Abstract
Background
In this retrospective study, the effects of cystic duct (C) tube use on the incidence of post-hepatectomy bile leak were assessed.
Methods
The subjects were 550 patients who underwent a hepatectomy during 1990–2011, with (n = 83) and without (n = 467) C tube drainage. The use of a C tube was based on the surgeon's choice.
Results
Bile leakage was observed in 44 (8%) patients, and its incidence post-operatively correlated with intrahepatic cholangiocarcinoma, parenchymal transection with forceps fracture and tie, a major hepatectomy, prolonged surgery and excessive blood loss (P < 0.050) but not with the use of a C tube. The incidence of an intra-abdominal infection was higher and the hospital stay was longer in the leak (49 days) than non-leak group (21 days, P < 0.001). ISGLS grade B and C bile leak post-hemi-hepatectomy and extended-hepatectomy were more frequent in the non-C than C tube group (P = 0.016). The duration of hospitalization was not different between the two groups; however, 7 patients in the non-C tube group had prolonged hospitalization (> 60 days) compared with none in the C tube group (P = 0.454).
Conclusion
The usefulness of the C tube in preventing post-hepatectomy bile leak could not be confirmed; however, both bile leak requiring clinical management and long hospitalization after a major hepatectomy could be reduced with C tube use.
Introduction
A hepatic resection is currently associated with low mortality but the morbidity remains high.1 In particular, biliary complications can lead to an intra-abdominal abscess or long hospital stay.2,3 Although haemostatic devices have improved the outcome in recent years, bile leakage from the liver cut surface or from a large bile duct remains problematic.4 Fujimura et al.5 described the insertion of a cystic duct tube (C tube), via the cystic duct into the common bile duct for biliary decompression. The C tube was first used in patients who underwent surgery for choledocholithiasis.6,7 Hotta et al.8 subsequently used the C tube to reduce the incidence of bile leaks in patients who underwent a hepatic resection. However, their results have not been well replicated.
The aim of the present study was to examine the relationship between the use of a C tube and the incidence of bile leakage, an associated intra-abdominal abscess and the duration of hospitalization, in patients who underwent a hepatectomy.
Materials and methods
Patients
The subjects were 550 patients who underwent a hepatic resection at the Division of Surgical Oncology, Department of Translational Medical Sciences, Nagasaki University Graduate School of Biomedical Sciences (NUGSBS) between April 1994 and October 2011. The protocol followed at the NUGSBS hospital includes pre-operative determination of the volume of the liver to be resected based on the results of the indocyanine green retention rate at 15 min (ICGR15) using Takasaki's formula.9 The estimated resected liver volume, excluding the tumour volume (cm3), was measured by computed tomography (CT) volumetry.10 Essentially, the planned hepatectomy was performed when the permitted resected volume of the liver was greater than the estimated resected volume of the liver.
The present study was a non-randomized retrospective analysis of data retrieved from both the anaesthetic and patient charts plus the NUGSBS database, and included the duration of hospitalization after a hepatectomy. The authors declare that this research did not receive any sponsorship or funding and no conflict of interest. The study design was approved by the local Ethical Review Board at the NUGSBS, and written informed consent for collecting data was obtained from each patient. The study followed the Declaration of Helsinki regarding ethical principles and human experimentation.
Technique of C tube insertion and data analysis
Although the C tube became available in 1994 in Japan, it was first used at NUGSBS in 2000 because of changes in operator's policy. In the present study, patients were divided into two groups: the C tube group and non-C tube group. The indication for use of the C tube was based on the surgeon's choice in each hepatectomy. A size 6 Fr C tube (length, 50 cm, Sumius, Sumitomo Bakelite Co., Tokyo, Japan) was routinely used. After a hepatectomy and cholecystectomy, the remnant cystic duct was cut and the lumen was extended using small and fine forceps. The tip of the C tube was placed into the common bile duct via the cystic duct and fixed by elastic thread inserted through the cystic duct. After insertion, bile reflux into the tube was confirmed and a bile leak test was performed using saline and air. In the non-C tube group, a bile leak test was routinely performed after a hepatectomy using a similar method and the cystic duct was ligated.
In the C tube group, the C tube was removed without a clamp after confirming the lack of intra-abdominal bile leak. An intra-abdominal drain was routinely placed around the resected area and total bilirubin level was examined at 1, 3, 5 and 7 post-operative days. A bile leak was considered to have occurred when the total bilirubin level in the drain was greater than three times the serum total bilirubin level. A bile leak was managed via the drain inserted during operation or re-insertion of the drainage tube. In cases with uncontrolled bile leak, an additional drain was placed. A massive bile leak from the main hepatic duct necessitated endoscopic biliary drainage. Based on the criteria of the International Study Group of Liver Surgery (ISGLS),11 the degree of bile leak was classified as Grade A (no impact of clinical management), B (requiring a change in clinical management) and C (a repeat laparotomy is necessary).
The analysed parameters were age, gender, background liver disease, liver functional status, extent of hepatectomy, associated vascular resection, operation time, blood loss, other post-operative complications and duration of hospitalization.
Statistical analysis
All continuous data were expressed as median and range values. Data of different groups were compared using one-way analysis of variance (anova). The chi-square test was used for comparison of categorical variables. Differences between groups were analysed using Fisher's exact test or Scheffé's multiple comparison test. A two-tailed P-value of less than 0.05 was considered significant. Multivariate analysis was performed using proportional hazards regression modelling. Except for the use of the C tube, variables with two-tailed P-values of < 0.250 on univariate analysis were entered into multivariate analysis. All statistical analyses were conducted using the StatView software for Windows, version 5.0 (SAS Institute, Inc., Cary, NC, USA).
Results
Post-operative bile leak and associated parameters
Patient demographics are shown in Table 1. A C tube was used in 83 (15%) patients including 7 who underwent a limited resection, 14 after a segmentectomy, 24 after a sectionectomy, 31 after a hemi-hepatectomy, 4 after an extended hemi-hepatectomy and 3 after a trisectionectomy. A C tube was used in 0 of 142 (0%) patients who underwent a hepatectomy between 1994 and 1999, 5 of 125 (4%) between 2000 and 2004, and 78 of 283 (28%) between 2005 and 2011. The frequency of use of the C tube was significantly higher during the period of 2005–2011 than 1994–1999 and 2000–2004 (P < 0.001, each). Bile leakage or a fistula was observed after a hepatectomy in 44 (8%) patients, including 4 who had undergone a limited resection, 4 a segmentectomy, 11 a sectionectomy, 8 a hemi-hepatectomy, 14 an extended hemi-hepatectomy and 3 a trisectionectomy. Dislocation of the C tube tip occurred in one patient who had undergone a central bisectionectomy, but C tube insertion was not associated with serious complications. None of the 550 patients required re-operation for bile leak repair.
Table 1.
Relationship between biliary leakage and various clinico-surgical parameters
| Bile leak (-) [n = 506] | Bile leak (+) [n = 44] | P-value | |
|---|---|---|---|
| Age (years, median) | 65 (17–86) | 67 (34–78) | 0.344 |
| Gender | |||
| Males | 351 (69%) | 31 (70%) | 1.000 |
| Females | 155 (31%) | 13 (30%) | |
| Background liver disease | |||
| Normal | 287 (57%) | 30 (68%) | 0.188 |
| Chronic hepatitis | 120 (24%) | 11 (25%) | |
| Cirrhosis | 79 (15%) | 3 (7%) | |
| Alcoholic or fatty | 20 (4%) | 0 (0%) | |
| Liver disease | |||
| HCC | 203 (39%) | 11 (25%) | 0.002 |
| Cholangiocarcinoma | 85 (18%) | 20 (45%) | |
| Liver metastasis | 183 (36%) | 11 (25%) | |
| GBC | 29 (6%) | 2 (5%) | |
| Others | 6 (1%) | 0 (0%) | |
| Child–Pugh classification | |||
| A | 489 (97%) | 42 (96%) | 0.658 |
| B | 17 (3%) | 2 (4%) | |
| Liver damage grade | |||
| A | 441 (87%) | 39 (89%) | 0.962 |
| B | 65 (13%) | 5 (11%) | |
| Pre-operative liver function tests | |||
| ICGR15 (%)a | 12 (1–64) | 11 (2.7–27) | 0.668 |
| Total bilirubin level (mg/dl) | 0.95 (0.63–2.34) | 0.94 (0.22–2.45) | 0.832 |
| Prothrombin activity (%) | 93 (55–145) | 93 (63–119) | 0.823 |
| Hyaluronic acid (ng/ml) | 83 (4–1730) | 74 (10–415) | 0.805 |
| Pre-operative arterial embolization | |||
| No | 472 (92%) | 42 (96%) | 0.758 |
| Yes | 34 (8%) | 2 (5%) | |
| Method of parenchymal transection | |||
| Forceps fracture and tie | 398 (79%) | 40 (91%) | 0.0076 |
| Use of haemostatic devices | 107 (21%) | 4 (9%) | |
| Extent of hepatectomy | |||
| Limited | 180 (36 | 4 (9%) | 0.0006 |
| Segmentectomy or sectionectomy | 156 (31%) | 15 (34%) | |
| Hemi-hepatectomy or more | 170 (33%) | 25 (57%) | |
| Side of hepatectomy | |||
| Right-side hepatectomy | 296 (59%) | 21 (48%) | 0.214 |
| Left-side hepatectomy | 209 (41%) | 23 (52%) | |
| Combined vascular anastomosis | 37 (7%) | 7 (16%) | 0.122 |
| Operation time (min) | 380 (50–1230) | 545 (176–974) | <0.001 |
| Blood loss (ml) | 773 (5–7150) | 1310 (100–3630) | <0.001 |
| Type of bile leak | |||
| Injury of aberrant bile duct | – | 0 | |
| Stump of main bile duct | – | 5 | |
| Use of a C tube | 76 (15%) | 7 (16%) | 1.000 |
| Other post-operative complications | |||
| Long-term ascites or pleural effusionb | 76 (15%) | 6 (14%) | 0.979 |
| Intra-abdominal infection | 24 (5%) | 24 (55%) | <0.001 |
| Hepatic failure | 21 (4%) | 4 (9%) | 0.258 |
| Hospital death | 11 (2%) | 3 (7%) | 0.168 |
| Systemic complications | |||
| Cardiac complications | 12 | 1 | 0.974 |
| Respiratory complications | 27 | 3 | |
| Others | 15 | 2 | |
| Hospital stay (day) | 21 (6–81) | 49 (14–152) | <0.001 |
Data are numbers/percentages of patients or (ranges).
HCC, hepatocellular carcinoma; CCC, cholangiocarcinoma; GBC, gall bladder carcinomas.
Data are mean ± SD.
Treated with diuretics for more than 7 days.
In 467 patients of the non-C tube group, endoscopic tube stenting was performed in 3 patients; however, percutaneous transhepatic biliary drainage was not performed. Fibrin glue was used in one patient who did not undergo C tube placement. Table 1 shows the relationship between biliary leakage and various clinico-surgical parameters. The bile leak rate correlated significantly with the extent of a hepatectomy, the method of parenchymal transection, operation time and blood loss. In some cases, bile also leaked from the closed stump of the main hepatic duct. The frequency of intra-abdominal infection and a longer duration of hospitalization were significantly associated with the bile leak group. Multivariate analysis of the parameters associated with post-operative bile leak identified a hepatic transection using the forceps fracture method with tie and long operation time, but not C tube use, as significant and independent factors that influenced the bile leak rate (Table 2).
Table 2.
Multivariate logistic analysis for parameters associated with post-operative bile leak
| Variables | Post-operative bile leak | |
|---|---|---|
| Risk ratio (95%CI) | P-value | |
| Liver disease | ||
| HCC | 0.763 (0.315–1.847) | 0.548 |
| Cholangiocarcinoma | 2.265 (0.923–8.301) | 0.0671 |
| Bile duct carcinoma | 0.897 (0.256–3.135) | 0.864 |
| Others | 1 | |
| Method of parenchymal transection | ||
| Forceps fracture and tie | 3.434 (1.063–11.074) | 0.0388 |
| Use of haemostatic devices | 1 | |
| Extent of hepatectomy | ||
| Hemi-hepatectomy or more | 2.134 (0.628–7.283) | 0.222 |
| Segmentectomy or sectionectomy | 1.722 (0.476–6.228) | 0.406 |
| Limited resection | 1 | |
| Side of hepatectomy | ||
| Left-side hepatectomy | 1.634 (0.732–4.289) | 0.322 |
| Right-side hepatectomy | 1 | |
| Combined vascular anastomosis | ||
| Yes | 0.984 (0.350–2.771) | 0.976 |
| No | ||
| Operating time (hours) | ||
| ≥500 | 5.128 (2.182–12.052) | 0.0002 |
| <500 | 1 | |
| Blood loss (ml) | ||
| ≥1000 | 1.661 (0.733–3.762) | 0.223 |
| <1000 | 1 | |
| Use of a C tube | ||
| Yes | 1.071 (0.397–2.885) | 0.893 |
| No | 1 | |
See Table 1 for abbreviations.
Relationship between bile leak and use of C tube
Next, the post-hepatectomy bile leak rate according to the use of a C tube and the extent of a hepatectomy was analysed (Table 3). A bile leak was limited to patients of the non-C tube group among those who underwent a limited hepatectomy. In patients who underwent a segmentectomy or sectionectomy, the bile leak rate was not different between the non-C tube and C tube groups. There was no significant difference in ISGLS grade among patients who underwent a partial, segmental or sectional hepatic resection of the C tube and non-C tube groups. In patients who underwent a hemi-hepatectomy or extended hepatectomy, the bile leak rate with ISGLS grade B or C, was higher in patients of the non-C tube group than the C tube group. A major bile leak via the main hepatic duct was only observed in patients who underwent a hemi-hepatectomy or an extended hepatectomy in patients of the non-C tube group.
Table 3.
Relationship between post-hepatectomy bile leak and C tube use with the extent of a hepatectomy
| C tube (-) [n = 467] | C tube (+) [n = 83] | P-value | |
|---|---|---|---|
| Age | 66 (17–83) | 68 (37–87) | 0.554 |
| Gender | 0.579 | ||
| Males | 327 (86%) | 55 (83%) | |
| Females | 140 (14%) | 28 (17%) | |
| Side of hepatectomy | 0.0891 | ||
| Right | 262 (56%) | 54 (65%) | |
| Left | 205 (44%) | 29 (35%) | |
| Partial hepatectomy | |||
| Bile leak negative | 173 | 9 | 1.000 |
| Bile leak positive | 4 | 0 | |
| Group A/ B/ Ca | 2/2/0 | 0/0/0 | 0.744 |
| Segmentectomy or sectionectomy | |||
| Bile leak negative | 123 | 32 | 0.448 |
| Bile leak positive | 10 | 5 | |
| Group A/ B/ Ca | 2/8/0 | 2/3/0 | 0.560 |
| Hemi-hepatectomy and more hepatectomy | |||
| Bile leak negative | 134 | 35 | 0.175 |
| Bile leak positive | 23 | 2 | |
| Group A/ B/ Ca | 4/18/5 | 2/0/0 | 0.016 |
Data are numbers/percentages of patients or (ranges).
ISGLS (International study group of liver surgery) grade11
The relation between C tube use and the duration of hospitalization was also examined (Table 4). The latter was not influenced by the use/non-use of a C tube. However, a longer hospital stay (more than 60 days) was observed only in patients of the non-C tube group. The median duration of hospitalization in the C tube group and the non-C tube group in patients with post-operative bile leak was 40 and 54 days, respectively (P = 0.323).
Table 4.
Duration of hospitalization according to C tube use in patients with post-operative biliary leak
| C tube (-) | C tube (+) | P value | |
|---|---|---|---|
| Hospital stay after a hepatectomy | 0.454 | ||
| <30 days | 4 | 1 | |
| 30–60 days | 26 | 6 | |
| 60–90 days | 4 | 0 | |
| >90 days | 3 (113, 116, 152 days) | 0 | |
Discussion
Intra-peritoneal bile leak is a major complication after a hepatectomy,2,3,12 which leads to a longer hospital stay and/or serious complications such as sepsis.12,13 While adequate drainage of an intra-abdominal bile prevents severe complications, it requires the prolonged use of a drainage tube. A biliary leak is sometimes difficult to repair even after intrahepatic biliary ablation with ethanol or endoscopic fibrin sealing.14,15 Furthermore, it is not uncommon to apply complex interventional treatment such as endoscopic intra-ductal tube stent or percutaneous transhepatic biliary drainage, for this purpose12,13 and some patients even require surgical repair or portal vein embolization.12,13,16 None of the patients in the present series required repair under re-laparotomy. An endoscopic biliary drainage tube was effective in one patient; however, the patient required long-term nasal tubing. Previous studies reported that the biliary leak/fistula rate after a hepatectomy ranged from 12% to 18%7,13,17 and the rate in the present study was within that range. However, a bile leak requires prolonged intervention and is associated with long hospital stay.12,13 In the present study, a post-hepatectomy bile leak was associated with a long hospital stay. Since the rates of major hepatic and systemic complications were not significantly different between patients with and without a bile leak, a bile leak itself was thought to be the main factor responsible for the prolonged hospital stay. Hotta et al.8 reported that a bile leak is correlated with a long operation time and a left-side hepatectomy and that it increased the likelihood of post-operative intra-abdominal abscess formation. The present study showed a tendency for bile leak to occur after a left-side hepatectomy, similar to the results reported by others.18 Furthermore, the use of haemostatic devices for parenchymal transection tended to be associated with low bile leak rate, similar to the finding of a previous study.19 It is thought that this method helps the sealing of tiny bile ducts at the transected plane. In the present series, a bile leak was associated with a large hepatectomy accompanied by large amount of bleeding and long operation time, and post-operative intra-abdominal infection. While the frequency of a biliary leak was higher after a major hepatectomy than a limited resection, a bile leak was still observed in four patients who underwent a limited resection. Thus, one can conclude that the type and extent of a hepatic resection has no effect on the frequency of a bile leak. In one patient who underwent a limited resection in segment 8, a bile leak continued 113 days after a hepatectomy. In the present study, a bile leak was not observed in patients with C tubes who underwent a limited resection. However, no definite conclusion can be made because the effect of C tube use on bile leak was not significant in both univariate and multivariate analyses (Tables 1 and 2).
As described above, C tube use was decided by the surgeon, and the frequency of its use tended to increase since 2004.7 In the NUGSBS hospital, the use of C tube also tended to increase since 2005. No criteria for C tube use were applied in the present series. The use of C tube may be warranted after major hepatectomy and/or when liver resection results in leakage from the main bile following exposure of the Glissonian pedicle on the transected edge. Considered collectively, there seems to be a need for establishment of criteria for C tube use after hepatectomy.
The insertion of a C tube is technically easy and safe compared with a T tube or retrograde transhepatic biliary drainage, and its removal within a couple of days is also easy and safe.4 Although interventional application through the C tube is difficult,7 the C tube drainage decompresses intraductal pressure, which leads to prevention of bile leakage from the biliary branches.7,20 The C tube drainage is also useful for bile leak from the upper biliary duct. It was hoped that C tube use would reduce the length of recovery; however, the present results did not show that this was true in the present series.
In the present study, C tube use did not lower the bile leak rate. Furthermore, the volume of bile leak was not different between the C tube users and non-users (data not shown). However, bile leakage was observed from the stump of the main hepatic duct in four patients of the non-C tube group. In patients with C tubes, this type of bile leak can be easily confirmed by fisterography or direct cholangiography. Based on the ISGLS classification, the frequency of a bile leak was higher in the non-C tube patients with a high ISGLS grade who underwent a major hepatectomy. C tube use might reduce the duration of bile leak by decompressing intraductal pressure and decreasing the amount of bile at the bile leak point as described above, thus resulting in the avoidance of invasive management such as a relaparotomy8,20 While the duration of hospital stay after a hepatectomy in patients with bile leak was not different between the C and non-C tube users, a longer hospital stay (more than 100 days) was noted in the non-C tube group. Hotta et al.20 reported the usefulness of examining liver function using bile samples during management. While the bile leakage rate in the present study was similar to that reported by Hotta et al., hepatic function tests were not performed in the present series. The C tube was used in the present series irrespective of the extent or location of the hepatectomy. The use of a C tube can provide useful information on patient management although careful analysis of the adverse effects and cost associated with C tube use should be conducted.
In conclusion, the present study examined the advantages and disadvantages of C tube use after a hepatectomy in 550 patients. The tube was used in 83 patients at the surgeon's decision, but no beneficial effects in preventing post-hepatectomy bile leak could be demonstrated. The results may suggest that C tube use is warranted for patients with ISGLS grade B and C and those who develop bile leak after a hemi-hepatectomy or a more extended hepatectomy. A C tube can be safely and easily placed, managed and removed. Further prospective and randomized studies of a larger number of patients are necessary to clarify the usefulness of a C tube after a hepatectomy.
Conflicts of interest
No disclaimer and no conflict of interest.
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