Biliary Leak Rates After Cholecystectomy and Intraoperative Cholangiogram in Surgical Residency

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1 MILITARY MEDICINE, 180, 5:565, 2015 Biliary Leak Rates After Cholecystectomy and Intraoperative Cholangiogram in Surgical Residency CPT Robert R. Shawhan, MC USA*; CPT C. Rees Porta, MC USA*; CPT Jason R. Bingham, MC USA*; CPT Derek P. McVay, MC USA*; CPT Daniel W. Nelson, MC USA*; MAJ M. Wayne Causey, MC USA*; Justin A. Maykel, MD ; LTC Scott R. Steele, MC USA* ABSTRACT Postoperative bile leak (BL) after cholecystectomy is a rare but dreaded complication, and is felt to be increased during surgical training. We sought to determine the incidence of BL after selective intraoperative cholangiogram (IOC) at a teaching hospital and identify risk factors for predicting BLs. A retrospective review was performed analyzing all cholecystectomy with IOCs between September 2004 and September Residents performed under staff supervision. Of 1,799 cholecystectomies performed during the study period, only 96 (5.3%) were with IOCs (mean age 43, 65% female) and 4 BLs occurred (4.2%, 1 major duct injury, 3 cystic duct stump leaks). Univariate analysis demonstrated that male gender, significant medical comorbidities, case duration, preoperative endoscopic retrograde cholangiopancreatography, and surgery type (laparoscopic versus open) increased the patient s risk of BL; however, age, performance of secondary procedures, common bile duct exploration, resident level (PGY), and diagnosis did not increase BL risk. Multivariate regression revealed that only surgery type lead to an increased risk of BL ( p = 0.001) (OR 31.61, 95% CI ). Patient factors and PGY level did not significantly affect BL rates, although open and converted procedures were associated with higher rates, suggesting an increased risk of a BL with more complex cases. INTRODUCTION Cholecystectomy is one of the most commonly performed surgical procedures worldwide, with over 750,000 operations performed annually in the United States alone. 1 First introduced in the 1980s, laparoscopic cholecystectomy has remained the gold standard for treatment of patients with biliary disease for the past few decades. In fact, approximately 90% of cholecystectomies today are performed using a laparoscopic approach. Of these, approximately 5% require conversion to an open procedure, usually because of significant inflammation, adhesions, or difficulty defining the biliary anatomy. 2 Postoperative bile leaks (BLs) following cholecystectomy may arise from the liver edge (i.e., ducts of Luschka), cystic duct stump, or injury to the biliary tree. Overall, they are relatively uncommon, occurring in 1% to 11% of all cases. When limiting the cohort to elective operations, rates of BL following laparoscopic cholecystectomy are even lower, reported to occur in 0.5% to 3%, including a recent review of over 10,000 patients reporting a rate of 0.5%. 2 5 Unfortunately, when they do occur, they carry a significant morbidity and mortality. 3 5 Risk factors for BL include the presence of an intraoperative complication or conversion to open surgery, and in cases of complicated acute cholecystitis leading to recommendations to leave the posterior *Department of Surgery, Madigan Army Medical Center, 9040 Jackson Avenue, Tacoma, WA Department of Surgery, UMass Memorial Medical Center, University of Massachusetts Medical School, 67 Belmont Street, Worcester, MA This manuscript was presented at the 9th Annual Academic Surgical Congress in San Diego, CA, February The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of Defense. doi: /MILMED-D wall of the gallbladder intact or place drains at the time of surgery. 6 In addition, intraoperative imaging of the biliary tree has been advocated to help avoid or identify BLs, though its practice is not universally accepted. 7 First described by Mirizzi in 1932, intraoperative cholangiography is often used to assess the common bile duct for the presence of choledocholithiasis and to define the anatomy of the biliary tract. 8 The exact role of intraoperative cholangiogram has been debated for decades, with some advocating routine use and others all but abandoning the technique. Advocates of routine use of intraoperative cholangiogram (IOC) tout its relative safety and ability to identify and prevent bile duct injuries. 9 Conversely, some authors contend that cholangiography is time consuming, of low yield, and may in fact cause bile duct injury. 10,11 Generally, intraoperative cholangiography is not considered to increase the risk of a BL; however, many surgeons today use IOC selectively based on preoperative imaging, laboratory results, or difficult patient anatomy. When performed appropriately by experienced surgeons facile in the technique, IOC can detect choledocholithiasis and help delineate difficult anatomy, thereby hypothetically reducing the risk of bile duct injury and subsequent postoperative bile duct leak. However, IOC can be a technically difficult procedure involving the cannulation of the biliary tree, and therefore in the hands of a novice surgeon could theoretically increase the risk of iatrogenic bile duct injury and postoperative leak. 12 With the changing face of the resident operative experience, including more widespread availability of endoscopic retrograde cholangiopancreatography (ERCP) and adoption of the selective approach to performing an IOC with cholecystectomy, there is concern that residents are receiving inadequate training to become competent in the procedure. 13 The purpose of this study was to determine the MILITARY MEDICINE, Vol. 180, May

2 incidence of BL after selective IOC following cholecystectomy performed by supervised resident surgeons at a teaching hospital, to identify risk factors that may help to predict a postoperative BL in a teaching environment, and compare our results with results in the published literature. METHODS After receiving human subject approval from our institutional review board, medical records including the postoperative courses of all patients who underwent cholecystectomy with intraoperative cholangiogram from September 2004 to September 2011 were retrospectively reviewed. A positive IOC was defined as the presence of a filling defect, failure of contrast to reach the duodenum, failure to visualize either hepatic radicals or extravasation of contrast. Patients were included regardless of disease severity, which ranged from symptomatic cholelithiasis to gangrenous cholecystitis and ascending cholangitis. Residents of various training levels (PGY1 PGY6) performed all procedures under the direct supervision of staff surgeons. For purposes of categorizing, when multiple residents were scrubbed in a case, the level of the resident primarily performing the procedure under staff guidance was selected for analysis. BLs were initially identified in the medical record by documented clinical suspicion; however, only those patients who had radiographic confirmation via ERCP/magnetic resonance choleangiopancreatography, computed tomography, or ultrasound by evidence of a biloma or contrast extravasation were defined as having postoperative BLs. Univariate analysis followed by multivariate logistic regression was utilized to evaluate potential risk factors for postoperative BL to include age, gender, significant medical comorbidities (Chronic Obstructive Pulmonary Disease, Cerebral Vascular Accident, Myocardial Infarction, Chronic Kidney Disease, Arrhythmia, Diabetes Mellitus, Morbid Obesity), case duration, preoperative ERCP, surgery type (laparoscopic versus open), performance of secondary procedures, common bile duct exploration (CBDE), and resident level of training (PGY). Statistical analysis was performed using PASW Version 19.0 (SPSS, Chicago, Illinois). Categorical variables are represented as rates and continuous variables as mean ± standard deviation, and were analyzed using c 2 analysis, although continuous variables were evaluated using Student s t tests. Factors significant on univariate analysis along with those deemed clinically significant were entered into multivariate logistic regression analysis a priori. Statistical significance was reported on the multivariate model using a 95% confidence interval with an alpha level set at RESULTS Out of 1,799 cholecystectomies performed at our institution between September 2004 and September 2011, we identified 96 patients (5.3%) (65 females; mean age 42.7 [range, 18 93]) who underwent IOC at time of cholecystectomy (Table I). IOC was performed selectively at our institution, and while the specific indications for performing an IOC vary with individual surgeon preference, underlying reasons to perform an IOC included patients with preoperative liver function test abnormalities, imaging suggestive of bile duct obstruction, difficult to delineate biliary anatomy, and anatomy precluding ERCP (e.g., Roux-en-y). In all but one patient (99%), the procedure was successful. For the entire cohort, mean case duration was 110 minutes (±43.9), and the mean length of stay was 3.0 days (range, 0 20). Breakdown of resident PGY level is shown in Table I. Mean PGY level for the resident on the case was PGY-3, but the mode was PGY-2. A laparoscopic approach for the IOC was attempted in 92 of the 96 cases (96%), of which 3 (3.2%) were converted to an open procedure, although in 4 cases the IOC was completed as part of a planned open procedure. Four patients (4.2%) experienced a postoperative BL (Table II). None of the four patients underwent an IOC specifically to evaluate for a suspected leak. Reasons for the IOC in a leak patient included obstructed duct on preoperative ERCP (n = 1), unclear anatomy (n = 2), and dilated common bile duct on preoperative imaging (n = 1). One patient sustained a bile duct injury that was detected intraoperatively by IOC and underwent immediate primary repair. Yet despite multiple attempts at primary repair, a small leak persisted from the cystic duct, common bile duct junction. The staff surgeon decided that further dissection in this area would be dangerous given the size of the leak, and a drain was left in the gallbladder fossa. The three remaining patients experienced cystic duct stump leaks. All four patients were male, and three of the four patients had a laparoscopic procedure converted to open procedure. Intraoperatively, all patients with leaks had a Jackson Pratt drain placed before the closure of the abdomen. All leaks were subsequently managed postoperatively with ERCP, sphincterotomy, and stent TABLE I. Overall Demographics of Cohort Patients Sex Age (mean) Case Duration (Minutes) LOS (days) Type of Surgery PGY Level (N) N = 96 F: 65 M: Range (18 93) 110 (±43.9) 3.01 Laparoscopic: 89 Lap!Open: 3 Open: 4 N, Number; LOS, Length of stay; M, male; F, female; Lap!Open, laparoscopic converted to open. R1:14 R2:43 R3:10 R4:10 R5:5 R6: MILITARY MEDICINE, Vol. 180, May 2015

3 TABLE II. Detailed Description of Patients That Developed BLs Age/Sex Indication Procedure Type Type of Injury Length of Case (minutes) Comorbidities 1 39 M Ascending Cholangitis Laparoscopic Converted to Open Major (CBD) 209 None 2 53 M Symptomatic Cholelithiasis Laparoscopic Converted to Open Cystic Duct Stump Leak 279 DM 3 71 M Symptomatic Cholelithiasis Laparoscopic Converted to Open Cystic Duct Stump Leak 192 CVA, MI, CRF, Arrhythmia 4 70 M Symptomatic Cholelithiasis Laparoscopic Cystic Duct Stump Leak 96 MO M, Male; DM, Diabetes mellitus; CVA, cerebrovascular accident; CRF, chronic renal failure; MO, Morbid obesity. TABLE III. Comparing Patients With BLs to Patients Without BLs by Univariate Analysis Patients With BLs Patients w/o BLs p Value Number of PTs 4 92 n/a Age (mean) Mean Case Duration (minutes) <0.001 LOS (mean) Sex M = 4 M = 27 <0.015 F = 65 Type of Surgery Lap!Open: 3 Laparoscopic: Laparoscopic: 1 Open 4 Pre-op ERCP PGY Level (N) R1: 0 R4: 1 R1: 14 R4: R2: 2 R5: 0 R2: 41 R5: 5 R3: 0 R6: 1 R3: 0 R6: 13 n/a, nonapplicable; LOS, Length of stay; M, male; F, female; Lap!Open, Laparoscopic converted to open procedure; Pre-op, preoperative. placement. Table III compares the four BL cases to the cases that did not develop a BL by univariate analysis. Average case time for patients with a BL was 193 minutes (median 199.5) compared to 106 minutes (median 94) for cases without a leak ( p < 0.001). Not surprisingly, patients with BLs tended to have a longer overall hospital stay, with an average length of 7.3 days (median 8.5), compared to 2.8 days (median 2) for patients without a BL ( p = 0.006). We found that sex, case duration, preoperative ERCP, and type of surgery were significantly associated with a BL following IOC (Table III). All BLs occurred in males (4/31; 13%), although none occurred in females ( p < 0.015). Cases that resulted in BLs took longer to perform than cases without BLs ( p = 0.005; OR = 1.03, 95% CI ). Similarly, when comparing pre- and postoperative ERCP, patients that had BLs were 17-fold more likely to have undergone preoperative ERCP ( p = 0.009; OR = 17.4; 95% CI ), suggesting an increased need for IOC in these patients. A strong correlation between type of procedure and development of a BL was noted with open procedures (typically from conversion to open) showing much greater leak rates when compared to laparoscopic procedures ( p = 0.001; OR = 66, 95% CI ). Interestingly, PGY level did not have an association with the risk of a postoperative BL ( p = 0.72). Multivariate analysis revealed that the only factor associated with the development of a postoperative BL was conversion from a laparoscopic case to an open case (Table IV). A stepwise logistical regression was performed adjusting for age, case duration, comorbidities, preoperative ERCP, PGY level, and CBDE found only surgery type (laparoscopic versus open versus conversion to open) was significant ( p = 0.001; OR 31.61, 95% CI ). DISCUSSION In this teaching environment cohort following cholecystectomy with selective IOC, supervised resident surgeons had a 4.2% rate of postoperative BL, which is consistent with previously published leak rates. 3 Although several risk factors were identified on univariate analysis to include patient sex, the presence of comorbidities, case duration, preoperative TABLE IV. Data Obtained by Multivariate Regression p Value OR 95% CI Surgery Type (Laparoscopic versus Open) a Surgery Type (Laparoscopic versus Open versus Conversion to Open) b a When data adjusted for age, case duration, pre-op Liver Function Test abnormalities, preoperative ERCP, PGY-level, and common bile duct exploration, only surgery proved to be statically significant. b Stepwise logistical regression used and data adjusted for age, case duration, PMHx, preoperative ERCP, PGY-level, and common bile duct exploration, once again only surgery type proved to be significant. MILITARY MEDICINE, Vol. 180, May

4 ERCP, and type of surgery, only conversion to open surgery was found to significantly increase the risk of BL on multivariate analysis. In fact, out of patients with an IOC, all laparoscopic cases that were converted to open procedures resulted in a postoperative BL. Certainly, conversion from laparoscopy to open is a marker of a technically challenging case with potentially unfavorable anatomy requiring extensive dissection, as indicated by the prolonged operative time. These findings are not unique to cholecystectomies. In one study by Tan et al 14 looking at laparoscopic colectomies, both technically challenging cases and those with longer operative times were associated with higher conversion to open rates and higher morbidity. The effect on resident involvement on complication rates has been evaluated for various surgical procedures. Mehall et al 15 showed the complication rate after laparoscopic colectomy was not significantly increased among supervised residents when compared to attending surgeons (18% for residents, 14% attending; p = NS). Similarly, studies looking at laparoscopic hernia repair, vascular surgeries, and laparoscopic gastric bypass have all shown that although resident involvement does result in a longer operating time, it does not increase postoperative complication rates Alternatively, others have demonstrated that resident involvement does, in fact, correlate with increased complication rates. One study specifically looking at pancreaticoduodenectomies (PDs) found that while PGY level alone was not associated with the rate of postoperative complications, the number of PDs performed by the trainee was inversely associated with the rate of postoperative complications, with a 3% decrease in complication rate for each PD performed. 19 Similarly, a study looking at the role of trainee involvement in nephrectomies showed that compared to surgeries performed by attending surgeons alone, surgeries that involved trainees had a higher rate of complications. Moreover, a larger multicenter study conducted by Iannuzzi et al, 20 utilizing NSQIP data of open and laparoscopic partial colectomy found that resident involvement did have an effect on the rate of postoperative major complications (OR 1.18, CI , p < 0.001). Interestingly, this is in contradiction to the findings of Mehall et al. 15 The reasons for the variation in outcomes seen with other types of surgeries is unclear but may be a result of study size, study design, or the complexity of the surgery that is studied. In our study, neither patient factors nor PGY level had a significant effect on BL rates. In our program, residents of all levels (PGY1 PGY6) perform cholecystectomies. Naturally, senior-level residents will have more experience, and likely greater technical proficiency with regards to the performance of IOC. Despite these variations in resident level and experience performing an IOC, our data showed that resident level did not have an impact on the rate of BLs. Other studies have come to similar conclusions. Hope et al 1 found that although lower level residents took more time on average to perform an IOC, it did not correlate with an increased complication rate. Although Hope s study found similar conclusions, this study is fundamentally different in a few key aspects. In their study, all laparoscopic cholecystectomies were performed under the guidance of a single attending surgeon, whereas we had multiple attending surgeons. In addition, IOCs were performed routinely in Hope s study, not selectively as in this one. Finally, we included open cases and CBDEs although Hope excluded these from his analysis. These differences bring out subtle, yet important, distinctions that may reflect a more common scenario in a training environment. Similarly, Naylor et al 21 found that PGY level did not correlate with complications after laparoscopic cholecystectomy. Importantly, they did find that case difficulty, as indicated by prolonged operative time, correlated with increased rate of complication following cholecystectomy. This resonates well with our finding that it is likely case complexity (i.e., those that required conversion to open surgery), which increases postoperative BL rates, and not the level of the resident performing the procedure. The exact reason why PGY level does not correlate with increased complications is unclear. Certainly, the fact that all resident procedures are supervised by attending surgeons likely compensates for any experiential deficiencies the resident may have. In addition, excellent training in advanced laparoscopy provided by modern resident training programs could also be a factor as there is an increasing emphasis on minimally invasive techniques. 13 Regardless of the reason, literature suggests that under appropriate supervision, an IOC appears to be safely performed by resident surgeons of all levels. Other factors, although not obtaining statistical significance, demonstrated some interesting trends. Patient s age showed a trend toward increased BL rate with increasing age ( p = 0.094; OR = 1.05, 95% CI, ). A similar trend was seen in a large nationwide study, which examined over 1.5 million patients that found that although not significant, patients with BLs on average were older. This trend is seen among other procedures as well, such as in laparoscopic anterior colon resections where increased age has also been associated with increased complications. 14 In addition, of the five patients with a positive IOC who underwent CBDE at the time of cholecystectomy, one developed a BL. This resulted in a nonsignificant trend toward increased leak rates in patients receiving CBDE ( p = 0.25; OR 4.05, 95% CI ). We acknowledge certain limitations to this study. First, as a retrospective review it is bound by the unavoidable selection bias that is inherent to such studies. Second is the relatively small sample size, which potentially lacks adequate power to show statistical significance for several independent risk factors. This point speaks to the larger issue of the diminishing use of intraoperative cholangiography, used in only 5.3% of cholecystectomies in this sample. With the growing availability of ERCP and the increased adoption of selective IOC use, it is likely that resident exposure to such procedures is growing more and more limited. This is concerning as knowledge of intraoperative cholangiography 568 MILITARY MEDICINE, Vol. 180, May 2015

5 and CBDE remain essential skills for the general surgeon given that ERCP is not universally available and is not possible in certain patient populations. In fact, with the growing problem of morbid obesity in the United States, and consequently increasing numbers of patients who have received obesity surgery with Roux-en-Y anatomy, thus making ERCP nearly impossible, it is arguable that skills such as laparoscopic IOC and CBDE are as needed as ever. Even more concerning is the recent data that when performed in the setting of a CBD injury, IOC is misinterpreted up to 80% of the time. 22,23 Given these issues, additional training in the use of intraoperative cholangiography should be considered to equip the surgical trainee with the skills he or she will need for modern practice. One potential way this may be possible is with the use of specific simulators. Finally, although leaks were more likely with open and conversion to open cases in this cohort, we do not have the rate of leaks from all open or converted to open cases. Despite our study s limitations, our data along with others, suggest that IOC is a safe procedure that can be performed by trainees at all levels. CONCLUSION Resident surgeons experienced a very low rate of postoperative BL following cholecystectomy with IOC. Neither patient factors nor PGY level significantly increased the rate of leak, although surgery type (open and converted procedures) was associated with significantly increased risk. These results correlate well with the results from literature. Overall, intraoperative cholangiography is performed relatively infrequently as ERCP continues to gain widespread availability. Nonetheless, performing an interpreting an IOC is an important skill set for the modern general surgeon to possess. REFERENCES 1. Hope WW, Bools L, Hooks WB, Adams A, Kotwall CA, Clancy TV: Teaching cholangiography in a surgical residency program. J Surg Educ 2013; 70(2): Albrecht R, Franke K, Koch H, Saeger HD: Prospective Evaluation of Risk Factors Concerning Intraoperative Conversion from Laparoscopic to Open Cholecystectomy. Zentralbl Chir 2013; July 3, Epub. 3. Henneman D, da Costa DW, Vrouenraets BC, van Wagensveld BA, Lagarde SM: Laparoscopic partial cholecystectomy for the difficult gallbladder: a systematic review. Surg Endosc 2013; 27(2): Barkun AN, Rezieg M, Mehta SN, et al: Postcholecystectomy biliary leaks in the laparoscopic era: risk factors, presentation, and management. McGill Gallstone Treatment Group. Gastrointest Endosc 1997; 45(3): Massoumi H, Kiyici N, Hertan H: Bile leak after laparoscopic cholecystectomy. J Clin Gastroenterol 2007; 41(3): Michalowski K, Bornman PC, Krige JE, Gallagher PJ, Terblanche J: Laparoscopic subtotal cholecystectomy in patients with complicated acute cholecystitis or fibrosis. Br J Surg 1998; 85(7): Spanos CP, Syrakos T: Bile leaks from the duct of Luschka (subvesical duct): a review. Langenbecks Arch Surg 2006; 391(5): Mirizzi P: Operative cholangiography its contribution to the physiopathology of the common bile duct. Lancet 1938; 232(5998): Ludwig K, Bernhardt J, Steffen H, Lorenz D: Contribution of intraoperative cholangiography to incidence and outcome of common bile duct injuries during laparoscopic cholecystectomy. Surg Endosc 2002; 16(7): White TT, Hart MJ: Cholangiography and small duct injury. Am J Surg 1985; 149(5): Corsale I, Ruggiero R, Mandato M, et al: [Intraoperative cholangiography in videolaparoscopic cholecystectomy: indications, advantages, and limitations]. G Chir 2002; 23(6 7): Ford JA, Soop M, Du J, Loveday BPT, Rodgers M: Systematic review of intraoperative cholangiography in cholecystectomy. Br J Surg 2012; 99(2): Eckert M, Cuadrado D, Steele S, Brown T, Beekley A, Martin M: The changing face of the general surgeon: national and local trends in resident operative experience. Am J Surg 2010; 199(5): Tan PY, Stephens JH, Rieger NA, Hewett PJ: Laparoscopically assisted colectomy: a study of risk factors and predictors of open conversion. Surg Endosc 2008; 22(7): Mehall JR, Shroff S, Fassler SA, Harper SG, Nejman JH, Zebley DM: Comparing results of residents and attending surgeons to determine whether laparoscopic colectomy is safe. Am J Surg 2005;189(6): Hernández-Irizarry R, Zendejas B, Ali SM, Lohse CM, Farley DR: Impact of resident participation on laparoscopic inguinal hernia repairs: are residents slowing us down? J Surg Educ 2012; 69(6): Jan A, Riggs DR, Orlando KL, Khan FJ: Surgical outcomes based on resident involvement: what is the impact on vascular surgery patients? J Surg Educ 2012; 69(5): Iordens GI, Klaassen RA, van Lieshout EM, Cleffken BI, van der Harst E: How to train surgical residents to perform laparoscopic Roux-en-Y gastric bypass safely. World J Surg 2012; 36(9): Relles DM, Burkhart RA, Pucci MJ, et al: Does resident experience affect outcomes in complex abdominal surgery? Pancreaticoduodenectomy as an example. J Gastrointest Surg 2013; 18(2): Iannuzzi JC, Rickles AS, Deeb AP, Sharma A, Fleming FJ, Monson JR: Outcomes associated with resident involvement in partial colectomy. Dis Colon Rectum 2013; 56(2): Naylor RA, Rege RV, Valentine RJ: Do resident duty hour restrictions reduce technical complications of emergency laparoscopic cholecystectomy? J Am Coll Surg 2005; 201(5): Way LW, Stewart L, Gantert W, et al: Causes and prevention of laparoscopic bile duct injuries: analysis of 252 cases from a human factors and cognitive psychology perspective. Ann Surg 2003; 237(4): Massarweh NN, Flum DR: Role of intraoperative cholangiography in avoiding bile duct injury. J Am Coll Surg 2007; 204(4): MILITARY MEDICINE, Vol. 180, May

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