International Journal of Surgery 12 (2014) 1077e1081

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Original research

Laparoscopic versus robot-assisted cholecystectomy: A retrospective cohort study Subhashini Ayloo a, *, Younghoon Roh b, Nabajit Choudhury a a b

Division of General, Minimally Invasive and Robotic Surgery, Department of Surgery, University of Illinois Hospital and Health Sciences, Chicago, IL, USA Department of Surgery, Dong-A University Hospital, Busan 602-715, South Korea

h i g h l i g h t s
This study compares experience between laparoscopic and robotic cholecystectomies.
The surgical outcomes were similar between both groups.
Robotic platform might address biliary injuries in minimal invasive approach.
True benefit of robotic platform is in complex biliary cases.
Robotic cholecystectomy might be a safe model to gain the robotic platform skills.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 June 2014 Received in revised form 16 August 2014 Accepted 20 August 2014 Available online 9 September 2014

Introduction: Robot-assisted surgery has permeated all surgical specialties including general surgery. Still, only a few small experimental series have compared experiences between laparoscopic cholecystectomy (LC) and robotic cholecystectomy (RC). We present a single surgeon's experience with LC versus RC in a large case series. Methods: We conducted an IRB-approved retrospective review of 326 patients (147 LC and 179 RC) who underwent surgery between September 2005 and June 2012. The same selection criteria and standardized surgical technique was used for all patients. Demographics collected included patient age, gender, body mass index (BMI), operating time, estimated blood loss (EBL), associated procedures, conversions, intraoperative and postoperative complications, and hospital length of stay (LOS). Results: The LC group (26 males/121 females) had a mean age, BMI, operative time, and EBL of 41.1 years, 31.8 kg/m2, 89.60 min, and 13.7 ml, respectively. Three cases were converted to open surgery and there were three major complications. The mean LOS was 1.01 days. The RC group (30 males/149 females) had a mean age, BMI, operative time, and EBL of 40.2 years, 32.9 kg/m2, 95.7 min, and 13.9 ml, respectively. Two cases were converted to open surgery and there were three major complications. The mean LOS was 0.9 days. Conclusions: LC and RC are comparable in terms of feasibility, safety, and reproducibility of outcomes in all cholecystectomy settings. Robotic assistance may be useful in managing biliary injuries during the LC procedure. © 2014 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.

Keywords: Cholecystectomy Laparoscopy Robot-assisted surgery Case series Safety Outcomes

1. Introduction The dawn of this millennium witnessed the introduction of robotics into surgery. Today, after more than a decade of use, robotic surgery has established clear benefits in certain complex procedures, including improved dexterity, stability, superior precision, enhanced instrument manipulation, 3-dimensional vision, and improved ergonomics [1e4]. Studies have been published that

* Corresponding author. Division of General Minimally Invasive and Robotic Surgery, 840 S. Wood, M/C 958, Suite 435E, Chicago, IL 60612, USA. E-mail address: [email protected] (S. Ayloo). http://dx.doi.org/10.1016/j.ijsu.2014.08.405 1743-9191/© 2014 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.

compared the outcomes of conventional laparoscopy versus robotassisted surgery for pyeloplasty [5], fundoplication [6], colectomy [7], and partial nephrectomy [8e10]. Although cholecystectomy remains one of the most common procedures performed by the general surgeon, there exist few studies that directly compared laparoscopic cholecystectomy (LC) with robot-assisted cholecystectomy (RC) [11e14]. The largest cohort study published to date was by Breitenstein et al., in 2008, which compared 50 RC patients to 50 LC patients [11]. The current study focuses on a larger patient sample and evaluates a single surgeon's experience with safety, feasibility, complications, and

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short- and procedures.

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long-term

outcomes

for

both

cholecystectomy

2. Materials and methods We conducted an IRB-approved retrospective review of a series of 326 patients (147 LC and 179 RC) that underwent surgery at our institution between September 2005 and June 2012. More specifically, the LC approach had been used since 2005 and the RC approach was introduced for cholecystectomies in 2009. The same selection criteria were used for RC and LC, which were any patient requiring cholecystectomy for clinical reasons and platform availability. The same standardized surgical technique was used for all patients and all procedures were performed at a tertiary academic center. Demographics collected included patient age, gender, body mass index (BMI), operating timeeskin incision to skin closureewhich included robot set-up, docking and undocking, estimated blood loss (EBL), associated procedures, conversions, intraoperative and postoperative complications, and hospitalization length of stay (LOS). A review of the available literature was performed to correlate our results with prior findings. Statistical analyses were performed using the OpenEpi [15] program. Quantitative data were analyzed as means ± standard deviations. Fisher's exact test and t-tests were done to compare data sets. P-values >0.05 were considered to be indicative of statistically significant differences. 2.1. Surgical techniques 2.1.1. Laparoscopic cholecystectomy The patient was positioned in the reverse Trendelenburg left lateral position under general anesthesia. Port placement is depicted in Fig. 1. A 5-mm trocar was placed at the umbilicus for a 5-mm 30 camera. Two additional 5-mm trocars were placed in the right mid-abdomen so the surgeon's grasper could hold the infundibulum and the assistant could retract the fundus of the gallbladder cranially over the liver. A 12-mm trocar was placed at the xiphoid to enable the surgeons to exchange instruments for gallbladder dissection, clipping the cystic duct and artery, and extracting the specimen.

The dissection started with the assistant retracting the gallbladder fundus over the liver and the surgeon holding the infundibulum of the gallbladder with one hand. Using a monopolar hook, the visceral peritoneal reflection was taken down at the neck of the gallbladder and, using a Maryland dissector, the cystic duct and artery were dissected by clipping proximally and distally and transecting in the middle. An intraoperative cholangiogram was routinely performed in the early cases, and selectively in performed in cases from 2007. The gallbladder was dissected from the gallbladder fossa using a hook, and then placed in an Endo Catch™ bag (Covidien, Mansfield, MA) and removed through the 12-mm trocar site. 2.1.2. Robot-assisted cholecystectomy The patient was positioned in the reverse Trendelenburg left lateral supine position with arms tucked to the sides. The da Vinci® Surgical System (Intuitive Surgical, Inc., Sunnyvale, CA) was docked cranially, with the arms hovering over the patient's upper abdomen. Port placement is depicted in Fig. 1. A four-port technique was used with a 12-mm trocar right of the umbilicus for the camera, and three 8-mm robotic trocars were placed on either side of the camera. Using a 10-mm 30 camera, a cadiere grasper was placed in the 3rd arm to retract the gallbladder fundus over the liver. A monopolar hook and bipolar grasper were used in the 1st and 2nd arms of the robot, as the surgeon's right- and left-hand instruments. The procedure was performed similar to conventional cholecystectomy. An intraoperative cholangiogram was selectively performed. The da Vinci® Si version offers a dual console, which allows flexibility for the assistant to dynamically manipulate the gallbladder and tissues using the 3rd arm. This can complement the surgeons' movements or can be controlled by the surgeon. Control of the arms can be switched with a tap on a foot pedal. Most of the cholecystectomy-associated procedures involved extensive adhesiolysis, hernia repairs, and bariatric procedures. Our usual practice was to dock the robot soon after the ports were placed and to take down the adhesions with the robotic platform. In procedures such as hernia repair, most often the ports placed for cholecystectomy were used to perform the procedure. Additional ports were placed if needed. In the case of simultaneous bariatric procedure, the bariatric procedure was the index procedure and

Fig. 1. Port positioning for Laparoscopic cholecystectomy (LC) versus Robotic cholecystectomy (RC). LC employed: (A) a 5-mm camera port); (B) a 5-mm surgeon's left-hand instrument port; (C) a 12-mm surgeon's right-hand instrument port; and (D) a 5-mm assistant port. RC employed: (A) a 12-mm camera port; (B) an 8-mm robotic trocar (surgeon's left hand instrument/2nd robotic arm); (C) an 8-mm robotic trocar (surgeon's right hand instrument/1st robotic arm); and (D) an 8-mm robotic trocar (3rd robotic arm).

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cholecystectomy was performed using the bariatric procedure ports. 3. Results 3.1. Laparoscopic cholecystectomy group The 147 patients that underwent LC consisted of 26 males (17.7%) and 121 females (82.3%), with a mean age of 41.1 years and a mean BMI of 31.8 kg/m2. The mean operating time was 89.6 min (range 34e235 min). The mean EBL was 13.8 ml (range 5e100 ml) with a mean LOS of 1.0 day (range 0.2e14.3 days). There were 43 cholecystectomy-associated procedures, including adhesiolysis in 39 patients (90.7%) who had a previous history of surgery. The four remaining additional procedures (9.3%) included common bile duct (CBD) exploration, hernia repair, and esophagogastroduodenoscopy. Due to extensive pericholecystic adhesions in three patients (2.0%), the LC procedures were converted to laparoscopic cholecystostomy and the patients underwent elective LC at a later date. In three patients (2.0%), the procedure was converted to open cholecystectomy due to difficulty in identifying vital structures in the Calot's triangle region. One patient with a previous history of seizure disorder developed generalized seizures during the postoperative period and was managed appropriately with neurology consultation. Postoperative complications included retained CBD stone in one patient which required endoscopic retrograde cholangiopancreatography for stone clearance. Another patient had a CBD injury that was diagnosed in the immediate postoperative period, which was treated via robot-assisted hepaticojejunostomy without any further complications. Another open cholecystectomy patient developed a sub-hepatic abscess with deep-wound infection and was managed with antibiotics and abscess drainage. 3.2. Robot-assisted cholecystectomy group The 179 patients that underwent RC consisted of 30 males (16.7%) and 149 females (83.2%), with a mean age of 40.2 years with a mean BMI of 32.9 kg/m2. Comparative preoperative diagnoses for both groups are shown in Table 1. The mean operating time was 95.7 min (range 37e268 min). The mean EBL was 13.9 ml (range 5e150 ml) with a LOS of 0.9 days (range 0.2e8.2 days). There were 36 cholecystectomy-associated procedures, including adhesiolysis in 23 patients (63.8%) who had a previous history of surgery. Other procedures included 3 hernia repairs (8.3%), 2 intraoperative cholangiograms (5.6%), 2 sleeve gastrectomies (5.6%), and 6 other procedures (16.6%), including cystogastrostomy, endoscopy, hysterectomy, liver biopsy and gastrostomy. In two patients (1.1%), the procedure was converted to open cholecystectomy due to difficulty in identifying structures in the region of Calot's Triangle, as a result of extensive scarring and adhesion. In one of these patients, a partial cholecystectomy was performed to avoid damaging vital structures. Postoperative complications included 6 patients (3.3%) who required hospitalization to manage postoperative complaints. Of these, two were admitted to evaluate abdominal pain. One had right upper-quadrant pain and the second had recurrent pancreatitis. Another patient with preoperative pancreatitis with pseudocyst required endoscopic dilation of cystogastrostomy due to cyst infection. Another patient with bile leak was admitted for percutaneous drainage and endoscopic sphincterotomy, and one patient had to undergo postoperative endoscopic retrograde cholangiopancreatography to remove a CBD stone. One patient required readmission for urinary retention and one patient was treated in the emergency room for postoperative pain.

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Table 1 Comparison of indication and outcomes in LC vs. RC. Variable

LC

RC

P-value

Preoperative diagnosis Symptomatic cholelithiasis Acute cholecystitis Chronic cholecystitis Gall bladder hydrops Cholecystitis with pancreatitis Others (polyp, biliary dyskinesia) BMI in kg/m2, (mean ± SD) Operative time in minutes, (mean ± SD) EBL in ml, (mean ± SD) LOS in days, (mean ± SD) Major complications

74 (50.3%) 29 (19.7%) 21 (14.3%) 7 (4.7%) 4(2.7%) 15 (10.2%) 31.8 ± 7.1 89.6 ± 33.7 13.7 ± 15.9 1.0 ± 1.4 3

76 (42.4%) 41(22.9%) 30 (16.7%) 4 (2.2%) 20 (11.2%) 8 (4.5%) 32.9 ± 7.7 95.7 ± 38.3 13.9 ± 18.1 0.9 ± 1.4 3

0.1a 0.1a 0.9a 0.9a 0.9b

LC, Laparoscopic cholecystectomy; RC, Robotic cholecystectomy; BMI, Body-mass index; SD, Standard deviation; EBL, Estimated blood loss; LOS, Length of stay. a T-test. b Fisher's exact test.

4. Discussion The robotic platform has rapidly gained ground in general surgery procedures. Despite increased robotic procedures, few studies to-date have compared RC with LC. Previously published reports re restricted to small case series that highlighted early surgeon experiences and focused on robotic platforms that are no longer on the market. In a prospective case-matched study of 50 RC patients and 50 LC patients, Breinstein et al. [11] concluded in 2008 that, while RC was safe and valuable, they were unable to justify its use because of the high cost of the robotic system. The authors found no added benefits to the patients versus LC. Heemskerk et al., in 2005 reported similar findings in a series of 24 patients [16]. Nio et al., in 2004 [13] observed that RC requires a significantly longer operative time than LC with no advantage from robotic assistance. Similar findings were echoed by Kornprat et al., in 2006 [12], who concluded that the time lost with equipment setup during the RC procedure prevented it from being considered as more beneficial than LC [12]. A 2003 study by Ruurda et al. [17], however, found that while robot-related activities including equipment set-up led to loss of time during the pre and postoperative phases, the total operating time did not vary considerably between RC and LC. Zhou et al. [14], in their series of 40 patients, found that robotic assistance provided better control of the operative field and had the advantage of increased precision and stability when compared with LC. In a 2012 meta-analysis of randomized clinical trials comparing LC and RC, Gurusamy et al. [18] included six trials with a total of 560 patients. All trials involved small series, had a high risk of systematic errors, and were limited to elective LC procedures. Only one trial of 40 patients reported mortality and morbidity, and there was a lack of data with regard to patient quality-of-life or procedures performed on an outpatient basis. The analysis pointed to a lack of data on acute cholecystitis, where the cases were more complex and a higher proportion of patients developed complications and required conversion to the open procedure. The authors concluded that RC did not provide significant benefits over LC. In our experience, the operative times of RC and LC were not significantly different (P ¼ 0.128; Table 1). This is likely due to the extent of the program and experience at our institution, where advanced robotic procedures are routinely performed across multiple specialties. As a result, our operating team is continually exposed to the robotic platform, leading to decreased procedural time. Because training new team members continues simultaneously, the docking time remains at just a few minutes, even for

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advanced cases. Other factors contributing to decreased set-up time include having a patient-side assistant who has been previously trained in a robotics lab and a surgeon with expertise using this platform that can rapidly troubleshoot any emergent system problems. It is true that the higher level of technically advanced platforms may not make a tremendous difference in outcomes for a basic procedure such as cholecystectomy. However, we concur with Zhou et al. [14] that the platform does provide stable precise movements with a higher degree of freedom, which subjectively translates into a superior quality of dissection. Using an additional robot arm under the control of the surgeon rather than the assistant, for either dynamic or static retraction of the gallbladder or segment 4, also simplifies performing the procedure. In fact, most cases can often be performed with a scrub nurse to exchange the instruments without a patient-side assistant. The current study reported here represents the largest series to-date. It is a single-surgeon experience at a tertiary facility where both the laparoscopic and robotic platforms are routinely applied to diverse complex procedures in multispecialty settings. Laparoscopic cholecystectomy procedures represent the early experience of the surgeon, with a switch to the robotic platform within a very short transition period. Upon adoption, the robotic platform has been applied without discrimination to all cholecystectomy procedures. In fact, 23% of RC patients had a preoperative diagnosis of acute cholecystitis compared to 20% of LC patients, and both groups had similar postoperative outcomes. This indicates that even in patients with acute cholecystitis, the RC procedure can be safely applied. Additionally, most of these cases were performed in an outpatient setting. When analyzing BMI, EBL, hospital stay, surgery duration, and the number of major complications (Table 1), we found no statistical differences between the LC and RC groups. This reinforces some of the findings from previous studies [11]. There was also no mortality in either group. One patient in the LC group experienced a CBD injury when the cystic duct and common hepatic duct were clipped together. This was the result of a difficult dissection during the initial operation. The patient had a preceding history of gallstone pancreatitis that led to gross inflammation in the region of Calot's Triangle. The injury was detected postoperatively when the patient presented with abdominal pain with increased total serum bilirubin. A preoperative ERCP was performed to confirm the diagnosis and a percutaneous transhepatic catheter was placed prior to re-exploration. The patient was reoperated on immediately and a robot-assisted hepaticojejunostomy was performed to bypass the injured CBD segment. The patient has done well and without further incidence, to-date. This situation demonstrates yet another utility of the robotic platform e to manage complications from LC. Advantages of the platform include precision, stability, 3-dimensional visualization, 7 þ 1 degrees of freedom, and a fourth arm to provide assistance. Together, these advantages allow the surgeon to safely undertake difficult bilioenteric anastomoses in the immediate perioperative period, using a minimally invasive approach. As a result, the duration of morbidity from injury is limited, and increased morbidity associated with the open procedure is avoided. We did not examine the cost difference between the platforms because it is already established that RC is more expensive than LC [11]. The real benefit of the robotic platform is many complex procedures that can be offered as a minimally invasive procedure rather than requiring an open approach. Still, because robotics in general surgery is considered an emerging technology, RC can be used to transition into more complex surgeries. In this way, RC should be looked upon as an investment in skill maintenance and development rather than as a no-benefit, high-cost application. In

summary, this single-surgeon large series found that LC and RC are comparable in terms of safety and feasibility in an acute setting, and in long-term patient outcomes. Robotics also has an important potential role in better managing biliary ductal injury during LC. Ethical approval There was no ethical approval necessary for this manuscript. Sources of funding There is no funding associated with this manuscript. Author contribution Ayloo: Data collection, concept and preparation of manuscript and final approval. Roh: Data collection, preparation of manuscript, final approval. Choudhury: Data collection, preparation of manuscript, final approval. Conflict of interest statement No author has any conflict of interest, financial or otherwise, to declare. Acknowledgments Authors like to thank Dr Nishank Jain for statistical analysis. References [1] P.C. Giulianotti, A. Coratti, M. Angelini, F. Sbrana, S. Cecconi, T. Balestracci, et al., Robotics in general surgery: personal experience in a large community hospital, Arch. Surg. 138 (2003) 777e784. [2] M. Talamini, K. Campbell, C. Stanfield, Robotic gastrointestinal surgery: early experience and system description, J. Laparoendosc. Adv. Surg. Tech. A 12 (2002) 225e232. [3] B.P. Jacob, M. Gagner, Robotics and general surgery, Surg. Clin. North Am. 83 (2003) 1405e1419. [4] E.J. Hanly, M.A. Talamini, Robotic abdominal surgery, Am. J. Surg. 188 (2004) 19Se26S. [5] R.E. Link, S.B. Bhayani, L.R. Kavoussi, A prospective comparison of robotic and laparoscopic pyeloplasty, Ann. Surg. 243 (2006) 486e491. [6] B.P. Muller-Stich, M.A. Reiter, M.N. Wente, V.V. Bintintan, J. Koninger, M.W. Buchler, et al., Robot-assisted versus conventional laparoscopic fundoplication: short-term outcome of a pilot randomized controlled trial, Surg. Endosc. 21 (2007) 1800e1805. [7] A.L. Rawlings, J.H. Woodland, R.K. Vegunta, D.L. Crawford, Robotic versus laparoscopic colectomy, Surg. Endosc. 21 (2007) 1701e1708. [8] J.M. DeLong, O. Shapiro, A. Moinzadeh, Comparison of laparoscopic versus robotic assisted partial nephrectomy: one surgeon's initial experience, Can. J. Urol. 17 (2010) 5207e5212. [9] B.M. Benway, S.B. Bhayani, C.G. Rogers, L.M. Dulabon, M.N. Patel, M. Lipkin, et al., Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: a multi-institutional analysis of perioperative outcomes, J. Urol. 182 (2009) 866e872. [10] L.A. Deane, H.J. Lee, G.N. Box, O. Melamud, D.S. Yee, J.B. Abraham, et al., Robotic versus standard laparoscopic partial/wedge nephrectomy: a comparison of intraoperative and perioperative results from a single institution, J. Endourol. 22 (2008) 947e952. [11] S. Breitenstein, A. Nocito, M. Puhan, U. Held, M. Weber, P.A. Clavien, Roboticassisted versus laparoscopic cholecystectomy: outcome and cost analyses of a case-matched control study, Ann. Surg. 247 (2008) 987e993. [12] P. Kornprat, G. Werkgartner, H. Cerwenka, H. Bacher, A. El-Shabrawi, P. Rehak, et al., Prospective study comparing standard and robotically assisted laparoscopic cholecystectomy, Langenbecks Arch. Surg. 391 (2006) 216e221. [13] D. Nio, W.A. Bemelman, O.R. Busch, B.C. Vrouenraets, D.J. Gouma, Robotassisted laparoscopic cholecystectomy versus conventional laparoscopic cholecystectomy: a comparative study, Surg. Endosc. 18 (2004) 379e382. [14] H.X. Zhou, Y.H. Guo, X.F. Yu, S.Y. Bao, J.L. Liu, Y. Zhang, et al., Zeus robotassisted laparoscopic cholecystectomy in comparison with conventional laparoscopic cholecystectomy, Hepatobiliary Pancreat. Dis. Int. 5 (2006) 115e118.

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