The Internal Biliary Reappraisal Incidence, Type

HPB Surgery, 1997, Vol.10, pp.143-147Reprints available directly from the publisherPhotocopying permitted by license only

(C) 1997 OPA (Overseas Publishers Association)Amsterdam B.V. Published in The Netherlands

by Harwood Academic PublishersPrinted in India

The Internal Biliary Fistula- Reappraisalof Incidence, Type, Diagnosis and

Management of 33 Consecutive CasesHIROYUKI YAMASHITA, KAZUO CHIJIIWA, YOSHIAKI OGAWA, SYOJI KUROKI

and MASAO TANAKA

Department of Surgery I, Kyushu University Faculty of Medicine, Fukuoka, Japan

(Received20 June 1994)

To reevaluate the current features of spontaneous internal biliary fistulas, we reviewed 1,929 consecutivepatients who had been treated for biliary tract diseases during the recent 12-year period. Thirty-threepatients had internal biliaryfistulas and the incidence was 1.9%. Of33 patients, 20 were women and 13 weremen with the average age 63 years, and their mean duration ofillness was 4 years. A total of 37 fistulas werefound and the most common type was choledochoduodenal (62%), followed by cholecystoduodenal (19%),cholecystocholedochal (11%) and cholecystocolonic (8%) fistulas. Internal biliary fistulas of thirty-onepatients were caused by biliary stones and those of two patients by malignant tumors. All of the 17 bilesamples examined were bacteria positive and the majority of calculi were brown pigment stones. All of thecholedochoduodenal fistulas were correctly diagnosed by endoscopic retrograde cholangiography. In 14patients with cholecystoenteric or cholecystocholedochal fistulas, direct evidence of the internal fistula wasobtained only in 7 patients(50%) preoperatively. Pneumobilia, a small atrophic gallbladder adherent to theneighboring organs and a history of spontaneous disappearance of jaundice in elderly patients mayindicate the presence ofa cholecystoentric fistula. Since the preoperative diagnostic rate for internal biliaryfistula involving the gallbladder is still low, care is necessary before and at the time of surgery especiallyduring laparoscopic cholecystectomy for elderly patients with cholelithiasis.

KEY WORDS: Internal biliary fistula cholelithiasisendoscopicretrogradecholangiographylaparoscopic cholecystectomy

INTRODUCTION

Although traditional open cholecystectomy and re-cently developed laparoscopic cholecystectomy showvery low mortality and morbidity rates1’ 2, the presenceof spontaneous internal biliary fistulae is reported toincrease the morbidity rate considerably and its poten-tial lethality has been appreciated3-5. The reported inci-dence of internal biliary fistulas is about 2% of totalbiliary diseases and the most common type has beenreported to be a cholecystoduodenal fistula, followed

All correspondence and reprints requests should be addressed to:Hiroyuki Yamshita, M.D. Department of Surgery I, KyushuUniversity Faculty of Medicine 3-1-1 Maidashi, Higashi-ku,Fukuoka 812-82, Japan. Tel: 81-92-641-1151 Ext. 2394, Fax: 81-92-632-2478.

by cholecystocolonic and cholecystogastric fistulas3’4.Their clinical importance as well as the managementdepends on the etiology and type of the fistulas. Thetreatment option can be selected only when such infor-mation is available. Although it is sometimes difficult todiagnose correctly the type of internal biliary fistulapreoperatively, surgeons must be aware of the possiblepresence of an internal biliary fistula before surgicalintervention. This might be particularly true when con-sidering laparoscopic cholecystectomy.The recent advances in hepatobiliary imaging tech-

niques have allowed us to reevaluate hepatobiliarydiseases. With the aid of endoscopic retrogradecholangiography, choledochoduodenal fistulas in theperiampullary region have been found more frequentlythan ever7-9. Despite the improvement in imagingmodalities, little literature is currently available about

143

144 H. YAMASHITA et al.

internal biliary fistula. In the present study, we thereforeanalyzed. 1,929 consecutive patients with biliary diseaseto evaluate the diagnostic methods, etiology, types andmanagements of internal biliary fistula.

PATIENTS AND METHODS

During the 12-year period, from January, 1982through December, 1993, 1,929 patients were treatedfor diseases of the biliary tract at the first Departmentof Surgery, Kyushu University Faculty of Medicine.Intravenous cholangiography and endoscopic retro-grade cholangiography were carried out for the evalu-ation of the biliary tract diseases. Percutaneoustranshepatic cholangiography and subsequent biliarydrainage were performed in patients with obstructivejaundice caused by stone impaction to common bileduct, or obstruction with carcinoma. Ultrasound, com-puted tomography scan (CT) and upper gastro-intestinal examination were employed in most of thepatients. Barium enema was given only when a biliaryenteric fistula or colon cancer was considered. Endo-scopic retrograde cholangiographic techniques havebeen generally used in our department, and the diag-nosis of internal biliaryfistulas with the techniquehasbeen described in detail7’. Internal biliary fistulaswere found in 33 patients of the 1929 consecutivecases. The type of the fistula was determined by thecombined use of the above imaging modalities andby operative findings if any.

RESULTS

Incidence and Patient Characteristics

The incidence of internal biliary fistulas was1.7%. Of 33 patients, 20 were women and 13 weremenwith a female/male ratio of 1.5. The mean age was 63years, ranging from 42 to 83; more than 60 % of thepatients were over 60 years old. Internal biliaryfistulas were caused by biliary calculi in 31 patients(94%) and by malignant tumors (bile duct cancer,carcinoma of the Papilla of Vater) in two patients(6%). The clinical features of the patients with biliaryfistulas are shown in Table I. Thirty-seven fistulas werefound in 33 patients and the most common typefistulawas choledochoduodenal (62%), followed by chole-cysto-duodenal (19%), cholecystocholedochal (11%)and cholecystocolonic (8%). Ninety percent of thecholedochoduodenal fistulas were found in the peri-ampullary region. Three patients (9%) had multiple

fistulas. Of three patients, one had choledo-choduodenal, cholecystoduodenal and cholecysto-colonic fistulas. The remaining two patients had acholedochoduodenal and cholecystoduodenal fistulas.The average duration ofillness prior to diagnosis was 4years, ranging from month to 23 years. Upper ab-dominal pain, fever and jaundice were the mainsymptoms. Twenty-nine percent ofthe patients with acholecystoenteric fistula had frequent diarrhea. Sixpatients (18%) presented a history of sudden disap-pearance ofjaundice. Associated diseases were foundin 15 patients (45%), ofwhom 7 had diabetes mellitus,6 patients had hypertension and liver cirrhosis inone patient. Peptic ulcer disease was found in twopatients. Thirteen patients had undergone varioustypes of previous biliary operations, of whom9 had cholecystectomy with (5 patients) or without(4 patients) choledocholithotomy, two had under-gone cholecystectomy, choledocholithotomy andsphincteroplasty and the remaining two had choledo-cholithotomy and choledochalcystojejunostomy.

Diagnosis

Diagnosis of the internal biliary fistula was made bythe combined use of various imaging methods (Tab.II). The choledochoduodenal fistulas including acholedochalcystoduodenal fistula were all correctlydiagnosed in 23 patients by endoscopic retrogradecholangiography. Of 14 patients with cholecystoen-teric (cholecystoduodenal and cholecystocolonic) orcholecystocholedochal fistulas, the preoperative correctdiagnosis was made correctly only in 7 patients (50%).CT scans demonstrated the presence of pneumobiliain 10 of 19 patients examined, and an atrophic gallbladderadherent to neighboring organs was observed in all ofthe patients with cholecystoentric fistulas.

Management

There was a wide variety of treatments in the pre-sent series (Tab. III). The choice of the treatmentwas established on the basis of the type, etiology, andseverity of the disease and general condition. Of 23patients with choledochoduodenalfistulas, 8 underwentsurgery alone or surgery plus endoscopic papillotomywith subsequent removal of the common bile ductstones. Endoscopic papillotomy including fistulotomywas adopted in the remaining 12 patients and commonbile duct stones were removed endoscopically. All thepatients with cholecystoenteric or cholecystochole-dochal fistulas underwent cholecystectomy and

INTERNAL BILIARY FISTULA 145

TABLE Clinical features of internal biliary fistulas

Type of fistula No. Age Sex Symptom(Mean: Years) (F/M) (No. of patients: percentage)

Duration of illnes(Mean: years)

Choledochoduodenal* 23(3)** 64.1 1.9 Pain (16: 70%) Fever (9: 39%)Jaundice (8: 36%)

Cholecystoenteric*** 10(3) 64.2 1.5 Pain (6: 60%) Fever (5: 50%)Jaundice (2: 20%) Diarrhea (2: 29%)

Cholecystocholedochal 4(1) 63.5 3.0 Pain (4: 100%) Fever (2: 50%)Jaundice (3: 75%)

*Including one case with choledochalcystoduodenal fistula.**Number in parentheses represents number of patients with multiple fistulas.

***Cholecystoenteric fistula includes cholecystoduodenal (7 patients) and cholecystocolonic (3 patients) fistulas.

4.1

3.3

3.7

repair of the fistula with or without choledocholi-thotomy, but one patient had only exploratory lapa-rotomy because of poor orientation of the biliarysystem due to severe adhesions. Pancreatoduo-denectomy was adopted for one patient who had acholedochoduodenal fistula caused by carcinoma ofthe Papilla of Vater. Wound infection (3 patients)was the most common postoperative early complica-tion. Bile leakage from the site of T-tube choledochaldrainage (2 patients) and enteritis by methicillin re-sistant staphylococcus aureus (1 patient) were alsoobserved. There was no operative death in 33 patientstreated.

Bile Culture and Classification ofStonesAll of the bile samples obtained from the gallbladder(2 samples) or common bile duct (15 samples) eitherat the time of surgery or endoscopic treatment hadbacterial positive cultures. The most common organ-ism was Klebsiella in combination with Escherichiacoli. All patients with choledochoduodenal fistulashad gallstones in the gallbladder. Five of 11 patientswith cholecystoenteric or cholecystocholedochal fis-tulas had gallstones in the gallbladder, but the re-maining 6 patients (55%) had gallstones only in thecommon bile duct (Tab. IV). Biliary stones were re-moved in 18 patients either surgically or endo-

scopically. Fifteen patients had brown pigmentstones and 3 had cholesterol stones (Tab. IV). Biliarystones could not be found in the remaining 13 patientsbecause they disappeared either after fistula forma-tion or after endoscopic papillotomy.

DISCUSSION

Spontaneous internal biliary fistulas are formed bet-ween the extrahepatic biliary tract and a variety ofadjacent organs. The incidence is reported to be0.9-3.2% of patients with biliary diseases and themost common type is cholecystoenteric, includingcholecystoduodenal (77%), cholecystocolonic (15%)and cholecystogastric (2%) fistulas3’4. In our series,the incidence was 1.9% and the most common typewas choledochoduodenal, followed by cholecys-toduodenal, cholecystocholedochal and cholecysto-colonic fistulas. The difference in the incidences ofa given type of internal fistula may be explained bythe fact that choledochoduodenal fistulas have beenfound more frequently because of the recent develop-ment of endoscopic retrograde cholangiography8. Theclinical features in our study were elderly female, witha long duration of illness and past history of a rapidrelief from jaundice, which agrees with previous

TABLE II Imaging modalities and their accuracy for the diagnosis of internal biliary fistulas

Type of fistula Number Imaging modalities Barium meal Barium enemaIVC* ERC**

Choledochoduodenal 23 0/9*** 23/23 (100%) 9/17 (53%)Cholecystoenteric 10 0/7 5/8 (63%) 4/7 (57%) 2/2 (100%)Cholecystocholedochal 4 0/3 1/4 (25%) 1/4 (25%)

*Intravenous cholangiography.**Endoscopic retrograde cholangiography.***Number of patients diagnosed correctly/number of patients examined.

146 H. YAMASHITA et al.

TABLE III Management of internal biliary fistulas

Type of fistula Surgery Surgery plus EPT** EPT Others

Choledochoduodenal (23)*

Cholecystoentric (10)

Cholecystocholedochal (4)

Cholecystectomy andcholedocholithotomy (2)

Choledochalcysto-jejunostomyand gastrojejunostomy (1)

Cholecystectomy andrepair of fistula (3)

Cholecystectomy,choledocholithotomyrepair of fistula (3)

Cholecystectomy,choledocholithotomyand repair of fistula (3)

Cholecystectomy and EPT and PTC ***(1)choledocholithotomy (1) stone removal (12)

Cholecystectomyand repair of fistula (2)

Choledocholithotomy (1)Pancreatoduodenectomy (1)Cholecystectomy andrepair of fistula (3)

Exploratory laparotomy (1)

Cholecystectomyand repair of fistula (1)

EPT andPTC (1)

Conserva-tive (1)

*Number in parentheses represents number of patients.**Endoscopic papillotomy (EPT).

***Percutaneous transhepatic cholangiodrainage (PTC).

reports3’4. The symptoms were similar to those ofcholelithiasis.

Internal biliary fistulas usually occur as a result ofpressure necrosis caused by calculi in the inflamedgallbladder or biliary tract3’4. The fistulas were alsoreported to be formed by peptic ulcer5, malignanttumor1, trauma11 and Crohn’s disease12. Choledocho-duodenal fistulas were reported to be caused mainly bypeptic ulcer5. However, this seems unlikely for those inthe periampullary region, because most of theperiampullary choledochoduodenal fistulas were pro-duced by a spontaneous migration of a common bileduct stone into the duodenum8. Hunt et al. 13 reportedthat choledochoduodenal fistulas in the periampullaryregion were iatrogenic caused by passage of a rigidcholedochal bougie during common duct exploration.Although this possibility could not be excluded, itseems to have less etiological significance because only8 of23 patients with this type offistula had a history of

common bile duct exploration. It should be noted thatall of the bile samples obtained from the biliary tracthad positive cultures and that the majority of biliarycalculi were brown pigment stones. These conditionsmay have predisposed to the formation of the biliaryfistula, because bacterial infection and biliary stasisplay a major role in the formation ofthis type ofstone 14.In our series, there was no patient with a choledoc-hoduodenal fistula caused by a peptic ulcer. This canpresumably be ascribed to be the recent therapeutic im-provement for peptic ulcers with H2 receptor antagonist.

In the present study, fifteen of 33 patients (44%)presented with pneumobilia. The diagnosis could bemade by direct cholangiography, barium meal or ba-rium enema. Intravenous cholangiography was notuseful because ofnonvisualization ofthe gallbladder inall cases with cholecystoenteric fistulas. Endoscopicretrograde cholangiography was the most valuablediagnostic method and revealed the presence of all

TABLE IV Distribution and classification of gallstones

Type of fistula No. Distribution of gallstonesGB* CBD** GB

and CBD

Classification of removed gallstonesBrown pigments Cholesterolstone stone

Choledochoduodenal 12(2)*** 0 9 3Cholecystoenteric 7(2) 2 5 0Cholecystocholedochal 4 2

116

3

*Stones in the gallbladder (GB).**Stones in the common bile duct (CBD).***Number in parentheses represents number of patients with multiple fistulas.

INTERNAL BILIARY FISTULA 147

choledochoduodenal fistulas. Only half of cholecy-stoenteric and cholecystocholedochal fistulas could bevisualized due to the obstruction of the cystic duct bygallstones. There were three patients who were ini-tially diagnosed to have Mirizzi syndrome. An incar-cerated stone responsible for the cholecystocholedochalfistula was found in the infundibulum of the gallbladderat the time of surgery. In such cases endoscopic retro-grade cholangiography could not demonstrate the fis-tula, because the impacted stone was so large that thefistula was occluded by the stone. Barium meal exami-nation could demonstrate the communication be-tween the duodenum and biliary tract only when thefistula was relatively large; however, deformity of theduodenal bulb was observed retrospectively in mostcases with cholecystoduodenal fistulas. Although ultra-sound and CT examinations were not diagnostic, thepresence of the internal biliary fistula was suggested insome cases by the findings ofpneumobilia, an atrophicgallbladder and biliary stones.Management may depend on the type and etiology

of the internal biliary fistula. Cholecystectomy, re-moval of common bile duct stones, if present, andrepair of the fistula are the best choice in patients withcholecystoenteric fistulas. In contrast, the preferredtherapy for the periampullary choledochoduodenalfistula is endoscopic papillotomy including fistulo-tomy in combination with bile duct stone extraction 8,9.Cholecystectomy may be mandatory if the patientsalso have gallbladder disease. In general, laparoscopiccholecystectomy should not be used in the patientswith cholecystoenteric or cholecystocholedochalfistu-las, although Velez et al. 15. have recently reported acase of a cholecystoduodenal fistula which was suc-cessfully repaired laparoscopically.Our recent experience in the treatment of internal

fistulas showed a high prevalence of choledochoduo-denalfistulas in the periampullary region, which could beconfirmed and managed endoscopically. Proper man-agement of the internal fistula can be achieved with theinformation of its type and etiology, therefore surgeons

should be aware of its possible presence for adoptingappropriate imaging modality before surgical interven-tion. Pneumobilia, a small atrophic gallbladder and ahistory of disappearance ofjaundice in elderly patientsmay suggest the presence of an internal biliary fistula.

REFERENCES

1. Roslyn, J.J., Binns, G.S., and Hughes, E.F.X. (1993) Opencholecystectomy A contemporary analysis of 42,474 patients.Ann. Surg., 218, 129-137.

2. NIH consensus development panel of gallstones and laparo-scopic cholecystectomy (1993) Gallstones and laparoscopiccholecystectomy. J.A.M.A. 269, 1018-1024.

3. Glenn, F., Reed, C. and Grafe, W. (1981). Biliary entericfistula. Surg. Gyneeol. Obstet., 153, 527-531.

4. Zwemer, F., Coffin-Kwart, V.E., and Conway, M. (1979)Biliary enteric fistulas: management of 47 cases in NativeAmericans. Am. J. Surg., 138, 301-304.

5. Feller, E.R., Warshaw, A.L., and Schapiro, R.H. (1980) Obser-vations on management of choledochoduodenal fistula due topenetrating peptic ulcer. Gastroenterology, 78, 126-131.

6. Chijiiwa, K., Sumiyoshi, K., and Nakayama, F. (1991) Impactof recent advance in hepatobiliary imaging techniques on thepreoperative diagnosis of carcinoma of the gallbladder. WormJ. Surg., 15, 322-327.

7. Ikeda, S., and Okada, Y. (1975) Classification of choledo-choduodenal fistula diagnosed by duodenal fiberscopy and itsetiological significance. Gastroenterology, 69, 130-137.

8. Tanaka, M., and Ikeda, S. (1983) Periampullary chole-dochoduodenal fistula: an analysis of 83 consecutive patientsdiagnosed at ERCP. Gastroenterol. Endosc., 29, 89-93.

9. Urakami, Y., and Kishi, S. (1978) Endoscopic fistulotomy(EFT) for papillary choledochoduodenal fistula. 10, 289-294.

10. Tanga, R.M., and Ewing, J.B. (1970) Primary malignanttumorsof the gallbladder-report of 43 cases. Surgery, 67, 418-426.

11. Griffith, C.D.M., Saunders, J.H. (1982) Cholecysto duo-denocolic fistula following abdominal trauma. Br. J. Surg., 69,99-100.

12. Porter, J.M., Mullen, D.C., and Silver, D. (1970) Spontaneousbiliary-enteric fistulae. Surgery, 68, 597-601.

13. Hunt, D.R., and Blumgart, L.H. (1980) Iatrogenic choledo-choduodenal fistula: and unsuspected cause of post-chole-cystectomy symptoms. Br. J. Surg., 67, 10-13.

14. Nakano, T., Tabata, M. and Nakayama, F. (1988) Uncon-jugated bilirubin in hepatic bile with brown pigment gall-stones and cholangitis. Dig. Dis. Sci., 33, 1121-1126.

15. Velez, M., Mule, J., Brandon, J. and Kannegieter. (1991)Laparoscopic repair of a cholecystoduodenal fistula. Surg.Endose., 5, 221-223.

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The Internal Biliary Reappraisal Incidence, Type