El Camino Women’s Medical Group offers the latest Minimally Invasive Solutions for gynecologic problems. Drs. Amy Teng, Erika Balassiano, and Pooja Gupta, all members of AAGL (American Association of Gynecologic Laparoscopy) are highly trained and experienced in the field of Minimally Invasive Gynecgologic Surgery. Dr. Erika Balassiano is also a graduate of the Minimally Invasive Gynecologic Surgery Fellowship at Stanford University, under the supervision of world-renowned Dr. Camran Nezhat.
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Background
Previous studies comparing robotic-assisted laparoscopic surgery to traditional laparoscopic or open surgery in gynecologic oncology have been retrospective. To our knowledge, no prospective randomized trials have thus far been performed on endometrial cancer.
Objective
We sought to prospectively compare traditional and robotic-assisted laparoscopic surgery for endometrial cancer.
Study Design
This was a randomized controlled trial. From December 2010 through October 2013, 101 endometrial cancer patients were randomized to hysterectomy, bilateral salpingo-oophorectomy, and pelvic lymphadenectomy either by robotic-assisted laparoscopic surgery or by traditional laparoscopy. The primary outcome measure was overall operation time. The secondary outcome measures included total time spent in the operating room, and surgical outcome (number of lymph nodes harvested, complications, and recovery). The study was powered to show at least a 25% difference in the operation time using 2-sided significance level of .05. The differences between the traditional laparoscopy and the robotic surgery groups were tested by Pearson χ2 test, Fisher exact test, or Mann-Whitney test.
Results
In all, 99 patients were eligible for analysis. The median operation time in the traditional laparoscopy group (n = 49) was 170 (range 126-259) minutes and in the robotic surgery group (n = 50) was 139 (range 86-197) minutes, respectively (P < .001). The total time spent in the operating room was shorter in the robotic surgery group (228 vs 197 minutes, P < .001). In the traditional laparoscopy group, there were 5 conversions to laparotomy vs none in the robotic surgery group (P = .027). There were no differences as to the number of lymph nodes removed, bleeding, or the length of postoperative hospital stay. Four (8%) vs no (0%) patients (P = .056) had intraoperative complications and 5 (10%) vs 11 (22%) (P = .111) had major postoperative complications in the traditional and robotic surgery groups, respectively.
Conclusion
In patients with endometrial cancer, robotic-assisted laparoscopic surgery was faster to perform than traditional laparoscopy. Also total time spent in the operation room was shorter in the robotic surgery group and all conversions to laparotomy occurred in the traditional laparoscopy group. Otherwise, the surgical outcome was similar between the groups. Robotic surgery offers an effective and safe alternative in the surgical treatment of endometrial cancer.
Key words:
endometrial cancer, gynecologic surgery, operation time, robotic-assisted surgery, traditional laparoscopic surgery
Introduction
Endometrial carcinoma is globally the sixth most common cancer in women, with 320,000 new cases annually, or 4.8% of cancers in women. The estimated age-standardized incidence rate (World standard) is 8.3 per 100,000 women. The highest incidence rates are found in North America (19.1 per 100,000) and Northern and Western Europe (12.9-15.6 per 100,000). The rates are low in South-Central Asia (2.7 per 100,000) and in most parts of Africa (<5 per 100,000).1 In developed countries, endometrial cancer is diagnosed often (80%) at International Federation of Gynecology and Obstetrics stage I and can thus be cured by surgery, albeit followed by adjuvant therapy if high-risk features are encountered.2 Over the last 20 years, laparotomy has been replaced by minimally invasive laparoscopic techniques, of which robotic-assisted surgery has lately become increasingly popular.3
The advantages of robotic-assisted surgery as opposed to conventional laparoscopy have been described in retrospective and observational studies.4 The 3-dimensional view, the better and more precise visibility of the operation area, the fatigue-resistant properties of robot hands, as well as the better mobility and the greater range of movement of the instrument head all facilitate working with the robot. Because of these advantages, the learning curve is faster than in conventional laparoscopy5, 6, 7, 8; eg, endoscopic suturing technique can be adopted faster.9 Based on the advantages presented above, robotic-assisted surgery has been adopted widely as the operative treatment of endometrial cancer, but as far as we are aware, it has not been tested in a randomized, controlled setting. The present study was initiated in December 2010 to answer to this obvious unmet need.
Materials and Methods
A total of 101 patients scheduled for laparoscopic hysterectomy, bilateral salpingo-oophorectomy (BSO), and pelvic lymphadenectomy (PLND) at the Department of Gynecology and Obstetrics of Tampere University Hospital were randomized preoperatively to undergo either robotic-assisted (da Vinci S Surgical System; Intuitive Surgical Inc, Sunnyvale, CA) or conventional laparoscopic operation from December 2010 through October 2013 (Figure 1). Only 1 patient refused to participate in the study.
Figure 1
Flow chart of study
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
Women eligible to the study had a low-grade (grade 1-2) endometrial carcinoma, and were scheduled for laparoscopic surgical staging, ie, for a laparoscopic hysterectomy along with BSO and PLND. The study exclusion criteria included a narrow vagina or a uterus too large to be removed through vagina, and the patient’s condition not allowing for a deep Trendelenburg position (Figure 1). The operations were all performed by gynecologic oncologists with several years of experience with laparoscopic surgery. Thus, a learning curve was not included in the operations. The patients were randomized to undergo either traditional or robotic-assisted laparoscopic surgery, and were stratified for overweight (body mass index [BMI] <30 and ≥30) and age (<65 and ≥65 years). The randomization was made with the minimization software for allocating patients to treatments in clinical trials (MINIM, Version 1.5/28-3-90, by S. Evans, P. Royston, and S. Day [https://www-users.york.ac.uk/∼mb55/guide/minim.htm]).
The surgical techniques (Table 1) differed between the groups in the insertion of trocars, entering the abdominal cavity, and closing the vagina. PLND was performed in the same way in both groups: The external iliac artery was skeletonized up to the bifurcation of the common iliac artery into the external and internal iliac arteries. The obturator lymph nodes were removed from the area between the obturator nerve and the external iliac vein. As antithrombotic prophylaxis, all patients were given low-molecular-weight-heparin and were wearing antithrombotic stockings. Cefuroxime was used as primary antibiotic prophylaxis, combined with metronidazole when indicated, and replaced with levofloxacin in case of cephalosporin allergy. A cytological sample from the pouch of Douglas was obtained from all patients.
| Traditional | Robot | |
|---|---|---|
| Entering abdominal cavity | Veress needle or open technique through umbilicus | Open technique |
| Size and placement of trocars | 10 mm for Camera in umbilicus, two 5 mm lateral to both epigastric arteries, 12 mm in midline above symphysis | 12 mm for Camera about 10 cm above umbilicus, two 8 mm in right and 8 mm in left upper and 12 mm in left lower abdomen |
| Uterine manipulator | Reusable | Disposable |
| Hysterectomy and BSO | Securing and dividing uterine vessels laparoscopically while ligating and dividing parametria vaginally | Uterus totally freed laparoscopically, and then removed via vagina |
| Closing vagina | Vaginal | Laparoscopic |
| Local cervical anesthesia | At onset of vaginal phase; levobupivacaine 0.5% 20 mL or lidocaine with adrenaline 0.25% 20 mL | At onset of operation; Chirocaine 0.5% 20 mL or lidocaine with adrenaline 0.25% 20 mL |
BSO, bilateral salpingo-oophorectomy.
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
The operative specimens were otherwise processed and evaluated as part of the hospital routine practice, but an experienced gynecopathologist (M.L.) reviewed all lymph node samples. The relevant gynecologic and medical histories of the patients can be found in Table 2. The patients’ hemoglobin level was measured preoperatively and postoperatively. By definition, a decrease in the hemoglobin level >40 g/L, and need of transfusion or estimated blood loss >500 mL were regarded as a bleeding complication. Early postoperative complications took place before discharge and late complications following discharge but during the next 6 months. Major infection required intravenous antibiotics and minor wound or urinary tract infection oral antibiotics.
| Traditional, n = 49 | Robot, n = 50 | P | |
|---|---|---|---|
| Age, y, median (range) | 70 (48–83) | 67 (43–84) | .298 |
| BMI, kg/m2, median (range) | 29 (20–45) | 29 (20–46) | .787 |
| Parity, n, median (range) | 2 (0–4) | 2 (0–9) | .971 |
| Preoperative hemoglobin, g/L, median (range) | 135 (88–160) | 136 (109–159) | .782 |
| Disease, n (%) | |||
| Cardiovascular | 27 (53) | 33 (66) | .181 |
| Pulmonary | 4 (8) | 6 (12) | .741 |
| Diabetes | 9 (18) | 4 (8) | .127 |
| Thromboembolic | 3 (6) | 3 (6) | 1.000 |
| Other | 20 (39) | 24 (49) | .373 |
| Existing antithrombotic medication, n (%) | 7 (14) | 7 (14) | .967 |
| Previous abdominal surgery,a n (%) | 28 (57) | 24 (48) | .362 |
BMI, body mass index.
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
Written informed consent was obtained from the study participants. The study was approved by the Ethics Committee of Tampere University Hospital (identification number ETL R10081). The trial was registered at ClinicalTrials.gov, www.clinicaltrials.gov, NCT01466777.
Statistical plan
The primary outcome measure was overall operation time (skin to skin; time from the first incision to the last suture). The study was powered to show at least a 25% difference in operation time using 2-sided significance level of .05. For this, at least 45 patients were needed in each treatment arm to achieve a power of 0.80.10 The secondary outcome measures included the total time spent in the operating room, number of lymph nodes harvested, intraoperative complications and conversions, amount of bleeding, length of postoperative stay, and postoperative pain scale.
The differences between traditional laparoscopy and robotic surgery groups were tested by Pearson χ2 test, Fisher exact test, or by Mann-Whitney and/or independent samples t test. The statistical analyses were performed using software (SPSS Statistics, Version 23; IBM Corp, Armonk, NY). P values <.05 were considered to be statistically significant.
Results
All but 3 patients were operated on according to the randomization plan (Figure 1). Two patients were diverted to a laparotomy because of anesthesiologic reasons, and were excluded from the analysis. One patient randomized to the traditional group was however operated on with the aid of the robot, chosen by a consultant outside the study team. This patient is included in the traditional group in the intention-to-treat analysis. The treatment arms were well balanced in relation to all factors studied (Tables 2 and 3). The median operation time in the traditional laparoscopy group (n = 49) was 170 (range 126-259) minutes, while it was 139 (range 86-197) minutes in the robotic surgery group (n = 50). The difference (18%) is statistically significant (P < .001) (Figure 2 and Table 4). The corresponding mean operation times were 178 (SD 32) vs 141 (SD 26) minutes (P < .001), respectively.
| Traditional, n = 49 | Robot, n = 50 | P | |
|---|---|---|---|
| Size of uterus, g, median (IQR; range) | 87 (70–116; 54–460) | 97.5 (80–125; 55–286) | .160 |
| Lymph node count, median (range) | 23 (11–50) | 25 (14–52) | .273 |
| Iliac area, median (range) | 11 (4–28) | 10.5 (3–31) | .481 |
| Obturator area, median (range) | 12 (1–29) | 14.5 (5–30) | .137 |
| Stage, n (%) | .437 | ||
| IA | 32 (65) | 31 (65) | |
| IB | 9 (18) | 12 (25) | |
| II | 3 (6) | 0 (0) | |
| III–IV | 5 (10) | 5 (10) | |
| Grade, n (%) | .324 | ||
| 1 | 31 (63) | 34 (68) | |
| 2 | 14 (29) | 10 (20) | |
| 3 | 0 (0) | 3 (6) | |
| Other | 4 (8) | 3 (6) | |
| Adjuvant therapy, n (%) | 19 (39) | 22 (44) | .598 |
| Chemotherapy | 5 (10) | 5 (10) | |
| External radiation | 6 (12) | 3 (6) | |
| Chemotherapy and external radiation | 3 (6) | 5 (10) | |
| Brachytherapy | 4 (8) | 9 (18) | |
| Hormonal therapy | 1 (2) | 0 (0) |
IQR, interquartile range.
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
Figure 2
Operation skin-to-skin times
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
| Traditional, n = 49 | Robot, n = 50 | P | |
|---|---|---|---|
| Operation time, h:min, median (range) | 2:50 (2:06–4:19) | 2:19 (1:26–3:17) | <.001 |
| Operating room time, h:min, median (range) | 3:48 (2:51–5:36) | 3:17 (2:27–4:22) | <.001 |
| Bleeding, mL, median (IQR; range) | 50 (50–125; 20–1200) | 50 (50–113; 5–500) | .504 |
| Conversions, n (%) | 5 (10) | 0 (0) | .027 |
| 1-d Postoperative hemoglobin, median (range) | 123 (90–145) | 118 (83–145) | .298 |
| Decrease in hemoglobin, g/L, median (%) | 15 (–10 to 44) n = 42 | 15 (2–65) n = 48 | .656 |
| Blood transfusion, (n) (%) | 2 (4) | 6 (12) | .269 |
| 1-d Postoperative VAS, median (range) | 2.5 (0–7) n = 35 | 3 (0–7) n = 42 | 1.000 |
| 2-d Postoperative VAS, median (range) | 2 (0–6) n = 14 | 2 (0–6) n = 13 | .430 |
| Hospital stay, d, median (IQR; range) | 2 (1–2; 1–7) | 1 (1–2;1–4) | .215 |
IQR, interquartile range; VAS, visual analog scale for pain (1–10).
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
There were 5 vs 0 conversions to laparotomy in the traditional laparoscopy and robotic surgery groups, respectively (P = .027). The reasons for these conversions included adhesions in 2 cases, and disseminated cancer, bleeding from the abdominal wall (trocar site), and a uterus too large to be removed through the vagina, 1 case each. The conversions did not extend operation times: excluding the cases with conversions, the operation times were median 171 (range 126-250) and mean 176 (SD 29) minutes (n = 44). The difference as compared to the robotic group is significant also in this setting (P = .001).
In addition to the operation time, the total time spent in the operation room was shorter in the robotic surgery group (Table 4) The median docking and robotic console times were 6 (range 1-16) and 106 (range 59-164) minutes, respectively. In both groups the operation times were significantly longer for obese patients. For 51 patients, whose BMI was <30, the operation times were median 144 (range 86-227) and mean 148 (SD 31) minutes, respectively. The corresponding figures for obese (BMI >30, n = 48) patients were 168 (range 104-259) and 171 (SD 33) minutes. The difference is statistically significant at P = .001. Interestingly, the time benefit by robotic surgery for obese patients, albeit significant at P = .001, was smaller (median 30 minutes) than for normal-weight patients (median 41 minutes) (P < .001).
The groups did not differ in the number of lymph nodes harvested (Table 3). Lymph node metastases were found in 1 patient in the traditional laparoscopy group and in 2 patients in the robotic surgery group. In both groups, lymphadenectomy was omitted in 2 cases, due to a disseminated disease for all 4 patients. The lymph node yield was greater in obese women: the median number of nodes was 21 (range 13-47) and 27.5 (range 11-51) in patients with a BMI <30 or >30, respectively (P = .001).
In the final histopathological report vs the preoperative biopsy, the diagnosis was changed for 10 patients. In the traditional laparoscopy group, 1 endometrioid adenocarcinoma was changed to carcinosarcoma and 3 endometrioid adenocarcinomas to mixed cell endometrial carcinomas, respectively. In the robotic surgery group, 3 low-grade endometrioid carcinomas were upgraded to high-grade endometrioid carcinomas, 1 tumor changed to a mixed-cell carcinoma, and finally, 2 endometrioid carcinomas changed to extrauterine carcinomas (1 tubal and 1 ovarian carcinoma).
The treatment arms did not differ from each other in respect to the amount of bleeding and the length of postoperative hospital stay (Table 4). However, obese women bled more than normal-weight women. The median volume of bleeding was 50 (range 5-400) vs 100 (range 20-1200) mL in women with a BMI <30 or >30, respectively (P = .017).
A total of 12 (24%) of the traditional laparoscopy patients and 18 (36%) of the robotic-assisted laparoscopy patients had complications (including intraoperative and all postoperative complications), respectively (P = .275) (Table 5). All 4 intraoperative complications occurred in the traditional laparoscopy group. One patient whose operation was converted to a laparotomy bled 1100 mL during laparotomy. Other surgical complications included a bladder injury and 1 case of intestinal thermal damage. Both were repaired laparoscopically. One patient had reversible carbon-dioxide retention that required a break in the operation.
| Traditional, n = 49 | Robot, n = 50 | P | |
|---|---|---|---|
| Complications | |||
| All complications, n (%) | 12 (24) | 18 (36) | .275 |
| Intraoperative, n (%) | 4 (8) | 0 (0) | .056 |
| Vascular injury/bleeding | 1 | 0 | |
| Bladder injury | 1 | 0 | |
| Intestine injury | 1 | 0 | |
| Respiratory insufficiency | 1 | 0 | |
| All postoperative, n (%) | 10 (20) | 18 (36) | .085 |
| Major early, n (%) | 1 (2) | 5 (10) | .204 |
| Intraabdominal bleeding | 1 | 4 | |
| Nerve injury | 0 | 1 | |
| Minor early, n (%) | 3 (6) | 4 (8) | 1.000 |
| Wound bleeding | 1 | 3 | |
| Nerve injury | 0 | 1 | |
| Urine retention | 2 | 0 | |
| Major late, n (%) | 4 (8) | 7 (14) | .525 |
| Infection | 4 | 6 | |
| Rectovaginal fistula | 0 | 1 | |
| Minor late, n (%) | 2 (4) | 5 (10) | .436 |
| Wound infection | 1 | 3 | |
| Urinary tract infection | 1 | 1 | |
| Foot swelling | 0 | 1 |
One patient may have >1 complication.
Mäenpää et al. Robotic surgery for endometrial cancer. Am J Obstet Gynecol 2016.
No postoperative deaths occurred during the study period, nor were any thromboembolic complications encountered. The total number of postoperative complications was higher, albeit not significantly, in the robotic surgery group (18 vs 10, P = .085) (Table 5). Five (10%) and 11 (22%) patients had major early and late postoperative complications in the traditional laparoscopy and robotic surgery groups, respectively (P = .111). In the robotic surgery group, 11 patients had 12 major complications, of which 4 were related to bleeding. One of the patients needed an embolization of the internal iliac artery in addition to transfusion. In the whole study population, only 1 patient in the robotic surgery group needed a reoperation. One month after the primary operation, she developed a rectovaginal fistula that required a temporary loop transversostomy, with full recovery. A nerve injury, located by electroneuromyography in the nerve of the left iliopsoas muscle, caused partly reversible pain and numbness of the left foot. Two patients in both groups developed an abscess, which required drainage procedures for both of the patients in the traditional laparoscopy group and for 1 patient in the robotic surgery group.
Comment
Several retrospective studies have implied that the operation time is longer in robotic-assisted than in traditional laparoscopic operations for endometrial cancer.11, 12, 13, 14, 15 We were not able to find previous randomized controlled trials on the use of robotic-assisted surgery for endometrial cancer, but the same tendency was seen in 2 of the randomized hysterectomy trials for benign indications we found.16, 17 However, in the study of Lönnerfors et al,18 comparing robotic-assisted hysterectomy to vaginal or traditional laparoscopic hysterectomy, the median operative times did not differ between the groups. The aim of this randomized, controlled prospective study was to show that robotic surgery does not take markedly longer to perform than traditional surgery. We set the limit of a “marked” lengthening to a 25% increase in operation time. Actually, robotic-assisted surgery turned out to be 18% less time-consuming than traditional surgery. In fact, there are some retrospective studies pointing at the same direction.19, 20, 21
Another general impression has been that in any case the total time spent in the operation room is longer for robotic-assisted than for traditional surgery, as the preparation takes longer. Even this impression turned out to be wrong: the total time spent in the operation room was shorter in the robotic surgery group, because the preparation time was in fact identical for both groups. However, one has to take into account that the operative team’s learning curve was already stabilized by the time the study was initiated, and the same surgeons, anesthesiologists, and nurses had already worked as a team in >100 robotic operations by the time the trial was begun. In our earlier study, we showed that the preparation and docking times get progressively shorter as the team gains experience.8 It should however be noted that our hospital is very experienced also with traditional laparoscopy, which has been used for endometrial cancer since 1990s.22
We expected the advantages of the robotic-assisted technique to become especially evident with obese patients. However, actually the time saved by robotic-assisted technique was more evident in normal-weight than in obese patients (41 vs 30 minutes, respectively). In previous studies addressing obesity and laparoscopic operations, the number of conversions has been lower in robotic-assisted surgery than in traditional laparoscopic surgery.19, 23 In the present study, all conversions had to be performed in the traditional laparoscopy group, and 4 of 5 conversions were performed on obese patients. It is of course possible that the lack of conversions in the robotic group is by chance only, and in the report of our initial experience with robotic-assisted surgery the conversion rate was in fact 4%.8 Those conversions took place in the beginning of our learning curve with robotic-assisted surgery, and similarly in the report by Paley et al,24 where they described their first 1000 robotic-assisted operations, the conversion rate was 2.9%. However, our learning curve was already well established, when this randomized trial was started, and in fact, a low rate of conversions has been evident in other studies. In the study of Cardenas-Goicoechea et al25 with 102 robotic-assisted and 173 traditional laparoscopic operations, there were only 1 vs 9 conversions, respectively.13 Also in their later report the rate of conversions in robotic-assisted staging operations was very low or 0.5%.25
The lymph node yield was not better in the robotic surgery group than in the traditional laparoscopy group. One explanation to this may be that, in our hospital, as stated above, there is a long tradition of laparoscopic surgery for endometrial cancer,22 which suggests that the laparoscopic technique was fully adopted by the time robotic assistance was introduced in our hospital in the beginning of the year 2009. On the other hand, according to the review by Gaia et al,26 the number of pelvic lymph nodes harvested is comparable between traditional and robotic-assisted laparoscopic surgery. In both of our treatment groups, the lymph node yield (median 23 and 25 in the traditional laparoscopy and robotic surgery groups, respectively) favors well with previous studies (17.8 vs 18.5, in the review of Gaia et al26 in 2010). Although the rate of postoperative complications was somewhat greater in the robotic surgery group, this was counterbalanced by the fact that intraoperative complications occurred and conversions had to be performed only in the traditional laparoscopy group. As a whole, both techniques turned out to be effective and safe alternatives for the operative treatment of endometrial cancer. Apart from the above-mentioned rectovaginal fistula, no significant late adverse events like hernias emerged during the follow-up. This is in agreement with previous studies, as the meta-analyses by Reza et al27 and Wright et al28 found similar and low25 morbidity rates for these 2 techniques. Also according to a recent study comparing robotic-assisted surgery to laparotomy for endometrial cancer, hernia formation was a problem only in the laparotomy group.29
The strengths of this study are the prospective randomized and controlled setting, and therefore a well-balanced and unbiased distribution of the patients into the groups. In addition, the learning curves of the surgeons and the whole team did not affect the results. The rather limited number of patients may be considered as a weakness. However, large randomized controlled trials in surgery are quite challenging to carry out; even in this trial it took 3 years to recruit the patients. However, the sample size was sufficient to perceive significant differences between the groups. Another shortcoming is that nowadays PLND is quite seldom carried out alone, without a simultaneous paraaortic lymphadenectomy.
In this randomized controlled trial we showed that contrary to previous assumptions, at least in our hands, hysterectomy, BSO, and PLND are faster to perform using robotic-assisted technique as compared to traditional laparoscopy. Hence, robotic surgery offers an effective and safe alternative in the surgical treatment of endometrial cancer.
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Disclosure: Dr Nieminen was proctor for robotic surgery from October 2010 to October 2014. The remaining authors report no conflict of interest.
Cite this article as: Mäenpää MM, Nieminen K, Tomás EI, et al. Robotic-assisted vs traditional laparoscopic surgery for endometrial cancer: a randomized controlled trial. Am J Obstet Gynecol 2016;215:588.e1-7.