Hemobilia Following Percutaneous Transhepatic Cholangiography C. ELTON CAHOW, M.D., MORTON BURRELL, M.D., RALPH GRECO, M.D.*
Percutaneous transhepatic cholangiography is a safe, effective diagnostic procedure for use in evaluating the jaundiced patient. As is the case with most invasive diagnostic procedures there is a risk: an overall mortality rate of 0.5% and morbidity rate of 3-10%N. Fortunately hemobilia is an uncommon complication, encountered only four times in our series of 102 percutaneous cholangiograms. In every case of hemobilia the clotting parameters were normal. The one factor common to each case was distal obstruction of the extra hepatic bile ducts. However, this one factor may play an important role in the etiology and therapy of post cholangiographic hemobilia. The hemorrhage subsided spontaneously in every case following surgical decompression of the bile ducts and there was no further active bleeding postoperatively. The possible explanation for the cause of bleeding and the fact that it subsided following decompression of the bile ducts is discussed. All four patients survived this complication and in the 102 patients there were no deaths attributable to percutaneous transhepatic cholangiography.
S INCE its description by Huard and Do-Xuan-Hop in 1937,8 percutaneous transhepatic cholangiography has steadily gained favor as a safe, effective diagnostic procedure for use in evaluating the jaundiced patient. The differentiation between jaundice caused by extrahepatic biliary obstruction and that due to hepatocellular disease is often difficult or impossible using information gained by the usual techniques of history taking, physical examination, liver function tests and percutaneous needle biopsy of the liver. In addition, oral cholecystograms and intravenous cholangiograms will not visualize the biliary tract in patients whose serum bilirubin level is greater than 3 mg/100 ml.12 In these cases, percutaneous Submitted for publication April 14, 1976. Reprint requests: C. Elton Cahow, M.D., Department of Surgery, Yale University Medical School, 333 Cedar Street, New Haven, Connecticut 06510. * Present Address: College of Medicine & Dentistry of New Jersey, Rutgers Medical School, P.O. Box 101, Piscataway, New Jersey 08854.
From the Department of Surgery and Radiology, Yale University Medical School and the Yale New Haven Hospital, New Haven, Connecticut
transhepatic needle puncture of an intrahepatic bile duct and injection of a radiopaque contrast agent will not only outline the biliary ducts but will also establish the level of obstruction. In most cases the cause of the obstruction can also be determined by this method. If the ductal system is normal, the diagnosis of hepatocellular disease can be established with relative certainty and an operative procedure which carries an increased risk of morbidity and mortality in these patients is avoided. Unfortunately, despite these advantages, percutaneous transhepatic cholangiography is not without risk. Mujahed and Evans,4'12 reviewing 811 cases from the literature, including 140 cases of their own, noted a mortality of 0.5% (4 deaths) attributable to the procedure. The most common complication is the leakage of bile and/or blood into the peritoneal cavity from the needle track in the liver. This occurs in about 3-10%o of reported series. It is usually not serious and can be controlled at the time of exploration. More serious bleeding can occur if larger vessels about the porta hepatis or stomach are punctured. The one death in Mujahed and Evans' series resulted from laceration of a branch of the hepatic artery.12 Pneumothorax has occurred once in our series and has also been reported by Flemma et al.6'7 Since 42% of patients with common duct stones and over 50o of patients with benign stricture have infected bile, it is not surprising that septicemia has been reported.6 This occurred once in our series but was controlled with broadspectrum antibiotics following which surgery to decom-
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moved and the flow of bile from the puncture hole then ceased." The second case was a 54-year-old man with returrent abdominal pain 4 years following cholecystectomy. Dilated but non-obstructed bile ducts were visualized with the first needle puncture. Upon withdrawal from the liver the catheter filled with blood. "At the same moment the patient felt severe abdominal pain in the right upper quadrant and some seconds later vomited about 200 ml of bloody fluid." Two hours later blood was aspirated from the stomach. He had no further bleeding. The third patient Seldinger described was a 73-year-old jaundiced man with severe coronary artery disease. A dilated ductal system containing stones was outlined on the first puncture which entered a duct near the hilum. Exploration three hours later revealed hemoperitoneum and large amounts of blood in the gallbladder and common duct. The patient subsequently died and autopsy revealed abundant blood evidence of continued bleeding; ". clots in the abdomen and bile ducts and an extensive hematoma in the retroperitoneal space." Flemma et al.7 reported one case of hemobilia FIG. 1. Patient 1 (R.L.) Percutaneous transhepatic cholangiogram occurring after multiple attempts at placing a catheter demonstrating two large common duct calculi, a dilated ductal system percutaneously into a biliary radicle for decompression. and multiple stones in the gallbladder. The patient, who was in extremis with an obstructing carcinoma had a prothrombin time of only pancreatic press an obstructing pancreatic carcinoma was successVitamin K therapy. Surgical exploration 20%o despite fully performed. some time later revealed blood local anesthesia under Hemobilia is an unusual complication encountered with tree. clots in the biliary this procedure which has been mentioned but not stressed in the literature. Hemorrhage from the liver parenchyma Material into the biliary ducts was first described by Owens in 1848.13 However, Sandblom, in 1948, was the first to Between 1966 and 1975, 102 percutaneous cholangiouse the term hemobilia to describe this condition.9 grams were performed in the Yale-New Haven Hospital. The most frequent cause of hemobilia is abdominal There were no deaths attributable to the procedure. trauma with rupture of the liver substance resulting in However, 4 patients developed hemobilia. A discussion laceration of intrahepatic blood vessels and bile ducts.1'17 of the diagnosis, operative findings and management of Aneurysms of the hepatic artery,2 foreign bodies in the these cases is the subject of this report. bile duct such as T-tubes'1 and calculi,19 and neoplasm,5 have also been reported as causes of hemobilia. PerCase Reports cutaneous needle biopsy of the liver is also a well docuCase 1. R.L., a 54-year-old Caucasian man, was admitted to the mented cause of hemobilia.3'10 Yale-New Haven Hospital with a 6-week history of vague upper Hemobilia resulting from percutaneous transhepatic abdominal pain and icterus of two weeks duration. He had undergone cholangiography has received little attention. Seldinger, a left hemicolectomy two years previously for carcinoma of the colon reporting a series of 156 percutaneous cholangiograms, at which time a small abdominal aortic aneurysm was noted. The mentions 6 cases of "blood in the bile ducts."116 He patient, a liquor salesman, had a past history of alcoholism. On admission a mass was palpable in the right upper quadrant discusses 3 of these patients briefly. One was a 67and a firm nodular liver extended 2 cm below the right costal year-old man with recurrent abdominal pain who had margin. Admission CBC, prothrombin time, BUN, electrolytes, undergone cholecystectomy 8 years previously and protein and A/G ratio were all normal. The total bilirubin was 10.6 choledochotomy 3 years prior to percutaneous cholangio- mg/100 ml, with a direct bilirubin of 5.4 mg/100 ml. SGOT was 116 units and alkaline phosphatase was 192 IU. ECG and chest gram. Three attempts to puncture a bile duct were were normal. x-ray unsuccessful. Three days later the patient developed On May 31, 1972 a percutaneous transhepatic cholangiogram peritonitis. At operation bile-colored fluid was en- was successfully performed which demonstrated markedly dilated countered in the peritoneal cavity. However, "no stones intra and extrahepatic bile ducts with calculi in the common hepatic were found in the common duct but blood clots were reand common bile ducts (Fig. 1). The patient was taken immediately .
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to the operating room where exploration revealed moderately advanced Laennec's cirrhosis, and a distended gallbladder, but no evidence of tumor. The abdominal aorta was the site of a S cm aneurysm. A cholecystectomy was performed without incident. The common bile duct was dilated and filled with soft clotted fresh blood. A choledochotomy was performed with removal of a large clot from the duct following which there was brisk bleeding from the proximal bile duct. The proximal end of the bile duct was packed off while distal common duct exploration was carried out. A #8 Bake's dilator could be passed into the duodenum after the two large common duct calculi were removed. Blood loss from the proximal common bile duct was estimated at 500 cc but during the course of the procedure this drainage changed gradually to bile. The source of the hemorrhage was felt to be the left lobe where the needle puncture had occurred but this could not be definitely determined. After the bleeding had stopped spontaneously the duct was closed about a #12 T-tube and the subhepatic space drained with penrose drains. The patient's postoperative course was unremarkable except for three separate episodes of hemobilia through the T-tube which never required transfusions. A T-tube cholangiogram performed two weeks postoperatively revealed a large clot in the left hepatic and common bile duct (Fig. 2). The T-tube was left in place and a repeat T-tube cholangiogram was performed two weeks later (4 weeks postoperatively) (Fig. 3). This demonstrated patency of all the ducts with no filling defects. The T-tube was then removed without incident. His followup has subsequently been uncomplicated and the liver function tests have returned to normal levels. Case 2. A.D., a 69-year-old man, was admitted to the Yale-New Haven Hospital on February 2, 1972 with a chief complaint of weight loss and right upper quadrant pain. In 1969 the patient suffered similar symptoms and underwent barium enema, upper GI series and gallbladder series, all of which were normal. In April, 1970, because of persistent symptoms he underwent exploration at another hospital and was found to have acute cholecystitis and choledocholithiasis with a choledochoduodenal fistula. A cholecystectomy was performed
FIG. 2. Patient 1 (R.L.) T-tube cholangiogram two weeks following surgery demonstrates a large clot in the left hepatic duct and in the common bile duct surrounding the T-tube.
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FIG. 3. Patient 1 (R.L.) T-tube cholangiogram four weeks following surgery demonstrating complete resolution of the clots and a clear intra and extra hepatic biliary tree. but because of hypotension the common bile duct was not explored and the fistula was left intact. In September, 1970, he developed hip pain. Hip x-rays and liver biopsy were normal. His bilirubin at that time was 4.2 mg/100 ml. He was then transferred to the Yale-New Haven Hospital. On admission, his sclerae were icteric and the liver was palpable 4 cm below the right costal margin. Admission CBC, BUN, serum electrolytes and prothrombin time were normal. The direct bilirubin was 2.1 mg/100 ml with a total bilirubin of 3.7 mg/100 ml. Alkaline phosphatase was 576 IU and the SGOT was 102 units. On March 8, 1972 a percutaneous transhepatic cholangiogram revealed a large solitary calculus in the distal common bile duct (Fig. 4). At laparotomy the common bile duct was enlarged. A choledochotomy was performed and a large clot was removed from the lumen followed by brisk bleeding. After one-half hour of irrigation and packing, the bleeding spontaneously stopped. Estimated blood loss was approximately 300 cc. A choledocholithotomy was then performed and a #8 dilator was easily passed through the ampulla. The choledochoduodenal fistula was excised and oversewn. A T-tube cholangiogram performed at the end of the procedure was unremarkable (Fig. 5). His postoperative course was uneventful. A repeat T-tube cholangiogram on March 20, 1971 was normal and on March 23, 1971 the T-tube was removed. His course since that time has been uncomplicated. Case 3. V.N., a 62-year-old Caucasian woman, was admitted with a chief complaint of painless jaundice of one month's duration. Physical examination was unremarkable except for deep jaundice. The patient suffered from adult onset diabetes mellitus. CBC, BUN, electrolytes, serum protein, prothrombin time and platelets were normal. The total bilirubin was 19.6 mg/100 ml with a direct bilirubin of 11.8 mg/100 ml. The SGOT was 77 units and alkaline phosphatase was 86 IU. Liver scan revealed two filling defects in the right lobe
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On September 25, 1972 percutaneous transhepatic cholangiography unsuccessfully attempted and was terminated after 4 needle punctures. At laparotomy shortly thereafter, a hematoma in the falciform ligament and free blood in the peritoneal cavity were noted. The common bile duct was dilated and filled with fresh blood. Blood clots and fresh unclotted blood were encountered when the common duct was opened. The bleeding eventually stopped after an estimated loss of 750 cc. Nine stones were then removed from the common bile duct and a #6 dilator could be passed through the ampulla. Because of the large number of stones, Fogarty catheters were passed proximally into the right and left hepatic ducts. No stones were found but the bleeding recurred from the left hepatic duct. When the bleeding had stopped, a T-tube was placed in the common duct and a cholangiogram was performed (Fig. 7). This was interpreted by the radiologist as demonstrating multiple stones in the left hepatic ducts. The common duct was re-opened, but after reirrigation of the proximal hepatic ducts revealed no further stones, it was agreed that the filling defects were blood clots. The operation was then terminated and the patient's course was thereafter uncomplicated. The postoperative T-tube cholangiogram performed two weeks later was unremarkable (Fig. 8) and the T-tube was removed without incident. was
Discussion From a review of the literature, one finds that hemobilia following percutaneous transhepatic cholangiography is fortunately an uncommon complication. The 4% incidence of this complication in our series of 102 FIG. 4. Patient 2 (A.D.) Transhepatic cholangiogram reveals a stone obstructing the distal common bile duct. A small fistula between the cystic duct remnant and duodenum may be seen. consistent with metastases. Needle biopsy of the liver revealed only cholestasis. On January 25, 1912, a percutaneous transhepatic cholangiogram demonstrated a dilated ductal system with distal common duct obstruction which was interpreted as carcinoma of the pancreas (Fig. 6). At laparotomy there was bloody fluid in the peritoneal cavity. The liver contained metastatic tumor nodules and there was a large, fixed stony-hard mass in the head of the pancreas. The hepatoduodenal liga-ment was infiltrated with blood and the common bile duct was enlarged and filled with clots and fresh blood. The pancreatic lesion was unresectable. Therefore, the gallbladder was opened in anticipation of performing a cholecystojejunostomy. At that point a large volume of clot and fresh blood were found within the lumen. After liberal irrigation, the bleeding cleared. The cholecystojejunostomy was performed but a choledochotomy was deferred. Estimated blood loss was 750 cc. Although she did not experience hematemesis or melena, the patient's postoperative course was complicated by a 12 point drop in hematocrit requiring two units of whole blood. She was discharged only to be readmitted 6 months later in a terminal state. She expired on June 6, 1972. Case 4. D.M., a 64-year-old Caucasian man, had undergone cholecystectomy 3 years prior to admission. Four days prior to admission to the Yale-New Haven Hospital on September 9, 1972, he developed abdominal pain, jaundice and pruritis. The admission physical examination was normal except for sclera icterus. CBC, BUN, electrolytes, prothrombin time and serum proteins were normal. The total bilirubin was 5.8 mg/100 ml with a direct bilirubin of 3.0 mg/100 ml. Alkaline phosphatase was 280 IU and SGOT was 120 units.
FIG. 5. Patient 2 (A.D.) Postoperative T-tube cholangiogram demonstrates free flow of contrast into the duodenum and no foreign bodies in the ductal system.
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studies seems unusually high when compared to other series. It may be that others have noted hemobilia at the time of exploration following transhepatic cholangiography but since it was self-limited or minimal they have not reported it. The clotting parameters, i.e. prothrombin time, partial thromboplastin time and platelet counts, were normal in all four of the patients who developed hemobilia following percutaneous cholangiogram in our series. Nor did any of them exhibit evidence of a bleeding problem clinically before, during or after surgery. It would also appear that the technique which was used in this series to obtain cholangiograms is not at fault. We have employed the standard technique using a teflon catheter over a steel 18-gauge needle. The cathetercovered needle is inserted into the right upper quadrant while the patient holds his breath in full inspiration. The steel needle is quickly removed leaving only the soft, pliable teflon catheter in the liver substance. After the catheter is in position, 50%o sodium diatrizoate (Hypaqueg) is injected into the liver under fluoroscopic visualization as the catheter is slowly withdrawn. In FIG. 7. Patient 4 (D.M.) Operative cholangiogram revealing two filling most cases the contrast agent enters the vascular struc- defects (clots) in the left hepatic duct misinterpreted as being stones. tures in the intrahepatic triads but this is quickly cleared by the rapid flow of blood in these vessels. We have never demonstrated a leak of the contrast agent from these vessels into a bile duct at the time transhepatic cholangiography was being performed. In none of our cases was a major vessel in the porta hepatis entered. In carefully reviewing the x-rays of the 4 patients who developed hemobilia, we could find nothing unusual which would make it possible to predict the presence of hemobilia prior to operation. This is an important consideration in patients who do not undergo exploration immediately after the study is performed. If hemobilia occurs in these patients the classical signs and symptoms of cramping abdominal or right upper quadrant pain, hematemesis or melena, hypotension, etc., with or without a palpable gallbladder should alert the surgeon to the diagnosis. The only factor common to all 4 patients in this series was dilatation of the biliary ducts secondary to distal obstruction. This one factor, however, may play an important role in the pathogenesis and method of therapy of hemobilia in these cases. Post-transhepatic cholangiographic hemobilia is due to the simultaneous puncture of closely adjacent bile ducts and blood vessels by the catheter-covered needle. As the catheter is withdrawn the communication between the vessel and bile duct persists, allowing the flow of blood from the high pressure system in the vessel to a low pressure system in the ducts. Judging from the force of the bleeding and the bright red color of the blood one would assume that the hemorrhage was coming from a FIG. 6. Patient 3 (V.N.) Percutaneous cholangiogram demonstrating complete occlusion of the common bile duct by carcinoma of the punctured intrahepatic artery. This cannot be factually substantiated by the x-rays and it is possible that the pancreas.
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and those reported elsewhere, has been simple decompression of the biliary ducts. In all cases except the one reported above by Seldinger,16 the bleeding has stopped spontaneously at the time of surgery. In only one of our patients (Case 1) was there any evidence of recurrent hemorrhage into the biliary tree. In that patient, bloody fluid was noted in the T-tube on three separate occasions during the postoperative period. The bleeding was never severe nor did he ever require transfusion. The postoperative cholangiogram (Fig. 2) revealed persistent clots in the left hepatic and common bile duct, but these cleared spontaneously within two weeks as noted on the second postoperative T-tube cholangiogram. The blood from the T-tube postoperatively was very dark and viscid suggesting that the patient was actually draining resolving intraductal clot rather than experiencing fresh bleeding. In none of the cases previously reported nor in any of the cases in our series was there evidence of intrahepatic hematoma with cavitation of the liver substance or abscess formation following percutaneous cholangiography. This probably accounts for the fact that there were no instances of delayed hemorrhage into the biliary tree which is often the case in hemobilia following other forms of penetrating or blunt hepatic trauma.9 Should persistent or delayed hemorrhage occur into the bile ducts, further steps should be considered. The source of the hemorrhage. should be accurately determined by selective hepatic artery arteriography. Once the source of the bleeding is found, surgical correction can be carried out by: 1) Simple suture ligation if the bleeding vessel is near the hepatic surface or 2) Limited hepatic resection or even lobectomy to control deep seated bleeding points. However, before lobectomy is considered, simple ligation of the appropriate hepatic artery should be considered if the bleeding is demonstrated to be coming from a branch of the hepatic artery. This will stop arterial bleeding with a lower morbidity and mortality rate than resection. None of the patients in our series required re-exploration and all survived this complication without undue morbidity. Use of the new thin needle (Chiba needle) instead of the standard 18 gauge needle that was employed in our cases may reduce or eliminate hemobilia as a complicacases,
S'.
''
"It' '-'I
LI
FIG. 8. Patient 4 (D.M.) T-tube cholangiogram two weeks following surgery shows free flow of contrast into the duodenum and complete filling of the biliary ducts with no filling defects.
bleeding resulted from puncture of the portal system. In most cases this communication closes spontaneously and little or no bleeding into the bile duct occurs. However, when the bile duct is dilated secondary to distal obstruction, it is unable to contract and the vascular biliary communication may remain open allowing blood to flow into the bile duct. Once the duct is opened and the obstruction removed or bypassed, the pressure in- tion of this excellent diagnostic test.14 side the duct is reduced and the tissues about the punctured bile duct and the wall of the blood vessel Conclusions can contract, thus closing the communication. Unlike Fortunately hemobilia is an uncommon complication needle biopsy of the liver, no tissue is removed by transhepatic cholangiography so that in the latter proce- following percutaneous transhepatic cholangiography. dure the blood vessel wall is essentially intact.18 This Four cases encountered at the Yale-New Haven Hospital puncture wound can seal itself in the same manner are presented. In every case there was obstruction with that occurs in peripheral vessels following needle punc- dilatation of the bile duct at the time the percutaneous ture. cholangiogram was performed. Prothrombin time and The therapy of postcholangiographic hemobilia in our platelets were within normal limits in all patients. The
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bleeding subsided spontaneously and did not recur in all cases once the ductal system was decompressed. The possible mechanism which caused hemobilia in these cases is reviewed. References 1. Amberson, J. R. and Ferguson, I. A.: Traumatic Hemobilia. Surgery, 54:729, 1963. 2. Ariyan, S., Cahow, C. E., Greene, F. L. and Stansel, H. C.: Successful Treatment of Hepatic Artery Aneurysm with Erosion into the Common Duct. Ann. Surg., 182:169, 1975. 3. Cox, E. F.: Hemobilia Following Percutaneous Needle Biopsy of the Liver. Arch. Surg., 95:198, 1967. 4. Evans, J. A. and Mujahed, Z.: Percutaneous Transhepatic Cholangiography. Conn. Med., 33:769, 1969. 5. Fisher, E. R. and Creed, D. L.: Clot Formation in the Common Duct: An Unusual Manifestation of Primary Hepatic Carcinoma. Arch. Surg., 73:261, 1956. 6. Flemma, R. J., Capp, M.D. and Shingleton, W. W.: Percutaneous Transhepatic Cholangiography. Arch. Surg., 90:5, 1965. 7. Flemma, R. J., Schauble, J. F., Gardner, C. E., Jr., et al.: Percutaneous Transhepatic Cholangiography in the Differential Diagnosis of Jaundice. Surg. Gynecol. Obstet., 116:559, 1963. 8. Huard, P. and Do-Xuan-Hop.: La Ponction Transhepatique
9. 10. 11. 12.
13. 14. 15.
16. 17.
18. 19.
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des Canaux Biliares. Bull. Soc. Med.-Chir. Indochine, 15: 1090, 1937. Katz, M.D. and Chien-Hsing Meng: Angiographic Evaluation of Traumatic Intrahepatic Pseudoaneurysm and Hemobilia. Radiology, 94:95, 1970. Levinson, J. D., Olsen, G., Terman, J. W., et al.: Hemobilia Secondary to Percutaneous Liver Biopsy. Arch. Intern. Med., 130:396, 1972. Manfredi, D. H.: Gastrointestinal Hemorrhage Originating in the Biliary Tract. New York J. Med., 58:2397, 1958. Mujahed, Z. and Evans, J. A.: Percutaneous Transhepatic Cholangiography. Rad. Clin. North Am. IV:3:535, 1966. Owens, H. K.: A Case of Lacerated Liver. London Med. Gaz., 7:1048, 1848. Redeker, A. G., et al.: Percutaneous Transhepatic Cholangiography: An Improved Technique. JAMA, 231:386, 1975. Sandblom, P.: Hemorrhage into the Biliary Tract Following Trauma: Traumatic Hemobilia. Surgery, 24:471, 1948. Seldinger, S. I.: Percutaneous Transhepatic Cholangiography. Acta. Radiol. Supplement 253, Stockholm, 1966. Steichen, F. M. and Scheiner, N. M.: Traumatic Intrahepatic Hemobilia. Arch. Surg., 92:838, 1966. Wallace, S., Medellin, H. and Nelson, R. S.: Angiographic Changes Due to Needle Biopsy of the Liver. Radiology, 105:13, 1972. White, F. W. and Jamkelson, I. R.: Gastrointestinal Hemorrhage in Diseases of the Gallbladder. N. Engl. J. Med., 25:793, 1931.
Percutaneous transhepatic cholangiography is a safe, effective diagnostic procedure for use in evaluating the jaundiced patient. As is the case with most invasive diagnostic procedures there is a risk: an overall mortality rate of 0.5% and morbidity rate of 3-10%N. Fortunately hemobilia is an uncommon complication, encountered only four times in our series of 102 percutaneous cholangiograms. In every case of hemobilia the clotting parameters were normal. The one factor common to each case was distal obstruction of the extra hepatic bile ducts. However, this one factor may play an important role in the etiology and therapy of post cholangiographic hemobilia. The hemorrhage subsided spontaneously in every case following surgical decompression of the bile ducts and there was no further active bleeding postoperatively. The possible explanation for the cause of bleeding and the fact that it subsided following decompression of the bile ducts is discussed. All four patients survived this complication and in the 102 patients there were no deaths attributable to percutaneous transhepatic cholangiography.
S INCE its description by Huard and Do-Xuan-Hop in 1937,8 percutaneous transhepatic cholangiography has steadily gained favor as a safe, effective diagnostic procedure for use in evaluating the jaundiced patient. The differentiation between jaundice caused by extrahepatic biliary obstruction and that due to hepatocellular disease is often difficult or impossible using information gained by the usual techniques of history taking, physical examination, liver function tests and percutaneous needle biopsy of the liver. In addition, oral cholecystograms and intravenous cholangiograms will not visualize the biliary tract in patients whose serum bilirubin level is greater than 3 mg/100 ml.12 In these cases, percutaneous Submitted for publication April 14, 1976. Reprint requests: C. Elton Cahow, M.D., Department of Surgery, Yale University Medical School, 333 Cedar Street, New Haven, Connecticut 06510. * Present Address: College of Medicine & Dentistry of New Jersey, Rutgers Medical School, P.O. Box 101, Piscataway, New Jersey 08854.
From the Department of Surgery and Radiology, Yale University Medical School and the Yale New Haven Hospital, New Haven, Connecticut
transhepatic needle puncture of an intrahepatic bile duct and injection of a radiopaque contrast agent will not only outline the biliary ducts but will also establish the level of obstruction. In most cases the cause of the obstruction can also be determined by this method. If the ductal system is normal, the diagnosis of hepatocellular disease can be established with relative certainty and an operative procedure which carries an increased risk of morbidity and mortality in these patients is avoided. Unfortunately, despite these advantages, percutaneous transhepatic cholangiography is not without risk. Mujahed and Evans,4'12 reviewing 811 cases from the literature, including 140 cases of their own, noted a mortality of 0.5% (4 deaths) attributable to the procedure. The most common complication is the leakage of bile and/or blood into the peritoneal cavity from the needle track in the liver. This occurs in about 3-10%o of reported series. It is usually not serious and can be controlled at the time of exploration. More serious bleeding can occur if larger vessels about the porta hepatis or stomach are punctured. The one death in Mujahed and Evans' series resulted from laceration of a branch of the hepatic artery.12 Pneumothorax has occurred once in our series and has also been reported by Flemma et al.6'7 Since 42% of patients with common duct stones and over 50o of patients with benign stricture have infected bile, it is not surprising that septicemia has been reported.6 This occurred once in our series but was controlled with broadspectrum antibiotics following which surgery to decom-
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moved and the flow of bile from the puncture hole then ceased." The second case was a 54-year-old man with returrent abdominal pain 4 years following cholecystectomy. Dilated but non-obstructed bile ducts were visualized with the first needle puncture. Upon withdrawal from the liver the catheter filled with blood. "At the same moment the patient felt severe abdominal pain in the right upper quadrant and some seconds later vomited about 200 ml of bloody fluid." Two hours later blood was aspirated from the stomach. He had no further bleeding. The third patient Seldinger described was a 73-year-old jaundiced man with severe coronary artery disease. A dilated ductal system containing stones was outlined on the first puncture which entered a duct near the hilum. Exploration three hours later revealed hemoperitoneum and large amounts of blood in the gallbladder and common duct. The patient subsequently died and autopsy revealed abundant blood evidence of continued bleeding; ". clots in the abdomen and bile ducts and an extensive hematoma in the retroperitoneal space." Flemma et al.7 reported one case of hemobilia FIG. 1. Patient 1 (R.L.) Percutaneous transhepatic cholangiogram occurring after multiple attempts at placing a catheter demonstrating two large common duct calculi, a dilated ductal system percutaneously into a biliary radicle for decompression. and multiple stones in the gallbladder. The patient, who was in extremis with an obstructing carcinoma had a prothrombin time of only pancreatic press an obstructing pancreatic carcinoma was successVitamin K therapy. Surgical exploration 20%o despite fully performed. some time later revealed blood local anesthesia under Hemobilia is an unusual complication encountered with tree. clots in the biliary this procedure which has been mentioned but not stressed in the literature. Hemorrhage from the liver parenchyma Material into the biliary ducts was first described by Owens in 1848.13 However, Sandblom, in 1948, was the first to Between 1966 and 1975, 102 percutaneous cholangiouse the term hemobilia to describe this condition.9 grams were performed in the Yale-New Haven Hospital. The most frequent cause of hemobilia is abdominal There were no deaths attributable to the procedure. trauma with rupture of the liver substance resulting in However, 4 patients developed hemobilia. A discussion laceration of intrahepatic blood vessels and bile ducts.1'17 of the diagnosis, operative findings and management of Aneurysms of the hepatic artery,2 foreign bodies in the these cases is the subject of this report. bile duct such as T-tubes'1 and calculi,19 and neoplasm,5 have also been reported as causes of hemobilia. PerCase Reports cutaneous needle biopsy of the liver is also a well docuCase 1. R.L., a 54-year-old Caucasian man, was admitted to the mented cause of hemobilia.3'10 Yale-New Haven Hospital with a 6-week history of vague upper Hemobilia resulting from percutaneous transhepatic abdominal pain and icterus of two weeks duration. He had undergone cholangiography has received little attention. Seldinger, a left hemicolectomy two years previously for carcinoma of the colon reporting a series of 156 percutaneous cholangiograms, at which time a small abdominal aortic aneurysm was noted. The mentions 6 cases of "blood in the bile ducts."116 He patient, a liquor salesman, had a past history of alcoholism. On admission a mass was palpable in the right upper quadrant discusses 3 of these patients briefly. One was a 67and a firm nodular liver extended 2 cm below the right costal year-old man with recurrent abdominal pain who had margin. Admission CBC, prothrombin time, BUN, electrolytes, undergone cholecystectomy 8 years previously and protein and A/G ratio were all normal. The total bilirubin was 10.6 choledochotomy 3 years prior to percutaneous cholangio- mg/100 ml, with a direct bilirubin of 5.4 mg/100 ml. SGOT was 116 units and alkaline phosphatase was 192 IU. ECG and chest gram. Three attempts to puncture a bile duct were were normal. x-ray unsuccessful. Three days later the patient developed On May 31, 1972 a percutaneous transhepatic cholangiogram peritonitis. At operation bile-colored fluid was en- was successfully performed which demonstrated markedly dilated countered in the peritoneal cavity. However, "no stones intra and extrahepatic bile ducts with calculi in the common hepatic were found in the common duct but blood clots were reand common bile ducts (Fig. 1). The patient was taken immediately .
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to the operating room where exploration revealed moderately advanced Laennec's cirrhosis, and a distended gallbladder, but no evidence of tumor. The abdominal aorta was the site of a S cm aneurysm. A cholecystectomy was performed without incident. The common bile duct was dilated and filled with soft clotted fresh blood. A choledochotomy was performed with removal of a large clot from the duct following which there was brisk bleeding from the proximal bile duct. The proximal end of the bile duct was packed off while distal common duct exploration was carried out. A #8 Bake's dilator could be passed into the duodenum after the two large common duct calculi were removed. Blood loss from the proximal common bile duct was estimated at 500 cc but during the course of the procedure this drainage changed gradually to bile. The source of the hemorrhage was felt to be the left lobe where the needle puncture had occurred but this could not be definitely determined. After the bleeding had stopped spontaneously the duct was closed about a #12 T-tube and the subhepatic space drained with penrose drains. The patient's postoperative course was unremarkable except for three separate episodes of hemobilia through the T-tube which never required transfusions. A T-tube cholangiogram performed two weeks postoperatively revealed a large clot in the left hepatic and common bile duct (Fig. 2). The T-tube was left in place and a repeat T-tube cholangiogram was performed two weeks later (4 weeks postoperatively) (Fig. 3). This demonstrated patency of all the ducts with no filling defects. The T-tube was then removed without incident. His followup has subsequently been uncomplicated and the liver function tests have returned to normal levels. Case 2. A.D., a 69-year-old man, was admitted to the Yale-New Haven Hospital on February 2, 1972 with a chief complaint of weight loss and right upper quadrant pain. In 1969 the patient suffered similar symptoms and underwent barium enema, upper GI series and gallbladder series, all of which were normal. In April, 1970, because of persistent symptoms he underwent exploration at another hospital and was found to have acute cholecystitis and choledocholithiasis with a choledochoduodenal fistula. A cholecystectomy was performed
FIG. 2. Patient 1 (R.L.) T-tube cholangiogram two weeks following surgery demonstrates a large clot in the left hepatic duct and in the common bile duct surrounding the T-tube.
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FIG. 3. Patient 1 (R.L.) T-tube cholangiogram four weeks following surgery demonstrating complete resolution of the clots and a clear intra and extra hepatic biliary tree. but because of hypotension the common bile duct was not explored and the fistula was left intact. In September, 1970, he developed hip pain. Hip x-rays and liver biopsy were normal. His bilirubin at that time was 4.2 mg/100 ml. He was then transferred to the Yale-New Haven Hospital. On admission, his sclerae were icteric and the liver was palpable 4 cm below the right costal margin. Admission CBC, BUN, serum electrolytes and prothrombin time were normal. The direct bilirubin was 2.1 mg/100 ml with a total bilirubin of 3.7 mg/100 ml. Alkaline phosphatase was 576 IU and the SGOT was 102 units. On March 8, 1972 a percutaneous transhepatic cholangiogram revealed a large solitary calculus in the distal common bile duct (Fig. 4). At laparotomy the common bile duct was enlarged. A choledochotomy was performed and a large clot was removed from the lumen followed by brisk bleeding. After one-half hour of irrigation and packing, the bleeding spontaneously stopped. Estimated blood loss was approximately 300 cc. A choledocholithotomy was then performed and a #8 dilator was easily passed through the ampulla. The choledochoduodenal fistula was excised and oversewn. A T-tube cholangiogram performed at the end of the procedure was unremarkable (Fig. 5). His postoperative course was uneventful. A repeat T-tube cholangiogram on March 20, 1971 was normal and on March 23, 1971 the T-tube was removed. His course since that time has been uncomplicated. Case 3. V.N., a 62-year-old Caucasian woman, was admitted with a chief complaint of painless jaundice of one month's duration. Physical examination was unremarkable except for deep jaundice. The patient suffered from adult onset diabetes mellitus. CBC, BUN, electrolytes, serum protein, prothrombin time and platelets were normal. The total bilirubin was 19.6 mg/100 ml with a direct bilirubin of 11.8 mg/100 ml. The SGOT was 77 units and alkaline phosphatase was 86 IU. Liver scan revealed two filling defects in the right lobe
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On September 25, 1972 percutaneous transhepatic cholangiography unsuccessfully attempted and was terminated after 4 needle punctures. At laparotomy shortly thereafter, a hematoma in the falciform ligament and free blood in the peritoneal cavity were noted. The common bile duct was dilated and filled with fresh blood. Blood clots and fresh unclotted blood were encountered when the common duct was opened. The bleeding eventually stopped after an estimated loss of 750 cc. Nine stones were then removed from the common bile duct and a #6 dilator could be passed through the ampulla. Because of the large number of stones, Fogarty catheters were passed proximally into the right and left hepatic ducts. No stones were found but the bleeding recurred from the left hepatic duct. When the bleeding had stopped, a T-tube was placed in the common duct and a cholangiogram was performed (Fig. 7). This was interpreted by the radiologist as demonstrating multiple stones in the left hepatic ducts. The common duct was re-opened, but after reirrigation of the proximal hepatic ducts revealed no further stones, it was agreed that the filling defects were blood clots. The operation was then terminated and the patient's course was thereafter uncomplicated. The postoperative T-tube cholangiogram performed two weeks later was unremarkable (Fig. 8) and the T-tube was removed without incident. was
Discussion From a review of the literature, one finds that hemobilia following percutaneous transhepatic cholangiography is fortunately an uncommon complication. The 4% incidence of this complication in our series of 102 FIG. 4. Patient 2 (A.D.) Transhepatic cholangiogram reveals a stone obstructing the distal common bile duct. A small fistula between the cystic duct remnant and duodenum may be seen. consistent with metastases. Needle biopsy of the liver revealed only cholestasis. On January 25, 1912, a percutaneous transhepatic cholangiogram demonstrated a dilated ductal system with distal common duct obstruction which was interpreted as carcinoma of the pancreas (Fig. 6). At laparotomy there was bloody fluid in the peritoneal cavity. The liver contained metastatic tumor nodules and there was a large, fixed stony-hard mass in the head of the pancreas. The hepatoduodenal liga-ment was infiltrated with blood and the common bile duct was enlarged and filled with clots and fresh blood. The pancreatic lesion was unresectable. Therefore, the gallbladder was opened in anticipation of performing a cholecystojejunostomy. At that point a large volume of clot and fresh blood were found within the lumen. After liberal irrigation, the bleeding cleared. The cholecystojejunostomy was performed but a choledochotomy was deferred. Estimated blood loss was 750 cc. Although she did not experience hematemesis or melena, the patient's postoperative course was complicated by a 12 point drop in hematocrit requiring two units of whole blood. She was discharged only to be readmitted 6 months later in a terminal state. She expired on June 6, 1972. Case 4. D.M., a 64-year-old Caucasian man, had undergone cholecystectomy 3 years prior to admission. Four days prior to admission to the Yale-New Haven Hospital on September 9, 1972, he developed abdominal pain, jaundice and pruritis. The admission physical examination was normal except for sclera icterus. CBC, BUN, electrolytes, prothrombin time and serum proteins were normal. The total bilirubin was 5.8 mg/100 ml with a direct bilirubin of 3.0 mg/100 ml. Alkaline phosphatase was 280 IU and SGOT was 120 units.
FIG. 5. Patient 2 (A.D.) Postoperative T-tube cholangiogram demonstrates free flow of contrast into the duodenum and no foreign bodies in the ductal system.
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studies seems unusually high when compared to other series. It may be that others have noted hemobilia at the time of exploration following transhepatic cholangiography but since it was self-limited or minimal they have not reported it. The clotting parameters, i.e. prothrombin time, partial thromboplastin time and platelet counts, were normal in all four of the patients who developed hemobilia following percutaneous cholangiogram in our series. Nor did any of them exhibit evidence of a bleeding problem clinically before, during or after surgery. It would also appear that the technique which was used in this series to obtain cholangiograms is not at fault. We have employed the standard technique using a teflon catheter over a steel 18-gauge needle. The cathetercovered needle is inserted into the right upper quadrant while the patient holds his breath in full inspiration. The steel needle is quickly removed leaving only the soft, pliable teflon catheter in the liver substance. After the catheter is in position, 50%o sodium diatrizoate (Hypaqueg) is injected into the liver under fluoroscopic visualization as the catheter is slowly withdrawn. In FIG. 7. Patient 4 (D.M.) Operative cholangiogram revealing two filling most cases the contrast agent enters the vascular struc- defects (clots) in the left hepatic duct misinterpreted as being stones. tures in the intrahepatic triads but this is quickly cleared by the rapid flow of blood in these vessels. We have never demonstrated a leak of the contrast agent from these vessels into a bile duct at the time transhepatic cholangiography was being performed. In none of our cases was a major vessel in the porta hepatis entered. In carefully reviewing the x-rays of the 4 patients who developed hemobilia, we could find nothing unusual which would make it possible to predict the presence of hemobilia prior to operation. This is an important consideration in patients who do not undergo exploration immediately after the study is performed. If hemobilia occurs in these patients the classical signs and symptoms of cramping abdominal or right upper quadrant pain, hematemesis or melena, hypotension, etc., with or without a palpable gallbladder should alert the surgeon to the diagnosis. The only factor common to all 4 patients in this series was dilatation of the biliary ducts secondary to distal obstruction. This one factor, however, may play an important role in the pathogenesis and method of therapy of hemobilia in these cases. Post-transhepatic cholangiographic hemobilia is due to the simultaneous puncture of closely adjacent bile ducts and blood vessels by the catheter-covered needle. As the catheter is withdrawn the communication between the vessel and bile duct persists, allowing the flow of blood from the high pressure system in the vessel to a low pressure system in the ducts. Judging from the force of the bleeding and the bright red color of the blood one would assume that the hemorrhage was coming from a FIG. 6. Patient 3 (V.N.) Percutaneous cholangiogram demonstrating complete occlusion of the common bile duct by carcinoma of the punctured intrahepatic artery. This cannot be factually substantiated by the x-rays and it is possible that the pancreas.
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o
February 1977
and those reported elsewhere, has been simple decompression of the biliary ducts. In all cases except the one reported above by Seldinger,16 the bleeding has stopped spontaneously at the time of surgery. In only one of our patients (Case 1) was there any evidence of recurrent hemorrhage into the biliary tree. In that patient, bloody fluid was noted in the T-tube on three separate occasions during the postoperative period. The bleeding was never severe nor did he ever require transfusion. The postoperative cholangiogram (Fig. 2) revealed persistent clots in the left hepatic and common bile duct, but these cleared spontaneously within two weeks as noted on the second postoperative T-tube cholangiogram. The blood from the T-tube postoperatively was very dark and viscid suggesting that the patient was actually draining resolving intraductal clot rather than experiencing fresh bleeding. In none of the cases previously reported nor in any of the cases in our series was there evidence of intrahepatic hematoma with cavitation of the liver substance or abscess formation following percutaneous cholangiography. This probably accounts for the fact that there were no instances of delayed hemorrhage into the biliary tree which is often the case in hemobilia following other forms of penetrating or blunt hepatic trauma.9 Should persistent or delayed hemorrhage occur into the bile ducts, further steps should be considered. The source of the hemorrhage. should be accurately determined by selective hepatic artery arteriography. Once the source of the bleeding is found, surgical correction can be carried out by: 1) Simple suture ligation if the bleeding vessel is near the hepatic surface or 2) Limited hepatic resection or even lobectomy to control deep seated bleeding points. However, before lobectomy is considered, simple ligation of the appropriate hepatic artery should be considered if the bleeding is demonstrated to be coming from a branch of the hepatic artery. This will stop arterial bleeding with a lower morbidity and mortality rate than resection. None of the patients in our series required re-exploration and all survived this complication without undue morbidity. Use of the new thin needle (Chiba needle) instead of the standard 18 gauge needle that was employed in our cases may reduce or eliminate hemobilia as a complicacases,
S'.
''
"It' '-'I
LI
FIG. 8. Patient 4 (D.M.) T-tube cholangiogram two weeks following surgery shows free flow of contrast into the duodenum and complete filling of the biliary ducts with no filling defects.
bleeding resulted from puncture of the portal system. In most cases this communication closes spontaneously and little or no bleeding into the bile duct occurs. However, when the bile duct is dilated secondary to distal obstruction, it is unable to contract and the vascular biliary communication may remain open allowing blood to flow into the bile duct. Once the duct is opened and the obstruction removed or bypassed, the pressure in- tion of this excellent diagnostic test.14 side the duct is reduced and the tissues about the punctured bile duct and the wall of the blood vessel Conclusions can contract, thus closing the communication. Unlike Fortunately hemobilia is an uncommon complication needle biopsy of the liver, no tissue is removed by transhepatic cholangiography so that in the latter proce- following percutaneous transhepatic cholangiography. dure the blood vessel wall is essentially intact.18 This Four cases encountered at the Yale-New Haven Hospital puncture wound can seal itself in the same manner are presented. In every case there was obstruction with that occurs in peripheral vessels following needle punc- dilatation of the bile duct at the time the percutaneous ture. cholangiogram was performed. Prothrombin time and The therapy of postcholangiographic hemobilia in our platelets were within normal limits in all patients. The
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bleeding subsided spontaneously and did not recur in all cases once the ductal system was decompressed. The possible mechanism which caused hemobilia in these cases is reviewed. References 1. Amberson, J. R. and Ferguson, I. A.: Traumatic Hemobilia. Surgery, 54:729, 1963. 2. Ariyan, S., Cahow, C. E., Greene, F. L. and Stansel, H. C.: Successful Treatment of Hepatic Artery Aneurysm with Erosion into the Common Duct. Ann. Surg., 182:169, 1975. 3. Cox, E. F.: Hemobilia Following Percutaneous Needle Biopsy of the Liver. Arch. Surg., 95:198, 1967. 4. Evans, J. A. and Mujahed, Z.: Percutaneous Transhepatic Cholangiography. Conn. Med., 33:769, 1969. 5. Fisher, E. R. and Creed, D. L.: Clot Formation in the Common Duct: An Unusual Manifestation of Primary Hepatic Carcinoma. Arch. Surg., 73:261, 1956. 6. Flemma, R. J., Capp, M.D. and Shingleton, W. W.: Percutaneous Transhepatic Cholangiography. Arch. Surg., 90:5, 1965. 7. Flemma, R. J., Schauble, J. F., Gardner, C. E., Jr., et al.: Percutaneous Transhepatic Cholangiography in the Differential Diagnosis of Jaundice. Surg. Gynecol. Obstet., 116:559, 1963. 8. Huard, P. and Do-Xuan-Hop.: La Ponction Transhepatique
9. 10. 11. 12.
13. 14. 15.
16. 17.
18. 19.
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des Canaux Biliares. Bull. Soc. Med.-Chir. Indochine, 15: 1090, 1937. Katz, M.D. and Chien-Hsing Meng: Angiographic Evaluation of Traumatic Intrahepatic Pseudoaneurysm and Hemobilia. Radiology, 94:95, 1970. Levinson, J. D., Olsen, G., Terman, J. W., et al.: Hemobilia Secondary to Percutaneous Liver Biopsy. Arch. Intern. Med., 130:396, 1972. Manfredi, D. H.: Gastrointestinal Hemorrhage Originating in the Biliary Tract. New York J. Med., 58:2397, 1958. Mujahed, Z. and Evans, J. A.: Percutaneous Transhepatic Cholangiography. Rad. Clin. North Am. IV:3:535, 1966. Owens, H. K.: A Case of Lacerated Liver. London Med. Gaz., 7:1048, 1848. Redeker, A. G., et al.: Percutaneous Transhepatic Cholangiography: An Improved Technique. JAMA, 231:386, 1975. Sandblom, P.: Hemorrhage into the Biliary Tract Following Trauma: Traumatic Hemobilia. Surgery, 24:471, 1948. Seldinger, S. I.: Percutaneous Transhepatic Cholangiography. Acta. Radiol. Supplement 253, Stockholm, 1966. Steichen, F. M. and Scheiner, N. M.: Traumatic Intrahepatic Hemobilia. Arch. Surg., 92:838, 1966. Wallace, S., Medellin, H. and Nelson, R. S.: Angiographic Changes Due to Needle Biopsy of the Liver. Radiology, 105:13, 1972. White, F. W. and Jamkelson, I. R.: Gastrointestinal Hemorrhage in Diseases of the Gallbladder. N. Engl. J. Med., 25:793, 1931.
