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Cirugía y cirujanos

versión On-line ISSN 2444-054Xversión impresa ISSN 0009-7411

Cir. cir. vol.89 no.1 Ciudad de México ene./feb. 2021  Epub 08-Nov-2021

https://doi.org/10.24875/ciru.20000055 

Original articles

Endoscopic retrograde cholangiopancreatography for treatment biliopleural fistulas

Uso de colangiopancreatografía retrógrada endoscópica en pacientes con fístula biliopleural

Edson R. Marcos-Ramírez1  * 

Alejandra Téllez-Aguilera1 

Martín A. Ramírez-Morín1 

María I. Treviño-Martínez1 

Francisco Vásquez-Fernández1 

Marco A. Hernández-Guedea1 

Gerardo Muñóz-Maldonado1 

1Service of General Surgery, Hospital Universitario "Dr. José Eleuterio González", Universidad Autónoma de Nuevo León, Monterrey, Nuevo León, Mexico


ABSTRACT

Background:

Biliopleural fistula is a rare communication between the biliary system and the pleural space secondary to ruptured hydatid cysts, hepatobiliary surgeries or penetrating wounds. There is not so much of the subject in the literature, so there is no standardized protocol for its management.

Objective:

The objective of this work is to determine advantages and disadvantages of the use of ERCP as a conservative initial treatment for biliopleural fistulas.

Method:

Our retrospective study included patients with a diagnosis of biliopleural fistula who underwent ERCP as initial treatment, older than 18 years in a period from August 2016 to August 2019.

Results:

Eight patients with a diagnosis of biliopleural fistula were included, 75% men and 25% women with a mean age of 24.5 years; the traumatic etiology was predominant in our group (89%), the diagnosis was made between days 3 and 14 after chest tube placement and we were successful in treating the fistula with ERCP in 87.5% of our patients.

Conclusions:

The use of ERCP as initial treatment for biliopleural fistula should be considered as the initial tool in the algorithm of management of this entity.

Key words: Fistula; Biliopleural; Endoscopic retrograde cholangiopancreatography; Complications; Pleural; Biliary

Abstract

Antecedentes:

La fístula biliopleural es una comunicación poco frecuente entre el sistema biliar y el espacio pleural secundario a ruptura de quistes hidatídicos, cirugías hepatobiliares o heridas penetrantes Existe poco sobre el tema en la literatura por lo que no existe un protocolo estandarizado para su manejo.

Objetivo:

El objetivo de este trabajo es determinar ventajas y desventajas del uso de CPRE como tratamiento inicial conservador para fístulas biliopleurales.

Método:

Nuestro estudio retrospectivo incluyó pacientes con diagnóstico de fístula biliopleural quienes fueron sometidos a CPRE como tratamiento inicial, mayores de 18 años en un período de Agosto de 2016 a Agosto de 2019.

Resultados:

Se incluyeron 8 pacientes con diagnístico de fístula biliopleural, 75% hombres y 25% mujeres con una media de edad de 24.5 años; la etiología traumática fue a predominante en nuestro grupo (89%), el diagnóstico se realizó entre los días 3 y 14 post colocación de sonda torácica y obtuvimos éxito en el tratamiento de la fístula con CPRE en el 87.5% de nuestros pacientes.

Conclusiones:

El uso de CPRE como tratamiento inicial para fístula biliopleural debe ser considerada como la herramienta inicial en el algoritmo de manejo de esta entidad.

Palabras clave: Fístula biliopleural; Colangiopancreatografía retrógrada endoscópica; Complicación; Pleura; Biliar

Introduction

Biliopleural fistula (BPF) is a pathological communication between the biliary tree and the pleural space. There are several causes described in the literature, which we can summarize in 5 groups1-3:

  • − Congenital

  • − Infectious (amebic liver abscess, pyogen, etc.)

  • − Bile duct obstruction (excluding iatrogenic or traumatic causes)

  • −Traumatic (blunt or penetrating)

  • − Iatrogenic (after liver resection, radiofrequency ablation, chest drainage, etc.)

Pathogenesis can be explained by two mechanisms3-5: in the first case, bile duct obstruction is the primary cause of BPF formation due to trauma, inflammation, tumors, etc. This obstruction leads to biliary retention, biloma, and an abscess that gradually erodes the diaphragm and creates communication to the pleural space. In the second case, there is no obstruction of the bile duct, but if the presence of a diaphragmatic/hepatic erosion, whether inflammatory, infectious, or traumatic that conditions biliopleural communication. In both cases, if there is a previous pulmonary condition that adheres the lung to the parietal pleura (old complicated parapneumonic effusion, empyema, etc.), there is a possibility that the path fistulizes to the bronchial tree and have a bronchobiliary fistula, a rare situation within the entity6. In any case, the preferred anatomical point for the formation of this communication is in the posteromedial region of the right hemidiaphragm, a site in contact with the naked area of the liver3,4,6,7.

BPF is a rare complication, so there is no epidemiological data on it. Among the most common causes reported in the literature were infectious causes such as liver abscess; however, in recent years, the traumatic cause (mainly penetrating) has been more frequent in the case and series reports (Table 1). In a reference trauma center such as our hospital, the traumatic cause is the most frequent, followed by infectious causes.

Table 1 Advance in the management of biliopleural fistulas 

Author Year No. of patients Etiology Type of fistula Initial therapy Second line of treatment Results Especial recommendations
Ferguson and Burford 20 1967 7 Trauma (×4)
Abscess (×2)
Biliary obstruction (×1)
BPF
BBF
Surgical No recurrences Summarize the basic steps for the Surgical treatment of BFP
Saylam et al.4 1974 6 Echinococcosis (×2)
Abscess (×2)
Desconocido (×2)
BPF Surgical Mortality: 1 due to septic shock It focuses on thoracotomy
If a biliary obstruction is found, it must be resolved first
Boyd6 1977 16 Biliary obstruction
Iatrogenic
BPF
BBF
Surgical Not specified Correction of biliary obstruction thoracic drainage are necessary
Terris et al.21 1997 3 Echinococcosis BPF
BBF
Surgical Reoperation in 1 patient 1 death from pulmonary embolism A case of left BBF is described
Oparah y Mandal22 1978 4 Trauma (penetrating) BPF Surgical: thoracotomy +/- laparotomy with pleural catheter No recurrence
Patients with only a thoracic catheter had prolonged hospitalization
The use of pleural drainage only with a probe is indicated only if drainage is performed early in combination with adequate subphrenic drainage.
Wei et al.23 1982 2 Biliary obstruction (stones) BBF Surgical: abdominal approach No recurrence
Warren et al.8 1983 15 Biliary obstruction iatrogenic (×10)
Congenital (×1)
Trauma (×2)
Stones (×2)
BPF (×13)
BBF (×2)
Surgical: abdominal approach
Only 1 patient with lobectomy
Reoperation in 9 patients 63 surgical procedures in total
They eventually recovered
Suggest abdominal approach for biliary obstruction
Crnjac et al.2 1987 30 Hydatid liver disease BBF Surgical: thoracotomy, laparotomy or both with pulmonary resection, cyst resection, diaphragmatic repair, and subphrenic drainage for 2-4 weeks Reoperation in 2 patients 3 patients died (10.3%)
2 patients with BBF recurrence
Thoracotomy if pre-operative studies show irreversible lung involvement and a single cyst
Gugenheim et al.24 1988 16 Biliary obstruction iatrogenic (×8)
Echinococcosis (×7)
Amoebic abscess (×1)
BBF Surgical: abdominal approach Reoperation 42 surgeries in total
They all recovered.
Abdominal approach when BBF results from a biliary condition
Thoracic approach to traumatic BBF and assess pulmonary resection
Yilmaz et al.25 1996 11 Complicated hydatid liver disease (×8)
Biliary obstruction iatrogenic (1)
Hydatid liver disease+ stones (×1)
Amoebic abscess (×1)
BBF Conservative: nasobiliary drainage in 4 patients
Biliary stent + nasobiliary drainage in 7 patients
Conservative treatment is repeated in 3 cases. Prolonged stay in patients with biliary stent + nasobiliary drainage Everyone resolved First successful series in non-surgical BFF treatment
Sentuk et al.26 1998 3 Alveolar-hydatid disease (×1)
Hydatid liver disease (×2)
BBF Conservative: ERCP + sphincterotomy post-surgery (1 case)
ERCP + nasobiliary drainage (2 cases)
Conservative treatment is repeated: octreotide (1 case) biliary stent (2 cases) Recurrence in all cases The treatment of BBF due to hydatid liver disease is not satisfactory either by surgical or conservative treatment; the reason is the most invasive nature of the disease
Chua et al.27 2000 2 Iatrogenic BBF Conservative: biliary drainage (1 case)
Surgical: thoracotomy with pulmonary and fistula resection (second case)
Surgical after the recurrence of the first case Both patients recovered Describes the use of vascularized intercostal pedicle and flat pericardial to close the fistula
Kabiri et al.28 2001 8 Abscess:
Amoebic (×3)
Pyogen (×1)
Trauma (×3)
Iatrogenic (×1)
BPF
BBF
Conservative: in 7 cases, sphincterotomy + pleural drainage + octreotide
Surgical: one case, repair of the biliary lesion
Reoperation: 2 cases Everyone improved BFP is successfully treated with conservative management
Surgery is reserved for the failure of this management
It is routinely used octreotide
Gerazounis et al.29 2002 3 Echinococcosis BBF Surgical: right posterolateral thoracotomy 2 patients died, the rest of the patients improved Suggests surgery in complicated cases of echinococcosis in BBF
Uchikov et al.9 2003 3 Hydatid liver disease (×2)
Echinococcosis (×1)
BBF Surgical: thoracotomy Everyone improved
Ong et al.17 2004 2 Biliary obstruction por stones (×1)
Iatrogenic (×1)
BBF Conservative: ERCP + sphincterotomy + stent + octreotide Surgical: only in 1 patient 1 muerte por laceración de la vena cava inferior Suggests the use of octreotide in conservative treatment
Peker et al.30 2007 4 Hydatid liver disease BBF Surgical: 2 cases
Conservative: 2 cases
Everyone improved Proposes a treatment algorithm for BFF
Tocchi et al.31 2007 31 Hydatid liver disease BBF Surgical: pulmonary resection was required in 25 cases 3 patients murieron (9.6%)
26 patients se recuperaron
It focuses on the thoracoabdominal approach
Erygit et al.5 2007 3 Abscess (×2)
Penetrating trauma (×1)
BFP Surgical: thoracotomy and pulmonary resection in two cases No recurrences reported
Aydin et al.32 2009 3 Abscess (×1)
Iatrogenic (×2)
BBF Conservative: percutaneous drainage with endoscopic sphincterotomy + stent No recurrences reported Suggest conservative treatment
Fistula embolization is described for the 1st time
Gandhi et al.33 2009 1 Trauma (blunt) BPF Conservative: ERCP + sphincterotomy + stent Thoracotomy Recurrence that needed surgery Complete resolution
Ball et al.34 2009 1 Trauma (penetrating) BFP Conservative: ERCP + sphincterotomy Complete resolution
Mehrzard et al.35 2012 1 Trauma (blunt) BPF Conservative: ERCP + sphincterotomy Late thoracotomy (1 year later) Recurrence after 1 year Thoracotomy was required after 1 year after the fistula was resolved
Liao et al.16 2012 1 Trauma (blunt) BPF Conservative: ERCP Full resolution

BPF: bilopleural fistula; BBF: biliobronchial fistula; ERCP: endoscopic retrograde cholangiopancreatography.

The clinical manifestations are described as acute or chronic: the acute event the patient begins with respiratory stress, febrile syndrome, pleuritic pain in the lower portion of the right hemithorax, irritative cough, yellowish sputum in cases of BBPF, and right pleural effusion. The chronic condition is characterized by chronic cough, occasional yellow sputum, intermittent fever, and pneumonia-like conditions8,9.

In recent years, conservative treatment has become more important in the treatment and the advent of endoscopic pancreatic cholangiography (endoscopic retrograde cholangiopancreatography [ERCP]) has resulted as an effective element in the treatment of BPF despite the few case series that exist in the literature10,11, which is why there are no guidelines for optimal treatment. In this paper, we present the experience of the use of ERCP in patients with BPF treated in our Hospital Universitario "Dr. José Eleuterio González" in the last 3 years.

Materials and methods

A descriptive retrospective study was carried out, including patients who were detected the presence of fructose bis-phosphate (FBP) for various causes, including penetrating wounds. We obtained the information of clinical records, diagnoses were assessed, characteristics of the lesions, initial repair technique, days of hospital stay, and their outcome after performing all of our ERCP patients. We made a statistical analysis with the JMP 10 program. These patients were in a period from August 2016 to August 2019 in our Hospital Universitario "Dr. José Eleuterio González" in Monterrey, N.L., Mexico.

Results

We obtained a total of 8 patients with a diagnosis of FBP in a period of 3 years, of which 6 were men (75%) and 2 women (25%), with a mean age of 24.5 years. The diagnoses were three in all, traumatic, which we divided into gunshot wound (GSW) and stab wounds and infectious (Fig. 1).

Figure 1 Diagnostics of our population. GSW: gunshot wound, SW: stab wound. 

Our 7 trauma diagnosis patients showed a double penetrating lesion, either by a projectile or by a knife, which required a surgical approach; all of them underwent an exploratory laparotomy and only 2 of the 7 trauma patients a concomitant right thoracotomy was required due to the initial trauma, either for the repair of pulmonary lesions or control of chest bleeding. Due to the double penetrating lesion, there was a need for diaphragmatic repair, which debrided the edges in the firearm injuries and performed primary repair of the diaphragm; in one patient, an omentum patch was performed and in the second trauma patient was placed a pleura patch (Table 2). The eighth patient was a female with a diagnosis of pyogenic liver abscess who had her laparotomy abscess drained with an omentum patch placed on the liver bed.

Table 2 Population with their initial diagnoses, initial surgery, and type of diaphragmatic repair 

Patient Diagnosis Injuries Surgery Repair
1 GSW Liver injury SII + Intestinal injury SIII + intercostal laceration Laparotomy + Right thoracotomy Primary + pleural patch
2 GSW Liver injury SIII Laparotomy Primary
3 GSW Liver injury SII Laparotomy Primary + omentum patch
4 SW Liver injury SII Laparotomy Primary
5 GSW Liver injury SIII + colon lesion SII + Intercostal artery laceration Laparotomy + Right thoracotomy Primary
6 GSW Liver injury SII+ lung laceration Laparotomy + Right thoracotomy Primary
7 SW Liver injury SIII Laparotomy Primary
8 Pyogenic liver abscess Does not apply Laparotomy Primary + omentum patch*

Firearm projectile wound (GSW), puncture wound (SW), injury stage (S).

*This patient underwent surgical drainage of the liver abscess and the omentum patch was placed on the liver bed; GSW: gunshot wound, SW: stab wound.

All our patients had a need for the placement of a pleural catheter (PC) from the beginning due to the double penetrating lesion. The outflow of liquid with biliary characteristics was observed by the PC between days 3 and 14 post-placement (mean of 5.7 days); the fistulas recorded an expense of approximately 100 cc of biliary characteristics in 24 h. No other imaging study was performed for diagnosis due to the obvious clinical signs of patients with the presence of right pleural effusion and the characteristics of the fluid drained by the PC. Clinically, patients diagnosed with BPF due to trauma remained hemodynamically stable, with no evidence of systemic inflammatory response; the patient with a diagnosis of liver abscess was detected the presence of BPF at 14 days post-PC placement, remained persistent febrile due to an intra-abdominal collection secondary to her diagnosis, which was evacuated by punction; however, the patient was complicated with intrahospital pneumonia which culminated in her death.

All of our patients underwent ERCP with sphincterotomy between days 2 and 10 after diagnosis of BPF (mean of 4.3 days). Once the procedure was performed, we obtained the resolution of the BPF in 7 of 8 patients (87.5%). We define as a response to treatment the decrease in the biliary expenditure by the thoracic catheter to < 10 cc in 24 h with radiological evidence of little or no residue in the pleural cavity, which was obtained from these 7 patients between days 3 and 5 post-ERCP (average of 3.12 days). No complications of ERCP were reported.

We had mortality in 2 patients which are worth analyzing in detail: the first patient who died was a GSW in which, in his associated lesions, a colon lesion was detected; in his post-operative, the patient was complicated with the presence of BPF which was detected on the 5th day after PC placement, ERCP was performed on the 10th day (ERCP delayed due to poor patient conditions) and we obtained a response to appropriate BPF treatment on the 5th day after ERCP; however, the patient's conditions did not improve and finally the patient dies from sepsis. The second case was a patient with a diagnosis of pyogenic liver abscess who was referred to our hospital with PC and for follow-up. We detect the presence of BPF on the 14th day after PC; late ERCP is performed due to poor conditions of the patient (on the 6th day after diagnosis); however, due to abdominal sepsis knotted to a diagnosis of hospital-acquired pneumonia, the patient passes away.

At present, at long-term follow-up, the 6 patients in whom we obtained a good response to ERCP treatment remained uncomplicated, these patients had PC withdrawn, major surgery was avoided, and no inflammatory response data were discharged for follow-up at the office. During his surveillance, there was no evidence of a recurrence of pleural effusion, an increase in bilirubin, or leukocytosis, so they were definitively discharged from the consultation.

Discussion

The presence of BPF is a low-frequency entity, as we saw reported in the literature, the infectious cause was the first cause described; however, in the most recent reviews, the penetrating traumatic cause is the one that currently prevails, probably due to the change in society and the current problems that we face and that we could verify in our study5,12-16. Its treatment begins from the early diagnosis, preventing the increase and complications of the BPF itself because the bile fluid it has a corrosive potential on the lung and pleura11,13. That is why a high degree of clinical suspicion is mandatory in its management.

Due to the analysis of the experience obtained in our study and compared to that described in the international literature, we propose standardization in the treatment of BPF. Once the presence of BPF has been demonstrated, it is proposed to start with conservative management, which consists of the use of intravenous antibiotics, low-fat diet, analyze the use of somatostatin17, and liver ultrasound with right pleural space screening in which it can be identified pleural effusion and/or the presence of right subdiaphragmatic collection, so the PC is placed for pleural effusion and/or percutaneous drainage for intra-abdominal collections. The persistence of bile fluid by the PC dictates the need to assess the use of ERCP. This procedure is beneficial due to its potential diagnosis when performing an endoscopic and subsequently therapeutic cholangiography; considering the principle of any fistula, ERCP with sphincterotomy will reduce the distal resistance of the sphincter of Oddi which is around 18 ± 2 mmHg, in addition to the normal pressure of the common duct which is between 10 ± 2 mmHg, this pressure gradient will be reduced to 1 ± 1 mmHg after a spherotomy18. Due to this principle, ERCP with sphincterotomy is recommended within 72-96 h after PC placement and persistence of bile fluid outflow. It is expected to have BPF resolution within the first 48 h11. This conservative management does not increase the morbidity that surgical treatment entails. The pharmacological agents that reduce the pressure of the sphincter of Oddi have been proposed; however, their role in the management of BPF is unclear19. The percentage of success reported in the literature is close to 97% of cases, and the rest of patients culminate in the need for surgical treatment. That is why a BPF management algorithm is proposed (Fig. 2). In studies published in the literature, it does not dictate a difference between results according to cause (infectious vs. traumatic); in this series of cases, we found traumatic as the most frequent cause; however, we obtained an infectious cause in which he died of sepsis. It is important to note that the infectious origin of this entity is much more infrequent, that is why infectious versus traumatic analysis is difficult.

Figure 2 Algorithm proposed for the management of biliopleural fistula. 

Conclusion

This study tries to be an initiator in the treatment of a very infrequent complication; its rarity is reflected in the few patients that were obtained in 3 years in a reference center in our country; however, good results were obtained with this observational study. This management algorithm is proposed to carry out prospective studies once this entity that is little described has been identified.

The importance of the benefit of biliary decompression in BPF is important, showing that it significantly reduces the morbidity and mortality offered by surgical treatment. The recommended time to perform it is 72-96 h after diagnosis of BPF when the patient's clinical conditions allow it; in this way, it has found the benefits of avoiding surgical treatment (intra-hospital days, costs, etc.).

Our series is the largest reported in the literature in recent years, which was treated with conservative management based on ERCP and sphincterotomy for BPF, obtaining promising results and promoting the use of this management algorithm in our center and serving as a basis for long-term prospective comparative studies.

Acknowledgment

Our deepest thanks to our patients, who are the first teachers on stage.

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Ethical disclosures

Protection of human and animal subjects. The authors declare that no experiments were performed on humans or animals for this study.

Confidentiality of data. The authors declare that they have followed the protocols of their work center on the publication of patient data.

Right to privacy and informed consent. The authors declare that no patient data appear in this article.

Received: January 30, 2020; Accepted: June 03, 2020

* Correspondence: Edson R. Marcos-Ramírez Ave. Francisco I Madero, s/n Mitras Centro C.P. 64460, Monterrey, N.L., México E-mail: ermarcos7@gmail.com

Conflicts of interest

There are no conflicts of interest between the proponents and participants in the present work.

Creative Commons License Instituto Nacional de Cardiología Ignacio Chávez. Published by Permanyer. This is an open ccess article under the CC BY-NC-ND license