Int J Clin Oncol DOI 10.1007/s10147-015-0854-z
REVIEW ARTICLE
Recent advances in robotic surgery for rectal cancer Soichiro Ishihara1 · Kensuke Otani1 · Koji Yasuda1 · Takeshi Nishikawa1 · Junichiro Tanaka1 · Toshiaki Tanaka1 · Tomomichi Kiyomatsu1 · Keisuke Hata1 · Kazushige Kawai1 · Hiroaki Nozawa1 · Shinsuke Kazama1 · Hironori Yamaguchi1 · Eiji Sunami1 · Joji Kitayama1 · Toshiaki Watanabe1
Received: 14 May 2015 / Accepted: 27 May 2015 © Japan Society of Clinical Oncology 2015
Abstract Robotic technology, which has recently been introduced to the field of surgery, is expected to be useful, particularly in treating rectal cancer where precise manipulation is necessary in the confined pelvic cavity. Robotic surgery overcomes the technical drawbacks inherent to laparoscopic surgery for rectal cancer through the use of multi-articulated flexible tools, three-dimensional stable camera platforms, tremor filtering and motion scaling functions, and greater ergonomic and intuitive device manipulation. Assessments of the feasibility and safety of robotic surgery for rectal cancer have reported similar operation times, blood loss during surgery, rates of postoperative morbidity, and circumferential resection margin involvement when compared with laparoscopic surgery. Furthermore, rates of conversion to open surgery are reportedly lower with increased urinary and male sexual functions in the early postoperative period compared with laparoscopic surgery, demonstrating the technical advantages of robotic surgery for rectal cancer. However, long-term outcomes and the cost-effectiveness of robotic surgery for rectal cancer have not been fully evaluated yet; therefore, large-scale clinical studies are required to evaluate the efficacy of this new technology. Keywords Rectal cancer · Robotic surgery · Laparoscopic surgery
* Toshiaki Watanabe [email protected] 1
Department of Surgical Oncology, The University of Tokyo Hospital, 7‑3‑1, Bunkyo‑ku, Hongo, Tokyo 113‑8655, Japan
Introduction The widespread application of total mesorectal excision (TME) for rectal cancer, originally proposed by Heald et al. in 1982, has greatly contributed to reductions in postoperative local recurrence rates, the most important oncological issue related to rectal cancer surgery [1]. TME principally involves sharp dissection and en bloc resection of mesorectal tissue, including the primary lesion and surrounding regional lymph nodes, by exposing precise pelvic anatomy, and the preservation of autonomic nerves to conserve postoperative urinary and sexual function. Recently, laparoscopic surgery was introduced for the treatment of rectal cancer as a minimally invasive alternative to conventional open surgery. Laparoscopic surgery has been shown to have a number of advantages over open surgery for the treatment of colon cancer, including reduced analgesic usage, faster recovery of oral intake, and shorter postoperative hospital stays without compromising long-term oncological outcomes [2–7]. However, in contrast to the case for colon cancer, there is relatively limited evidence regarding the safety and efficacy of laparoscopic surgery for rectal cancer, and some technical and oncological issues have been raised, including high rates of conversion to open surgery and circumferential resection margin (CRM) involvement of the specimen [5]. In laparoscopic surgery, precise manipulation is possible using magnified views of the surgical field; however, major drawbacks that are intrinsic to laparoscopic surgery include straight and inflexible devices, unstable intraoperative views with handheld two-dimensional cameras, and uncomfortable ergonomic positions of surgeons [8, 9]. Robotic technology, which has recently been introduced to the field of surgery, is expected to overcome these issues associated with laparoscopic surgery by using flexible devices with seven degrees of freedom of movement,
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stable three-dimensional camera platforms, more precise surgical manipulation by tremor filtering and motion scaling, and a more intuitive and ergonomic operative environment [8, 9]. In this article, we review recent advances in and future perspectives on robotic surgery for rectal cancer.
The da Vinci Surgical System® The da Vinci Surgical System® (Intuitive Surgical, Sunnyvale, CA, USA) is a robot that is currently available for use in surgical treatment (Fig. 1). The Zeus Surgical System® (Computer Motion, Santa Barbara, CA, USA) is another such robot, albeit one that is not currently available. A prototype da Vinci Surgical System® was developed in the late 1980s and was made commercially available in 1999 after several refinements. Currently, more than 3000 da Vinci Surgical Systems® are in operation worldwide and are
widely used in urological, gynecological, colorectal, cardiovascular, and thoracic surgery.
Surgical outcomes Among the various procedures performed by robotic surgery, the most evident benefits have been reported with robotic prostatectomy, including decreased blood loss during surgery, a lower incidence of perioperative morbidity, shorter hospital stays, reduced autonomic nerve injury, and faster recovery of urinary and male sexual functions [10]. Similar benefits are expected for robotic surgery for the treatment of rectal cancer, as both prostatectomy and rectal cancer surgery involve resection of organs from the confined bony pelvis with preservation of adjacent autonomic nerves (Fig. 2). Operation time
Fig. 1 The da Vinci Surgical System®. a Surgeon console. b Patient cart. Reproduced with permission from [55]
a
Proper rectal fascia
Conflicting results have been reported regarding the operation time of robotic surgery as compared with that of conventional laparoscopic surgery. A number of reports have demonstrated a longer operation time with robotic surgery [9, 11–13], whereas others have reported no difference in operation time between robotic and laparoscopic surgeries [14–18]. Patriti et al. reported a shorter operation time for robotic rectal resection; however, they are minority in this regard [19]. The variation in the reported operation time of robotic surgery for rectal cancer may be due to differences in the use of the robotic system, either “full robotic” surgery or “hybrid” surgery, where laparoscopic and robotic surgery are combined. Furthermore, the use of single or dual docking to the patient cart or the premature use of the procedure before adequate standardization may have impacted the findings of some studies. All published
b Proper rectal fascia
Pelvic floor Fig. 2 Intraoperative views of robotic total mesorectal excision (TME). a, b Robotic systems enable proper dissection in the deep pelvic area that tends to be tangential with laparoscopic surgery by
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virtue of multi-articulated devices with stable three-dimensional views. Reproduced with permission from [55]
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meta-analyses conclude that there is no difference in operation time between robotic and laparoscopic surgeries for rectal cancer [20–23]. Blood loss during surgery The majority of studies reporting blood loss during surgery found no difference between robotic and laparoscopic surgeries for rectal cancer [12, 17, 19, 24]. Popescu et al. demonstrated that the volume of blood loss was smaller for robotic surgery; however, the result of a recent meta-analysis demonstrated that there was no difference in operative blood loss between the two procedures [22]. Conversion to open surgery In the MRC-CLASSIC trial conducted in the UK, a high rate of conversion from laparoscopic to open surgery was reported for rectal cancer [5]. This high conversion rate is believed to reflect the technical difficulties involved in laparoscopic surgery for rectal cancer, due to the inherent problems mentioned above. In cases of laparoscopic surgery for colon cancer, conversion to open surgery has been reported to be associated with postoperative complications and morbidity and reduced survival rates [4, 5]. Therefore, conversion rates are considered an important indicator of the efficacy and oncological safety of minimally invasive surgery. In studies that compare robotic and laparoscopic surgeries, conversion rates to open surgery have been reported to be 0–7 % and 0–22 %, respectively [9, 11, 15–18, 25, 26], with the majority of studies demonstrating lower conversion rates with robotic surgery. In a published meta-analysis, the conversion rate of robotic surgery for rectal cancer was demonstrated to be lower than that of laparoscopic surgery, indicating the technical advantages of robotic surgery for rectal cancer.
Findings in resected specimens CRM, the distal resection margin (DRM), and the number of retrieved lymph nodes are important short-term oncologic markers in rectal cancer surgery, and are considered to be surrogate markers for long-term outcomes. Robotic systems may provide an oncologically safer option for surgery in the confined pelvic cavity because of the intuitive and ergonomically superior manipulation possible with flexible devices. In fact, a number of studies have reported lower rates of CRM involvement [18] and an increased number of retrieved lymph nodes [16, 25] with robotic surgery compared with laparoscopic surgery; however, the majority of studies have reported no difference in CRMand DRM-positive rates and the number of retrieved lymph nodes, and these results have been confirmed by a number of meta-analyses [20–23]. Postoperative recovery A number of studies reported shorter intervals to oral intake and hospital stays with robotic surgery compared with those following laparoscopic surgery [9, 15]; however, meta-analyses have demonstrated no significant difference in either of these measures [20–23]. Therefore, there appears to be no difference in the degree of surgical stress between robotic and laparoscopic surgeries, which is further corroborated by our recent study evaluating surgical stress using immunological parameters [27]. In this study, the expression of HLA-DR by peripheral blood lymphocytes, which is considered a marker of immune competence, was significantly higher in robotic surgery cases than in open surgery cases, and no difference was found from laparoscopic surgery cases, indicating that robotic and laparoscopic surgery for rectal cancer lead to reduced surgical stress compared with open surgery.
Perioperative complications
Postoperative urinary and sexual function
Perioperative complication rates are, in general, an important indicator of the safety of a surgical procedure. Although Baik et al. reported that serious complication rates were significantly lower with robotic surgery (5.4 %) compared with laparoscopic surgery (19.3 %) [15], complication rates did not differ between robotic and laparoscopic surgeries in other reports [9, 11, 14, 16, 19, 25]. The results of meta-analyses have demonstrated that there is no difference in complication rates [20–23]. In particular, anastomotic leakage—the most clinically important complication following rectal cancer surgery—has been reported to occur in 3–14 % of robotic surgery cases and 2–12 % of laparoscopic surgery cases [9, 11–13, 15–18, 24–26], with no significant difference between these rates.
Urinary and sexual dysfunction due to autonomic nerve injury occasionally occurs following TME for rectal cancer, and these issues may substantially impair the quality of life of patients. Although laparoscopic surgery is considered a minimally invasive surgery, a study has reported that male sexual function following laparoscopic surgery was poorer than that following open surgery [28], indicating the technical difficulty of laparoscopic surgery for rectal cancer. Kim et al. compared postoperative urinary and male sexual function following robotic and laparoscopic surgery using uroflowmetry and questionnaires [29] and found that, in the early postoperative period, these functions were better after robotic surgery than after laparoscopic surgery. Park et al. evaluated these functions using questionnaires [30]
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and also demonstrated that male sexual function was better following robotic surgery in the early postoperative period, although no difference in urinary function was observed. Postoperative function following robotic surgery is yet to be fully evaluated. Long‑term outcomes Robotic surgery for rectal cancer has only recently been introduced, so there have been only a few reports evaluating long-term oncological outcomes. Park et al. evaluated oncological outcomes of patients with rectal cancer treated with robotic or laparoscopic surgery who were followed up for a median period of 58 months, and demonstrated that overall and disease-free survival did not significantly differ between the treatment groups [31]. Local recurrence rates were reported as 2.3 % in the robotic surgery group and 1.2 % in the laparoscopic surgery group, with no significant difference found. However, as only the results of nonrandomized studies are currently available, future randomized controlled trials are required to evaluate long-term outcomes following robotic TME that may potentially be optimized by the da Vinci system.
Learning curves Analysis of the learning process is important when introducing a new technique into clinical practice, not only for the assessment of safety and efficacy but also to encourage wide acceptance of the technique. To evaluate the learning process, learning curve analyses of surgical approaches for rectal cancer using the cumulative sum (CUSUM) methodology have recently been reported [32–34]. In the case of laparoscopic surgery, the learning curve for rectal cancer surgery has been demonstrated to be relatively long and gradual compared with other widely performed procedures such as laparoscopic cholecystectomy, and the number of cases that are required to achieve the learning curve is estimated to be between 60 and 80 [35]—greater than the estimated 50–60 cases required for laparoscopic colonic resection [36]. When considering the advantages of the robotic system, the number of cases necessary to achieve the learning curve for robotic rectal cancer surgery is expected to be smaller than that for laparoscopic rectal cancer surgery. In learning curve analyses for robotic rectal cancer surgery using the CUSUM technique, it has been shown that there are multiple phases of the learning process [32–34]. Jimenez-Rodriguez et al. reported that the operative duration significantly decreased after 21–23 cases, eventually reaching a plateau when the learning curve was achieved [34]. Kim et al. reported that the first plateau in the operation time occurred after 33 cases; therefore, the first 32 cases
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had a greater impact on the learning process for robotic TME [33]. From these analyses, fewer cases appear to be required to achieve the learning curve of robotic rectal cancer surgery than that of laparoscopic rectal cancer surgery. Robotic surgery is considered to be more intuitive; i.e., the robotic system simulates the manipulation of tools and techniques used for open surgery. Therefore, the robotic interface is expected to allow surgeons who are not experienced in laparoscopic surgery to perform minimally invasive surgery for rectal cancer, as has already been demonstrated for prostatectomy [37]. Kim et al. analyzed the leaning curve of an open surgeon with limited laparoscopy experience and demonstrated that operation times significantly decreased after as few as 20 cases without compromising surgical and oncological outcomes [38]. However, though laparoscopic experience is desirable, the degree of impact of experience or inexperience in laparoscopic surgery on the ability to master robotic surgery for rectal cancer has yet to be clarified.
Cost issues with robotic surgery Robotic surgery for rectal cancer is apparently more expensive than open or laparoscopic surgery because of the high cost of the instruments used and the robotic system itself. In Korea, one of the most advanced countries in the use of robotic surgery, the total cost of robotic surgery for rectal cancer is estimated as $14,000, which is 1.5 times as expensive as the cost of laparoscopic surgery, $9000 [9]. Bryn et al. reported that the cost of robotic surgery has gradually decreased as institutional experience has increased [39]. Furthermore, instruments and the robotic system are expected to become increasingly sophisticated and rationalized, resulting in future decreases in the cost of robotic surgery. However, superior surgical outcomes with robotic surgery in addition to an equal or comparable cost to that of conventional laparoscopic surgery are required before wide acceptance of this new technique becomes likely.
Clinical trials To date, only one randomized controlled trial (RCT) has compared the outcomes of robotic and laparoscopic surgery for rectal cancer [19]. This study reported decreased operation times, lower conversion rates, comparable postoperative morbidities, and overall and disease-free survival rates in the robotic surgery group, concluding that robotic surgery for rectal cancer is both safe and effective. However, the number of cases examined was very small (29 cases for robotic surgery and 37 cases for laparoscopic surgery), and the follow-up period for robotic surgery
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cases was short (mean 18.7 months). Therefore, the results of this study must be interpreted with caution. Recently, an international RCT conducted by Leeds University in the UK (the ROLARR trial) was initiated [8]. In this trial, 200 cases will be enrolled into a robotic surgery group and another 200 into a laparoscopic surgery group (giving a total of 400 cases) to assess the following end-points: rate of conversion to open surgery; CRM positive rate; local recurrence; disease-free survival; overall survival; morbidity and mortality rates; postoperative quality of life; and cost-effectiveness. The results of this trial are eagerly awaited.
Application of robotic techniques to advanced procedures Intersphincteric resection Intersphincteric resection (ISR) of rectal cancer was first reported by Schiessel et al. in 1994 and is now performed as the frontline sphincter-preserving surgery in very lowlying rectal cancer [40]. When performing ISR, manipulation in deeper and narrower areas of the pelvic cavity is required; therefore, robotic techniques are expected to demonstrate their full potential in this setting (Fig. 3). Park et al. reported that robotic ISR was oncologically safe, with faster recovery of male sexual function noted in cases treated with robotic surgery compared with laparoscopic ISR [41]. Furthermore, they reported that transabdominal ISR, in which the intersphincteric dissection transects the distal margin within the pelvic cavity, could be performed more frequently with robotic assistance than with laparoscopic surgery [41], indicating the technical aptitude of robotic systems in performing ISR.
Distal resecon margin Rectum Fig. 3 Robotic intersphincteric resection of rectal cancer. Robotic systems enable precise transection of distal resection margins in the anal canal. Reproduced with permission from [55]
Lateral pelvic lymph node dissection The efficacy of lateral pelvic lymph node dissection for rectal cancer outside the TME plane is yet to determined, particularly in cases where lateral pelvic lymph nodes are not clinically involved (termed “prophylactic dissection”) or after preoperative chemoradiotherapy [42–44]. In Japan, lateral pelvic lymph node dissection is regarded as a standard procedure for T3–T4 low rectal cancer as a result of the findings of a retrospective analysis [45–47]. Lateral pelvic lymph node dissection is performed in the deep region of the pelvic cavity, where the magnified view obtained in laparoscopic surgery is considered to be a significant advantage of laparoscopic lateral pelvic lymph node dissection [48]. However, manipulation during lateral pelvic lymph node dissection tends to be tangential and uncomfortable for surgeons using straight laparoscopic surgical instruments. Conversely, lateral pelvic lymph node dissection with robotic surgery using multi-articulated flexible devices appears to decrease surgeon stress (Fig. 4), with the efficacy of this approach being reported by several advanced institutions [49, 50]. Transanal robotic surgery The use of a transanal approach in the surgical treatment of rectal cancer appears to be reasonable because rectal cancer is located near the anus. Retrieval of resected specimens from the anus, where possible, is considered to decrease rectal cancer surgery invasiveness because an additional incision for specimen retrieval is not necessary. However, manipulation in the narrow anal canal and pelvic cavity through the anal canal is technically demanding when using the open technique under direct vision. Robotic systems are expected to be suitable for transanal procedures in which precise manipulation in confined spaces is necessary. Atallah et al. first reported the feasibility and efficacy of transanal endoscopic microsurgery, in which the local resection of benign rectal lesions and early rectal cancers are performed [51]. Furthermore, Gomez et al. recently reported their clinical experience of robotic transanal TME, in which transanal pelvic dissection is performed up to the peritoneal reflection using a robotic platform applied to the anus. Moreover, they suggested that robotic transanal TME is feasible and safe with uninvolved CRM in all cases [52]. Transanal TME using robotic systems is expected to be a viable therapeutic option for low rectal cancers that are difficult to approach because of individual variations or lesional characteristics [53, 54]. However, further clinical studies are required to confirm the safety and efficacy of transanal TME using robotic systems.
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Int J Clin Oncol Obturator foramen
a
b
Obturator nodes Internal iliac nodes
Fat ssue containing obturator nodes
Fig. 4 Robotic lateral pelvic lymph node dissection. a Dissection of obturator nodes (left side). b Completion of lateral pelvic lymph node dissection (left side). Reproduced with permission from [55]
Table 1 Surgical outcomes of robotic surgery for rectal cancer (vs. laparoscopic surgery) Operation time and blood loss Many studies report a longer operation time, but there are conflicting results No significant difference noted in meta-analyses Conversion to open surgery 0–7 % for robotic and 0–22 % for laparoscopic surgery Lower conversion rate in the majority of studies and meta-analyses Perioperative complications No significant difference in the majority of studies and meta-analyses Anastomotic leak: 3–14 % for robotic, and 2–12 % for laparoscopic surgery Findings in resected specimens Some studies report lower circumferential resection margin (CRM)-positive rates and higher lymph node counts No difference noted in meta-analyses Postoperative recovery and function No difference in surgical stress, interval to oral intake, and hospital stay Better urinary and sexual function in the early postoperative period Long-term outcomes Few nonrandomized studies so far No difference in overall and disease-free survival, or in local recurrence Learning curve Fewer cases seem to be required to achieve learning curve Cost issues Higher cost
Conclusions Surgical outcomes and other issues of robotic surgery for rectal cancer are summarized in Table 1. Robotic surgery is a new technique that allows precise manipulation in a confined space, such as the pelvic cavity; therefore, it is expected to be advantageous in performing minimally invasive, function-preserving surgery for rectal cancer.
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However, the oncological safety, functional outcomes, postoperative patient quality of life, and cost-effectiveness of this technique must be extensively evaluated and demonstrated before it can be widely accepted as an option for the surgical treatment of cancer. Furthermore, individual patient and rectal cancer tumor characteristics that predict superior outcomes with robotic surgery versus laparoscopic or open surgery should be determined in future studies.
Int J Clin Oncol Conflict of interest The authors declare that they have no conflict of interest. 17.
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REVIEW ARTICLE
Recent advances in robotic surgery for rectal cancer Soichiro Ishihara1 · Kensuke Otani1 · Koji Yasuda1 · Takeshi Nishikawa1 · Junichiro Tanaka1 · Toshiaki Tanaka1 · Tomomichi Kiyomatsu1 · Keisuke Hata1 · Kazushige Kawai1 · Hiroaki Nozawa1 · Shinsuke Kazama1 · Hironori Yamaguchi1 · Eiji Sunami1 · Joji Kitayama1 · Toshiaki Watanabe1
Received: 14 May 2015 / Accepted: 27 May 2015 © Japan Society of Clinical Oncology 2015
Abstract Robotic technology, which has recently been introduced to the field of surgery, is expected to be useful, particularly in treating rectal cancer where precise manipulation is necessary in the confined pelvic cavity. Robotic surgery overcomes the technical drawbacks inherent to laparoscopic surgery for rectal cancer through the use of multi-articulated flexible tools, three-dimensional stable camera platforms, tremor filtering and motion scaling functions, and greater ergonomic and intuitive device manipulation. Assessments of the feasibility and safety of robotic surgery for rectal cancer have reported similar operation times, blood loss during surgery, rates of postoperative morbidity, and circumferential resection margin involvement when compared with laparoscopic surgery. Furthermore, rates of conversion to open surgery are reportedly lower with increased urinary and male sexual functions in the early postoperative period compared with laparoscopic surgery, demonstrating the technical advantages of robotic surgery for rectal cancer. However, long-term outcomes and the cost-effectiveness of robotic surgery for rectal cancer have not been fully evaluated yet; therefore, large-scale clinical studies are required to evaluate the efficacy of this new technology. Keywords Rectal cancer · Robotic surgery · Laparoscopic surgery
* Toshiaki Watanabe [email protected] 1
Department of Surgical Oncology, The University of Tokyo Hospital, 7‑3‑1, Bunkyo‑ku, Hongo, Tokyo 113‑8655, Japan
Introduction The widespread application of total mesorectal excision (TME) for rectal cancer, originally proposed by Heald et al. in 1982, has greatly contributed to reductions in postoperative local recurrence rates, the most important oncological issue related to rectal cancer surgery [1]. TME principally involves sharp dissection and en bloc resection of mesorectal tissue, including the primary lesion and surrounding regional lymph nodes, by exposing precise pelvic anatomy, and the preservation of autonomic nerves to conserve postoperative urinary and sexual function. Recently, laparoscopic surgery was introduced for the treatment of rectal cancer as a minimally invasive alternative to conventional open surgery. Laparoscopic surgery has been shown to have a number of advantages over open surgery for the treatment of colon cancer, including reduced analgesic usage, faster recovery of oral intake, and shorter postoperative hospital stays without compromising long-term oncological outcomes [2–7]. However, in contrast to the case for colon cancer, there is relatively limited evidence regarding the safety and efficacy of laparoscopic surgery for rectal cancer, and some technical and oncological issues have been raised, including high rates of conversion to open surgery and circumferential resection margin (CRM) involvement of the specimen [5]. In laparoscopic surgery, precise manipulation is possible using magnified views of the surgical field; however, major drawbacks that are intrinsic to laparoscopic surgery include straight and inflexible devices, unstable intraoperative views with handheld two-dimensional cameras, and uncomfortable ergonomic positions of surgeons [8, 9]. Robotic technology, which has recently been introduced to the field of surgery, is expected to overcome these issues associated with laparoscopic surgery by using flexible devices with seven degrees of freedom of movement,
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stable three-dimensional camera platforms, more precise surgical manipulation by tremor filtering and motion scaling, and a more intuitive and ergonomic operative environment [8, 9]. In this article, we review recent advances in and future perspectives on robotic surgery for rectal cancer.
The da Vinci Surgical System® The da Vinci Surgical System® (Intuitive Surgical, Sunnyvale, CA, USA) is a robot that is currently available for use in surgical treatment (Fig. 1). The Zeus Surgical System® (Computer Motion, Santa Barbara, CA, USA) is another such robot, albeit one that is not currently available. A prototype da Vinci Surgical System® was developed in the late 1980s and was made commercially available in 1999 after several refinements. Currently, more than 3000 da Vinci Surgical Systems® are in operation worldwide and are
widely used in urological, gynecological, colorectal, cardiovascular, and thoracic surgery.
Surgical outcomes Among the various procedures performed by robotic surgery, the most evident benefits have been reported with robotic prostatectomy, including decreased blood loss during surgery, a lower incidence of perioperative morbidity, shorter hospital stays, reduced autonomic nerve injury, and faster recovery of urinary and male sexual functions [10]. Similar benefits are expected for robotic surgery for the treatment of rectal cancer, as both prostatectomy and rectal cancer surgery involve resection of organs from the confined bony pelvis with preservation of adjacent autonomic nerves (Fig. 2). Operation time
Fig. 1 The da Vinci Surgical System®. a Surgeon console. b Patient cart. Reproduced with permission from [55]
a
Proper rectal fascia
Conflicting results have been reported regarding the operation time of robotic surgery as compared with that of conventional laparoscopic surgery. A number of reports have demonstrated a longer operation time with robotic surgery [9, 11–13], whereas others have reported no difference in operation time between robotic and laparoscopic surgeries [14–18]. Patriti et al. reported a shorter operation time for robotic rectal resection; however, they are minority in this regard [19]. The variation in the reported operation time of robotic surgery for rectal cancer may be due to differences in the use of the robotic system, either “full robotic” surgery or “hybrid” surgery, where laparoscopic and robotic surgery are combined. Furthermore, the use of single or dual docking to the patient cart or the premature use of the procedure before adequate standardization may have impacted the findings of some studies. All published
b Proper rectal fascia
Pelvic floor Fig. 2 Intraoperative views of robotic total mesorectal excision (TME). a, b Robotic systems enable proper dissection in the deep pelvic area that tends to be tangential with laparoscopic surgery by
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virtue of multi-articulated devices with stable three-dimensional views. Reproduced with permission from [55]
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meta-analyses conclude that there is no difference in operation time between robotic and laparoscopic surgeries for rectal cancer [20–23]. Blood loss during surgery The majority of studies reporting blood loss during surgery found no difference between robotic and laparoscopic surgeries for rectal cancer [12, 17, 19, 24]. Popescu et al. demonstrated that the volume of blood loss was smaller for robotic surgery; however, the result of a recent meta-analysis demonstrated that there was no difference in operative blood loss between the two procedures [22]. Conversion to open surgery In the MRC-CLASSIC trial conducted in the UK, a high rate of conversion from laparoscopic to open surgery was reported for rectal cancer [5]. This high conversion rate is believed to reflect the technical difficulties involved in laparoscopic surgery for rectal cancer, due to the inherent problems mentioned above. In cases of laparoscopic surgery for colon cancer, conversion to open surgery has been reported to be associated with postoperative complications and morbidity and reduced survival rates [4, 5]. Therefore, conversion rates are considered an important indicator of the efficacy and oncological safety of minimally invasive surgery. In studies that compare robotic and laparoscopic surgeries, conversion rates to open surgery have been reported to be 0–7 % and 0–22 %, respectively [9, 11, 15–18, 25, 26], with the majority of studies demonstrating lower conversion rates with robotic surgery. In a published meta-analysis, the conversion rate of robotic surgery for rectal cancer was demonstrated to be lower than that of laparoscopic surgery, indicating the technical advantages of robotic surgery for rectal cancer.
Findings in resected specimens CRM, the distal resection margin (DRM), and the number of retrieved lymph nodes are important short-term oncologic markers in rectal cancer surgery, and are considered to be surrogate markers for long-term outcomes. Robotic systems may provide an oncologically safer option for surgery in the confined pelvic cavity because of the intuitive and ergonomically superior manipulation possible with flexible devices. In fact, a number of studies have reported lower rates of CRM involvement [18] and an increased number of retrieved lymph nodes [16, 25] with robotic surgery compared with laparoscopic surgery; however, the majority of studies have reported no difference in CRMand DRM-positive rates and the number of retrieved lymph nodes, and these results have been confirmed by a number of meta-analyses [20–23]. Postoperative recovery A number of studies reported shorter intervals to oral intake and hospital stays with robotic surgery compared with those following laparoscopic surgery [9, 15]; however, meta-analyses have demonstrated no significant difference in either of these measures [20–23]. Therefore, there appears to be no difference in the degree of surgical stress between robotic and laparoscopic surgeries, which is further corroborated by our recent study evaluating surgical stress using immunological parameters [27]. In this study, the expression of HLA-DR by peripheral blood lymphocytes, which is considered a marker of immune competence, was significantly higher in robotic surgery cases than in open surgery cases, and no difference was found from laparoscopic surgery cases, indicating that robotic and laparoscopic surgery for rectal cancer lead to reduced surgical stress compared with open surgery.
Perioperative complications
Postoperative urinary and sexual function
Perioperative complication rates are, in general, an important indicator of the safety of a surgical procedure. Although Baik et al. reported that serious complication rates were significantly lower with robotic surgery (5.4 %) compared with laparoscopic surgery (19.3 %) [15], complication rates did not differ between robotic and laparoscopic surgeries in other reports [9, 11, 14, 16, 19, 25]. The results of meta-analyses have demonstrated that there is no difference in complication rates [20–23]. In particular, anastomotic leakage—the most clinically important complication following rectal cancer surgery—has been reported to occur in 3–14 % of robotic surgery cases and 2–12 % of laparoscopic surgery cases [9, 11–13, 15–18, 24–26], with no significant difference between these rates.
Urinary and sexual dysfunction due to autonomic nerve injury occasionally occurs following TME for rectal cancer, and these issues may substantially impair the quality of life of patients. Although laparoscopic surgery is considered a minimally invasive surgery, a study has reported that male sexual function following laparoscopic surgery was poorer than that following open surgery [28], indicating the technical difficulty of laparoscopic surgery for rectal cancer. Kim et al. compared postoperative urinary and male sexual function following robotic and laparoscopic surgery using uroflowmetry and questionnaires [29] and found that, in the early postoperative period, these functions were better after robotic surgery than after laparoscopic surgery. Park et al. evaluated these functions using questionnaires [30]
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and also demonstrated that male sexual function was better following robotic surgery in the early postoperative period, although no difference in urinary function was observed. Postoperative function following robotic surgery is yet to be fully evaluated. Long‑term outcomes Robotic surgery for rectal cancer has only recently been introduced, so there have been only a few reports evaluating long-term oncological outcomes. Park et al. evaluated oncological outcomes of patients with rectal cancer treated with robotic or laparoscopic surgery who were followed up for a median period of 58 months, and demonstrated that overall and disease-free survival did not significantly differ between the treatment groups [31]. Local recurrence rates were reported as 2.3 % in the robotic surgery group and 1.2 % in the laparoscopic surgery group, with no significant difference found. However, as only the results of nonrandomized studies are currently available, future randomized controlled trials are required to evaluate long-term outcomes following robotic TME that may potentially be optimized by the da Vinci system.
Learning curves Analysis of the learning process is important when introducing a new technique into clinical practice, not only for the assessment of safety and efficacy but also to encourage wide acceptance of the technique. To evaluate the learning process, learning curve analyses of surgical approaches for rectal cancer using the cumulative sum (CUSUM) methodology have recently been reported [32–34]. In the case of laparoscopic surgery, the learning curve for rectal cancer surgery has been demonstrated to be relatively long and gradual compared with other widely performed procedures such as laparoscopic cholecystectomy, and the number of cases that are required to achieve the learning curve is estimated to be between 60 and 80 [35]—greater than the estimated 50–60 cases required for laparoscopic colonic resection [36]. When considering the advantages of the robotic system, the number of cases necessary to achieve the learning curve for robotic rectal cancer surgery is expected to be smaller than that for laparoscopic rectal cancer surgery. In learning curve analyses for robotic rectal cancer surgery using the CUSUM technique, it has been shown that there are multiple phases of the learning process [32–34]. Jimenez-Rodriguez et al. reported that the operative duration significantly decreased after 21–23 cases, eventually reaching a plateau when the learning curve was achieved [34]. Kim et al. reported that the first plateau in the operation time occurred after 33 cases; therefore, the first 32 cases
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had a greater impact on the learning process for robotic TME [33]. From these analyses, fewer cases appear to be required to achieve the learning curve of robotic rectal cancer surgery than that of laparoscopic rectal cancer surgery. Robotic surgery is considered to be more intuitive; i.e., the robotic system simulates the manipulation of tools and techniques used for open surgery. Therefore, the robotic interface is expected to allow surgeons who are not experienced in laparoscopic surgery to perform minimally invasive surgery for rectal cancer, as has already been demonstrated for prostatectomy [37]. Kim et al. analyzed the leaning curve of an open surgeon with limited laparoscopy experience and demonstrated that operation times significantly decreased after as few as 20 cases without compromising surgical and oncological outcomes [38]. However, though laparoscopic experience is desirable, the degree of impact of experience or inexperience in laparoscopic surgery on the ability to master robotic surgery for rectal cancer has yet to be clarified.
Cost issues with robotic surgery Robotic surgery for rectal cancer is apparently more expensive than open or laparoscopic surgery because of the high cost of the instruments used and the robotic system itself. In Korea, one of the most advanced countries in the use of robotic surgery, the total cost of robotic surgery for rectal cancer is estimated as $14,000, which is 1.5 times as expensive as the cost of laparoscopic surgery, $9000 [9]. Bryn et al. reported that the cost of robotic surgery has gradually decreased as institutional experience has increased [39]. Furthermore, instruments and the robotic system are expected to become increasingly sophisticated and rationalized, resulting in future decreases in the cost of robotic surgery. However, superior surgical outcomes with robotic surgery in addition to an equal or comparable cost to that of conventional laparoscopic surgery are required before wide acceptance of this new technique becomes likely.
Clinical trials To date, only one randomized controlled trial (RCT) has compared the outcomes of robotic and laparoscopic surgery for rectal cancer [19]. This study reported decreased operation times, lower conversion rates, comparable postoperative morbidities, and overall and disease-free survival rates in the robotic surgery group, concluding that robotic surgery for rectal cancer is both safe and effective. However, the number of cases examined was very small (29 cases for robotic surgery and 37 cases for laparoscopic surgery), and the follow-up period for robotic surgery
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cases was short (mean 18.7 months). Therefore, the results of this study must be interpreted with caution. Recently, an international RCT conducted by Leeds University in the UK (the ROLARR trial) was initiated [8]. In this trial, 200 cases will be enrolled into a robotic surgery group and another 200 into a laparoscopic surgery group (giving a total of 400 cases) to assess the following end-points: rate of conversion to open surgery; CRM positive rate; local recurrence; disease-free survival; overall survival; morbidity and mortality rates; postoperative quality of life; and cost-effectiveness. The results of this trial are eagerly awaited.
Application of robotic techniques to advanced procedures Intersphincteric resection Intersphincteric resection (ISR) of rectal cancer was first reported by Schiessel et al. in 1994 and is now performed as the frontline sphincter-preserving surgery in very lowlying rectal cancer [40]. When performing ISR, manipulation in deeper and narrower areas of the pelvic cavity is required; therefore, robotic techniques are expected to demonstrate their full potential in this setting (Fig. 3). Park et al. reported that robotic ISR was oncologically safe, with faster recovery of male sexual function noted in cases treated with robotic surgery compared with laparoscopic ISR [41]. Furthermore, they reported that transabdominal ISR, in which the intersphincteric dissection transects the distal margin within the pelvic cavity, could be performed more frequently with robotic assistance than with laparoscopic surgery [41], indicating the technical aptitude of robotic systems in performing ISR.
Distal resecon margin Rectum Fig. 3 Robotic intersphincteric resection of rectal cancer. Robotic systems enable precise transection of distal resection margins in the anal canal. Reproduced with permission from [55]
Lateral pelvic lymph node dissection The efficacy of lateral pelvic lymph node dissection for rectal cancer outside the TME plane is yet to determined, particularly in cases where lateral pelvic lymph nodes are not clinically involved (termed “prophylactic dissection”) or after preoperative chemoradiotherapy [42–44]. In Japan, lateral pelvic lymph node dissection is regarded as a standard procedure for T3–T4 low rectal cancer as a result of the findings of a retrospective analysis [45–47]. Lateral pelvic lymph node dissection is performed in the deep region of the pelvic cavity, where the magnified view obtained in laparoscopic surgery is considered to be a significant advantage of laparoscopic lateral pelvic lymph node dissection [48]. However, manipulation during lateral pelvic lymph node dissection tends to be tangential and uncomfortable for surgeons using straight laparoscopic surgical instruments. Conversely, lateral pelvic lymph node dissection with robotic surgery using multi-articulated flexible devices appears to decrease surgeon stress (Fig. 4), with the efficacy of this approach being reported by several advanced institutions [49, 50]. Transanal robotic surgery The use of a transanal approach in the surgical treatment of rectal cancer appears to be reasonable because rectal cancer is located near the anus. Retrieval of resected specimens from the anus, where possible, is considered to decrease rectal cancer surgery invasiveness because an additional incision for specimen retrieval is not necessary. However, manipulation in the narrow anal canal and pelvic cavity through the anal canal is technically demanding when using the open technique under direct vision. Robotic systems are expected to be suitable for transanal procedures in which precise manipulation in confined spaces is necessary. Atallah et al. first reported the feasibility and efficacy of transanal endoscopic microsurgery, in which the local resection of benign rectal lesions and early rectal cancers are performed [51]. Furthermore, Gomez et al. recently reported their clinical experience of robotic transanal TME, in which transanal pelvic dissection is performed up to the peritoneal reflection using a robotic platform applied to the anus. Moreover, they suggested that robotic transanal TME is feasible and safe with uninvolved CRM in all cases [52]. Transanal TME using robotic systems is expected to be a viable therapeutic option for low rectal cancers that are difficult to approach because of individual variations or lesional characteristics [53, 54]. However, further clinical studies are required to confirm the safety and efficacy of transanal TME using robotic systems.
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a
b
Obturator nodes Internal iliac nodes
Fat ssue containing obturator nodes
Fig. 4 Robotic lateral pelvic lymph node dissection. a Dissection of obturator nodes (left side). b Completion of lateral pelvic lymph node dissection (left side). Reproduced with permission from [55]
Table 1 Surgical outcomes of robotic surgery for rectal cancer (vs. laparoscopic surgery) Operation time and blood loss Many studies report a longer operation time, but there are conflicting results No significant difference noted in meta-analyses Conversion to open surgery 0–7 % for robotic and 0–22 % for laparoscopic surgery Lower conversion rate in the majority of studies and meta-analyses Perioperative complications No significant difference in the majority of studies and meta-analyses Anastomotic leak: 3–14 % for robotic, and 2–12 % for laparoscopic surgery Findings in resected specimens Some studies report lower circumferential resection margin (CRM)-positive rates and higher lymph node counts No difference noted in meta-analyses Postoperative recovery and function No difference in surgical stress, interval to oral intake, and hospital stay Better urinary and sexual function in the early postoperative period Long-term outcomes Few nonrandomized studies so far No difference in overall and disease-free survival, or in local recurrence Learning curve Fewer cases seem to be required to achieve learning curve Cost issues Higher cost
Conclusions Surgical outcomes and other issues of robotic surgery for rectal cancer are summarized in Table 1. Robotic surgery is a new technique that allows precise manipulation in a confined space, such as the pelvic cavity; therefore, it is expected to be advantageous in performing minimally invasive, function-preserving surgery for rectal cancer.
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However, the oncological safety, functional outcomes, postoperative patient quality of life, and cost-effectiveness of this technique must be extensively evaluated and demonstrated before it can be widely accepted as an option for the surgical treatment of cancer. Furthermore, individual patient and rectal cancer tumor characteristics that predict superior outcomes with robotic surgery versus laparoscopic or open surgery should be determined in future studies.
Int J Clin Oncol Conflict of interest The authors declare that they have no conflict of interest. 17.
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