ORIGINAL ARTICLE
Laparoscopic Common Bile Duct Exploration in Cirrhotic Patients With Choledocholithiasis Jianguo Qiu, MD,* Haichao Yuan, MD,w Shuting Chen, MD,* and Hong Wu, MD, PhD*
Background and Aims: Although laparoscopic common bile duct exploration (LCBDE) has become the standard procedure for most choledocholithiasis patients, the application of this procedure to liver cirrhosis is still in debate. The aim of the current study was to evaluate the feasibility and safety of LCBDE in choledocholithiasis patients with compensated liver cirrhosis. Patients and Methods: From January 2006 to December 2012, 346 LCBDEs were performed in our hospital. According to the previously defined liver condition, the patients were divided into group A (liver cirrhosis, n = 132) and group B (without cirrhosis, n = 214). The perioperative data for the 2 groups were retrospectively reviewed and compared. Results: LCBDE was successfully completed in 326 patients. Conversion from laparoscopic to open surgery was necessary for 20 patients (5.7%) mainly because of hemorrhage (5, 25%) and severe adhesions (8, 40%). A T-tube was placed in 211 patients (64.7%), and primary closure was performed in 115 (35.3%) patients. There was a significant difference for groups A and B in terms of intraoperative blood loss (85 vs. 35 mL; P < 0.01). However, the 2 groups showed no significant differences with respect to the mean operation time (2.1 vs. 1.9 h; P = 0.07), complication rates (10.6% vs. 8.8%; P = 0.6), mean hospital stay (4.2 vs. 4.0 d; P = 0.6), conversion rate (5.3% vs. 6.1%; P = 0.77), and retained choledocholithiasis rate (8.3% vs. 7.1%; P = 0.65). There was no mortality in both groups.
diagnosed during cholecystectomy had not been previously detected.3 Since the first introduction of endoscopic retrograde cholangiopancreatography (ERCP) was reported in 1974, it has gained universal acceptance,4–6 especially in older patients.7,8 However, ERCP has some disadvantages, including acute pancreatitis and as high as 10% to 25% failure rate.9,10 Progress in laparoscopic technology and increased experience in laparoscopic procedures including laparoscopic hepatectomy11–13 enabled surgeons to perform laparoscopic common bile duct exploration (LCBDE), which reduced postsurgical pain, hospital stay, and period of disability.14,15 LCBDE has become the gold standard for the removal of CBD stones in the patients with unsuccessful ERCP procedures; however, the safety and efficacy of LCBDE in patients with liver cirrhosis has not been established. In the current study, we present the results of a retrospective study of our experience in a cohort of 364 consecutive patients from our department and evaluate the feasibility and safety of LCBDE in 134 cirrhotic Child A and B patients by comparing LCBDE in 214 patients who were without cirrhosis.
Conclusions: LCBDE is a feasible, effective, and safe surgical procedure for choledocholithiasis patients with compensated cirrhosis. Key Words: laparoscopy, cholecystectomy, common bile duct, liver, cirrhosis
(J Clin Gastroenterol 2015;49:132–136)
C
ommon bile duct (CBD) stones represent a significant danger to patients and are the most frequent complications of cholecystolithiasis and occur in 10% to 15% of patients.1,2 The diagnosis of CBD stones may be achieved by the preoperative examination including ultrasonography (USG), magnetic resonance imaging (MRI), and magnetic resonance cholangiopancreatography (MRCP). However, it is suspected that >30% of the cholecystolithiasis
Received for publication August 26, 2013; accepted December 1, 2013. From the Departments of *Hepatobiliary Pancreatic Surgery; and wUrology Surgery, West China Hospital, Sichuan University, Cheng du, Sichuan Province, China. H.W.: designed the study. J.Q.: wrote the manuscript. S.C. and H.Y.: analyzed the data and interpreted the results. Supported by Science and Technology Support Project of Sichuan Province (2009FC0093). The authors declare that they have nothing to disclose. Reprints: Hong Wu, MD, PhD, Department of Hepatobiliary Pancreatic Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China (e-mail: [email protected]). Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved.
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PATIENTS AND METHODS Patients The protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki as reflected in a priori approval by the Clinical Trial Ethics Committee of West China Hospital, Sichuan University. From January 2006 to December 2012, a total of 3658 laparoscopic cholecystectomies (LC) were performed at our hospital. Overall, 346 consecutive patients accompanied with choledocholithiasis underwent LCBDE. According to previously defined liver condition, the patients were divided into group A (liver cirrhosis, n = 132) and group B (without cirrhosis, n = 214). Data of each patient were retrospectively collected by chart review and analyzed in terms of demographic characteristics, surgical outcomes (including operation time, estimated blood loss, and conversion rate), postoperative variables (including hospital stays, analgesia requirements, complications, and retained choledocholithiasis rate), and hematology tests at first and third postoperative day (including serum bilirubin, transaminases, alkaline phosphatase, serum albumin, and prothrombin time). Complications or death occurring during the same hospitalization or within 90 days after operation were defined as postoperative complications and postoperative mortality, respectively. Operating time was the number of minutes for which the operation continues. Hospital stay was defined as the number of days from the date of J Clin Gastroenterol
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operation to discharge. Postoperative pain scores were assessed using a standard 10 cm visual analog scale with options ranging from 0 (no pain) to 10 (worst pain).
Preoperative Evaluation The preoperative evaluation involved history-taking; physical examination; abdominal USG, MRI, or MRCP; and laboratory tests. Liver cirrhosis was diagnosed from using abdominal USG that showed multiple nodular irregularities of the liver surface, small liver size, echo coarseness, or ascites, splenomegaly, and esophageal varices.16 Cirrhosis was further confirmed by the intraoperative USG or liver biopsy.
Indications and Operative Techniques of LCBDE In accordance with our protocol for the management of CBD stone (Fig. 1), LCBDE is performed during LC procedure for all cases in which CBD stones can be confirmed by intraoperative cholangiogram (IOC) or laparoscopic intraoperative ultrasound (LIOU). Otherwise, the following situations were also warranted LCBDE in some patients: (1) unexplained liver damage; (2) sonographic, endoscopic, or radiographic evidence of CBD stones; (3) a dilated bile duct; or (4) a history of biliary pancreatitis. The comprehensive IOC approaches utilized have been detailed elsewhere.3,17 IOC was performed at the right midclavicular line using a 5-Fr needle. An olive-tip ureteral catheter attached to a metal wire was introduced through the cystic duct.17 Whenever this procedure was not possible, LIOU was used. After confirmation of the presence of CBD stones, a 5-mm trocar was inserted into the same place in which the IOC catheter was introduced. In the current study, LCBDE was mainly accomplished through the cystic duct or through a choledochotomy after cholecystectomy. If CBD stones are detected, primary extraction through the cystic duct is intended. We have no experience with balloon dilatation of the cystic duct. If transcystic retrieval cannot be achieved because of the size or position of stones, the stones are removed through direct choledochotomy.
LCBDE for Choledocholithiasis
For choledochotomy procedure, a longitudinal incision on the cystic duct was made onto the anterior surface of the CBD. The choledochoscope was inserted through the midclavicular port and guided into the CBD. Once a CBD stone is visualized, a basket is inserted into the working channel of the choledochoscope and the stone is captured with forceps. Then the basket and entrapped stone are pulled against the choledochoscope, and both the choledochoscope and basket are removed from the biliary system. If several stones are to be removed, it can be useful to collect the stones in a bag placed in the abdomen and that will be pulled out at the end of the procedure. Usually, if the stone has been cleared completely, there is no need to place a T-tube into the CBD.
Statistical Analysis All values were presented as mean ± SD, the w2 test or the Fisher exact test were used to evaluate the significant differences between 2 groups. A value of P < 0.05 was considered statistical significance. All analyses were performed using SPSS 16.0 statistical software.
RESULTS Since January 2006, CBD stones were detected by preoperative studies and IOS or LIOU in 346 of 3658 patients (9.46%) who underwent LC at West China Hospital, Sichuan University. Of those 346 patients, 86 were diagnosed with CBD stones only by IOS or LIOU during LC procedure, without preoperative suspicion of bile duct stones. The clinicopathologic characteristics of all included patients are summarized in Table 1. There were no significant differences between the 2 groups in demographic characteristics. Choledochotomy was successful in 40.8% of patients, whereas the transcystic approach was 59.2% successful. Conversion to laparotomy was necessary in 20 of the 346 patients (5.8%). The reasons for conversion included bleeding in the cystic artery (n = 3), right hepatic artery (n = 2), colon injury (n = 1), severe inflammation (n = 6), and difficult dissection to adhesions (n = 8).
FIGURE 1. The protocol for the laparoscopic management of common bile duct (CBD) stone at our hospital.
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TABLE 1. Patient Characteristic of all Included Patients
Parameters Total patients (n) Age (y) Sex (M/F) BMI (m3/kg) Child-Pugh Class (n) A B ASA status (n) I II III IV Cirrhosis etiology (n) Hepatitis B Hepatitis C Alcohol Previous biliary surgery [n (%)] Preoperative ERCP [n (%)]
Group A
Group B
132 45.3 ± 12.5 65/67 21.4 ± 2.8
214 46.7 ± 20.4 100/114 21.2 ± 2.1
87 45
— —
65 46 17 4
105 74 27 8
97 17 12 14 (10.6) 20 (15.1)
0 0 0 21 (9.8) 26 (11.2)
P 0.43 0.65 0.48 0.00 0.97
0.00
0.87 0.43
BMI indicates body mass index; ERCP, endoscopic retrograde cholangiopancreatography; F, female; M, male.
There was no significant difference between the 2 groups in conversion rates (3.0% vs. 3.5%, P = 0.35). The surgical parameters between the 2 groups were demonstrated in Table 2. There were no intraoperative transfusion requirements in both groups. The intraoperative blood loss was minimal in the majority of patients; the patients in group A had a significantly higher estimated blood loss than the patients in group B (85.5 vs. 30.4 mL; P < 0.001). The median operation duration was 1.9 hours and the operative time did not differ significantly between the 2 groups (2.1 vs. 1.9 h; P = 0.07). Laboratory tests on the first and third postoperative day were not statistically different between the 2 groups, despite a relative increase in the serum aminotransferase level observed in group A compared with that in group B (P = 0.11). The specific complications and patients’ number were listed in Table 3. There was no mortality in both groups. Perioperative complications arose in 33 (9.1%) patients (14 cases in group A and 19 cases in group B; P < 0.05). A total of 11 patients experienced minor bile leakage, which stopped spontaneously with extended peritoneal drainage (group A: 4.5%; group B: 3.8%; P = 0.61). Two patients each in groups A and B had postoperative bleeding. Both were successfully controlled and resolved by conservative management. According to Dindo Classification of surgical complications,18 no other postoperative major morbidity occurred, and all the patients were discharged in good health. The hospital stay was not significantly different for the groups A and B (4.2 vs. 4.0; P = 0.60). There were no significant differences between the 2 groups with respect to the incidence of pneumonia, incisional hematoma, acute pancreatitis, diarrhea, and acute biliary peritonitis after T-tube removal.
DISCUSSION The optimal management of CBD stones in the era of LC is still in debate. The choices range from conventional open procedure19 to mini-invasive surgery, such as ERCP4,5 and LCBDE.14,15 Conventional open CBD exploration is
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TABLE 2. Operative Characteristics and Postoperative Hematology Examination
Surgical Parameters Operative time (h) Blood loss (mL) Conversion rate [n (%)] Hospital stay (d) T-tube drainage [n (%)] Primary suture [n (%)] Analgesia requirements (dolantin) (mg) Approach to choledocholithiasis Transcystic Direct choledochotomy VAS score Retained choledocholithiasis [n (%)] Hematology test (after 1-3 d) Bilirubin (mmol/L) Albumin (g/L) ALT (mmol/L) Prothrombin time (s)
Group A (n = 132)
Group B (n = 214)
P
2.1 ± 0.6 1.9 ± 1.4 0.07 85.5 ± 23.6 30.4 ± 15.5 < 0.001 7 (5.3) 13 (6.1) 0.77 4.2 ± 3.6 4.0 ± 3.2 0.60 84 (63.6) 127 (59.3) 0.43 48 (36.4) 87 (41.7) 0.41 115.5 ± 55.8 110.5 ± 63 0.44 0.47 75 47 3.5 ± 2.2 11 (8.3)
130 84 3.2 ± 2.0 15 (7.1)
0.20 0.65
21.7 ± 13.5 35.8 ± 12.4 65.3 ± 20.6 11.4 ± 2.7
19.2 ± 18.4 37.2 ± 11.5 52.5 ± 20.2 10.8 ± 3.1
0.15 0.29 0.11 0.06
ALT indicates alanine aminotransferase; VAS, visual analog scale.
still widely used in our developing countries. However, such a surgical procedure is excessively invasive in terms of blood loss and wound pain. In the past few decades, ERCP clearance of CBD stones has gained universal acceptance and become the standard procedure for most choledocholithiasis patients, but it is likely to increase patient morbidity from ERCP failure and subsequent feared need for further surgery.4 Because of recent technological advances and improved surgical experience, LCBDE is routinely
TABLE 3. Number and Types of Complication Between the 2 Groups
Complications Total complications No. patients with complications [n (%)] Bile leak (grade IIIa) Ascities (grade I) Acute pancreatitis (grade II) Pulmonary inflammation (grade II) Incision hematoma (grade I) Diarrhea (grade II) Bleeding (grade IIIa) Acute biliary peritonitis after T-tube removal (grade II) Grade I total Grade II total Grade III total
Group A Group B (n = 132) (n = 214)
P
24 14 (10.6)
22 19 (8.8)
0.06 0.60
5 8 2 3 1 2 2 1
6 7 2 2 1 1 2 1
0.61 0.22 0.63 0.33 0.73 0.33 0.63 0.73
9 8 7
8 6 8
0.20 0.14 0.49
According to Clavien-Dindo classification of surgical complications. Grade 1 complications required no surgical or medicinal treatment; Grade 2 complications required medicinal therapy; Grade 3 complications required surgical, endoscopic, or radiologic treatment. Grades 1 and 2 were considered as minor complications, whereas grades 3-5 were considered as major complications.
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performed by surgeons at many centers worldwide.14,15 There is increasing evidence supporting this procedure to significantly reduce postoperative pain, hospital stay, and blood loss.20,21 However, the indications that preclude LCBDE are not clearly defined, and the efficacy and safety of LCBDE for patients with liver cirrhosis has not been well established. To date, there was no comparative study that compared LCBDE in cirrhotic and noncirrhotic patients. Hence, we conducted the first study to compare the postoperative course and complications of LCBDE in cirrhosis with those patients without cirrhosis. In summary, LCBDE performed in the cirrhosis group was associated with significantly higher amount of blood loss in comparison with that in noncirrhosis group. There were no significant differences between the 2 groups in operative time, analgesic requirements, visual analog scale pain score, hospital stay, and postoperative complications, respectively. The LCBDE procedure can be performed transcystically or by choledochotomy. A successful transcystic extraction of stones (eg, CBD) usually makes external biliary drainage unnecessary, and this approach is preferred whenever feasible, because it is the least invasive option and the least expensive.17 However, this approach may be limited by smaller stones and a duct that can be dilated to accept choledochoscope insertion. Otherwise, laparoscopic direct choledochotomy is an alternative method, but it may carry higher morbidity rates and increase hospital duration. To avoid these disadvantages and biliary complications, Ttube is performed. In the present study, the T-tube is placed into the CBD through the choledochotomy. The remainder of the opening CBD is closed with a 4-0 absorbable suture. After placement of the T-tube, a completion cholangiogram must be performed. The T-tube is tested by pushing fluid through it and verifying that there is no leak. If a T-tube is not going to be used, the entire choledochotomy is closed primarily. A T-tube x-ray cholangiogram is obtained before removing the tube 2 to 4 weeks after surgery. Currently, a systematic review and meta-analysis of primary closure versus T-tube drainage after CBD exploration for choledocholithiasis conducted by Zhu et al22 had been published, which demonstrated that the primary closure might be as effective as T-tube drainage after choledochotomy in the prevention of the development of postoperative complications. In the current study, there were no significant differences between the primary closure and T-tube drainage groups in surgery-related complications and retained choledocholithiasis rates. Compared with conventional open CBD exploration, the advantages (including less bleeding, lower morbidity, and shorter hospital stay) of LCBDE for patients with symptomatic choledocholithiasis have been extensively published. However, its benefits and successful use for patients with cirrhosis are less well documented. There are several key issues that should be kept in mind when considering application of LCBDE in cirrhotic patients: (1) appropriate selection of candidates according to Child-Pugh classification, which is a means of predicting perioperative complications and is an independent risk factor in the multivariate analysis.16,23 In our study, all included patients were confirmed to Child A and Child B (216 patients were classified as Child class A cirrhotic and 130 patients were classified as Child class B cirrhotic), which was verified as an important factor during the course of the disorder between surgery and postoperative recovery; (2) maximally reducing bleeding is Copyright
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LCBDE for Choledocholithiasis
another issue of worthy concern: for patients with cirrhosis, careful attention to intraoperative bleeding from the liver bed and arteries during the procedure is necessary; (3) approach to choledocholithiasis: transcystic or direct choledochotomy. If technically feasible, the transcystic approach is preferred; otherwise, direct choledochotomy was used; (4) liver function deteriorated: Morino et al24 first described the phenomenon of the impairment of liver function after laparoscopic surgery. Thereafter, other authors reported similar outcomes.25,26 In our study, deterioration of liver function was present in both cirrhotic and noncirrhotic patients who underwent LCBDE. However, there was no significant difference between the 2 groups (Table 2). The reason for liver function impairment in liver cirrhosis after laparoscopic surgery remains unknown and requires further investigation. In conclusion, the current series demonstrates that LCBDE in selected patients with Child-Pugh A and B cirrhosis has acceptable minor complications and comparable postoperative courses compared with patients without cirrhosis. LCBDE is a technically feasible, safe, and effective procedure for cirrhosis. Liver cirrhosis was not a contraindication of LCBDE. In the future, we believe that more and more cirrhotic patients may benefit from the minimally invasive surgical procedure of LCBDE. This study was retrospective in nature; however, further investigation in a randomized setting is needed.
REFERENCES 1. Hungness ES, Soper NJ. Management of common bile duct stones. J Gastrointest Surg. 2006;10:612–619. 2. Williams EJ, Green J, Beckingham I, et al. Guidelines on the management of common bile duct stones. Gut. 2008;57: 1004–1021. 3. Tinoco R, Tinoco A, El-Kadre L, et al. Laparoscopic common bile duct exploration. Ann Surg. 2008;24:674–679. 4. Nathanson LK, O’Rourke NA, Martin IJ, et al. Postoperative ERCP versus laparoscopic choledochotomy for clearance of selected bile duct calculi: a randomized trial. Ann Surg. 2005;242:188–192. 5. Yu W, Li W, Wang Z, et al. Early percutaneous transhepatic gallbladder drainage compared with endoscopic retrograde cholangiopancreatography and papillotomy treatment for severe gallstone associated acute pancreatitis. Postgrad Med J. 2007;83:187–191. 6. Ney MV, Maluf-Filho F, Sakai P, et al. Echo-endoscopy versus endoscopic retrograde cholangiography for the diagnosis of choledocholithiasis: the influence of the size of the stone and diameter of the common bile duct. Arq Gastroenterol. 2005;42:239–243. 7. Talar-Wojnarowska R, Szulc G, Woz´niak B, et al. Assessment of frequency and safety of endoscopic retrograde cholangiopancreatography in patients over 80 years of age. Pol Arch Med Wewn. 2009;19:136–140. 8. Fritz E, Kirchgatterer A, Hubner D, et al. ERCP is safe and effective in patients 80 years of age and older compared with younger patients. Gastrointest Endosc. 2006;64:899–905. 9. Chen CM, Tay KH, Hoe MN, et al. Endoscopic retrograde cholangiopancreatography management of common bile duct stones in a surgical unit. ANZ J Surg. 2005;75:1070–1072. 10. Wang P, Li ZS, Liu F, et al. Risk factors for ERCP-related complications: a prospective multicenter study. Am J Gastroenterol. 2009;104:31–40. 11. Qiu J, Pankaj P, Jiang H, et al. Laparoscopy versus open distal gastrectomy for advanced gastric cancer: a systematic review and meta-analysis. Surg Laparosc Endosc Percutan Tech. 2013; 23:1–7.
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12. Qiu J, Chen S, Pankaj P, et al. Laparoscopic hepatectomy for hepatic colorectal metastases—a retrospective comparative cohort analysis and literature review. PLoS One. 2013; 8:e60153. 13. Taylor EF, Thomas JD, Whitehouse LE, et al. Populationbased study of laparoscopic colorectal cancer surgery 20062008. Br J Surg. 2013;100:553–560. 14. Lo HC, Wang YC, Huang JC, et al. Laparoscopic common bile duct exploration in patients with complicated cholecystitis: a safety and feasibility study. World J Surg. 2012;36: 2455–2460. 15. Paik KY, Kim EK. Laparoscopic common bile duct exploration after unsuccessful endoscopic stone removal. J Laparoendosc Adv Surg Tech A. 2013;23:137–140. 16. Hamad MA, Thabet M, Badawy A, et al. Laparoscopic versus open cholecystectomy in patients with liver cirrhosis: a prospective randomized study. J Laparoendosc Adv Surg Tech A. 2010;20:405–409. 17. Verbesey JE, Birkett DH. Common bile duct exploration for choledocholithiasis. Surg Clin North Am. 2008;88:1315–1328. 18. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and result of a survey. Ann Surg. 2004;240: 205–213.
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19. Kusano T, Isa T, Shimoji H, et al. Results of retrograde transhepatic biliary drainage after a common bile duct exploration for choledocholithiasis. Hepatogastroenterology. 1999;46:2776–2780. 20. Chander J, Vindal A, Lal P, et al. Laparoscopic management of CBD stones: an Indian experience. Surg Endosc. 2011;25:172–181. 21. Hanif F, Ahmed Z, Samie MA, et al. Laparoscopic transcystic bile duct exploration: the treatment of first choice for common bile duct stones. Surg Endosc. 2010;24:1552–1556. 22. Zhu QD, Tao CL, Zhou MT, et al. Primary closure versus T-tube drainage after common bile duct exploration for choledocholothiasis. Langenbecks Arch Surg. 2011;396:53–62. 23. El-Awadi S, El-Nakeeb A, Youssef T, et al. Laparoscopic versus open cholecystectomy in cirrhotic patients: a prospective randomized study. Int J Surg. 2009;7:66–69. 24. Morino M, Giraudo G, Festa V. Alterations in hepatic function during laparoscopic surgery. An experimental clinical study. Surg Endosc. 1998;12:968–972. 25. Omari A, Bani-Hani KE. Effect of carbon dioxide pneumoperitoneum on liver function following laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A. 2007;17:419–424. 26. Zhu JH, Wang YD, Ye ZY, et al. Laparoscopic versus open splenectomy for hypersplenism secondary to liver cirrhosis. Surg Laparosc Endosc Percutan Tech. 2009;19:258–262.
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Laparoscopic Common Bile Duct Exploration in Cirrhotic Patients With Choledocholithiasis Jianguo Qiu, MD,* Haichao Yuan, MD,w Shuting Chen, MD,* and Hong Wu, MD, PhD*
Background and Aims: Although laparoscopic common bile duct exploration (LCBDE) has become the standard procedure for most choledocholithiasis patients, the application of this procedure to liver cirrhosis is still in debate. The aim of the current study was to evaluate the feasibility and safety of LCBDE in choledocholithiasis patients with compensated liver cirrhosis. Patients and Methods: From January 2006 to December 2012, 346 LCBDEs were performed in our hospital. According to the previously defined liver condition, the patients were divided into group A (liver cirrhosis, n = 132) and group B (without cirrhosis, n = 214). The perioperative data for the 2 groups were retrospectively reviewed and compared. Results: LCBDE was successfully completed in 326 patients. Conversion from laparoscopic to open surgery was necessary for 20 patients (5.7%) mainly because of hemorrhage (5, 25%) and severe adhesions (8, 40%). A T-tube was placed in 211 patients (64.7%), and primary closure was performed in 115 (35.3%) patients. There was a significant difference for groups A and B in terms of intraoperative blood loss (85 vs. 35 mL; P < 0.01). However, the 2 groups showed no significant differences with respect to the mean operation time (2.1 vs. 1.9 h; P = 0.07), complication rates (10.6% vs. 8.8%; P = 0.6), mean hospital stay (4.2 vs. 4.0 d; P = 0.6), conversion rate (5.3% vs. 6.1%; P = 0.77), and retained choledocholithiasis rate (8.3% vs. 7.1%; P = 0.65). There was no mortality in both groups.
diagnosed during cholecystectomy had not been previously detected.3 Since the first introduction of endoscopic retrograde cholangiopancreatography (ERCP) was reported in 1974, it has gained universal acceptance,4–6 especially in older patients.7,8 However, ERCP has some disadvantages, including acute pancreatitis and as high as 10% to 25% failure rate.9,10 Progress in laparoscopic technology and increased experience in laparoscopic procedures including laparoscopic hepatectomy11–13 enabled surgeons to perform laparoscopic common bile duct exploration (LCBDE), which reduced postsurgical pain, hospital stay, and period of disability.14,15 LCBDE has become the gold standard for the removal of CBD stones in the patients with unsuccessful ERCP procedures; however, the safety and efficacy of LCBDE in patients with liver cirrhosis has not been established. In the current study, we present the results of a retrospective study of our experience in a cohort of 364 consecutive patients from our department and evaluate the feasibility and safety of LCBDE in 134 cirrhotic Child A and B patients by comparing LCBDE in 214 patients who were without cirrhosis.
Conclusions: LCBDE is a feasible, effective, and safe surgical procedure for choledocholithiasis patients with compensated cirrhosis. Key Words: laparoscopy, cholecystectomy, common bile duct, liver, cirrhosis
(J Clin Gastroenterol 2015;49:132–136)
C
ommon bile duct (CBD) stones represent a significant danger to patients and are the most frequent complications of cholecystolithiasis and occur in 10% to 15% of patients.1,2 The diagnosis of CBD stones may be achieved by the preoperative examination including ultrasonography (USG), magnetic resonance imaging (MRI), and magnetic resonance cholangiopancreatography (MRCP). However, it is suspected that >30% of the cholecystolithiasis
Received for publication August 26, 2013; accepted December 1, 2013. From the Departments of *Hepatobiliary Pancreatic Surgery; and wUrology Surgery, West China Hospital, Sichuan University, Cheng du, Sichuan Province, China. H.W.: designed the study. J.Q.: wrote the manuscript. S.C. and H.Y.: analyzed the data and interpreted the results. Supported by Science and Technology Support Project of Sichuan Province (2009FC0093). The authors declare that they have nothing to disclose. Reprints: Hong Wu, MD, PhD, Department of Hepatobiliary Pancreatic Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China (e-mail: [email protected]). Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved.
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PATIENTS AND METHODS Patients The protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki as reflected in a priori approval by the Clinical Trial Ethics Committee of West China Hospital, Sichuan University. From January 2006 to December 2012, a total of 3658 laparoscopic cholecystectomies (LC) were performed at our hospital. Overall, 346 consecutive patients accompanied with choledocholithiasis underwent LCBDE. According to previously defined liver condition, the patients were divided into group A (liver cirrhosis, n = 132) and group B (without cirrhosis, n = 214). Data of each patient were retrospectively collected by chart review and analyzed in terms of demographic characteristics, surgical outcomes (including operation time, estimated blood loss, and conversion rate), postoperative variables (including hospital stays, analgesia requirements, complications, and retained choledocholithiasis rate), and hematology tests at first and third postoperative day (including serum bilirubin, transaminases, alkaline phosphatase, serum albumin, and prothrombin time). Complications or death occurring during the same hospitalization or within 90 days after operation were defined as postoperative complications and postoperative mortality, respectively. Operating time was the number of minutes for which the operation continues. Hospital stay was defined as the number of days from the date of J Clin Gastroenterol
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operation to discharge. Postoperative pain scores were assessed using a standard 10 cm visual analog scale with options ranging from 0 (no pain) to 10 (worst pain).
Preoperative Evaluation The preoperative evaluation involved history-taking; physical examination; abdominal USG, MRI, or MRCP; and laboratory tests. Liver cirrhosis was diagnosed from using abdominal USG that showed multiple nodular irregularities of the liver surface, small liver size, echo coarseness, or ascites, splenomegaly, and esophageal varices.16 Cirrhosis was further confirmed by the intraoperative USG or liver biopsy.
Indications and Operative Techniques of LCBDE In accordance with our protocol for the management of CBD stone (Fig. 1), LCBDE is performed during LC procedure for all cases in which CBD stones can be confirmed by intraoperative cholangiogram (IOC) or laparoscopic intraoperative ultrasound (LIOU). Otherwise, the following situations were also warranted LCBDE in some patients: (1) unexplained liver damage; (2) sonographic, endoscopic, or radiographic evidence of CBD stones; (3) a dilated bile duct; or (4) a history of biliary pancreatitis. The comprehensive IOC approaches utilized have been detailed elsewhere.3,17 IOC was performed at the right midclavicular line using a 5-Fr needle. An olive-tip ureteral catheter attached to a metal wire was introduced through the cystic duct.17 Whenever this procedure was not possible, LIOU was used. After confirmation of the presence of CBD stones, a 5-mm trocar was inserted into the same place in which the IOC catheter was introduced. In the current study, LCBDE was mainly accomplished through the cystic duct or through a choledochotomy after cholecystectomy. If CBD stones are detected, primary extraction through the cystic duct is intended. We have no experience with balloon dilatation of the cystic duct. If transcystic retrieval cannot be achieved because of the size or position of stones, the stones are removed through direct choledochotomy.
LCBDE for Choledocholithiasis
For choledochotomy procedure, a longitudinal incision on the cystic duct was made onto the anterior surface of the CBD. The choledochoscope was inserted through the midclavicular port and guided into the CBD. Once a CBD stone is visualized, a basket is inserted into the working channel of the choledochoscope and the stone is captured with forceps. Then the basket and entrapped stone are pulled against the choledochoscope, and both the choledochoscope and basket are removed from the biliary system. If several stones are to be removed, it can be useful to collect the stones in a bag placed in the abdomen and that will be pulled out at the end of the procedure. Usually, if the stone has been cleared completely, there is no need to place a T-tube into the CBD.
Statistical Analysis All values were presented as mean ± SD, the w2 test or the Fisher exact test were used to evaluate the significant differences between 2 groups. A value of P < 0.05 was considered statistical significance. All analyses were performed using SPSS 16.0 statistical software.
RESULTS Since January 2006, CBD stones were detected by preoperative studies and IOS or LIOU in 346 of 3658 patients (9.46%) who underwent LC at West China Hospital, Sichuan University. Of those 346 patients, 86 were diagnosed with CBD stones only by IOS or LIOU during LC procedure, without preoperative suspicion of bile duct stones. The clinicopathologic characteristics of all included patients are summarized in Table 1. There were no significant differences between the 2 groups in demographic characteristics. Choledochotomy was successful in 40.8% of patients, whereas the transcystic approach was 59.2% successful. Conversion to laparotomy was necessary in 20 of the 346 patients (5.8%). The reasons for conversion included bleeding in the cystic artery (n = 3), right hepatic artery (n = 2), colon injury (n = 1), severe inflammation (n = 6), and difficult dissection to adhesions (n = 8).
FIGURE 1. The protocol for the laparoscopic management of common bile duct (CBD) stone at our hospital.
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TABLE 1. Patient Characteristic of all Included Patients
Parameters Total patients (n) Age (y) Sex (M/F) BMI (m3/kg) Child-Pugh Class (n) A B ASA status (n) I II III IV Cirrhosis etiology (n) Hepatitis B Hepatitis C Alcohol Previous biliary surgery [n (%)] Preoperative ERCP [n (%)]
Group A
Group B
132 45.3 ± 12.5 65/67 21.4 ± 2.8
214 46.7 ± 20.4 100/114 21.2 ± 2.1
87 45
— —
65 46 17 4
105 74 27 8
97 17 12 14 (10.6) 20 (15.1)
0 0 0 21 (9.8) 26 (11.2)
P 0.43 0.65 0.48 0.00 0.97
0.00
0.87 0.43
BMI indicates body mass index; ERCP, endoscopic retrograde cholangiopancreatography; F, female; M, male.
There was no significant difference between the 2 groups in conversion rates (3.0% vs. 3.5%, P = 0.35). The surgical parameters between the 2 groups were demonstrated in Table 2. There were no intraoperative transfusion requirements in both groups. The intraoperative blood loss was minimal in the majority of patients; the patients in group A had a significantly higher estimated blood loss than the patients in group B (85.5 vs. 30.4 mL; P < 0.001). The median operation duration was 1.9 hours and the operative time did not differ significantly between the 2 groups (2.1 vs. 1.9 h; P = 0.07). Laboratory tests on the first and third postoperative day were not statistically different between the 2 groups, despite a relative increase in the serum aminotransferase level observed in group A compared with that in group B (P = 0.11). The specific complications and patients’ number were listed in Table 3. There was no mortality in both groups. Perioperative complications arose in 33 (9.1%) patients (14 cases in group A and 19 cases in group B; P < 0.05). A total of 11 patients experienced minor bile leakage, which stopped spontaneously with extended peritoneal drainage (group A: 4.5%; group B: 3.8%; P = 0.61). Two patients each in groups A and B had postoperative bleeding. Both were successfully controlled and resolved by conservative management. According to Dindo Classification of surgical complications,18 no other postoperative major morbidity occurred, and all the patients were discharged in good health. The hospital stay was not significantly different for the groups A and B (4.2 vs. 4.0; P = 0.60). There were no significant differences between the 2 groups with respect to the incidence of pneumonia, incisional hematoma, acute pancreatitis, diarrhea, and acute biliary peritonitis after T-tube removal.
DISCUSSION The optimal management of CBD stones in the era of LC is still in debate. The choices range from conventional open procedure19 to mini-invasive surgery, such as ERCP4,5 and LCBDE.14,15 Conventional open CBD exploration is
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TABLE 2. Operative Characteristics and Postoperative Hematology Examination
Surgical Parameters Operative time (h) Blood loss (mL) Conversion rate [n (%)] Hospital stay (d) T-tube drainage [n (%)] Primary suture [n (%)] Analgesia requirements (dolantin) (mg) Approach to choledocholithiasis Transcystic Direct choledochotomy VAS score Retained choledocholithiasis [n (%)] Hematology test (after 1-3 d) Bilirubin (mmol/L) Albumin (g/L) ALT (mmol/L) Prothrombin time (s)
Group A (n = 132)
Group B (n = 214)
P
2.1 ± 0.6 1.9 ± 1.4 0.07 85.5 ± 23.6 30.4 ± 15.5 < 0.001 7 (5.3) 13 (6.1) 0.77 4.2 ± 3.6 4.0 ± 3.2 0.60 84 (63.6) 127 (59.3) 0.43 48 (36.4) 87 (41.7) 0.41 115.5 ± 55.8 110.5 ± 63 0.44 0.47 75 47 3.5 ± 2.2 11 (8.3)
130 84 3.2 ± 2.0 15 (7.1)
0.20 0.65
21.7 ± 13.5 35.8 ± 12.4 65.3 ± 20.6 11.4 ± 2.7
19.2 ± 18.4 37.2 ± 11.5 52.5 ± 20.2 10.8 ± 3.1
0.15 0.29 0.11 0.06
ALT indicates alanine aminotransferase; VAS, visual analog scale.
still widely used in our developing countries. However, such a surgical procedure is excessively invasive in terms of blood loss and wound pain. In the past few decades, ERCP clearance of CBD stones has gained universal acceptance and become the standard procedure for most choledocholithiasis patients, but it is likely to increase patient morbidity from ERCP failure and subsequent feared need for further surgery.4 Because of recent technological advances and improved surgical experience, LCBDE is routinely
TABLE 3. Number and Types of Complication Between the 2 Groups
Complications Total complications No. patients with complications [n (%)] Bile leak (grade IIIa) Ascities (grade I) Acute pancreatitis (grade II) Pulmonary inflammation (grade II) Incision hematoma (grade I) Diarrhea (grade II) Bleeding (grade IIIa) Acute biliary peritonitis after T-tube removal (grade II) Grade I total Grade II total Grade III total
Group A Group B (n = 132) (n = 214)
P
24 14 (10.6)
22 19 (8.8)
0.06 0.60
5 8 2 3 1 2 2 1
6 7 2 2 1 1 2 1
0.61 0.22 0.63 0.33 0.73 0.33 0.63 0.73
9 8 7
8 6 8
0.20 0.14 0.49
According to Clavien-Dindo classification of surgical complications. Grade 1 complications required no surgical or medicinal treatment; Grade 2 complications required medicinal therapy; Grade 3 complications required surgical, endoscopic, or radiologic treatment. Grades 1 and 2 were considered as minor complications, whereas grades 3-5 were considered as major complications.
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performed by surgeons at many centers worldwide.14,15 There is increasing evidence supporting this procedure to significantly reduce postoperative pain, hospital stay, and blood loss.20,21 However, the indications that preclude LCBDE are not clearly defined, and the efficacy and safety of LCBDE for patients with liver cirrhosis has not been well established. To date, there was no comparative study that compared LCBDE in cirrhotic and noncirrhotic patients. Hence, we conducted the first study to compare the postoperative course and complications of LCBDE in cirrhosis with those patients without cirrhosis. In summary, LCBDE performed in the cirrhosis group was associated with significantly higher amount of blood loss in comparison with that in noncirrhosis group. There were no significant differences between the 2 groups in operative time, analgesic requirements, visual analog scale pain score, hospital stay, and postoperative complications, respectively. The LCBDE procedure can be performed transcystically or by choledochotomy. A successful transcystic extraction of stones (eg, CBD) usually makes external biliary drainage unnecessary, and this approach is preferred whenever feasible, because it is the least invasive option and the least expensive.17 However, this approach may be limited by smaller stones and a duct that can be dilated to accept choledochoscope insertion. Otherwise, laparoscopic direct choledochotomy is an alternative method, but it may carry higher morbidity rates and increase hospital duration. To avoid these disadvantages and biliary complications, Ttube is performed. In the present study, the T-tube is placed into the CBD through the choledochotomy. The remainder of the opening CBD is closed with a 4-0 absorbable suture. After placement of the T-tube, a completion cholangiogram must be performed. The T-tube is tested by pushing fluid through it and verifying that there is no leak. If a T-tube is not going to be used, the entire choledochotomy is closed primarily. A T-tube x-ray cholangiogram is obtained before removing the tube 2 to 4 weeks after surgery. Currently, a systematic review and meta-analysis of primary closure versus T-tube drainage after CBD exploration for choledocholithiasis conducted by Zhu et al22 had been published, which demonstrated that the primary closure might be as effective as T-tube drainage after choledochotomy in the prevention of the development of postoperative complications. In the current study, there were no significant differences between the primary closure and T-tube drainage groups in surgery-related complications and retained choledocholithiasis rates. Compared with conventional open CBD exploration, the advantages (including less bleeding, lower morbidity, and shorter hospital stay) of LCBDE for patients with symptomatic choledocholithiasis have been extensively published. However, its benefits and successful use for patients with cirrhosis are less well documented. There are several key issues that should be kept in mind when considering application of LCBDE in cirrhotic patients: (1) appropriate selection of candidates according to Child-Pugh classification, which is a means of predicting perioperative complications and is an independent risk factor in the multivariate analysis.16,23 In our study, all included patients were confirmed to Child A and Child B (216 patients were classified as Child class A cirrhotic and 130 patients were classified as Child class B cirrhotic), which was verified as an important factor during the course of the disorder between surgery and postoperative recovery; (2) maximally reducing bleeding is Copyright
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another issue of worthy concern: for patients with cirrhosis, careful attention to intraoperative bleeding from the liver bed and arteries during the procedure is necessary; (3) approach to choledocholithiasis: transcystic or direct choledochotomy. If technically feasible, the transcystic approach is preferred; otherwise, direct choledochotomy was used; (4) liver function deteriorated: Morino et al24 first described the phenomenon of the impairment of liver function after laparoscopic surgery. Thereafter, other authors reported similar outcomes.25,26 In our study, deterioration of liver function was present in both cirrhotic and noncirrhotic patients who underwent LCBDE. However, there was no significant difference between the 2 groups (Table 2). The reason for liver function impairment in liver cirrhosis after laparoscopic surgery remains unknown and requires further investigation. In conclusion, the current series demonstrates that LCBDE in selected patients with Child-Pugh A and B cirrhosis has acceptable minor complications and comparable postoperative courses compared with patients without cirrhosis. LCBDE is a technically feasible, safe, and effective procedure for cirrhosis. Liver cirrhosis was not a contraindication of LCBDE. In the future, we believe that more and more cirrhotic patients may benefit from the minimally invasive surgical procedure of LCBDE. This study was retrospective in nature; however, further investigation in a randomized setting is needed.
REFERENCES 1. Hungness ES, Soper NJ. Management of common bile duct stones. J Gastrointest Surg. 2006;10:612–619. 2. Williams EJ, Green J, Beckingham I, et al. Guidelines on the management of common bile duct stones. Gut. 2008;57: 1004–1021. 3. Tinoco R, Tinoco A, El-Kadre L, et al. Laparoscopic common bile duct exploration. Ann Surg. 2008;24:674–679. 4. Nathanson LK, O’Rourke NA, Martin IJ, et al. Postoperative ERCP versus laparoscopic choledochotomy for clearance of selected bile duct calculi: a randomized trial. Ann Surg. 2005;242:188–192. 5. Yu W, Li W, Wang Z, et al. Early percutaneous transhepatic gallbladder drainage compared with endoscopic retrograde cholangiopancreatography and papillotomy treatment for severe gallstone associated acute pancreatitis. Postgrad Med J. 2007;83:187–191. 6. Ney MV, Maluf-Filho F, Sakai P, et al. Echo-endoscopy versus endoscopic retrograde cholangiography for the diagnosis of choledocholithiasis: the influence of the size of the stone and diameter of the common bile duct. Arq Gastroenterol. 2005;42:239–243. 7. Talar-Wojnarowska R, Szulc G, Woz´niak B, et al. Assessment of frequency and safety of endoscopic retrograde cholangiopancreatography in patients over 80 years of age. Pol Arch Med Wewn. 2009;19:136–140. 8. Fritz E, Kirchgatterer A, Hubner D, et al. ERCP is safe and effective in patients 80 years of age and older compared with younger patients. Gastrointest Endosc. 2006;64:899–905. 9. Chen CM, Tay KH, Hoe MN, et al. Endoscopic retrograde cholangiopancreatography management of common bile duct stones in a surgical unit. ANZ J Surg. 2005;75:1070–1072. 10. Wang P, Li ZS, Liu F, et al. Risk factors for ERCP-related complications: a prospective multicenter study. Am J Gastroenterol. 2009;104:31–40. 11. Qiu J, Pankaj P, Jiang H, et al. Laparoscopy versus open distal gastrectomy for advanced gastric cancer: a systematic review and meta-analysis. Surg Laparosc Endosc Percutan Tech. 2013; 23:1–7.
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12. Qiu J, Chen S, Pankaj P, et al. Laparoscopic hepatectomy for hepatic colorectal metastases—a retrospective comparative cohort analysis and literature review. PLoS One. 2013; 8:e60153. 13. Taylor EF, Thomas JD, Whitehouse LE, et al. Populationbased study of laparoscopic colorectal cancer surgery 20062008. Br J Surg. 2013;100:553–560. 14. Lo HC, Wang YC, Huang JC, et al. Laparoscopic common bile duct exploration in patients with complicated cholecystitis: a safety and feasibility study. World J Surg. 2012;36: 2455–2460. 15. Paik KY, Kim EK. Laparoscopic common bile duct exploration after unsuccessful endoscopic stone removal. J Laparoendosc Adv Surg Tech A. 2013;23:137–140. 16. Hamad MA, Thabet M, Badawy A, et al. Laparoscopic versus open cholecystectomy in patients with liver cirrhosis: a prospective randomized study. J Laparoendosc Adv Surg Tech A. 2010;20:405–409. 17. Verbesey JE, Birkett DH. Common bile duct exploration for choledocholithiasis. Surg Clin North Am. 2008;88:1315–1328. 18. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and result of a survey. Ann Surg. 2004;240: 205–213.
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19. Kusano T, Isa T, Shimoji H, et al. Results of retrograde transhepatic biliary drainage after a common bile duct exploration for choledocholithiasis. Hepatogastroenterology. 1999;46:2776–2780. 20. Chander J, Vindal A, Lal P, et al. Laparoscopic management of CBD stones: an Indian experience. Surg Endosc. 2011;25:172–181. 21. Hanif F, Ahmed Z, Samie MA, et al. Laparoscopic transcystic bile duct exploration: the treatment of first choice for common bile duct stones. Surg Endosc. 2010;24:1552–1556. 22. Zhu QD, Tao CL, Zhou MT, et al. Primary closure versus T-tube drainage after common bile duct exploration for choledocholothiasis. Langenbecks Arch Surg. 2011;396:53–62. 23. El-Awadi S, El-Nakeeb A, Youssef T, et al. Laparoscopic versus open cholecystectomy in cirrhotic patients: a prospective randomized study. Int J Surg. 2009;7:66–69. 24. Morino M, Giraudo G, Festa V. Alterations in hepatic function during laparoscopic surgery. An experimental clinical study. Surg Endosc. 1998;12:968–972. 25. Omari A, Bani-Hani KE. Effect of carbon dioxide pneumoperitoneum on liver function following laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A. 2007;17:419–424. 26. Zhu JH, Wang YD, Ye ZY, et al. Laparoscopic versus open splenectomy for hypersplenism secondary to liver cirrhosis. Surg Laparosc Endosc Percutan Tech. 2009;19:258–262.
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