Gallstone disease is among the commonest causes

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1 Single-stage Original Article surgery / Biliary for gallstone pancreatitis Single-stage laparoscopic management of acute gallstone pancreatitis: outcomes at different timings Antonio Navarro-Sánchez, Hutan Ashrafian, Aggelos Laliotis, Kamran Qurashi and Alberto Martinez-Isla London, UK BACKGROUND: Definitive therapy for gallstone pancreatitis requires eradication of gallstones with cholecystectomy and common bile duct (CBD) clearance. Current guidelines recommend this be done within the same admission and preferably by laparoscopic cholecystectomy and CBD exploration. We report our experience of laparoscopic single-stage management with cholecystectomy and intraoperative cholangiogram followed by laparoscopic bile duct exploration (LBDE) when necessary performed at three different stages. METHODS: From January 1998 to December 2012, 134 patients (100 females and 34 males) underwent single-stage laparoscopic management of gallstone pancreatitis. Patients were classified according to the timing of surgery: A, 7 days from symptom onset (n=27); B, 8 to 30 days (n=58) and C, >30 days (n=49). RESULTS: LBDE was performed in 30 patients with a success rate of 100%. CBD stones were found in 25 patients (A: 22.2%, B: 22.4%, C: 12.2%). CBD stones were more common in patients undergoing surgery within 30 days of presentation than after this time point (P=0.35). Multiple choledocholithiasis Author Affiliations: Northwick Park and St Mark s Hospital, North West London Hospitals NHS Trust, Watford Road, Harrow, Middlesex, London, HA1 3UJ, UK (Navarro-Sánchez A, Ashrafian H, Qurashi K and Martinez-Isla A); Department of Surgery and Cancer, Imperial College London, 10th Floor QEQM Building, St Mary s Hospital, Praed Street, W2 1NY, UK (Ashrafian H); Guy s and St. Thomas NHS Foundation Trust, Great Maze Pond, London, SE1 9RT and Westminster Bridge Road, London, SE1 7EH, UK (Laliotis A); and Ealing Hospital NHS Trust, Uxbridge Rd, Southall, Middlesex, UB1 3HW, UK (Qurashi K) Corresponding Author: Alberto Martinez-Isla, FRCS, Consultant Surgeon, Department of Upper GI Surgery, Northwick Park Hospital, North West London Hospitals NHS Trust, Watford Road, Harrow, Middlesex, London, HA1 3UJ, UK (Tel: ; Fax: ; a.isla@imperial.ac.uk) 2016, Hepatobiliary Pancreat Dis Int. All rights reserved. doi: /S (16) Published online February 2, was more frequent in patients treated within 7 days (P=0.04). The 30-day mortality after surgery was 0, with no conversion to an open approach. Overall complication rate was 11.9%, which did not differ significantly between patients treated within 7 days or after this time point (P=0.83). CONCLUSIONS: This study demonstrated the feasibility and reproducibility of single-stage laparoscopic management of acute gallstone pancreatitis, which has a low complication rate at any stage. Patients undergoing early treatment have a higher incidence of choledocholithiasis and multiple stones than those treated after 30 days, supporting the passage of stones with time. (Hepatobiliary Pancreat Dis Int 2016;15: ) KEY WORDS: bile duct; cholecystectomy; pancreatitis Introduction Gallstone disease is among the commonest causes of emergency surgical admission and it is the etiological factor of acute pancreatitis in 30%-50% of cases. [1] The definitive therapy for eradication of gallstones and prevention of recurrence in these patients is cholecystectomy and clearance of the common bile duct (CBD) after being imaged. The optimal timing of intervention is considered to be during the same admission but only after recovery from the acute episode, and to prevent recurrence and potentially life-threatening biliary complications. [2, 3] It is also mandatory to image the CBD during inpatient admission to ensure the absence of lithiasis, [4] most commonly by means of magnetic resonance cholangiopancreatography (MRCP). Endoscopic retrograde cholangiopancreatography (ERCP) [5] is commonly reserved for interventional purposes to clear the duct prior to cholecystectomy when on table surgical Hepatobiliary Pancreat Dis Int,Vol 15,No 3 June 15,

2 Hepatobiliary & Pancreatic Diseases International imaging and clearance is not available, or in case of unfit patients for cholecystectomy. Endoscopic ultrasound (EUS) is becoming more popular not only for the diagnosis of microlithiasis but also for excluding the presence of stones within the CBD. Since 1998 we have offered single-stage laparoscopic management for acute gallstone pancreatitis with excellent results. [6] In this study, we present our institutional results to-date, assessing its feasibility, the impact of the timing of intervention on the incidence of choledocholithiasis found, and major morbidity and mortality at the different stages. Methods The data from 134 patients admitted between January 1998 and December 2012 fulfilling our inclusion criteria included: (1) Diagnosis of pancreatitis (scored by the modified Glasgow Scoring System); [7] (2) Diagnosis of gallstones confirmed by abdominal ultrasound scan (USS) or EUS in late stage patients; and (3) Medically fit for surgical intervention. The data were prospectively collected and retrospectively reviewed. Patients presenting with acute cholangitis were excluded from the study and referred for ERCP and sphincterotomy. The diagnosis of gallstone pancreatitis was established through clinical evaluation of the patient s presenting signs and symptoms, elevation of serum amylase above three times the normal level, radiological demonstration of gallstones, and absence of other trigger factors of pancreatitis. All patients were admitted to the surgical department and treated conservatively in the acute phase. An urgent abdominal USS was also performed in all patients in order to determine the presence of gallstones. Those patients with negative abdominal USS underwent EUS as an outpatient examination and consequently most of them were operated on after 30 days. We favored definitive treatment for acute gallstone pancreatitis in a single surgical precedure. Patients included in the study underwent single-stage laparoscopic management associated with cholecystectomy and imaging of the duct obtained by an intra-operative cholangiography (IOC), followed by concomitant laparoscopic bile duct exploration (LBDE) if choledocholithiasis was present. This is the recommended approach for the management of CBD stones in the latest the National Institute for Health and Care Excellence (NICE) guidelines for gallstones disease. [8] All patients were consented according to the national UK guidelines (General Medical Council) before undergoing surgery and all patient information was anonymized before subsequent data analysis of our series. Since 1998, our method of access to the CBD has evolved according to our experience and technique-related complications. [9-11] Choledochotomy and closure over a T-tube was performed in the first 6 patients. This was changed in 2002 to choledochorraphy over an anterograde biliary endoprosthesis [9, 10] in the subsequent 15 patients. However, this technique was later abandoned due to the incidence of stent-related pancreatitis (6 patients). For the remaining cases, primary closure of the CBD was performed using a running 5/0 polyglactin suture. This remains the preferred technique when we perform choledochotomy [9] but we are currently experiencing an increased use of the transcystic route in almost 40% of patients due to its safety (unpublished data). In order to compare the outcome of the technique and the incidence of choledocholithiasis according to the timing of the surgical procedure, our patients were classified in three groups: (I) Group A (patients operated on within 7 days), same admission; (II) Group B (patients operated on between 8 and 30 days); and (III) Group C (patients surgically treated after 30 days). The characteristics of these groups are shown in Table 1. Patients from group A were considered as early treated. Patients in groups B and C ( delayed treatment groups) were those in whom clinical signs and biochemical values were slow to normalize and thus an optimization period was required, those selecting a delayed procedure for medical or personal reasons, those in whom there was an administrative error (i.e. clinical notes not found during Table 1. Surgical procedures and findings based on the timing of treatment (n, %) Variables Group A Group B Group C 7 days (n=27) 8-30 days (n=58) >30 days (n=49) Total P value Age (yr) (22-75) (23-83) (20-82) 53 (20-83) Gender (Male/Female) 8/19 14/44 12/37 34/100 LC+IOC 19 (70.4) 45 (77.6) 40 (81.6) 104 (77.6) 0.51 LC+IOC+LBDE 8 (29.6) 13 (22.4) 9 (18.4) 30 (22.4) 0.53 Choledocholithiasis 6 (22.2) 13 (22.4) 6 (12.2) 25 (18.7) 0.35 Multiple choledocholithiasis 5 (18.5) 5 (8.6) 3 (6.1) 13 (9.7) 0.04 LC: laparoscopic cholecystectomy; IOC: intra-operative cholangiography; LBDE: laparoscopic bile duct exploration. 298 Hepatobiliary Pancreat Dis Int,Vol 15,No 3 June 15,2016

3 Single-stage surgery for gallstone pancreatitis assessments) leading to delayed intervention, and those undergoing EUS for the diagnosis of gallstones. Statistical analysis was performed using PASW version 17.0 for Windows software (SPSS, Chicago, IL, USA) and the Chi-square test was used for categorical variables with significance determined as P<0.05. Results A hundred and thirty-four patients [100 females and 34 males; median age 53 (20-83) years] with gallstone pancreatitis were admitted to this hospital between January 1998 and December 2012 and considered for single-stage laparoscopic treatment (cholecystectomy and IOC +/- LBDE). Laparoscopic cholecystectomy and IOC constituted the only treatment for 104 patients. Small CBD filling defects found on the IOC were managed with instillation of 10 ml of 1% lidocaine into the bile duct and intravenous injection of 20 ml of buscopan to diminish sphincter of Oddi spasm. [12, 13] Following this, repeat IOC showed a duct without debris, with a good passage of contrast into the duodenum in most cases, and bile duct exploration was not required. IOC demonstrated filling defects in 30 patients who underwent LBDE in the same surgical procedure. Among the 30 LBDE patients, 6 were subjected this operation via the transcystic route and 24 through choledochotomy. Choledocholithiasis was found in 25 patients (16.7% IOC false positive rate). Currently, with the availability of the 3 mm choledochoscope, a more liberal use of the transcystic choledochoscopy has been applied, as mentioned above, accounting for almost 40% of our CBD explorations. The presence of CBD stones was higher in patients operated on within 30 days of admission (22.2% in group A and 22.4% in group B) than in those operated on after this period (group C, 12.2%), although this was not statistically significant (P=0.35). Notably, however, patients operated on within a week were more likely to have multiple CBD stones than delayed treated patients (P=0.04). All operations were completed laparoscopically without conversion. The overall complication rate was 11.9%. This result was not different significantly between early treated patients (group A) and those in the delayed treatment groups (groups B and C) (P=0.83). Complications included: 1 case of T-tube dislodgement (Clavien- Dindo grade IIIb), 6 cases of post-stent pancreatitis (Clavien-Dindo grade I), 3 cases of bile leaks (two of them were Clavien-Dindo grade IIIb and one Clavien- Dindo grade IIIa), 2 cases of retained calculus (Clavien- Dindo grade IIIa), 1 case of intrabdominal haematoma (Clavien-Dindo grade II), and 3 cases of medical com- Table 2. Comparison of morbidity, reoperations and mortality based on timing of treatment (n, %) Variables Group A Group B Group C Total 7 days 8-30 days >30 days (n=134) P value (n=27) (n=58) (n=49) Complication 4 (14.8) 6 (10.3) 6 (12.2) 16 (11.9) 0.83 Reoperation 0 1 (1.7) 2 (4.1) 3 (2.2) 0.24 Death (2.0) 1 (0.7) 0.42 plications (Clavien-Dindo grade II). The patient with T-tube dislodgement and two of the three patients with bile leaks required reintervention, which was performed laparoscopically. A patient died of severe pneumonia 90 days after surgery (Clavien-Dindo grade V) (Table 2). Discussion Current national and international guidelines recommend that treatment of gallstone pancreatitis should be given during the same admission or within two weeks of presentation in an attempt to avoid the risk of gallstonerelated complications as well as to diminish the [2, 4, 14] number of admissions. The timing of treatment of gallstones by means of cholecystectomy seems to be clear but the management of concomitant choledocholithiasis remains controversial despite the recent NICE guidelines supporting laparoscopic cholecystectomy with bile duct exploration. [8] It has been reported that up to 20% of patients with gallstone pancreatitis have associated CBD stones, [15] which is reflected in the overall 18.7% observed in the current study. Therefore, we feel imaging of the biliary tree with CBD clearance is mandatory where [3, 4] choledocholithiasis is present. In cases of gallstone pancreatitis, pre-operative assessment of the biliary tree may be performed using MRCP or EUS followed by ERCP with sphincterotomy for CBD clearance in case of choledocholithiasis. [16] The mean time between these procedures and cholecystectomy most commonly ranges from 5 days for MRCP and EUS to 54 days for ERCP. [17, 18] However, we advocate that CBD imaging should be contemporary with surgery as the period of time between MRCP/EUS or ERCP and cholecystectomy may allow the further passage of stones into the bile duct. [19] This is of particular importance given that the cystic duct dilatation and multiple small stones are common features in gallstone pancreatitis patients, which may result in choledocholithiasis being left behind at the time of cholecystectomy. Furthermore, because of its potential complications, ERCP should never be used for imaging purposes only. In their large multicenter prospective cohort study, Glomsaker et al reported an overall morbidity of 11.6% and a mortality of 1.4% Hepatobiliary Pancreat Dis Int,Vol 15,No 3 June 15,

4 Hepatobiliary & Pancreatic Diseases International associated with ERCP procedures. [20] Therefore, where adequate surgical experience in bile duct exploration is available we (in line with the recent NICE guidelines) recommend the laparoscopic single-stage approach with bile duct exploration for gallstone pancreatitis. Furthermore, ERCP should be reserved for patients who are not candidates for surgery, elderly patients, or when intraoperative bile duct exploration is unsuccessful. This also has an economic impact, as the preoperative ERCP followed by laparoscopic cholecystectomy, the standard management in most hospitals has been reported to cost , whereas the laparoscopic single-stage approach that we use costs [8] Our series demonstrats the presence of choledocholithiasis in 22.4% of patients treated within 30 days of presentation, dropping to 12.2% in those treated after this period. In view of the limited size of this single-surgeon study, further review with a larger number of patients is required to achieve statistical significance to enable the derivation of more robust conclusions. Patients undergoing early surgery were also more likely to have multiple CBD stones (P=0.04), which diminished with time after presentation. This finding echoes that of several other reports demonstrating a decrease in the presence of CBD stones from 74% on the day of admission to less than 10% when definitive treatment is performed a week later. [21-24] Consequently, according to our opinion, we strongly recommend early laparoscopic treatment with concomitant surgical management of choledocholithiasis in order to minimize the potential risk of gallstone-related complications. This may be particularly beneficial in younger patients under 75 years of age in whom we have experienced a procedure-related mortality of 0 in performing CBD exploration. [9] Furthermore, in accordance with previous studies, [21-24] we highlight the clinical implication that patients undergoing early treatment have a higher incidence of choledocholithiasis, which should be considered when making the decision to operate. Notably in our study, only one patient classified in group B had relapse of pancreatitis, leading to the conjuncture that previous passage of stones could dilate the sphincter of Oddi naturally and protect in developing recurrent pancreatitis. Further randomized studies are necessary to demonstrate this. The current study shows an IOC false positive rate of 16.7% confirmed by failure to demonstrate choledocholithiasis upon subsequent laparoscopic bile duct exploration. This compares to 11.5% in our non-pancreatitis patients with a positive IOC requiring bile duct exploration. [9] These results may be attributable to a lower threshold for bile duct exploration in pancreatitis patients, mainly now with the availability of 3 mm choledochoscope and the increased use of the transcystic route, or to the presence of smaller stones that may be more difficult to identify. After the insertion of the choledochoscope, some stones may have passed spontaneously, assisted by water irrigation. As such, we recommend whenever possible to use the transcystic route, preferably with the 3 mm choledochoscope, to avoid the complications related to choledochotomy. This laparoscopic single-stage surgical approach may also confer a number of additional benefits that remain to be fully investigated. First, single-stage surgery may reduce the burden on already overstretched ERCP services. Second, although the aim of this report is not to appraise formal cost-efficacy, there is an additional economic advantage secondary to reduced costs incurred from pre-operative MRCP, EUS or ERCP. [8] In addition, as previously suggested by other authors, the reduction in overall hospital stay and readmission in these patients may reduce healthcare expenditure, improve the patient experience and reduce the morbidity and mortality as- [16, 22-24] sociated with ERCP. There are some limitations for this study. This is a single-surgeon study appraising results for single-stage laparoscopic management of acute gallstone pancreatitis over a 14-year period. This represents one of the largest single-surgeon studies to date in this field. However, in view of the retrospective nature of the analysis and the relatively low number of subjects for longitudinal studies, any conclusions from this data set should be considered within these limitations. In conclusion, the presence of CBD stones is higher in patients operated on within 30 days of admission than in those operated on after this period. There is no significant difference in overall complication rate, reoperation or mortality between patients undergoing acute early intervention and those delayed beyond 30 days. The single-stage laparoscopic approach for uncomplicated gallstone pancreatitis is safe and effective in the treatment of gallbladder related choledocholithiasis. Contributors: NSA and MIA proposed the study. NSA and AH performed the research and wrote the first draft. NSA, QK and MIA collected the data. LA analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts. MIA is the guarantor. Funding: None. Ethical approval: Not needed. Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. References 1 El-Dhuwaib Y, Deakin M, David GG, Durkin D, Corless DJ, 300 Hepatobiliary Pancreat Dis Int,Vol 15,No 3 June 15,2016

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