ORIGINAL STUDY
Comparing Robotic Surgery With Conventional Laparoscopy and Laparotomy for Cervical Cancer Management Ching-Hui Chen, MD,*Þþ Li-Hsuan Chiu, PhD,* Ching-Wen Chang, MD,*Þ Yuan-Kuei Yen, MD,*Þ Yan-Hua Huang, MD,* and Wei-Min Liu, MD*Þ
Objective: The aim of this study was to compare the outcomes of robotic surgery, laparoscopy, and laparotomy for the surgical treatment of stage IA to IIB cervical cancer. Methods: This retrospective study was carried out in a university-affiliated teaching hospital. A total of 100 women with an initial diagnosis of stage IA to IIB cervical cancer, without preoperative brachytherapy or chemotherapy, were included in this study. With selection of the cases, 44 patients received laparotomy surgery, 32 patients received laparoscopic surgery, and 24 patients received robotic surgery. The perioperative parameters measured included operation time, blood loss, transfusion rate, lymph node yield, adhesion score, laparotomy conversion rate, postoperative and 24-hour pain scores, time to full diet resumption, and hospital stay. The perioperative complication and disease-free survival were also evaluated. Results: The robotic group showed a shorter operation time, less blood loss, lower transfusion rate, and lower laparotomy conversion rate than the laparoscopic or laparotomy group. As for the postoperative parameters, the robotic group showed reduced postoperative and 24-hour pain scores, shortened length of hospital stay, and decreased time to full diet resumption compared with the other 2 surgical groups. No significant differences were found between the groups in perioperative complication rate or disease-free survival. Conclusions: The data suggested that robotic surgery is a feasible and potentially optimal option for the treatment of stage IA to IIB cervical cancer with favorable short-term surgical outcomes. Key Words: Cervical cancer, Radical hysterectomy, Laparotomy, Laparoscopic surgery, Robotic surgery (Int J Gynecol Cancer 2014;24: 1105Y1111)
surgery has been applied to various gynecologic R obotic procedures such as sacral colpopexy, cystectomy, myomec-
tomy, hysterectomy, lymphadenectomy, and cancer management.1Y4 Recent studies have demonstrated the feasibility of
*Department of Obstetrics and Gynecology, Taipei Medical University Hospital, Taipei, Taiwan; †Department of Obstetrics and Gynecology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan; and ‡Graduate School of Human Sexuality, Shu-Te University, Kaohsiung County, Taiwan. Address correspondence and reprint requests to Wei-Min Liu, MD, Department of Obstetrics and Gynecology, Taipei Medical University Hospital and Taipei Medical University, No 252, Wu-Hsing St, Sinyi District, Taipei 11031, Taiwan. E-mail: [email protected]. The authors declare no conflicts of interest. Copyright * 2014 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000160 International Journal of Gynecological Cancer
robotic surgery for gynecologic cancer management.5Y8 Favorable results have been obtained for robotic surgery to manage early stage cervical cancer3,9Y12 and locally advanced cervical cancer.13,14 However, there have also been reports suggesting that robotic procedures showed no significant benefits as compared with laparoscopic procedures in short-term surgical outcomes.4,15 In this study, we analyzed the surgical results of robotic surgery, laparoscopy and laparotomy for treating stage IA to IIB cervical cancer. The perioperative parameters included blood loss, transfusion rate, operation time, adhesion score, pelvic lymph node yield, postoperative pain scores, duration to full diet resumption, and length of hospital stay. The postoperative complications and disease-free survival (DFS) were also evaluated. Compared with the conventional approaches, the feasibility of robotic surgery for treating stage IA to IIB cervical cancer was examined in this current study.
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METHODS According to the pathology report, a total of 162 consecutive patients with cervical cancer were reviewed for their medical history. Among the cases, 57 patients who were not eligible to receive surgical intervention due to advanced clinical stage (greater than IIB) and 5 patients who received preoperative brachytherapy or chemotherapy were excluded; a total of 100 patients with stage IA to IIB were included in this study (Fig. 1). Of the enrolled cases, 24 received robotic radical hysterectomy, 32 received laparoscopic radical hysterectomy, and 44 received abdominal radical hysterectomy. All patients were informed of their options for the types of surgical procedures including robotic surgery, laparoscopic surgery, and laparotomy and the risks and benefits of these procedures according to their surgical history, disease condition, and insurance coverage. The choice of the surgical approach was according to the patient’s will, except for the patients with previous pelvic surgeries (Q2 times) who were suggested to receive robotic or laparotomy procedure. Before surgery, patients underwent 2 days of bowel preparation, and preoperative antibiotics were administered. The surgical procedures performed were radical hysterectomy, bilateral salpingo-oophorectomy, and bilateral pelvic lymph node dissection. All patients received pain control with patientcontrolled analgesia or nonsteroidal anti-inflammatory drugs during postoperative care. The reviewed patient characteristics were age, body mass index (BMI), histology type, and the disease stage according to the International Federation of Gynecology and Obstetrics. The assessed intraoperative parameters included operation time, blood loss, transfusion rate, lymph node yield, adhesion score, and laparotomy conversion rate. Blood loss was defined as the total volume of suctioned fluids.
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To evaluate the severity of pelvic adhesions during the procedure, we adopted the scoring system from the Adhesion Scoring Group.16 The operation time was measured from the time of skin incision until all surgical staging procedures were completed. The postoperative parameters included the postoperative pain score and 24-hour pain score, the duration until the patient resumed a full diet after the operation, and the length of hospital stay. The pain score was self-reported and routinely evaluated for each patient during postoperative care using an adult pain score numerical rating scale, and the data were obtained both postoperatively (on the operation day after the patient was awakened from anesthesia) and at 24 hours after the operation. For reference scoring, score 0 indicates no pain, and score 10 represents the worst pain imaginable. The time duration before full diet resumption was defined as the number of postoperative days until patients can tolerate regular intake of solid food. The length of hospital stay was defined as the number of postoperative days until the patient was discharged. For statistical analysis, all obtained data were analyzed using SPSS statistics (version 21.0, IBM). The mean value, SD, median, and range of each perioperative parameter were reported. The statistical analysis was performed with 1-way ANOVA, Tukey HSD post hoc analysis, or W2 analysis; a p G .05 was considered statistically significant between the groups.
RESULTS According to the inclusion criteria, 100 women were included in the current study. Among the participants, 24 received robotic radical hysterectomy, 32 received laparoscopic radical hysterectomy, and 44 received abdominal radical hysterectomy. As shown in Figure 1, only patients who
FIGURE 1. Inclusion flowchart of all enrolled patients.
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received surgical intervention, with clinical stage IA to IIB, and without preoperative brachytherapy or chemotherapy were included. Patients with a clinical stage greater than IIB were excluded and defined as patients who were not eligible to receive surgical intervention. To avoid the bias caused by case selection, the baseline characteristics of all enrolled patients were examined. Table 1 lists the baseline characteristics of the enrolled patients. The mean (SD) ages were 51.9 (11.3) (laparotomy group), 51.2 (11.9) (laparoscopic group), and 53.7 (15.3) (robotic group), demonstrating no significant difference among the groups. The mean (SD) BMIs were 24.9 (4.6) kg/m2 (laparotomy group), 23.2 (3.4) kg/m2 (laparoscopic group), and 24.4 (4.9) kg/m2 (robotic group), also demonstrating no significant difference among the groups. The numbers of cases with positive lymph node finding were reported as 20.5% (laparotomy group), 9.4% (laparoscopic group), and 12.5% (robotic group). The percentage of each FIGO stage and the histology types of the disease were presented as well (Table 1). The percentage of stage I and II cases, along with the case number with positive lymph nodes, was found to be not significant between the groups, indicating that the study population from each surgical group was comparable. Table 2 lists the intraoperative parameters. The robotic group showed a higher mean adhesion score than did the other groups, although the differences were not significant among the groups. No significant differences were determined in the mean number of pelvic lymph nodes retrieved between the groups. However, the operation time was significantly reduced in the robotic group (192.3 [51.2] minutes) compared
Robotic Surgery for Cervical Cancer
with the laparoscopic group (292.8 [65.2] minutes) and the laparotomy group (302.9 [76.4] minutes). The volume of blood loss during the operation was also significantly decreased in the robotic (116.7 [107.0] mL) and laparoscopic (225.0 [164.1] mL) groups compared with the laparotomy group (1139.0 [656.8] mL). Correspondingly, the transfusion rates of the robotic group (8.3%) and the laparoscopic group (25.0%) were much lower than the laparotomy group (75.0%). Of the patients in the laparoscopic group, 3.0% (1/33) underwent conversion from laparoscopy to laparotomy; none of the patients in the robotic group were converted. Table 2 also lists the postoperative evaluation factors. The robotic group showed a significantly lower postoperative pain score (2.8 [1.4]) than did the laparoscopic (4.5 [2.3]) or laparotomy (5.6 [2.3]) group. The 24-hour pain score of the robotic group was also decreased (2.0 [0.9]) compared with the laparoscopic group (3.7 [2.4]) or the laparotomy group (4.6 [2.0]). Moreover, compared with the laparotomy group (3.4 [1.7] days), the laparoscopic (2.1 [0.9] days) and robotic (1.9 [0.7] days) groups showed significantly reduced amount of time before patients resumed a full diet after surgery. The duration of the hospital stay was also significantly decreased in the robotic group (4.6 [2.6] days) compared with the laparoscopic (9.0 [2.7] days) and laparotomy (11.2 [3.3] days) groups. The complication rates were reported in Table 3. For perioperative complications, 4 patients (2 patients with ureter laceration, 1 patient with iliac vein rupture, and 1 patient with postoperative wound infection) were examined in the laparotomy group. A total of 3 cases (1 case of bladder
TABLE 1. Baseline characteristics of enrolled patients
Age, y Mean (SD) Median Range BMI, kg/m2 Mean (SD) Median Range Stage, % (n) IA to IB IIA to IIB No. cases with positive lymph nodes, % (n) Histology, % (n) Squamous Adenocarcinoma Other
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
51.9 (11.3) 50.0 28Y80
51.2 (11.9) 50.0 32Y83
53.7 (15.3) 50.5 29Y89
0.83
24.9 (4.6) 24.9 11.9Y37.5
23.2 (3.4) 22.5 17.2Y31.3
24.4 (4.9) 23.1 17.9Y38.0
0.15
77.3 (34/44) 22.7 (10/44) 20.5 (9/44)
84.4 (27/32) 15.6 (5/32) 9.4 (3/32)
75.0 (18/24) 25.0 (6/24) 12.5 (3/24)
0.75 0.12 0.07
75.0 (33/44) 22.7 (10/44) 2.3 (1/44)
81.3 (26/32) 15.6 (5/32) 3.1 (1/32)
54.2 (13/24) 37.5 (9/24) 8.3 (2/24)
0.06 G0.05 0.09
P
Baseline characteristics of enrolled patients were summarized. Data were presented as mean (SD) or percentage (case number). The median and range of each data set were listed as well. The statistical analysis was performed with 1-way ANOVA and Turkey HSD post hoc analysis or W2 analysis. n, number of cases.
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TABLE 2. Intraoperative and postoperative parameters in the laparotomy group, laparoscopic group, and robotic group
Adhesion Score Mean (SD) Median Range Lymph node yield Mean (SD) Median Range Operation time, min Mean (SD) Median Range Blood loss, mL Mean (SD) Median Range Transfusion rate, % (n) Conversion rate Pain score (postoperative) Mean (SD) Median Range Pain score (24 hrs) Mean (SD) Median Range Receiving full diet, d Mean (SD) Median Range Hospital stay, d Mean (SD) Median Range
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
0.7 (1.6) 0 0Y5
0.9 (1.9) 0 0Y5
27.8 (11.0) 25 10Y49
Post Hoc Analysis
P
1.6 (2.2) 0 0Y6
LAPA = LPS = ROBO
0.311
29.7 (15.4) 26 7Y66
29.0 (10.9) 27 13Y60
LAPA = LPS = ROBO
0.816
302.9 (76.4) 298 193Y540
292.8 (65.2) 292.5 136Y435
192.3 (51.2) 192.5 88Y270
LAPA = LPS 9 ROBO
G0.05
1139.0 (656.8) 1080 100Y3000 75.0 (33/44) V
225.0 (164.1) 150 50Y750 25.0 (8/32) 3.0 (1/33)
116.7 (107.0) 75 50Y500 8.3 (2/24) 0 (0/24)
LAPA 9 LPS = ROBO
G0.05
V V
G0.05 V
5.6 (2.3) 6 2Y10
4.5 (2.3) 5 0Y8
2.8 (1.4) 3 0Y5
LAPA = LPS 9 ROBO
G0.05
4.6 (2.0) 5 2Y8
3.7 (2.4) 3 0Y8
2.0 (0.9) 2 0Y4
LAPA = LPS 9 ROBO
G0.05
3.4 (1.7) 3 1Y11
2.1 (0.9) 2 1Y4
1.9 (0.7) 2 1Y3
LAPA 9 LPS = ROBO
G0.05
11.2 (3.3) 11 5Y21
9.0 (2.7) 10 4Y15
4.6 (2.6) 4 1Y12
LAPA 9 LPS 9 ROBO
G0.05
Intraoperative and postoperative parameters for each surgical group were listed. Data were presented as mean (SD) or percentage (case number). The median and range of each data set were listed as well. The statistical analysis was performed with 1-way ANOVA and Turkey HSD post hoc analysis or W2 analysis. LAPA, laparotomy group; LPS, laparoscopic group; n, number of cases; ROBO, robotic group.
perforation, 1 case of postoperative ileus, and 1 case of postoperative pelvic infection) were reported in the laparoscopic group. In the robotic group, only 1 patient with postoperative pelvic infection was examined. The overall complication rates were 9.1% for the laparotomy group, 9.4% for the laparoscopic group, and 4.2% for the robotic group. No significant differences were found between the groups.
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Table 4 demonstrated the follow-up of the patients of each surgical group. The mean (SD) follow-up times were 37.1 (23.6) months for the laparotomy group, 34.6 (25.4) months for the laparoscopic group, and 13.9 (7.4) months for the robotic group. The overall survival was not evaluated because of the short follow-up interval. To determine the disease-free interval (DFI) and DFS at 13.9 months, the * 2014 IGCS and ESGO
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TABLE 3. Perioperative complications in the laparotomy group, laparoscopic group, and robotic group Complications Bladder perforation Ureter laceration Iliac vein rupture Postoperative ileus Postoperative pelvic infection Postoperative wound infection Total, % (n)
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
Significance
V 2 1 V V 1 9.1 (4/44)
1 V V 1 1 V 9.4 (3/32)
V V V V 1 V 4.2 (1/24)
0.26
Perioperative complications in the laparotomy, laparoscopic, and robotic groups were reported. Data were presented as percentage (case number). The statistical analysis was performed with Pearson W2 analysis. n, number of cases.
events were defined as recurrence or progression of the disease within the observation interval. In the laparotomy group, a DFS of 90.9% was reported, and the DFI was 13.6 (0.2) months (95% confidence interval [CI], 13.2Y14.1). In the laparoscopic group, a DFS of 90.6% was examined; the DFI was 13.5 (0.3) months (95% CI, 12.9Y14.1). As for the robotic group, a DFS of 95.8% was reported, and the DFI was 13.9 (0.0) (95% CI, 13.8Y13.9). The overall comparison analyses revealed no significant difference between the groups in DFI and DFS.
DISCUSSION For the management of cervical cancer, Tinelli et al3 showed that no significant difference was found between robotic and laparoscopic approaches in blood loss, hospital stay, complications, or recurrence rates. Besides, the operation time for robotic surgery was longer than that of the laparoscopic approach.3 On the other hand, Soliman et al10 reported that robotic surgery is associated with decreased blood loss and shortened hospital stay; however, both the robotic and laparoscopic approaches showed a longer operation time than did the laparotomy. Geetha and Nair9 further demonstrated that blood loss and transfusion rates were lower in either robotic or laparoscopic surgery as compared with laparotomy; length of hospital
stay of the robotic group was also shorter than that of the other 2 groups. This study corresponds with our results showing that the robotic approach is associated with decreased blood loss, low transfusion rate, and shortened hospital stay. However, it also showed an inconsistency with our data in mean operation time. From our study, the operation time of robotic surgery (192.3 [51.2] minutes) was significantly shorter than that of laparoscopy (292.8 [65.2] minutes) or laparotomy (302.9 [76.4] minutes) (Table 2). Robotic surgery has been demonstrated to have a relatively shorter learning curve and lower proficiency plateau than the conventional approaches.17 A significant reduction in operative time, blood loss, and complication rates in the latter phase of the learning curvewas noted.18 By our data, it is suggested that, with a proper caseload and training of the surgical team, a significantly better short-term operative parameters for the robotic approach could be achieved. The robotic group was also found to associate with a shortened hospital stay than the other 2 groups (4.6 [2.6] days for the robotic group, 9.0 [2.7] days for the laparoscopic group, and 11.2 [3.3] days for the laparotomy group). However, a prolonged postoperative hospital stay from each group was also noticed in our data, which is longer than that from the other reports in average. A speculation is that the inconsistency in the mean length of hospital stay might be due to the societal difference between Taiwan and other countries. With the coverage of subsidies from national health insurance in
TABLE 4. Follow-up of enrolled patients of various surgical groups Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
P*
37.1 (23.6) 13.6 (0.2) (95% CI, 13.2Y14.1) 90.9 (40/44)
34.6 (25.4) 13.5 (0.3) (95% CI, 12.9Y14.1) 90.6 (29/32)
13.9 (7.4) 13.9 (0.0) (95% CI, 13.8Y13.9) 95.8 (23/24)
V 0.9* 0.52*
Follow-up, mo DFI, mo† DFS, %†
Survival analysis of each surgical group was presented. Data were presented as mean (SD) or percentage (case number). *The statistical analysis was performed with W2 analysis. †DFI and DFS at 13.9 months. n, number of cases.
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Taiwan, cancer patients tend to extend their hospital stay for longer postoperative care. Pelvic lymph node dissection is considered as a critical step in cervical cancer management.19Y24 Robotic surgery has been suggested to facilitate lymph node dissection in various cancer management procedures.12,25,26 Nonetheless, compared with laparoscopy, robotic surgery was associated with only comparable lymph node yields and similar overall survival rates.8,27 To evaluate the performance for lymphadenectomy by robotic approach, we compared the lymph node yields from each surgical group. Corresponding with the previous reports, our data suggested that the total lymph node yield of the robotic approach (29.0 [10.9]) was comparable with that of the laparoscopic (29.7 [15.4]) or laparotomy (27.8 [11.0]) approach (Table 2). A low complication rate of 4.2% was reported for the robotic group, compared with the laparoscopic (9.4%) or laparotomy (9.1%) group; however, no significant difference was found between the groups (Table 3). These data partially correspond with the report of Geetha and Nair,9 demonstrating that robotic surgery was associated with a lower complication rate whereas the numbers of lymph node retrieval among the groups were similar. Interestingly, the robotic group showed a higher mean (SD) adhesion score (1.6 [2.2]) than did the laparoscopic (0.9 [1.9]) or laparotomy (0.8 [1.6]) groups, yet the differences were nonsignificant (Table 2). In contrast, the robotic group exhibited a relatively lower laparotomy conversion rate (0%) than did the laparoscopy group (3.3%) (Table 2). These outcomes imply that the robotic approach may achieve comparable surgical outcomes with laparoscopy or laparotomy, even with complicated surgical conditions such as pelvic adhesions. It is then speculated that, under similar circumstances, the flexibility of the robotic surgery may contribute to its short-term surgical performance and lower the conversion rate to laparotomy. El Hachem et al28 demonstrate that robotic surgery is equivalent to conventional laparoscopy in subjective and objective measures of postoperative pain during laparoscopic gynecologic procedures. On the contrary, for cervical cancer management, Soliman et al29 reported that significantly less analgesics were required for the robotic group than the laparoscopic group. By our data, reduced postoperative and 24-hour pain scores were examined in the robotic group (Table 2). These results suggest that the robotic approach was associated with a lower postoperative pain. Besides, the outcomes from our study indicated that the robotic group was associated with a significantly shortened hospital stay, which corresponds to the results from Geetha and Soliman.9Y10 Moreover, patients in the robotic and laparoscopic groups resumed a full diet sooner after surgery than did the laparotomy group (Table 2). These results indicated that the robotic approach is associated with favorable perioperative parameters, significantly improving the short-term surgical outcomes of cervical cancer patients. In DFS, the DFI and DFS of each surgical group were analyzed (Table 4). The robotic group showed a similar DFI and DFS to the other 2 groups without significant difference. However, because of the restriction of the retrospective design of this study, the observation period of the robotic group was set from 2011 to 2013. In contrast, the
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observation period for the laparoscopic and laparotomy groups was from 2005 to 2013. To avoid a possible bias due to the short observation period, an overall survival analysis was not performed. An additional follow-up is still needed to examine the long-term survival outcomes. Wright et al30 compared robotic hysterectomy and laparoscopic hysterectomy during a 3-year period and found that robotic surgery showed no significant clinical advantage than laparoscopy for treating benign gynecologic conditions. In contrast, another study from the same research group examined the effectiveness of robotic procedures in 1894 cases of cervical cancer patients.11 In their study, both the robotic group and the laparoscopic group had lower transfusion requirements and shorter hospital stays than the laparotomy group. Interestingly, the laparoscopic group was associated with higher costs than the abdominal group, as the cost of robotic group was not statistically different from the abdominal group. The outcomes implied that, although not significant in treating patients with benign gynecologic condition, robotic surgery still showed certain clinical benefits in managing gynecologic cancer patients. Our findings corresponded with the previous reports and further demonstrated that robotic surgery was associated with favorable shortterm outcomes in treating cervical cancer patients compared with the conventional means. The limitation of this current study is that the observation period is short and a larger randomized controlled trial is required to examine the long-term survival.31 Another limitation is that the cohort of patients was not unselected cases, whereas the surgeon made suggestions on the surgical approach and the patients did selfselection to undergo robotic, laparoscopic, or laparotomy procedure. In conclusion, we suggest that robotic surgery is a feasible and potentially optimal option for the management of stage IA to IIB cervical cancer.
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Comparing Robotic Surgery With Conventional Laparoscopy and Laparotomy for Cervical Cancer Management Ching-Hui Chen, MD,*Þþ Li-Hsuan Chiu, PhD,* Ching-Wen Chang, MD,*Þ Yuan-Kuei Yen, MD,*Þ Yan-Hua Huang, MD,* and Wei-Min Liu, MD*Þ
Objective: The aim of this study was to compare the outcomes of robotic surgery, laparoscopy, and laparotomy for the surgical treatment of stage IA to IIB cervical cancer. Methods: This retrospective study was carried out in a university-affiliated teaching hospital. A total of 100 women with an initial diagnosis of stage IA to IIB cervical cancer, without preoperative brachytherapy or chemotherapy, were included in this study. With selection of the cases, 44 patients received laparotomy surgery, 32 patients received laparoscopic surgery, and 24 patients received robotic surgery. The perioperative parameters measured included operation time, blood loss, transfusion rate, lymph node yield, adhesion score, laparotomy conversion rate, postoperative and 24-hour pain scores, time to full diet resumption, and hospital stay. The perioperative complication and disease-free survival were also evaluated. Results: The robotic group showed a shorter operation time, less blood loss, lower transfusion rate, and lower laparotomy conversion rate than the laparoscopic or laparotomy group. As for the postoperative parameters, the robotic group showed reduced postoperative and 24-hour pain scores, shortened length of hospital stay, and decreased time to full diet resumption compared with the other 2 surgical groups. No significant differences were found between the groups in perioperative complication rate or disease-free survival. Conclusions: The data suggested that robotic surgery is a feasible and potentially optimal option for the treatment of stage IA to IIB cervical cancer with favorable short-term surgical outcomes. Key Words: Cervical cancer, Radical hysterectomy, Laparotomy, Laparoscopic surgery, Robotic surgery (Int J Gynecol Cancer 2014;24: 1105Y1111)
surgery has been applied to various gynecologic R obotic procedures such as sacral colpopexy, cystectomy, myomec-
tomy, hysterectomy, lymphadenectomy, and cancer management.1Y4 Recent studies have demonstrated the feasibility of
*Department of Obstetrics and Gynecology, Taipei Medical University Hospital, Taipei, Taiwan; †Department of Obstetrics and Gynecology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan; and ‡Graduate School of Human Sexuality, Shu-Te University, Kaohsiung County, Taiwan. Address correspondence and reprint requests to Wei-Min Liu, MD, Department of Obstetrics and Gynecology, Taipei Medical University Hospital and Taipei Medical University, No 252, Wu-Hsing St, Sinyi District, Taipei 11031, Taiwan. E-mail: [email protected]. The authors declare no conflicts of interest. Copyright * 2014 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000160 International Journal of Gynecological Cancer
robotic surgery for gynecologic cancer management.5Y8 Favorable results have been obtained for robotic surgery to manage early stage cervical cancer3,9Y12 and locally advanced cervical cancer.13,14 However, there have also been reports suggesting that robotic procedures showed no significant benefits as compared with laparoscopic procedures in short-term surgical outcomes.4,15 In this study, we analyzed the surgical results of robotic surgery, laparoscopy and laparotomy for treating stage IA to IIB cervical cancer. The perioperative parameters included blood loss, transfusion rate, operation time, adhesion score, pelvic lymph node yield, postoperative pain scores, duration to full diet resumption, and length of hospital stay. The postoperative complications and disease-free survival (DFS) were also evaluated. Compared with the conventional approaches, the feasibility of robotic surgery for treating stage IA to IIB cervical cancer was examined in this current study.
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METHODS According to the pathology report, a total of 162 consecutive patients with cervical cancer were reviewed for their medical history. Among the cases, 57 patients who were not eligible to receive surgical intervention due to advanced clinical stage (greater than IIB) and 5 patients who received preoperative brachytherapy or chemotherapy were excluded; a total of 100 patients with stage IA to IIB were included in this study (Fig. 1). Of the enrolled cases, 24 received robotic radical hysterectomy, 32 received laparoscopic radical hysterectomy, and 44 received abdominal radical hysterectomy. All patients were informed of their options for the types of surgical procedures including robotic surgery, laparoscopic surgery, and laparotomy and the risks and benefits of these procedures according to their surgical history, disease condition, and insurance coverage. The choice of the surgical approach was according to the patient’s will, except for the patients with previous pelvic surgeries (Q2 times) who were suggested to receive robotic or laparotomy procedure. Before surgery, patients underwent 2 days of bowel preparation, and preoperative antibiotics were administered. The surgical procedures performed were radical hysterectomy, bilateral salpingo-oophorectomy, and bilateral pelvic lymph node dissection. All patients received pain control with patientcontrolled analgesia or nonsteroidal anti-inflammatory drugs during postoperative care. The reviewed patient characteristics were age, body mass index (BMI), histology type, and the disease stage according to the International Federation of Gynecology and Obstetrics. The assessed intraoperative parameters included operation time, blood loss, transfusion rate, lymph node yield, adhesion score, and laparotomy conversion rate. Blood loss was defined as the total volume of suctioned fluids.
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To evaluate the severity of pelvic adhesions during the procedure, we adopted the scoring system from the Adhesion Scoring Group.16 The operation time was measured from the time of skin incision until all surgical staging procedures were completed. The postoperative parameters included the postoperative pain score and 24-hour pain score, the duration until the patient resumed a full diet after the operation, and the length of hospital stay. The pain score was self-reported and routinely evaluated for each patient during postoperative care using an adult pain score numerical rating scale, and the data were obtained both postoperatively (on the operation day after the patient was awakened from anesthesia) and at 24 hours after the operation. For reference scoring, score 0 indicates no pain, and score 10 represents the worst pain imaginable. The time duration before full diet resumption was defined as the number of postoperative days until patients can tolerate regular intake of solid food. The length of hospital stay was defined as the number of postoperative days until the patient was discharged. For statistical analysis, all obtained data were analyzed using SPSS statistics (version 21.0, IBM). The mean value, SD, median, and range of each perioperative parameter were reported. The statistical analysis was performed with 1-way ANOVA, Tukey HSD post hoc analysis, or W2 analysis; a p G .05 was considered statistically significant between the groups.
RESULTS According to the inclusion criteria, 100 women were included in the current study. Among the participants, 24 received robotic radical hysterectomy, 32 received laparoscopic radical hysterectomy, and 44 received abdominal radical hysterectomy. As shown in Figure 1, only patients who
FIGURE 1. Inclusion flowchart of all enrolled patients.
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received surgical intervention, with clinical stage IA to IIB, and without preoperative brachytherapy or chemotherapy were included. Patients with a clinical stage greater than IIB were excluded and defined as patients who were not eligible to receive surgical intervention. To avoid the bias caused by case selection, the baseline characteristics of all enrolled patients were examined. Table 1 lists the baseline characteristics of the enrolled patients. The mean (SD) ages were 51.9 (11.3) (laparotomy group), 51.2 (11.9) (laparoscopic group), and 53.7 (15.3) (robotic group), demonstrating no significant difference among the groups. The mean (SD) BMIs were 24.9 (4.6) kg/m2 (laparotomy group), 23.2 (3.4) kg/m2 (laparoscopic group), and 24.4 (4.9) kg/m2 (robotic group), also demonstrating no significant difference among the groups. The numbers of cases with positive lymph node finding were reported as 20.5% (laparotomy group), 9.4% (laparoscopic group), and 12.5% (robotic group). The percentage of each FIGO stage and the histology types of the disease were presented as well (Table 1). The percentage of stage I and II cases, along with the case number with positive lymph nodes, was found to be not significant between the groups, indicating that the study population from each surgical group was comparable. Table 2 lists the intraoperative parameters. The robotic group showed a higher mean adhesion score than did the other groups, although the differences were not significant among the groups. No significant differences were determined in the mean number of pelvic lymph nodes retrieved between the groups. However, the operation time was significantly reduced in the robotic group (192.3 [51.2] minutes) compared
Robotic Surgery for Cervical Cancer
with the laparoscopic group (292.8 [65.2] minutes) and the laparotomy group (302.9 [76.4] minutes). The volume of blood loss during the operation was also significantly decreased in the robotic (116.7 [107.0] mL) and laparoscopic (225.0 [164.1] mL) groups compared with the laparotomy group (1139.0 [656.8] mL). Correspondingly, the transfusion rates of the robotic group (8.3%) and the laparoscopic group (25.0%) were much lower than the laparotomy group (75.0%). Of the patients in the laparoscopic group, 3.0% (1/33) underwent conversion from laparoscopy to laparotomy; none of the patients in the robotic group were converted. Table 2 also lists the postoperative evaluation factors. The robotic group showed a significantly lower postoperative pain score (2.8 [1.4]) than did the laparoscopic (4.5 [2.3]) or laparotomy (5.6 [2.3]) group. The 24-hour pain score of the robotic group was also decreased (2.0 [0.9]) compared with the laparoscopic group (3.7 [2.4]) or the laparotomy group (4.6 [2.0]). Moreover, compared with the laparotomy group (3.4 [1.7] days), the laparoscopic (2.1 [0.9] days) and robotic (1.9 [0.7] days) groups showed significantly reduced amount of time before patients resumed a full diet after surgery. The duration of the hospital stay was also significantly decreased in the robotic group (4.6 [2.6] days) compared with the laparoscopic (9.0 [2.7] days) and laparotomy (11.2 [3.3] days) groups. The complication rates were reported in Table 3. For perioperative complications, 4 patients (2 patients with ureter laceration, 1 patient with iliac vein rupture, and 1 patient with postoperative wound infection) were examined in the laparotomy group. A total of 3 cases (1 case of bladder
TABLE 1. Baseline characteristics of enrolled patients
Age, y Mean (SD) Median Range BMI, kg/m2 Mean (SD) Median Range Stage, % (n) IA to IB IIA to IIB No. cases with positive lymph nodes, % (n) Histology, % (n) Squamous Adenocarcinoma Other
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
51.9 (11.3) 50.0 28Y80
51.2 (11.9) 50.0 32Y83
53.7 (15.3) 50.5 29Y89
0.83
24.9 (4.6) 24.9 11.9Y37.5
23.2 (3.4) 22.5 17.2Y31.3
24.4 (4.9) 23.1 17.9Y38.0
0.15
77.3 (34/44) 22.7 (10/44) 20.5 (9/44)
84.4 (27/32) 15.6 (5/32) 9.4 (3/32)
75.0 (18/24) 25.0 (6/24) 12.5 (3/24)
0.75 0.12 0.07
75.0 (33/44) 22.7 (10/44) 2.3 (1/44)
81.3 (26/32) 15.6 (5/32) 3.1 (1/32)
54.2 (13/24) 37.5 (9/24) 8.3 (2/24)
0.06 G0.05 0.09
P
Baseline characteristics of enrolled patients were summarized. Data were presented as mean (SD) or percentage (case number). The median and range of each data set were listed as well. The statistical analysis was performed with 1-way ANOVA and Turkey HSD post hoc analysis or W2 analysis. n, number of cases.
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TABLE 2. Intraoperative and postoperative parameters in the laparotomy group, laparoscopic group, and robotic group
Adhesion Score Mean (SD) Median Range Lymph node yield Mean (SD) Median Range Operation time, min Mean (SD) Median Range Blood loss, mL Mean (SD) Median Range Transfusion rate, % (n) Conversion rate Pain score (postoperative) Mean (SD) Median Range Pain score (24 hrs) Mean (SD) Median Range Receiving full diet, d Mean (SD) Median Range Hospital stay, d Mean (SD) Median Range
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
0.7 (1.6) 0 0Y5
0.9 (1.9) 0 0Y5
27.8 (11.0) 25 10Y49
Post Hoc Analysis
P
1.6 (2.2) 0 0Y6
LAPA = LPS = ROBO
0.311
29.7 (15.4) 26 7Y66
29.0 (10.9) 27 13Y60
LAPA = LPS = ROBO
0.816
302.9 (76.4) 298 193Y540
292.8 (65.2) 292.5 136Y435
192.3 (51.2) 192.5 88Y270
LAPA = LPS 9 ROBO
G0.05
1139.0 (656.8) 1080 100Y3000 75.0 (33/44) V
225.0 (164.1) 150 50Y750 25.0 (8/32) 3.0 (1/33)
116.7 (107.0) 75 50Y500 8.3 (2/24) 0 (0/24)
LAPA 9 LPS = ROBO
G0.05
V V
G0.05 V
5.6 (2.3) 6 2Y10
4.5 (2.3) 5 0Y8
2.8 (1.4) 3 0Y5
LAPA = LPS 9 ROBO
G0.05
4.6 (2.0) 5 2Y8
3.7 (2.4) 3 0Y8
2.0 (0.9) 2 0Y4
LAPA = LPS 9 ROBO
G0.05
3.4 (1.7) 3 1Y11
2.1 (0.9) 2 1Y4
1.9 (0.7) 2 1Y3
LAPA 9 LPS = ROBO
G0.05
11.2 (3.3) 11 5Y21
9.0 (2.7) 10 4Y15
4.6 (2.6) 4 1Y12
LAPA 9 LPS 9 ROBO
G0.05
Intraoperative and postoperative parameters for each surgical group were listed. Data were presented as mean (SD) or percentage (case number). The median and range of each data set were listed as well. The statistical analysis was performed with 1-way ANOVA and Turkey HSD post hoc analysis or W2 analysis. LAPA, laparotomy group; LPS, laparoscopic group; n, number of cases; ROBO, robotic group.
perforation, 1 case of postoperative ileus, and 1 case of postoperative pelvic infection) were reported in the laparoscopic group. In the robotic group, only 1 patient with postoperative pelvic infection was examined. The overall complication rates were 9.1% for the laparotomy group, 9.4% for the laparoscopic group, and 4.2% for the robotic group. No significant differences were found between the groups.
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Table 4 demonstrated the follow-up of the patients of each surgical group. The mean (SD) follow-up times were 37.1 (23.6) months for the laparotomy group, 34.6 (25.4) months for the laparoscopic group, and 13.9 (7.4) months for the robotic group. The overall survival was not evaluated because of the short follow-up interval. To determine the disease-free interval (DFI) and DFS at 13.9 months, the * 2014 IGCS and ESGO
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Robotic Surgery for Cervical Cancer
TABLE 3. Perioperative complications in the laparotomy group, laparoscopic group, and robotic group Complications Bladder perforation Ureter laceration Iliac vein rupture Postoperative ileus Postoperative pelvic infection Postoperative wound infection Total, % (n)
Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
Significance
V 2 1 V V 1 9.1 (4/44)
1 V V 1 1 V 9.4 (3/32)
V V V V 1 V 4.2 (1/24)
0.26
Perioperative complications in the laparotomy, laparoscopic, and robotic groups were reported. Data were presented as percentage (case number). The statistical analysis was performed with Pearson W2 analysis. n, number of cases.
events were defined as recurrence or progression of the disease within the observation interval. In the laparotomy group, a DFS of 90.9% was reported, and the DFI was 13.6 (0.2) months (95% confidence interval [CI], 13.2Y14.1). In the laparoscopic group, a DFS of 90.6% was examined; the DFI was 13.5 (0.3) months (95% CI, 12.9Y14.1). As for the robotic group, a DFS of 95.8% was reported, and the DFI was 13.9 (0.0) (95% CI, 13.8Y13.9). The overall comparison analyses revealed no significant difference between the groups in DFI and DFS.
DISCUSSION For the management of cervical cancer, Tinelli et al3 showed that no significant difference was found between robotic and laparoscopic approaches in blood loss, hospital stay, complications, or recurrence rates. Besides, the operation time for robotic surgery was longer than that of the laparoscopic approach.3 On the other hand, Soliman et al10 reported that robotic surgery is associated with decreased blood loss and shortened hospital stay; however, both the robotic and laparoscopic approaches showed a longer operation time than did the laparotomy. Geetha and Nair9 further demonstrated that blood loss and transfusion rates were lower in either robotic or laparoscopic surgery as compared with laparotomy; length of hospital
stay of the robotic group was also shorter than that of the other 2 groups. This study corresponds with our results showing that the robotic approach is associated with decreased blood loss, low transfusion rate, and shortened hospital stay. However, it also showed an inconsistency with our data in mean operation time. From our study, the operation time of robotic surgery (192.3 [51.2] minutes) was significantly shorter than that of laparoscopy (292.8 [65.2] minutes) or laparotomy (302.9 [76.4] minutes) (Table 2). Robotic surgery has been demonstrated to have a relatively shorter learning curve and lower proficiency plateau than the conventional approaches.17 A significant reduction in operative time, blood loss, and complication rates in the latter phase of the learning curvewas noted.18 By our data, it is suggested that, with a proper caseload and training of the surgical team, a significantly better short-term operative parameters for the robotic approach could be achieved. The robotic group was also found to associate with a shortened hospital stay than the other 2 groups (4.6 [2.6] days for the robotic group, 9.0 [2.7] days for the laparoscopic group, and 11.2 [3.3] days for the laparotomy group). However, a prolonged postoperative hospital stay from each group was also noticed in our data, which is longer than that from the other reports in average. A speculation is that the inconsistency in the mean length of hospital stay might be due to the societal difference between Taiwan and other countries. With the coverage of subsidies from national health insurance in
TABLE 4. Follow-up of enrolled patients of various surgical groups Laparotomy Group, n = 44
Laparoscopic Group, n = 32
Robotic Group, n = 24
P*
37.1 (23.6) 13.6 (0.2) (95% CI, 13.2Y14.1) 90.9 (40/44)
34.6 (25.4) 13.5 (0.3) (95% CI, 12.9Y14.1) 90.6 (29/32)
13.9 (7.4) 13.9 (0.0) (95% CI, 13.8Y13.9) 95.8 (23/24)
V 0.9* 0.52*
Follow-up, mo DFI, mo† DFS, %†
Survival analysis of each surgical group was presented. Data were presented as mean (SD) or percentage (case number). *The statistical analysis was performed with W2 analysis. †DFI and DFS at 13.9 months. n, number of cases.
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Taiwan, cancer patients tend to extend their hospital stay for longer postoperative care. Pelvic lymph node dissection is considered as a critical step in cervical cancer management.19Y24 Robotic surgery has been suggested to facilitate lymph node dissection in various cancer management procedures.12,25,26 Nonetheless, compared with laparoscopy, robotic surgery was associated with only comparable lymph node yields and similar overall survival rates.8,27 To evaluate the performance for lymphadenectomy by robotic approach, we compared the lymph node yields from each surgical group. Corresponding with the previous reports, our data suggested that the total lymph node yield of the robotic approach (29.0 [10.9]) was comparable with that of the laparoscopic (29.7 [15.4]) or laparotomy (27.8 [11.0]) approach (Table 2). A low complication rate of 4.2% was reported for the robotic group, compared with the laparoscopic (9.4%) or laparotomy (9.1%) group; however, no significant difference was found between the groups (Table 3). These data partially correspond with the report of Geetha and Nair,9 demonstrating that robotic surgery was associated with a lower complication rate whereas the numbers of lymph node retrieval among the groups were similar. Interestingly, the robotic group showed a higher mean (SD) adhesion score (1.6 [2.2]) than did the laparoscopic (0.9 [1.9]) or laparotomy (0.8 [1.6]) groups, yet the differences were nonsignificant (Table 2). In contrast, the robotic group exhibited a relatively lower laparotomy conversion rate (0%) than did the laparoscopy group (3.3%) (Table 2). These outcomes imply that the robotic approach may achieve comparable surgical outcomes with laparoscopy or laparotomy, even with complicated surgical conditions such as pelvic adhesions. It is then speculated that, under similar circumstances, the flexibility of the robotic surgery may contribute to its short-term surgical performance and lower the conversion rate to laparotomy. El Hachem et al28 demonstrate that robotic surgery is equivalent to conventional laparoscopy in subjective and objective measures of postoperative pain during laparoscopic gynecologic procedures. On the contrary, for cervical cancer management, Soliman et al29 reported that significantly less analgesics were required for the robotic group than the laparoscopic group. By our data, reduced postoperative and 24-hour pain scores were examined in the robotic group (Table 2). These results suggest that the robotic approach was associated with a lower postoperative pain. Besides, the outcomes from our study indicated that the robotic group was associated with a significantly shortened hospital stay, which corresponds to the results from Geetha and Soliman.9Y10 Moreover, patients in the robotic and laparoscopic groups resumed a full diet sooner after surgery than did the laparotomy group (Table 2). These results indicated that the robotic approach is associated with favorable perioperative parameters, significantly improving the short-term surgical outcomes of cervical cancer patients. In DFS, the DFI and DFS of each surgical group were analyzed (Table 4). The robotic group showed a similar DFI and DFS to the other 2 groups without significant difference. However, because of the restriction of the retrospective design of this study, the observation period of the robotic group was set from 2011 to 2013. In contrast, the
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observation period for the laparoscopic and laparotomy groups was from 2005 to 2013. To avoid a possible bias due to the short observation period, an overall survival analysis was not performed. An additional follow-up is still needed to examine the long-term survival outcomes. Wright et al30 compared robotic hysterectomy and laparoscopic hysterectomy during a 3-year period and found that robotic surgery showed no significant clinical advantage than laparoscopy for treating benign gynecologic conditions. In contrast, another study from the same research group examined the effectiveness of robotic procedures in 1894 cases of cervical cancer patients.11 In their study, both the robotic group and the laparoscopic group had lower transfusion requirements and shorter hospital stays than the laparotomy group. Interestingly, the laparoscopic group was associated with higher costs than the abdominal group, as the cost of robotic group was not statistically different from the abdominal group. The outcomes implied that, although not significant in treating patients with benign gynecologic condition, robotic surgery still showed certain clinical benefits in managing gynecologic cancer patients. Our findings corresponded with the previous reports and further demonstrated that robotic surgery was associated with favorable shortterm outcomes in treating cervical cancer patients compared with the conventional means. The limitation of this current study is that the observation period is short and a larger randomized controlled trial is required to examine the long-term survival.31 Another limitation is that the cohort of patients was not unselected cases, whereas the surgeon made suggestions on the surgical approach and the patients did selfselection to undergo robotic, laparoscopic, or laparotomy procedure. In conclusion, we suggest that robotic surgery is a feasible and potentially optimal option for the management of stage IA to IIB cervical cancer.
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