Skip to main content

Advertisement

Log in

Robot-assisted versus laparoscopic short- and long-term outcomes in complete mesocolic excision for right-sided colonic cancer: a systematic review and meta-analysis

  • Review
  • Published:
Techniques in Coloproctology Aims and scope Submit manuscript

Abstract

Background

Complete mesocolic excision (CME) surgery is increasingly implemented for the resection of right-sided colonic cancer, possibly resulting in improved 5-year overall and disease-free survival compared to non-CME surgery. However, it is not clear what surgical platform should be used. The aim of this study was to compare the following outcomes between robot-assisted and laparoscopic CME-surgery for right-sided colonic cancer: (i) short-term clinical outcomes, (ii) pathological specimen quality, and (iii) long-term oncological outcomes.

Methods

Medline, Embase, and Cochrane Database of Systematic Reviews were searched from inception until August 2021. Pooled proportions were calculated by applying the inverse variance method. Heterogeneity was explored by I-square and supplemented by sensitivity- and meta-regression analyses. The risk of bias was evaluated by either MINORS or Cochrane's risk-of-bias tool (RoB 2).

Results

Fifty-five studies with 5.357 patients (740 robot-assisted and 4617 laparoscopic) were included in the meta-analysis. Overall postoperative morbidity was 17% [95% CI (14–20%)] in the robot-assisted group and 13% [95%CI (12–13%)] in the laparoscopic group. Robot-assisted CME was associated with a shorter hospital stay, lower intraoperative blood loss, a higher amount of harvested lymph nodes, and better 3-year oerall and disease-free survival. MINORS and RoB2 indicated a serious risk of bias across studies included.

Conclusions

This review which includes predominantly non-randomized studies suggests a possible advantage of the robot-assisted CME compared with a laparoscopic technique for several short-term outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation–technical notes and outcome. Colorectal Dis 11(4):354–364 (discussion 64–5)

    Article  CAS  Google Scholar 

  2. Heald RJ, Ryall RD (1986) Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1(8496):1479–1482

    Article  CAS  Google Scholar 

  3. Sondenaa K, Quirke P, Hohenberger W, Sugihara K, Kobayashi H, Kessler H et al (2014) The rationale behind complete mesocolic excision (CME) and a central vascular ligation for colon cancer in open and laparoscopic surgery : proceedings of a consensus conference. Int J Colorectal Dis 29(4):419–428

    Article  CAS  Google Scholar 

  4. Emmanuel A, Haji A (2016) 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 31(4):797–804

    Article  Google Scholar 

  5. Feng B, Sun J, Ling TL, Lu AG, Wang ML, Chen XY et al (2012) Laparoscopic complete mesocolic excision (CME) with medial access for right-hemi colon cancer: feasibility and technical strategies. Surg Endosc 26(12):3669–3675

    Article  Google Scholar 

  6. Kim HJ, Choi GS, Park JS, Park SY (2014) Comparison of surgical skills in laparoscopic and robotic tasks between experienced surgeons and novices in laparoscopic surgery: an experimental study. Ann Coloproctol 30(2):71–76

    Article  Google Scholar 

  7. Corcione F, Esposito C, Cuccurullo D, Settembre A, Miranda N, Amato F et al (2005) Advantages and limits of robot-assisted laparoscopic surgery: preliminary experience. Surg Endosc 19(1):117–119

    Article  CAS  Google Scholar 

  8. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71

    Article  Google Scholar 

  9. Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J (2003) Methodological index for non-randomized studies (minors): development and validation of a new instrument. ANZ J Surg 73(9):712–716

    Article  Google Scholar 

  10. Sterne JAC, Savovic J, Page MJ, Elbers RG, Blencowe NS, Boutron I et al (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 366:l4898

    Article  Google Scholar 

  11. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13

    Article  Google Scholar 

  12. Cumpston M, Li T, Page MJ, Chandler J, Welch VA, Higgins JP, et al (2019) Updated guidance for trusted systematic reviews: a new edition of the Cochrane Handbook for Systematic Reviews of Interventions. Cochrane Database Syst Rev 10:ED000142

  13. De Simoni O, Barina A, Sommariva A, Tonello M, Gruppo M, Mattara G et al (2021) Complete mesocolic excision versus conventional hemicolectomy in patients with right colon cancer: a systematic review and meta-analysis. Int J Colorectal Dis 36(5):881–892

    Article  Google Scholar 

  14. Ow ZGW, Sim W, Nistala KRY, Ng CH, Koh FH, Wong NW et al (2021) Comparing complete mesocolic excision versus conventional colectomy for colon cancer: a systematic review and meta-analysis. Eur J Surg Oncol 47(4):732–737

    Article  Google Scholar 

  15. Anania G, Davies RJ, Bagolini F, Vettoretto N, Randolph J, Cirocchi R et al (2021) Right hemicolectomy with complete mesocolic excision is safe, leads to an increased lymph node yield and to increased survival: results of a systematic review and meta-analysis. Tech Coloproctol 25(10):1099–1113

    Article  CAS  Google Scholar 

  16. Ferri V, Vicente E, Quijano Y, Duran H, Diaz E, Fabra I et al (2021) Right-side colectomy with complete mesocolic excision vs conventional right-side colectomy in the treatment of colon cancer: a systematic review and meta-analysis. Int J Colorectal Dis 36(9):1885–1904

    Article  Google Scholar 

  17. Pilka R, Marek R, Adam T, Kudela M, Ondrova D, Neubert D et al (2016) Systemic inflammatory response after open, laparoscopic and robotic surgery in endometrial cancer patients. Anticancer Res 36(6):2909–2922

    CAS  Google Scholar 

  18. Zawadzki M, Krzystek-Korpacka M, Gamian A, Witkiewicz W (2017) Comparison of inflammatory responses following robotic and open colorectal surgery: a prospective study. Int J Colorectal Dis 32(3):399–407

    Article  Google Scholar 

  19. Skjold KP, Palmfeldt J, Norregaard R, Borre M, Jensen JB (2017) Perioperative systemic inflammatory response following robot-assisted laparoscopic cystectomy vs. open mini-laparotomy cystectomy: a prospective study. Urol Int 99(4):436–445

    Article  Google Scholar 

  20. Cuk P, Simonsen RM, Komljen M, Nielsen MF, Helligso P, Pedersen AK et al (2021) Improved perioperative outcomes and reduced inflammatory stress response in malignant robot-assisted colorectal resections: a retrospective cohort study of 298 patients. World J Surg Oncol 19(1):155

    Article  Google Scholar 

  21. Xu L, Su X, He Z, Zhang C, Lu J, Zhang G et al (2021) Short-term outcomes of complete mesocolic excision versus D2 dissection in patients undergoing laparoscopic colectomy for right colon cancer (RELARC): a randomised, controlled, phase 3, superiority trial. Lancet Oncol 22(3):391–401

    Article  Google Scholar 

  22. Bertelsen CA, Neuenschwander AU, Jansen JE, Tenma JR, Wilhelmsen M, Kirkegaard-Klitbo A et al (2019) 5-year outcome after complete mesocolic excision for right-sided colon cancer: a population-based cohort study. Lancet Oncol 20(11):1556–1565

    Article  Google Scholar 

  23. Bianchi PP, Giuliani G, Salaj A, Ferraro L, Opocher E, Toti F et al (2021) Bottom-up suprapubic approach for robotic right colectomy: technical aspects and preliminary outcomes. Minerva Surg 76(2):129–137

    Article  Google Scholar 

  24. Bianchi PP, Salaj A, Giuliani G, Ferraro L, Formisano G (2021) Feasibility of robotic right colectomy with complete mesocolic excision and intracorporeal anastomosis: short-term outcomes of 161 consecutive patients. Updates Surg 73(3):1065–1072

    Article  Google Scholar 

  25. Schulte AEJ, Iosivan S-I, Steinfurth F, Mahdi A, Forster C, Wilkens L et al (2019) A standardized suprapubic bottom-to-up approach in robotic right colectomy: technical and oncological advances for complete mesocolic excision (CME). BMC Surg 19(1):72

    Article  Google Scholar 

  26. Petz W, Bertani E, Borin S, Fiori G, Ribero D, Spinoglio G (2021) Fluorescence-guided D3 lymphadenectomy in robotic right colectomy with complete mesocolic excision. Int J Med Robot 17(3):e2217

    Article  Google Scholar 

  27. Hamzaoglu I, Ozben V, Sapci I, Aytac E, Aghayeva A, Bilgin IA et al (2018) “Top down no-touch” technique in robotic complete mesocolic excision for extended right hemicolectomy with intracorporeal anastomosis. Tech Coloproctol 22(8):607–611

    Article  CAS  Google Scholar 

  28. Yang Y, Malakorn S, Zafar SN, Nickerson TP, Sandhu L, Chang GJ (2019) Superior mesenteric vein-first approach to robotic complete mesocolic excision for right colectomy: technique and preliminary outcomes. Dis Colon Rectum 62(7):894–897

    Article  Google Scholar 

  29. Ouyang M, Luo Z, Wu J, Zhang W, Tang S, Lu Y et al (2019) Comparison of outcomes of complete mesocolic excision with conventional radical resection performed by laparoscopic approach for right colon cancer. Cancer Manag Res 11:8647–8656

    Article  Google Scholar 

  30. Huang JL, Wei HB, Fang JF, Zheng ZH, Chen TF, Wei B et al (2015) Comparison of laparoscopic versus open complete mesocolic excision for right colon cancer. Int J Surg 23(Pt A):12–17

    Article  Google Scholar 

  31. Adamina M, Manwaring ML, Park KJ, Delaney CP (2012) Laparoscopic complete mesocolic excision for right colon cancer. Surg Endosc 26(10):2976–2980

    Article  Google Scholar 

  32. Melich G, Jeong DH, Hur H, Baik SH, Faria J, Kim NK et al (2014) Laparoscopic right hemicolectomy with complete mesocolic excision provides acceptable perioperative outcomes but is lengthy–analysis of learning curves for a novice minimally invasive surgeon. Can J Surg 57(5):331–336

    Article  Google Scholar 

  33. Kang J, Kim IK, Kang SI, Sohn SK, Lee KY (2014) Laparoscopic right hemicolectomy with complete mesocolic excision. Surg Endosc 28(9):2747–2751

    Article  Google Scholar 

  34. Bae SU, Saklani AP, Lim DR, Kim DW, Hur H, Min BS et al (2014) Laparoscopic-assisted versus open complete mesocolic excision and central vascular ligation for right-sided colon cancer. Ann Surg Oncol 21(7):2288–2294

    Article  Google Scholar 

  35. Liang JT, Lai HS, Huang J, Sun CT (2015) Long-term oncologic results of laparoscopic D3 lymphadenectomy with complete mesocolic excision for right-sided colon cancer with clinically positive lymph nodes. Surg Endosc 29(8):2394–2401

    Article  Google Scholar 

  36. Mori S, Baba K, Yanagi M, Kita Y, Yanagita S, Uchikado Y et al (2015) Laparoscopic complete mesocolic excision with radical lymph node dissection along the surgical trunk for right colon cancer. Surg Endosc 29(1):34–40

    Article  Google Scholar 

  37. An MS, Baik H, Oh SH, Park YH, Seo SH, Kim KH et al (2018) Oncological outcomes of complete versus conventional mesocolic excision in laparoscopic right hemicolectomy. ANZ J Surg 88(10):E698–E702

    Article  Google Scholar 

  38. Wang Y, Zhang C, Zhang D, Fu Z, Sun Y (2017) Clinical outcome of laparoscopic complete mesocolic excision in the treatment of right colon cancer. World J Surg Oncol 15(1):174

    Article  Google Scholar 

  39. Conti C, Pedrazzani C, Turri G, Fernandes E, Lazzarini E, De Luca R et al (2021) Comparison of short-term results after laparoscopic complete mesocolic excision and standard colectomy for right-sided colon cancer: analysis of a western center cohort. Ann Coloproctol 37(3):166–173

    Article  Google Scholar 

  40. Yi XJ, Lu XQ, Li HM, Wang W, Xiong WJ, Wan J et al (2019) Feasibility and efficacy of laparoscopic radical right hemicolectomy with complete mesocolic excision using an “artery-first” approach. Gastroenterol Rep (Oxf) 7(3):199–204

    Article  Google Scholar 

  41. Feng B, Ling TL, Lu AG, Wang ML, Ma JJ, Li JW et al (2014) Completely medial versus hybrid medial approach for laparoscopic complete mesocolic excision in right hemicolon cancer. Surg Endosc 28(2):477–483

    Article  Google Scholar 

  42. Tschann P, Seitinger G, Lechner D, Adler S, Feurstein B, Girotti PNC et al (2021) Reduced port versus open right hemicolectomy for colorectal cancer: a retrospective comparison study of two centers. Int J Colorectal Dis 36(7):1469–1477

    Article  Google Scholar 

  43. Ceccarelli G, Costa G, Ferraro V, De Rosa M, Rondelli F, Bugiantella W (2020) Robotic or three-dimensional (3D) laparoscopy for right colectomy with complete mesocolic excision (CME) and intracorporeal anastomosis? A propensity score-matching study comparison. Surg Endosc

  44. Kim IY, Kim BR, Choi EH, Kim YW (2016) Short-term and oncologic outcomes of laparoscopic and open complete mesocolic excision and central ligation. Int J Surg 27:151–157

    Article  Google Scholar 

  45. Chen S, Ying C (2017) Comparison of laparoscopic versus open complete mesocolic excision in elderly patients with right hemicolon cancer: retrospective analysis of one single cancer. Int J Clin Exp Med 10:5116–6124

    Google Scholar 

  46. Siani LM, Lucchi A, Berti P, Garulli G (2017) Laparoscopic complete mesocolic excision with central vascular ligation in 600 right total mesocolectomies: safety, prognostic factors and oncologic outcome. Am J Surg 214(2):222–227

    Article  Google Scholar 

  47. Pedrazzani C, Lazzarini E, Turri G, Fernandes E, Conti C, Tombolan V et al (2019) Laparoscopic Complete Mesocolic Excision for Right-Sided Colon Cancer: Analysis of Feasibility and Safety from a Single Western Center. J Gastrointest Surg 23(2):402–407

    Article  Google Scholar 

  48. Koc MA, Celik SU, Guner V, Akyol C (2021) Laparoscopic vs open complete mesocolic excision with central vascular ligation for right-sided colon cancer. Medicine (Baltimore) 100(6):e24613

    Article  CAS  Google Scholar 

  49. Zedan A, Elshiekh E, Omar MI, Raafat M, Khallaf SM, Atta H et al (2021) Laparoscopic versus open complete mesocolic excision for right colon cancer. Int J Surg Oncol 2021:8859879

    Google Scholar 

  50. Xie D, Yu C, Gao C, Osaiweran H, Hu J, Gong J (2017) An optimal approach for laparoscopic D3 lymphadenectomy plus complete mesocolic excision (D3+CME) for right-sided colon cancer. Ann Surg Oncol 24(5):1312–1313

    Article  Google Scholar 

  51. Di Buono G, Buscemi S, Cocorullo G, Sorce V, Amato G, Bonventre G et al (2021) Feasibility and safety of laparoscopic complete mesocolic excision (CME) for right-sided colon cancer: short-term outcomes. A randomized clinical study. Ann Surg 274(1):57–62

    Article  Google Scholar 

  52. Magistro C, Bertoglio CL, Giani A, Mazzola M, Rubicondo C, Maspero M et al (2021) Laparoscopic complete mesocolic excision versus conventional resection for right-sided colon cancer: a propensity score matching analysis of short-term outcomes. Surg Endosc

  53. He Z, Zhang S, Xue P, Yan X, Zhou L, Li J et al (2019) Completely medial access by page-turning approach for laparoscopic right hemi-colectomy: 6-year-experience in single center. Surg Endosc 33(3):959–965

    Article  Google Scholar 

  54. Du S, Zhang B, Liu Y, Han P, Song C, Hu F et al (2018) A novel and safe approach: middle cranial approach for laparoscopic right hemicolon cancer surgery with complete mesocolic excision. Surg Endosc 32(5):2567–2574

    Article  Google Scholar 

  55. Benz S, Tam Y, Tannapfel A, Stricker I (2016) The uncinate process first approach: a novel technique for laparoscopic right hemicolectomy with complete mesocolic excision. Surg Endosc 30(5):1930–1937

    Article  Google Scholar 

  56. Takemasa I, Uemura M, Nishimura J, Mizushima T, Yamamoto H, Ikeda M et al (2014) Feasibility of single-site laparoscopic colectomy with complete mesocolic excision for colon cancer: a prospective case-control comparison. Surg Endosc 28(4):1110–1118

    Article  Google Scholar 

  57. Zhu DJ, Chen XW, OuYang MZ, Lu Y (2016) Three surgical planes identified in laparoscopic complete mesocolic excision for right-sided colon cancer. World J Surg Oncol 14(1):7

    Article  Google Scholar 

  58. Aziz ME-D, Hasanien AH (2020) Short term outcomes of laparoscopic complete mesocolic excision with central vascular ligation for right colonic cancer. Indian J Public Health Res Dev 11:1674–1679

    Google Scholar 

  59. Subbiah R, Bansal S, Jain M, Ramakrishnan P, Palanisamy S, Palanivelu PR et al (2016) Initial retrocolic endoscopic tunnel approach (IRETA) for complete mesocolic excision (CME) with central vascular ligation (CVL) for right colonic cancers: technique and pathological radicality. Int J Colorectal Dis 31(2):227–233

    Article  Google Scholar 

  60. Olmi S, Oldani A, Cesana G, Ciccarese F, Uccelli M, Giorgi R, et al (2020) Surgical outcomes of laparoscopic right colectomy with complete mesocolic excision. JSLS 24(2)

  61. Matsuda T, Iwasaki T, Sumi Y, Yamashita K, Hasegawa H, Yamamoto M et al (2017) Laparoscopic complete mesocolic excision for right-sided colon cancer using a cranial approach: anatomical and embryological consideration. Int J Colorectal Dis 32(1):139–141

    Article  Google Scholar 

  62. West NP, Kennedy RH, Magro T, Luglio G, Sala S, Jenkins JT et al (2014) Morphometric analysis and lymph node yield in laparoscopic complete mesocolic excision performed by supervised trainees. Br J Surg 101(11):1460–1467

    Article  CAS  Google Scholar 

  63. Enomoto M, Katsumata K, Kasahara K, Tago T, Okazaki N, Wada T et al (2020) Laparoscopic complete mesocolic excision with true central vascular ligation for right-sided colon cancer. Surg Endosc 34(12):5640–5641

    Article  Google Scholar 

  64. Takahashi H, Takemasa I, Haraguchi N, Nishimura J, Hata T, Yamamoto H et al (2017) The single-center experience with the standardization of single-site laparoscopic colectomy for right-sided colon cancer. Surg Today 47(8):966–972

    Article  CAS  Google Scholar 

  65. Li J, Zhu S, Juan J, Yi B (2020) Preliminary exploration of robotic complete mesocolic excision for colon cancer with the domestically produced Chinese minimally invasive Micro Hand S surgical robot system. Int J Med Robot 16(6):1–8

    Article  Google Scholar 

  66. Hwang DY, Lee GR, Kim JH, Lee YS (2020) Laparoscopic complete mesocolic excision with D3 lymph node dissection for right colon cancer in elderly patients. Sci Rep 10(1):12633

    Article  Google Scholar 

  67. Tei M, Suzuki Y, Ohtsuka M, Yoshiwaka Y, Sueda T, Imasato M et al (2021) Single-port laparoscopic extended right hemicolectomy with complete mesocolic excision and central vascular ligation using a right colon rotation technique (flip-flap method). Surg Endosc 35(9):5359–5364

    Article  Google Scholar 

  68. Magouliotis DE, Baloyiannis I, Mamaloudis I, Bompou E, Papacharalampous C, Tzovaras GA (2021) Laparoscopic Versus Open Right Colectomy for Cancer in the Era of Complete Mesocolic Excision with Central Vascular Ligation: Pathology and Short-Term Outcomes. J Laparoendosc Adv Surg Tech A

  69. Yozgatli TK, Aytac E, Ozben V, Bayram O, Gurbuz B, Baca B et al (2019) Robotic complete mesocolic excision versus conventional laparoscopic hemicolectomy for right-sided colon cancer. J Laparoendosc Adv Surg Tech A 29(5):671–676

    Article  Google Scholar 

  70. Larach JT, Flynn J, Wright T, Rajkomar AKS, McCormick JJ, Kong J et al (2021) Robotic complete mesocolic excision versus conventional robotic right colectomy for right-sided colon cancer: a comparative study of perioperative outcomes. Surg Endosc

  71. Ramachandra C, Sugoor P, Karjol U, Arjunan R, Altaf S, Patil V et al (2020) Robotic complete mesocolic excision with central vascular ligation for right colon cancer: surgical technique and short-term outcomes. Indian J Surg Oncol 11(4):674–683

    Article  CAS  Google Scholar 

  72. Khan JS, Ahmad A, Odermatt M, Jayne DG, Ahmad NZ, Kandala N et al (2021) Robotic complete mesocolic excision with central vascular ligation for right colonic tumours—a propensity score-matching study comparing with standard laparoscopy. BJS Open 5(2)

  73. Siddiqi N, Stefan S, Jootun R, Mykoniatis I, Flashman K, Beable R et al (2021) Robotic Complete Mesocolic Excision (CME) is a safe and feasible option for right colonic cancers: short and midterm results from a single-centre experience. Surg Endosc

  74. Spinoglio G, Bianchi PP, Marano A, Priora F, Lenti LM, Ravazzoni F et al (2018) Robotic versus laparoscopic right colectomy with complete mesocolic excision for the treatment of colon cancer: perioperative outcomes and 5-year survival in a consecutive series of 202 patients. Ann Surg Oncol 25(12):3580–3586

    Article  Google Scholar 

  75. Ozben V, Aytac E, Atasoy D, Erenler Bayraktar I, Bayraktar O, Sapci I et al (2019) Totally robotic complete mesocolic excision for right-sided colon cancer. J Robot Surg 13(1):107–114

    Article  Google Scholar 

  76. Schulte Am Esch J, Iosivan SI, Steinfurth F, Mahdi A, Forster C, Wilkens L et al (2019) A standardized suprapubic bottom-to-up approach in robotic right colectomy: technical and oncological advances for complete mesocolic excision (CME). BMC Surg 9(1):72

    Article  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pedja Cuk.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 146 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cuk, P., Jawhara, M., Al-Najami, I. et al. Robot-assisted versus laparoscopic short- and long-term outcomes in complete mesocolic excision for right-sided colonic cancer: a systematic review and meta-analysis. Tech Coloproctol 27, 171–181 (2023). https://doi.org/10.1007/s10151-022-02686-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10151-022-02686-x

Keywords

Navigation