (Fig. 13).
ORAL CHOLECYSTOGRAPHY The introduction of cholecystography into diagnostic radiology by Graham and Cole in 1924 was based on two physiologic facts. 16 It had been shown by Abel and Rowntree that certain halogenated dyes are excreted almost entirely into the bile. Rous and McMaster then discovered that the gallbladder concentrates bile 8 to 10 times. Thus the halogen appears in bile and is sufficiently concentrated to permit radiographic visualization of the gallbladder. Since 1952, the most frequently used contrast material in the United States has been iopanoic acid (Telepaque''). This material, which is highly insoluble in water, is absorbed by passive diffusion across the intestinal mucosa, transported in the blood bound to albumin, and taken up by the liver where it is con*Winthrop Laboratories Inc., New York, N.Y.
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Figure 13. Barium study of the duodenum showing a gallstone (arrows) impacted in the third portion. A small amount of barium can be seen entering a cholecystoduodenal fistula at the apex of the duodenal cap. (Courtesy of Dr. William Pogue.)
jugated into the more water-soluble glucuronide. 29 The rate of excretion into the bile is directly related to the volume of bile flow. 11 Once in the gallbladder, the contrast material is concentrated by reabsorption of water from the bile. A concentration of 0.25 to 1.0 per cent iodine is required in the gallbladder for radiographic visualization. 24 Impaired visualization of the gallbladder may result from a variety of extrabiliary as well as biliary causes. The former include failure to take the contrast material, vomiting, gastric obstruction, malabsorption, diarrhea, and poor liver function. Biliary factors include obstruction of the common or cystic duct and inability of the gallbladder to concentrate bile. Poor opacification of the gallbladder without detectable cholelithiasis occurs in 20 per cent of patients on the initial cholecystogram performed with iopanoic acid. 3 Repeat examination in these cases is required because visualization is inadequate for accurate diagnosis. Gallbladder opacification is not always maximum on the first examination even in the normal. Ten per cent of patients with initial non visualization and 65 per cent of those with poor visualization are normal on the second examination.3 Consequently, initial impaired visualization does not definitely indicate the presence of disease and a second examination is required. 4 This waste of time and effort is regrettable, but failure to perform the repeat examination significantly impairs the accuracy of the procedure
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Figure 14. Supine (A) and erect (B) radiographs made during an oral cholecystogram. The gallstones are more easily detected on the erect projection because they form a distinct layer in the bile.
and invites unacceptable diagnostic error. The reasons for this phenomenon are unclear, but may be related to poor intestinal absorption15 or decreased hepatic excretion of the contrast materiaP 1 and to bile stasis in the gallbladder. 45 In performing cholecystography, careful attention must be given to radiographic technique. Properly exposed radiographs are essential. Upright spot films of the gallbladder made under fluoroscopic control or lateral decubitus projections should be made in every case since small gallstones may be overlooked on supine or prone projections. In the upright or decubitus views the stones fall to the dependent portion of the gallbladder where they become visible on the radiograph (Fig. 14). If, after the first examination of the gallbladder with 3.0 gm. of iopanoic acid, visualization is insufficient to exclude cholelithiasis, one of three courses may be followed. The cholecystogram may be repeated on the following day with a second dose of 3.0 gm. of iopanoic acid. The use of a double dose is never justified because it increases the risk of nephrotoxicity without improving radiographic visualization. A second alternative after initial impaired visualization is to perform an intravenous cholangiogram on the same day. This is more hazardous for the patient than the oral study and time consuming for the radiology department, but it provides drect evidence of biliary tract disease. Third, calcium ipodate (Oragraffin':') may be administered on the same day. This will improve gallbladder opacification within a few hours in one third of the patients *E. R. Squibb Inc., Princeton, N.J.
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with impaired visualization. 34 If no visualization is obtained, however, most authors still advise a third study with either ipodate or iopanoic acid on the next day. Burhenne recommends that every patient have a two day iopanoic acid preparation prior to the initial cholecystogram (personal communication, December 1971). This eliminates the need for two radiographic studies, but requires a two day preparation which may increase the patient's hospitalization unnecessarily. Use of the sodium salt of iopanoic acid or sodium tyropanoate (Bilopaque*) may circumvent the irregular absorption of iopanoic acid caused by its marked insolubility in water and reduce the need for a second cholecystogram. 42 In 40 per cent of cases, iopanoic acid produces side effects which are usually mild and without sequelae. 42 Approximately one quarter have diarrhea. Dysuria, nausea, vomiting, and a skin rash may occur. Coronary insufficiency and acute renal failure have been reported, both probably related to hypotension and localized ischemia. Transient retention of sulfobromophthalein and bilirubin may result when iopanoic acid is given because of competition for hepatic excretion. Pseudoalbuminuria for several days and elevation of the protein-bound iodine for several months may occur. Iopanoic acid has a marked urosuric effect, equal to probenecid.ao The use of a fatty meal as a routine part of cholecystography is of doubtful merit. Occasionally, however, cholesterolosis, adenomyomatosis, or small calculi become visible when the gallbladder contracts. When no calculi are identified on oral cholecystography in patients with a strong clinical history of biliary tract disease, cholecystokinin may be given in an attempt to identify chronic cholecystitis or biliary dyskinesia. Cholecystokinin is a hormone produced by the duodenal mucosa which is a potent stimulus to gallbladder contraction. Nathan et al. found acalcareous chronic cholecystitis at surgery in all patients who developed localized contraction of the fundus, body, or neck of the gallbladder following cholecystokinin and in whom cholecystokinin produced right upper quadrant pain (Fig. 15).31 Ninety-four per cent of these patients were either free of symptoms or markedly improved 3 to 48 months after cholecystectomy. Valberg studied 13 women with intermittent attacks of typical biliary-type pain in whom cholecystokinin reproduced the symptomsY In 12 who underwent cholecystectomy, no pathologic abnormality of the gallbladder was identified. These patients were followed for 30 to 44 months after surgery and all were relieved of their pain. The size, shape, and position of the gallbladder vary considerably. Large gallbladders are frequent in diabetics or after a vagotomy. 6 Small, trabeculated, poorly functioning gallbladders occur in many patients with cystic fibrosisP Occasionally, when the gallbladder has a long mesentery, the gallbladder may herniate into the foramen of Winslow. In these cases, cholecystography shows the body and fundus of the gallbladder rotated upward and medially. Such herniation is of doubtful clinical significance. Cholecystography is 97 to 99 per cent accurate in the detection of *Winthrop Laboratories Inc.
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* Figure 15. Oral cholecystogram showing localized contraction of the body of the gallbladder after the intravenous injection of cholecystokinin. Chronic acalcareous cholecystitis was found at surgery. (Courtesy of Dr. M. H. Nathan.)
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Figure , partly Figure16. 16. Oral Oralcholecystograms cholecystogramsinintwo twopatients patientsshowing showinga asingle single, partlycalcified calcifiedgallgallstone . stone(A) (A)and andmultiple multiplesmall smallstones stones(B) (B).
. ~. . .
Figure 17. 17.Upright radiograph made during an an oral cholecystogram showing layering Figure Upright radiograph made during oral cholecystogram showing layering of small gallstones in the bile. of small gallstones in the bile.
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cholelithiasis. 32 Gallstones may be single or multiple, large or sand-like (Fig. 16). Frequently they form a radiolucent layer at their own specific gravity in the bile on the upright projections (Fig. 1 7). Occasionally, the contrast material may precipitate in the gallbladder due to bacterial deconjugation of the glucuronide forming the original water insoluble compound. 40 In these cases, upright projections reveal opaque amorphous debris in the fundus of the gallbladder which must be differentiated from sand-like gallstones. Differentiation is usually possible on repeat cholecystogram. Precipitation does not usually recur, while cholelithiasis persists unchCiilged. Benign tumors of the gallbladder such as adenomatous polyps and a variety of pseudotumors such as pancreatic rests present as a radiolucent defect fixed to the wall of opacified gallbladders. Fixed defects in opacified gallbladders are almost never malignant since gallbladders with carcinoma rarely visualize on cholecystography (Fig. 18). The hyperplastic cholecystoses are a group of noninflammatory diseases of the gallbladder consisting primarily of cholesterolosis and adeno-
I
* Figure 18. Radiograph of the gallbladder showing faint opacification and multiple gallstones in a patient with diffuse carcinoma of the gallbladder wall. Radiographic visualization of the gallbladder in this circumstance is unusual.
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Figure 19. Upright radiograph made during an oral cholecystogram showing multiple radiolucencies in the gallbladder due to cholesterolosis.
myomatosis."n Either disease may be localized or diffuse in the gallbladder. Cholesterolosis produces radiolucencies in the gallbladder of varying size which do not fall to the fundus on upright radiographs (Fig. 19). This is in distinction to gallstones which usually are the same size and are free to collect in the fundus when the patient is upright. Adenomyomatosis produces small out-pouches of the gallbladder lumen which fill with contrast material (Fig. 20). In the localized form, defects in the fundus of the gallbladder are common. All forms of hyperplastic cholecystoses often exhibit hyperconcentration and tend to contract more vigorously after a fatty meal than do normal gallbladders. The clinical significance of these abnormalities is uncertain.
INTRA VENOUS CHOLANGIOGRAPHY The contrast material used for intravenous cholangiography in the United States is methyglucamine iodipamide (Cholograffin':'). After intravenous injection, the compound is carried in the blood bound to al'''E. R. Squibb Inc., Prip.ceton, N.J.
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humin and excreted by the liver by an active transport process without chemical modification. Various attempts by Fischer to increase the biliary excretion with bile salts, renal tubular blockers, and cortisone failed.'7 Raising the dose above an optimum range serves only to decrease hepatic excretory efficiency and to increase the amount of iodipamide eliminated by the kidneys. 18 In recent years several investigators have noted a marked reduction in nausea and vomiting when iodipamide is given by slow intravenous infusion rather than in a single bolus. 10 Some authors claim that the infusion technique also increases the degree of opacification of the biliary tree. 33 Ansell emphasizes that iodipamide is one of the most toxic contrast materials in use in clinical radiology. 2 In the United Kingdom, one death occurred in 5000 examinations with iodipamide compared to one death in 40,000 urographic procedures. With iodipamide, one patient in 160G.o;.ltad a severe reaction and one in 700 had an intermediate reaction compilred to one in 14,000 and one in 2000 respectively for urography patients. Clinical indications for the use of intravenous cholangiography include patients with an acute abdomen in whom it is desirable to diagnose or exclude cholecystitis promptly, patients with right upper quadrant abdominal symptoms after cholecystectomy, and patients with nonvisualization of the gallbladder on oral cholecystography when the nonvisuali-
* Figure 20. Oral cholecystogram showing localized (A) and generalized (B) adenomyomatosis of the gallbladder (arrows).
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Figure 21. Tomogram made during an intravenous cholangiogram showing contrast material in the duodenal cap simulating a gallbladder (arrow).
zation may be due to extrabiliary factors. According to Wise, visualization of the biliary tract is nearly always possible when the serum bilirubin is less than 1.0 mg. per 100 ml.44 It almost never occurs when the bilirubin is greater than 4.0 mg. per 100 ml. When the serum bilirubin is 2.0 mg. per 100 ml. visualization is usually possible, while at 3.0 mg. per 100 ml. opacification usually does not occur. Errors in interpretation may occur in a number of circumstances. Accumulation of contrast material in the duodenal cap may be mistaken for an opacified gallbladder (Fig. 21). Faint calcification in the left costal cartilages may have the appearance of the common duct. Also, incomplete mixing of opaque and nonopaque bile produces radiolucent defects in the gallbladder on the radiograph which may simulate gallstones (Fig. 22). The average diameter of the normal common duct is 8 mm. and the maximum normal diameter is 10 to 12 mm. 4 '3 Dilatation does not normally occur after cholecystectomy. 44 In postoperative patients when the common duct drains properly, maximum opacification of the duct occurs at 60 to 90 minutes followed by diminution of opacification at 2 hours.4 4
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Figure 22. Upright radiograph of the gallbladder made during an intravenous cholangiogram showing poorly defined radiolucencies in the gallbladder due to incomplete mixing of opaque and non-opaque bile.
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Figure 23. Tomogram made during an intravenous cholangiogram showing a single large gallstone in the common duct (arrows).
Reversal of these time-density relationships associated with loss of normal tapering of the duct indicates common duct obstruction at the ampulla. Gallstones in the common duct are visible as radiolucencies in the duct (Fig. 23). When impacted at the ampulla of Vater, only the convex proximal margin of the calculus may be identified. ·Wise claims that 10 per cent of patients with nonvisualization of the gallbladder on consecutive oral cholecystograms have a normal intravenous cholangiogram and probably do not have biliary tract disease. 43 In addition, according to Wise, 30 per cent of this group have visualization of the gallbladder which provides important direct evidence of biliary tract disease. However, most other authors find 97 to 99 per cent accuracy in the diagnosis of cholecystitis and cholelithiasis after nonvisualization of the gallbladder on consecutive oral cholecystograms when extrabiliary causes of nonvisualization have been excluded.a 2 Because of this, and in view of the hazards associated with the use of iodipamide reported by Ansell,2 routine use of intravenous cholangiography to further establish the diagnosis of gallbladder disease in these circumstances is not indicated.
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In cases of an acute abdomen, visualization of the common duct without opacification of the gallbladder after 4 hours is almost conclusive evidence of cholelithiasis. 21 Rarely gallbladder visualization may be delayed until 24 hours in normal patients. Visualization of the gallbladder in this circumstance excludes the diagnosis of acute cholecystitis. However, in Wise's series only 55 per cent of gallstones in the gallbladder were detected on intravenous cholangiography. 43 Hence, to exclude calculi, oral studies should follow the intravenous examination.
TRANSHEPATIC CHOLANGIOGRAPHY Transhepatic cholangiography permits the differentiation between obstructive and nonobstructive jaundice in patients in whom opacification of the biliary tree by oral or intravenous cholangiography is impossible (Fig. 24). By inserting a needle into the liver parenchyma percutaneously under fluoroscopic guidance either from a lateral or an anterior direction, contrast material can be injected into the hepatic bile ducts. Radiographs made in multiple positions including the upright disclose the presence and location of biliary obstruction and may determine its eti-
Figure 24. Transhepatic cholangiogram showing obstruction of the common duct due to carcinoma of the pancreas (arrow).
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Figure 25.
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Arterial phase of a normal celiac angiogram showing the cholecystic artery
(large arrows) arising from the right hepatic artery. The size of the gallbladder can be determined by the position of the smaller arterial branches (small arrows).
ology. This information can be of great importance to the surgeon who, at operation, may have difficulty identifying the structures at the porta hepatis because of adhesions or tumor. A successful examination is possible in nearly every case in which the biliary tree is dilated, whereas filling of a nondilated system is possible in only one half of the cases. The main complications of the technique are hemorrhage due to puncture of a blood vessel and bile peritonitis caused by leak of bile from the liver. Evans tabulated the world literature, collecting 851 patients in whom transhepatic cholangiography was attempted. 14 Cholangiograms were obtained in 653 with 4 fatalities attributed to the procedure or a mortality incidence of 0.5 per cent. While some insist that surgery be undertaken immediately after the procedure when obstructive jaundice is discovered in order to prevent bleeding and bile leakage, most authorities are confident that this is an unnecessary precaution.
CELIAC ANGIOGRAPHY The gallbladder is often visualized by angiography, especially with the use of superselective methods. In the arterial phase the cystic artery is usually seen arising from the proper hepatic artery close to its bifurca-
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tion (Fig_ 25)_ The two main branches of the cystic artery encircle the gallbladder and, together with secondary branches, outline its position, size, and shape_ The capiliary phase usually distinctly outlines the gallbladder by delineating its wall as a 2 to 3 mm_ thick radiopaque line (Fig_ 26). A large range of pathologic angiographic findings occur in patients with cholecystitis depending on the severity of the inflammatory reaction. With chronic inflammation, the vascularity is diminished. The gallbladder is small and the wall is opacified poorly. In acute cholecystitis, the cystic artery may be enlarged and the gallbladder wall opacifies intensely in the capillary phase. Rosch et al. studied 7 cases of carcinoma of the gallbladder angiographically and found abnormal findings in every case. 37 Tumor neovascularity and arterial encasement were the most constant finding. Extension of tumor into the liver hilus was determined by the presence of abnormal vessels and neovascularity in the porta hepatis. In jaundiced patients the detection of an enlarged gallbladder on the angiogram suggests the presence of obstructive jaundice. 36 When the jaundice is due to carcinoma of the pancreas, the angiogram may also show abnormal arterial branches and venous occlusion in the head of the pancreas. In the absence of jaundice, an enlarged gallbladder may indicate the presence of hydrops or empyema of the gallbladder.
Figure 26. Capillary phase of a normal celiac angiogram showing opacification of the wall of the gallbladder (arrows).
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Angiography is a complementary procedure in clinical diagnosis providing valuable information about the normal and pathological anatomy of the gallbladder. It allows the early diagnosis of malignant tumor, aids in the differentiation between inflammation and tumor, shows the extent of advanced tumor and helps in the evaluation of tumor operability.
OPERATIVE AND POSTOPERATIVE CHOLANGIOGRAPHY The purpose of operative cholangiography is to avoid unnecessary exploration of the common duct, to detect residual common duct calculi after duct exploration, to identify congenital anomalies, strictures and tumors of the biliary tree, and to determine the presence of a cystic duct remnant. In recent years there has been a definite trend toward more frequent use of operative cholangiography. Many surgeons and radiologists now recommend its routine use during cholecystectorny. 7 • 27 A number of papers in the literature confirm its value.' In a review of 3012 patients undergoing cholecystectomy by Kakos et al., the use of operative cholangiography rose progressively from 2.9 per cent in the 1951-1955 period to 93 per cent in the 1966-1970 period. 27 This change was associated with a decrease in the number of patients undergoing choledochotomy from 41 per cent to 25 per cent and by a striking increase in the number of positive explorations from 28 per cent to 62 per cent. Jolly noted a decrease of common duct exploration with the routine use of cholangiography from 70 per cent to 20 per cent. 25 Schulenburg had a decrease from 50 per cent to 10 per cent.3 8 In a series reported by Hicken, 23 the incidence of retained stones fell from 19 per cent when cholangiography was not used to 4 per cent with cholangiography. Several authors found that from 3 to 10 per cent of gallstones noted on cholangiography were clinically unsuspected. 16 • 20 Jolly noted 78 per cent accuracy for operative cholangiography and only 54 per cent for clinical judgment. 25 · Authorities who argue against the routine use of operative cholangiography claim the procedure significantly adds to the length of the operation.20 Some state that the cholangiogram is not reliable in the detection of calculi. However, when cholangiography is done routinely, technical efficiency improves. Most authors report that only 5 to 10 minutes are added to the operative time by the cholangiogram. 16• 38 False positive interpretations have been reported in from 2 to 7 per cent, while false negatives occur in from less than 2 to 4 per cent.'"· 22 • as Success with operative cholangiography depends on careful attention to the technical aspects of the examination. A preliminary radiograph before the injection of contrast material is mandatory. Precise radiographic technique using proper collimation, a short exposure time, and proper kilovoltage is necessary. All surgical instruments must be removed from the field during the x-ray exposure. The contrast material should be properly diluted so that it is neither too radiopaque nor too
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radiolucent. Fifty per cent sodium diatrizoate diluted one half is generally recommended, although when the common duct is markedly dilated, further dilution is usually necessary. An attempt should be made to fill both the right and left hepatic ducts in order to avoid overlooking calculi in the ducts within the liver. Air bubbles must be carefully eliminated from the injection tubing. The patient should be rotated 15° into the right posterior oblique positions so that the common duct is not obscured by the spine. This is best accomplished by putting the patient in the oblique position before surgery. During the operation, the patient is turned supine by rotating the operating table. If the table cannot be turned, the proper obliquity for the radiograph can be obtained by angling the x-ray tube. In this case, the radiographic grid must be turned at right angles to the patient. An appropriate tunnel must be available for easy positioning of the radiographic cassette and the surgeon must assist in properly positioning the cassette under the common duct. A radiologist should be available to ensure that the radiographic technique is satisfactory and to
*
Figure 27. (arrows).
Normal operative cholangiogram showing filling of the pancreatic duct
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Figure 28. Operative cholangiogram showing two stones in the common duct which were not palpable at surgery (arrows).
review the radiographs as they are made. Whenever uncertainties arise, the examination should be repeated until the situation is clarified. Sources of error besides improper radiographic technique include confusion of functional for organic obstruction at the ampulla, inclination on the part of the surgeon to disregard evidence before him, and failure to persist until complete delineation of the biliary tree is obtained. 9 The pancreatic duct may fill during the cholangiogram (Fig. 27). It is not unusual to recognize gallstones on the cholangiogram when they are not palpable (Fig. 28). Occasionally the cholangiogram detects filling of the entire biliary system with gallstones or a congenital anomaly such as a choledochal cyst (Figs. 29 and 30). Postoperative cholangiography is valuable for the detection of retained calculi and for the evaluation of duct obstruction and other abnormalities such as tumors and strictures (Fig. 31).
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A number of techniques have been described recently for the nonoperative removal of retained common duct calculi using fluoroscopic guidance.3 9 Burhenne uses a ureteral stone extraction basket inserted through a steerable catheter':' to snare retained calculi.B He waits 4 weeks before removing the T-tube in order to allow a sinus tract to form. Then the T-tube is removed and the catheter is guided into the common duct through the tract. The wire basket is inserted through the catheter and into the common duct beyond the gallstone. The stone falls into the basket as the basket and catheter are withdrawn and the stone is removed.
*Medi-Tech Inc., Watertown, Mass.
Figure 29. Operative cholangiogram showing gallstones throughout the entire biliary tree. (Courtesy Dr. Theodore Hilbish.)
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Figure 30. Operative cholangiogram showing a choledochal cyst. (Courtesy of Dr. Lawrence Sweeney.)
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Figure 31. Postoperative cholangiogram showing irregularity of the distal portion of the common duct due to carcinoma of the pancreas (arrow).
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SUMMARY Radiology of the biliary tree plays a major role in the diagnosis of diseases of the gallbladder and bile ducts. The clinician must be aware of the diagnostic potential of all of the radiologic examinations that are available. A review of the various x-ray studies in use is presented. These include the plain abdominal radiograph, barium studies of the gastrointestinal tract, oral cholecystography, intravenous cholangiography, transhepatic cholangiography, celiac angiography, and operative and postoperative cholangiography.
REFERENCES 1. Acosta, J. M., Fotheringham, W. T., Ruiz, L. 0., and Nardi, G. L.: Operative cholangiography. Arch. Surg., 99:29-32, 1969. 2. Ansell, G.: Adverse reactions to contrast agents. Inves. Rad., 5:374-391, 1970. 3. Berk, R. N.: Consecutive dose phenomenon in oral cholecystography. Am. J. Roent., 110:230-234, 1970. 4. Berk, R.N.: The problem of impaired first-dose visualization of the gallbladder. Am. J. Roent., 113:186-188, 1971. 5. Berk, R.N., Armbuster, R., and Salzstein, S.: Carcinoma of the gallbladder associated with the porcelain gallbladder. Rad., 106:29-33, 1973. 6. Bloom, A. A., and Stachenfeld, R.: Diabetic cholecystomegaly. J.A.M.A., 208:357-359, 1969. 7~ Bordenheier, J. A., Kaminski, D. L., Willman, V. L., and Hanlon, C. R.: Ten year experience with direct cholangiography. Am. J. Surg., 118:900-905, 1969. 8. Burhenne, J. H.: Non-operative retained biliary tract stone extraction: a new roentgenologic technique. Am. J. Roent., 117:388-399, 1973. 9. Custer, D. C., and Clore, J. N.: Source of error in operative cholangiography. Arch. Surg., 100:664-667, 1970. 10. Darnborough, A., and Geffen, N.: Drip infusion cholangiography. Brit. J. Rad., 39:827832, 1966. 11. Dunn, C. R., and Berk, R.N.: The pharmaco-kinetics of Telepaque metabolism: The relation of blood concentration and bile flow to the rate of hepatic excretion. Am. J. Roent., 114:758-766, 1972. 12. Edmunds, R., and Hughes, J. H.: Re-exploration of common bile duct. Arch. Surg., 90:876-878, 1965. 13. Esterly, J. R., and Oppenheimer, E. H.: Observations in cystic fibrosis of the pancreas. I. The gallbladder. Bull. Johns Hopkins Hosp., 110:247-254,1962. 14. Evans, J. A., Glenn, F., Thorbjarna,rson, B., and Mujahed, Z.: Percutaneous transhepatic cholangiography. Rad., 78:362-370, 1962. 15. Evens, R. G., Schroer, C., and Koehler, P.R.: Importance of contrast absorption i:il evaluation of nonvisualized gallbladder. Rad., 98:354-368, 1971. 16. Ferris, D. 0., and Sterling, W. A.: Surgery of the biliary tract. SuRG. GLIN. N. AMER., 47:861-865, 1967. 17. Fischer, H. W.: Attempts to improve iodipamide intravenous cholangiography. Am. J. Roent., 96:477-483, 1966. 18. Fischer, H. W.: Excretion of iodipamide-relation of bile and urine output to dose. Rad., 84:483-491, 1965. 19. Genereux, F. P., and Tchang, S. P.: Hydrops of the gallbladder: Unusual roentgenographic demonstration. J. Can. Assoc. Rad., 21:39-42, 1970. 20. Glass, T. J.: Cholecystectomy and cholangiography. Surg., 43:452-464, 1968. 21. Harrington, 0. B., Beall, A. C., Noon, G., DeBakey, M. E.: Intravenous cholangiography in acute cholecystitis. Arch. Surg., 88:585-589, 1964. 22. Herman, R. E., and Hoerr, S. 0.: The value of routine use of operative cholangiography. Surg. Gynec. Obstet., 121:1015-1020, 1967. 23. Hicken, N. F., and McAllister, A. J.: Operative cholangiography as an aid in reducing the incidence of "overlooked" common duct stones. Surg., 55:753-758, 1964. 24. Joffe, H., and Wachowski, R. J.: Relation of density of cholecystographic shadows of the gallbladder to the iodine content. Rad., 38:43-45, 1942. 25. Jolly, P. C., Baker, J. W., and Schmidt, H. M.: Operative cholangiography. Arch. Surg., 99:29-32, 1969.
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26. Jutras, J. A.: Hyperplastic cholecystoses. Am. J. Roent., 83:795-827, 1960. 27. Kakos, G. S., Tompkins, R. K., Turnipseed, W., and Zollinger, R. M.: Operative cholangiography during routine cholecystectomy. Arch. Surg., 104:484-487, 1972. 28. Knoefel, P. K.: Radiocontrast Agents. New York, Pergamon Press, Inc., 1971. 29. Lasser, E. C.: Pharmacodynamics of biliary contrast media. RAD. CLrN. N. AMER., 4:511516, 1966. 30. Mudge, G. H.: Uricosuric action of cholecystographic agents. N. Eng. J. Med., 294:929933, 1971. 31. Nathan, M. H., Newman, A., Murray, D. J., and Camponovo, R.: Cholecystokinin cholecystography. Am. J. Roent., 110:240-251, 1970. 32. Ochsner, S. F.: Performance and reliability of cholecystography. South. Me d. J ., 63:12681272, 1970. 33. Payne, R. F.: Drip infusion cholangiography. Clin. Rad., 19:281-285, 1968. 34. Pogonowska, M. J ., and Collins, L. C.: Immediate repeat cholecystography with Oragrafincalcium after initial nonvisualization of the gallbladder. Rad., 93:178-181, 1969. 35. Rabushka, J. E., Love, L., and Moncada, R.: Infusion Tomography of the Gallbladder. Exhibit at the neeting of the Radiological Society of North America, Chicago, Illinois, 1972. 36. Redman, H. C., and Reuter, S. R.: Roentgenographic evaluation of patients with suspected obstructive jaundice. Sur g. Gynec. Obstet., 131:1110-1114, 1970. 37. Rosch, J., GroHman, J. H., and Steckel, R. J.: Arteriography in the diagnosis of gallbladder disease. Rad., 92:1485-1491, 1969. 38. Schulenburg, C. A. P.: Operative Cholangiography. London, Butterworth & Co. (Publishers) Ltd., 1966. 39. Short, W., and Howard, P.: Trans-T-tube biliary catheterization: Diagnostic and therapeutic tool. Inves. Rad., 5:274-276, 1970. 40. Theander, G.: Pseudoconcretions in precipitate of contrast medium in the gallbladder. Am. J. Roent., 86:828-830, 1969. 41. Valberg, L. S., Jabbari, M., Kerr, J. W., Curtis, A. C., and Ramchand, S.: Biliary pain in young women in the absence of gallstones. Gastroent., 60:1020-1025, 1971. 42. White, W. W., and Fischer, H. W.: A double blind study of Oragrafin and Telepaque. Am. J. Roent., 87:745-758, 1972. 43. Wise, R. E.: Intravenous Cholangiography. Springfield, Illinois, Charles C Thomas, 1962. 44. Wise, R. E., Johnston, D. 0., and Salzman, F. A.: The intravenous cholangiographic diagnosis of partial obstruction of the common duct. Rad., 68:507-525, 1957. 45. Zboralske, F. F., and Amberg, J. R.: Cholecysto-cholestasis: A cause of cholecystographic error. Am. J. Dig. Dis., 7:339-346, 1962.
Department of Radiology University Hospital 225 West Dickinson Street San Diego, California 92103