Abstract
Objective:
To compare the safety and feasibility of T-tube drainage and primary suture after laparoscopy combined with choledochoscopy in the treatment of secondary choledocholithiasis.
Methods:
The clinical data of patients who underwent laparoscopic choledochoscopy combined with choledochoscopic common bile duct exploration (LCBDE) for secondary choledocholithiasis from June 2015 to June 2020 were analyzed retrospectively. According to the different treatment method of common bile duct (CBD) incision, the patients were divided into a T-tube drainage group and a primary suture group. The preoperative clinical characteristics, results of preoperative liver function tests (LFTs), LFTs on the first day after the operation and the fourth day after the operation, operation time, intraoperative bleeding, postoperative complications, and times of postoperative hospital stay were compared between the two groups.
Results:
There was no significant difference in preoperative clinical data, preoperative LFTs, and postoperative complications between the two groups (P > .05). However, primary suture demonstrated significant advantages (P < .05) in terms of the operation time, intraoperative blood loss, postoperative hospital stay, and other related factors. Bilirubin levels on the first day after the operation and the fourth day after the operation between the two groups suggested that T-tube drainage reduces bilirubin in the short term, but that long-term bilirubin draining is similar between the two strategies. Univariate and multivariate analyses showed that choledochal diameter less than 8 mm was an independent risk factor for bile leakage.
Conclusions:
Laparoscopy combined with intraoperative choledochoscopic CBD exploration is superior to T-tube drainage in terms of the operation time, intraoperative blood loss, and postoperative hospital stay. The ability of reducing bilirubin by traditional T-tube drainage is indeed better than that of primary suture in the early stage after operation, but there is no difference in long-term outcome between the two groups. Choledochal diameter ≤8 mm was an independent risk factor for bile leakage. To summarize, LCBDEs primary suture for secondary choledocholithiasis is safe and feasible.
Introduction
Simple choledocholithiasis typically occurs secondary to cholecystolithiasis, and it represents the most impactful complication of cholecystolithiasis. The incidence of choledocholithiasis in patients with symptomatic cholecystolithiasis is 10%–15%, and it is more common in older patients (aged >70 years). Choledocholithiasis may manifest with the unique Charcot's triad of symptoms associated with biliary obstruction, epigastric pain, chills and fever, and jaundice, and it may even result in acute biliary pancreatitis. If biliary obstruction exists for an extended period, it may induce liver cirrhosis and seriously affect the patient's quality of life. There are many methods for the treatment of choledocholithiasis, such as open common bile duct (CBD) exploration and T-tube drainage. The development of laparoscopic technology has led to the implementation of laparoscopic common bile duct exploration (LCBDE), which can reduce trauma to the bile duct because of its optical magnification, direct visualization, and finer instruments, and LCBDE has gradually replaced laparotomy and become the first choice for surgical treatment of choledocholithiasis.1–3
In the past, T-tube drainage has been used to enable postoperative CBD decompression and to facilitate the removal of residual stones. However, it is now recognized that T-tube usage can lead to significant complications, including electrolyte disturbance, localized pain, biliary peritonitis, wound infection, bile duct stricture, and bile leakage, and these complications can be complicated if the T-tube slips prematurely. In addition, the T-tube needs to be carried for a long time before removal, which increases patient inconvenience and negatively impacts their quality of life.4,5 To avoid these complications, Halste described the use of primary suture after open CBD exploration as early as 1917, 6 and the debate between the use of primary suture or indwelling T-tube drainage continues.
However, there are no clear data to support the preferential usage of one technique or the other. Therefore, we retrospectively analyzed the clinical and follow-up data of patients from 2015 to 2020 who underwent T-tube drainage and primary suture after laparoscopy combined with choledochoscopic CBD exploration because of secondary choledocholithiasis. Postoperative liver function tests (LFTs) and postoperative complications were compared between the two groups to analyze the relative safety of primary suture.
Materials and Methods
Patients and methods
This study retrospectively analyzed 228 cases of cholecystolithiasis complicated with choledocholithiasis (secondary choledocholithiasis) who successfully received laparoscopy combined with choledochoscopic CBD exploration in the Department of Hepatobiliary Surgery of the Affiliated Hospital of Southwest Medical University between June 2015 and December 2020. Among them, 158 cases were treated with T-tube drainage and 70 cases with primary suture. Due to failure to meet the inclusion criteria, lack of data, or failure of follow-up, data from 153 patients treated with T-tube drainage and 67 patients with primary suture were included. The characteristics of patients before surgical procedures are shown in Table 1. All operations were performed by qualified and experienced doctors. The median follow-up time of the T-tube drainage group was 20 months (from 6 to 35 months). The median follow-up time of the primary suture group was 19 months (from 6 to 35 months). All patients enrolled met the following inclusion conditions: (1) Presence of simple choledocholithiasis with or without cholecystolithiasis and without complicated biliary calculi such as hepatolithiasis was confirmed by preoperative B-scan ultrasonography or magnetic resonance cholangiopancreatography and intraoperative choledochoscopy. (2) Operative observation confirmed that the biliary wall was in good condition, without obvious edema, suppuration, necrosis or deformity, and no stricture or obstruction of the lower end of the CBD. (3) After choledochoscopy and stone extraction, surgeons confirmed that there were no stones in the CBD, the common hepatic duct, the left and right hepatic bile ducts, and other sites that could be explored by choledochoscopy. (4) Patients did not present with viral hepatitis, liver cirrhosis, liver cancer, or other liver diseases. (5) There was no previous history of biliary surgery or endoscopic retrograde cholangiopancreatography (ERCP) treatment. If the above basic conditions were not met, even though the operation may have been successful, the introduced variables may have affected the interpretation of some postoperative clinical data.
Comparison of Preoperative General Conditions, Clinical Features, and Liver Function Tests Between the Two Groups
All P-values in the Table 1 are not less than 0.5.
ALP, alkaline phosphatase; ALT, alanine transaminase; AST, aspartate transaminase; CBD, common bile duct; DBIL, direct bilirubin; GGT, gamma-glutamyl transferase; TBA, total bile acid; TBIL, total bilirubin.
Operative technique
All patients were placed in the supine position, routine disinfection was performed after anesthesia took effect, and the traditional four-hole operation method was used (Fig. 1). An SU piercing hole of ∼10 mm was positioned at the upper edge of the navel. A 10 mm SX hole was positioned below the xiphoid process. A 5 mm MC hole was positioned at the midline of the right clavicle. A 5 mm auxiliary hole was positioned near the right axillary front. In some cases, another auxiliary hole was made at the midline of the left clavicle to help expose the surgical site. The operating table was adjusted so that the head was elevated above the feet, and it was tilted to the left to help expose the triangular area of the gallbladder. A pneumoperitoneum was established with carbon dioxide, and the pressure was maintained at ∼12–13 mmHg. The gallbladder triangle was separated, and the cystic duct and cystic artery were completely exposed as completely as possible. The cystic duct was clamped ∼0.5 cm away from the CBD (Fig. 2a). Upon encountering the gallbladder, the integrity of the organ was ensured, and the cystic duct was clamped completely to prevent bile from flowing into the abdominal cavity and to prevent stones in the gallbladder from continuing to flow into the CBD. The surface of the serous membrane of the exposed CBD was cut open, and the location of the CBD was confirmed. The CBD was cut longitudinally along the front wall. A choledochoscope (Olympus, Tokyo, Japan) was inserted through the SX hole to facilitate the determination of the size, location, and quantity of stones. Stones were typically removed with a Dormia basket. For large stones, electro-hydraulic lithotripsy was frequently necessary to reduce stone size. After all the stones were removed, choledochoscopy was used to determine whether the bile duct was narrow and unobstructed. In the T-tube drainage group, different types of T-tubes were inserted into the CBD according to the diameter of the CBD, and then, the bile duct wall was sutured intermittently with polydioxanone sutures (4-0 PDS), and the T-tube was fixed. Any bile leakage was detected by injecting normal saline into the T-tube, and the T-tube was drawn out from the MC hole. For the primary suture group, the bile duct wall was sutured with 4-0 PDS simply and intermittently, with a margin of 2.0 mm and a needle distance of ∼2.0 mm (Fig. 2b, c), and bile leakage was detected with endoscopic gauze. Subsequently, the gallbladder was removed according to the routine method. Finally, the abdominal cavity was washed, and the indwelling drainage tube was placed in the Winslow hole to exit through the right auxiliary hole.

Schematic diagram demonstrating the port placement for a laparoscopic bile duct exploration. The patient is placed in the supine position. Color images are available online.

Example of a CBD exploratory surgery.
Outcomes and follow-up
The basic clinical data of the two groups before the operation were compared. These data included age, sex, history of diabetes and hypertension, cholangitis and pancreatitis at hospitalization, CBD diameter, and results of preoperative LFTs such as alanine transaminase (ALT), aspartate transaminase (AST), total bilirubin (TBIL), direct bilirubin (DBIL), gamma-glutamyl transferase (GGT), alkaline phosphatase (ALP), and total bile acid (TBA). Comparisons of intraoperative conditions, including operation time and intraoperative blood loss, were also performed. The LFTs were compared between the two groups on the first day after the operation and the fourth day after the operation. Additional data included length of postoperative hospital stay, biliary leakage, biliary residual stones, and biliary stricture. Univariate and multivariate analyses were performed on the cases of postoperative bile leakage to examine the risk factors of bile leakage.
Statistical methods
The data were analyzed by the SPSS 25 Software. Numerical values are expressed as percentages and were compared using chi-square test (χ 2 test). The Kolmogorov–Smirnov Z test was used to determine whether the data in each group were normally distributed. Normally distributed data are expressed as mean ± standard deviation, and t-tests were used to compare the two groups. Measurement data that did not conform to the normal distribution are expressed as M (P25, P75), and comparisons between the two groups were performed with the Mann–Whitney U test. Univariate and multivariate analyses of bile leakage were performed by logistic regression. Differences were considered statistically significant with P < .05.
Results
A comparison of the preoperative data for the two groups is shown in Table 1. No differences between indexes reached statistical significance. Results of the noted LFTs on the first day after the operation and the fourth day after the operation were also compared (Table 2). There was no significant difference in the results of ALT, AST, DBIL, GGT, ALP, and TBA. However, values of the two main indicators of biliary obstruction, TBIL and DBIL, were significantly higher in the primary suture group relative to the T-tube drainage group at both postoperative measurement points (P < .05 for all comparisons). In 23 patients (31.3%) of the primary suture group, these two values increased on the first day after the operation relative to their values before the operation, whereas these values increased in only 21 cases (11.1%) of the T-tube drainage group.
Comparison of Liver Function Tests on the First Day After the Operation and the Fourth Day After the Operation Between the Two Groups
P < .05.
ALP, alkaline phosphatase; ALT, alanine transaminase; AST, aspartate transaminase; DBIL, direct bilirubin; GGT, gamma-glutamyl transferase; LFT, liver function tests; TBA, total bile acid; TBIL, total bilirubin.
Because of the differences in these values, and because the difference of bilirubin at two time points is used to indicate the efficiency of bilirubin reduction, we investigated the bilirubin decrease in more detail. In comparing bilirubin values before the operation and on the first day after the operation, there was a significant difference between the T-tube drainage group and the primary suture group. Specifically, there was an elevated efficiency of bilirubin clearance in the T-tube drainage group relative to that of the primary suture group. However, there was no significant difference between the two groups in the efficiency of bilirubin clearance on the first day after the operation and the fourth day after the operation (Table 3). According to intraoperative conditions and postoperative follow-up investigations, there was no significant difference in the number of stones, residual stones, bile leakage, biliary stricture, or other major operative complications between the two groups (P > .05). The operation time, intraoperative blood loss, and length of hospital stay of the primary suture group were significantly lower than those of the T-tube drainage group (Table 4). To determine whether the occurrence of bile leakage was related to other analyzed factors, we performed single-factor and multi-factor analyses. Univariate analysis showed that bile leakage was related to the diameter of the CBD and the increase of postoperative bilirubin. The results of multivariate analysis showed that the diameter of CBD was an independent risk factor for bile leakage
Comparison of Bilirubin Reduction Rate Between the Two Groups of Patients with Postoperative Bilirubin Decrease
P < .05.
DBIL, direct bilirubin; TBIL, total bilirubin.
Comparison of Intraoperative, Postoperative, and Follow-Up Results Between the Two Groups
P < .05.
CBD, common bile duct.
Discussion
The pathogenesis of secondary choledocholithiasis is based on cholecystolithiasis secondary to choledocholithiasis, and T-tube drainage after choledocholithotomy and exploration has frequently been used in treatment protocols. The advantage of the T-tube procedure is that it can be used not only for postoperative biliary decompression but also for postoperative cholangiography to find any residual stones and to provide access for stone extraction through T-tubes.7–13 However, T-tube placement is associated with a number of challenges, such as bile leakage around T-tube, persistent biliary fistula, biliary peritonitis, accidental slippage or displacement of T-tube leading to CBD obstruction, and electrolyte disturbance.5,14 Some clinicians have proposed the alternative surgical method of one-stage suture after CBD exploration. The biggest concern for primary suture comes from the increase of postoperative biliary pressure, which may lead to biliary fistula and serious biliary peritonitis. Another concern is that it is not as easy to deal with early postoperative biliary residual stones as with T-tube indwelling. However, for these two problems, several studies4,14–19 provide evidence that there is no difference in the incidence of bile leakage and the incidence of biliary residual stones between primary suture and T-tube drainage. In addition, some studies have proposed that when primary suture is utilized, complicating choledocholithiasis can be resolved successfully by ERCP; in this case, however, complications related to ERCP must be considered. Therefore, the dispute about the advantages and disadvantages of the two surgical methods continues, and at present, most reports simply summarize and compare the postoperative complications of the two methods to evaluate the relative advantages and disadvantages. Little attention has been paid to the use of quantitative changes of the results of early postoperative LFTs as a mechanism to compare the two strategies.
To comprehensively evaluate the advantages and disadvantages of primary suture and indwelling T-tube drainage after CBD exploration, we not only compared the preoperative basic clinical data, intraoperative conditions, and postoperative complications between the two groups but also compared the results of LFTs between the two groups before and after operation. Among the examined LFTs, postoperative serum liver enzyme indices (ALT and AST) 20 are considered to have no obvious clinical significance in patients with preoperatively abnormal liver function, and they can be affected by many factors; in our study, there was no significant difference in these values. TBA is the main component of bile and a good index to reflect hepatocyte damage and biliary obstruction. 21 Its specificity and sensitivity are better than traditional enzyme indices. Similarly, in a study involving 1002 patients, 22 ALP and GGT were considered to be independent predictors of cholecystolithiasis and secondary choledocholithiasis. But in this study, these three sets of data did not show statistical significance. Bilirubin concentrations are particularly important aspects of LFTs to consider in cases involving bile duct obstruction. In fact, increases of TBIL and DBIL have been shown to provide direct evidence of bile duct obstruction.23,24 In our study, while we found no difference in preoperative basic data and LFT results between the two groups, we did find significant postoperative differences in TBIL and DBIL between the two groups. Specifically, the TBIL and DBIL of primary suture patients were significantly higher than those of T-tube drainage patients. The reason for this difference may be that when using a choledochoscope to remove stones and suture the CBD, the duodenal papilla was stimulated, resulting in early postoperative edema of the duodenal papilla and CBD, and the primary suture may have blocked the outlet of the bile duct. These factors may also cause that in the primary suture group, early postoperative bilirubin levels were higher than they were preoperatively. Based on these results, we continued to analyze the bilirubin reduction efficiency in patients with postoperative bilirubin decrease. The decrease rate of bilirubin in the primary suture group was significantly lower than that in the T-tube drainage group over the short term: from preoperation to the first day after the operation. However, there was no significant difference in the decreasing rate of bilirubin between the two groups over the longer term, from the first day after the operation to the fourth day after the operation. This result further confirmed our analysis that after biliary edema and duodenal papilla edema gradually subsided, the drainage ability of primary suture becomes considerable. Based on this result, it is clear that the traditional T-tube technique does provide good drainage in the early stages after operation, which confirms the previously recognized advantages of T-tube placement.7.8,12 This effective drainage seems to play a positive role in preventing the occurrence of biliary fistula because it effectively reduces the pressure in the biliary tract. In addition, combined with the results of other studies, 25 our results suggest that for patients with persistent elevated bilirubin after operation, complications with residual biliary stones must not be ignored. We should fully consider whether LCBDE surgery is successful in removing all biliary calculi. In the patients with elevated postoperative bilirubin in this study, the bilirubin index decreased to lower than the preoperative level during hospitalization. Therefore, according to the long-term postoperative results, primary suture provides sufficient bile drainage ability.
In this study, there was no significant difference in the incidence of postoperative bile leakage between the two surgical methods (P > .05). This is consistent with the results observed by most other studies and analyses.15,19,26,27 Similarly, in this study, the incidence of biliary fistula in primary suture was 2.9%, which was basically consistent with the incidence of biliary fistula described by Khaled et al. 16 and Xiao et al., 19 and our noted incidence of biliary fistula is consistent with the 1.6%–7% rate found by Hua et al. 1 All the patients with biliary fistula in the two groups were relieved only by abdominal drainage and did not undergo other surgical treatment. Furthermore, to determine the risk factors of postoperative bile leakage, we carried out univariate and multivariate analyses. As shown in Table 5, the results of a univariate analysis showed that the diameter of the CBD and the increase of postoperative bilirubin were independent risk factors for bile leakage. Multivariate analysis showed that only CBD diameter was an independent risk factor for bile leakage, a finding that coincided with that of Hua et al. and Khaled et al. that leakage was more likely to occur with a CBD diameter smaller than 8 mm. Although the multivariate analysis here suggests that the increase of postoperative bilirubin is not an independent risk factor for the incidence of bile leakage, this factor does show statistical significance in univariate analysis. This may suggest that the occurrence of bile leakage is closely related to the increase of CBD pressure after operation; however, we would need more cases to support this claim. According to previous work27,28 and the results of postoperative LFTs discussed in this study, postoperative T-tube drainage has a better effect on reducing CBD pressure. However, according to the results of various studies, differences in incidence of bile leakage are difficult to detect between patients treated with T-tube primary suture. Notably, however, in this study, bile leakage correlated with increases in bilirubin levels after operation. In other words, whether T-tube or primary suture was used in surgery, there was an increase in bilirubin after an operation, and this increase reflected the impact of increased biliary tract pressure on bile leakage. Of course, our operations are performed by experienced doctors, and more experienced doctors can reduce the risk of bile leakage, but it is a pity that we do not have enough time to explore the relationship between doctors' learning curve and the incidence of bile leakage. When the CBD was sutured during the operation, surgeons confirmed that there was no bile exudation from the incision, but due to the postoperative CBD wall edema caused by the operation, the originally tight incision loosened as the edema subsided, which led to bile extravasation. The loosening of the choledochal incision caused by the regression of edema will occur regardless of whether or not a T-tube is placed, so this effect may also explain why there is no difference in incidence of postoperative bile leakage between the T-tube drainage group and the primary suture group.
Univariate and Multivariate Analyses of Risk Factors for Bile Leakage
CBD, common bile duct.
Residual stones of biliary tract are another potential complication of LCBDE that cannot be ignored. In this study, 5 cases of biliary residual stones were found in the T-tube drainage group and two cases in the primary suture group. Therefore, in terms of the incidence of residual stones, T-tube drainage does not show a greater advantage over primary suture. We know that the previously recognized advantage of T-tube drainage involves reduction of biliary pressure, but another important advantage is that the T-tube can be used to treat early postoperative biliary residual stones. 13 However, among the 5 patients with choledochal residual stones found during follow-up in the T-tube drainage group in this study, the shortest time was 3 months after operation, when the T-tube had already been removed, the sinus formed by the T-tube had already collapsed, and the patient could no longer have stones removed through the sinus. These 5 patients ultimately chose ERCP to remove stones, whereas 2 patients with primary suture found residual stones at 5 and 13 months after operation. And in at least one previous study, it was mentioned that patients with T-tube drainage who presented with residual stones as identified by T-tube cholangiography when the T-tube was not removed still received ERCP to successfully remove the stone. 28 Similarly, patients with primary suture with residual stones also undergo ERCP to remove stones. 16 Therefore, in our experience, T-tube drainage does not show superiority compared with primary suture in this respect as removal of residual stones through T-tube is not a necessary choice, yet the patient's quality of life is greatly affected by the presence of the T-tube after the operation. But it is important to note that the deficiency of our study is that the number of patients with primary suture is relatively small and no patients with residual stones are found in the early stage after operation. So we do not completely deny the advantage of removing residual stones through T-tube sinus in the early stage after operation. Meanwhile, it is undeniable that indwelling T-tube drainage has unique advantages for patients with complex choledocholithiasis (i.e., choledocholithiasis with hepatolithiasis) because it can allow removal of stones from the biliary tree through the T-tube sinus after operation. This can limit the need for other surgical procedures for this type of patient.
There were no cases of choledochal stricture encountered in this study. This result is to be expected, according to the data from Khaled et al. in which only patients with CBD diameters of 7.1 mm experienced CBD stricture. 16 However, according to a different study, this one by Nathanson et al., 29 choledochal stricture occurs in patients with CBD diameters of 11 mm. In our study, there were 8 patients (5.22%) with CBD diameter of less than 8 mm in the T-tube drainage group, of which 4 patients (2.61%) had a CBD diameter of ∼7 mm, whereas 4 patients (5.97%) in the primary suture group had a CBD diameter of less than 8 mm, of which 2 patients (2.99%) had a CBD diameter of about 7 mm. We focused on the information of these 12 patients during later follow-up but found no evidence of significant choledochal stricture. Therefore, combined with the results of this study and previous literature, it seems that the small diameter of CBD is not the only risk factor for postoperative biliary stricture. We believe that postoperative choledochal stricture is also related to the basic physiological status of the biliary tract, such as severe biliary inflammation and edema. In addition, it may also be related to the quality of the incision and suture during the operation. We chose to cut the bile duct longitudinally during CBD exploration. In our study, CBD exploration was performed after longitudinal choledochotomy. Khaled et al. 16 explained that transverse choledocholithotomy simplifies the suture process and is less likely to cause choledochal stricture. Decker et al. 30 also reported that one-stage suture of LCBDE was performed by transverse incision of CBD, and there was no bile duct stricture after operation. However, to avoid cutting off the CBD during the transverse incision of the CBD, we still choose to cut the CBD longitudinally, which was similar to the procedure of Cai et al. 27 In this report, surgeons made the same longitudinal incision of the CBD and did not have choledochal stricture. Therefore, we propose that randomized controlled trials are still needed to explore the risk factors of choledochal stricture after LCBDE.
Considering operation time, intraoperative blood loss, and postoperative hospital stay, there is no doubt that primary suture is advantageous. These three results complement each other. In most cases, a shorter operation time means less bleeding, and the lack of an indwelling T-tube drainage will lead to the avoidance of potential T-tube-related complications, thus shortening the postoperative hospital stay. This is consistent with the results of many studies.19,26–28 From the point of view of the burden of the surgeon and the financial status of the patient, primary suture after LCBDE is superior to T-tube drainage.
A limitation of this study is that due to its retrospective and nonrandomized nature, the number of patients undergoing primary suture during the study period was relatively small. We, therefore, need additional rigorous randomized controlled trials to verify the advantages and disadvantages of both strategies. However, we first analyzed the efficiency of early postoperative T-tube drainage and primary suture in reducing bilirubin. We can observe that traditional T-tube drainage is indeed superior to primary suture in the short term, but there is no difference in the ability to reduce bilirubin in the long term after operation. At the same time, there is no difference in the incidence of postoperative complications between the two groups, but one-stage suture can not only reduce the time of operation and intraoperative bleeding but also reduce socioeconomic burdens on patients. To summarize, primary choledochal suture is feasible in LCBDE for the treatment of cholecystolithiasis secondary to choledocholithiasis.
Footnotes
Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received.
