Bernardini, Marcus Q. MD*; Gien, Lilian T. MD†; Tipping, Helen RN‡; Murphy, Joan MD*; Rosen, Barry P. MD*
The prevalence of obesity is a significant problem in Canada and the rest of the Western world. The World Health Organization and Health Canada divide obesity into 3 categories based on body mass index (BMI): class I (BMI, 30–35 kg/m2), class II (BMI, 35–40 kg/m2), and class III (BMI >40 kg/m2).1,2 Eight percent of Canadian women were obese in 1981,3 12% in 1996, and 24% in 2004. Even more striking is that the proportion of women in class II or III made up 42% of the obese population and 10% of the population as a whole in 2004.4 This group of women is often referred to as morbidly obese and presents a unique set of challenges to surgeons, as they tend to have more comorbidities and a higher risk of perioperative complications.5
Two randomized surgical clinical trials6,7 have shown that patients undergoing minimally invasive surgery (MIS) for endometrial cancer have better outcomes when compared with those undergoing laparotomy; however, data on the value of MIS for the morbidly obese patient is limited. In the GOG LAP 2 study, the median BMI was 28 kg/m2, and there were no women with a BMI in class II or higher in the interquartile range of the patients enrolled. The Laparoscopic Approach to Cancer of the Endometrium (LACE) study was designed to assess quality-of-life outcome in women surgically treated for endometrial cancer and included 72 women (40.7%) with a BMI of class II or higher in the laparoscopic arm and 49 (36.3%) in the open arm, although the results were not analyzed separately for this subgroup. Thus, randomized data about optimal surgery for class II or III obesity are lacking.
Although several groups have published their experience in using laparoscopy for the morbidly obese patient with endometrial cancer, the data are sparse. In 2002, Scribner et al8 reported a 44% successful completion rate for laparoscopic staging procedures in 28 women with a BMI greater than 35 kg/m2. In 2006, Yu et al9 reported on 4 women who underwent successful laparoscopy for the surgical management of endometrial cancer, with a median BMI of 45 kg/m2 (range, 40.4–50 kg/m2). One cystotomy was reported, and no woman underwent surgical staging. In the same year, O’Hanlan reported their experience with laparoscopy and the surgical management of endometrial cancer.10 Twelve women were morbidly obese, and the study did not show any difference in complication rates for this group of women compared to women with lower BMI.
Robotic surgery, first used in 2005 in gynecologic oncology and introduced in 2008 at our institution, has overcome some of the limitations of laparoscopy when operating on the morbidly obese patient. Two of the advantages over conventional laparoscopy in the obese patient population are the following: the third arm, which aids in retraction of bowel; and the immobile position of the trocars, which are maintained in a fixed position owing to the robotic configuration. This allows the surgeon to reduce intraperitoneal pressures, thereby reducing the burden on anesthetic ventilation of the patient. Seamon et al11 reported their experience with robotic surgery in the management of the obese patient with endometrial cancer; and although they did not analyze the group of class II or higher separately, they reported a perioperative complication rate of 11% and a conversion rate of only 15.6% for the entire cohort.
This manuscript reports specifically on women with obesity class II or higher. We compare women who underwent robotic surgery to a historical cohort of women who underwent laparotomy for the management of endometrial cancer and endometrial hyperplasia.
With Research Ethics Board (09-0094-C) approval at the University Health Network, we collected data prospectively on all women who have undergone a robotic procedure using the da Vinci surgical system (Intuitive Surgical, Sunnydale, CA) at our institution. Between November 2008 and November 2010, there have been 124 robotic procedures.
At our institution, we do not routinely perform imaging on women with low-risk histology before surgery, and because the physical examination is limited in the morbidly obese patient, the decision about whether a woman undergoes MIS versus open surgery often occurs in the operating room the day of surgery. We do not perform uterine morcellation in cases of malignancy, once the camera is inserted; if MIS is deemed not possible owing to uterine size, the woman undergoes a laparotomy. If uterine size permits a minimally invasive approach, we proceed with this type of surgery by introducing the robotic trocars. For the purpose of this analysis, however, we included all women who were brought to the operating room with the intention of having a robotic procedure as a robotic case, whether or not MIS surgery was possible. Women who underwent a robotic surgical procedure with a BMI of 35 kg/m2 or greater (class II or greater) at the time of surgery and with a diagnosis of endometrial cancer were included in this analysis (n = 45).
Research Ethics Board (10-0575-CE) approval was also obtained to identify a historical cohort of morbidly obese women (at least class II) between 2006 and January 2009 who underwent surgery for endometrial cancer. All of these women underwent surgery before the introduction of the robotic system. Sixty-five women were identified. For the primary analysis, we compared women who had open surgery (n = 41) with those who had robotic surgery (n = 45). Because the primary analysis was to compare surgical outcomes for the management of women with endometrial cancer, 8 women in the open surgery group who underwent a panniculectomy as part of their open procedure were included in the analysis. These patients were included because it was felt that their obesity necessitated the panniculectomy to facilitate the surgery for their endometrial cancer. Data were also collected on 24 morbidly obese women who had laparoscopic procedures, but these data ware not included in the primary analysis.
As part of the data collection, the following variables were recorded: age, histology, surgical type, lymph node assessment, BMI, medical comorbidities, prior abdominal surgery, surgical stage, operative and postoperative complications, length of hospital stay, estimated blood loss, and time in the operating room (OR). Prior abdominal surgery included any surgical intervention into the abdomen, whether or not it was performed via laparotomy. Total time in the OR denotes the time from when the patient entered the room to when they exited the room. This time includes anesthetic preparation time; and at our institution, all lines (venous and arterial) are often placed after the patient is brought into the OR.
All 3 surgeons who use the da Vinci system (M.B., B.R., and J.M.) follow the same surgical protocol. At the beginning of each procedure, uterine manipulation is obtained with the VCARE® (ConMed Endosurgical) device. This is placed before docking of the robot. Insufflation is obtained through the use of the Veress needle through a stab incision at the umbilicus. The trochars are then placed in a standard “ARC” configuration, with the camera port placed midway between the umbilicus and xiphisternum. In total, 5 ports are used. The camera port and the accessory ports are facilitated with 12-mm disposable trochars, and the 3 robotic ports use the 8-mm trochars provided by Intuitive Surgical. All ports in these women are placed at the level of the umbilicus or higher and are above any pannus. Robotic arm 1 controls the endoshear scissors; robotic arm 2 controls the fenestrated bipolar graspers. When we initiated the program, the third robotic arm was used on the left side of the patient; however, after 1 year of the program, we switched to having the accessory third arm on the right. This facilitated having 2 robotic grasping devices available for use at the same time. The vaginal cuff was closed with interrupted figure of 8 sutures using a dissolvable suture.
The departmental policy at our institution regarding lymphadenectomy in endometrial cancer is based on preoperative risk stratification. For women with a central pathology–reviewed grade 1 endometrial cancer, we do not routinely perform a lymphadenectomy, unless there is gross evidence of lymph node enlargement. For women of grade 2 or higher, we perform a lymphadenectomy in the pelvis and, where possible, the para-aortic region. The definition of a pelvic lymphadenectomy includes removing the lymph node tissue overlying the external iliac artery and vein from the deep circumflex vein to the bifurcation of the internal and external iliac vessels. In addition, the lymphatic tissue in the obturator space is removed. The superior border of the para-aortic lymph node dissection is the inferior mesenteric artery and will include tissue from the common iliac region.
Statistical analysis was done using SAS 9.2. Chi-square analysis was used to compare categorical data, with the Fisher exact test for small cell comparisons. The Mann-Whitney U test was used to compare nonparametric data. A 2-tailed P < 0.05 was considered statistically significant.
A total of 86 women with a BMI of 35 kg/m2 or greater (class II or greater) who underwent primary surgery for endometrial cancer were analyzed in this study. Forty-five women had robotic surgery, and 41 women had open surgery. There were no differences between the groups in age, BMI, number of comorbidities, prior abdominal surgery, or histology (Table 1). This population has a high percentage of women with multiple (>3) comorbidities: 51% in the robotic group and 51% in the open group.
Table 2 outlines the operative characteristics for each group. In the robotic group, the total time in the OR was significantly higher; however, estimated blood loss was less and total hospital stay was significantly shorter. The median length of stay was 2 days for all robotic procedures compared to 4 for open procedures (P < 0.0001). There were no differences in median pelvic lymph node counts between the 2 groups (open, 10.5, vs robotic, 11); however, para-aortic lymph nodes were removed more often in the robotic procedures (20% vs 7%). In total, 3 women (9%) had positive lymph nodes, 2 in the open group and 1 in the robotic group.
The overall intraoperative complication risk in the study population was 5.8% (5/86; Table 3). In the open surgery group, the risk was 7.3%, and in the robotic group, it was 4.4% (P = 0.884). Two patients required blood transfusions owing to bleeding in the open surgery. In one case, the estimated blood loss was 3500 cm3 owing to an enlarged uterus (20-week size) and pelvic sidewall bleeding. In the second case, the estimated blood loss was 2000 cm3 owing to an enlarged ovary stuck along the pelvic sidewall. Only 1 patient in the robotic group received a blood transfusion, and this was after conversion to laparotomy. The blood loss in this case was 1500 cm3. There was one enterotomy in the robotic group and one obturator nerve injury in the open surgery group.
In total, there were 4 conversions (4/45) from the robotic to the open approach. In one case, this was due to adhesions and uterine size; and in the other 3 cases, this was due to uterine size. In 2 of those cases, the conversion occurred before initiating robotic surgery after visualization of the uterine size with the camera. In all conversions, a midline laparotomy was used to complete the procedure. One woman, whose surgery resulted in a conversion to laparotomy, had a hospital stay of 24 days. She had previous renal disease and developed acute tubular necrosis after surgery.
Table 4 outlines the postoperative complications in this group of women. The total postoperative complication rate for the entire study population is 31%. The results for postoperative complications are presented in 2 formats. Intention to treat includes complications for all robotic cases, irrespective of whether a robotic procedure was even attempted; and actual treatment results, which include only the cases for which robotic surgery was attempted. There were significantly less postoperative complications in the robotic group compared to the open surgery group in both the intention-to-treat group (17.7% vs 44%l; P = 0.007) and the actual treatment group (16.3% vs 44%; P = 0.004). The major difference in the 2 groups was postoperative wound infection. There were 8 wound infections necessitating intervention in the open surgery group compared to one in the robotic group (P = 0.014). In addition, the postoperative transfusion rate was 7% in the open surgery group compared to 2% in the robotic surgery group, although this result was not statistically significant.
Minimally invasive surgery has been demonstrated to be safe and superior to open surgery in 2 randomized clinical trials comparing the techniques for the management of endometrial cancer. One limitation of laparoscopy, however, is the difficulty in performing these cases for morbidly obese patients. In the LAP 2 study,7 conversion rates were 27% in women with BMI greater than 35 kg/m2 and 57% in women with BMI greater than 40 kg/m2. These women now comprise greater than 10% of the adult female population in Canada, and effective strategies are needed to manage this population who are at an increased risk of perioperative complications. Currently, most of the women in North America continue to have their endometrial cancer surgery done through a laparotomy.12
Two primary factors are responsible for low uptake of laparoscopy in the morbidly obese population. First, visibility is poor. With excess adipose tissue, especially in periperitoneal areas, and bowel mesentery, the surgeon is often unable to visualize the surgical field in an optimal manner. Even if one is able to perform the hysterectomy, the inability to achieve an adequate lymphadenectomy precludes one from attempting the procedure in this manner. The second major limitation for laparoscopic surgery has to do with the ventilation requirements of these patients. The inability to ventilate the morbidly obese patient owing to the combination of steep Trendelenburg position, the added weight of the body tissue, and the intraperitoneal pressures required for laparoscopic visualization again preclude this type of surgery for many of these patients.13 Thus, even in patients that have been selected as candidates for MIS, conversion rates for laparoscopic endometrial cancer surgery in women BMI class II or greater range from 14% to 36%.8,14
The introduction of robotic surgery has rapidly changed the surgical landscape in gynecologic oncology, and increasingly more women are now being treated in a minimally invasive approach. Robotic surgery seems to overcome both of the limitations described above. Visualization is improved in part owing to the third robotic arm, which can be used to retract tissue and be fixed in position. This allows the assistant to introduce a second accessory port, when needed, and have a total of 3 instruments retracting tissue. The second advantage involves reducing the pressure on the chest cavity, thereby minimizing the inability to ventilate the patient effectively. Once the robotic system is docked, one can effectively reduce the intraperitoneal pressure to lower than 10 mm Hg without impairing visualization. This is a result of the robotic arms supporting the anterior abdominal wall independent of CO2 insufflation. This is not possible with laparoscopy, as reducing intraperitoneal pressures will obscure visibility. When closing the vaginal cuff, robotically, one is often working at reduced intraperitoneal pressures without difficulty. In addition, many of these women have a weight distribution that falls below the umbilicus and are thereby supported by the robotic arms. The authors feel that the added advantage of fixed robotic ports in addition to the retracting ability of the third robotic arm facilitate MIS surgery in this patient population and are the explanation for the low conversion rate seen in robotic surgery.
In the current study, the conversion rate to laparotomy was 8.9% (4/45) for women who were brought to the operating room with the intention of a robotic procedure and only 4.8% (2/42) for women in whom a robotic procedure was attempted, showing the surgical advantages for robotic surgery in this patient population. For the 2 women who were converted before docking, the uterine weights were 442.4 and 99.2 g. In the case of the second patient, intraperitoneal adhesions were the reason for abandoning the procedure. For the 2 women who were converted after initiation of the robotic procedure, the uterine weights were 725.5 and 265.3 g. In both cases, visualization did affect the ability to continue with the robotic procedure.
No correlation could be made between the inability to perform a robotic procedure and prior abdominal surgery. Of the 4 women for whom robotic surgery was not possible, only 2 of them had prior abdominal surgery. In the case of the woman who had an enterotomy as part of her robotic procedure, she had no history of abdominal surgery. The injury was made with the introduction of the trochars and was repaired by slightly extending the trochar incision, thus avoiding conversion to a laparotomy. The woman in the open group who sustained an injury to the obturator nerve had 2 previous caesarean sections; however, it is unlikely that these contributed to the injury that occurred during the lymph node dissection. This injury was the result of hemostatic clips that were applied along the nerve during hemostatic control. These were identified and removed before the completion of the case, and no effects were evident in the patient after the operation.
Through the cooperation of 2 large academic centers with access to the da Vinci robotic system, Seamon et al11 were able to show the impact of robotics in the obese population by reporting on the largest collection of obese women treated with the Da Vinci robotic system. In their series, they present 109 women with a BMI of greater than 30 kg/m3. Among these women were 70% with class II obesity or higher. They reported a perioperative complication rate of 11%. In 2007, Gehrig et al14 compared outcomes in the obese population between robotics and laparoscopy. Compared to laparoscopy, robotic surgery resulted in decreased blood loss, shorter operating time, and increased lymph node removal. In their analysis, however, only 13 women were classified as morbidly obese.
In this paper, we show that even with a relatively small number of cases at our institution, we have been able to extend robotic technology to this high-risk population who previously did not have an effective option for MIS. Thirty-five percent of the cases performed on the robot at our institution to date have been on women with class II obesity or higher. This population had a lower rate of operative and postoperative complications. The median length of stay in the robotic group was 2 days; however, this was influenced by the fact that initially, we were conservative in discharging these patients. If only the last 20 morbidly obese cases are analyzed, the median length of stay is 1 day, which matches our total robotic population.
One of the major differences between the robotic cases and open cases in our series is the total OR time. This measure was chosen because it was the only time collected in both sets of patients: open and robotic, and also from a practical perspective is what influences OR resources. The median percentage of surgical operative time to total OR time was 81% for the robotic cases (data not shown). This means that 19% of the total OR time is taken up by patient preparation; this includes anesthetic preparation. Although we do not have this same measure for the open cases, we postulate that this increased preparatory time is higher in robotic cases, thereby providing the opportunity to reduce total OR time for robotics moving forward.
The greatest difference between the open and robotic cohorts relates to the perioperative complications. There were only 2 postoperative wound infections in the robotic group compared to 8 in the open group. One of these women was converted to laparotomy before attempting robotic surgery; thus, the true wound infection rate is really 1/43 (2.3%). Only wound infections that necessitated intervention either pharmacologically or through mechanical drainage were considered an infection. Women who had a panniculectomy as part of their procedure had a wound infection rate of 50%. Even after excluding these women, the overall complication rate for the laparotomy group remained at 39%; however, the wound infection rate dropped from 19.5% to 12%. Postoperative wound infections are an important measure when studying health economics. These infections may potentially result in increased health care expenditure owing to the introduction of home nursing. For the purpose of the current study, however, these data were not collected. There was 1 death in the laparotomy group. This patient suffered a postoperative pulmonary embolism. There were no clinically apparent thrombotic events in the robotic group compared to 5% (2/41) in the open surgery group.
Regarding lymph node dissection, most of the women were of preoperative grade 1 histology. At our institution, we do not routinely perform lymph node dissection on this patient population. Rates of lymph node dissection were equivalent in the open surgery group (34%) and the robotic group (35%); however, para-aortic dissection was performed on only 3 women (7%) in the open surgery group with a median node count of 2 compared to 9 (21%) women in the robotic group with a median node count of 6. Although these differences did not reach statistical significance owing to small numbers, better visualization of the para-aortic region in robotic cases likely contributed to the higher percentage of women who underwent para-aortic lymph node dissection in this patient population.
Laparoscopic procedures in the morbidly obese population have been performed at our institution; however, in most of these cases, the surgery has been limited to hysterectomy and bilateral salpingo-oophorectomy. Only 3 of 24 women had a lymph node dissection, and of the 3 women, the largest BMI was 36.8 kg/m3 (data not shown). Furthermore, no woman in the laparoscopic group had a para-aortic lymph node dissection. Length of hospital stay and estimated blood loss were equivalent between the laparoscopic cases and those performed robotically.
The data presented in this manuscript describe the successful implementation of robotic surgery at our institution in morbidly obese women. Robotic surgery has made MIS feasible in this population, reducing operative and postoperative complications, increasing assessment of lymph nodes, and reducing length of hospital stay. For programs with access to the da Vinci robotic system, this surgical approach should be considered as the ideal approach for the morbidly obese patient. This group should not be excluded from any future trials addressing open surgery versus MIS.