1Department of General and Digestive Surgery,
2Department of General and Digestive Surgery,
Correspondence Address: Dr. Aleix Martínez-Pérez, Department of General and Digestive Surgery, Hospital Universitario Doctor Peset, Avenida Gaspar Aguilar 90, Valencia 46017, Spain. E-mail: firstname.lastname@example.org
© The Author(s) 2019. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, sharing, adaptation, distribution and reproduction in any medium or format, for any purpose, even commercially, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
Minimally-invasive conventional up-to-down laparoscopic approach is a widespread alternative for rectal cancer resection. Its potential benefits towards open surgery have been shown to rely, however, at secondary clinical outcomes, and its oncological non-inferiority compared with the traditional open approach has not been demonstrated yet. In this scenario, robotic-assisted minimally-invasive rectal resection has gained increasing popularity and promising expectancies. This narrative review aims to assemble the most updated evidence available and to discuss the future perspectives and challenges for this emergent surgical tool. The main benefit over conventional laparoscopy appears to be a reduction of conversion rates to open surgery, whereas the oncologic and functional outcomes seem similar than the other alternatives. Increased costs are the main limitation of the widespread of robotic technology. Low quality of the current evidence is remarkable.
Rectal cancer, total mesorectal excision, robotic surgery, minimally-invasive surgery
In 2018, colorectal cancer (CRC) was the third most commonly diagnosed cancer (10.2%), and the second leading cause of cancer death (9.2%). Nearby two million of new CRC cases and more than 800,000 deaths were estimated to occur worldwide in 2018. Surgery remains as the mainstay treatment for rectal cancer, improvements on the outcomes have been observed since the introduction and widespread of the principles of total mesorectal excision (TME). Preoperative radiotherapy and chemotherapy have a major role in the treatment of locally advanced rectal tumors. To perform an accurate mesorectal dissection achieving clean margins is mandatory for rectal resections. Obtaining both negative circumferential resection margin (CRM-) and a complete mesorectal excision is associated with lower recurrence rates an improved long-term survival[4-10].
Laparoscopic rectal surgery was introduced shortly after 1990. The earliest large randomized controlled trials (RCT) comparing conventional laparoscopic and open approaches for rectal cancer showed that the use of laparoscopy was associated with a lower blood loss, an earlier return of bowel movement, and a shorter length of hospital stay[11-14]. Further studies questioned the oncological safety of the approach, by means of obtaining a complete mesorectal quality or a composite pathologic outcome associating also free circumferential and distal margins[15-17]. Remarkably, the observed impairment should be reflected in the long-term oncologic prognosis in order to reach any clinical interest. The question remains still open after the publication of the mid-term (2-year) results of the latest trials[18-20]. Conventional laparoscopic instruments may not be appropriate for assuring the achievement of the best plane of dissection in all patients, especially in those with the narrow or irradiated pelvis. Due to this, TME seems to be one of the procedures in which the robotic assistance will have a critical role[22-25].
At the time of the present review, the ROLARR study was the largest RCT comparing robotic-assisted vs. conventional laparoscopic surgery for patients with rectal cancer. Two recent systematic reviews with meta-analyses summarized the outcomes from 7 and 5 RCTs with a similar design[27,28]. Other meta-analyses have been published including also non-randomized clinical trials[29,30]. No guidelines are now available suggesting the true role of robotics in colorectal surgery, high-quality clinical data is similarly lacking. In the present review, we dissected the current status of robotic TME, with special emphasis on surgical outcomes and near future perspectives.
A robot is a device that can be programmed to carry out a task, being controlled by mechanical and computing systems. The concept of robotic surgery appeared in the 1970s as a military project of the Defense Advanced Research Project Administration endorsed by the National Aeronautics and Space Administration aiming to keep the surgeon from the battlefield. In 1985, a robot was introduced into an operating theatre, an industrial robotic arm (PUMA 200) was modified to perform a preprogrammed intracranial biopsy. Shortly thereafter, the PROBOT® and ROBODOC® systems were developed, designed for transurethral prostatic resections and total hip arthroplasties, respectively[33,34]. The earliest systems required prior task programming, implying longer procedure duration and poor response to unexpected events. At the end of the 20th century, the way of conceiving abdominal surgery changed by the introduction of laparoscopy. The first laparoscopic colorectal surgery was performed in 1990 by Fowler. In 1994, the automated endoscopic system for optimal positioning was the first real-time surgical manipulation system being commercialized. It consisted of an endoscope attached to a voice-controlled mechanical arm that modified its position following surgeon’s orders. It allowed greater image stability and sometimes dispensed the need for an assistant but provided longer operative time compared with conventional laparoscopy[36,37].
In 2000, ZEUS® (Computer Motion, Goleta, California, USA), a three-armed robot mounted on the operating table; and the da Vinci® robot (Intuitive Surgical, Sunnyvale, California, USA) were developed. In 2003 Computer Motion was incorporated into Intuitive Surgical. The da Vinci® system provided a fourth arm and an independent console where the surgeon has a three-dimensional view of the field. Specifically designed devices with Endowrist® technology allow for 7º of freedom, 180º articulation and 540º rotation. The latest release to date, the Xi version, appeared in 2014. It offers the possibility of adjusting the operating table without undocking the system, shortening the procedure length and allowing multi-quadrant single-docking procedures. Augmented-reality software allows the assessment of intestinal perfusion or real-time three-dimensional (3D) anatomical simulation of abdominal structures[39-41]. Senhance® Surgical Robotic System and the REVO-I® Robot Platform are the two other systems commercially available nowadays. Competitive industry players like Medtronic and Verb surgical (powered by GOOGLE® and Johnson & Johnson®) platforms are expected soon.
The learning curve for robotic TME, from the beginning to the higher expertise, should include at least 20-23 cases, which is faster than for conventional laparoscopy[43,44]. Contrasting results have been reported regarding the impact of the previous proficiency on laparoscopy on the duration of the period[45,46]. Most of the publications evaluated the expertise with variables as “operative time”, “bleeding” or “conversion” which may not be the most critical outcomes. There is a wide agreement on the fact that operative times are longer during a learning curve, but a recent study on robotic rectal resection showed no relationship between extended operative time and morbidity. The evaluation of the experience in oncologic surgery should also focus on the quality of the resected specimen, especially for rectal cancer resection. Only a recent meta-analysis showed no significant differences in CRM involvement between learning and competent surgeons. The authors did not found significant differences in the other clinic and pathologic variables, without evaluating the quality of the TME.
A learning curve is unavoidable, and robotic surgery requires special training and the development of new skills. The companies responsible for robotic systems are compelled by the Food and Drug Agency to develop technical training for the surgeons. The European Association of Endoscopic Surgeons (EAES) recommended a training officially-certified and based on a formal curriculum for skills and procedures. The lack of standardization in robotic rectal surgery was specifically noted, this is critical to assure the safety and success of training surgeons in their future practice. Recent resources aim to provide an objective assessment of the acquired surgical skills to produce future standards for robotic surgeons on basic knowledge and procedural safety. If any superiority favouring robotic TME is proven soon, the learning curve should not be an obstacle, but a necessary step for novel surgeons to reach the standards of quality. Noteworthy, there is an underlying and not despicable risk if surgeons abandon conventional laparoscopic surgery learning in favour of robotics. We may have soon a generation of surgeon incapable of performing laparoscopic surgery, with unclear but potentially serious consequences.
Current robotic platforms display a 3D image, enhancing the visualization of the anatomical structures by improving the surgeon’s depth perception and image quality. Compared to conventional laparoscopy, robotic surgery also allows to control a stable camera. The system has recently incorporated the EndoWrist® technology, which improves dexterity and eliminates physiological tremor reducing the challenge of laparoscopic intra-corporeal suturing. These technical advantages are expected to allow a better mesorectal dissection, preserving the integrity of the fascia and decreasing the odds of autonomic nerve injury resulting in sexual dysfunction, anterior resection syndrome, or urinary retention.
The use of robotic platforms is associated with better surgeon’s ergonomics than those provided by conventional laparoscopy. Robotic assistance results in lesser activation of the upper-body mussels reducing musculoskeletal discomfort. Berguer et al. reported that robotic help makes less stressful performing complex tasks. Previous laparoscopic experience has a complex influence on the adaptation to the new approach. Tele-surgery is the latest potential advantage of robotic surgery, allowing real-time international collaborations and mentoring.
The loss of haptic feedback is still the main technical limitation of the available robotic platforms. A multi-modal pneumatic feedback system offering tactile, kinesthetic, and vibrotactile feedback was incorporated in the da Vinci® Surgical System. Other platforms, as Senhance® Surgical Robotic System and the REVO-I® Robot Platform, also incorporated haptic feedback assistance.
Increased costs attributed to robotic surgery are the most important current impediment for the widespread of this technology. The economic impact is an important point to assess in the setting of increasing demands on limited health resources. To accurately measure costs has a particular difficulty at economic evaluations. Total costs rely on direct, indirect and intangible costs. Direct costs can be divided into fixed costs (to buy and maintain the robotic system), and variable costs (consumable instruments). The cost of a robotic platform is $1-$2.3 million. Cost-analysis studies determined that robotic is more expensive than open and laparoscopic surgeries[57,58]. Baek et al. in 2012, reported that robotic rectal surgery charges were between $7,150-10,700, and $1,240 for laparoscopic surgery. The ROLARR trial showed that health-care costs in the robotic-assisted laparoscopic group (£11 853 or $13 668) were higher than in the conventional laparoscopic group (£10 874 or $12 556). The higher costs were attributed to longer theater occupation and the use of specific instruments. Conversely, Ielpo et al. found that the mean overall costs were similar between robotic and laparoscopic approach, excluding the initial purchase of the robotic system.
Few studies have assessed the cost-effectiveness of robotic rectal surgery, it is difficult to assign a monetary value to the measured outcomes in this particular scenario. Morelli et al. observed that excluding fixed costs and comparing experienced phase of robotic surgery with the laparoscopic approach, the variable operative costs were similar. Therefore, robotic expertise has a critical role in the operative costs, similar to the procedures standardization, the surgical team’s consistency, and the institution’s volume. Robotic surgery could mitigate increased expenditures whether provide lesser risk of conversion and shorter hospitalization[29,63]. Indirect costs have not been deeply evaluated for robotic rectal resections. Only Bertani et al. found a faster physical recovery after 1 month in the robotic group compared with open surgery. The ROLARR did not found differences between laparoscopic and robotic surgery in bladder and sexual dysfunction rates. No cost-utility study aiming to determine indirect costs has been reported to date. Further research is needed to evaluate the quality of life; including sexual, stool, and urinary functions, using utility measures like the disability-adjusted life-year and the quality-adjusted life-year, to accurately compare the outcomes of the different surgical alternatives. For the latest 20 years, da Vinci® System has dominated robotic surgery, the lack of adversaries led to rising costs and maybe slowed the evolution of the technology. In the near future, with the introduction of new robotic platforms, this situation is expected to change dramatically.
Some authors suggested the potential advantage of robotic TME over conventional laparoscopy decreasing the conversion rates to open surgery: Prete et al. [Risk Ratio (RR), 0.58; 95%CI: 0.35-0.97; P = 0.04], Jones et al. [Odds Ratio (OR), 0.40; 95%CI: 0.29-0.55; P < 0.00001], Ohtani et al. (OR, 0.30; 95%CI: 0.19-0.46; P < 0.00001), and Lee et al. (RR, 0.28; 95%CI: 0.15-0.54; P < 0.0001)[28,29,64,65]. The benefit has been related to the use of three-dimensional vision and articulated instruments, facilitating the dissection during TME. The ROLARR study, however, only found benefits in the men subgroup. Although the study found no significant differences in the rest of the short-term outcomes being evaluated, trial’s sample estimation, and the varying expertise on robotics of the participating surgeons assured the debate after its publication. Existing research demonstrated longer operative time for robotics compared with open and laparoscopic rectal resections[28,65,66]. Ohtani et al. reported an operative time 44 minutes greater than laparoscopy [weighted mean difference (MD), 44.80; 95%CI: 28.44-61.15; P < 0.00001]. Lee et al. showed no differences in operative time between robotic and transanal-TME. Other studies reported less blood loss for robotic TME, compared with the open and laparoscopic approaches[68,69]. Intraoperative complications were found similar for robotic surgery when compared with the open and laparoscopic approaches[26,66].
Anastomotic leak rate was not significantly different for robotics compared with open and laparoscopic operations[28,69]. Laparoscopic, transanal, and robotic TME also showed similar leak and reoperation rates[67,70]. Postoperative ileus, wound infection, and urinary retention were similar between open, laparoscopic, transanal procedures in comparison with robotic approach[30,65,69]. Length of hospital stay was shorter after robotic surgery compared with open (7.5 days vs. 13.24 days)[66,69], but no difference was found when comparing it with conventional laparoscopy[28,70]. Perioperative complications and mortality rates appear to be similar for all four approaches[28,30,69]. Mortality is low in elective rectal surgery, with only 2 cases in each arm among 466 patients (0.9%) in the ROLARR study.
As robotic assistance seems to facilitate mesorectal dissection, particularly in mid and low rectal tumours, a reduced rate of positive CRM+ was presupposed to be one of the major benefits conferred by the novel technology. However, different studies showed that CRM+ is similar when compared with the other techniques. Jayne et al. reported no statistically significant differences in the odds of CRM+ between robotic and laparoscopic groups (OR, 0.78; 95%CI: 0.35-1.76; P = 0.56). Accordingly, a propensity adjusted analysis of 7616 patients support both for the resection of locally advanced rectal cancer, with equivalent CRM- rates (93% vs. 94%; 95%CI: 0.69-1.06).
The completeness of the mesorectal resection became a valuable item to assess the oncologic safety of a rectal resection and predicts tumor recurrence in the pelvis. Rausa et al. showed no significant differences in complete, near-complete or incomplete mesorectal excision between laparoscopic and robotic approaches (complete RR, 0.8; 95%CI: 0.7-1.0; nearly-complete RR, 1.6; 95%CI: 0.9-2.7; incomplete RR, 1.5; 95%CI: 0.8-2.5).
Liao et al. associated the robotic approach with a longer distance to the distal margin in comparison with laparoscopy (MD, 0.83 cm, 95%CI: 0.29-1.37; P = 0.003). When comparing robotic and open surgeries, no differences were found (MD, 0.17; 95%CI: -0.14 to 0.48; P = 0.27).
Truong et al. analysed a retrospective cohort of patients looking at successful resections, defined as a circumferential and distal resection margins < 1 mm and complete mesorectal resection, which were similar between the robotic (75%) and open (76%) approaches. There were no differences in the studies comparing all four approaches for rectal cancer regarding the number of lymph nodes retrieved[26,27,30,69].
Local recurrence rates were similar between laparoscopic vs. robotic (RR, 1.4; 95%CI: 0.7-2.4) and transanal-TME vs. robotic (RR, 1.4; 95%CI: 0.5-3.4) in the meta-analysis performed by Rausa et al.. Moreover, Ohtani et al. also reported no differences in terms of local, metastatic, and overall recurrences, 3-year OS and 3-year DFS between robotic and laparoscopic approaches. In their recent meta-analysis, Liao et al. described the OS and DFS after a mean follow-up of 29.2 months in the robotic group and 18.7 months in the laparoscopic group. The OS was 100% in the robotic group and 94.1% in the laparoscopic group. The DFS was 100% in the robotic group and 88.2% in the laparoscopic group. Studies comparing robotic and open resections also found non-significant long-term outcomes between them. Five-year DFS was 73.2% and 69.5% in the robotic and open groups, respectively. Five-year OS was 85.0% in the robotic and 76.1% in the open approach.
Two trials evaluated the urinary function of using the International Prostate Symptom Score (I-PSS) comparing robotic and laparoscopy TME. Lee et al. showed improved urinary continence for robotic surgery at 3 months, but there was no statistical difference on I-PSS at 6 or 12 months after surgery. Erectile dysfunction rates did not differ between robotic and laparoscopic groups (OR, 0.54; 95%CI: 0.19-1.58; P = 0.26). Somashekhar et al. analyzed erectile dysfunction and retrograde ejaculation using the European Organization for Research and Treatment of Cancer questionnaire QLQ-C38. A total of 18 % of male patients in the robotic group and 26% in the open group had sexual dysfunction. Li et al. published a meta-analysis reporting lesser incidence of urinary retention using robotic TME. The ROLARR trial evaluated bladder function, male sexual function and female sexual function separately by using I-PSS, International Index of Erectile Function and Female Sexual Function Index, respectively. This study did not find any differences between laparoscopic and robotic surgery after 6-months follow-up.
Near-infrared (NIR) light (650-900 nm) has optimum characteristics for in vivo imaging, resulting in higher penetration depth and minimum background auto-fluorescence. Indocyanine green (ICG) is the only available fluorophore in the NIR window, it is confined into the vascular compartment through binding plasmatic proteins presenting low toxicity. The applications of ICG are increasing, especially at colorectal cancer surgery. NIR has been used for assessing tissue perfusion and to detect sentinel nodes, peritoneal carcinomatosis, or liver metastases[77-80]. Anastomotic leak remains as the main complication in colorectal surgery, ischemia of intestinal stumps constitutes a major risk factor[81,82]. To determine the viability of the intestinal stumps when performing the anastomosis may decrease the odds of leak development. The earliest RCT on the subject just showed a reduction (9% vs. 5%), but non-significant, of the anastomotic leak rate in the fluorescence arm after colorectal resection. Only two retrospective studies have been conducted using robotic technology[84,85].
The “enhanced permeability and retention” effect is the mechanism involved. It reflects the affinity of ICG towards tumoral and near-tumoral tissue due to neovascularization. Few studies are trying to elucidate the role of ICG in carcinomatosis, with contrasting results[79,86]. Neoadjuvant therapy with bevacizumab decreases the sensitivity of ICG to detect peritoneal metastases of colorectal cancer. Mucinous metastases cannot be identified with ICG. A recent RCT comparing the use of white light versus NIR and ICG showed increasing sensitivity from 80% to 96%. ICG can be alternatively used to improve surgical safety when marking important structures, as the ureters or the hepatic ducts, and even for tattooing colonic neoplasms instead of ink.
Over the last few years, the transanal approach gained popularity as seemed to facilitate complex pelvic dissections. Several studies reported that Ta-TME achieved similar technical success and perioperative outcomes than laparoscopic TME, with a lower conversion rate. Recent studies also showed that serious complications secondary to wrong down-to-up dissection planes were not despicable, same for anastomotic leaks. To improve the accuracy of the transanal dissection, robotic technology could also be helpful. Two surgical teams (abdominal and perineal) can work together with the new platforms. At present, however, further investigations are still needed to assure the long-term functional, and more critically, the oncological outcomes of the transanal approach for resecting rectal tumors.
The use of robotic assistance provides interesting improvements that may overcome some of the technical limitations of conventional laparoscopic instruments. Acceptable oncologic outcomes have been similarly reported. Increased costs, poor availability, and special training requirements are still important barriers to be overcome. Surgeons and health-care providers should notice that no important benefits have been yet demonstrated for robotic TME compared with the other available surgical alternatives. The combination of emerging technology, technical refinements, and an optimal trainee learning system may allow robotic surgery to be a gold standard for rectal cancer in the near future.
Concept and design: Sebastián-Tomás JC, García-Granero E, Martínez-Pérez A
Collection and assembly of data: Sebastián-Tomás JC, Santarrufina-Martínez S, Navarro-Martínez S, Gonzálvez-Guardiola P, Martínez-López E, Payá-Llorente C
Provision of study materials or patients, data analysis and interpretation, manuscript writing and final approval: All authorsAvailability of data and materials
Not applicable.Financial support and sponsorship
None.Conflicts of interest
All authors declared that there are no conflicts of interest.Ethical approval and consent to participate
Not applicable.Consent for publication
© The Author(s) 2019.
1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394-424.DOIPubMed
2. Heald RJ, Husband EM, Ryall RD. The mesorectum in rectal cancer surgery--the clue to pelvic recurrence? Br J Surg 1982;69:613-6.DOIPubMed
3. De Caluwe L, Van Nieuwenhove Y, Ceelen WP. Preoperative chemoradiation versus radiation alone for stage II and III resectable rectal cancer. Cochrane Database Syst Rev 2013:CD006041.DOIPubMed
4. Quirke P, Steele R, Monson J, Grieve R, Khanna S, et al. Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG CO16 randomised clinical trial. Lancet 2009;373:821-8.DOIPubMedPMC
5. Leonard D, Penninckx F, Laenen A, Kartheuser A; Procare. Scoring the quality of total mesorectal excision for the prediction of cancer-specific outcome. Colorectal Dis 2015;17:O115-22.DOIPubMed
6. Kitz J, Fokas E, Beissbarth T, Strobel P, Wittekind C, et al. Association of plane of total mesorectal excision with prognosis of rectal cancer: secondary analysis of the CAO/ARO/AIO-04 Phase 3 randomized clinical trial. JAMA Surg 2018;153:e181607.DOIPubMedPMC
7. Kusters M, Marijnen CA, van de Velde CJ, Rutten HJ, Lahaye MJ, et al. Patterns of local recurrence in rectal cancer; a study of the Dutch TME trial. Eur J Surg Oncol 2010;36:470-6.DOIPubMed
8. Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol 2008;26:303-12.DOIPubMed
9. Birbeck KF, Macklin CP, Tiffin NJ, Parsons W, Dixon MF, et al. Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg 2002;235:449-57.DOIPubMedPMC
10. Garcia-Granero E, Faiz O, Munoz E, Flor B, Navarro S, et al. Macroscopic assessment of mesorectal excision in rectal cancer: a useful tool for improving quality control in a multidisciplinary team. Cancer 2009;115:3400-11.DOIPubMed
11. van der Pas MH, Haglind E, Cuesta MA, Furst A, Lacy AM, et al. Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 2013;14:210-8.DOIPubMed
12. Kang SB, Park JW, Jeong SY, Nam BH, Choi HS, et al. Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol 2010;11:637-45.DOIPubMed
13. Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 2005;365:1718-26.DOIPubMed
14. Martinez-Perez A, Carra MC, Brunetti F, de’Angelis N. Short-term clinical outcomes of laparoscopic vs open rectal excision for rectal cancer: A systematic review and meta-analysis. World J Gastroenterol 2017;23:7906-16.DOIPubMedPMC
15. Fleshman J, Branda M, Sargent DJ, Boller AM, George V, et al. Effect of laparoscopic-assisted resection vs open resection of Stage II or III rectal cancer on pathologic outcomes: the ACOSOG Z6051 randomized clinical trial. JAMA 2015;314:1346-55.DOIPubMedPMC
16. Stevenson AR, Solomon MJ, Lumley JW, Hewett P, Clouston AD, et al. Effect of laparoscopic-assisted resection vs open resection on pathological outcomes in rectal cancer: the ALaCaRT randomized clinical trial. JAMA 2015;314:1356-63.DOIPubMed
17. Martinez-Perez A, Carra MC, Brunetti F, de’Angelis N. Pathologic outcomes of laparoscopic vs open mesorectal excision for rectal cancer: a systematic review and meta-analysis. JAMA Surg 2017;152:e165665.DOIPubMed
18. Fleshman J, Branda ME, Sargent DJ, Boller AM, George VV, et al. Disease-free survival and local recurrence for laparoscopic resection compared with open resection of Stage II to III rectal cancer: follow-up results of the ACOSOG Z6051 randomized controlled trial. Ann Surg 2019;269:589-95.DOIPubMedPMC
19. Stevenson ARL, Solomon MJ, Brown CSB, Lumley JW, Hewett P, et al. Disease-free survival and local recurrence after laparoscopic-assisted resection or open resection for rectal cancer: the australasian laparoscopic cancer of the rectum randomized clinical trial. Ann Surg 2019;269:596-602.DOIPubMed
20. Martinez-Perez A, de’Angelis N. Comment on “Mid-term results of ACOSOG Z6051 trial sustain the unresolved debate”. Ann Surg 2019;270:e52-3.DOIPubMed
21. Petrucciani N, Martinez-Perez A, Bianchi G, Memeo R, Brunetti F, et al. The use of laparoscopy for locally advanced rectal cancer. Minerva Chir 2018;73:77-92.DOIPubMed
22. de’Angelis N, Lizzi V, Azoulay D, Brunetti F. Robotic versus laparoscopic right colectomy for colon cancer: analysis of the initial simultaneous learning curve of a surgical fellow. J Laparoendosc Adv Surg Tech A 2016;26:882-92.DOIPubMed
23. Ahmed J, Nasir M, Flashman K, Khan J, Parvaiz A. Totally robotic rectal resection: an experience of the first 100 consecutive cases. Int J Colorectal Dis 2016;31:869-76.DOIPubMed
24. de’Angelis N, Portigliotti L, Azoulay D, Brunetti F. Robotic surgery: a step forward in the wide spread of minimally invasive colorectal surgery. J Minim Access Surg 2015;11:285-6.DOIPubMedPMC
25. de’Angelis N, Portigliotti L, Brunetti F. Robot-assisted rectal cancer surgery deserves a fair trial. Colorectal Dis 2015;17:824-5.DOIPubMed
26. Jayne D, Pigazzi A, Marshall H, Croft J, Corrigan N, et al. Effect of robotic-assisted vs conventional laparoscopic surgery on risk of conversion to open laparotomy among patients undergoing resection for rectal cancer: the ROLARR randomized clinical trial. Jama 2017;318:1569-80.DOIPubMedPMC
27. Liao G, Zhao Z, Deng H, Li X. Comparison of pathological outcomes between robotic rectal cancer surgery and laparoscopic rectal cancer surgery: A meta-analysis based on seven randomized controlled trials. Int J Med Robot 2019;15:e2027.DOIPubMed
28. Prete FP, Pezzolla A, Prete F, Testini M, Marzaioli R, et al. Robotic versus laparoscopic minimally invasive surgery for rectal cancer: a systematic review and meta-analysis of randomized controlled trials. Ann Surg 2018;267:1034-46.DOIPubMed
29. Jones K, Qassem MG, Sains P, Baig MK, Sajid MS. Robotic total meso-rectal excision for rectal cancer: a systematic review following the publication of the ROLARR trial. World J Gastrointest Oncol 2018;10:449-64.DOIPubMedPMC
30. Rausa E, Bianco F, Kelly ME, Aiolfi A, Petrelli F, et al. Systemic review and network meta-analysis comparing minimal surgical techniques for rectal cancer: quality of total mesorectum excision, pathological, surgical, and oncological outcomes. J Surg Oncol 2019;119:987-98.DOIPubMed
31. Diana M, Marescaux J. Robotic surgery. Br J Surg 2015;102:e15-28.DOIPubMed
32. George EI, Brand TC, LaPorta A, Marescaux J, Satava RM. Origins of robotic surgery: from skepticism to standard of care. JSLS 2018;22:e2018.00039.DOIPubMedPMC
33. Bargar WL, Bauer A, Borner M. Primary and revision total hip replacement using the robodoc system. Clin Orthop Relat Res 1998:82-91.DOIPubMed
34. Harris SJ, Arambula-Cosio F, Mei Q, Hibberd RD, Davies BL, et al. The probot--an active robot for prostate resection. Proc Inst Mech Eng H 1997;211:317-25.DOIPubMed
35. Fowler DL, White SA. Laparoscopy-assisted sigmoid resection. Surg Laparosc Endosc 1991;1:183-8.PubMed
36. Kraft BM, Jager C, Kraft K, Leibl BJ, Bittner R. The AESOP robot system in laparoscopic surgery: increased risk or advantage for surgeon and patient? Surg Endosc 2004;18:1216-23.DOIPubMed
37. Cheng CL, Rezac C. The role of robotics in colorectal surgery. BMJ 2018;360:j5304.DOIPubMed
38. Nozawa H, Watanabe T. Robotic surgery for rectal cancer. Asian J Endosc Surg 2017;10:364-71.DOIPubMed
39. Gorpas D, Phipps J, Bec J, Ma D, Dochow S, et al. Autofluorescence lifetime augmented reality as a means for real-time robotic surgery guidance in human patients. Sci Rep 2019;9:1187.DOIPubMedPMC
40. Atallah S, Parra-Davila E, Melani AGF, Romagnolo LG, Larach SW, et al. Robotic-assisted stereotactic real-time navigation: initial clinical experience and feasibility for rectal cancer surgery. Tech Coloproctol 2019;23:53-63.DOIPubMed
41. Porpiglia F, Checcucci E, Amparore D, Autorino R, Piana A, et al. Augmented-reality robot-assisted radical prostatectomy using hyper-accuracy three-dimensional reconstruction (HA3D) technology: a radiological and pathological study. BJU Int 2019;123:834-45.DOIPubMed
42. Andolfi C, Umanskiy K. Appraisal and current considerations of robotics in colon and rectal surgery. J Laparoendosc Adv Surg Tech A 2019;29:152-8.DOIPubMed
43. Huang CW, Yeh YS, Ma CJ, Choy TK, Huang MY, et al. Robotic colorectal surgery for laparoscopic surgeons with limited experience: preliminary experiences for 40 consecutive cases at a single medical center. BMC Surg 2015;15:73.DOIPubMedPMC
44. Jimenez-Rodriguez RM, Rubio-Dorado-Manzanares M, Diaz-Pavon JM, Reyes-Diaz ML, Vazquez-Monchul JM, et al. Learning curve in robotic rectal cancer surgery: current state of affairs. Int J Colorectal Dis 2016;31:1807-15.DOIPubMed
45. Odermatt M, Ahmed J, Panteleimonitis S, Khan J, Parvaiz A. Prior experience in laparoscopic rectal surgery can minimise the learning curve for robotic rectal resections: a cumulative sum analysis. Surg Endosc 2017;31:4067-76.DOIPubMed
46. Foo CC, Law WL. The learning curve of robotic-assisted low rectal resection of a novice rectal surgeon. World J Surg 2016;40:456-62.DOIPubMed
47. Mohd Azman ZA, Kim SH. A review on robotic surgery in rectal cancer. Transl Gastroenterol Hepatol 2016;1:5.DOIPubMedPMC
48. Duchalais E, Machairas N, Kelley SR, Landmann RG, Merchea A, et al. Does prolonged operative time impact postoperative morbidity in patients undergoing robotic-assisted rectal resection for cancer? Surg Endosc 2018;32:3659-66.DOIPubMed
49. Gachabayov M, You K, Kim SH, Yamaguchi T, Jimenez-Rodriguez R, et al. Meta-analysis of the impact of the learning curve in robotic rectal cancer surgery on histopathologic outcomes. Surg Technol Int 2019;34:139-55.PubMed
50. Szold A, Bergamaschi R, Broeders I, Dankelman J, Forgione A, et al. European association of endoscopic surgeons (EAES) consensus statement on the use of robotics in general surgery. Surg Endosc 2015;29:253-88.DOIPubMed
51. Baek SJ, Kim SH. Robotics in general surgery: an evidence-based review. Asian J Endosc Surg 2014;7:117-23.DOIPubMed
52. Zihni AM, Ohu I, Cavallo JA, Cho S, Awad MM. Ergonomic analysis of robot-assisted and traditional laparoscopic procedures. Surg Endosc 2014;28:3379-84.DOIPubMed
53. Berguer R, Smith W. An ergonomic comparison of robotic and laparoscopic technique: the influence of surgeon experience and task complexity. J Surg Res 2006;134:87-92.DOIPubMed
54. Choi PJ, Oskouian RJ, Tubbs RS. Telesurgery: past, present, and future. Cureus 2018;10:e2716.DOIPubMedPMC
55. Abiri A, Pensa J, Tao A, Ma J, Juo YY, et al. Multi-Modal haptic feedback for grip force reduction in robotic surgery. Sci Rep 2019;9:5016.DOIPubMedPMC
56. Rao PP. Robotic surgery: new robots and finally some real competition! World J Urol 2018;36:537-41.DOIPubMed
57. Bertani E, Chiappa A, Biffi R, Bianchi PP, Radice D, et al. Assessing appropriateness for elective colorectal cancer surgery: clinical, oncological, and quality-of-life short-term outcomes employing different treatment approaches. Int J Colorectal Dis 2011;26:1317-27.DOIPubMed
58. Baek SJ, Kim SH, Cho JS, Shin JW, Kim J. Robotic versus conventional laparoscopic surgery for rectal cancer: a cost analysis from a single institute in Korea. World J Surg 2012;36:2722-9.DOIPubMed
59. Ielpo B, Duran H, Diaz E, Fabra I, Caruso R, et al. Robotic versus laparoscopic surgery for rectal cancer: a comparative study of clinical outcomes and costs. Int J Colorectal Dis 2017;32:1423-9.DOIPubMed
60. Kim CW, Baik SH, Roh YH, Kang J, Hur H, et al. Cost-effectiveness of robotic surgery for rectal cancer focusing on short-term outcomes: a propensity score-matching analysis. Medicine (Baltimore) 2015;94:e823.DOIPubMedPMC
61. Morelli L, Guadagni S, Lorenzoni V, Di Franco G, Cobuccio L, et al. Robot-assisted versus laparoscopic rectal resection for cancer in a single surgeon’s experience: a cost analysis covering the initial 50 robotic cases with the da Vinci Si. Int J Colorectal Dis 2016;31:1639-48.DOIPubMed
62. Biffi R, Luca F, Bianchi PP, Cenciarelli S, Petz W, et al. Dealing with robot-assisted surgery for rectal cancer: Current status and perspectives. World J Gastroenterol 2016;22:546-56.DOIPubMedPMC
63. Cleary RK, Mullard AJ, Ferraro J, Regenbogen SE. The cost of conversion in robotic and laparoscopic colorectal surgery. Surg Endosc 2018;32:1515-24.DOIPubMed
64. Ohtani H, Maeda K, Nomura S, Shinto O, Mizuyama Y, et al. Meta-analysis of robot-assisted versus laparoscopic surgery for rectal cancer. In Vivo 2018;32:611-23.DOIPubMedPMC
65. Lee SH, Lim S, Kim JH, Lee KY. Robotic versus conventional laparoscopic surgery for rectal cancer: systematic review and meta-analysis. Ann Surg Treat Res 2015;89:190-201.DOIPubMedPMC
66. Somashekhar SP, Ashwin KR, Rajashekhar J, Zaveri S. Prospective randomized study comparing robotic-assisted surgery with traditional laparotomy for rectal cancer-Indian study. Indian J Surg 2015;77:788-94.DOIPubMedPMC
67. Lee L, de Lacy B, Gomez Ruiz M, Liberman AS, Albert MR, et al. A multicenter matched comparison of transanal and robotic total mesorectal excision for mid and low-rectal adenocarcinoma. Ann Surg 2018; doi: 10.1097/SLA.0000000000002862.DOIPubMed
68. Yang Y, Wang F, Zhang P, Shi C, Zou Y, et al. Robot-assisted versus conventional laparoscopic surgery for colorectal disease, focusing on rectal cancer: a meta-analysis. Ann Surg Oncol 2012;19:3727-36.DOIPubMed
69. Liao G, Li YB, Zhao Z, Li X, Deng H, et al. Robotic-assisted surgery versus open surgery in the treatment of rectal cancer: the current evidence. Sci Rep 2016;6:26981.DOIPubMedPMC
70. Li X, Wang T, Yao L, Hu L, Jin P, et al. The safety and effectiveness of robot-assisted versus laparoscopic TME in patients with rectal cancer: A meta-analysis and systematic review. Medicine (Baltimore) 2017;96:e7585.DOIPubMedPMC
71. Hopkins MB, Geiger TM, Bethurum AJ, Ford MM, Muldoon RL, et al. Comparing pathologic outcomes for robotic versus laparoscopic surgery in rectal cancer resection: a propensity adjusted analysis of 7616 patients. Surg Endosc 2019; doi: 10.1007/s00464-019-07032-1.DOIPubMed
72. Martinez-Perez A, de’Angelis N. Oncologic results of conventional laparoscopic TME: is the intramesorectal plane really acceptable? Tech Coloproctol 2018;22:831-4.DOIPubMed
73. Truong A, Lopez N, Fleshner P, Zaghiyan K. Preservation of pathologic outcomes in robotic versus open resection for rectal cancer: can the robot fill the minimally invasive gap? Am Surg 2018;84:1876-81.PubMed
74. Owens EA, Henary M, El Fakhri G, Choi HS. Tissue-specific near-infrared fluorescence imaging. Acc Chem Res 2016;49:1731-40.DOIPubMedPMC
75. Frangioni JV. In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol 2003;7:626-34.PubMed
76. Alander JT, Kaartinen I, Laakso A, Patila T, Spillmann T, et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012;2012:940585.DOIPubMedPMC
77. Liberale G, Bourgeois P, Larsimont D, Moreau M, Donckier V, et al. Indocyanine green fluorescence-guided surgery after IV injection in metastatic colorectal cancer: a systematic review. Eur J Surg Oncol 2017;43:1656-67.DOIPubMed
78. Degett TH, Andersen HS, Gogenur I. Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg 2016;401:767-75.DOIPubMed
79. Liberale G, Bohlok A, Bormans A, Bouazza F, Galdon MG, et al. Indocyanine green fluorescence imaging for sentinel lymph node detection in colorectal cancer: A systematic review. Eur J Surg Oncol 2018;44:1301-6.DOIPubMed
80. Lieto E, Auricchio A, Cardella F, Mabilia A, Basile N, et al. Fluorescence-guided surgery in the combined treatment of peritoneal carcinomatosis from colorectal cancer: preliminary results and considerations. World J Surg 2018;42:1154-60.DOIPubMed
81. Kang CY, Halabi WJ, Chaudhry OO, Nguyen V, Pigazzi A, et al. Risk factors for anastomotic leakage after anterior resection for rectal cancer. JAMA Surg 2013;148:65-71.DOIPubMed
82. Vignali A, Gianotti L, Braga M, Radaelli G, Malvezzi L, et al. Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum 2000;43:76-82.DOIPubMed
83. De Nardi P, Elmore U, Maggi G, Maggiore R, Boni L, et al. Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc 2019; doi: 10.1007/s00464-019-06730-0.DOIPubMed
84. Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, et al. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 2013;27:3003-8.DOIPubMed
85. Kim JC, Lee JL, Park SH. Interpretative guidelines and possible indications for indocyanine green fluorescence imaging in robot-assisted sphincter-saving operations. Dis Colon Rectum 2017;60:376-84.DOIPubMed
86. Barabino G, Klein JP, Porcheron J, Grichine A, Coll JL, et al. Intraoperative near-infrared fluorescence imaging using indocyanine green in colorectal carcinomatosis surgery: proof of concept. Eur J Surg Oncol 2016;42:1931-7.DOIPubMed
87. Filippello A, Porcheron J, Klein JP, Cottier M, Barabino G. Affinity of Indocyanine green in the detection of colorectal peritoneal carcinomatosis. Surg Innov 2017;24:103-8.DOIPubMed
88. Sluiter NR, Vlek SL, Wijsmuller AR, Brandsma HT, de Vet HCW, et al. Narrow-band imaging improves detection of colorectal peritoneal metastases: a clinical study comparing advanced imaging techniques. Ann Surg Oncol 2019;26:156-64.DOIPubMedPMC
89. Lee SJ, Sohn DK, Han KS, Kim BC, Hong CW, et al. Preoperative tattooing using indocyanine green in laparoscopic colorectal surgery. Ann Coloproctol 2018;34:206-11.DOIPubMedPMC
90. Penna M, Hompes R, Arnold S, Wynn G, Austin R, et al. Transanal total mesorectal excision: international registry results of the first 720 cases. Ann Surg 2017;266:111-7.DOIPubMed
91. Roodbeen SX, Penna M, Mackenzie H, Kusters M, Slater A, et al. Transanal total mesorectal excision (TaTME) versus laparoscopic TME for MRI-defined low rectal cancer: a propensity score-matched analysis of oncological outcomes. Surg Endosc 2019;33:2459-67.DOIPubMedPMC
92. Gomez Ruiz M, Parra IM, Palazuelos CM, Martin JA, Fernandez CC, et al. Robotic-assisted laparoscopic transanal total mesorectal excision for rectal cancer: a prospective pilot study. Dis Colon Rectum 2015;58:145-53.DOIPubMed
93. Protyniak B, Jorden J, Farmer R. Multiquadrant robotic colorectal surgery: the da Vinci Xi vs Si comparison. J Robot Surg 2018;12:67-74.DOIPubMed
94. Larsen SG, Pfeffer F, Kørner H; Norwegian Colorectal Cancer Group. Norwegian moratorium on transanal total mesorectal excision. Br J Surg 2019;106:1120-1.DOIPubMed
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