Current status of minimally invasive surgery in colorectum

Colorectal cancer (CRC) is the third most common cancers in men and second most common in women with incidence rates of 15–21 per 10,000 worldwide (1). Surgery is the only curative therapy for CRC, with the advancement in surgical technology and understanding the concepts of anatomy and pathology impelled to increase in survival. Technology and experience had transformed the field of colorectal surgery in diverse aspect, as there are no standardization of surgical technique and minimally invasive surgery (MIS) still it is in evolving process, whether to adopt with the new perspective depends on the experience and available evidence which this article brings forth the current practice of MIS in colorectal surgery.

Present state of MIS in colon surgery

Laparoscopic colorectal surgery follows the same oncological principles as open surgery with adequate lymphadenectomy, high ligation of vessel, adequate bowel margins. Since first reported laparoscopic colectomy by Jacob it has become standard surgical procedure in majority of centres. During initial period of MIS there were concern of port site metastasis and long term outcome in laparoscopic colon surgery, but last 2 decades have shown level one evidence suggesting that laparoscopy has good short and long term benefits as compared to open surgery. There are randomised control trials (RCTs) (1-9) (Table 1) and meta-analysis (10) suggesting the laparoscopy has better outcome compared to open colectomy showing benefits in terms of decreased intraoperative complications, decreased transfusions, early recovery of bowel function, decreased analgesic, short hospital stay, smaller incision, CRM margins and cost. However, laproscopy did not jeopardise the oncological outcome (2-6).

In large data base of over 3,00,000 cases from ACS NSQIP (national surgical quality improvement programme, 2006–2013) the number of laparoscopic colorectal cases performed are 36–49% (11). The context of the studies and the practical applicability differs with the experience of the surgeon, high volume centres and the standardised technique practised which finally gives better outcomes.

Concepts and controversies of complete mesocolic excision (CME)

In rectal cancer adoption of total mesocolic excision principles of surgery has reduced the local recurrence (LR) rates and improved the survival. The anatomical and embryological planes continue from rectosigmoid, descending colon, and run posteriorly behind the pancreas to include duodenum, cecum, ascending colon and the mesenteric root. Removal of tumour along the mesocolic plane increases survival benefits, concept of CME raised from this anatomical basis. The 10-year outcomes of CLASSIC trial (6) concluded in subgroup analysis that laparoscopic right hemicolectomy has increased propensity for LR than left hemicolectomy. Whether the long term outcomes of surgery based on the CME principles results could transform in better outcome is the matter of debate.

CME involves three principles: (I) removal of central envelop in mesocolic plane; (II) high vascular tie; (III) sufficient length of bowel both proximally and distally (12). Proponents of CME put forward that there are high number of lymph node harvested and eradicating the lymphatic’s better achieves local control of cancer, high lymph node ratio, identify the skip metastasis, stage migration, identification of micrometastasis, high quality of surgical specimen, and sufficient length of bowel. Opponents argued that the theoretical benefit of removing mesocolic lymph node is minimal as there are other confounding factors for the survival, there is no difference in survival if more than 12 lymph nodes are removed, incidence of D3 lymph node involvement is less and CME leads to over treatment of disease and there are no RCT to support the evidence. There are scepticisms regarding implementation of CME technique in terms of feasibility, and safety in clinical practice.

CME involves sharp dissection under embryological planes between visceral and parietal fascia which was first described by Hohenberger et al. (13), he achieved improvement in 5-year survival from 82% to 89% and reduction in 5-year LR from 6.5% to 3.6%. West et al. (14) demonstrated 15% survival advantage, increase plane of resection in CME specimens (92% vs. 40%) and increase LN retrieval (30 vs. 18). The study concluded that CME produced good quality specimens, this was further validated by number of studies (15-22). Storli et al. (23) supported the CME with high 3-year SR 88% and increase in DFS (82% vs. 75%) compared to non CME patients. Bertelsen et al. (24) in a population based study demonstrated that CME has a predictor of better survival with 4-year SR (85% vs. 75%) and low RR (11% vs. 16%). Kanemitsu et al. study concluded that CME produced better long term survival in right colon cancers (25). Laparoscopic CME offers the similar oncological outcome with advantages of MIS (Table 2). JCOG 0404 (15) is the first RCT comparing laparoscopy verses open D3 dissection, this study concluded that laparoscopy has better short term safety and clinical benefits.

Current role of MIS in rectum

Laparoscopic techniques has gained promising role in rectal surgery as it provides precise pelvic dissection, better identification of pelvic structure in narrow pelvis, improved magnification and visual angles. Sphincter preserving surgery has been recent trend made achievable with adequate pelvic dissection and adequate distal margins feasible by endostapling. Laparoscopic surgery has technical advantage in male pelvis, morbid obese and in prior chemordiotherapy and bulky distal tumours.

Meta-analysis and RCT comparing laparoscopy verses open in rectal cancers have shown the feasibility and safety and better short term advantages of laparoscopic surgery in rectal cancers (4-6,26-30). The difference in the operating time and conversion depends on the experience of the surgeon as COREAN, COLOR, ACOSOG Z6051, ALACaRT trials recorded 1%, 16%, 11%, 9% conversion rates respectively.

The CLASSIC trial (4-6) which included 48% rectal cancer cases concluded the there is no difference in OS (lap 78% vs. 82% open), DFS (lap 89% vs. 77% open), LR (lap 9% vs. 10% open) in 10-year follow up. This study analysis raised concern about a potentially higher positive CRM (laparoscopy 12% vs. 6% open, P<0.14) in laparoscopic anterior resection (LAR) group but is not significant. In APR the CRM positivity is higher in laparoscopy (16% vs. 14%) but did not reach statistical significance and there is no survival difference in 5-year follow up. There is no difference in mortality and morbidity between laparoscopic and open rectal surgery. Laparoscopy has shorter stay than open in rectal surgery. The COREAN trial (28) observed no difference between CRM, macroscopic quality of the total mesorectal excision (TME), number of harvested lymph nodes or perioperative morbidity between the two groups. COLOR 2 trial included 29% low rectal cancers, the CRM positivity in laparoscopy 9% vs. 22% in open and LR 3% in laparoscopy vs. 12% in open which was less compared to CLASSIC trial which showed more CRM positivity in laparoscopy (16%), with high LR of 9% in lap vs. 10% in open. CLASSIC trial (4-6) had 16% CRM positive after laparoscopic surgery (AR group 12% vs. 9%). Higher CRM positivity in COLOR ll (26,27) trial is due to the fact that margin involvement is taken as within 2 mm from the lateral surface of the mesorectum, whereas the COREAN (28) study used a 1-mm margin. COREAN (28) study concluded that laparoscopy had better advantages than open in low rectal cancers with low CRM positivity and low recurrence rates. ACOSOG Z6051, ALACaRT multi centric RCT showed non-inferiority of laparoscopic surgery compared with open surgery determined by histopathological evidence (29,30).

After the introduction of TME there is significant reduction in complication of Urinary dysfunction and sexual dysfunction due to preservation of autonomic nerves. With open TME the urinary dysfunction has been 0% to 12% and sexual dysfunction in 10% to 30%. The CLASSIC trial (4-6) reported no difference in bladder dysfunction between laparoscopy and open TME. Hur et al. showed that laparoscopy had decrease sexual dysfunction compared to open TME (31).

Emerging trend of robotic colorectal surgery

Advance imaging and technology has made major leap through with use of robotic in CRCs surgery. With difficult pelvic dissection due to narrow pelvis and anatomical complexity in dissection by laparoscopy, adoption of robotic has added advantage of 3D binocular vision, 7 degrees of motion, high resolution, improved dexterity, tremor reduction, improves pelvic dissection, surgeon controlled camera, stable traction and surgeon comfort.

Since the adoption of robotic in colorectal surgery from 2001 there has been increase studies to validate the outcomes comparing robotic and laparoscopic colorectal surgery. Kang et al. (32) concluded that robotic is better in terms of faster recovery, short stay, early recover of bowel, decrease wound infection sand decrease complication rate (20% vs. 27%) (P<0.034). This has been similar in other studies published by Saklani et al. (33) supporting decrease morbidity (16% vs. 26%), Park et al. reported no difference in complication in robotic compared to laparoscopy (34).

The CLASSIC trial (4-6) showed conversion rates of 16% in laparoscopic rectal surgery. After the adoption of robotic the data showed conversion rates of 0–8% (33-35). In Saklani et al.’s series of 74 robotic low rectal cases, the conversion rate is 1% (33). Surgical outcomes in rectal cancer depend on the quality of the specimen, and with the implementation of robotics yielded high quality TME specimen. Kang et al. (32) reported low CRM positivity in robotic (4.2% vs. 10% lap, P<0.034), Yoo et al. 2015 (35) also supported low CME positivity in robotic 9% vs. 19%. The drawbacks of robotics are the increase in operating time and cost. Patriti et al. demonstrated shorter operating time (165 min) (36).

There are few studies (37,38) to show the long term outcome in robotic surgery, Park et al. (37) compared 133 cases of robotic LAR with 5-year follow up showed no difference in OS, DFS, LR. The ROLARR (39) multicentre RCT concluded that there is no difference in conversion rates (8% vs. 12%), CRM positivity (5% vs. 6%), but robotic surgery showed benefits in males, in low tumour and obese patients.

Contention in management of transverse colon (T-colon) cancers

T-colon deserves special mention as T-colectomy surgeries are quite challenging. Laparoscopy has better benefits in T-colon as better visualization of mesentery base, identification of middle colic vessels, better dissection of mesentery from pancreas. T-colon has special anatomical and embryological status and surgery in T-colon is not standardised, because of an embryological fusion of mesenteric fascia, metastatic nodes incidence is 5% in subpyloric and 4% in right gastroepiploic nodal station (40). Most of the randomised trials like CLASSIC, COST, COLOR, ALCCas, have not included T-colon cancer.

Agarwal et al. (41) showed that laparoscopy retrieved more LN yield (22 vs. 18) and laparoscopy is feasible with conversion of 10% cases, further laparoscopy had decreased stay and similar 5-year OS and DFS, RR. Chong et al. published largest series of 1,060 patients comparing outcomes of T-colectomy verses extended colectomy which showed no difference in 5-year DFS/OS (42).

Distinction of combined endoscopic and laparoscopic surgery (CELS) in colorectal surgery

CELS is a recent development for removal of colonic polys when endoscopically difficult for excision when polyp is large, broad base, difficult visualization between the folds of mucosa, torturous colon. The advantages of CELS is the real time visualization of full thickness injury, avoids bowel resection, suture repair laparoscopic, invagination and mobilization of intestine. In recent review complication of CELS is coagulopathy (0–18%), and cancer risk of 2–10% (43). CELS has advantage of short stay and less operating time, the success rate of CELS is 75%. The long term outcome of CELS is safe and effective (44). Additional surgery is not necessary if the tumour is early stage and margins are clear, but CELS need dedicated OR room, two skilled doctors, endoscopic suturing, preoperative preparation, frozen section and learning curve.

Application of fluorescence imaging in colorectal surgery

Anastomotic leak in colorectal surgery is major concern in terms of mortality and morbidity and long term outcomes. Most of the anastomotic leak occurs due to the inadequate perfusion at the anastomosis, there is no reliable tool to confirm the micro perfusion at time of anastomosis. Fluorescence angiography is a new tool introduced in laparoscopic MIS to assess the adequate perfusion at the time of anastomosis. PILLAR II multi-institutional trial of 139 patients on use of fluorescence angiography showed that the success rate of angiography is 99% and by performing a fluorescence angiography study changed the planned proximal margin of transection in 7.9% of patients, with resulting leak rates of 0% (45). This is new technique and studies have showed safety and feasibility of this technique. This technique can be useful mainly where there is high risk anastomosis, and extended resections and re-resections of CRC where there is risk of precarious blood supply.

Natural orifice translumenal endoscopic surgery (NOTES) in rectal surgery

The leading edge of minimal invasive surgery is NOTES. Organ preserving surgery has been the recent trend in rectal surgery which has less pelvic complications and no anastomotic leak when compared to radical surgery. Since the introduction of Transanal endoscopic surgery platform in 1980 by Dr. Gerhart Buess there has been many modification, in 2009 the technique of transanal minimally invasive surgery (TAMIS) was introduced by Dr. Mathew Albert. Transanal surgery is mainly performed for benign rectal lesions and T1 lesions. The advantage of NOTES is that it avoids stoma, and complications of anastomic leak, and prevents neurovascular injury to bladder and preserves sexual function. Advantages of TEM is it has stable platform, specific insufflation, and dedicated suction and more proximal rectal lesions up to 20 cm can be resected, 3D vision. TAMIS has short learning curve as it has the similar instrumentation and techniques of SILS, decrease set up time for platform, flexibility of instruments use and better working angle for instruments. There is robust data on safety and feasibility of TEM/TAMIS, meta-analysis (46) compared three RCT concluded that TEM showed oncological outcomes equivalent to TME in early rectal cancer (cT1–2N0M0). TEM is also associated with a significantly shorter operative time, decreased intraoperative blood loss, decreased need for stoma and analgesia, and shorter hospital stay. TEM and TME were similar in terms of perioperative mortality and complete tumour resection. There are further CARTS, TESAR trial awaited to show whether there is advantage of transanal surgery in rectal cancer.

Trans anal total mesorectal excision (TaTME) is a new extension of MIS in treatment of rectal cancers. It can be performed as pure Transanal or hybrid procedure. The advantage of TaTME is in narrow pelvis, obese patients, large rectal tumours, irradiated patients, reoperative surgery. It is a bottom up approach which helps in clear visualization or rectum and mesorectum. Till now less than 500 cases have been reported which showed safety and feasibility of the procedure, recent systematic review (47) showed TaTME has good quality specimens with CRM clear in 98% and 1% LR in 14-month follow up, long term outcomes are still awaited. Further on-going COLOR III trial is awaited to know the long term outcomes.

Summary

Minimal invasive surgery in colorectal cancer results in good short term benefits with equivalent long term outcomes compared to open surgery. CME produces better quality specimen and showing promising long term outcomes, further studies need to address the long term benefit of CME. Robotic rectal surgery is an emerging technique with advantage in low rectal cancer, male pelvis and in obese patients. Trans anal surgery is a new platform in management of rectal cancer.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Annals of Laparoscopic and Endoscopic Surgery. The article did not undergo external peer review.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/ales.2016.11.23). Chen WT serves as an unpaid editorial board member of Annals of Laparoscopic and Endoscopic Surgery from Jun 2016 to May 2018. Li MK serves as an unpaid editorial board member of Annals of Laparoscopic and Endoscopic Surgery from Aug 2016 to Jul 2018. Chand A has no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. GLOBOCAN 2012: Estimated cancer incidence, Mortality and Prevalence Worldwide in 2012. Available online: http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx. Accesses 6th Sep 2016.
2. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350:2050-9. [Crossref] [PubMed]
3. Fleshman J, Sargent DJ, Green E, et al. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 2007;246:655-62; discussion 662-4. [Crossref] [PubMed]
4. Guillou PJ, Quirke P, Thorpe H, 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. [Crossref] [PubMed]
5. Jayne DG, Guillou PJ, Thorpe H, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol 2007;25:3061-8. [Crossref] [PubMed]
6. Green BL, Marshall HC, Collinson F, et al. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 2013;100:75-82. [Crossref] [PubMed]
7. Veldkamp R, Kuhry E, Hop WC, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 2005;6:477-84. [Crossref] [PubMed]
8. Colon Cancer Laparoscopic or Open Resection Study Group. Buunen M, Veldkamp R, Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 2009;10:44-52. [Crossref] [PubMed]
9. Hewett PJ, Allardyce RA, Bagshaw PF, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg 2008;248:728-38. [Crossref] [PubMed]
10. Ohtani H, Tamamori Y, Arimoto Y, et al. A meta-analysis of the short- and long-term results of randomized controlled trials that compared laparoscopy-assisted and open colectomy for colon cancer. J Cancer 2012;3:49-57. [Crossref] [PubMed]
11. Schlussel AT, Delaney CP, Maykel JA, et al. A National Database Analysis Comparing the Nationwide Inpatient Sample and American College of Surgeons National Surgical Quality Improvement Program in Laparoscopic vs Open Colectomies: Inherent Variance May Impact Outcomes. Dis Colon Rectum 2016;59:843-54. [Crossref] [PubMed]
12. Emmanuel A, Haji A. Complete mesocolic excision and extended (D3) lymphadenectomy for colonic cancer: is it worth that extra effort? A review of the literature. Int J Colorectal Dis 2016;31:797-804. [Crossref] [PubMed]
13. Hohenberger W, Weber K, Matzel K, et al. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation--technical notes and outcome. Colorectal Dis 2009;11:354-64; discussion 364-5. [Crossref] [PubMed]
14. West NP, Kobayashi H, Takahashi K, et al. Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J Clin Oncol 2012;30:1763-9. [Crossref] [PubMed]
15. Yamamoto S, Inomata M, Katayama H, et al. Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg 2014;260:23-30. [Crossref] [PubMed]
16. Shin JW, Amar AH, Kim SH, et al. Complete mesocolic excision with D3 lymph node dissection in laparoscopic colectomy for stages II and III colon cancer: long-term oncologic outcomes in 168 patients. Tech Coloproctol 2014;18:795-803. [Crossref] [PubMed]
17. Kim IY, Kim BR, Choi EH, et al. Short-term and oncologic outcomes of laparoscopic and open complete mesocolic excision and central ligation. Int J Surg 2016;27:151-7. [Crossref] [PubMed]
18. Liang JT, Lai HS, Huang J, et al. Long-term oncologic results of laparoscopic D3 lymphadenectomy with complete mesocolic excision for right-sided colon cancer with clinically positive lymph nodes. Surg Endosc 2015;29:2394-401. [Crossref] [PubMed]
19. Munkedal DL, West NP, Iversen LH, et al. Implementation of complete mesocolic excision at a university hospital in Denmark: An audit of consecutive, prospectively collected colon cancer specimens. Eur J Surg Oncol 2014;40:1494-501. [Crossref] [PubMed]
20. Siani LM, Pulica C. Laparoscopic complete mesocolic excision with central vascular ligation in right colon cancer: Long-term oncologic outcome between mesocolic and non-mesocolic planes of surgery. Scand J Surg 2015;104:219-26. [Crossref] [PubMed]
21. Liang JT, Huang KC, Lai HS, et al. Oncologic results of laparoscopic D3 lymphadenectomy for male sigmoid and upper rectal cancer with clinically positive lymph nodes. Ann Surg Oncol 2007;14:1980-90. [Crossref] [PubMed]
22. West NP, Hohenberger W, Weber K, et al. Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 2010;28:272-8. [Crossref] [PubMed]
23. Storli KE, Søndenaa K, Furnes B, et al. Short term results of complete (D3) vs. standard (D2) mesenteric excision in colon cancer shows improved outcome of complete mesenteric excision in patients with TNM stages I-II. Tech Coloproctol 2014;18:557-64. [Crossref] [PubMed]
24. Bertelsen CA, Bols B, Ingeholm P, et al. Can the quality of colonic surgery be improved by standardization of surgical technique with complete mesocolic excision? Colorectal Dis 2011;13:1123-9. [Crossref] [PubMed]
25. Kanemitsu Y, Komori K, Kimura K, et al. D3 Lymph Node Dissection in Right Hemicolectomy with a No-touch Isolation Technique in Patients With Colon Cancer. Dis Colon Rectum 2013;56:815-24. [Crossref] [PubMed]
26. van der Pas MH, Haglind E, Cuesta MA, 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. [Crossref] [PubMed]
27. Bonjer HJ, Deijen CL, Abis GA, et al. A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med 2015;372:1324-32. [Crossref] [PubMed]
28. Kang SB, Park JW, Jeong SY, 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. [Crossref] [PubMed]
29. Fleshman J, Branda M, Sargent DJ, 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. [Crossref] [PubMed]
30. Stevenson AR, Solomon MJ, Lumley JW, 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. [Crossref] [PubMed]
31. Hur H, Bae SU, Kim NK, et al. Comparative study of voiding and male sexual function following open and laparoscopic total mesorectal excision in patients with rectal cancer. J Surg Oncol 2013;108:572-8. [Crossref] [PubMed]
32. Kang J, Yoon KJ, Min BS, et al. The impact of robotic surgery for mid and low rectal cancer: a case-matched analysis of a 3-arm comparison--open, laparoscopic, and robotic surgery. Ann Surg 2013;257:95-101. [Crossref] [PubMed]
33. Saklani AP, Lim DR, Hur H, et al. Robotic versus laparoscopic surgery for mid-low rectal cancer after neoadjuvant chemoradiation therapy: comparison of oncologic outcomes. Int J Colorectal Dis 2013;28:1689-98. [Crossref] [PubMed]
34. Park JS, Choi GS, Park SY, et al. Randomized clinical trial of robot-assisted versus standard laparoscopic right colectomy. Br J Surg 2012;99:1219-26. [Crossref] [PubMed]
35. Yoo BE, Cho JS, Shin JW, et al. Robotic versus laparoscopic intersphincteric resection for low rectal cancer: comparison of the operative, oncological, and functional outcomes. Ann Surg Oncol 2015;22:1219-25. [Crossref] [PubMed]
36. Patriti A, Ceccarelli G, Bartoli A, et al. Short- and medium-term outcome of robot-assisted and traditional laparoscopic rectal resection. JSLS 2009;13:176-83. [PubMed]
37. Park EJ, Cho MS, Baek SJ, et al. Long-term oncologic outcomes of robotic low anterior resection for rectal cancer: a comparative study with laparoscopic surgery. Ann Surg 2015;261:129-37. [Crossref] [PubMed]
38. Lim DR, Min BS, Kim MS, et al. Robotic versus laparoscopic anterior resection of sigmoid colon cancer: comparative study of long-term oncologic outcomes. Surg Endosc 2013;27:1379-85. [Crossref] [PubMed]
39. 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;27:233-41. [Crossref] [PubMed]
40. Toyota S, Ohta H, Anazawa S. Rationale for extent of lymph node dissection for right colon cancer. Dis Colon Rectum 1995;38:705-11. [Crossref] [PubMed]
41. Agarwal S, Gincherman M, Birnbaum E, et al. Comparison of long-term follow up of laparoscopic versus open colectomy for transverse colon cancer. Proc (Bayl Univ Med Cent) 2015;28:296-9. [PubMed]
42. Chong CS, Huh JW, Oh BY, et al. Operative Method for Transverse Colon Carcinoma: Transverse Colectomy Versus Extended Colectomy. Dis Colon Rectum 2016;59:630-9. [Crossref] [PubMed]
43. Nakajima K, Sharma SK, Lee SW, et al. Avoiding colorectal resection for polyps: is CELS the best method? Surg Endosc 2016;30:807-18. [Crossref] [PubMed]
44. Lee SW, Garrett KA, Shin JH, et al. Dynamic article: long-term outcomes of patients undergoing combined endolaparoscopic surgery for benign colon polyps. Dis Colon Rectum 2013;56:869-73. [Crossref] [PubMed]
45. Jafari MD, Wexner SD, Martz JE, et al. Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 2015;220:82-92.e1. [Crossref] [PubMed]
46. Chiniah M, Ganganah O, Cheng Y, et al. Transanal endoscopic microsurgery is an oncologically safe alternative to total mesorectal excision for stage I rectal cancer: results of a meta-analysis of randomized controlled trials. Int J Colorectal Dis 2016;31:1501-4. [Crossref] [PubMed]
47. Arunachalam L, O'Grady H, Hunter IA, et al. A Systematic Review of Outcomes After Transanal Mesorectal Resection for Rectal Cancer. Dis Colon Rectum 2016;59:340-50. [Crossref] [PubMed]