Endoscopic management of biliary complications after liver ...

Original Article

Endoscopic management of biliary complications after liver transplantation Terapêutica endoscópica nas complicações biliares pós-transplantes hepáticos Fernanda Prata Martins1, Jean Rodrigo Tafarel2, Angelo Paulo Ferrari3

ABSTRACT Objective: To retrospectively evaluate endoscopic treatment outcomes of biliary complications in post-liver transplants. Methods: The sample consisted of post-liver transplantation patients referred to the Endoscopy Unit of Hospital Israelita Albert Einstein, from July 2005 to July 2008, for endoscopic retrograde cholangiopancreatography due to suspected biliary complications. Results: Eighty-two patients were retrospectively assessed (six were excluded). From July 2005 to July 2008, 82 patients (57 male, mean age of 49.4 years) were reviewed and 276 endoscopic retrograde cholangiopancreatographies were undertaken (3.2/ patient). There were 57.3% cadaver and 42.7% living donors in this group. Biliary stricture was diagnosed in 56 patients (91% were anastomotic) and endoscopic treatment was successful in 56% (7% still in treatment). Biliary leaks were found in 28 patients (50% anastomotic). The endoscopic success rate was 62.9% and 7.1% are still in treatment. Conclusions: Post-liver transplantation biliary complications were relatively common and endoscopic treatment had a satisfactory outcome. Keywords: Liver transplantation/adverse effects; Postoperative complications; Biliary fistula/etiology; Bile ducts/pathology; Constriction, pathologic; Cholangiopancreatography, endoscopic retrograde/methods

RESUMO Objetivo: Avaliar retrospectivamente os resultados do tratamento endoscópico das complicações biliares em pacientes submetidos a transplante hepático. Métodos: Foram avaliados pacientes transplantados hepáticos encaminhados ao Serviço de Endoscopia do Hospital Israelita Albert Einstein, no período de Julho de 2005 a Julho de 2008, para realização de colangiopancreatografia retrógrada endoscópica por suspeita de complicação biliar. Resultados: Oitenta e dois pacientes (57 homens, média de idade de 49,4 anos) foram estudados retrospectivamente entre Julho

de 2007 e Julho de 2008. Nesse período foram realizadas 276 colangiopancreatografias retrógradas endoscópicas (3,2/paciente). Neste grupo, 57,3% receberam órgão de doador cadáver e 42,7% intervivos. Estenose biliar foi diagnosticada em 56 pacientes (91% anastomótica) e o sucesso da terapêutica endoscópica nestes casos foi de 56% (7% ainda em tratamento). Fístula biliar foi diagnosticada em 28 pacientes (50% anastomóticas) e a taxa de sucesso do tratamento endoscópico foi de 62,9%, sendo que 7,1% estão ainda em tratamento. Conclusões: Complicações biliares pós-transplante hepático são relativamente comuns e o tratamento endoscópico mostra bons resultados. Descritores: Transplante hepático/efeitos adversos; Complicações pós-operatórias; Fístula biliar/etiologia; Ductos biliares/patologia; Constrição patológica; Pancreatocolangiografia retrógrada endoscópica/métodos

INTRODUCTION Liver transplants are the third most common transplants in Brazil(1). Notwithstanding the advances in surgical technique, biliary complications remain significant causes of postoperative morbidity and mortality, involving 6 to 39.5% of the patients(2-9). Complications may be due to various factors related to the underlying disease or to surgical technique(8-9). An early diagnosis and appropriate treatment are essential for decreasing morbidity and mortality. Image exams are the first diagnostic methods to be used for assessing injury and the differential diagnosis in patients with suspected biliary complications. Endoscopic retrograde cholangiopancreatography (ERCP) and percutaneous transhepatic cholangiography (PTHC) are currently available for identification and treatment of post-liver transplant biliary complications.

Study carried out at Endoscopy Unit of Hospital Israelita Albert Einstein – HIAE, São Paulo (SP), Brazil. PhD, Hospital Israelita Albert Einstein – HIAE, São Paulo (SP), Brazil.

1

MD, Universidade Federal de São Paulo – UNIFESP, São Paulo (SP), Brazil.

2

Post-doctorate degree, Hospital Israelita Albert Einstein – HIAE, São Paulo (SP), Brazil.

3

Corresponding author: Angelo Paulo Ferrari – Rua Doutor Bacelar, 317 – apto. 231 – Vila Clementino – CEP 04026-001 – São Paulo (SP), Brasil – e-mail: [email protected] Received on April 31, 2008 – Accepted on Oct 30, 2008

einstein. 2008; 6(4):422-7

Endoscopic management of biliary complications after liver transplantation

The success rate ranges from 59 to 100%; many reoperations are thus avoided(3-5,8,10-13).

OBJECTIVE The purpose of this study was to retrospectively assess the results of endoscopic treatment of biliary complications in patients undergoing liver transplants. METHODS Eighty-two liver transplant patients (cadaver or living donors) referred to the Endoscopy Unit of Hospital Israelita Albert Einstein (HIAE), from July 2005 to July 2008, for ERCP with suspected post-transplant biliary complications were evaluated. The clinical suspicion of biliary complications was based on elevated hepatic or cholestatic enzymes, jaundice, pruritus, pain, choleperitoneum following removal of the biliary tube, fever, and cholangitis. ERCP and the appropriate treatment were done individually, as indicated by the physician at the time of examination. Complications were classified as mild (bacteremia, occlusion or migration of the prosthesis) and severe (acute pancreatitis, bleeding, perforation); these were also evaluated retrospectively. The result of the endoscopic treatment was also assessed retrospectively; success was defined as an improved clinical, laboratory and/or endoscopic status. Failure was defined as the absence of improvement in the abovementioned parameters and/or when patients required other procedures for treatment (percutaneous or surgical drainage). RESULTS A retrospective analysis was made of 88 post-liver transplant patients; six cases were excluded because data was not available. Thus, it was reported data on 82 patients, 57 (69.5%) male and 25 (30.5%) female. The mean age of patients was 49.4 years (10 to 77 years). The most common cause of hepatic disease leading to transplantation was hepatitis C (27 patients – 32.9%), followed by the combinations hepatitis C and hepatocarcinoma (10 patients – 12.2%), and hepatitis C with alcohol abuse (8 patients – 97%) (Table 1). Cadaver transplants were done in 42 cases (47,7%); 34 cases (38,6%) were living donor transplants (right lobe), 5 cases (5,7%) were combined liver-kidney transplants, 6 cases (6,8%) were second transplants from cadaver donors, and 1 case (1.2%) was a second transplant from a live donor (right lobe). The biliary anastomosis was choledoco-choledocal) in 52 patients

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with cadaver liver donors and in Roux-en-Y in one patient. A single anastomosis was done in 24 cases (68.6%) among the living donor recipients, a double anastomosis was done in 9 cases (25.7%), and other variants were performed in two cases (5.7%). These data are summarized on Table 1. Table 1. Demographic data, etiology of cirrhosis, type of transplant and biliary anastomosis of liver transplant patients, submitted to ERCP for suspected biliary complication Parameters Sex Male Female Age (years) Etiology HCV HCV + HCC HCV + alcohol Cryptogenic Others AIH / PBC / PSC Alcohol Fulminant HCV + HCC + alcohol HBV HBV + HCC HCV + AIH Type of transplant Cadaver Living Combined liver-kidney Second transplant from cadaver donor Second transplant from living donor Type of anastomosis choledoco-choledocal Roux-en-Y Single choledoco-RHD Double choledoco-RHD Others

n (%) 57 (69.5) 25 (30.5) 49.4 (10-77) 27 (32.9) 10 (12.2) 8 (9.7) 8 (9.7) 8 (9.7) 5 (6.1) 5 (6.1) 5 (6.1) 2 (2.4) 2 (2.4) 1 (1.2) 1 (1.2) 42 (51.2) 34 (41.5) 5 (6.1) 6 (7.3) 1 (1.2) 52 1 24 9 2

HCV = hepatitis C virus; HCC = hepatocellular carcinoma; AIH = autoimmune hepatitis; PBC = primary biliary cirrhosis; PSC = primary sclerosing cholangitis; HBV = hepatitis B virus; RHD = right hepatic duct; ERCP = Endoscopic retrograde cholangiopancreatography

Symptoms of biliary complications were increased enzymes in 53 patients (64.6%), jaundice in 20 patients (24.4%), suspected choleperitoneum following removal of the biliary tube in 14 patients (17.1%), cholangitis in 14 patients (17.1%), abdominal pain in 8 patients (9.7%), pruritus in one patient (1.2%), and fever in one patient (1.2%). The mean time between transplantation and the onset of symptoms was 80.4 days (7 to 418 days). Eight patients had late symptoms, one of them after two and a half years and the other after more than three years. These data were not included in the complication time calculation, since they were outliers. einstein. 2008; 6(4):422-7

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During the period of the study there were 276 ERCP in 82 patients, a mean 3.2 exams (1 to 13) per patient. ERCP revealed no biliary complications in ten of these patients (12.1%). Biliary stenosis was diagnosed in 56 patients (68.3%); it was anastomotic in 51 patients (91%), nonanastomotic in 2 patients (3.6%), both in 2 patients (3.6%), and due to kinking of the anastomosis in one patient (1.8%) (Table 2).

Table 3. Success of endoscopic therapy according to site of biliary lesions after liver transplant Type of lesion

n (%)

Stenosis Anastomotic

28/50 (56)*

Non-anastomotic

0/2 (0)

Fistula Anastomotic

7/14 (50.0)**

Non-anastomotic

10/13 (76.9)

*7 (14%) still on endoscopic treatment; **1 (7.1%) still on endoscopic treatment

Table 2. Cholangiographic findings in liver transplant patients, submitted to ERCP for suspected biliary complication ERCP finding

n (%)

Normal

10 (12.1)

Stenosis

56 (67.5)

Anastomotic

51 (91.0)

Non-anastomotic

2 (3.6)

Combination

2 (3.6)

Kinking

1 (1.8)

Fistula

28 (34.1)

Anastomotic

14 (50.0)

Non-anastomotic

13 (46.4)

Peripheral

Biliary leaks were diagnosed in 28 patients (34.1%); 14 of these cases (50.0%) were anastomotic, of which one was a loss of the anastomosis (Figure 2A and B); 13 cases (46.4%) were non-anastomotic, and one case (3.6%) was a peripheral leak (Table 2). Biliary leaks presented on average 57.2 days (7 to 185) after liver transplantation.

1 (3.6)

Calculii

18 (21.9)

Cholangitis

11 (13.4)

ERCP = Endoscopic retrograde cholangiopancreatography

Stenoses were dilated with catheters or hydrostatic balloons, followed by placement of prostheses (on average, 1.3 per patient), as indicated by the endoscopist during the exam (Figures 1A and B).

A

B

Figure 2. A) Large anastomotic fistula. B) Same patient of Figure 2A, showing slight contrast in the biliary tree, confirming disconnection between recipient and graft, and indication for surgical treatment

A

B

Figure 1. A) Anastomotic stenosis in cadaver transplant, with guide wire and hydrostatic balloon placed. B) Two plastic protheses placed after hydrostatic dilation

Four patients were excluded in the results analysis phase since their data were incomplete. The mean time between the onset of symptoms in stenosis patients and the ERCP was 67.8 days. Success of endoscopic therapy in these cases was 53.8% (28/52); 13.5% patients (7 patients) are still under treatment. The success rate in anastomotic stenoses was 56% (26/50); 7 patients (14%) are still being treated. Endoscopic therapy failed in all cases of non-anastomotic stenoses (Table 3). einstein. 2008; 6(4):422-7

Leaks were treated by sphincterotomy combined or not with prostheses based on the endoscopist’s judgment while carrying out the ERCP. The total success rate of the endoscopic treatment of posttransplant leaks was 63%. The success rate in anastomotic leaks was 50.0%; the success rate for those cases with leaks on the site of the biliary tube was 76.9% of cases (Table 3). Biliary stones were found in 18 patients (21.9%); cholangitis was diagnosed in 11 patients (13.4%) (Table 2). Mild complications were seen in 18.5% (51) of exams; occlusion of the prostheses was the most common complication (38 cases – 13.8%), followed by migration (10 patients – 3.6%), and bacteremia (3 cases – 1.1%). Severe complications were found in nine cases (3.3%), acute pancreatitis in four cases (1.4%),


bleeding in four cases (1.4%) and perforation in one case (0.3%). There were two deaths from complications of endoscopy; one of them was in a patient who had undergone gastrectomy (an afferent intestinal loop was perforated) and the other was a post-sphincterotomy hemorrhage case. Abdominal Doppler ultrasound was done in 72 patients (87.8%); this exam revealed hepatic artery thrombosis in five cases (6.9%), all of which had biliary complications and required a second transplant. Eight patients underwent arteriography, of which hepatic artery obstruction was found in five patients. Of these, three patients presented anastomotic stenoses, two with stenosis and biliary leaks (one anastomotic, one non-anastomotic) and one with a non-anastomotic biliary leak. One was given endovascular treatment, three were given percutaneous treatment and one was referred for a second transplant. The analysis by type of transplant revealed that biliary stenosis was diagnosed in 47.8% (22) and leaks in 36.9% (17) of 46 cadaver liver donor patients; of these, four were excluded from the final analysis due to incomplete data. The success rate for the treatment of stenosis in this group was 55.5% (ten cases); 16.7% (three cases) are still being treated. The success rate in cases of leaks was 58.8% (ten cases); 5.9% (one case) remains in treatment. Among the 35 live transplant donors, stenosis (Figure 3) was seen in 77.1% (27 cases), of which endoscopic treatment was successful in 15 cases (55.6%); one patient (3.7%) remains in therapy. Biliary leaks were found in ten patients (37%); the efficacy of endoscopic therapy was 40% (Table 4). There was no statistically significant difference between the cadaver and live liver donor transplant patients in terms of response to endoscopic treatment.

Figure 3. Anastomotic stenosis in living transplant

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Table 4. Success of endoscopic therapy according to type of liver transplant (graft) Type of transplant Stenosis Cadaver Living Fistula Cadaver Living

n (%) 10/18 (55.5)* 15/27 (55.6)** 10/17 (58.8)*** 4/10 (40)

* 3 (16.7%) still on endoscopic treatment; ** 1 (3.7%) still on endoscopic treatment; *** 1 (5.9%) still on endoscopic treatment

DISCUSSION ERCP and PTHC are currently used for defining and treating post-liver transplant biliary complications; the success rate is satisfactory, and these procedures avoid many reoperations(5,8,12). Biliary complications may occur in 6 to 39.5% of liver transplant patients(2-9), they are more frequent in live donor transplants(8). Complications may arise due to various factors, such as underlying diseases, prior biliary surgery, the type of anastomosis, a disproportion between the size of the donor and recipient biliary canals, insufficient length of the grafted biliary canal, and the anatomical complexity of the right biliary canals that may require anastomosis of more than one biliary branch(8,11). Other factors leading to such complications are the use of biliary drainage tubes, infection (CMV) and ischemia(8,11). The type of preferred biliary reconstruction in receptors with no biliary disease is the duct to duct biliary anastomosis; this method is more difficult in living donor transplants due to disproportion in the diameter, number of ducts and configuration of the biliary system. The direct biliary anastomosis has the advantage of preserving the sphincter, which avoids ascending bacterial infection in this group of immunosuppressed subjects. Furthermore, in this approach there are fewer postoperative complications, and endoscopy may be done more easily(5,8). There was no statistical difference between the cadaver and live donor transplant groups in the response to endoscopic treatment in this series. Early biliary complications are those that occur in the first two to three months after transplant, and include biliary leaks, biloma, anastomotic or non-anastomotic stenosis, disproportion between the donor-recipient biliary ducts, torsion or bleeding of the Roux-en-Y segment, and dehiscence due to necrosis of the biliary anastomosis(8). Late complications generally occur following the removal of the biliary drainage tube; these include leaks, stenosis (anastomotic, non-anastomotic or diffuse intrahepatic), cholangitis, choledocolithiasis, biliary duct ‘kinking,’ Oddi sphincter dysfunction, mucocele, einstein. 2008; 6(4):422-7

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and recurrent biliary disease (primary sclerosing cholangitis)(3,8,14). Here, the mean time between transplantation and the onset of symptoms agreed with the literature; a few cases were out of the normal curve. The diagnosis of biliary complications following liver transplantation is not easy; symptoms are generally nonspecific and may include anorexia, pruritus, jaundice, and rarely fever, since surgical denervation precludes pain. Laboratory tests may reveal an asymptomatic raise in transaminases, cholestasis and hyperbilirrubinemia. Most patients had increased enzymes and eventual jaundice as manifestations of biliary complications, in the present series. Fever and pruritus were uncommon findings, as reported in the literature. Imaging exams are the first choice for investigating any injury and the differential diagnosis of patients with suspected biliary complications. Ultrasound, computed tomography and magnetic resonance imaging may reveal dilated biliary ducts, stenosis with upstream dilatation, biliary calculi or biloma(15). Doppler ultrasound should be used for screening purposes and to reveal cases with arterial injury, who should be referred to arteriography or surgery(4,12,15). This imaging procedure was the most common in the present series. Magnetic resonance cholangiography is the method of choice for assessing these patients; its accuracy is 95.6 to 100%, enabling physicians to select those cases that should undergo endoscopic treatment(4,15). Eckhoff et al. showed that routine ERCP to assess asymptomatic changes in hepatic enzymes was not useful; the rate of normal exams was 96%. These authors recommended performing liver biopsies for diagnosing chronic rejection in these cases, especially in patients with no biliary dilatation in imaging exams(12). The choice of treatment depends on its availability, professional experience, and mostly on the type of surgical reconstruction that is required. ERCP is the first choice in patients with a choledoco-choledocal anastomosis; on the other hand, PTHC should be the first choice in patients with a hepaticojejunal anastomosis(3,8). Success rates described in the literature ranges from 59 to 100% for both methods. The need for surgical reoperation is the exception; it is reserved for those cases in which endoscopy or radiology has failed(3,4,8,10,11,13). Global success rates in this study were similar to that reported in the literature; there were minor variations depending on the type of complication. Complications of ERCP are specific to the exam and procedure. Acute pancreatitis is the most common complication, occurring in 1 to 7% of exams(16). Hemorrhage is directly related to the sphincterotomy; einstein. 2008; 6(4):422-7

it is reported incidence ranges from 0.7 to 2.5%. Perforation may occur in up to 1% of cases(16). Surgery may consist of converting the reconstruction into a biliary derivation (hepaticojejunal Roux-en-Y anastomosis) or a second transplant in extreme cases(8). Biliary leaks are generally early complications – within 30 days – in 70% of cases, and may be located in the anastomosis, the cystic stump, the insertion point of the biliary drainage tube, or on the raw surface of the liver in cases of live donor transplants(8). Leaks along the anastomosis may be due to technical errors or ischemia of the biliary duct(8). A further important factor for biliary leaks is believed to be the presence and handling of a biliary drainage tube(5,7-8). Alsharabi et al. found fewer biliary leaks in liver transplant patients in which biliary drainage tubes were not inserted, compared to patients with these tubes (8 versus 20%)(7). As described in the literature, biliary leaks presented early in this series; most of them manifested within the first 30 days. The principles for treating biliary leaks endoscopically are the same as those used in other postoperative leaks. Treatment includes sphincterotomy done singly or associated with a plastic prosthesis, or a prosthesis without sphincterotomy(3,8). Endoscopic follow-up should be performed in six to eight weeks. The prosthesis is removed if there are no signs of leaks. A new prosthesis should be placed if contrast extravasates. The reported success rate of endoscopic treatment of post-liver transplant biliary leaks is 66.6 to 100%(3,4,8,11). Surgery should be considered in patients with associated arterial injury, biliary duct necrosis, loss of anastomosis, and leaks with major extravasation of contrast in the ERCP(3,5,8). Successful endoscopic treatment of post-liver transplant biliary leaks was attained in half of the cases; the success rate was higher in leaks along the drainage tube site. Stenoses developing during the first posttransplantation weeks are generally anastomotic and secondary to ischemia or surgical technique issues(8,13). Non-anastomotic stenoses may be secondary to ischemia, infection or immune reactions(8). Anastomotic stenoses respond better to therapy compared to non-anastomotic stenoses, probably due to ischemia, which occurs more often in the latter(8). Late stenoses may be classified as anastomotic, hilar or intrahepatic; they may result from arterial obstruction, prolonged ischemia, chronic rejection, and recurrence of the underlying disease(8). Nonanastomotic stenoses often require additional exams, such as Doppler ultrasound or arteriography, to discard any association with arterial injuries(13).


ERCP is helpful to study the morphology of nonanastomotic stenoses, and to start therapy. These patients apparently respond less than those with anastomotic stenoses; surgery is required in some cases, involving biliary drainage or a second transplant(13). There was no difference in the success rate of the endoscopic treatment of anastomotic and non-anastomotic stenoses in the present series. Endoscopic treatment may be done by dilating a hydrostatic balloon or by using dilators, followed by the insertion of a plastic prosthesis or a nasobiliary drainage tube. Costamagna et al. showed the benefit of using multiple prostheses in the treatment of benign biliary stenosis(17). There are no studies, however, comparing the use of a single prosthesis and multiple prostheses in post-liver transplant stenosis. These patients should undergo a second endoscopy within six to eight weeks for follow-up purposes and to replace the prosthesis if needed(3-4,8,10,11,13). Successful treatment of post-liver transplant biliary stenosis occurs in 59 to 100% of cases(3-4,8,10,11,13), especially in duct-to-duct anastomoses. Anastomotic stenoses with no ischemia respond better to endoscopic treatment. Morelli et al. reported a long-term response (mean follow-up of 54 months) in 90% of patients(13). A second surgical procedure should be considered if the stenosis does not resolve within this period; there is no proven benefit of extending further the endoscopic treatment. As shown in the literature, the success rate of endoscopic treatment for anastomotic stenoses was higher than that for non-anastomotic stenoses here. Doppler ultrasound revealed thrombosis of the hepatic artery in one case of non-anastomotic stenosis. Stenoses may also be caused by incorrect placement of biliary drainage tubes; these may present as kinking of biliary ducts, and was seen in a few patients. Although rare, residual biliary calculi may be found, as in other biliary surgeries. Stones were also found in the present series.

CONCLUSIONS Post-liver transplant biliary complications are relatively frequent; leaks and stenosis are the most common of these complications. Endoscopic treatment was effective in most patients: 53.8% of patients with stenosis, and 63% of patients with leaks.

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einstein. 2008; 6(4):422-7