Perioperative Outcomes in Robotic-Assisted Versus Conventional Laparoscopic Treatment of Endometrial Cancer

Abstract

Objective:

To compare perioperative outcomes of robotic-assisted laparoscopic surgery (RALS) versus conventional laparoscopic surgery (CLS) in endometrial cancer.

Methods:

This is a retrospective analysis of a prospectively maintained database of procedures performed from January 2009 to January 2014 by a single surgeon experienced in both minimally invasive techniques. One hundred five patients underwent surgical staging of endometrial cancer through either conventional laparoscopy (CL) or robotic-assisted laparoscopy. Characteristics such as age, body mass index (BMI), prior abdominal surgery, number of comorbidities, stage of disease, and extent of surgery were compared. Outcomes, including estimated blood loss (EBL), operating room time (ORT), length of stay (LOS), number of lymph nodes resected, conversion rates, and intraoperative and postoperative complications, were analyzed.

Results:

Fifty-seven patients received RALS; 48 had CLS. RALS patients had a higher mean BMI (38.1 ± 11.8 vs. 30.1 ± 7.5 kg/m²; p = 0.0003) and more comorbidities. Median ORT was longer for RALS patients [277 (135–660) vs. 223.5 (120–547) minutes; p = 0.0012]. RALS ORT remained significantly longer for BMI ≥25 kg/m² to <30 kg/m², and appeared near significance in the BMI <25 kg/m² and BMI >35 kg/m² groups. Only in the BMI ≥30 kg/m² to <35 kg/m² group there was no apparent difference in the ORT. Among patients with endometrioid adenocarcinoma histology, ORT was longer in the RALS group [273 (135–660) vs. 222 (120–420) minutes; p = 0.0018]. There was no difference in EBL or LOS between the two surgical approaches.

Conclusions:

In our experience, perioperative outcomes of endometrial cancer staging are comparable between RALS and CL. Furthermore, the overall ORT is significantly longer in the RALS group. Further studies of patients stratified by BMI are needed.

Introduction

Endometrial cancer is the most common gynecologic cancer in the United States. In 2015, ∼54,870 new cases of uterine cancer are estimated to be diagnosed and ∼10,170 deaths are projected.¹ The mean age of diagnosis is 63 years with a lifetime risk of ∼2.7%.² The majority of uterine cancers are diagnosed at an early stage with an overall 5-year survival of ∼74% to 90%.³

Minimally invasive techniques have taken a leading role in the treatment of gynecologic cancers. The introduction of robotic-assisted laparoscopic surgery (RALS) (DaVinci^®; Intuitive Surgical, Sunnyvale, CA) has brought a new wave of innovations to the surgical arena. Most advantages are its use in surgically challenging cases, such as patients with prior abdominal surgeries, obesity, or severe adhesive disease.⁴ Major institutions have included RALS as an option in the treatment of malignancies, and the technique is now available in the majority of teaching institutions.

One reason for the sudden institutional uptake of RALS is the long learning curve associated with conventional laparoscopic surgery (CLS). RALS addresses common problems of CLS, such as fatigue and muscle strain, that are minimized by having the surgeon sit ergonomically at a console, improved imaging and instrument control, by eliminating two-dimensional imaging and counterintuitive hand movements. Several studies have described the large number of surgeries needed to become proficient in CLS for treatment of gynecologic cancers.^5,6

There are limited data comparing outcomes of RALS with those of CLS for treatment of endometrial cancer. Most studies have compared RALS with laparotomy.^7–13 In addition, most studies comparing the various surgical techniques include several surgeons, whose potential differences in skill level may introduce a confounding variable into results.

Recently, RALS has come under scrutiny: it has been reported that laparotomy and CLS are more cost-effective, whereas the literature showing surgical benefits of RALS over CLS in endometrial cancer is limited.^14–18

There has been an exponential increase in the use of RALS for gynecologic surgeries since its Food and Drug Administration approval in 2005. In all specialties, studies should define any scenarios, including patient characteristics and procedure types, in which RALS provides clear benefits.¹⁸ Such information will allow appropriate treatment choices to be made, for the physical health of patients and financial well-being of the health care system. We report the experience of a single surgeon with RALS versus conventional laparoscopy (CL) in early and advanced stage endometrial cancer and compare perioperative outcomes, including intraoperative and postoperative complications, as well as oncologic outcomes such as lymph node sampling.

Materials and Methods

This is a retrospective analysis of a prospectively maintained database from January 2009 to January 2014 of CL and RALS performed for the surgical staging of endometrial carcinoma. Institutional review board approval was obtained and data were collected from two urban university-affiliated community hospitals in the aforementioned time period. The same board-certified gynecologic oncologist performed the surgeries with the assistance of a fellow in minimally invasive gynecologic surgery and a resident.

Demographic data included age, race, body mass index (BMI; calculated as weight in kilograms/square of height in meters), and previous abdominal or pelvic surgical procedures. Surgical data included a description of the procedure performed; estimated blood loss (EBL) as the amount of fluid in the suction canister at the end of the procedure, minus the total amount of irrigation; operating room time (ORT), defined as starting at the first surgical incision to the completion of all skin closures; intraoperative complications; postoperative complications; and length of stay (LOS) as measured in days, with patients discharged the day of surgery considered to have an LOS of 1 day. In all cases, the postoperative course was monitored for 30 days. Parameters such as the hospital LOS and postoperative complications were collected.

The surgical device used for RALS was the DaVinci surgical platform (Intuitive Surgical). Within each group (CLS or RALS), techniques and instrumentation were uniformly employed. Complete details on surgical techniques and instrumentation have been published elsewhere.^19–21

Preoperative endometrial sampling results and intraoperative gross inspection and/or frozen section were used to make decisions regarding performance or omission of lymphadenopathy. The incidence of lymph node metastasis is low in patients with low-risk endometrial carcinoma and, therefore, lymphadenopathy in these patients was not performed. Comprehensive pelvic and para-aortic lymphadenopathy was performed in patients with intermediate- and high-risk endometrial cancer.

The Wilcoxon rank-sum test was used to compare median ORT, EBL, and LOS between CLS and RALS groups overall and within the endometrioid and serous/clear cell histologic subgroups. The Wilcoxon rank-sum test was also used to compare median ORT between the CLS and RALS groups after stratification by BMI. The Fisher's exact test was used to compare intraoperative and postoperative complications between the CLS and RALS groups. All statistical analyses were performed using SAS version 9.2 (SAS Institute, Inc., Cary, NC). For all estimates, the threshold for statistical significance was set at the 0.05 level of significance.

Results

One hundred five patients underwent minimally invasive endometrial cancer staging during the study period and were included; among them were 57 RALS and 48 CLS patients. The procedures included total hysterectomy, bilateral salpingo-oophorectomy, with or without pelvic and para-aortic lymphadenectomy, cystoscopy, and treatment of any associated pathology such as adhesions or endometriosis. Pelvic and para-aortic lymphadenectomy and partial omentectomy were performed based on the preoperative histology and grade of the tumor as well as intraoperative determination of the depth of myometrial invasion.²²

As shown in Table 1, mean BMI in both treatment groups was above the obesity weight status; however, in the RALS group, it was significantly higher than in the CLS group (38.1 ± 11.8 vs. 30.1 ± 7.5; p = 0.0003). The two groups were similar in age (RALS vs. CLS, 60.3 ± 10.2 vs. 63.1 ± 11.1; p = 0.18). Each patient was categorized as having either 0 to 2 or ≥3 comorbidities, with more RALS patients falling into the ≥3 category (p = 0.0156). Thirty (54%) patients in the RALS group had undergone previous abdominal surgery versus 24 (55%) of the CLS patients; in this regard, the groups were statistically equivalent (p = 0.92).

Table 1.

Patient Characteristics

	CL (N = 48)	Robotic-assisted laparoscopy (N = 57)	p
Age	63.06 (11.09)	60.25 (10.17)	0.1779
BMI, mean (SD)	30.74 (7.51)	38.07 (11.76)	0.0003
Comorbidities, n (%)			0.0941
0–2	39 (81)	35 (61)	0.0156
≥3	9 (19)	22 (39)	0.0156
Prior abdominal surgeries, n (%)	24 (55)	30 (53)	0.9227
Pathology
FIGO grade, n (%)			0.4068
1	27 (56)	32 (56)	0.3536
2	6 (13)	11 (19)
3	15 (31)	14 (25)
Stage, n (%)
I	38 (79)	47 (82)	0.1664
II	1 (2)	4 (7)
III	8 (17)	5 (9)
IV	1 (2)	1 (2)
Histology, n (%)
Endometroid	40 (83)	46 (81)	0.9570
Serous/clear cell	8 (17)	11 (19)	0.9570

BMI, body mass index; CL, conventional laparoscopy; FIGO, International Federation of Gynecology and Obstetrics; SD, standard deviation.

International Federation of Gynecology and Obstetrics (FIGO) grade, stage, and histologic type of endometrial cancer are reviewed in Table 1. The proportion of endometrioid to serous/clear cell histology was the same in both groups (p = 0.9570), with endometrioid histology predominant at 83%. Pelvic lymphadenectomy was performed in 38 of 57 (66.7%) cases in the RALS group and in 31 of 48 (64.58%) cases of the CLS group. Para-aortic lymphadenectomy was performed in 18 of 57 (31.6%) cases of the RALS group and 12 of 48 (25%) cases of the CLS group. There was no significant difference in mean number of lymph nodes resected in cases who had both pelvic and para-aortic lymph node resection between RALS group and CLS group (26.3 ± 11.4 vs. 25.8 ± 8.7; p = 0.89). No significant difference was observed in number of positive lymph nodes between RALS group and CLS group (19/738 vs. 15/549; p = 0.86).

As seen in Table 2, median ORT was significantly longer in the RALS group than in the CLS group [277 (135–660) vs. 223.5 (120–547) minutes; p = 0.0012]. After stratifying both groups by BMI, ORT remained significantly longer for RALS versus CLS when BMI was ≥25 kg/m² and <30 kg/m² [293 (171–453) vs. 222 (120–268) minutes; p = 0.0151]; in addition, longer ORT for RALS appeared to approach significance in both the BMI <25 kg/m² and BMI >35 kg/m² categories as well. Only in the BMI ≥30 kg/m² and <35 kg/m² group was there no appearance of a difference (Table 3). When comparing all patients with endometrioid cancers, ORT was also significantly longer in the RALS group [273 (135–660) vs. 222 (120–420) minutes; p = 0.0018]. However, no difference in ORT was observed between RALS and CLS for serous/clear-cell carcinomas [278 (220–453) vs. 281 (202–547) minutes; p = 0.89]. Furthermore, there was no statistically significant difference in EBL or LOS between the overall RALS and CLS groups, nor in their histologic subgroups.

Table 2.

Surgical Outcomes

	CL (N = 48)	Robotic-assisted laparoscopy (N = 57)	p
ORT	223.50 [120–547]	277 [135–660]	0.0012
EBL	150 [50–1300]	150 [50–2000]	0.7848
LOS	2 [1–9]	2 [1–21]	0.9714
Intraoperative complications	1 (2%)	6 (11%)	0.1166
Postoperative complications	1 (2%)	7 (13%)	0.0647

EBL, estimated blood loss; LOS, length of stay; ORT, operating room time.

Table 3.

Differences in Operating Room Time After Body Mass Index Stratification

	CL ORT (minutes)	Robotic-assisted laparoscopy ORT (minutes)	p
BMI <25 kg/m² (RALS N = 13; CLS N = 7)	224 [147–547]	278 [212–366]	0.1697
BMI ≥25 kg/m² and <30 kg/m² (RALS N = 14; CLS N = 10)	222 [120–268]	294 [171–453]	0.0151
BMI ≥30 kg/m² and <35 kg/m² (RALS N = 9; CLS N = 7)	228 [215–420]	239 [206–443]	1.0000
BMI ≥35 kg/m² (RALS N = 12; CLS N = 32)	227 [174–362]	273[135–660]	0.1096

CLS, conventional laparoscopic surgery; RALS, robotic-assisted laparoscopic surgery.

In Table 4, it can be seen that neither intraoperative nor postoperative complications were statistically different between the RALS and CLS groups [intraoperative, 6 (11%) vs. 1 (2%); p = 0.12 and postoperative, 7 (13%) vs. 1 (2%); p = 0.06], but would have likely reached statistical significance with a larger cohort. Although no difference was seen among the two surgical groups, once patients were stratified by BMI, regardless of type of surgery, we found that in class III obese patients (BMI ≥40 kg/m²), there were more postoperative complications than nonobese patients (BMI <30 kg/m²) [6 (18%) vs. 1 (2%); p = 0.038].

Table 4.

Complications

	CL	Robotic-assisted laparoscopy
Intraoperative complications
Transection of left genitofemoral nerve		1
Obturator nerve transection		1
Ureteral injury		1
Right external illiac vein injury		1
Sigmoid thermal injury		1
Cystotomy		2
Postoperative complications
ARDS, SBO, urosepsis, pneumonia		1
SBO		1
Hydronephrosis (ureteral stricture)		1
Pelvic hematoma	1	1
Vaginal cuff deshicensce		1
Laparotomy conversions		1

ARDS, acute respiratory distress syndrome; SBO, small bowel obstruction.

One conversion to laparotomy was performed in the RALS group. In that case, during pelvic lymphadenectomy, a patient with BMI of 45.8 kg/m² received a right external iliac vein injury due to monopolar electrosurgical sparking; after a failed attempt to repair the injury robotically, the procedure was converted to laparotomy.²³ One RALS patient with multiple comorbidities suffered postoperative complications and prolonged hospitalization (LOS = 21 days). She was first diagnosed with acute respiratory distress syndrome requiring intensive care unit treatment, and subsequently had pneumonia, a small bowel ileus, and urosepsis. These complications were managed medically.

Discussion

Surgical staging for endometrial cancer was traditionally performed through laparotomy. With the advent of laparoscopy, novel instrumentation, and new techniques, surgical staging for endometrial cancer has now evolved into a minimally invasive approach.

Laparoscopy has now become the standard of care for endometrial cancer surgery and its advantages over laparotomy are well documented.^10,24 The largest randomized study to date, comparing laparoscopy with laparotomy, the GOG Lap2 study gave us an insight into the advantages of CL over laparotomy when treating endometrial cancer.^10,25,26 The results showed that laparoscopic surgery is feasible and safe. Mean operative time was significantly longer in the CLS group, however, the LOS was significantly lower than that in laparotomy. The conversion to laparotomy occurred in 25.8% of cases, primarily because of poor exposure, and was dependent on BMI (17.5% among patients with a BMI of 25 kg/m² or less, 26.5% among patients with a BMI of 34 to 35 kg/m², and 57.1% among patients with a BMI >40 kg/m²). Complication rates were similar regardless of the surgical approach.^25,26

It has been widely believed that the most likely candidates to benefit from minimally invasive techniques are the surgically challenging patients. Most endometrial cancer patients fit this description due to associated obesity, and subsequently, multiple comorbidities. As obesity rate increases in the United States, endometrial cancer can also be expected to rise, making it vital to understanding the benefits of different minimally invasive surgical approaches.

Although RALS has not been compared prospectively with CLS in a randomized trial, RALS seems to have a shorter learning curve and similar benefits.²⁷ Furthermore, EBL appears lower in the RALS group.²⁸ Several studies have reported improved ORT and overall outcomes of RALS when compared with CLS for treatment of endometrial cancer.^28–30 Coronado et al. performed a retrospective review of 71 patients undergoing RALS and 84 patients undergoing CLS at a single institution.²⁸ The majority of their patients, similarly to our cohorts, had endometrioid adenocarcinoma, but in contrast, their surgeries had a lower mean rate of lymph node resection and lower mean BMI. They reported the operative time as the time lapse from when the patient was anesthetized until the end of the surgery, and reported a shorter mean ORT in the RALS group than in the CLS group [189.2 ± 35.4 vs. 218.2 ± 54.3 minutes; p = 0.000]. Gehrig et al. performed a retrospective review of 49 obese patients undergoing RALS from 2008 to 2009 and compared them with a historic cohort of 32 obese patients undergoing CLS from 2004 to 2005 at a single institution by several surgeons.²⁹ Similar to our study, the majority of their patients had endometrioid adenocarcinoma and underwent lymph node resection. Although Gehrig et al. did not specify how ORT was determined, they reported a shorter mean ORT in the RALS group than the CLS group [189 (111–263) vs. 215 (156–324) minutes; p = 0.0004], and a lower mean EBL in the RALS group than in the CLS group [50 (25–300) vs. 150 (50–700); p ≤ 0.0001]. Boggess et al. performed a retrospective review of 103 patients who underwent RALS and compared them with a historic cohort of 81 patients who underwent CLS for endometrial cancer by a single surgeon.³⁰ However, they did not report on endometrial cancer type. The majority of their patients underwent pelvic and para-aortic lymph node resection with an average of 17.4 for pelvic and 6.3 for para-aortic in the laparoscopic group, and 20.5 and 12.0 in the robotic group, respectively. However, their robotic group had a lower BMI than our cohort. In this particular study, the ORT, measured from the time of skin incision to skin closure, was reported to have a shorter mean ORT in the RALS group than in the CLS group [191.2 ± 36.0 vs. 213.4 ± 34.7 minutes; p < 0.0001].³⁰

Although the aforementioned studies reported improved ORT and other outcomes for RALS when compared with CLS, we found the opposite with respect to ORT, and no difference in other parameters. Our RALS group had a longer ORT than our CLS group [277 (135–660) vs. 223.5 (120–547) minutes; p = 0.0012].

It is our belief that this study provides a more significant comparison between the RALS and CLS treatment groups than the mentioned studies. Whereas we compared two groups, comprised mostly of obese patients undergoing complex procedures and performed by a single surgeon during the same time period, other studies compare RALS patients from a set time period with a historical CLS cohort or lower complexity surgeries. Comparing patients with a historical cohort can be biased because of likely changes in surgeon's skill, operating room efficiency, and documentation, among other factors. Therefore, this study is likely to be free of some of the confounding variables found in the aforementioned studies.

Although, in this study, the RALS group had a higher BMI than the CLS group, both groups had a mean BMI above the obesity threshold. As described in Table 3, after stratification of both treatment groups by BMI, ORT remained significantly longer among RALS patients than among CLS patients, in patients with BMI ≥25 kg/m² and <30 kg/m², and appeared longer in the BMI <25 kg/m² and BMI >35 kg/m² group as well. Power to detect a difference is reduced when groups are stratified by BMI; larger number of patients in comparable BMI categories may be required to ascertain the role of BMI on ORT. However, our results show a generally longer ORT with RALS than in CLS.

Leitao et al. showed that the ORT was similar in CLS and RALS, among various surgeons, following a learning curve of 40 cases.³¹ In contrast, despite our surgeon being past the learning curve, we found a higher ORT in the RALS group. In more complex surgeries, RALS would be expected to be beneficial; however, in our serous or clear-cell subtypes, there was no difference in ORT between RALS and CLS [278 (220–453) vs. 281 (202–547) minutes; p = 0.89]. These findings are in agreement with reports by other authors.¹⁷

The majority of our patients had early-stage disease, FIGO Grade 1, stage IA. In our series of patients, no lymph node resection was aborted due to technical difficulties.

Owing to the difficulty of arranging for large prospective studies comparing RALS with CLS, we are only now beginning to understand the costs and benefits of minimally invasive surgery. By contrast, most studies evaluating minimally invasive treatments for endometrial cancer are small, retrospective studies comparing laparotomy with either RALS or CLS.^{7–9,11,12,32–35} Our group has previously reported on similar outcomes when comparing RALS with CLS in other types of gynecologic cancer.^20,21

Expenses related to surgery can be broadly divided into operating room and hospitalization costs. Operating room costs are higher in association with CLS and RALS, whereas hospitalization costs are higher in patients undergoing laparotomy. In a cost analysis of RALS and CLS for endometrial cancer, RALS was found to be more expensive than CLS; however, this difference declined as surgeon volume increased.¹⁷

The main limitations of this study are its retrospective nature, and as discussed, its small sample size, especially in the number of comparable patients. Another limitation of this study is that although a single surgeon performed the cases, fellows and residents were involved given that our practice is in an academic setting. There have been reports of >26 minutes of total added time for teaching cases versus nonteaching cases.²⁹ One of this study's strengths was that it followed results of a single surgeon experienced in both approaches, limiting the effect of different surgeons and their correspondingly different skills.

Given the high incidence of obesity in endometrial cancer, future studies should focus on determining which minimally invasive technique is most beneficial in this subgroup of patients. To date, we are aware of only one study comparing minimally invasive techniques in obese patients, which showed improved outcomes in RALS when compared with CLS.²⁹ In this study, when stratifying by BMI, we observed that class III obese patients undergoing minimally invasive surgery have more postoperative complications than their nonobese counterparts [6 (18%) vs. 1 (2%); p = 0.038]. This finding is different from that of Helm et al., who report no association between BMI and postoperative complications.³⁶ Although BMI can affect the type of surgery used and the types of complications, currently there are no large prospective studies from single surgeons comparing both. To our knowledge, this is the first report comparing outcomes between RALS and CLS in endometrial cancer staging performed by a single surgeon, with both groups of procedures occurring during the same time period.

In conclusion, there are many reports on improved outcomes with RALS over CLS. However, in the hands of a surgeon experienced in both techniques, we did not find any obvious advantage to RALS when performing surgical stating for endometrial cancer, other than the surgeon's comfort during the procedure. Although the long learning curve associated with CL has kept many surgeons from embracing minimally invasive surgery, RALS will allow more surgeons to offer various techniques to their patients.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Siegel

, Miller

, Jemal

. Cancer statistics, 2015. CA Cancer J Clin, 2015; 65:5.

Howlader

, Noone

, Krapcho

, et al., eds. SEER Cancer Statistics Review, 1975–2011. Bethesda, MD: National Cancer Institute.

Lewin

, Herzog

, Barrena Medel

, Deutsch

, Burke

, Sun

, Wright

. Comparative performance of the 2009 International Federation of Gynecology and Obstetrics' staging system for uterine corpus cancer. Obstet Gynecol, 2010; 116:1141.

El Hachem

, Acholonu

Jr. , Nezhat

. Postoperative pain and recovery after conventional laparoscopy compared with robotically assisted laparoscopy. Obstet Gynecol, 2013; 121:547.

Altgassen

, Possover

, Krause

, Plaul

, Michels

, Schneider

. Establishing a new technique of laparoscopic pelvic and para-aortic lymphadenectomy. Obstet Gynecol, 2000; 95:348.

Lin

, Frey

, Huang

. Learning curve analysis of the first 100 robotic-assisted laparoscopic hysterectomies performed by a single surgeon. Int J Gynaecol Obstet, 2014; 124:88.

Bernardini

, Gien

, Tipping

, Murphy

, Rosen

. Surgical outcome of robotic surgery in morbidly obese patient with endometrial cancer compared to laparotomy. Int J Gynecol Cancer, 2012; 22:76.

Seamon

, Bryant

, Rheaume

, et al. Comprehensive surgical staging for endometrial cancer in obese patients: Comparing robotics and laparotomy. Obstet Gynecol, 2009; 114:16.

Subramaniam

, Kim

, Bryant

, et al. A cohort study evaluating robotic versus laparotomy surgical outcomes of obese women with endometrial carcinoma. Gynecol Oncol, 2011; 122:604.

10.

Walker

, Piedmonte

, Spirtos

, et al. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group Study LAP2. J Clin Oncol, 2009; 27:5331.

11.

Fader

, Seamon

, Escobar

, et al. Minimally invasive surgery versus laparotomy in women with high grade endometrial cancer: A multi-site study performed at high volume cancer centers. Gynecol Oncol, 2012; 126:180.

12.

Farache

, Alonso

, Ferrer Marsollier

, Masia

, de Tayrac

, Triopon

. [Robotic surgery in gynecologic oncology: Retrospective and comparative study with laparotomy and laparoscopy]. J Gynecol Obstet Biol Reprod (Paris), 2012; 41:353.

13.

Holtz

, Miroshnichenko

, Finnegan

, Chernick

, Dunton

. Endometrial cancer surgery costs: Robot vs laparoscopy. J Minim Invasive Gynecol, 2010; 17:500.

14.

Barnett

, Judd

, Wu

, Scales

, Myers

, Havrilesky

. Cost comparison among robotic, laparoscopic, and open hysterectomy for endometrial cancer. Obstet Gynecol, 2010; 116:685.

15.

, Lum

, Kiet

, et al. Utilization of and charges for robotic versus laparoscopic versus open surgery for endometrial cancer. J Surg Oncol, 2013 May; 107:653.

16.

Wright

, Ananth

, Lewin

, et al. Robotically assisted vs laparoscopic hysterectomy among women with benign gynecologic disease. JAMA, 2013; 309:689.

17.

Wright

, Ananth

, Tergas

, et al. An economic analysis of robotically assisted hysterectomy. Obstet Gynecol, 2014; 123:1038.

18.

, Gu

, Lipsitz

, Barry

, D'Amico

, Weinberg

, Keating

. Comparative effectiveness of minimally invasive vs open radical prostatectomy. JAMA, 2009; 302:1557.

19.

Nezhat

, Sirota

. Perioperative outcomes of robotic assisted laparoscopic surgery versus conventional laparoscopy surgery for advanced-stage endometriosis. JSLS, 2014; 18:pii: e2014.00094.

20.

Nezhat

, Finger

, Vetere

, et al. Comparison of perioperative outcomes and complication rates between conventional versus robotic-assisted laparoscopy in the evaluation and management of early, advanced, and recurrent stage ovarian, fallopian tube, and primary peritoneal cancer. Int J Gynecol Cancer, 2014; 24:600.

21.

Nezhat

, Datta

, Liu

, Chuang

, Zakashansky

. Robotic radical hysterectomy versus total laparoscopic radical hysterectomy with pelvic lymphadenectomy for treatment of early cervical cancer. JSLS, 2008; 12:227.

22.

Mariani

, Dowdy

, Cliby

, Gostout

, Jones

, Wilson

, Podratz

. Prospective assessment of lymphatic dissemination in endometrial cancer: A paradigm shift in surgical staging. Gynecol Oncol, 2008; 109:11.

23.

Cormier

, Nezhat

, Sternchos

, Sonoda

, Leitao

Jr.

Electrocautery-associated vascular injury during robotic-assisted surgery. Obstet Gynecol, 2012; 120(2 Pt 2):491.

24.

Acholonu

Jr , Chang-Jackson

, Radjabi

, Nezhat

. Laparoscopy for the management of early-stage endometrial cancer: From experimental to standard of care. J Minim Invasive Gynecol, 2012; 19:434.

25.

Walker

, Piedmonte

, Spirtos

, et al. Recurrence and survival after random assignment to laparoscopy versus laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group LAP2 Study. J Clin Oncol, 2012; 30:695.

26.

Gunderson

, Java

, Moore

, Walker

. The impact of obesity on surgical staging, complications, and survival with uterine cancer: A Gynecologic Oncology Group LAP2 ancillary data study. Gynecol Oncol, 2014; 133:23.

27.

Lim

, Kang

, Park do

. 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, 2011; 120:413.

28.

Coronado

, Herraiz

, Magrina

, Fasero

, Vidart

. Comparison of perioperative outcomes and cost of robotic-assisted laparoscopy, laparoscopy and laparotomy for endometrial cancer. Eur J Obstet Gynecol Reprod Biol, 2012; 165:289.

29.

Gehrig

, Cantrell

, Shafer

, Abaid

, Mendivil

, Boggess

. What is the optimal minimally invasive surgical procedure for endometrial cancer staging in the obese and morbidly obese woman?. Gynecol Oncol, 2008; 111:41.

30.

Boggess

, Gehrig

, Cantrell

, Shafer

, Ridgway

, Skinner

, Fowler

. A comparative study of 3 surgical methods for hysterectomy with staging for endometrial cancer: Robotic assistance, laparoscopy, laparotomy. Am J Obstet Gynecol, 2008; 199:360.e361.

31.

Leitao

Jr , Briscoe

, Santos

, et al. Introduction of a computer-based surgical platform in the surgical care of patients with newly diagnosed uterine cancer: Outcomes and impact on approach. Gynecol Oncol, 2012; 125:394.

32.

Holloway

, Ahmad

, DeNardis

, et al. Robotic-assisted laparoscopic hysterectomy and lymphadenectomy for endometrial cancer: Analysis of surgical performance. Gynecol Oncol, 2009; 115:447.

33.

Holloway

, Ahmad

. Robotic-assisted surgery in the management of endometrial cancer. J Obstet Gynaecol Res, 2012; 38:1.

34.

Paley

, Veljovich

, Shah

, Everett

, Bondurant

, Drescher

, Peters

. Surgical outcomes in gynecologic oncology in the era of robotics: Analysis of first 1000 cases. Am J Obstet Gynecol, 2011; 204:551.e551.

35.

Tozzi

, Malur

, Koehler

, Schneider

. Laparoscopy versus laparotomy in endometrial cancer: First analysis of survival of a randomized prospective study. J Minim Invasive Gynecol, 2005; 12:130.

36.

Helm

, Arumugam

, Gordinier

, Metzinger

, Pan

, Rai

. Laparoscopic surgery for endometrial cancer: Increasing body mass index does not impact postoperative complications. J Gynecol Oncol, 2011; 22:168.