Clinical Outcomes of Robotic Versus Open Radical Hysterectomy in Endometrial Cancer Staging: An Experience at a Tertiary Referral Care Center

Abstract

Objective:

Comprehensive surgical staging is the mainstay of initial treatment for most patients with endometrial cancer. This study compared hysterectomy and lymphadenectomy for endometrial-cancer staging via robotics and open routes in terms of clinicopathologic factors, perioperative outcomes, recurrences, and survival.

Materials and Methods:

Patients were identified retrospectively to find those with clinically uterus-confined endometrial cancers, who underwent staging via a robotic approach between October 2011 and October 2016. These patients were matched in a 1:1 ratio with patients staged via conventional laparotomy during the same time period. Data were analyzed for demographics, operative time, blood loss, surgicopathologic factors, complications, conversions, length of hospital stay, adjuvant treatment, recurrences, and follow-up.

Results:

The study included 150 patients (75 in a robotic-surgery group and 75 in an open-surgery group). The overall rate of complications was much higher in the open-surgery group (38.6%), compared to the robotic surgery group (9.3%; p = 0.0001). Statistically significant differences occurred in both groups in terms of reduced estimated blood loss in the robotic-surgery group (149.99 ± 85.77 mL), compared to the open-surgery group (444.2 ± 273.09 mL; p < 0.0001), leading to transfusions in 10.6% patients in the robotic-surgery group and 49.3% patients in the open-surgery group (p < 0.0001). There was a lower median operative time in the robotic-surgery group than in the open-surgery group (160 minutes versus 180 minutes; p = 0.038). The median length of stay in the hospital was 3 versus 5 days in the robotic-surgery and open-surgery groups, respectively (p < 0.0001). The age and body mass indices were similar in both groups (p = 0.073 and p = 0.18, respectively). The nodal yields (27 versus 26; p = 0.869), grades (p = 0.11), International Federation of Gynecology and Obstetrics stages (p = 0.78), and histology (p = 0.546) were similar in both groups as were deep myometrial invasions (p = 0.51) and lymphovascular-space invasions (p = 0.54). Recurrences occurred in 9.3% of robotic-surgery and 14.6% of open-surgery cases (p = 0.451), with death due to disease in 6.6% versus 10.6% in the robotic-surgery and open-surgery groups (p = 0.608).

Conclusions:

Robotic staging for endometrial cancer has clear advantages over conventional laparotomy in terms of less operative time, reduced blood loss, shorter hospital stay, and fewer complications without compromising the oncologic outcomes. Recurrences and disease related-mortality are not influenced by this minimally invasive modality.

Introduction

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

Surgical staging for endometrial cancer was introduced in 1988 and is considered the standard of care. Surgical approach varies from conventional laparotomy to minimally invasive techniques via a laparoscope or a robot depending on surgeon expertise, availability of resources, patients' choices, and logistics. The U.S. Food and Drug Administration approved the use of robots in gynecologic surgery in 2005. Prior to the inception of this technology, many patients with endometrial cancer underwent laparotomy, with relatively few receiving the laparoscopic approach. The benefits of robotic technology are high-definition 3-dimensional optics; wristed instrumentation for improved range of motion and surgical dexterity; and robotic control of a camera, eliminating dependence on a surgical assistant and improved ergonomics, resulting in decreased surgeon fatigue. Despite these advantages, the cost of robotic surgery and the long learning curve for performing robotic surgeries are heated points of discussion by the critics of robotic surgery.

With this in mind, the current authors describe their experience of incorporating robotic technology for treating endometrial malignancy at their tertiary-care referral cancer center, the Rajiv Gandhi Cancer Institute and Research Centre, in Delhi, India. Thus, this study compared hysterectomy and lymphadenectomy for endometrial-cancer staging via robotics and open routes in terms of clinicopathologic factors, perioperative outcomes, recurrences, and survival.

Materials and Methods

Institutional review board approval was sought prior to performing this study. Patients' consent was not required as this was a retrospective chart study not having any bearing on patient privacy or management. A retrospective analysis was performed on the medical records of 75 patients with clinically early stage endometrial cancer, who underwent robotic staging between October 2011 and October 2016 at the center. These records were compared with the records of 75 patients (at a 1:1 ratio) who were staged with an open-surgery approach (laparotomy).

A robot was brought to the center in 2011; hence, the robotic-surgery cohort in the study was comprised of the first robotic-surgery cases treated there by a single surgeon. This cohort was compared to patients who opted for an open-staging procedure during the same study period because of logistical issues or personal preferences. Cases of patients who had other surgical procedures performed during the same operation—such as cholecystectomy, hernia repair, etc.—and patients who had incomplete charts were excluded from the study. Thus, 150 patients in all were studied with respect to age, body mass index (BMI), parity, comorbidities, previous abdominal surgeries, operating time, estimated blood loss (EBL), conversions to laparotomy, need for transfusions, and length of hospital stay.

Intraoperative and postoperative complications were recorded in terms of vascular, nerve, ureteric, or bowel injuries, including readmissions or reexplorations. Postoperative complications occurring within 30 days of surgery were recorded and classified into major and minor as according to the Clavien–Dindo system.^4,5 Surgicopathologic factors recorded were International Federation of Gynecology and Obstetrics (FIGO) stage, grade, myometrial invasion, histology, lymphovascular-space invasion (LVSI), and number of nodes harvested. Adjuvant treatment with radiation and/or chemotherapy were also studied. The follow-up of all patients were studied to calculate disease-free survival and overall survival.

The operative time for robotic surgeries included the docking time and the console time, followed by the closure of port-site incisions. The operative time for laparotomies was calculated from skin incision to closure. Blood loss was calculated by subtracting the irrigation fluid from the total suction-container volume and an estimation of the weight of used sponges at the end of the surgery. No robotic surgeries were converted to laparotomies in this group. Length of stay included the number of nights spent in the hospital postoperatively, which did not take into account 2–3 days' prior admission for some patients who required optimization prior to major surgery as well as patients who underwent hysteroscopy and guided biopsy followed by staging during the same admission if the biopsy results were reported as malignant.

Robotic staging was performed on each patient in this group with the da Vinci® Si surgical system (Intuitive Surgical, Sunnyvale CA). Six ports were inserted through the anterior abdominal wall (after creating pneumoperitoneum using a standard technique with a Veress needle) as follows:

One 12-mm port supraumbilically in the midline 25 cm above the symphysis pubis for the camera

Two 8-mm robotic-instrument ports on the right (for monopolar curved scissors) and the left (for bipolar) respectively ∼10 cm lateral to the rectus in the line of the anterior superior iliac spine and 15° inferior to the camera port

One 12-mm assistant port in the right upper quadrant 5 cm above the anterior superior iliac spine

One 8-mm instrument port in the left upper quadrant 5 cm above the anterior superior iliac spine for the ProGrasp^tm (Intuitive Surgical)

One 5-mm suction port on right side at the apex of a triangle with a base formed by the camera port and the 8-mm right lateral instrument port.

A vaginal sponge was kept in situ. The patient was placed in a steep Trendelenburg position at 29°. Robot docking was done at the ports described. Central docking was accomplished with the robot in-between the patient's legs. Peritoneal washings were taken through the suction port, followed by staging surgery by the primary surgeon at the da Vinci Si console and the assistant surgeon at the right of the patient, while visualizing a monitor placed caudal to and to the right of the patient's right knee.

As the current authors' center, the protocol for patients with endometrial cancer is a type II radical hysterectomy. In the current study, all patients also underwent pelvic lymph-node dissection, while para-aortic lymph-node sampling with omental biopsy or omentectomy was performed in patients with aggressive histology or high-grade lesions. All specimens were retrieved vaginally at the end of the procedures. A Stratafix^tm 2-0 suture of 30-cm length was used to close each patient's vault. Open staging was performed via the standard midline vertical incision.

All patients received preoperative antibiotic prophylaxis and bowel preparation. Postoperatively, all patients were given thromboprophylaxis. Patients who were staged robotically were usually discharged on the third postoperative day while patients who underwent open surgery had a hospital stay of ∼5–6 days.

Statistical analyses

Categorical variables were presented as numbers and percentages (%), and continuous variables were presented as means ± standard deviations (SDs) and medians. Normality of data was tested with a Kolmogorov–Smirnov test. If the normality was rejected then a nonparametric test was used. Data analysis was performed with the Statistical Package for Social Sciences, version 21.0 (Chicago, IL). Quantitative variables were compared using an independent t-test/Mann–Whitney-U test (when the data sets were not normally distributed) between the 2 groups. Qualitative variables were correlated using a χ²test/Fisher's exact test. A p-value of <0.05 was considered statistically significant.

Results

The current study included 75 patients who underwent robotic surgery for endometrial cancer staging, compared to 75 patients who were staged via a conventional open-surgery technique. The median age of patients who underwent robotic radical hysterectomy and open radical hysterectomy were 61 (range: 42–80) and 58 (range: 29–85) years, respectively (p = 0.073). Both groups did not differ much in terms of BMI, with means of 32.39 ± 6.9 kg/m² in the robotic-surgery group and 31.03 ± 5.4 kg/m² in the open-surgery group (p = 0.18). Nine patients in the robotic-surgery group and 5 patients in the open-surgery group were morbidly obese with BMIs >40 kg/m². The major comorbidities in both groups were hypertension (p = 0.867), followed by diabetes (p = 0.861) and thyroid disorders (p = 1.0). History of previous abdominal surgeries occurred more in the open-surgery group, compared to the robotic surgery group (28% versus 13.3%; p = 0.044). The median parity was 2 in both groups. Demographic profiles of the patients are shown in Table 1.

Table 1.

Demographic Profile of Study Patients

Characteristics	Open surgery	Robotic surgery	p-value
Characteristics	(n = 75)	(n = 75)	p-value
Age
Mean ± SD	57.85 ± 10.15	60.96 ± 8.21	0.073
Median	58	61
Min–Max	29–85	42–80
BMI (kg/m²)			0.18
Mean ± SD	31.03 ± 5.4	32.39 ± 6.9
Median	30.95	31.92
Min–Max	18.13–43.98	15.78–51.44
Comorbidities
Hypertension	45	47	0.867
Diabetes	23	25	0.861
Thyroid disorder	14	13	1.00
Previous abd Sx	21	10	0.044
CAD	8	2	0.097
CVA	2	1	1.00
Parity
Median (range)	2 (0–7)	2 (0–9)

SD, standard deviation; Min, minimum; Max, maximum; BMI, body mass index; abd Sx, abdominal surgery; CAD, coronary artery disease; CVA, cerebrovascular accident.

The average time taken to dock the robot was 17.85 (range: 5–32) minutes. Table 2 shows statistically significant outcomes in the 2 groups with less median operative time in the robotic-surgery than in the open-surgery group (160 minutes versus 180 minutes; p = 0.038). EBL was much lower in the robotic-surgery group (149.99 ± 85.77 mL), compared to the open-surgery group (444.2 ± 273.09 mL, p < 0.0001), leading to a lower transfusion rate in the robotic-surgery group than in the open-surgery group (10.6% versus. 49.3%; p < 0.0001). The median length of hospital stay was 3 days in the robotic-surgery group and 5 days in the open-surgery group (p < 0.0001).

Table 2.

Surgical Outcomes

Surgical events	Open surgery	Robotic surgery	p-Value
Surgical events	(n = 75)	(n = 75)	p-Value
SX time (minutes)			0.038
Mean ± SD	181.95 ± 45.21	168.73 ± 45.34
Median	180	160
Min–Max	97–286	104–320
EBL (mL)			< 0.0001
Mean ± SD	444.2 ± 273.09	149.99 ± 85.77
Median	380	140
Min–Max	75–1740	50–350
LOS (days)			< 0.0001
Mean ± SD	6.15 ± 2.5	3.11 ± 0.89
Median	5	3
Min–Max	4–23	2–7
Transfusions			< 0.0001
N (%)	37 (49.3)	8 (10)	< 0.0001

Bolding denotes significant results.

SX, surgical; SD, standard deviation; Min, minimum; Max, maximum; EBL, estimated blood loss; LOS, length of (hospital) stay.

The overall rate of complications was much higher in the open-surgery group (38.6%) than in the robotic-surgery group (9.3%; p = 0.0001). Complications are listed in Table 3.

Table 3.

Complications in the Study Patients

Complication	Open surgery	Robotic surgery	p-Value
Complication	(n)	(n)	p-Value
Intraoperative
Ureteral injury requiring anastomosis and DJ-stenting	1	0	1
Postoperative within 30 days
Major
Reoperation for ureteric leak	1	0	1
Readmission for clot evacuation under general anesthesia	1	0	1
Resuturing	2	0	0.479
Minor
Fever	2	0	0.479
Ileus	6	0	0.028
UTI	0	1	1
Wound infection	1	0	1
Readmissions managed conservatively	4	4	1
Delayed voiding	2	1	1
Long-term
Lymphocyst	5	1	0.209
Incisional hernia	4	0	0.120

DJ, double-J; UTI, urinary-tract infection.

There was a single intraoperative complication of ureteral injury requiring ureteric repair and double-J stenting in the open-surgery group. Postoperative complications occurring within 30 days of surgery were recorded and were classified as per the Clavien–Dindo system,^4,5 in which grades 1 and 2 are considered minor complications and grades 3 and 4 are considered major complications. There was no major postoperative complication in the robotic-surgery group, and in 5.3% of the open-surgery group, there was a readmission for clot evacuation on postoperative day 17 in 1 patient and reexploration for a ureteric leak on postoperative day 6 in another patient requiring uretero–ureterostomy. Minor postoperative complications were much fewer in the robotic-surgery group, compared to the open-surgery group (8% versus 32%). The long-term complications in the robotic-surgery and open groups included lymphocyst formations and incisional hernias (1% versus 12%).

None of the patients in the robotic-surgery group required conversion to laparotomy. Lymph-nodal harvesting was not statistically significant between the 2 groups with the median being 27 in the robotic-surgery group and 26 in the open-surgery group (p = 0.869) as shown in Table 4. Pelvic lymph-node dissection was done in all 150 patients, while retroperitoneal lymph-node sampling was done in 65 (86.6%) patients in the robotic-surgery group and in 56 (74.6%) patients in the open-surgery group (p = 0.098). The median number of pelvic nodes removed were 24 and 23, respectively, for the robotic- and open-surgery cases (p = 0.459), while the median para-aortic nodes harvested were 2 each for the robotic-surgery and the open-surgery groups (p = 0.054). Metastatic disease in nodes was found in 9 (12%) patients in the robotic-surgery group and in 8 (10.6%) patients in the open-surgery group (p = 1). None of the patients in the robotic-surgery group had skip metastasis while 2 patients in the open-surgery group had the same results, with para-aortic nodes being positive without pelvic-node positivity.

Table 4.

Surgical Pathology Data

Pathology	Robotic-surgery group n (%)	Open-surgery group n (%)	p-Value
Myometrial invasion
< 50%	40 (53.3)	45 (60)	0.51
> 50%	35 (46.6)	30 (40)	0.51
Final histology
Endometrioid adenocarcinoma	66 (88)	63 (84)	0.546
Papillary serous carcinoma	5 (6.6)	5 (6.6)
MMMT	1 (1.3)	4 (5.3)
Clear-cell carcinoma	2 (2.6)	3 (4)
Mixed	1 (1.3)	0
Grade
G1	51 (68)	39 (52)	0.11
G2	10 (13.3)	12 (16)
G3	14 (18.6)	24 (32)
Stage
IA	35 (46.6)	40 (53.3)	0.78
IB	23 (30.6)	21 (28)
II	4 (5.3)	1 (1.3)
IIIA	1 (1.3)	1 (1.3)
IIIB	0	0
IIIC	10 (13.3)	9 (12)
IV	2 (2.6)	3 (4)
LVSI	13(17.3)	17(22.6)	0.54
Positive cytology	0	3(4)	0.245
Pelvic nodes
Mean	24.09	24.28	0.459
Median	24	23
Range	9–46	11–54
P/As
Mean	3.1	3.4
Median	2	2	0.054
Range	0–14	0–13
Total nodes (pelvic + P/As)
Mean ± SD	27.2 ± 9.06	27.73 ± 9.93	0.869
Median	27	26
Min–Max	10–51	11–54
Node positives: n (%)	9 (12)	8 (10.6)	1

MMMT, malignant mixed Müllerian tumor/carcinosarcoma; LVSI, lymphovascular-space invasion; P/As, para-aortic nodes; SD, standard deviation; Min, minimum; Max, maximum.

FIGO stages in the robotic-surgery group were as follows: stage I, 77.3%; stage II, 5.3%; stage III, 14.6%; and stage IV, 2.6%. FIGO stages for the open-surgery group were: stage I, 81.3%; stage II, 1.3%; stage III, 13.3%; and stage IV, 4% (p = 0.78). Tumor grades were: G1, 68%; G2, 13.3%; and G3, 18.6% in the robotic-surgery group. Tumor grades in the open-surgery group were: G1, 52%; G2, 16%; and G3, 32% (p = 0.11). The final histology results in the robotic-surgery versus the open-surgery cases were endometrioid (88% versus 84%), papillary serous (6.6% each), clear-cell carcinoma (2.6% versus 4%), and carcinosarcoma (1.3% versus 5.3%; p = 0.546). Deep myometrial invasion was seen more in the robotic-surgery group, compared to the open-surgery group (46.6% versus 40%, p = 0.51). LVSI was noted in 17.3% of the robotic-surgery group and in 22.6% of the open-surgery group (p = 0.54). None of the patients in the robotic-surgery group had positive cytology, while this pathology was found in 4% of patients in the open-surgery group (p = 0.245). Surgical pathology data are in Table 4.

The robotic-surgery group received more adjuvant radiation, compared to the open-surgery group (44% versus 38.6%; p = 0.619). Adjuvant chemotherapy was given to 18.6% of the patients in the robotic-surgery group and 21.3% of the patients in the open-surgery group (p = 0.838). Table 5 shows adjuvant treatment, recurrences, and status of the patients in the robotic-surgery and open-surgery groups.

Table 5.

Adjuvant Therapies, Recurrences, and Status of Patients in Both Groups

Factors	Robotic-surgery group n (%)	Open-surgery group n (%)	p-Value
Adjuvant treatment
Radiation	33 (44)	29 (38.6)	0.619
Chemotherapy	14 (18.6)	16 (21.3)	0.838
Total recurrences	7 (9.3)	11 (14.6)	0.451
Died	5 (6.6)	6 (8)	0.314
Alive	2 (2.6)	2 (2.6)
Lost to follow-up	0	3 (4)
Total deaths	8 (10.6)	10 (13.3)	0.802
Death due to disease	5 (6.6)	8 (10.6)	0.608
Unrelated death	3 (4)	2 (2.6)	0.608
Lost to follow-up	13 (17.3)	16 (21.3)	0.679

The median length of follow-up was 4.6 years (55.2 months; range: 0.36–89.2 months). Recurrence was seen in 7 (9.3%) patients in the robotic-surgery group and in 11 (14.6%) patients in the open-surgery group (p = 0.451). The sites of recurrence in the robotic-surgery and open-surgery groups were the vault (0% versus 1.3%), pelvis (0% versus 1.3%), abdomen (nodes [1.3% versus 4%] and liver [1.3% each]), and lung (5.3% versus 6.6%; p = 0.640). Death due to disease was seen in 6.6% patients in the robotic-surgery group and in 10.6% in the open-surgery group (p = 0.608). Both the robotic-surgery and open-surgery groups, as of this writing, have 2.6% patients alive with disease. Thirteen patients were lost to follow-up in the robotic-surgery group while 16 patients in the open-surgery group was lost to follow-up (p = 0.679). The 5-year disease-free survival (Fig. 1) was 89.68% in the robotic-surgery group and 82.35% in the open-surgery group (p = 0.192). The 5-year overall survival (Fig. 2) was 89.25% in the robotic surgery group and 82.41% in the open surgery group (p = 0.361).

FIG. 1.

Kaplan–Meier disease-free survival (DFS) curve for the study population. The DFS at the end of 5 years was 89.68% in the robotic group and was 82.35% in the open group (p = 0.192). The p-value was not statistically significant, showing that DFS was not affected by the minimally invasive approach. Cum, cumulative; yrs, years.

FIG. 2.

Kaplan–Meier overall survival (OS) curve for the study population. The OS at the end of 5 years was 89.25% in the robotic group and was 82.41% in the open group (p = 0.361). The p-value was not statistically significant, showing that OS was not affected by the minimally invasive approach. Cum, cumulative; yrs, years.

Discussion

The role of minimally invasive surgical staging for managing apparently early stage endometrial cancer continues to evolve⁶; however, the role of robotic surgery in endometrial cancer is even less-defined.⁷ The current authors' experience has mimicked several other centers' experience with endometrial cancer staging in an evolution from historical laparotomy to robotics. The current study demonstrated statistically significant differences in operative time, EBL, transfusion rates, length of hospital stay, and complications in patients undergoing endometrial cancer staging via robotics or an open approach without compromising the nodal yield, recurrence, death due to disease, 5-year disease-free survival, and overall survival.

Gehrig et al. showed reduced robotic operative time (189 min),⁸ which was consistent with the robotic time in the current study (160 minutes). None of robotic-surgery cases required conversion to laparotomy. The robotic-surgery cohort showed a decreased average EBL (140 mL) and length of hospital stay (3 days), compared to the open-open surgery group (380 mL and 5 days). Bernardini et al. compared the outcomes of patients with early stage endometrial cancer who were staged via laparotomy and robotics and found that hospital stay was significantly longer in the laparotomy-surgery group, compared with the robotic-surgery group (4 versus 2 days; p < 0.001).⁹ Gehrig et al. also observed reduced hospital stay in their robotic-surgery group, compared to their laparotomy-surgery group.⁸

The current study found significantly fewer postoperative complications in patients undergoing surgery via the robotic approach, compared to the open approach (9.3% versus 38.6%; p = 0.0001), a result that was found in several previous studies.^10–13 Robotic surgery offers greater reproducibility for the primary surgeon who maintains control of the camera and instrument movements. Primary advantages of robotic surgery include a shorter hospital stay, faster recovery time, and more-rapid return to normal activity after surgery.^14,15 Many hospitals are now considering the initial cost of a robot as a one-time investment and therefore own at least one robotic unit.

Lymph-node yield, a measure of surgical quality, was similar between the two groups with the median being 27 in the robotic group and 26 in the open group (p = 0.869). This was consistent with that shown by Gaia et al.¹⁶

The overall recurrence rate was lower in the robotic-surgery group than the open-surgery group (9.3% versus 14.6%; p = 0.451). Lau et al. also observed lower recurrence rates in women who were staged robotically, compared to those who underwent endometrial cancer staging via laparotomy or laparoscopy (7.7% versus 11.9%; p < 0.001), during a 2-year follow up period.¹⁷ Given that there are few long-term studies comparing endometrial cancer recurrence in patients staged surgically via robotic and open approaches, the current study is important because it emphasizes that recurrence and death due to disease are not compromised by the minimally invasive approach. The 5-year disease-free survival and overall survival in both the robotic-surgery and open-surgery groups did not differ significantly, showing that the robotic route for endometrial cancer staging is oncologically on a par with the open approach.

The primary console surgeons in the current authors' center moved on from laparotomies for endometrial-cancer staging directly to robotic staging without laparoscopic surgeries in-between, which proved that it is not necessary to master laparoscopy prior to mastering robotics.

The retrospective nature of the study with an inherent selection bias was a potential weakness of this study.

Conclusions

Gynecologic oncology is clearly the fastest-growing specialty in the adoption of robotic surgery. Robotic surgery offers a means to decrease the morbidity caused by endometrial-cancer therapy.¹⁸ The current authors have found robotic surgery to be a safe and feasible approach to staging endometrial cancer, resulting in shorter operative time, reduced EBL leading to lower transfusion rates, fewer postoperative complications, and reduced length of hospital stay without compromising the oncologic outcomes. Recurrences and disease-related mortality are not influenced by this minimally invasive modality. The current authors' belief is that the robotic approach for treating endometrial cancer has clear advantages over conventional laparotomy and will dominate in the near future.

Footnotes

Author Disclosure Statement

No financial conflicts of interest exist.

References

Siegel

, Miller

, Jemal

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

Howlader

, Noone

, Krapcho

, et al. SEER Cancer Statistics Review, 1975–2011. Bethesda, MD: National Cancer Institute, 2015.

Lewin

, Herzog

, Barrena Medel

, et al. Comparative performance of the 2009 International Federation of Gynecology and Obstetrics' staging system for uterine corpus cancer. Obstet Gynecol, 2010; 116:1141. DOI:10.1097/AOG.06013e3181f39849.

Dindo

, Demartines

, Clavien

. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg, 2004; 240:205.

Barrie

, Freeman

, Lyon

, et al. Classification of postoperative complications in robotic-assisted compared with laparoscopic hysterectomy for endometrial cancer. J Minim Invasive Gynecol, 2016; 23:1181.

Fowler

JM.

The role of laparoscopic staging in the management of patients with early endometrial cancer. Gynecol Oncol, 1999; 73:1.

Seamon

, Cohn

, Henretta

, Kim

, Carlson

, Phillips GS Fowler

. Minimally invasive comprehensive surgical staging for endometrial cancer: Robotics or laparoscopy?. Gynecol Oncol, 2009; 113:36.

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.

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.

10.

Boggess

JF.

A comparative study of three surgical methods for hysterectomy with staging for endometrial cancer: Robotic assistance, laparoscopy, laparotomy. Am J Obstet Gynecol, 2008; 199:360.e1.

11.

Zullo

, Falbo

, Palomba

Safety of laparoscopy vs laparotomy in the surgical staging of endometrial cancer: A systematic review and metaanalysis of randomized controlled. Am J Obstet Gynecol, 2012; 207:94.

12.

Wattiez

, Soriano

, Cohen

, et al. The learning curve of total laparoscopic hysterectomy: Comparative analysis of 1647 cases. J Am Assoc Gynecol Laparosc, 2002; 9:339.

13.

DeNardis

, Holloway

, Bigsby

GE 4th

, Pikaart

, Ahmad

, Finkler

. Robotically assisted laparoscopic hysterectomy versus total abdominal hysterectomy and lymphadenectomy for endometrial cancer. Gynecol Oncol, 2008; 111:412.

14.

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.

15.

Bell

, Torgerson

, Seshadri-Kreaden

, Suttle

, Hunt

. Comparison of outcomes and cost for endometrial cancer staging via traditional laparotomy, standard laparoscopy and robotic techniques. Gynecol Oncol, 2008; 111:407.

16.

Gaia

, Holloway

, Santoro

, Ahmad

, Di Silverio

, Spinillo

. Robotic-assisted hysterectomy for endometrial cancer compared with traditional laparoscopic and laparotomy approaches: A systematic review. Obstet Gynecol, 2010; 116:1422.

17.

Lau

, Vaknin

, Ramana-Kumar

, Halliday

, Franco

, Gotlieb

. Outcomes and cost comparisons after introducing a robotics program for endometrial cancer surgery. Gynecol Oncol, 2012; 119:717.

18.

Walker

, Piedmonte

, Spirtos

, Eisenkop

, Schlaerth

, Mannel

, Spiegel

. Surgical staging of uterine cancer: Randomized phase III trial of laparoscopy versus laparotomy—a Gynecologic Oncology Group Study (GOG): Preliminary results. J Clin Oncol, 2006; 24(18[suppl]):18S.