Dual-console robotic surgery compared to laparoscopic surgery with respect to surgical outcomes in a gynecologic oncology fellowship program

Dual-console robotic surgery compared to laparoscopic surgery with respect to surgical outcomes in a gynecologic oncology fellowship program

Gynecologic Oncology 126 (2012) 432–436 Contents lists available at SciVerse ScienceDirect Gynecologic Oncology journal homepage: www.elsevier.com/l...

156KB Sizes 0 Downloads 27 Views

Gynecologic Oncology 126 (2012) 432–436

Contents lists available at SciVerse ScienceDirect

Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno

Dual-console robotic surgery compared to laparoscopic surgery with respect to surgical outcomes in a gynecologic oncology fellowship program Ashlee L. Smith a,⁎, Thomas C. Krivak a, Eirwen M. Scott a, Jose Alejandro Rauh-Hain b, Paniti Sukumvanich a, Alexander B. Olawaiye a, Scott D. Richard a a b

Division of Gynecologic Oncology, Magee-Womens Hospital of UPMC, Pittsburgh, PA, USA Division of Gynecologic Oncology, Vincent Obstetrics and Gynecology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

a r t i c l e

i n f o

Article history: Received 29 February 2012 Accepted 13 May 2012 Available online 18 May 2012 Keywords: Dual-console robotic surgery Laparoscopic surgery Gynecologic oncology Fellowship training program

a b s t r a c t Objective. Minimally invasive surgical techniques decrease surgical morbidity and recovery time. Studies demonstrate similar surgical outcomes comparing robotic to laparoscopic surgery. These studies have not accounted for the incorporation of fellow education. With the dual-console da Vinci Si Surgical System®, a two surgeon approach could be performed. We sought to compare surgical outcomes at a gynecologic oncology fellowship program of traditional laparoscopic to robotic surgeries using the dual-console system. Methods. We identified patients who underwent laparoscopic or robotic surgery performed by a gynecologic oncologist from November 2009–November 2010. Robotic surgeries were conducted using the dualconsole, utilizing a two surgeon approach. Surgeries involved a staff physician with a gynecologic oncology fellow. Statistical analysis was performed using student t-test and chi-squared analysis. Results. A total of 222 cases were identified. Cases were analyzed in groups: all cases identified, all cancer cases, and endometrial cancer cases only. When analyzing all cases, no statistical difference was noted in total operating room time (172 vs. 175 min; p = 0.6), pelvic lymph nodes removed (10.1 vs. 9.6; p = 0.69), paraaortic lymph nodes dissected (3.7 vs. 3.8; p = 0.91), or length of stay (1.5 vs. 1.3 days; p = 0.3). There was a significant difference in total surgical time (131 vs.110 min; p b 0.0001) and EBL (157 vs.94 ml; p b 0.0001), favoring robotic surgery. When analyzing all cancer cases, the advantage in total surgical time for robotic surgery was lost. Complications were similar between cohorts. Conclusion. Incorporating fellow education into robotic surgery does not adversely affect outcomes when compared to traditional laparoscopic surgery. © 2012 Elsevier Inc. All rights reserved.

Introduction The 21st century brought with it a movement towards minimally invasive surgery (MIS) in the field of gynecologic oncology [1]. As gynecologic oncologists were exploring and adapting to laparoscopic surgery and practices, the robotic surgical platform emerged as an additional surgical tool to utilize for MIS. The da Vinci Surgical System® (Intuitive Surgical Corporations, Sunnyvale, California, USA) was approved by the Food and Drug Administration for gynecologic surgeries in April 2005 [2]. Currently there are two surgical techniques that allow a surgeon to perform minimally invasive surgeries, traditional laparoscopy and robotic-assisted laparoscopic surgery. This has allowed surgeons to individualize which method to perform for specific patients and procedures. A report by Magrina et al. compared the data on robotic, laparoscopic, and open surgeries [3]. The authors noted that operating times for robotic and open procedures were ⁎ Corresponding author at: Magee-Womens Hospital of UPMC, Department of Gynecologic Oncology, 300 Halket St., Pittsburgh, PA 15213, USA. Fax: + 1 412 641 5417. E-mail address: [email protected] (A.L. Smith). 0090-8258/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.ygyno.2012.05.017

significantly shorter when compared to laparoscopy. Boggess et al. noted that endometrial cancer staging using a robotic-assisted surgical approach was feasible and preferable over laparoscopic or open techniques [4]. Additional studies have drawn similar conclusions, however most have not accounted for the incorporation of resident and fellow education into robotic surgery [1,5–7]. Incorporation of robotic surgery requires the development and understanding of the robotic platform and new surgical skills for both the experienced surgeon and the trainee. With the continued decrease in trainee work duty hours, trainees are exposed to fewer surgical procedures and are faced with the challenge of adapting to new surgical technology as it continues to advance [8]. Simulation models have been developed for MIS training in an effort to improve patient outcomes and safety, all while optimally utilizing operative resources and decreasing the learning curve for these techniques [9]. With the advent of the dual-console da Vinci Si Surgical System® in 2009, a two surgeon approach to gynecologic procedures could be implemented. This new platform would allow for a resident or fellow to operate at the same time as an attending physician. Simulated experience can be improved upon with hands-on training and actual

A.L. Smith et al. / Gynecologic Oncology 126 (2012) 432–436

intra-operative skill development. Through these applications, a new training algorithm has become available for residents and fellows. We sought to compare surgical outcomes and operative times of traditional laparoscopic and robotic surgeries using the dual-console method at a teaching institution. Methods After obtaining Institutional Review Board approval, we retrospectively identified patients who underwent laparoscopic or roboticassisted surgery using the dual-console da Vinci Si Surgical System® performed by a gynecologic oncologist from November 2009–November 2010 at Magee-Womens Hospital of UPMC. Cases were collected concurrently during the noted time period. Decision to perform robotic versus laparoscopic surgery was left to the discretion of the attending physician and the availability of the robotic platform. The cohort of robotic surgery patients came from all robotically trained staff physicians at our institution (SR, AO, and TK). Laparoscopic cases for all gynecologic oncology attendings were included. All patients received appropriate informed consent prior to the procedure. The primary endpoint was total surgical time. Additional endpoints included estimated blood loss (EBL) and complications. Records were reviewed for patients' age, body mass index, pre and post-operative diagnosis, procedure, number of pelvic and/or paraaortic lymph nodes retrieved, total operating room time, and length of hospital stay. For robotically-assisted cases, surgical time was calculated from port placement until the completion of the procedure. Laparoscopic operative time was calculated starting from placement of the laparoscopic ports until completion of the procedure. All procedures were performed with the dual console da Vinci Si Surgical System® with two operating surgeons and at least one bedside assistant. Operating surgeons consisted of an attending staff physician and a gynecologic oncology fellow, each at a surgical console. Four clinical gynecologic oncology fellows were included in this analysis; two were second year clinical fellows and two were first year clinical fellows. A resident physician was utilized as a bedside assistant during these cases for uterine manipulation, suction/irrigation, and specimen extraction as indicated. Staff physicians had completed the required off-site training and proctored cases to be robotically certified. Fellow and resident physicians had received in-house training prior to assisting with the surgery. All laparoscopic cases were completed by an attending physician with a fellow as the co-surgeon. The robotic surgical technique used is similar to that found on the Intuitive Surgical Instructional website for robotic hysterectomy. Uterine manipulation was accomplished with the V-Care uterine manipulator (Conmed, Utica, NY). Three 8 mm robotic trocars, a 12 mm camera port, and a 12 mm bedside assistant port were used. For the purposes of these procedures, the primary surgeon controlled two robotic arms. These instruments were the primary operating instruments for the procedure. The second surgeon controlled the third robotic arm and assisted primarily with retraction and manipulation of the uterus with a da Vinci Prograsp®. Portions of the surgery were shared between the operating surgeons at each console. Fellows were the primary surgeons both laparoscopically and robotically, completing the hysterectomies as well as lymphadenectomies in all patients included in our analysis. Robotically, the attending physicians would assist from the second console as needed but were primarily providing guidance and instruction. For the laparoscopic cases, the same attending–fellow pairs were participating in the roles as previously described. Prior to surgery all patients underwent a mechanical bowel preparation and received appropriate pre-operative antibiotics. DVT prophylaxis consisted of intra-operative pneumatic compression stockings and post-operative Enoxaparin therapy. Patients with a known malignant condition following surgery were identified as “high-risk” for thrombosis and were maintained on outpatient Enoxaparin therapy for fourteen

433

days in accordance with our institution practices. All patients were admitted after their surgery for inpatient observation. Complications were recorded up to 90 days post-operatively. Characteristics of the study population and study endpoints were analyzed and described using usual statistics: mean with standard deviation and 95% confidence intervals (CI). Continuous variables were evaluated by Student's t test or Wilcoxon–Mann–Whitney test, as appropriate. The Kolmogorov–Smirnov test was used to test normal distribution. Categorical variables were evaluated by chi square test or Fisher's exact test as appropriate for category size. Statistical analyses were plotted using SPSS statistical software (version 18.0, SPSS, Inc., Chicago, IL).

Results A total of 222 cases were identified; 106 laparoscopic and 116 robotic cases. Cases were analyzed in groups including all cases performed, all cancer cases, and endometrial cancer cases. All cohorts were similar with regard to demographic information (Table 1). The mean ages for the laparoscopic and robotic cohorts were 58.5 and 55 years old, respectively. With regard to pre-operative diagnosis, 62% of laparoscopic cases and 47% of robotic cases (p = 0.026) had a known diagnosis of cancer. Seventy-four percent of laparoscopic cases and 78% of robotic cases had BMI classifications as overweight, obese, and morbidly obese. When evaluating endometrial cancer cases alone, 70% of laparoscopic cases and 78% of robotic cases had

Table 1 Pre-operative characteristics.

Age (y) Mean BMI (kg/m2) Mean BMI classificationa Underweight Normal weight Overweight Obese Morbidly obese Race Caucasian African American Other Pre-operative diagnosisb Endometrial cancer Dysplasiac Pelvic massd Pelvic paine Cervical cancer High risk of ovarian cancerf Uterine sarcoma

Laparoscopic (n = 106)

Robotic (n = 116)

58.5 (25–91)

55.3 (22–87)

31.0 (18–58)

30.3 (15–53)

2 26 25 18 35

6 19 36 22 33

101 4 1

112 3 1

49 24 20 9 4 2 2

46 31 26 12 3 1 0

a Underweight = BMI b 20, normal weight= BMI 20–24.9, overweight= BMI 25–29.9; obese = BMI 30–34.9; morbidly obese= BMI ≥ 35. b Three laparoscopic cases were performed for two pre-operative indications. As such, the total number of pre-operative diagnoses is three greater than the total number of laparoscopic cases included in the review. Two robotic cases were performed for two preoperative indications. As such, the total number of preoperative diagnoses is two greater than the total number of robotic cases included in the review. c Cases included those performed for endometrial complex atypical hyperplasia, cervical dysplasia, and post-menopausal bleeding. d Cases included those performed for known dysgerminoma, known LMP tumor of the ovary, known ovarian cyst, known carcinoid tumor of the ovary, known granulosa cell tumor, elevated testosterone suspicious for tumor of ovarian origin, and other uncharacterized pelvic masses. e Cases included those performed for dysfunctional uterine bleeding, endometriosis, fibroids, and other uncharacterized pelvic pain. f Cases included those performed for patients with a history of breast cancer or BRCA positivity.

434

A.L. Smith et al. / Gynecologic Oncology 126 (2012) 432–436

BMI classifications as overweight, obese, and morbidly obese. Postoperative diagnosis included 102 benign conditions (46%), 96 endometrial cancer cases (43%), and 24 other malignant conditions (11%) including cervical, ovarian, and sarcoma cases. When analyzing all surgeries, no statistical difference was noted in total operating room time (172 vs. 175 min; p = 0.6), number of pelvic lymph nodes removed (10.1 vs. 9.6; p = 0.69), number of paraaortic lymph nodes dissected (3.7 vs. 3.8; p = 0.91), or length of stay (1.5 vs. 1.3 days; p = 0.3) for laparoscopic vs. robotic-assisted surgeries respectively. There was a significant difference in total surgical time (131 vs.110 min; p b 0.0001) and EBL (157 vs.94 ml; p b 0.0001) both favoring robotic surgery (Table 2). Interestingly, although a number of total para-aortic lymph nodes (PALN) sampled were similar between the two cohorts, surgeons were less likely to perform PALN dissection robotically (84% vs. 63%; p = 0.02) (Table 3). When analyzing all cancer cases and all endometrial cancer cases, the advantage seen in total surgical time for robotic surgery was lost. However, a significant difference in EBL was maintained between the groups again favoring robotic surgery. Although there is a statistically significant difference in EBL between the two surgical methods, this did not translate into a clinically significant difference. There were no differences noted among intra or post-operative transfusion rates between groups. Complications were similar between all cohorts (Table 4). The overall intra-operative complication rates for laparoscopic and robotic cases were 6% and 2.5% (p = 0.201), respectively. Five laparoscopic (4.7%) and 3 robotic (2.5%) cases were converted to open procedures (p = 0.2). For the laparoscopic cases, one case required laparotomy for dense intra-abdominal adhesions. The additional four cases were converted to laparotomy secondary to intra-operative findings of ovarian carcinoma. One robotic case was converted to open surgery for repair an IVC laceration which was encountered during lymphadenectomy. The 2 additional robotic conversions required minilaparotomies for intact specimen extraction. Post-operative complication rates were 12% and 19% (p = 0.199) for laparoscopic and robotic cases respectively. There were 9 (8.5%) wound complications in the laparoscopic group and 13 (11.2%) cases in the robotic group (p = 0.499). Wound complications included both wound infections and seromas. Each group had one case of thrombosis reported. One patient (BMI 36) diagnosed with Stage IB, grade 2, endometrioid adenocarcinoma that underwent a robotic-assisted staging procedure was diagnosed with a PE after presenting with shortness of breath Table 2 Operative results. ADR Total operating room time (min) All cases All malignant cases Endometrial cancer cases Total surgical time (min) All cases All malignant cases Endometrial cancer cases Estimated blood loss all (cc) All cases All malignant cases Endometrial cancer cases Length of stay (days) All cases All malignant cases Total pelvic lymph nodes all cancer cases (n) Mean Positive pelvic lymph nodes (n) Mean Total para-aortic lymph nodes all cancer cases (n) Mean Positive para-aortic lymph nodes (n) Mean

Laparoscopic Robotic p-value 171.7 181.1 175.5

174.9 191.4 193.2

0.605 0.264 0.081

131.3 139.9 132.9

110.6 126.1 125.0

b0.0001 0.081 0.332

157.1 183.5 183.0

94.1 112.5 115.0

b0.0001 0.005 0.023

1.5 1.3

1.3 1.5

0.344 0.388

10.1

9.6

0.695

0.05

0.04

3.7

3.8

0.913

Table 3 Para-aortic lymph node sampling in cases of endometrial cancer.

LN sampling completed LN sampling not completed Percentage

0.03

Robotic

p-value

42 8 84%

29 16 63%

b 0.02

6 weeks post-operatively. In the laparoscopic group, one patient (BMI 31) presented with left lower extremity pain and swelling 7 weeks following her laparoscopic staging surgery for Stage IA, grade 2, endometrioid adenocarcinoma. A left lower extremity DVT was confirmed on imaging. Both patients were started on anticoagulation therapy without any further complications.

Discussion Minimally invasive surgery in gynecology and gynecologic oncology has continued to gain popularity due to improvements in patient outcomes with decreased hospitalization and quicker patient recovery. The ultimate goal is to maximize those procedures that can be performed safely and accurately via a minimally invasive approach with equivalent oncologic outcomes. In 2009, the Gynecologic Oncology Group published results of a multi-center randomized trial which demonstrated favorable surgical outcomes when comparing laparoscopy and laparotomy [1,10]. As more physicians utilized laparoscopic surgery, robotic-assisted minimally invasive procedures have emerged and gained popularity after its approval by the Food and Drug Administration in 2005 for gynecologic procedures [3,11]. A study by Boggess et al. examined the outcomes of all three surgical approaches: laparotomy, laparoscopy, and robotics, when staging endometrial cancer patients. The authors found that mean blood loss and operative times were lower for robotic compared with laparoscopic hysterectomies [4]. Specifically, in the setting of gynecologic oncology, robotic hysterectomy has been found to require more operative time then laparotomy, but it has been shown to be equivalent or superior to laparoscopy in terms of operative time [12,13]. Despite the potential benefits of robotic hysterectomy, studies comparing it with laparoscopic hysterectomy have been small and nonrandomized. The largest systematic review of robotic hysterectomies for endometrial cancer included 589 procedures and found no difference in intra or post-operative complications, transfusion requirements, rates of conversions to laparotomy, operative times, or length of stay between women that were treated with conventional laparoscopic or robotic methods [6]. Results from our current study are consistent with the above noted findings, however only a statistically significant difference is

Table 4 Complications. Laparoscopic

Robotic

p-value

Intra-operative complications Vascular injury Bladder injury Bowel/mesentery injury Vaginal laceration Total

2 1 3 1 7 (6%)

2 1 0 0 3 (2.5%)

0.201

Post-operative complications Wound infection Vaginal cuff complicationa DVT/PE Anemia requiring blood transfusion Fistula Total

8 1 1 2 1 13 (12%)

13 7 1 1 0 22 (19%)

0.199

a

0

Laparoscopic

Vaginal cuff complications included dehiscence, cellulitis, hematoma, bleeding, abscess, and seroma.

A.L. Smith et al. / Gynecologic Oncology 126 (2012) 432–436

maintained when including benign surgeries as well as malignant cases. In comparison to the above cited studies, our experience includes gynecologic oncology fellows operating at the second console. Therefore, some of the difference in surgical time could be attributed to operator skill level, as well as instruction by attending physicians. We also noted little difference in total operating room time between the two groups. This is likely attributed to longer preparation of the patient to ensure secure and proper positioning, docking and undocking of the robotic console, and a longer time to close the larger number of surgical ports. Notably, the time period reviewed reflects some of our initial experiences with the robotic console in this setting. This is also likely to lead to an increase in total operating room time as we familiarize ourselves with and make adjustments to our techniques. We are unable to perform an assessment of fellow training at a single console at our institution for comparison, as this platform is not available to us currently and has been replaced by the dual-console machine. In our study, we noted that surgeons were less likely to perform para-aortic lymphadenectomy robotically as compared to laparoscopically. Decisions to remove lymph nodes for low-grade endometrial cancers at our institution are surgeon dependent. We noted that more low-grade endometrial cancer cases were completed robotically as compared to laparoscopically, potentially accounting for this observed difference. Completion of lymphadenectomy for lowgrade endometrial cancer varies across the attending surgeons that were included in this cohort and not all surgeons opt to complete lymph node dissection in these cases. Sometimes, pelvic lymph node dissections are initiated until the pathologic assessment from the frozen section is obtained. Findings consistent with a low-grade carcinoma often result in discontinuation of the lymphadenectomy, likely resulting in less para-aortic lymph nodes being sampled robotically. Even though complete lymphadenectomies are routinely performed to the level of the renal vessels, lymph node counts at our institution have continuously been reported at numbers lower than what is identified in the literature. Review of this finding has previously identified pathology processing protocols as the source of our reported low lymph node counts. At our institution, serial sectioning is not completed on the tissue bundle and palpation is used to identify lymph nodes, which are then subsequently sectioned. Although lymph node yield is lower than in the reported literature, it is similar for both types of procedures evaluated in our study. Using this identified data allows us to analyze a measure of surgical quality between the two procedures. The authors acknowledge a higher than anticipated wound infection and complication rate with regards to both types of surgical techniques. We attribute this wound complication rate to several factors in our operative setting, which have since been modified following their identification in this review. Modifications to sterile preparation of the patient and sterile draping of the patient have been carried out. Specifically, our institution has switched from sterile preparation with Hibiclens® to ChloraPrep®. We have noted an observational difference in the rate of wound infections and wound seromas since altering our practice. There is little data published evaluating mean operative time, patient outcomes, and surgical complications using the dual-console da Vinci Si Surgical System® in a teaching environment. A recently published manuscript cited the benefits of the dual-console robotic training approach, however it should be noted that the assistant at the second console was participating primarily in tissue retraction as compared to actual completion of the surgery [14]. In our training program, fellows participate and complete significant portions of the surgery, including the hysterectomy and lymphadenectomy with the guidance and instruction of the attending physician at the second console. However, one of the limitations to our study is that specific portions of the cases were not recorded and timed for fellow vs. attending procedure completion. Total surgical time was identified

435

as one of the primary endpoints to be consistent with endpoints currently cited in the literature [4,5,15,16]. Although most of these manuscripts do not incorporate fellow training, we felt it would be important to use this consistent endpoint to demonstrate that this technique is feasible in this environment. In 2008 a survey of SGO members was performed by Mabrouk et al., 76% of respondents reported no or limited laparoscopic training during their fellowship, and 78% now believe that maximum emphasis should be placed on laparoscopic training [17]. When a similar survey was completed in 2004, only 55% of respondents noted a high importance of minimally invasive surgery, suggesting that across the field more emphasis is being placed on MIS techniques [18]. From this same group surveyed, only 24% indicated that they performed robotic-assisted surgery in 2008. Utilization of the dualconsole allows fellows to obtain exposure to these techniques and affords surgeons another option in the realm of minimally invasive surgery. A major impediment to robotic surgery success is the associated learning curve, which applies to both the surgeon and the surgical team. Lenihan et al. demonstrated that the learning curve for benign conditions stabilized at 95 min after having completed 50 cases [19]. Similar improvements in operative time have been noted in gynecologic oncology, however none of these reviews has evaluated the use of the dual-console system [2]. It has been determined that approximately 20–25 surgical robotic cases are required to obtain proficiency using this technique [20,21]. A recent study by Lim et al. established that the learning curve for robotic surgeries at their institution required half the number of cases for proficiency when compared to the same cases completed laparoscopically [16]. This could in part be due to the overall increase in exposure of physicians to laparoscopy prior to adopting robotic surgery. However, the mean operative time in this study for completion of a TRH/PPLAND was 147.2 ± 48.2 min. The mean operative time differed by only 38.1 min when comparing the surgeons times from before and after their 24th cases. We believe that utilization of the dual-console system allows a second surgeon the opportunity to gain robotic experience, which will allow for improvement in instruction and earlier proficiency. Importantly, our study examines the outcomes of various surgical teams of attendings and fellows that perform both robotic and laparoscopic surgery together allowing us both opportunities to examine the outcomes from these two types of MIS procedures. Recently, studies emphasizing cost effectiveness of these various surgical methods have been published in the literature. Concerns are continuously expressed regarding the costs of acquiring and maintaining robotic systems. In a study by Wright et al. the authors performed a population-based analysis to compare laparoscopic and robotic-assisted hysterectomies for endometrial cancer [22]. From their multivariate analysis, they found that robotic hysterectomy was more costly ($1,291; (95% CI, $985 to $1,597). Another study by Martino et al. evaluated post-operative pain management and costs in endometrial cancer patients who underwent robotic or laparoscopic-assisted hysterectomy [5]. Patients undergoing robotic surgery had a lower initial post-operative pain score, a 50% reduction in pain medication costs on the day of surgery, and a 56% cost reduction for the rest of their stay. It is important to note the differences in endpoints compared between these cited manuscripts. Although not the scope of this paper, the authors acknowledge the issues of cost effectiveness and expenses related to robotic surgery and advancing technology. By improving precision and dexterity, robotic technology allows the surgeon to perform operations that were previously not amenable to minimally invasive surgery or were very difficult for many gynecologic oncologists and therefore not readily adapted as a type of surgery that would be performed via MIS techniques. This is especially true for patients that are morbidly obese. Using the dual-console robotic system has allowed us at our institution to develop and

436

A.L. Smith et al. / Gynecologic Oncology 126 (2012) 432–436

optimize techniques and surgeries that are safe, effective, and beneficial to patients who were not previously laparoscopic candidates. It has allowed for the development of a training module that can be used among physicians with various levels of experience. In our training environment, operating with the dual-console da Vinci Si® is a safe and feasible option for completion of hysterectomies and staging procedures. Utilizing the dual-console allows for integrated teaching, surgical cooperation with proctoring and supervision, without compromising operative times or patient outcomes. Conflict of interest statement No conflict of interest.

Acknowledgments/disclosures The authors have no personal or financial affiliations to disclose. References [1] Bandera CA, Magrina JF. Robotic surgery in gynecologic oncology. Curr Opin Obstet Gynecol Feb 2009;21:25–30. [2] Sfakianos GP, Frederick PJ, Kendrick JE, Straughn JM, Kilgore LC, Huh WK. Robotic surgery in gynecologic oncology fellowship programs in the USA: a survey of fellows and fellowship directors. Int J Med Robot Dec 2010;6:405–12. [3] Magrina JF, Kho RM, Weaver AL, Montero RP, Magtibay PM. Robotic radical hysterectomy: comparison with laparoscopy and laparotomy. Gynecol Oncol Apr 2008;109:86–91. [4] Boggess JF, Gehrig PA, Cantrell L, Shafer A, Ridgway M, Skinner EN, et al. A comparative study of 3 surgical methods for hysterectomy with staging for endometrial cancer: robotic assistance, laparoscopy, laparotomy. Am J Obstet Gynecol Oct 2008;199:360.e1–9. [5] Martino MA, Shubella J, Thomas MB, Morcrette RM, Schindler J, Williams S, et al. A cost analysis of postoperative management in endometrial cancer patients treated by robotics versus laparoscopic approach. Gynecol Oncol Dec 2011;123: 528–31. [6] Gaia G, Holloway RW, Santoro L, Ahmad S, Di Silverio E, Spinillo A. Robotic-assisted hysterectomy for endometrial cancer compared with traditional laparoscopic and laparotomy approaches: a systematic review. Obstet Gynecol Dec 2010;116:1422–31. [7] Hoekstra AV, Morgan JM, Lurain JR, Buttin BM, Singh DK, Schink JC, et al. Robotic surgery in gynecologic oncology: impact on fellowship training. Gynecol Oncol Aug 2009;114:168–72.

[8] Geller EJ, Schuler KM, Boggess JF. Robotic surgical training program in gynecology: how to train residents and fellows. J Minim Invasive Gynecol Mar-Apr 2011;18: 224–9. [9] Aggarwal R, Tully A, Grantcharov T, Larsen CR, Miskry T, Farthing A, et al. Virtual reality simulation training can improve technical skills during laparoscopic salpingectomy for ectopic pregnancy. BJOG Dec 2006;113:1382–7. [10] Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, et al. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group Study LAP2. J Clin Oncol Nov 10 2009;27:5331–6. [11] Field JB, Benoit MF, Dinh TA, Diaz-Arrastia C. Computer-enhanced robotic surgery in gynecologic oncology. Surg Endosc Feb 2007;21:244–6. [12] Bell MC, Torgerson J, Seshadri-Kreaden U, Suttle AW, Hunt S. Comparison of outcomes and cost for endometrial cancer staging via traditional laparotomy, standard laparoscopy and robotic techniques. Gynecol Oncol Dec 2008;111: 407–11. [13] Estape R, Lambrou N, Diaz R, Estape E, Dunkin N, Rivera A. A case matched analysis of robotic radical hysterectomy with lymphadenectomy compared with laparoscopy and laparotomy. Gynecol Oncol Jun 2009;113:357–61. [14] Marengo F, Larrain D, Babilonti L, Spinillo A. Learning experience using the double-console da Vinci surgical system in gynecology: a prospective cohort study in a university hospital. Arch Gynecol Obstet Feb 2012;285:441–5. [15] ElSahwi KS, Hooper C, De Leon MC, Gallo TN, Ratner E, Silasi DA, et al. Comparison between 155 cases of robotic vs. 150 cases of open surgical staging for endometrial cancer. Gynecol Oncol Feb 2012;124:260–4. [16] Lim PC, Kang E, Park do H. A comparative detail analysis of the learning curve and surgical outcome for robotic hysterectomy with lymphadenectomy versus laparoscopic hysterectomy with lymphadenectomy in treatment of endometrial cancer: a case-matched controlled study of the first one hundred twenty two patients. Gynecol Oncol Mar 2011;120:413–8. [17] Mabrouk M, Frumovitz M, Greer M, Sharma S, Schmeler KM, Soliman PT, et al. Trends in laparoscopic and robotic surgery among gynecologic oncologists: a survey update. Gynecol Oncol Mar 2009;112:501–5. [18] Frumovitz M, Ramirez PT, Greer M, Gregurich MA, Wolf J, Bodurka DC, et al. Laparoscopic training and practice in gynecologic oncology among Society of Gynecologic Oncologists members and fellows-in-training. Gynecol Oncol Sep 2004;94: 746–53. [19] Lenihan Jr JP, Kovanda C, Seshadri-Kreaden U. What is the learning curve for robotic assisted gynecologic surgery? J Minim Invasive Gynecol Sep-Oct 2008;15: 589–94. [20] Lim PC, Kang E, Park do H. Learning curve and surgical outcome for robotic-assisted hysterectomy with lymphadenectomy: case-matched controlled comparison with laparoscopy and laparotomy for treatment of endometrial cancer. J Minim Invasive Gynecol Nov-Dec 2010;17:739–48. [21] Seamon LG, Cohn DE, Richardson DL, Valmadre S, Carlson MJ, Phillips GS, et al. Robotic hysterectomy and pelvic–aortic lymphadenectomy for endometrial cancer. Obstet Gynecol Dec 2008;112:1207–13. [22] Wright JD, Burke WM, Wilde ET, Lewin SN, Charles AS, Kim JH, et al. Comparative effectiveness of robotic versus laparoscopic hysterectomy for endometrial cancer. J Clin Oncol Mar 2012;30(8):783–91.