Asian J Endosc Surg ISSN 1758-5902
R E V I E W A RT I C L E
Robotic surgery for rectal cancer Hiroaki Nozawa & Toshiaki Watanabe Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan
Keywords: Laparoscopic surgery; rectal cancer; robotic surgery Correspondence Toshiaki Watanabe, Department of Surgical Oncology, The University of Tokyo Hospital, 7-31, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. Tel: +81 3 5800 8653 Fax: +81 3 3811 6822 Email: [email protected] Received 26 July 2017; accepted 30 July 2017 DOI: 10.1111/ases.12427
Abstract Laparoscopic surgery has gained acceptance as a less invasive approach in the treatment of colon cancer. However, laparoscopic surgery for rectal cancer, particularly cancer of the lower rectum, is still challenging because of limited accessibility. Robotic surgery overcomes the limitations of laparoscopy associated with anatomy and offers certain advantages, including 3-D imaging, dexterity and ambidextrous capability, lack of tremors, motion scaling, and a short learning curve. Robotic rectal surgery has been reported to reduce conversion rates, particularly in low anterior resection, but it is associated with longer operative times than the conventional laparoscopic approach. Postoperative morbidities are similar between the robotic and conventional laparoscopic approaches, and oncological outcomes such as the quality of the mesorectum and the status of resection margins are also equivalent. The possible superiority of robotic surgery in terms of the preservation of autonomic function has yet to be established in research based on larger numbers of patients. Although robotic rectal surgery is safe, feasible, and appears to overcome some of the technical limitations associated with conventional laparoscopic surgery, the advantages provided by this technical innovation are currently limited. To justify its expensive cost, robotic surgery is more suitable for select patients, such as obese patients, men, those with cancer of the lower rectum, and those receiving preoperative chemoradiotherapy.
Introduction Total mesorectal excision (TME), proposed by Heald et al., involves en-bloc dissection of the rectum and surrounding fatty mesorectum, including the regional lymph nodes, while preserving the autonomic nerves in the pelvis (1). TME is now considered to be a key component of surgical procedures for rectal cancer, and it contributes to reducing local recurrence after surgery. Laparoscopic surgery has recently been introduced as a less invasive treatment option for colon cancer. Many randomized trials have demonstrated that laparoscopic surgery is more beneficial than open surgery in terms of the reduced use of analgesics, early oral intake, and a shorter hospital stay after surgery, with similar oncological outcomes being reported (2–5). However, there is limited evidence regarding the safety and oncological outcomes of laparoscopic surgery for rectal cancer in spite of several clinical trials having been conducted and published (6–9).
In laparoscopic surgery, a magnified view of the surgical field enables surgeons to perform more precise procedures. However, straight and inflexible devices, unstable intraoperative views with handheld 2-D cameras, and uncomfortable ergonomic positions are major drawbacks, and these technical issues may lead to potentially inferior clinical outcomes. For example, randomized controlled trials revealed higher rates of a circumferential margin in laparoscopic surgery for rectal cancer than in open surgery (8,9). Robotic surgery will overcome these issues because it offers EndoWrists (Intuitive Surgical, Inc., Sunnyvale, CA) with seven degrees of freedom, 180 articulation, 540 rotation, tremor-reducing and motion-scaling functions, stable 3-D 10-fold magnification vision, and a better ergonomic work space. The application of robotics to urological, gynecological, vascular, and cardiac surgery has enhanced competence because of these features (10–15). Since 2000, robotic surgery has been applied to rectal resection in several
Asian J Endosc Surg (2017) © 2017 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and John Wiley & Sons Australia, Ltd
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institutes (10), but there remains a paucity of literature available on direct comparisons between open or laparoscopic surgery and robotic rectal surgery. Moreover, the existing research is heterogenous in terms of design, selection criteria of patients, and outcome measures, which makes it difficult to obtain clear conclusions. In this review article, we will provide an overview of the history, current applications, evidence from clinical studies, and future of robotic surgery for rectal cancer.
Background of Robots for Surgery The most prevalent platform for robotic surgery is currently the da Vinci Surgical System (Intuitive Surgical, Sunnyvale, USA). This system was approved by the US Food and Drug Administration in 1999, and since then, da Vinci models have changed periodically. As of June 2017, 4149 da Vinci series have been installed worldwide, including 538 in Asia (16). The da Vinci systems have been widely used for urological, gynecological, cardiothoracic, and gastrointestinal surgery. Total prostatectomy has been the most frequently performed robotic surgery to date because it leads to reduced blood loss, low complication rates, early postoperative recovery, a shorter hospital stay, reduced risk of neural damage, and early recovery of genitourological functions (17). Because the prostate and rectum are both located in the pelvis, robotic surgery is considered to be useful for rectal surgery, similar to urological surgery, which has a narrow surgical field. The da Vinci systems are not perfect surgical robots. A major drawback is the loss of tactile sensation. Surgeons cannot feel tension well, which increases the risks of perforation and injury. Tissue tension on sutures needs
Figure 1 The arrangement of surgical ports and docking of the patient cart. (a) The first docking. (b) The second docking. Dark arrows indicate the directions of instruments. A, assistant port; C, camera port; R, ports used by robot arms.
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to be gathered from visual information. The manufacturer developed surgical simulators and a dual-console system as training methods to compensate for this disadvantage. Several other limitations of robotic systems, such as a fixed operating table position and collisions between the robotic arms outside of the body, have been reported. The latest model, the da Vinci Xi, which was launched by the manufacturer in 2014, has an integrated table motion feature that can adjust the operating table without undocking. In addition, the overhead arrangement of thinner arms with additional joints maximizes access, minimizes collisions, shortens the console time, and enables single-dock multi-quadrant robotic surgery (18–20). Collectively, these features may give impetus to robotic surgery for rectal cancer.
Procedures of Robotic Anterior Resection with TME (in Our Institute) In this section, we describe our standardized method of surgical procedures for rectal surgery using the da Vinci system. We employ the dual-docking method for robotic rectal surgery. After pneumoperitoneum with an intraabdominal pressure of 10 mmHg is obtained, a 12-mm balloon trocar is inserted at the umbilicus for the camera. Following an examination of the intra-abdominal cavity for distant metastasis, another five ports are inserted. After mobilization of the small intestine, the patient cart is obliquely docked from the left caudal side of the patient (Figure 1a), and dissection around the inferior mesenteric artery under a medial-to-lateral approach and mobilization of the sigmoid colon are performed. When required, the splenic flexure is taken down. The cart is moved away and then docked again between the patient’s legs so that sharp dissection of the pre-hypogastric nerve fascia and behind Denonvilliers’ fascia can be performed while avoiding autonomic nerve injury during mobilization of the rectum (Figures 1b,2a). The rectum is transected more than 2 cm below the lower border of the tumor, thereby completing TME. When the lower border of the tumor is located distal to the peritoneal reflection and is found to have invaded beyond the muscularis propria (clinical T3 or T4, any N), lateral pelvic lymph node dissection (LLND) is considered. Bilateral LLND is performed on patients without preoperative (chemo)radiation therapy (CRT or RT), whereas after CRT/RT, selective LLND is indicated for patients who had clinically positive lymph nodes of the pelvic wall at the initial diagnosis (21). This procedure includes complete removal of the lymph nodes in the fat tissues outside the pelvic plexus and around the common iliac artery, internal iliac artery, and obturator space (Figure 2b), while preserving all autonomic nerves
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Figure 2 Intraoperative view of robotic rectal surgery. (a) Dissection just behind the mesorectum. (b) The lateral pelvic wall after lateral pelvic lymph node dissection. Ext., external; inf., inferior; sup., superior.
when they are not encased. The robotic surgery in LLND offers some possible advantages. A specimen is removed through the extended incision at the umbilicus after the proximal end of the tumorbearing segment has been divided extracorporeally. Anastomosis and drainage tube placement are performed via a conventional laparoscopic technique.
Intraoperative Outcomes In laparoscopic surgery for rectal cancer, a high conversion rate to open surgery (34%) was initially reported (22). Obesity, narrow pelvis, bulky tumor, mesorectum, and adhesions from previous surgery can lead to conversion to open method because of the limitations of the laparoscopic instruments. Postoperative complications and poor survival are associated with conversion in colon cancer (22,23), so it is also a critical issue to reduce the conversion rate in rectal cancer. Meta-analyses showed that the conversion rate was lower in robotic surgery for rectal cancer (range: 0%–7.3%) than in laparoscopic surgery (range, 0%–26.3%) (24–29). Many advantageous features of the robotic system appear to have contributed to the favorable result, and the
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difference was particularly prominent in surgery for lower rectal cancer, as reported by Ielpo et al. (robotic surgery conversion rate, 1.8%; laparoscopic surgery conversion rate, 9.2%) (30). However, if serious life-threatening intraoperative events occur (e.g. uncontrolled bleeding), the time needed to undock the robot for conversion to open laparotomy may result in a disastrous outcome (31). Several meta-analyses showed that robotic surgery was generally associated with longer operative times (27,29), whereas others concluded that there was no significant difference between robotic and laparoscopic surgery (25,26,28). These controversial conclusions appear to stem from various differences among institutions in terms of surgical procedures (e.g. full robotic vs hybrid surgery, routine takedown of the splenic flexure vs no mobilization, and single vs multiple dockings). The docking and separation procedure for a robotic cart is known to be time-consuming. However, operative times can be decreased if the robotic arms are positioned and the forceps are manipulated in a manner than avoids collisions (32). In addition, improvements to the robotic system itself, such as da Vinci Xi, will reduce repeated docking, which may result in shorter operative times. The operative time also depends on the learning curve of surgeons. Less experience is generally required for learning robotic surgery than conventional laparoscopic surgery. The learning curve for robotic rectal surgery is typically analyzed using the cumulative method. Transferring surgical skills from open surgery to the robotic approach may rapidly decrease the operative time during the first phase of the learning curve (33,34). The second phase allows for the consolidation of additional experience. The third phase is the post-learning period of surgery for more complex cases. Several institutes reported a markedly shorter learning curve for robotic surgery than for conventional laparoscopic surgery, which has a steep and long learning curve (35,36). In contrast, Park et al. did not observe differences in learning curves between conventional laparoscopic and robotic low anterior resection (37). Previous studies showed that estimated blood loss during procedures was similar between robotic and laparoscopic surgery (28,38,39), but some found a significantly lower volume of blood loss with the robotic than the laparoscopic approach (40).
Short-term Postoperative Outcomes Postoperative complications are important for discussing the safety of robotic surgery. Meta-analyses showed that there was no significant difference in the frequency of overall complications between robotic and conventional laparoscopic surgery (24–29). For example, anastomotic
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leakage, the most frequent complication, occurred in 2.4%–11.2% of cases that underwent conventional laparoscopic rectal surgery and in 1.8%–13.5% that underwent robotic surgery (27). There is no evidence of the superiority of robotic rectal surgery over laparoscopy in terms of the incidence of other postoperative complications (24–29). The time to normal diet was shown to be similar between robotic and conventional laparoscopic surgery (24–26,28), except for a few studies that reported a significant difference in favor of robotic surgery (39,41). Postoperative hospital stay was also similar between robotic and conventional laparoscopic surgery according to meta-analyses. However, some studies reported a shorter stay after robotic surgery, and others had the opposite finding (24–26,28,29). Surgical stress was evaluated subjectively and objectively in a few studies. Kang et al. showed that postoperative analgesic usage was lower after robotic surgery than after open surgery, and the visual analog scale score was significantly lower after robotic surgery than after laparoscopic surgery for rectal cancer (39). Kamali et al. similarly reported that robotic anterior resection was less painful than laparoscopic surgery based on the European Organisation for Research and Treatment of Cancer quality of life questionnaire (QLQ)-C30 questionnaires score (42). In our institute, immune responses were compared among patients who underwent open, laparoscopic, and robotic rectal surgery by evaluating Creactive protein levels, lymphocyte subset counts, and Human Leukocyte Antigen-D Related (HLA-DR) marker levels in blood samples. HLA-DR expression on monocytes, an index of immune competence, was higher on day 3 after robotic surgery than after open surgery, suggesting that robotic surgery is less invasive (43). These anecdotal findings need to be validated by evaluating different sets of patient cohorts.
Functional Outcomes Intraoperative injury to the pelvic autonomic nerves may result in urinary retention, sexual dysfunction, and fecal incontinence. The preservation of these nerves is a crucial component in rectal surgery in order to avoid anterior resection syndrome. However, only a few studies have examined this issue after robotic surgery. Park et al. reported earlier recovery of erectile function after robotic surgery than after conventional laparoscopic surgery (44). Kim et al. found earlier recovery of urinary function (i.e. 6 months after robotic surgery), but no significant difference was noted thereafter between the robotic and conventional laparoscopic approaches (45). Luca et al. stated that robotic surgery allows for the
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preservation of urinary and sexual functions after nervepreserving TME (46). However, most studies did not reveal any significant difference between the conventional laparoscopic and robotic approaches with regard to urinary retention, sexual disorders, and fecal incontinence after rectal surgery (27,38).
Oncological Outcomes The number of lymph nodes harvested, the distal resection margin, the circumferential resection margin, and the quality of the mesorectum are representative measures of the pathological quality of surgical resection. Meta-analyses have generally shown that there is no significant difference in these parameters between robotic and laparoscopic resection (24,25,27,29). Long-term outcome measures such as relapse-free survival and overall survival have not been extensively investigated. The heterogenous lengths of the follow-up periods in previous studies and the relatively short history of robotic rectal surgery make it difficult to address this issue. Park et al. reported that relapse-free survival and overall survival were similar between the laparoscopic and robotic approaches based on a median follow-up of 58 months (47).
Cost One main disadvantage of robotic surgery is the high costs associated with the purchase and maintenance of robot technology. The high capital and running costs of the robotic system have hindered its installation in many countries. In addition, health insurance systems do not necessarily cover the whole cost of robotic surgery, although this differs from nation to nation. Overall, robotic surgery is 1.5–3 times as expensive as laparoscopic surgery (27). Hottenrott projected that the disadvantage of the cost may be overcome by limiting the use of robotic surgery to specialized centers (48). In contrast, Byrn et al. reported that the accumulation of robotic cases will decrease costs (49). It may be important to identify patients who will obviously benefit from robotic surgery despite its high cost. Obesity, male sex, lower rectal cancer, and preoperative CRT represent selection criteria for robotic surgery that may help to justify its overwhelming cost (27,50).
Surgery Beyond Standard Rectal Surgery Intersphincteric resection (ISR) ISR is a relatively new sphincter-preserving surgical procedure for very low rectal cancer and anal canal cancer; it is an alternative to abdominoperineal resection, which
Asian J Endosc Surg (2017) © 2017 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and John Wiley & Sons Australia, Ltd
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is physically and mentally burdensome to the patient. Since Schiessel et al. first reported ISR in 1994 (51), the procedure has been widely accepted. However, it is difficult to perform ISR without causing functional anal deterioration and avoiding local recurrence (52,53). Because robot-assisted rectal surgery is beneficial for patients with lower rectal cancer, the need for ISR appears to be a good indication for the robotic approach. A Korean group confirmed that robotic ISR may be performed with oncological safety (54).
locally advanced rectal cancer in most Asian countries, including in Japan, where extended surgery without preoperative CRT is the standard treatment (68–70). LLND via conventional laparoscopy may be challenging with straight instruments. In contrast, robotic LLND is considered easier to perform because of its stable magnified view and multi-articulated forceps (71). Yamaguchi et al. reported that robotic LLND was superior to open surgery because of the lower rate of urinary retention (32).
Robotic surgery from a transanal approach
Pelvic exenteration
A transanal approach, such as transanal minimally invasive surgery for cancer very close to the anus, is increasingly attracting attention. Atallah et al. first described the usefulness of robotic-assisted transanal minimally invasive surgery for early cancer or benign neoplasms located near the anus (55). Moreover, transanal TME was recently introduced as a minimally invasive transanal procedure to facilitate difficult pelvic dissections. Several studies reported that transanal TME for distal mesorectal dissection achieved similar technical success to laparoscopic TME and offered acceptable oncologic and perioperative outcomes (56,57). Robotic surgery has also been applied for this manipulation technique from the perineal side for early-stage rectal cancers. Gómez Ruiz et al. demonstrated that the procedure was a feasible and safe option, but the follow-up period was short (58).
In patients with locally advanced rectal cancer invading adjacent organs such as the prostate and seminal vesicles, pelvic exenteration represents a treatment option. This extremely radical surgery may be performed using a robotic technique by experienced colorectal surgeons and urologists (72).
Ileal pouch-anal anastomosis (IPAA) Restorative proctocolectomy with IPAA is one of the standard procedures for inflammatory bowel disease. For the same reasons as robot-assisted ISR in patients with very lower rectal cancer, IPAA via a robotic approach may be beneficial for patients with inflammatory bowel disease-associated neoplasm. Pedraza et al. and our group recently reported patients with ulcerative colitis with dysplasia or cancer in the rectum who underwent robot-assisted restorative proctocolectomy with IPAA (59,60).
Conclusions The use of a robotic approach has attracted increasing attention in the field of pelvic surgery, including rectal surgery. This technique appears to overcome most of the limitations of conventional laparoscopic surgery. The precise procedures provided by this new technology are in demand for surgery performed in a narrow space such as the pelvis. Although we are still at the dawn of robotic-assisted rectal surgery, its technical safety and oncological safety have been proven. Moreover, the similar outcomes achieved by the robotic and conventional laparoscopic approaches suggest the potential superiority of robotic surgery in rectal cancer because surgeons are more likely to prefer robotic surgery for more challenging lesions. However, the related cost may restrict its use to patients with features that absolutely demand robotic techniques. More evidence is needed to confirm the benefits of robotic rectal surgery. The potential benefits will be addressed by ongoing phase 3 prospective randomized controlled trials such as the robotic versus laparoscopic resection for rectal cancer (ROLLAR trial) and the comparison of laparoscopic versus robot-assisted for rectal cancer (COLRAR trial) (73,74).
Lateral pelvic lymph node dissection (LLND) Locally advanced rectal cancer may metastasize to the lymph nodes of the pelvic wall, with frequencies reported to be 15%–20% (61–65). Even after preoperative CRT, they do not necessarily diminish. Recent studies suggested that LLND reduces local recurrence and improves survival rates (66,67). Therefore, LLND represents a crucial element in the surgical procedure for
Acknowledgments Toshiaki Watanabe received lecture fees from Intuitive Surgical, Covidien, Olympus, and Johnson & Johnson. Hiroaki Nozawa has no conflicts of interest to declare in association with the present study. This work was supported by Grants-in-Aids for Scientific Research from the Japan Society for the Promotion
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of Science (A, no.16H02672; C, no.17K10621) and from the Japan Agency for Medical Research and Development’s Project for Cancer Research and Therapeutic Evolution (no. 16cm0106502h0001).
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57. Penna M, Hompes R, Arnold S et al. Transanal total mesorectal excision: International registry results of the first 720 cases. Ann Surg 2017; 266: 111–117. 58. Gómez Ruiz M, Parra IM, Palazuelos CM et al. Roboticassisted laparoscopic transanal total mesorectal excision for rectal cancer: A prospective pilot study. Dis Colon Rectum 2015; 58: 145–153. 59. Pedraza R, Patel CB, Ramos-Valadez DI et al. Roboticassisted laparoscopic surgery for restorative proctocolectomy with ileal J pouch-anal anastomosis. Minim Invasive Ther Allied Technol 2011; 20: 234–239. 60. Anzai H, Ishihara S, Kiyomatsu T et al. Robot-assisted restorative proctocolectomy and ileal pouch–anal anastomosis for ulcerative colitis. Videoscopy 2016; 27. Available from URL: http://online.liebertpub.com/doi/full/10.1089/ vor.2016.0383. accessed on July 25 2017. 61. Sugihara K, Moriya Y, Akasu T et al. Pelvic autonomic nerve preservation for patients with rectal carcinoma. Oncologic and functional outcome. Cancer 1996; 78: 1871–1880. 62. Moriya Y, Sugihara K, Akasu T et al. Importance of extended lymphadenectomy with lateral node dissection for advanced lower rectal cancer. World J Surg 1997; 21: 728–732. 63. Ueno H, Mochizuki H, Hashiguchi Y et al. Prognostic determinants of patients with lateral nodal involvement by rectal cancer. Ann Surg 2001; 234: 190–197. 64. Shimoyama M, Yamazaki T, Suda T et al. Prognostic significance of lateral lymph node micrometastases in lower rectal cancer: An immunohistochemical study with CAM5.2. Dis Colon Rectum 2003; 46: 333–339. 65. Ueno M, Oya M, Azekura K et al. Incidence and prognostic significance of lateral lymph node metastasis in patients with advanced low rectal cancer. Br J Surg 2005; 92: 756–763.
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66. Sugihara K, Kobayashi H, Kato T et al. Indication and benefit of pelvic sidewall dissection for rectal cancer. Dis Colon Rectum 2006; 49: 1663–1672. 67. Kobayashi H, Mochizuki H, Kato T et al. Outcomes of surgery alone for lower rectal cancer with and without pelvic sidewall dissection. Dis Colon Rectum 2009; 52: 567–576. 68. Hojo K, Koyama Y, Moriya Y. Lymphatic spread and its prognostic value in patients with rectal cancer. Am J Surg 1982; 144: 350–354. 69. Moriya Y, Hojo K, Sawada T et al. Significance of lateral node dissection for advanced rectal carcinoma at or below the peritoneal reflection. Dis Colon Rectum 1989; 32: 307–315. 70. Watanabe T, Muro K, Ajioka Y et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 2017. https://doi.org/10.1007/s10147-017-1101-6. 71. Kagawa H, Kinugasa Y, Shiomi A et al. Robotic-assisted lateral lymph node dissection for lower rectal cancer: Shortterm outcomes in 50 consecutive patients. Surg Endosc 2015; 29: 995–1000. 72. Shin JW, Kim J, Kwak JM et al. First report: Robotic pelvic exenteration for locally advanced rectal cancer. Colorectal Dis 2014; 16: O9–O14. 73. Collinson FJ, Jayne DG, Pigazzi A et al. An international, multicentre, prospective, randomised, controlled, unblinded, parallel-group trial of robotic-assisted versus standard laparoscopic surgery for the curative treatment of rectal cancer. Int J Colorectal Dis 2012; 27: 233–241. 74. ClinicalTrials.gov. A trial to assess robot-assisted surgery and laparoscopy-assisted surgery in patients with mid or low rectal cancer (COLRAR). Available from URL: https://clinicaltrials.gov/ct2/show/NCT01423214?term=NCT +01423214. ClinicalTrials.gov indetifier: NCT01423214; accessed on July 25 2017.
Asian J Endosc Surg (2017) © 2017 Japan Society for Endoscopic Surgery, Asia Endosurgery Task Force and John Wiley & Sons Australia, Ltd
R E V I E W A RT I C L E
Robotic surgery for rectal cancer Hiroaki Nozawa & Toshiaki Watanabe Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan
Keywords: Laparoscopic surgery; rectal cancer; robotic surgery Correspondence Toshiaki Watanabe, Department of Surgical Oncology, The University of Tokyo Hospital, 7-31, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. Tel: +81 3 5800 8653 Fax: +81 3 3811 6822 Email: [email protected] Received 26 July 2017; accepted 30 July 2017 DOI: 10.1111/ases.12427
Abstract Laparoscopic surgery has gained acceptance as a less invasive approach in the treatment of colon cancer. However, laparoscopic surgery for rectal cancer, particularly cancer of the lower rectum, is still challenging because of limited accessibility. Robotic surgery overcomes the limitations of laparoscopy associated with anatomy and offers certain advantages, including 3-D imaging, dexterity and ambidextrous capability, lack of tremors, motion scaling, and a short learning curve. Robotic rectal surgery has been reported to reduce conversion rates, particularly in low anterior resection, but it is associated with longer operative times than the conventional laparoscopic approach. Postoperative morbidities are similar between the robotic and conventional laparoscopic approaches, and oncological outcomes such as the quality of the mesorectum and the status of resection margins are also equivalent. The possible superiority of robotic surgery in terms of the preservation of autonomic function has yet to be established in research based on larger numbers of patients. Although robotic rectal surgery is safe, feasible, and appears to overcome some of the technical limitations associated with conventional laparoscopic surgery, the advantages provided by this technical innovation are currently limited. To justify its expensive cost, robotic surgery is more suitable for select patients, such as obese patients, men, those with cancer of the lower rectum, and those receiving preoperative chemoradiotherapy.
Introduction Total mesorectal excision (TME), proposed by Heald et al., involves en-bloc dissection of the rectum and surrounding fatty mesorectum, including the regional lymph nodes, while preserving the autonomic nerves in the pelvis (1). TME is now considered to be a key component of surgical procedures for rectal cancer, and it contributes to reducing local recurrence after surgery. Laparoscopic surgery has recently been introduced as a less invasive treatment option for colon cancer. Many randomized trials have demonstrated that laparoscopic surgery is more beneficial than open surgery in terms of the reduced use of analgesics, early oral intake, and a shorter hospital stay after surgery, with similar oncological outcomes being reported (2–5). However, there is limited evidence regarding the safety and oncological outcomes of laparoscopic surgery for rectal cancer in spite of several clinical trials having been conducted and published (6–9).
In laparoscopic surgery, a magnified view of the surgical field enables surgeons to perform more precise procedures. However, straight and inflexible devices, unstable intraoperative views with handheld 2-D cameras, and uncomfortable ergonomic positions are major drawbacks, and these technical issues may lead to potentially inferior clinical outcomes. For example, randomized controlled trials revealed higher rates of a circumferential margin in laparoscopic surgery for rectal cancer than in open surgery (8,9). Robotic surgery will overcome these issues because it offers EndoWrists (Intuitive Surgical, Inc., Sunnyvale, CA) with seven degrees of freedom, 180 articulation, 540 rotation, tremor-reducing and motion-scaling functions, stable 3-D 10-fold magnification vision, and a better ergonomic work space. The application of robotics to urological, gynecological, vascular, and cardiac surgery has enhanced competence because of these features (10–15). Since 2000, robotic surgery has been applied to rectal resection in several
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institutes (10), but there remains a paucity of literature available on direct comparisons between open or laparoscopic surgery and robotic rectal surgery. Moreover, the existing research is heterogenous in terms of design, selection criteria of patients, and outcome measures, which makes it difficult to obtain clear conclusions. In this review article, we will provide an overview of the history, current applications, evidence from clinical studies, and future of robotic surgery for rectal cancer.
Background of Robots for Surgery The most prevalent platform for robotic surgery is currently the da Vinci Surgical System (Intuitive Surgical, Sunnyvale, USA). This system was approved by the US Food and Drug Administration in 1999, and since then, da Vinci models have changed periodically. As of June 2017, 4149 da Vinci series have been installed worldwide, including 538 in Asia (16). The da Vinci systems have been widely used for urological, gynecological, cardiothoracic, and gastrointestinal surgery. Total prostatectomy has been the most frequently performed robotic surgery to date because it leads to reduced blood loss, low complication rates, early postoperative recovery, a shorter hospital stay, reduced risk of neural damage, and early recovery of genitourological functions (17). Because the prostate and rectum are both located in the pelvis, robotic surgery is considered to be useful for rectal surgery, similar to urological surgery, which has a narrow surgical field. The da Vinci systems are not perfect surgical robots. A major drawback is the loss of tactile sensation. Surgeons cannot feel tension well, which increases the risks of perforation and injury. Tissue tension on sutures needs
Figure 1 The arrangement of surgical ports and docking of the patient cart. (a) The first docking. (b) The second docking. Dark arrows indicate the directions of instruments. A, assistant port; C, camera port; R, ports used by robot arms.
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to be gathered from visual information. The manufacturer developed surgical simulators and a dual-console system as training methods to compensate for this disadvantage. Several other limitations of robotic systems, such as a fixed operating table position and collisions between the robotic arms outside of the body, have been reported. The latest model, the da Vinci Xi, which was launched by the manufacturer in 2014, has an integrated table motion feature that can adjust the operating table without undocking. In addition, the overhead arrangement of thinner arms with additional joints maximizes access, minimizes collisions, shortens the console time, and enables single-dock multi-quadrant robotic surgery (18–20). Collectively, these features may give impetus to robotic surgery for rectal cancer.
Procedures of Robotic Anterior Resection with TME (in Our Institute) In this section, we describe our standardized method of surgical procedures for rectal surgery using the da Vinci system. We employ the dual-docking method for robotic rectal surgery. After pneumoperitoneum with an intraabdominal pressure of 10 mmHg is obtained, a 12-mm balloon trocar is inserted at the umbilicus for the camera. Following an examination of the intra-abdominal cavity for distant metastasis, another five ports are inserted. After mobilization of the small intestine, the patient cart is obliquely docked from the left caudal side of the patient (Figure 1a), and dissection around the inferior mesenteric artery under a medial-to-lateral approach and mobilization of the sigmoid colon are performed. When required, the splenic flexure is taken down. The cart is moved away and then docked again between the patient’s legs so that sharp dissection of the pre-hypogastric nerve fascia and behind Denonvilliers’ fascia can be performed while avoiding autonomic nerve injury during mobilization of the rectum (Figures 1b,2a). The rectum is transected more than 2 cm below the lower border of the tumor, thereby completing TME. When the lower border of the tumor is located distal to the peritoneal reflection and is found to have invaded beyond the muscularis propria (clinical T3 or T4, any N), lateral pelvic lymph node dissection (LLND) is considered. Bilateral LLND is performed on patients without preoperative (chemo)radiation therapy (CRT or RT), whereas after CRT/RT, selective LLND is indicated for patients who had clinically positive lymph nodes of the pelvic wall at the initial diagnosis (21). This procedure includes complete removal of the lymph nodes in the fat tissues outside the pelvic plexus and around the common iliac artery, internal iliac artery, and obturator space (Figure 2b), while preserving all autonomic nerves
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Figure 2 Intraoperative view of robotic rectal surgery. (a) Dissection just behind the mesorectum. (b) The lateral pelvic wall after lateral pelvic lymph node dissection. Ext., external; inf., inferior; sup., superior.
when they are not encased. The robotic surgery in LLND offers some possible advantages. A specimen is removed through the extended incision at the umbilicus after the proximal end of the tumorbearing segment has been divided extracorporeally. Anastomosis and drainage tube placement are performed via a conventional laparoscopic technique.
Intraoperative Outcomes In laparoscopic surgery for rectal cancer, a high conversion rate to open surgery (34%) was initially reported (22). Obesity, narrow pelvis, bulky tumor, mesorectum, and adhesions from previous surgery can lead to conversion to open method because of the limitations of the laparoscopic instruments. Postoperative complications and poor survival are associated with conversion in colon cancer (22,23), so it is also a critical issue to reduce the conversion rate in rectal cancer. Meta-analyses showed that the conversion rate was lower in robotic surgery for rectal cancer (range: 0%–7.3%) than in laparoscopic surgery (range, 0%–26.3%) (24–29). Many advantageous features of the robotic system appear to have contributed to the favorable result, and the
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difference was particularly prominent in surgery for lower rectal cancer, as reported by Ielpo et al. (robotic surgery conversion rate, 1.8%; laparoscopic surgery conversion rate, 9.2%) (30). However, if serious life-threatening intraoperative events occur (e.g. uncontrolled bleeding), the time needed to undock the robot for conversion to open laparotomy may result in a disastrous outcome (31). Several meta-analyses showed that robotic surgery was generally associated with longer operative times (27,29), whereas others concluded that there was no significant difference between robotic and laparoscopic surgery (25,26,28). These controversial conclusions appear to stem from various differences among institutions in terms of surgical procedures (e.g. full robotic vs hybrid surgery, routine takedown of the splenic flexure vs no mobilization, and single vs multiple dockings). The docking and separation procedure for a robotic cart is known to be time-consuming. However, operative times can be decreased if the robotic arms are positioned and the forceps are manipulated in a manner than avoids collisions (32). In addition, improvements to the robotic system itself, such as da Vinci Xi, will reduce repeated docking, which may result in shorter operative times. The operative time also depends on the learning curve of surgeons. Less experience is generally required for learning robotic surgery than conventional laparoscopic surgery. The learning curve for robotic rectal surgery is typically analyzed using the cumulative method. Transferring surgical skills from open surgery to the robotic approach may rapidly decrease the operative time during the first phase of the learning curve (33,34). The second phase allows for the consolidation of additional experience. The third phase is the post-learning period of surgery for more complex cases. Several institutes reported a markedly shorter learning curve for robotic surgery than for conventional laparoscopic surgery, which has a steep and long learning curve (35,36). In contrast, Park et al. did not observe differences in learning curves between conventional laparoscopic and robotic low anterior resection (37). Previous studies showed that estimated blood loss during procedures was similar between robotic and laparoscopic surgery (28,38,39), but some found a significantly lower volume of blood loss with the robotic than the laparoscopic approach (40).
Short-term Postoperative Outcomes Postoperative complications are important for discussing the safety of robotic surgery. Meta-analyses showed that there was no significant difference in the frequency of overall complications between robotic and conventional laparoscopic surgery (24–29). For example, anastomotic
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leakage, the most frequent complication, occurred in 2.4%–11.2% of cases that underwent conventional laparoscopic rectal surgery and in 1.8%–13.5% that underwent robotic surgery (27). There is no evidence of the superiority of robotic rectal surgery over laparoscopy in terms of the incidence of other postoperative complications (24–29). The time to normal diet was shown to be similar between robotic and conventional laparoscopic surgery (24–26,28), except for a few studies that reported a significant difference in favor of robotic surgery (39,41). Postoperative hospital stay was also similar between robotic and conventional laparoscopic surgery according to meta-analyses. However, some studies reported a shorter stay after robotic surgery, and others had the opposite finding (24–26,28,29). Surgical stress was evaluated subjectively and objectively in a few studies. Kang et al. showed that postoperative analgesic usage was lower after robotic surgery than after open surgery, and the visual analog scale score was significantly lower after robotic surgery than after laparoscopic surgery for rectal cancer (39). Kamali et al. similarly reported that robotic anterior resection was less painful than laparoscopic surgery based on the European Organisation for Research and Treatment of Cancer quality of life questionnaire (QLQ)-C30 questionnaires score (42). In our institute, immune responses were compared among patients who underwent open, laparoscopic, and robotic rectal surgery by evaluating Creactive protein levels, lymphocyte subset counts, and Human Leukocyte Antigen-D Related (HLA-DR) marker levels in blood samples. HLA-DR expression on monocytes, an index of immune competence, was higher on day 3 after robotic surgery than after open surgery, suggesting that robotic surgery is less invasive (43). These anecdotal findings need to be validated by evaluating different sets of patient cohorts.
Functional Outcomes Intraoperative injury to the pelvic autonomic nerves may result in urinary retention, sexual dysfunction, and fecal incontinence. The preservation of these nerves is a crucial component in rectal surgery in order to avoid anterior resection syndrome. However, only a few studies have examined this issue after robotic surgery. Park et al. reported earlier recovery of erectile function after robotic surgery than after conventional laparoscopic surgery (44). Kim et al. found earlier recovery of urinary function (i.e. 6 months after robotic surgery), but no significant difference was noted thereafter between the robotic and conventional laparoscopic approaches (45). Luca et al. stated that robotic surgery allows for the
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preservation of urinary and sexual functions after nervepreserving TME (46). However, most studies did not reveal any significant difference between the conventional laparoscopic and robotic approaches with regard to urinary retention, sexual disorders, and fecal incontinence after rectal surgery (27,38).
Oncological Outcomes The number of lymph nodes harvested, the distal resection margin, the circumferential resection margin, and the quality of the mesorectum are representative measures of the pathological quality of surgical resection. Meta-analyses have generally shown that there is no significant difference in these parameters between robotic and laparoscopic resection (24,25,27,29). Long-term outcome measures such as relapse-free survival and overall survival have not been extensively investigated. The heterogenous lengths of the follow-up periods in previous studies and the relatively short history of robotic rectal surgery make it difficult to address this issue. Park et al. reported that relapse-free survival and overall survival were similar between the laparoscopic and robotic approaches based on a median follow-up of 58 months (47).
Cost One main disadvantage of robotic surgery is the high costs associated with the purchase and maintenance of robot technology. The high capital and running costs of the robotic system have hindered its installation in many countries. In addition, health insurance systems do not necessarily cover the whole cost of robotic surgery, although this differs from nation to nation. Overall, robotic surgery is 1.5–3 times as expensive as laparoscopic surgery (27). Hottenrott projected that the disadvantage of the cost may be overcome by limiting the use of robotic surgery to specialized centers (48). In contrast, Byrn et al. reported that the accumulation of robotic cases will decrease costs (49). It may be important to identify patients who will obviously benefit from robotic surgery despite its high cost. Obesity, male sex, lower rectal cancer, and preoperative CRT represent selection criteria for robotic surgery that may help to justify its overwhelming cost (27,50).
Surgery Beyond Standard Rectal Surgery Intersphincteric resection (ISR) ISR is a relatively new sphincter-preserving surgical procedure for very low rectal cancer and anal canal cancer; it is an alternative to abdominoperineal resection, which
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is physically and mentally burdensome to the patient. Since Schiessel et al. first reported ISR in 1994 (51), the procedure has been widely accepted. However, it is difficult to perform ISR without causing functional anal deterioration and avoiding local recurrence (52,53). Because robot-assisted rectal surgery is beneficial for patients with lower rectal cancer, the need for ISR appears to be a good indication for the robotic approach. A Korean group confirmed that robotic ISR may be performed with oncological safety (54).
locally advanced rectal cancer in most Asian countries, including in Japan, where extended surgery without preoperative CRT is the standard treatment (68–70). LLND via conventional laparoscopy may be challenging with straight instruments. In contrast, robotic LLND is considered easier to perform because of its stable magnified view and multi-articulated forceps (71). Yamaguchi et al. reported that robotic LLND was superior to open surgery because of the lower rate of urinary retention (32).
Robotic surgery from a transanal approach
Pelvic exenteration
A transanal approach, such as transanal minimally invasive surgery for cancer very close to the anus, is increasingly attracting attention. Atallah et al. first described the usefulness of robotic-assisted transanal minimally invasive surgery for early cancer or benign neoplasms located near the anus (55). Moreover, transanal TME was recently introduced as a minimally invasive transanal procedure to facilitate difficult pelvic dissections. Several studies reported that transanal TME for distal mesorectal dissection achieved similar technical success to laparoscopic TME and offered acceptable oncologic and perioperative outcomes (56,57). Robotic surgery has also been applied for this manipulation technique from the perineal side for early-stage rectal cancers. Gómez Ruiz et al. demonstrated that the procedure was a feasible and safe option, but the follow-up period was short (58).
In patients with locally advanced rectal cancer invading adjacent organs such as the prostate and seminal vesicles, pelvic exenteration represents a treatment option. This extremely radical surgery may be performed using a robotic technique by experienced colorectal surgeons and urologists (72).
Ileal pouch-anal anastomosis (IPAA) Restorative proctocolectomy with IPAA is one of the standard procedures for inflammatory bowel disease. For the same reasons as robot-assisted ISR in patients with very lower rectal cancer, IPAA via a robotic approach may be beneficial for patients with inflammatory bowel disease-associated neoplasm. Pedraza et al. and our group recently reported patients with ulcerative colitis with dysplasia or cancer in the rectum who underwent robot-assisted restorative proctocolectomy with IPAA (59,60).
Conclusions The use of a robotic approach has attracted increasing attention in the field of pelvic surgery, including rectal surgery. This technique appears to overcome most of the limitations of conventional laparoscopic surgery. The precise procedures provided by this new technology are in demand for surgery performed in a narrow space such as the pelvis. Although we are still at the dawn of robotic-assisted rectal surgery, its technical safety and oncological safety have been proven. Moreover, the similar outcomes achieved by the robotic and conventional laparoscopic approaches suggest the potential superiority of robotic surgery in rectal cancer because surgeons are more likely to prefer robotic surgery for more challenging lesions. However, the related cost may restrict its use to patients with features that absolutely demand robotic techniques. More evidence is needed to confirm the benefits of robotic rectal surgery. The potential benefits will be addressed by ongoing phase 3 prospective randomized controlled trials such as the robotic versus laparoscopic resection for rectal cancer (ROLLAR trial) and the comparison of laparoscopic versus robot-assisted for rectal cancer (COLRAR trial) (73,74).
Lateral pelvic lymph node dissection (LLND) Locally advanced rectal cancer may metastasize to the lymph nodes of the pelvic wall, with frequencies reported to be 15%–20% (61–65). Even after preoperative CRT, they do not necessarily diminish. Recent studies suggested that LLND reduces local recurrence and improves survival rates (66,67). Therefore, LLND represents a crucial element in the surgical procedure for
Acknowledgments Toshiaki Watanabe received lecture fees from Intuitive Surgical, Covidien, Olympus, and Johnson & Johnson. Hiroaki Nozawa has no conflicts of interest to declare in association with the present study. This work was supported by Grants-in-Aids for Scientific Research from the Japan Society for the Promotion
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of Science (A, no.16H02672; C, no.17K10621) and from the Japan Agency for Medical Research and Development’s Project for Cancer Research and Therapeutic Evolution (no. 16cm0106502h0001).
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