Laparoscopic cholecystectomy (LC) is one of the most common surgeries in the United States, with over 700,000 performed per year [1]. LC was popularized in the 1980s after the advent of laparoscopy and quickly became the standard of care for symptomatic cholelithiasis. However, the rapid adoption of this procedure precluded detailed research into the technique at the time, and no level 1 studies were ever conducted to validate the overall safety of LC. More recently, a systematic review of laparoscopic versus open cholecystectomy found no difference in morbidity or mortality, but the authors were unable to find and include low-bias trials from the literature [2]. However, there have been many studies that expand the indications for LC. Systematic reviews examining the safety of LC in various circumstances, including acute cholecystitis, gallstone pancreatitis, and biliary colic, have encountered significant bias in many included studies [3,4,5].

Despite the popularity and wide use of laparoscopic cholecystectomy, the rate of serious complications with LC remains higher than seen with open cholecystectomy. One of the most serious intraoperative complications is common bile duct injury (CBDI), treatment of which may require additional procedures ranging from ERCP to surgical reconstruction and even liver transplantation. Previously, a 0.1–0.25% rate of CBDI was cited for open surgery [6, 7]; however, the rate of CBDI is generally acknowledged to be higher in LC. Various sources cite different rates of bile duct injury in LC, ranging from 0.3% [8, 9] to as high as 2.6% using NSQIP data [10]. In response to the increased rate of CBDI, Strasberg et al. introduced the Critical View of Safety in 1995, a technique designed to minimize the risk of injury to the extrahepatic bile ducts by identifying all structures within the triangle of Calot and that enter the gallbladder before dividing any [11]. This approach has three components: the triangle of Calot (bordered by the cystic duct, common hepatic duct, and inferior liver edge) is cleared, the lower third of the gallbladder is separated from the liver, and only two structures are seen entering the gallbladder. The common bile duct does not need to be exposed to achieve a Critical View, which could prevent injuries incurred while dissecting this structure. This technique has been widely disseminated, and the Society of Gastrointestinal and Endoscopic Surgeons (SAGES) Safe Cholecystectomy Task Force Program has encouraged more consistent implementation to improve the safety of LC (https://www.sages.org/safe-cholecystectomy-program/). However, the rate of CBDI during LC has not fallen to OC levels.

Common bile duct injury remains overall rare, though the true rate of CBDI after LC is difficult to determine. Definitions of bile duct injury vary within the literature, and study design has hindered the identification of risk factors for biliary injury. Many single-center series are too small to discover biliary injuries, given the low rate of occurrence; these studies often lack sufficient power to analyze complications. Larger cohorts studied by aggregating cases from ICD codes or examining cases referred to tertiary hepatobiliary centers may miss injuries that were repaired intraoperatively or not documented separately within the medical record.

NorthShore University HealthSystem consists of four teaching hospitals affiliated with the University of Chicago, and has a robust minimally invasive surgery practice, with an estimated 500–600 cholecystectomies performed per year and a mature electronic medical record dating to the year 2000. Our study sought to determine the prevalence of, and risk factors for, common bile duct injury during laparoscopic cholecystectomy at this four-hospital institution.

Materials and methods

This study was reported based on recommendations of the STROBE statement for reporting observational studies [12]. After institutional review board approval, 800 of approximately 3000 cholecystectomy cases performed at NorthShore between 2009 and 2015 were randomly selected. The electronic medical record was retrospectively reviewed to complete a database consisting of preoperative, intraoperative, and postoperative data. A data dictionary was created to ensure consistent data collection, and chart review strategies were designed to minimize missing data; any missing data were excluded from analysis. A single reviewer examined all operative notes, thereby including all cases of biliary injury regardless of severity, ICD code, or need for a second procedure.

Continuous variables were recorded as-is in the database and were not categorized. Cases where the gallbladder was removed only as part of a partial hepatectomy, with no history of gallbladder pathology, were excluded from the database. Intraoperative choledocholithiasis was determined by any intraoperative cholangiography or postop diagnosis of choledocholithiasis by the surgeon. Bile duct injuries were assigned a Strasberg class according to published standards [11] (Table 1). Intentional openings to the common bile duct, e.g., for laparoscopic common bile duct exploration, were not counted as biliary injuries and were analyzed as part of the no-injury cohort [11]. The Critical View of Safety was defined as per Strasberg [11, 13] and the SAGES Safe Cholecystectomy Task Force Program: (1) the triangle of Calot is fully cleared, (2) the lower third of the gallbladder is separated to expose the liver bed, and (3) only two structures are seen entering the gallbladder, with the liver bed visible, before any structure is divided. Operative reports where the surgeon chose and described a different method of dissection (e.g., fundus-first) or the surgery was converted to open before dissecting the triangle of Calot were recorded separately.

Table 1 Strasberg classification of biliary injury
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Differences in patient demographics, preoperative, and surgical characteristics were compared using non-parametric methods for small sample size (Fisher’s Exact test or the Wilcoxon Rank-Sum test). Logistic regression analysis was utilized to identify predictors of biliary injury. Factors with p < 0.10 on univariable analysis were entered into a multivariable logistic model. Either pathology or surgeon diagnosis of a disease was entered into the multivariable model, due to colinearity. Patients with missing data were excluded from logistic regression analysis. All statistical analysis was performed using SAS 9.3 (SAS Institute, Cary, NC). Statistical significance was defined as a p value <0.05.

Results

All 800 cases in the database were confirmed as eligible and included in this analysis. Of these 800 cases, cholangiography was performed selectively and attending surgeons were present in OR for critical parts of every case.

Seven patients (0.9%) had a biliary injury discovered intra- or postoperatively (Tables 2, 3). Three patients (0.4%) had a cystic duct stump leak, and four had an injury to the common bile duct (0.5%). Two patients had two unique biliary complications; in total, there were four Strasberg class A injuries, four class D injuries, and one class E2 injury. Only three of these cases were completed laparoscopically, and the remainder were converted to open procedures. No patient required surgical re-intervention or referral to an outside hospital for further care. The Critical View of Safety was stated to be obtained in 31.0% of charts; however, only 12.4% of charts described the critical view in detail consistent with the definitions by Strasberg and SAGES, and 12.0% both stated and described CVS correctly.

Table 2 Preoperative characteristics of patients with biliary injury
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Table 3 Perioperative characteristics of patients with biliary injury
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There were no statistically significant differences (p ≤ 0.05) on demographic data or preoperative workup, except for lower hemoglobin in biliary injury patients (Table 4). Patients with biliary injuries were more likely to have had urgent surgery rather than elective, and the surgeon was more likely to choose a non-CVS dissection technique or convert the procedure to open. Biliary injury patients were significantly more likely to have acute inflammatory conditions (acute cholecystitis, gangrene, necrosis, suppurative cholecystitis, or empyema), by both surgeon and pathologic diagnosis, and there were significantly lower rates of chronic cholecystitis in biliary injury patients per pathology. There were no significant differences in whether the Critical View of Safety was stated or described correctly.

Table 4 Differences between patients with BDI/cystic duct leak versus those without
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Univariable analysis of risk factors for BDI (Table 5) identified risk factors for biliary injury (p ≤ 0.05) to be higher ASA class; urgent surgery; preoperative diagnosis of acute cholecystitis; postoperative diagnosis of acute cholecystitis per pathology, gangrene/necrosis per pathology and surgeon; suppurative cholecystitis/gallbladder empyema per surgeon; and intraoperative choledocholithiasis. Converting to open, a longer operative time, and a different dissection method were also significantly associated with cases where biliary injury occurred. Protective factors included higher preoperative hemoglobin and a postoperative diagnosis of chronic cholecystitis by pathology.

Table 5 Univariable logistic regression model for predicting biliary injury
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Multivariable analysis (Table 6) demonstrated that higher preoperative hemoglobin was independently protective of BDI (OR 0.64, p = 0.0065). Converting to open, choledocholithiasis documented intraoperatively, a diagnosis of acute cholecystitis by pathology, or a postoperative diagnosis of gangrene or necrosis by the surgeon were also independently predictive of biliary injury.

Table 6 Multivariable logistic regression model for predicting biliary injury, N = 765
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Discussion

The rate of biliary injury in this study was 0.9%, with a 0.5% rate of common bile duct injury. Nearly all of the patients with biliary injury in this study had Class A (cystic duct leak) and Class D (partial common bile duct transection) injuries, and all were repaired within the institution; these are less likely to be identified by larger BDI studies. Longer operative duration and increased conversion to open were expected to be predictive of biliary injury, as all major biliary injuries in this study were discovered and repaired intraoperatively. In this study, choledocholithiasis was independently predictive of biliary injury, in keeping with previous studies [14].

Acute inflammation and a need for urgent surgery were independently predictive of biliary injury during LC. This seems to contradict findings from the Cochrane review of early LC for acute cholecystitis [3], which found no increase in BDI for patients having acute surgery for acute cholecystitis; however, the review also found high levels of bias in the studies used. Despite the increase in risk found by this study, it may remain more appropriate to perform surgery for acute cholecystitis urgently, given an increased risk of perioperative complications in patients who are treated with antibiotics and later undergo interval surgery [15,16,17,18].

Higher preoperative hemoglobin was independently protective of BDI based on multivariable analysis. Given that both groups of patients have close to normal-range hemoglobin (12.0 in BDI, 13.4 in no BDI), this may not be specifically related to preoperative anemia, but rather may function as another indication of increased preoperative inflammation that may increase risk for BDI. Although preoperative anemia has not been well documented as a contributing factor to laparoscopic cholecystectomy complications [19], it has been associated with an increased postoperative complications in other surgical specialties [20,21,22,23]; further examination of LC outcomes for patients with anemia may be warranted. Caution in interpreting this result is necessary, given the few data points in the biliary injury group.

There was no correlation of Critical View of Safety with prevention of biliary injury, although only 31.0% of charts stated it had been obtained, and only 12.0% of charts both stated that CVS had been obtained and described it correctly. This low rate of documentation suggests that this technique is not universally used at NorthShore. Of the operative notes where CVS was stated as obtained, 13.9% were too brief to determine precisely how the dissection had occurred, and 5.0% of charts where CVS was stated had inaccurate descriptions, mainly relating to dividing the cystic artery prior to identification of the cystic duct or dissecting the cystic duct—common bile duct junction. Although the Critical View of Safety should be effective in reducing bile duct injuries, rates of CBD injury have not fallen in countries where CVS is now mandatory during laparoscopic cholecystectomy [24]. However, it is also important to note that the utility of the Critical View is to prevent injury due to misidentification of structures, and is probably less likely to prevent class A injuries (cystic duct stump leaks).

The number of charts with dissections not consistent with CVS suggests two possibilities: either surgical documentation does not reflect actual technique in the OR or some surgeons may be aware of the Critical View of Safety but lack complete understanding of its requirements. Programs such as the Safe Cholecystectomy Task Force may be helpful in increasing surgeon awareness of proper CVS technique. Moreover, photographic or video documentation of the Critical View intraoperatively has been shown to be feasible [24, 25]; these additional methods of recording the Critical View intraoperatively would improve documentation, and could also assist with continuing education for surgeons and residents. With consistently improved operative technique and documentation, it would be valuable to see if consistent application of the Critical View actually reduces common bile duct injury.

The limitations of this study included reduced statistical power, given the rarity of biliary injuries; the data will be stronger with eventual completion of the 3000-patient database when resources permit. Moreover, known risk factors for biliary injury could not be analyzed due to the retrospective nature of this study. Due to the format of operative documentation, we could not analyze the impact on biliary injury of surgical residents, who were actively supervised by attending surgeons in all cases, or the role of operating room equipment malfunction on biliary injury. Despite these limitations, this study may yield a greater biliary injury rate and greater detail of injuries than a large national administrative database review, potentially providing a better understanding of biliary injury causes during LC.

In conclusion, our findings suggest that acute inflammation remains a risk factor for biliary injury during laparoscopic cholecystectomy. Better implementation of the Critical View of Safety, and increased caution in dissecting acutely inflamed tissues, may be in order to prevent even minor biliary injuries. Patients must also be appropriately informed on the risks of laparoscopic cholecystectomy for acute cholecystitis.