World J Surg DOI 10.1007/s00268-013-2435-5
Massive Hemobilia: A Diagnostic and Therapeutic Challenge Satish Devakumar Murugesan • Jeswanth Sathyanesan • Anand Lakshmanan • Sukumar Ramaswami • Senthilkumar Perumal • Srinivasan Ulagendra Perumal Ravi Ramasamy • Ravichandran Palaniappan
•
Ó Socie´te´ Internationale de Chirurgie 2013
Abstract Background Massive hemobilia is a rare but potentially life-threatening cause of upper gastrointestinal hemorrhage. In this retrospective analysis, we have evaluated the challenges involved in the diagnosis and management of massive hemobilia. Methods Between 2001 and 2011, a total of 20 consecutive patients (14 males) who were treated in our department for massive hemobilia were included in the study and their records were retrospectively analyzed. Results Causes of hemobilia were blunt liver trauma (n = 9), hepatobiliary intervention (n = 4), post-laparoscopic cholecystectomy hepatic artery pseudoaneurysm (n = 3), hepatobiliary tumors (n = 3), and vascular malformation
S. Devakumar Murugesan (&) J. Sathyanesan A. Lakshmanan S. Ramaswami S. Perumal S. Ulagendra Perumal R. Ramasamy R. Palaniappan Institute of Surgical Gastroenterology and Liver Transplantation, Government Stanley Medical College, Chennai 600001, India e-mail: [email protected] J. Sathyanesan e-mail: [email protected] A. Lakshmanan e-mail: [email protected] S. Ramaswami e-mail: [email protected] S. Perumal e-mail: [email protected] S. Ulagendra Perumal e-mail: [email protected] R. Ramasamy e-mail: [email protected] R. Palaniappan e-mail: [email protected]
(n = 1). Melena, abdominal pain, hematemesis, and jaundice were the leading symptoms. All patients had undergone upper GI endoscopy, abdominal ultrasound, and computerized tomography of the abdomen. An angiogram and therapeutic embolization were done in 12 patients and was successful in nine but failed in three, requiring surgery. Surgical procedures performed were right hepatectomy (n = 4), extended right hepatectomy (n = 1), segmentectomy (n = 1), extended cholecystectomy (n = 1), repair of the pseudoaneurysm (n = 3), and right hepatic artery ligation (n = 1). Conclusion The successful diagnosis of hemobilia depends on a high index of suspicion for patients with upper GI bleeding and biliary symptoms. Although transarterial embolization is the therapeutic option of choice for massive hemobilia, surgery has a definitive role in patients with hemodynamic instability, after failed embolization, and in patients requiring laparotomy for other reasons.
Introduction Hemorrhage into the biliary tract occurs when trauma or disease produces an abnormal communication between blood vessels and bile ducts, either within the liver or in the extrahepatic biliary tract. Based on clinical symptoms and severity, hemobilia is divided into massive hemobilia, which can be life-threatening and requires invasive treatment, and minor hemobilia, which is usually treated conservatively with blood transfusion. Massive hemobilia is a rare but potentially life-threatening condition that may be difficult to recognize, but it is, nonetheless, important to include it in the differential diagnosis of upper gastrointestinal (GI) bleeding. The diagnosis is not always easy to establish and often a long period elapses between the onset of the symptoms and identification of the source of the bleeding. Hemobilia is
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now being diagnosed with increasing frequency owing to widespread knowledge of the problem and improved diagnostic modalities [1]. In addition, there is an absolute increase in the frequency of massive hemobilia because of the increase in road traffic accidents and hepatobiliary intervention procedures. The objective of this retrospective study was to highlight the challenges involved in the diagnosis and management of massive hemobilia.
Materials and methods Twenty patients with massive hemobilia, treated at our institution between January 2001 and December 2011, were identified from a prospectively maintained database and registry. The demographic data, history, diagnostic features, including presenting symptoms, physical examination, investigations, and therapeutic modalities, were analyzed retrospectively. Initial treatment was directed at patient resuscitation and hemodynamic stabilization. Upper GI endoscopy, abdominal ultrasonography (USG), and contrast-enhanced computerized tomography (CECT) of the abdomen (CECT abdomen) were done in all patients after stabilization to identify the cause of bleeding. Angiography was done in selected patients to determine the source of bleeding. The algorithm used for the diagnosis and management of our patients with suspected hemobilia is depicted in Fig. 1. Definitive therapy was selected based on hemodynamic stability, overall performance status, underlying cause, and available expertise. Before 2006, all patients who presented with massive hemobilia underwent surgery after resuscitation. Due to the availability of the interventional radiology facility at our institution starting in November 2006, transarterial embolization (TAE) was used as a definitive therapy in patients with stable hemodynamics. Typically, the approach was through the right femoral artery using Seldinger’s method. The bleeding vessel was obliterated with gel foam or metallic coils. Surgery was performed in those with failed embolization, unstable hemodynamics, or resectable tumor. Depending on the cause of the hemobilia, hepatectomy, extended cholecystectomy, pseudoaneurysm repair, and hepatic artery ligation were performed. All patients, regardless of treatment, were monitored in the intensive care unit during the immediate post-treatment period. Postoperative complications and mortality were documented. Data were reported as the mean with range and percentage.
Results Of the 20 patients in our study group with massive hemobilia, 14 were males. The mean age of the group was
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34 years (range = 21–55 years). The most common presenting symptom was melena (n = 12), followed by abdominal pain, hematemesis, jaundice, and hypovolemic shock. Quincke’s triad of symptoms was present in 35 % of the cases. The mean transfusion requirement was 6 U (range = 3–12 U). Upper GI endoscopy revealed blood in the duodenum in only 12 patients (60 %). Abdominal ultrasound identified the source of bleeding in 15 patients (75 %). CECT abdomen demonstrated Grade III liver injury in 3 patients, Grade IV liver injury in 6 patients, pseudoaneurysm of hepatic artery (as seen in Fig. 2) in 5 patients, hepatocellular carcinoma in 1 patient, and gallbladder carcinoma in 1 patient. Conventional angiography was carried out in 12 patients, and it identified the source of bleeding in 11 patients (92 %). The most common cause for massive hemobilia in our series (Table 1) was blunt liver trauma, which was seen in 9 patients (45 %). Of these 9 patients, grade III and grade IV injuries were seen in 3 and 6 patients, respectively. There was no case of penetrating liver injury. The interventional procedures that caused hemobilia were percutaneous transhepatic biliary drainage for hilar cholangiocarcinoma (n = 1) and liver biopsy (n = 3). Indications for liver biopsy were post-necrotic cirrhosis (n = 1), cirrhosis of unknown origin (n = 1), and suspicion of hepatocellular carcinoma complicating alcoholic cirrhosis (n = 1). The time interval between liver puncture and clinical expression of hemobilia ranged from 1 to 28 days. Selective arterial embolization (Figs. 3 and 4) was attempted in all 12 patients who presented after November 2006 and was successful in 9 patients, as outlined in Table 2. The pre- and post-embolization films following superselective angiography with microcatheterization of the right hepatic artery pseudoaneurysm following laparoscopic cholecystectomy are shown in Figs. 5 and 6. The cause of failure of TAE in our series was due to not visualizing the source of the bleeding in one patient with blunt liver trauma. Two other patients had recurrent bleeding following TAE: one following gel-foam embolization and the other 15 days later from another part of the injured liver. Prior to the availability of interventional radiology expertise, eight patients underwent primary surgical intervention. After 2006, three patients (following failed embolization) required surgery. The procedures performed were right hepatectomy in four patients and hepatic artery pseudoaneurysm repair in three patients. Extended right hepatectomy, extended cholecystectomy, segmentectomy and right hepatic artery ligation were performed in one patient each. There were two deaths (10 %) in our series: one from sepsis and the other from liver failure. Six patients developed complications (30 %): two developed a bile leak that resolved spontaneously, three had a wound
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Fig. 1 Algorithm for the diagnosis and management of massive hemobilia
infection, and one developed a pulmonary complication (Table 3).
Discussion The phenomenon of bleeding into the biliary tree was first recorded in 1654 by Francis Glisson in his treatise, Anatomica Hepatis and a century later by Morgagni in 1765 [2–4]. The term ‘‘hemobilia’’ was first used by Sandblom in 1948 to describe a case of post-traumatic bleeding into the biliary tract [4]. Right hepatic artery ligation was first described by Kehr [4] in 1903 and angiographic embolization was first introduced by Walter [4] in 1976 for the treatment of hemobilia.
Classical clinical manifestation of hemobilia constitutes Quincke’s [4] triad of symptoms, consisting of abdominal pain (70 %), symptoms of bleeding from the upper digestive tract (melena in 90 % of cases and hematemesis in 60 %), and jaundice (60 %). However, the whole triad is present in only 22–30 % of patients with hemobilia [2]. In our series, melena was found in 60 %, abdominal pain in 40 %, hematemesis in 40 %, and jaundice in 35 % of cases. The triad of symptoms was present in 35 % of our patients. Hemorrhage is usually intermittent and repetitive and may be severe enough to cause hemodynamic instability due to the usual arterial origin of the bleeding. Thirty percent of patients presented with hemodynamic instability in our series. The onset of GI bleeding may occur within a few days after trauma or an interventional procedure, but
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Fig. 2 Computerized tomogram of abdomen showing large pseudoaneurysm with partial thrombus arising from hepatic artery Table 1 Etiology of hemobilia in various series
Fig. 4 Post coil embolization film showing effective obliteration of post-traumatic pseudoaneurysm in the anterior sectoral branch of the right hepatic artery
Etiology
Sandblom et al. [3]
Curet et al. [5]
Yoshida et al. [6]
Present series
Iatrogenic trauma
59 (17)
50 (58)
42 (41)
4 (20)
Accidental trauma
137 (38)
23 (27)
20 (19)
9 (45)
Table 2 Therapeutic interventions performed in 20 patients with massive hemobilia
Gallstones
53 (15)
–
9 (9)
3 (15)
No. cases
Inflammation
46 (13)
–
10 (10)
–
Vascular condition
38 (11)
–
15 (14)
1 (5)
Neoplastic disease Other
22 (6) –
– 13 (15)
7 (7) –
3 (15) –
Percentages in parentheses
Fig. 3 Superselective angiogram with microcatheter showing posttraumatic pseudoaneurysm in the anterior sectoral branch of the right hepatic artery
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Angioembolization
12 (60 %)
Successful
9 (75 %)
Failed
3 (25 %)
Surgery
11 (55 %)
Primary surgical intervention
8
Following failed TAE
3
more commonly it is delayed by weeks to months. The mean duration between trauma or the interventional procedure and onset of symptoms in our series was 9 days (range = 1–25 days). The etiology of bleeding into the biliary tract is diverse. Post-traumatic hemobilia is the most common etiological category, accounting for 55–85 % of cases in various series [3, 5, 6]. In the past, the most common cause of posttraumatic hemobilia was road traffic accidents (38 % in Sandblom’s series). Later, with the expanded use of interventional procedures, both diagnostic and therapeutic, iatrogenic hemobilia has become the most frequent etiological factor [5, 6]. Interestingly, in our series, post-traumatic hemobilia (45 %) was more common than iatrogenic hemobilia (20 %).This may be due to referral bias and the small cohort of patients in the present study. Iatrogenic hemobilia may occur during percutaneous liver procedures, liver or biliary surgery, or therapeutic
World J Surg Table 3 Outcomes after therapeutic interventions in 20 patients presented with massive hemobilia No. cases
Fig. 5 Selective hepatic angiogram demonstrating a right hepatic artery pseudoaneurysm following laparoscopic cholecystectomy
Fig. 6 Post-embolization film revealing effective obliteration of post laparoscopic cholecystectomy right hepatic artery pseudoaneurysm
anticoagulation. The frequency of clinical hemobilia is less than 1 % for liver biopsies [7, 8], 4 % for transhepatic cholangiography [9], and 3–14 % for percutaneous transhepatic catheter drainage [10, 11]. In our series, iatrogenic hemobilia occurred from liver biopsy (75 %) and percutaneous transhepatic biliary drainage (25 %). The other causes of hemobilia in our series were similar to those of other reported series, as summarized in Table 1. In gallstone-related hemobilia, hemorrhage may result from direct
Mortality
2 (10 %)
Sepsis
1
Liver failure
1
Morbidity
6 (30 %)
Bile leak
2
Wound infection
3
Pneumonitis
1
mucosal erosion, from hemorrhagic necrosis complicating severe cholecystitis, or cholangitis [12, 13]. An acalculous inflammatory condition of the biliary tract that causes hemobilia is most commonly due to ascariasis, followed by hepatic abscess, acalculous cholecystitis, cholangitis, hepatitis, pancreatitis, and chemical inflammation or erosion due to heterotopic gastric mucosa [14–17]. There were no cases of hemobilia due to inflammation in our series. Primary vascular causes of hemobilia include aneurysmal disease of the hepatic artery or portal vein, vasculitis, and portal hypertension. Lastly, hepatocellular carcinoma is the main neoplastic disease that causes hemobilia, with other neoplastic causes being hemangioma, cholangiocarcinoma, gallbladder carcinoma, and adenocarcinoma of the pancreas [6, 18, 19]. We had two patients with hepatocellular carcinoma and one patient with gallbladder carcinoma that caused hemobilia. Hemobilia is difficult to diagnose because the bleeding is usually intermittent. In patients with suspected hemobilia, the initial investigation is upper GI endoscopy, which may directly reveal blood flowing out of the papilla of Vater or indirectly by the presence of fresh blood in second part of the duodenum without an active bleeding site. Upper GI endoscopy may also rule out other common causes of bleeding such as erosive gastritis, peptic ulcers, and esophageal and gastric varices. In the present series, upper GI endoscopy was performed in all patients; it revealed fresh blood oozing from the papilla in 6 patients (30 %). Diagnosis was indirectly suggested in another 6 patients (30 %). The remaining 8 patients (40 %) had normal endoscopic findings. USG also may be helpful in the diagnosis of hemobilia, but it is nonspecific. Partial or total biliary obstruction can cause dilatation of the proximal segment of the biliary tract [20]. Blood clots are usually hyperechoic or isoechoic, assuming the shape of the bile duct and rendering them invisible. Echogenicity of clots decreases with time and with thrombus organization. Hypoechogenic clots can easily be missed during an ultrasound examination. Visualization of clots in the gallbladder is much easier and a newly formed thrombus in the
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gallbladder is usually hyperechogenic without acoustic shadow and does not change with position. Thrombus attached to the gallbladder wall may be misinterpreted as a polyp, bile sludge, neoplasm, or gangrenous cholecystitis. Adding Doppler ultrasound can be very useful to detect an aneurysm or a pseudoaneurysm of the hepatic artery [21– 23]. Abdominal USG was done in all patients, with positive findings in 15 patients (75 %). It is used mainly in blunt liver trauma for the detection of hepatic parenchymal injuries and hemoperitoneum. The sensitivity of ultrasound varies widely between 41 % [24] and 90 % [25], depending on the sonographer’s experience, the severity of the injury, the criteria used for determining the presence of liver injury, and when the ultrasound was performed relative to the timing of the injury [26, 27]. CECT abdomen is currently the diagnostic modality of choice for the evaluation of blunt liver trauma in hemodynamically stable patients [28]. The major CT features of blunt liver trauma are lacerations, subcapsular and parenchymal hematomas, active hemorrhage, and juxtahepatic venous injuries. Minor CT features include periportal low attenuation and a flat inferior vena cava (IVC). CECT abdomen revealed diffuse parenchymal injury resulting in large cavity-like lesions in seven patients and linear lacerations with an adjacent pseudoaneurysm in two patients. CECT abdomen can show focal change in the liver, the extent of hepatic injury or tumor, bile duct dilation, and blood clots [21]. CECT abdomen may also show simultaneous opacification of an aneurysmal artery in the arterial phase. Again, these findings are only suggestive of the diagnosis. Angiography made the correct diagnosis in more than 90 % of reported series [21]. Angiography delineates the arterial anatomy and the site of the pseudoaneurysm for therapeutic intervention. It can also show the presence of arteriobiliary fistula and vascular malformations like aneurysms, pseudoaneurysms, and hemangiomas. False-negative studies may occur if there is no active bleeding [29]. The advantage of angiography is that therapeutic embolization can be done immediately after identification of the bleeding vessel or pseudoaneurysm. In the present study, angiography was able to establish the diagnosis in 11 of 12 patients (97 %). Anecdotal reports indicate that technetium-labeled erythrocyte scans and the presence of fecal occult blood occasionally support or suggest the diagnosis, but a reliance on these tests for diagnosis cannot be justified [30]. Massive hemobilia can be diagnosed on clinical, endoscopic, and radiological findings, but a definitive diagnosis can be established only with angiography. In about 40 % of our cases, treatment for hemobilia was instituted based on clinical findings of upper GI bleeding and radiological findings. Overall, the diagnosis of hemobilia requires a high index of suspicion in patients with biliary symptoms and GI bleeding.
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The goals of therapy in massive hemobilia are (1) to stop the bleeding and (2) to restore bile flow. Patients with massive hemobilia usually present with hypovolemic shock and require resuscitation and hemodynamic stabilization. The management of hemobilia depends on the clinical state of patient, the rate of blood loss, the underlying cause of the hemobilia, and available expertise. Some studies have reported a conservative approach to the management of hemobilia [2, 31]. In a study by Green et al. [2], 43 % of patients with hemobilia were treated conservatively, embolization was performed in 36 %, and surgery was done in 20 % of the cases. The therapeutic options in massive hemobilia are angiographic embolization and surgery. Once hemodynamic stability is achieved, interventional radiographic methods are used for initial treatment and good results are achieved in 75–100 % of cases. We achieved a 75 % success rate in our series. Coil embolization not only provokes a thrombus in the aneurysm but may also obliterate the artery. The important prerequisite before TAE is to ensure the patency of the portal vein to avoid procedure-related liver necrosis and liver failure (6 %). Other less serious complications such as abscess formation (9 %), bleeding (6 %), and gallbladder fibrosis (2 %) have been reported following TAE [13, 32, 33]. Like Moodley et al. [34] and Forlee et al. [35], we did not encounter any procedure-related complications, but we had three failed embolization cases. The reasons for the failed embolizations were inability to isolate the bleeding vessel, incomplete arterial occlusion, or misidentification of the bleeding vessel. Surgical treatment is indicated for patients with hemodynamic instability, failed angioembolization, and for cases requiring laparotomy for liver trauma [36], resectable neoplasm, and hemorrhagic cholecystitis [3, 37–39]. Selective ligation of the bleeding vessel or aneurysm resection is a surgical maneuver that may be useful in some cases [13]. When the bleeding vessel cannot be identified, nonselective ligation of the right or left hepatic artery may be performed [3]. If bleeding continues from collateral vessels, even after ligation of the hepatic artery, resection of the affected liver segment may be required [40]. Hemorrhage from the gallbladder and hemorrhagic cholecystitis require urgent cholecystectomy [3, 37–39]. Surgical management of massive hemobilia in the present series achieved an overall success rate of 90 %, with rebleeding rates of less than 5 % and a mortality rate of 10 %.
Conclusions Upper GI bleeding in a patient with a history of trauma or hepatobiliary intervention and biliary symptoms should arouse suspicion for hemobilia. The successful diagnosis of
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hemobilia depends on a high index of suspicion, especially when the common causes of hemorrhaging in the upper GI tract have been excluded. A clinical suspicion of hemobilia should prompt confirmation of the diagnosis with endoscopy, ultrasound with Doppler, and/or computed tomography. Angiography is needed if the diagnosis is in doubt or other investigations are not contributory. Initial treatment involves patient resuscitation and hemodynamic stabilization. Careful consideration of the etiology, hemodynamic status, results of imaging, and available expertise will help to define the therapeutic options. Although TAE is the therapeutic option of choice in massive hemobilia, surgery has a definitive role in patients with hemodynamic instability, after failed angioembolization and in patients requiring laparotomy for other reasons.
Conflict of interest No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.
References 1. Blumgart LH (2007) Hemobilia and bilhemia. In: Blumgart LH (ed) Surgery of the liver, biliary tract, and pancreas, 4th edn. Elsevier, Philadelphia, pp 1067–1081 2. Green MH, Duell RM, Johnson CD, Jamieson NV (2001) Hemobilia. Br J Surg 88:773786 3. Sandblom P (1948) Hemorrhage into the biliary tract following trauma: ‘traumatic hemobilia’. Surgery 24:571–586 4. Merrell SW, Schneider PD (1991) Hemobilia: evolution of current diagnosis and treatment. West J Med 155:621–625 5. Curet P, Baumer R, Roche A, Grellet J, Mercadier M (1984) Hepatic hemobilia of traumatic or iatrogenic origin: recent advances in diagnosis and therapy, review of the literature from 1976 to 1981. World J Surg 8:2–8. doi:10.1007/BF01658356 6. Yoshida J, Donahue PE, Nyhus LM (1987) Hemobilia: review of recent experience with a worldwide problem. Am J Gastroenterol 82:448–453 7. Levinson JD, Olsen G, Terman JW (1972) Hemobilia secondary to percutaneous liver biopsy. Arch Intern Med 130:396–400 8. Lee SP, Tasman-Jones C, Wattie WJ (1977) Traumatic hemobilia: a complication of percutaneous liver biopsy. Gastroenterology 72:941–944 9. Cahow CE, Burrell M, Greco R (1977) Hemobilia following percutaneous transhepatic cholangiography. Ann Surg 185:235–241 10. Monden M, Okamura J, Kobayashi N et al (1980) Hemobilia after percutaneous transhepatic biliary drainage. Arch Surg 115:161– 164 11. Sarr MG, Kaufman SL, Zuidema GD, Cameron JL (1984) Management of hemobilia associated with transhepatic internal biliary drainage catheters. Surgery 95:603–607 12. Sandblom P, Mirkovitch V (1979) Minor hemobilia. Clinical significance and patho-physiological background. Ann Surg 190:254–264 13. Czemiak A, Thompson JN, Hemingway AP et al (1988) Hemobilia: a disease in evolution. Arch Surg 123:718–721
14. Blumenthal DS (1988) Ascariasis. In: Wyngaarden JB, Smith LH (eds) Cecil Textbook of Medicine, 18th edn. WB Saunders, Philadelphia, p 1908 15. Koshy A, Khuroo MS, Suri S, Datta DV, Khanna SK (1979) Amoebic liver abscess with hemobilia. Am J Surg 138:453–455 16. Wagner DS, Flynn MA (1985) Hemorrhagic acalculous cholecystitis causing acute pancreatitis after trauma. J Trauma 25:253–256 17. Adam R, Fabiani B, Bismuth H (1989) Hematobilia resulting from heterotopic stomach in the gallbladder neck. Surgery 105:564–569 18. Wright RC, Roberts JW (1988) Fibro lamellar carcinoma of the liver presenting with hemobilia. Contemp Surg 33:29–35 19. Hasan S, Quintana J, Siddiqui Y, Maldonado V (1986) Carcinoma of the pancreas presenting with hemobilia (Letter). Gastrointest Endosc 32:305–306 20. Laing FC, Frates MC, Feldstein VA, Goldstein RB, Mondro S (1997) Hemobilia: sonographic appearances in the gallbladder and biliary tree with emphasis on intracholecystic blood. J Ultrasound Med 16:537–543 21. Walter JF, Passo BT, Cannon WB (1976) Successful trans-catheter embolic control of massive hemobilia secondary to liver biopsy. AJR Am J Roentgenol 127:847–849 22. Greenberg M, Rubin JM, Crass JR (1983) The ultrasound appearance of an arteriobiliary fistula. J Clin Ultrasound 11:323–325 23. Grant EG, Smimiotopoulos JG (1983) Intraluminal gall bladder hematoma: sonographic evidence of hemobilia. J Clin Ultrasound 1:507–509 24. Poletti PA, Kinkel K, Vermeulen B et al (2003) Blunt abdominal trauma: should US be used to detect both free fluid and organ injuries? Radiology 227:95–103 25. Yoshii H, Sato M, Yamamoto S et al (1998) Usefulness and limitations of ultrasonography in the initial evaluation of blunt abdominal trauma. J Trauma 45:45–50 discussion 50–51 26. Kendall JL, Faragher J, Hewitt GJ, Burcham G, Haukoos JS (2009) Emergency department ultrasound is not a sensitive detector of solid organ injury. West J Emerg Med 10:1–5 27. Richards JR, McGahan JP, Pail MJ et al (1999) Sonographic detection of blunt hepatic trauma: hemoperitoneum and parenchymal injury patterns of injury. J Trauma 47:1092–1097 28. Yoon W, Jeong YY, Kim JK, Seo JJ, Lim HS, Shin SS et al (2005) CT in blunt liver trauma. Radiographics 25:87–104 29. Sharipo MJ (1994) The role of the radiologist in the management of gastrointestinal bleeding. Gastroenterol Clin North Am 23:123–131 30. Lee SM, Lee RGL, Clouse ME, Hill TC (1986) Demonstration of hemobilia using technetium-99m labeled red blood cells. Clin Nucl Med 11:52 31. Hsu KL, Ko SF, Chou FF, Sheen-Chen SM, Lee TY (2002) Massive hemobilia. Hepatogastroenterology 40:306–310 32. Franklin RH, Bloom WF, Schoffstall RO (1980) Angiographic embolization as the definitive treatment of post-traumatic hemobilia. J Trauma 20:702–705 33. Wagner WH, Lundell CJ, Donovan AJ (1985) Percutaneous angiographic embolization for hepatic arterial hemorrhage. Arch Surg 120:1241–1249 34. Moodley J, Sing B, Lallo S, Pershad S, Robbs JV (2001) Nonoperative management of hemobilia. Br J Surg 88:1073–1076 35. Forlee MV, Krige JE, Welman CJ, Beningfield SJ (2004) Hemobilia after penetrating and blunt liver injury: treatment with selective hepatic artery embolization. Injury 35:23–28 36. Sandblom P, Saegesser F, Mirovitch V (1984) Hepatic hemobilia: hemorrhage from the intrahepatic biliary tract, a review. World J Surg 8:41–50. doi:10.1007/BF01658362
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World J Surg 37. Dousset B, Sauvanet A, Barddou M, Legman P, Vilgrain V, Belghiti J (1997) Selective surgical indications for iatrogenic hemobilia. Surgery 121:37–41 38. Kaman L, Kumar S, Behera A, Katariya RN (1998) Pseudoaneurysm of the cystic artery: a rare cause of hemobilia. Am J Gastroenterol 93:1535–1537
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39. Lee SL, Caruso DM (1999) Acute cholecystitis secondary to hemobilia. J Laparoendosc Adv Surg Tech A 9:347–349 40. Hubens A, De Schepper A (1979) Hepatic artery aneurysm: a pitfall in biliary surgery. Br J Surg 66:259–261
Massive Hemobilia: A Diagnostic and Therapeutic Challenge Satish Devakumar Murugesan • Jeswanth Sathyanesan • Anand Lakshmanan • Sukumar Ramaswami • Senthilkumar Perumal • Srinivasan Ulagendra Perumal Ravi Ramasamy • Ravichandran Palaniappan
•
Ó Socie´te´ Internationale de Chirurgie 2013
Abstract Background Massive hemobilia is a rare but potentially life-threatening cause of upper gastrointestinal hemorrhage. In this retrospective analysis, we have evaluated the challenges involved in the diagnosis and management of massive hemobilia. Methods Between 2001 and 2011, a total of 20 consecutive patients (14 males) who were treated in our department for massive hemobilia were included in the study and their records were retrospectively analyzed. Results Causes of hemobilia were blunt liver trauma (n = 9), hepatobiliary intervention (n = 4), post-laparoscopic cholecystectomy hepatic artery pseudoaneurysm (n = 3), hepatobiliary tumors (n = 3), and vascular malformation
S. Devakumar Murugesan (&) J. Sathyanesan A. Lakshmanan S. Ramaswami S. Perumal S. Ulagendra Perumal R. Ramasamy R. Palaniappan Institute of Surgical Gastroenterology and Liver Transplantation, Government Stanley Medical College, Chennai 600001, India e-mail: [email protected] J. Sathyanesan e-mail: [email protected] A. Lakshmanan e-mail: [email protected] S. Ramaswami e-mail: [email protected] S. Perumal e-mail: [email protected] S. Ulagendra Perumal e-mail: [email protected] R. Ramasamy e-mail: [email protected] R. Palaniappan e-mail: [email protected]
(n = 1). Melena, abdominal pain, hematemesis, and jaundice were the leading symptoms. All patients had undergone upper GI endoscopy, abdominal ultrasound, and computerized tomography of the abdomen. An angiogram and therapeutic embolization were done in 12 patients and was successful in nine but failed in three, requiring surgery. Surgical procedures performed were right hepatectomy (n = 4), extended right hepatectomy (n = 1), segmentectomy (n = 1), extended cholecystectomy (n = 1), repair of the pseudoaneurysm (n = 3), and right hepatic artery ligation (n = 1). Conclusion The successful diagnosis of hemobilia depends on a high index of suspicion for patients with upper GI bleeding and biliary symptoms. Although transarterial embolization is the therapeutic option of choice for massive hemobilia, surgery has a definitive role in patients with hemodynamic instability, after failed embolization, and in patients requiring laparotomy for other reasons.
Introduction Hemorrhage into the biliary tract occurs when trauma or disease produces an abnormal communication between blood vessels and bile ducts, either within the liver or in the extrahepatic biliary tract. Based on clinical symptoms and severity, hemobilia is divided into massive hemobilia, which can be life-threatening and requires invasive treatment, and minor hemobilia, which is usually treated conservatively with blood transfusion. Massive hemobilia is a rare but potentially life-threatening condition that may be difficult to recognize, but it is, nonetheless, important to include it in the differential diagnosis of upper gastrointestinal (GI) bleeding. The diagnosis is not always easy to establish and often a long period elapses between the onset of the symptoms and identification of the source of the bleeding. Hemobilia is
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now being diagnosed with increasing frequency owing to widespread knowledge of the problem and improved diagnostic modalities [1]. In addition, there is an absolute increase in the frequency of massive hemobilia because of the increase in road traffic accidents and hepatobiliary intervention procedures. The objective of this retrospective study was to highlight the challenges involved in the diagnosis and management of massive hemobilia.
Materials and methods Twenty patients with massive hemobilia, treated at our institution between January 2001 and December 2011, were identified from a prospectively maintained database and registry. The demographic data, history, diagnostic features, including presenting symptoms, physical examination, investigations, and therapeutic modalities, were analyzed retrospectively. Initial treatment was directed at patient resuscitation and hemodynamic stabilization. Upper GI endoscopy, abdominal ultrasonography (USG), and contrast-enhanced computerized tomography (CECT) of the abdomen (CECT abdomen) were done in all patients after stabilization to identify the cause of bleeding. Angiography was done in selected patients to determine the source of bleeding. The algorithm used for the diagnosis and management of our patients with suspected hemobilia is depicted in Fig. 1. Definitive therapy was selected based on hemodynamic stability, overall performance status, underlying cause, and available expertise. Before 2006, all patients who presented with massive hemobilia underwent surgery after resuscitation. Due to the availability of the interventional radiology facility at our institution starting in November 2006, transarterial embolization (TAE) was used as a definitive therapy in patients with stable hemodynamics. Typically, the approach was through the right femoral artery using Seldinger’s method. The bleeding vessel was obliterated with gel foam or metallic coils. Surgery was performed in those with failed embolization, unstable hemodynamics, or resectable tumor. Depending on the cause of the hemobilia, hepatectomy, extended cholecystectomy, pseudoaneurysm repair, and hepatic artery ligation were performed. All patients, regardless of treatment, were monitored in the intensive care unit during the immediate post-treatment period. Postoperative complications and mortality were documented. Data were reported as the mean with range and percentage.
Results Of the 20 patients in our study group with massive hemobilia, 14 were males. The mean age of the group was
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34 years (range = 21–55 years). The most common presenting symptom was melena (n = 12), followed by abdominal pain, hematemesis, jaundice, and hypovolemic shock. Quincke’s triad of symptoms was present in 35 % of the cases. The mean transfusion requirement was 6 U (range = 3–12 U). Upper GI endoscopy revealed blood in the duodenum in only 12 patients (60 %). Abdominal ultrasound identified the source of bleeding in 15 patients (75 %). CECT abdomen demonstrated Grade III liver injury in 3 patients, Grade IV liver injury in 6 patients, pseudoaneurysm of hepatic artery (as seen in Fig. 2) in 5 patients, hepatocellular carcinoma in 1 patient, and gallbladder carcinoma in 1 patient. Conventional angiography was carried out in 12 patients, and it identified the source of bleeding in 11 patients (92 %). The most common cause for massive hemobilia in our series (Table 1) was blunt liver trauma, which was seen in 9 patients (45 %). Of these 9 patients, grade III and grade IV injuries were seen in 3 and 6 patients, respectively. There was no case of penetrating liver injury. The interventional procedures that caused hemobilia were percutaneous transhepatic biliary drainage for hilar cholangiocarcinoma (n = 1) and liver biopsy (n = 3). Indications for liver biopsy were post-necrotic cirrhosis (n = 1), cirrhosis of unknown origin (n = 1), and suspicion of hepatocellular carcinoma complicating alcoholic cirrhosis (n = 1). The time interval between liver puncture and clinical expression of hemobilia ranged from 1 to 28 days. Selective arterial embolization (Figs. 3 and 4) was attempted in all 12 patients who presented after November 2006 and was successful in 9 patients, as outlined in Table 2. The pre- and post-embolization films following superselective angiography with microcatheterization of the right hepatic artery pseudoaneurysm following laparoscopic cholecystectomy are shown in Figs. 5 and 6. The cause of failure of TAE in our series was due to not visualizing the source of the bleeding in one patient with blunt liver trauma. Two other patients had recurrent bleeding following TAE: one following gel-foam embolization and the other 15 days later from another part of the injured liver. Prior to the availability of interventional radiology expertise, eight patients underwent primary surgical intervention. After 2006, three patients (following failed embolization) required surgery. The procedures performed were right hepatectomy in four patients and hepatic artery pseudoaneurysm repair in three patients. Extended right hepatectomy, extended cholecystectomy, segmentectomy and right hepatic artery ligation were performed in one patient each. There were two deaths (10 %) in our series: one from sepsis and the other from liver failure. Six patients developed complications (30 %): two developed a bile leak that resolved spontaneously, three had a wound
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Fig. 1 Algorithm for the diagnosis and management of massive hemobilia
infection, and one developed a pulmonary complication (Table 3).
Discussion The phenomenon of bleeding into the biliary tree was first recorded in 1654 by Francis Glisson in his treatise, Anatomica Hepatis and a century later by Morgagni in 1765 [2–4]. The term ‘‘hemobilia’’ was first used by Sandblom in 1948 to describe a case of post-traumatic bleeding into the biliary tract [4]. Right hepatic artery ligation was first described by Kehr [4] in 1903 and angiographic embolization was first introduced by Walter [4] in 1976 for the treatment of hemobilia.
Classical clinical manifestation of hemobilia constitutes Quincke’s [4] triad of symptoms, consisting of abdominal pain (70 %), symptoms of bleeding from the upper digestive tract (melena in 90 % of cases and hematemesis in 60 %), and jaundice (60 %). However, the whole triad is present in only 22–30 % of patients with hemobilia [2]. In our series, melena was found in 60 %, abdominal pain in 40 %, hematemesis in 40 %, and jaundice in 35 % of cases. The triad of symptoms was present in 35 % of our patients. Hemorrhage is usually intermittent and repetitive and may be severe enough to cause hemodynamic instability due to the usual arterial origin of the bleeding. Thirty percent of patients presented with hemodynamic instability in our series. The onset of GI bleeding may occur within a few days after trauma or an interventional procedure, but
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Fig. 2 Computerized tomogram of abdomen showing large pseudoaneurysm with partial thrombus arising from hepatic artery Table 1 Etiology of hemobilia in various series
Fig. 4 Post coil embolization film showing effective obliteration of post-traumatic pseudoaneurysm in the anterior sectoral branch of the right hepatic artery
Etiology
Sandblom et al. [3]
Curet et al. [5]
Yoshida et al. [6]
Present series
Iatrogenic trauma
59 (17)
50 (58)
42 (41)
4 (20)
Accidental trauma
137 (38)
23 (27)
20 (19)
9 (45)
Table 2 Therapeutic interventions performed in 20 patients with massive hemobilia
Gallstones
53 (15)
–
9 (9)
3 (15)
No. cases
Inflammation
46 (13)
–
10 (10)
–
Vascular condition
38 (11)
–
15 (14)
1 (5)
Neoplastic disease Other
22 (6) –
– 13 (15)
7 (7) –
3 (15) –
Percentages in parentheses
Fig. 3 Superselective angiogram with microcatheter showing posttraumatic pseudoaneurysm in the anterior sectoral branch of the right hepatic artery
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Angioembolization
12 (60 %)
Successful
9 (75 %)
Failed
3 (25 %)
Surgery
11 (55 %)
Primary surgical intervention
8
Following failed TAE
3
more commonly it is delayed by weeks to months. The mean duration between trauma or the interventional procedure and onset of symptoms in our series was 9 days (range = 1–25 days). The etiology of bleeding into the biliary tract is diverse. Post-traumatic hemobilia is the most common etiological category, accounting for 55–85 % of cases in various series [3, 5, 6]. In the past, the most common cause of posttraumatic hemobilia was road traffic accidents (38 % in Sandblom’s series). Later, with the expanded use of interventional procedures, both diagnostic and therapeutic, iatrogenic hemobilia has become the most frequent etiological factor [5, 6]. Interestingly, in our series, post-traumatic hemobilia (45 %) was more common than iatrogenic hemobilia (20 %).This may be due to referral bias and the small cohort of patients in the present study. Iatrogenic hemobilia may occur during percutaneous liver procedures, liver or biliary surgery, or therapeutic
World J Surg Table 3 Outcomes after therapeutic interventions in 20 patients presented with massive hemobilia No. cases
Fig. 5 Selective hepatic angiogram demonstrating a right hepatic artery pseudoaneurysm following laparoscopic cholecystectomy
Fig. 6 Post-embolization film revealing effective obliteration of post laparoscopic cholecystectomy right hepatic artery pseudoaneurysm
anticoagulation. The frequency of clinical hemobilia is less than 1 % for liver biopsies [7, 8], 4 % for transhepatic cholangiography [9], and 3–14 % for percutaneous transhepatic catheter drainage [10, 11]. In our series, iatrogenic hemobilia occurred from liver biopsy (75 %) and percutaneous transhepatic biliary drainage (25 %). The other causes of hemobilia in our series were similar to those of other reported series, as summarized in Table 1. In gallstone-related hemobilia, hemorrhage may result from direct
Mortality
2 (10 %)
Sepsis
1
Liver failure
1
Morbidity
6 (30 %)
Bile leak
2
Wound infection
3
Pneumonitis
1
mucosal erosion, from hemorrhagic necrosis complicating severe cholecystitis, or cholangitis [12, 13]. An acalculous inflammatory condition of the biliary tract that causes hemobilia is most commonly due to ascariasis, followed by hepatic abscess, acalculous cholecystitis, cholangitis, hepatitis, pancreatitis, and chemical inflammation or erosion due to heterotopic gastric mucosa [14–17]. There were no cases of hemobilia due to inflammation in our series. Primary vascular causes of hemobilia include aneurysmal disease of the hepatic artery or portal vein, vasculitis, and portal hypertension. Lastly, hepatocellular carcinoma is the main neoplastic disease that causes hemobilia, with other neoplastic causes being hemangioma, cholangiocarcinoma, gallbladder carcinoma, and adenocarcinoma of the pancreas [6, 18, 19]. We had two patients with hepatocellular carcinoma and one patient with gallbladder carcinoma that caused hemobilia. Hemobilia is difficult to diagnose because the bleeding is usually intermittent. In patients with suspected hemobilia, the initial investigation is upper GI endoscopy, which may directly reveal blood flowing out of the papilla of Vater or indirectly by the presence of fresh blood in second part of the duodenum without an active bleeding site. Upper GI endoscopy may also rule out other common causes of bleeding such as erosive gastritis, peptic ulcers, and esophageal and gastric varices. In the present series, upper GI endoscopy was performed in all patients; it revealed fresh blood oozing from the papilla in 6 patients (30 %). Diagnosis was indirectly suggested in another 6 patients (30 %). The remaining 8 patients (40 %) had normal endoscopic findings. USG also may be helpful in the diagnosis of hemobilia, but it is nonspecific. Partial or total biliary obstruction can cause dilatation of the proximal segment of the biliary tract [20]. Blood clots are usually hyperechoic or isoechoic, assuming the shape of the bile duct and rendering them invisible. Echogenicity of clots decreases with time and with thrombus organization. Hypoechogenic clots can easily be missed during an ultrasound examination. Visualization of clots in the gallbladder is much easier and a newly formed thrombus in the
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gallbladder is usually hyperechogenic without acoustic shadow and does not change with position. Thrombus attached to the gallbladder wall may be misinterpreted as a polyp, bile sludge, neoplasm, or gangrenous cholecystitis. Adding Doppler ultrasound can be very useful to detect an aneurysm or a pseudoaneurysm of the hepatic artery [21– 23]. Abdominal USG was done in all patients, with positive findings in 15 patients (75 %). It is used mainly in blunt liver trauma for the detection of hepatic parenchymal injuries and hemoperitoneum. The sensitivity of ultrasound varies widely between 41 % [24] and 90 % [25], depending on the sonographer’s experience, the severity of the injury, the criteria used for determining the presence of liver injury, and when the ultrasound was performed relative to the timing of the injury [26, 27]. CECT abdomen is currently the diagnostic modality of choice for the evaluation of blunt liver trauma in hemodynamically stable patients [28]. The major CT features of blunt liver trauma are lacerations, subcapsular and parenchymal hematomas, active hemorrhage, and juxtahepatic venous injuries. Minor CT features include periportal low attenuation and a flat inferior vena cava (IVC). CECT abdomen revealed diffuse parenchymal injury resulting in large cavity-like lesions in seven patients and linear lacerations with an adjacent pseudoaneurysm in two patients. CECT abdomen can show focal change in the liver, the extent of hepatic injury or tumor, bile duct dilation, and blood clots [21]. CECT abdomen may also show simultaneous opacification of an aneurysmal artery in the arterial phase. Again, these findings are only suggestive of the diagnosis. Angiography made the correct diagnosis in more than 90 % of reported series [21]. Angiography delineates the arterial anatomy and the site of the pseudoaneurysm for therapeutic intervention. It can also show the presence of arteriobiliary fistula and vascular malformations like aneurysms, pseudoaneurysms, and hemangiomas. False-negative studies may occur if there is no active bleeding [29]. The advantage of angiography is that therapeutic embolization can be done immediately after identification of the bleeding vessel or pseudoaneurysm. In the present study, angiography was able to establish the diagnosis in 11 of 12 patients (97 %). Anecdotal reports indicate that technetium-labeled erythrocyte scans and the presence of fecal occult blood occasionally support or suggest the diagnosis, but a reliance on these tests for diagnosis cannot be justified [30]. Massive hemobilia can be diagnosed on clinical, endoscopic, and radiological findings, but a definitive diagnosis can be established only with angiography. In about 40 % of our cases, treatment for hemobilia was instituted based on clinical findings of upper GI bleeding and radiological findings. Overall, the diagnosis of hemobilia requires a high index of suspicion in patients with biliary symptoms and GI bleeding.
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The goals of therapy in massive hemobilia are (1) to stop the bleeding and (2) to restore bile flow. Patients with massive hemobilia usually present with hypovolemic shock and require resuscitation and hemodynamic stabilization. The management of hemobilia depends on the clinical state of patient, the rate of blood loss, the underlying cause of the hemobilia, and available expertise. Some studies have reported a conservative approach to the management of hemobilia [2, 31]. In a study by Green et al. [2], 43 % of patients with hemobilia were treated conservatively, embolization was performed in 36 %, and surgery was done in 20 % of the cases. The therapeutic options in massive hemobilia are angiographic embolization and surgery. Once hemodynamic stability is achieved, interventional radiographic methods are used for initial treatment and good results are achieved in 75–100 % of cases. We achieved a 75 % success rate in our series. Coil embolization not only provokes a thrombus in the aneurysm but may also obliterate the artery. The important prerequisite before TAE is to ensure the patency of the portal vein to avoid procedure-related liver necrosis and liver failure (6 %). Other less serious complications such as abscess formation (9 %), bleeding (6 %), and gallbladder fibrosis (2 %) have been reported following TAE [13, 32, 33]. Like Moodley et al. [34] and Forlee et al. [35], we did not encounter any procedure-related complications, but we had three failed embolization cases. The reasons for the failed embolizations were inability to isolate the bleeding vessel, incomplete arterial occlusion, or misidentification of the bleeding vessel. Surgical treatment is indicated for patients with hemodynamic instability, failed angioembolization, and for cases requiring laparotomy for liver trauma [36], resectable neoplasm, and hemorrhagic cholecystitis [3, 37–39]. Selective ligation of the bleeding vessel or aneurysm resection is a surgical maneuver that may be useful in some cases [13]. When the bleeding vessel cannot be identified, nonselective ligation of the right or left hepatic artery may be performed [3]. If bleeding continues from collateral vessels, even after ligation of the hepatic artery, resection of the affected liver segment may be required [40]. Hemorrhage from the gallbladder and hemorrhagic cholecystitis require urgent cholecystectomy [3, 37–39]. Surgical management of massive hemobilia in the present series achieved an overall success rate of 90 %, with rebleeding rates of less than 5 % and a mortality rate of 10 %.
Conclusions Upper GI bleeding in a patient with a history of trauma or hepatobiliary intervention and biliary symptoms should arouse suspicion for hemobilia. The successful diagnosis of
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hemobilia depends on a high index of suspicion, especially when the common causes of hemorrhaging in the upper GI tract have been excluded. A clinical suspicion of hemobilia should prompt confirmation of the diagnosis with endoscopy, ultrasound with Doppler, and/or computed tomography. Angiography is needed if the diagnosis is in doubt or other investigations are not contributory. Initial treatment involves patient resuscitation and hemodynamic stabilization. Careful consideration of the etiology, hemodynamic status, results of imaging, and available expertise will help to define the therapeutic options. Although TAE is the therapeutic option of choice in massive hemobilia, surgery has a definitive role in patients with hemodynamic instability, after failed angioembolization and in patients requiring laparotomy for other reasons.
Conflict of interest No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.
References 1. Blumgart LH (2007) Hemobilia and bilhemia. In: Blumgart LH (ed) Surgery of the liver, biliary tract, and pancreas, 4th edn. Elsevier, Philadelphia, pp 1067–1081 2. Green MH, Duell RM, Johnson CD, Jamieson NV (2001) Hemobilia. Br J Surg 88:773786 3. Sandblom P (1948) Hemorrhage into the biliary tract following trauma: ‘traumatic hemobilia’. Surgery 24:571–586 4. Merrell SW, Schneider PD (1991) Hemobilia: evolution of current diagnosis and treatment. West J Med 155:621–625 5. Curet P, Baumer R, Roche A, Grellet J, Mercadier M (1984) Hepatic hemobilia of traumatic or iatrogenic origin: recent advances in diagnosis and therapy, review of the literature from 1976 to 1981. World J Surg 8:2–8. doi:10.1007/BF01658356 6. Yoshida J, Donahue PE, Nyhus LM (1987) Hemobilia: review of recent experience with a worldwide problem. Am J Gastroenterol 82:448–453 7. Levinson JD, Olsen G, Terman JW (1972) Hemobilia secondary to percutaneous liver biopsy. Arch Intern Med 130:396–400 8. Lee SP, Tasman-Jones C, Wattie WJ (1977) Traumatic hemobilia: a complication of percutaneous liver biopsy. Gastroenterology 72:941–944 9. Cahow CE, Burrell M, Greco R (1977) Hemobilia following percutaneous transhepatic cholangiography. Ann Surg 185:235–241 10. Monden M, Okamura J, Kobayashi N et al (1980) Hemobilia after percutaneous transhepatic biliary drainage. Arch Surg 115:161– 164 11. Sarr MG, Kaufman SL, Zuidema GD, Cameron JL (1984) Management of hemobilia associated with transhepatic internal biliary drainage catheters. Surgery 95:603–607 12. Sandblom P, Mirkovitch V (1979) Minor hemobilia. Clinical significance and patho-physiological background. Ann Surg 190:254–264 13. Czemiak A, Thompson JN, Hemingway AP et al (1988) Hemobilia: a disease in evolution. Arch Surg 123:718–721
14. Blumenthal DS (1988) Ascariasis. In: Wyngaarden JB, Smith LH (eds) Cecil Textbook of Medicine, 18th edn. WB Saunders, Philadelphia, p 1908 15. Koshy A, Khuroo MS, Suri S, Datta DV, Khanna SK (1979) Amoebic liver abscess with hemobilia. Am J Surg 138:453–455 16. Wagner DS, Flynn MA (1985) Hemorrhagic acalculous cholecystitis causing acute pancreatitis after trauma. J Trauma 25:253–256 17. Adam R, Fabiani B, Bismuth H (1989) Hematobilia resulting from heterotopic stomach in the gallbladder neck. Surgery 105:564–569 18. Wright RC, Roberts JW (1988) Fibro lamellar carcinoma of the liver presenting with hemobilia. Contemp Surg 33:29–35 19. Hasan S, Quintana J, Siddiqui Y, Maldonado V (1986) Carcinoma of the pancreas presenting with hemobilia (Letter). Gastrointest Endosc 32:305–306 20. Laing FC, Frates MC, Feldstein VA, Goldstein RB, Mondro S (1997) Hemobilia: sonographic appearances in the gallbladder and biliary tree with emphasis on intracholecystic blood. J Ultrasound Med 16:537–543 21. Walter JF, Passo BT, Cannon WB (1976) Successful trans-catheter embolic control of massive hemobilia secondary to liver biopsy. AJR Am J Roentgenol 127:847–849 22. Greenberg M, Rubin JM, Crass JR (1983) The ultrasound appearance of an arteriobiliary fistula. J Clin Ultrasound 11:323–325 23. Grant EG, Smimiotopoulos JG (1983) Intraluminal gall bladder hematoma: sonographic evidence of hemobilia. J Clin Ultrasound 1:507–509 24. Poletti PA, Kinkel K, Vermeulen B et al (2003) Blunt abdominal trauma: should US be used to detect both free fluid and organ injuries? Radiology 227:95–103 25. Yoshii H, Sato M, Yamamoto S et al (1998) Usefulness and limitations of ultrasonography in the initial evaluation of blunt abdominal trauma. J Trauma 45:45–50 discussion 50–51 26. Kendall JL, Faragher J, Hewitt GJ, Burcham G, Haukoos JS (2009) Emergency department ultrasound is not a sensitive detector of solid organ injury. West J Emerg Med 10:1–5 27. Richards JR, McGahan JP, Pail MJ et al (1999) Sonographic detection of blunt hepatic trauma: hemoperitoneum and parenchymal injury patterns of injury. J Trauma 47:1092–1097 28. Yoon W, Jeong YY, Kim JK, Seo JJ, Lim HS, Shin SS et al (2005) CT in blunt liver trauma. Radiographics 25:87–104 29. Sharipo MJ (1994) The role of the radiologist in the management of gastrointestinal bleeding. Gastroenterol Clin North Am 23:123–131 30. Lee SM, Lee RGL, Clouse ME, Hill TC (1986) Demonstration of hemobilia using technetium-99m labeled red blood cells. Clin Nucl Med 11:52 31. Hsu KL, Ko SF, Chou FF, Sheen-Chen SM, Lee TY (2002) Massive hemobilia. Hepatogastroenterology 40:306–310 32. Franklin RH, Bloom WF, Schoffstall RO (1980) Angiographic embolization as the definitive treatment of post-traumatic hemobilia. J Trauma 20:702–705 33. Wagner WH, Lundell CJ, Donovan AJ (1985) Percutaneous angiographic embolization for hepatic arterial hemorrhage. Arch Surg 120:1241–1249 34. Moodley J, Sing B, Lallo S, Pershad S, Robbs JV (2001) Nonoperative management of hemobilia. Br J Surg 88:1073–1076 35. Forlee MV, Krige JE, Welman CJ, Beningfield SJ (2004) Hemobilia after penetrating and blunt liver injury: treatment with selective hepatic artery embolization. Injury 35:23–28 36. Sandblom P, Saegesser F, Mirovitch V (1984) Hepatic hemobilia: hemorrhage from the intrahepatic biliary tract, a review. World J Surg 8:41–50. doi:10.1007/BF01658362
123
World J Surg 37. Dousset B, Sauvanet A, Barddou M, Legman P, Vilgrain V, Belghiti J (1997) Selective surgical indications for iatrogenic hemobilia. Surgery 121:37–41 38. Kaman L, Kumar S, Behera A, Katariya RN (1998) Pseudoaneurysm of the cystic artery: a rare cause of hemobilia. Am J Gastroenterol 93:1535–1537
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39. Lee SL, Caruso DM (1999) Acute cholecystitis secondary to hemobilia. J Laparoendosc Adv Surg Tech A 9:347–349 40. Hubens A, De Schepper A (1979) Hepatic artery aneurysm: a pitfall in biliary surgery. Br J Surg 66:259–261
