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Chong: Robotic radical hysterectomy for early-stage cervical cancer: A systematic literature review

Abstract

Robotic technology has recently come into widespread use to overcome the limitations of laparoscopic radical hysterectomy in the treatment of early-stage cervical cancer. Most comparative studies showed that blood loss and hospital stays for patients undergoing minimally invasive surgery, including robotic procedures, were superior compared to open surgery. Moreover, the survival outcomes of robotic radical hysterectomy were not inferior to open radical hysterectomy. Unexpectedly, the Laparoscopic Approach to Cervical Cancer (LACC) trial, a randomized, open-label, noninferiority study that compared minimally invasive radical hysterectomy with open radical hysterectomy, revealed that minimally invasive surgery was associated with a higher risk of recurrence and death compared with open surgery. Strict guidelines for robotic radical hysterectomy for the treatment of early-stage cervical cancer should be established in accordance with objective Korean data. In addition, it is recommended that further studies should be performed on how to avoid the use of uterine manipulators and the dissemination of cancer cells by ensuring a more effective vaginal closure using a standardized approach.

INTRODUCTION

Radical hysterectomy (RH) is a well-established treatment modality of early-stage cervical cancer. RH is defined as the en bloc removal of the uterus and cervix with the surrounding parametrial tissue and upper vagina. Since the introduction of conventional laparoscopy, improvements in gynecologic surgery have been notable. However, laparoscopic RH (LRH) remains a rather unpopular choice among gynecologic oncologists because of the increased operative time and the steep learning curve required for competency [1]. Robotic technology has recently come into widespread use to overcome the limitations of laparoscopic surgery [2]. This is because robotic surgery provides more surgical options, such as nerve-sparing technique, due to its superior visualization (3-dimensional imaging of the operative field), mechanical improvement (seven degrees of instrument mobility inside the body) and stabilization/tremor filtration of the instrument within the surgical field [2].
Unexpectedly, the Laparoscopic Approach to Cervical Cancer (LACC) trial, a randomized, open-label, noninferiority study that compared minimally invasive RH with open RH (ORH), found that minimally invasive surgery (MIS) was associated with a higher risk of recurrence and death compared with open surgery. Female patients randomized to the minimally invasive surgery arm experienced an almost four times greater risk of recurrence and six times greater risk of death compared with female patients that were randomized to laparotomy [3]. In a statement released after the publication of the LACC trial, the Society of Gynecologic Oncology encouraged surgeons to discuss these data with patients undergoing surgery for cervical cancer [4], and the National Comprehensive Cancer Network cervical cancer guidelines were revised accordingly to define the open abdominal approach as the “standard and recommended approach to RH” [5].
Consequently, this study performed a systemic literature review to appraise and synthesize the available real-world evidence on robotic RH (RRH). Moreover, we compared the risk of recurrence and death between patients who underwent MIS vs. ORH for early-stage cervical cancer.

CASE SERIES OF RRH

After Marchal et al. [6] performed RRH in 2005, several case series of RRH were published (Table 1) [7-10]. In Korea, Kim et al. [7] for the first time reported 10 cases of RRH and concluded that RRH for selected patients with IB1 cervical cancer is feasible, promising and related with a low morbidity (Table 1).

MIS (ROBOT AND LAPAROSCOPY) VS. OPEN

Most initial comparative studies between MIS and ORH focused on the respective surgical outcomes [11-14]. Most comparative studies showed that blood loss and hospital stays for the MIS group were superior compared to the open group [11-17]. Furthermore, previous retrospective comparative studies revealed that the survival outcomes of MIS were comparable to the survival outcomes of open surgery [15-17]. In the LACC trial, however, MIS was associated with a lower range of disease-free survival (DFS; 3-year rate, 91.2% vs. 97.1%; hazard ration [HR], 3.74; 95% confidence interval [CI], 1.63–8.58) and overall survival (OS; 3-year rate, 93.8% vs. 99.0%; HR, 6.00; 95% CI, 1.77–20.30) [3]. Following the LACC trial, several retrospective comparative studies reported on the survival outcomes of MIS and open surgery [18-20]. Cusimano et al. [18] showed that MIS was associated with increased rates of death (HR, 2.20; 95% CI, 1.15–4.19) and recurrence (HR, 1.97; 95% CI, 1.10–3.50) after adjusting for individual patients’ factors and surgeon volume. Moreover, an international European cohort observation study (the SUCCOR study) demonstrated that the risk of recurrence for patients who underwent MIS was twice as high compared to the open surgery group (HR, 2.07; 95% CI, 1.35–3.15; P=0.001). Similarly, the risk of death was 2.42-times higher than in the open surgery group (HR, 2.45; 95% CI, 1.30–4.60, P=0.005) [19]. Finally, Brandt et al. [20] reported that MIS RH did not confer worse oncologic outcomes in a singlecenter retrospective study (Table 2).

ROBOT VS. OPEN SURGERY

Most comparative studies showed that blood loss and hospital stays for the robot group were superior to those of the open group [21-31]. However, the majority of these studies demonstrated that the operative time of ORH was significantly shorter compared to RRH [21,23,26,28,29]. The survival outcomes of RRH and ORH were first reported in 2010, and for a 3-year progression free survival (PFS) were 94% in RRH and 89% in ORH (P=0.27) and the 3-year OS were 94% in RRH and 93% in ORH (P=0.47), respectively [24]. After this study [24], several retrospective comparative studies showed that survival outcomes were similar between the two groups [28,29,31]. However, Wallin et al. [30] used a multivariate regression analysis and demonstrated that RRH was significantly more associated with tumor recurrence (HR, 2.13; 95% CI, 1.06–4.26; P<0.05). Moreover, abdominal radical hysterectomy had a greater PFS advantage over RRH for tumors ≥2 cm (HR, 0.31; 95% CI, 0.11–0.90; P=0.04) [32]. Furthermore, recent retrospective studies have also reported poor survival outcomes in RRH compared to ORH after propensity score matching (Table 3) [33,34].

ROBOT VS. LAPAROSCOPY

Surgical outcomes, such as the operative time and comlication rate were different for different studies [35-45]. However, most studies reported that blood loss of RRH was superior to that of LRH [35,37-39,45]. Finally, several retrospective studies have reported similar survival outcomes between the two groups (Table 4) [36-38,41,42,44,45].

ROBOTIC SINGLE-SITE RH

Sinno and Tanner [46] reported the first surgical film of robotic single-site RH. Recently, Jang et al. [47] compared the surgical outcomes of robotic single-site and multiport RH. Hospital stay and total hospital cost for single-site were significantly shorter and lower, respectively, compared to multiport surgery (P<0.01) [47].

NATIONWIDE POPULATION-BASED STUDIES

In an epidemiologic study performed in the USA, MIS was associated with shorter OS rates compared to open surgery (HR, 1.65; 95% CI, 1.22–2.22; P=0.002) [48]. In contrast, nationwide population-based studies in Scandinavia, reported different outcomes [49,50]. For instance, a Swedish nationwide population-based cohort study showed that the 5-year OS was 94% and 92%, and DFS was 88% and 84% for the robotic and open cohorts, respectively [49]. Moreover, the 5-year OS after propensity score matching was 92% for both cohorts (HR, 1.003; 95% CI, 0.5–2.01; P=0.99) [49]. In a Danish nationwide population- based cohort study, adoption of RRH for early-stage cervical cancer was not associated with either an increased risk of recurrence or reduction in survival outcomes [50].

ISSUES OF TUMOR SPILLAGE IN MIS

In the LACC trials, the potential reasons for the inferior oncologic outcomes in the MIS included the routine use of uterine manipulator, effect of the insufflation gas (CO2) on tumor-cell growth and that spread might increase the propensity for tumor spillage [3]. In the SUCCOR study, the use of uterine manipulator during MIS was associated with worse 4.5-year DFS (82% vs. 93%; HR, 3.48; 95% CI, 1.17–9.48, P=0.028) and 4.5-year OS (88% vs. 96%; P=0.016) [19]. Klapdor et al. [51] evaluated peritoneal contamination with indocyanine green stained cervical secretion as surrogate for potential cervical cancer cell dissemination during colpotomy. Peritoneal contamination was detected in 75% (9/12) patients during laparoscopic hysterectomy and uterine manipulator contamination was detected in 60% [51]. However, Nica et al. [52], reported that the use of intrauterine manipulator in patients with early cervical cancer who underwent MIS was not an independent factor with a significant rate of recurrence after controlling for adverse pathological factors (HR, 0.4; 95% CI, 0.2–1.0; P=0.05). Kong et al. [53] demonstrated that the rate of disease recurrence was higher in the intracorporeal colpotomy group compared to the vaginal colpotomy group (16% vs. 5%), and among patients with recurrence in the intracorporeal group, 62% had intraperitoneal spread or carcinomatosis. The author concluded that exposure of cervical cancer to circulating CO2 may result in tumor spillage into the peritoneal cavity [53]. Furthermore, other previous studies also presented intraperitoneal recurrences only in robot or MIS during RH [33,42].

UPCOMING TRIALS

Two novel noninferiority randomized controlled trials (RCTs) have been launched in terms of evaluating early-stage cervical cancer following the publication of the LACC trial results. The first one is a multicenter Chinese trial that compares RRH or LRH vs. ORH with DFS at 5 years as its primary objective, which has a planned sample size of 1,488 patients from 28 participating centers with an individual surgeon case volume [54]. The second one is performed in an international multicenter RCT (Robot-assisted Approach to Cervical Cancer [RACC] trial), and compares RRH vs. ORH with the 5-year DFS as its primary end-point and a planned sample size of 800 patients [55].

CONCLUSION

The authors of the LACC study and the US Cancer Resist Evaluation stated that MIS RH was associated with a higher rate of recurrence and poorer OS compared to ORH. Previous meta-analysis based on retrospective studies, showed that open surgery had no significant superiority.
The results were not interpreted as the end of MIS in terms of treating cervical cancer; instead, it was recommended that studies should be performed on how to avoid the use of uterine manipulators and the dissemination of cancer cells by ensuring a more effective vaginal closure using a standardized approach.
In agreement with previous nationwide population-based studies, our findings underline a disagreement on survival outcomes according to the specific conditions and parameters of each nation. Therefore, it is necessary to perform a Korean nationwide population-based study that will focus on the respective oncologic outcomes. Furthermore, strict guidelines for MIS in the treatment of early-stage cervical cancer should be implemented which will be consistent with objective data from the Korean population.

Notes

Conflict of interest

No potential conflict of interest relevant to this article was reported.

Table 1.
Case series of robotic radical hysterectomy
Year Nation Number Design Stage Operative time (minutes) Blood loss (mL) Hospital stays (days) Lymph Complication (%) Survivals Reference No.
2008 Korea 10 Single IA2-IB1 207 355 7.9 27.6 0.0 NA [7]
2008 USA 20 Singe IB1-IIA 309 300 1 18 10.0 2-year DFS 90% [8]
2009 Sweden 80 Single IA1-IIA 262 150 NA 26 41.0 NA [9]
2009 USA 42 Multi IA1-IB2 215 50 1 25 16.8 NA [10]

NA, not available; DFS, disease-free survival.

Table 2.
Comparative studies between minimally invasive and open surgery
Year Nation Design Number robot vs. LSC vs. open Period Stage Operative time Blood loss LN Stay Cx Recurrence Death Reference No.
2008 USA Retrospective, single 27 vs. 31 vs. 35 2003 to 2006 IA2-IB2 Open robot MIS ND MIS ND NA NA [11]
1993 to 2006
2009 USA Retrospective, single 32 vs. 17 vs. 14 2006 to 2008 IA2-IB2 ND MIS Robot MIS ND NA NA [12]
2002 to 2006
2011 USA, Brazil Prospective, multi 34 vs. 31 vs. 30 2007 to 2010 IA2-IIA Open MIS NA MIS ND NA NA [13]
2011 Norway Prospective, single 35 vs. 7 vs. 26 2005 to 2009 IA1-IB1 Open Robot Open Robot NA 5 recurrence in only robot NA [14]
2004 to 2005
2014 Taiwan Retrospective, single 32 vs. 24 vs. 44 NA IA-IIB Robot MIS ND MIS ND 95.8% vs. 90.6% vs. 90.9% NA [15]
2016 USA Retrospective, single 58 vs. 49 vs. 39 2009 to 2013 IA2-IIB LSC Robot NA Robot Robot 89.7% vs. 89.8% vs. 84.6% 96.6% vs. 95.9% vs. 92.3% [16]
2018 Italy Retrospective, multi 88 vs. 152 vs. 101 2001 to 2016 IB1 ND MIS Open MIS ND 89.5% vs. 87.2% vs. 91.3% (MIS = open) 88.8% vs. 89.7% vs. 88.7% (MIS = open) [17]
2018 USA et al. Prospective, RCT 319 (88.4% LSC) vs. 485 2008 to 2017 IA1-IB1 NA NA NA NA ND 3 years; 91.2% vs. 97.1% (HR, 3.74) 3 years; 93.8% vs. 99.0% (HR, 6.00) [3]
2019 Canada Retrospective, multi 473 (89.6% LSC) vs. 485 2006 to 2017 IA-II NA NA NA Robot ND 16.2% vs. 8.4% (P=0.008) 12.5% vs. 5.4% (P=0.019) [18]
2020 EU Retrospective, multi 291 (78.5% LSC) vs. 402 2013 to 2014 IB1 NA NA NA NA NA 4.5 years; 79% vs. 89% (P=0.003) 4.5 years; 89% vs. 97% (P=0.003) [19]
2020 USA Retrospective, single 117 (90.6% Robot) vs. 79 2007 to 2017 IA1-IB1 NA NA NA NA MSI 5 years; 87.0% vs. 86.6% (P=0.93) 5 years; 96.5% vs. 87.4% (P=0.15) [20]

LN, lymph node; Cx, complication; MIS, minimally invasive surgery; ND, no difference; NA, not available; LSC, laparoscopy; RCT, randomized controlled trial; HR, hazard ratio.

Table 3.
Comparative studies between robot and open surgery
Year Nation Design Number robot vs. open Period Stage Operative time Blood loss LN Stay Cx Recurrence Death Reference No.
2008 USA Retrospective, single 16 vs. 32 2006 to 2007 IA1-IB1 Open Robot ND Robot ND NA NA [21]
2009 USA Prospective, single 51 vs. 49 2005 to 2007 IA1-IIA Robot Robot Robot Robot ND NA NA [22]
2009 Italy Prospective, single 40 vs. 40 2007 to 2009 IA2-IIA Open Robot Open Robot ND NA NA [23]
2010 USA Retrospective, single 63 vs. 64 2005 to 2008 IA1-IIB NA Robot NA Robot ND 3 years; 94% vs. 89% (P=0.27) 3 years; 94% vs. 93% (P=0.47) [24]
1995 to 2007
2010 Korea Prospective, single 32 vs. 32 2005 to 2007 IA2-IIB ND Robot ND Robot ND NA NA [25]
2002 to 2009
2010 Canada Prospective, single 16 vs. 24 2005 to 2007 IA1-IIA Open Robot ND Robot Robot NA NA [26]
2002 to 2009
2010 USA Retrospective, single 15 vs. 30 2007 to 2008 IA2-IB2 ND Robot ND Robot ND NA NA [27]
2016 USA, Norway Retrospective, multi 259 vs. 232 2005 to 2011 IA1-IB2 Open Robot ND Robot Robot 23% vs. 21% (P=1.00) 7% vs. 9% (P=0.48) [28]
2016 EU Retrospective, multi 210 vs. 195 2006 to 2014 IA2-IB2 Open Robot NA Robot ND 5 years; 89% vs. 90% (P=0.917) 5 years; 98% vs. 97% (P=0.626) [29]
2017 Sweden Retrospective, single 149 vs. 155 2009 to 2015 IA1-IB1, IIA1 ND Robot Robot Robot Robot 5 years; 91.1% vs. 95.2% (HR, 2.13; P<0.05) 5 years; 91.1% vs. 92.7% [30]
2017 USA Retrospective, multi 109 vs. 202 2001 to 2012 IA1-IB2 NA Robot Open Robot Robot 3 years; 89.9% vs. 89.1% (P=0.140) 3 years; 97.2% vs. 95% (P=0.960) [31]
2019 USA Retrospective, multi 49 vs. 56 2010 to 2016 IB1 NA NA NA NA ND 24% vs. 14% (P=0.22) ≥2 cm open 14% vs. 5% (P=0.18) ≥2 cm open [32]
2020 USA, China Retrospective, multi 152 vs. 181 2000 to 2017 IA2-IIA Open Robot NA Robot NA 5 years; 91.4% vs. 91.1% (P=0.98) 5 years; 96.7% vs. 96.6% (P=0.98) [33]
IPTW IPTW
5 years; 79% vs. 90.5% (P=0.01) 5 years; 85.8% vs. 95.3% (P<0.01)
2020 China Retrospective, multi 1,048 vs. 9,266 2004 to 2016 IA-IIA2 NA NA NA NA NA 3 years; 91.1% vs. 95.4% (P=0.002) 3 years; 94.4% vs. 97.8% (P=0.002) [34]

LN, lymph node; Cx, complication; ND, no difference; NA, not available; IPTW, inverse probability of weighting using the propensity score.

Table 4.
Comparative studies between robot and laparoscopic surgery
Year Nation Design Number robot vs. LSC Period Stage Operative time Blood loss LN Stay Cx Recurrence Death Reference No.
2007 Norway Retrospective, single 7 vs. 7 2005 to 2006 IA1-IB1 ND Robot ND Robot ND NA NA [35]
2004 to 2005
2011 Italy, USA Retrospective, multi 23 vs. 76 2003 to 2010 IA2-IIA LSC ND ND ND ND 4.3% vs. 5.3% (P>0.05) NA [36]
2014 Korea Retrospective, single 23 vs. 69 2008 to 2013 IA1-IB2 LSC Robot ND ND ND 3 years; 91.3% vs. 89.9% (P=0.778) NA [37]
2014 Korea Retrospective, single 60 vs. 42 2009 to 2013 IA1-IIA1 ND Robot NA ND ND 3 years; 96.4% vs. 91.9% (P=0.482) NA [38]
2017 China Retrospective, single 100 vs. 833 2009 to 2016 IA2-IIA1 Robot Robot ND Robot Robot 0.0% vs. 4.2% (P=0.03) 0.0% vs. 2.9% (P=0.07) [39]
2018 USA Retrospective, single 13 vs. 30 2006 to 2008 IA2-IIA ND ND ND ND ND 0% vs. 0% NA [40]
2000 to 2006
2018 Italy Retrospective, multi 70 vs. 140 2010 to 2016 IA2-IB2 LSC ND ND ND ND 3 years; 88.0% vs. 84.0% (P=0.866) 3 years; 90.8% vs. 94.0% (P=0.924) [41]
2018 Korea Retrospective, multi 65 vs. 60 2008 to 2013 IB1-IIA2 LSC ND ND ND LSC 20% vs. 13.3% (P=0.3212) 9.2% vs. 3.3% (P=0.2762) [42]
2019 Japan Retrospective, single 64 vs. 57 2010 to 2017 IA2-IIB LSC LSC Robot ND ND NA NA [43]
2019 China Retrospective, single 92 vs. 60 2014 to 2017 IA-IIB ND ND Robot ND Robot 81.02% vs. 85.67% (P=0.669) 92.13% vs. 94.45% (P=0.292) [44]
2019 China Retrospective, single 216 vs. 342 2014 to 2018 IA1-IIB Robot Robot ND ND ND 3 years; 89.9% vs. 89.1% (P=0.669) 3 years; 97.2% vs. 95.0% (P=0.292) [45]

LSC, laparoscopy; LN, lymph node; Cx, complication; ND, no difference; NA, not available.

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