Skip to main content

Advertisement

SpringerLink
Log in

Complete mesocolic excision and D3 lymphadenectomy with central vascular ligation in right-sided colon cancer: a systematic review of postoperative outcomes, tumor recurrence and overall survival

  • Review Article
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

In right-sided colon cancer surgery, currently there is a great deal of discussion and debate regarding complete mesocolic excision (CME) versus conventional right hemicolectomy (CRH) on postoperative outcomes and oncological results.

Our aim was to perform a systematic review of the short- and long-term outcomes of CME to standardize surgical approach in patients with right-sided colon cancer.

Methods

A systematic review was performed examining available data on randomized and non-randomized studies evaluating the role of CME and D3 lymphadenectomy in the treatment of right-sided colon cancer, in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) standards.

Results

After literature search, 919 studies have been recorded, 110 studies underwent full-text reviews and 30 studies met inclusion criteria. The total number of CME procedures was 5931. Postoperative complications was reported in 28 studies with pooled overall complications of 1.88% for CME surgery. Six studies reported 0% of overall postoperative complications and they demonstrated a low incidence of complications following CME procedure. Anastomotic leak was reported in 27 studies with pooled proportion of 0.92% after CME resections. There were 16 papers reporting overall survival following CME procedure, with a mean of 85% of patients survived at 5 years. Mean 5-year overall survival was 93.05% in stage I patients, 89.76% in stage II patients and 79.65% in stage III patients. Local and distant recurrence were included in 21 studies, reporting tumor recurrence rate of 12.25% following CME. 5-year tumor recurrence was 5.8% in stage I patients, 7.68% in stage II patients and 15.69% in stage III patients.

Conclusions

CME does not increase the risk of postoperative complications and significantly improves the long-term oncological impact. Prospective multicentre studies results are needed to verify if CME could be considered standard surgery for right colon cancer.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Heald RJ, Husband EM, Ryall RD (1982) The mesorectum in rectal cancer surgery–the clue to pelvic recurrence? Br J Surg 69(10):613–616

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. Hashiguchi Y, Muro K, Saito Y, Ito Y, Ajioka Y, Hamaguchi T, Hasegawa K, Hotta K, Ishida H, Ishiguro M, Ishihara S, Kanemitsu Y, Kinugasa Y, Murofushi K, Nakajima TE, Oka S, Tanaka T, Taniguchi H, Tsuji A, Uehara K, Ueno H, Yamanaka T, Yamazaki K, Yoshida M, Yoshino T, Itabashi M, Sakamaki K, Sano K, Shimada Y, Tanaka S, Uetake H, Yamaguchi S, Yamaguchi N, Kobayashi H, Matsuda K, Kotake K, Sugihara K (2020) Japanese society for cancer of the colon and rectum. Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 25(1):1–42

    Article  PubMed  Google Scholar 

  4. West NP, Kobayashi H, Takahashi K, Perrakis A, Weber K, Hohenberger W, Sugihara K, Quirke P (2012) Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J Clin Oncol 30(15):1763–1769

    Article  PubMed  Google Scholar 

  5. West NP, Hohenberger W, Weber K, Perrakis A, Finan PJ, Quirke P (2010) Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol. 28(2):272–278

    Article  PubMed  Google Scholar 

  6. Bertelsen CA, Bols B, Ingeholm P, Jansen JE, Neuenschwander AU, Vilandt J (2011) Can the quality of colonic surgery be improved by standardization of surgical technique with complete mesocolic excision? Colorectal Dis 13(10):1123–1129

    Article  CAS  PubMed  Google Scholar 

  7. Kobayashi H, West NP, Takahashi K, Perrakis A, Weber K, Hohenberger W, Quirke P, Sugihara K (2014) Quality of surgery for stage III colon cancer: comparison between England, Germany, and Japan. Ann. Surg. Oncol. 21(3):S398–S404

    Article  PubMed  Google Scholar 

  8. Bertelsen CA, Neuenschwander AU, Jansen JE, Kirkegaard-Klitbo A, Tenma JR, Wilhelmsen M, Rasmussen LA, Jepsen LV, Kristensen B, Gogenur I, Copenhagen Complete Mesocolic Excision Study, Danish Colorectal Cancer Group (2016) Short-term outcomes after complete mesocolic excision compared with ‘conventional’ colonic cancer surgery. Br J Surg 103:581–589

    Article  CAS  PubMed  Google Scholar 

  9. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Prefferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann intern Med 151:264–269

    Article  PubMed  Google Scholar 

  10. Benz S (2013) Survival after complete mesocolic excision (CME) for right sided colon cancer compared to standard surgery. Open Surg J 7:6–10

    Article  Google Scholar 

  11. Bertelsen CA, Neuenschwander AU, Jansen JE, Tenma JR, Wilhelmsen M, Kirkegaard-Klitbo A, Iversen ER, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Born PW, Kristensen B, Kleif J (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  PubMed  Google Scholar 

  12. Siani LM, Pulica C (2015) 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 104(4):219–226

    Article  CAS  PubMed  Google Scholar 

  13. 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  PubMed  Google Scholar 

  14. Spinoglio G, Bianchi PP, Marano A, Priora F, Lenti LM, Ravazzoni F, Petz W, Borin S, Ribero D, Formisano G, Bertani E (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  PubMed  Google Scholar 

  15. Garcia-Granero A, Pellino G, Frasson M, Fletcher-Sanfeliu D, Bonilla F, Sánchez-Guillén L, Domenech Dolz A, Primo Romaguera V, Sabater Ortí L, Martinez-Soriano F, Garcia-Granero E, Valverde-Navarro AA (2019) The fusion fascia of Fredet: an important embryological landmark for complete mesocolic excision and D3-lymphadenectomy in right colon cancer. Surg Endosc 33(11):3842–3850

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  17. Shin JK, Kim HC, Lee WY, Yun SH, Cho YB, Huh JW, Park YA, Chun HK (2018) Laparoscopic modified mesocolic excision with central vascular ligation in right-sided colon cancer shows better short- and long-term outcomes compared with the open approach in propensity score analysis. Surg Endosc 32(6):2721–2731

    Article  PubMed  Google Scholar 

  18. Schulte Am Esch J, Iosivan SI, Steinfurth F, Mahdi A, Förster C, Wilkens L, Nasser A, Sarikaya H, Benhidjeb T, Krüger M (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  PubMed  PubMed Central  Google Scholar 

  19. 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  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Bae SU, Yang SY, Min BS (2019) Totally robotic modified complete mesocolic excision and central vascular ligation for right-sided colon cancer: technical feasibility and mid-term oncologic outcomes. Int J Colorectal Dis 34(3):471–479

    Article  PubMed  Google Scholar 

  22. Sheng QS, Pan Z, Chai J, Cheng XB, Liu FL, Wang JH, Chen WB, Lin JJ (2017) Complete mesocolic excision in right hemicolectomy: comparison between hand-assisted laparoscopic and open approaches. Ann Surg Treat Res 92(2):90–96

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ouyang M, Luo Z, Wu J, Zhang W, Tang S, Lu Y, Hu W, Yao X (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  PubMed  PubMed Central  Google Scholar 

  24. Deng X, Hu T, Wei M, Wu Q, Yang T, Meng W, Wang Z (2018) Feasibility of a unidirectionally progressive, pancreas-oriented procedure for laparoscopic D3 right hemicolectomy. Langenbecks Arch Surg 403(6):761–768

    Article  PubMed  Google Scholar 

  25. Elias AW, Merchea A, Moncrief S, Wise KB, Colibaseanu DT, Dozois EJ, Mathis KL (2020) Recurrence and long-term survival following segmental colectomy for right-sided colon cancer in 813 patients: a single-institution study. J Gastrointest Surg 24(7):1648–1654

    Article  PubMed  Google Scholar 

  26. Petz W, Ribero D, Bertani E, Borin S, Formisano G, Esposito S, Spinoglio G, Bianchi PP (2017) Suprapubic approach for robotic complete mesocolic excision in right colectomy: oncologic safety and short-term outcomes of an original technique. Eur J Surg Oncol 43(11):2060–2066

    Article  CAS  PubMed  Google Scholar 

  27. He Z, Zhang S, Xue P, Yan X, Zhou L, Li J, Wang M, Lu A, Ma J, Zang L, Hong H, Dong F, Su H, Sun J, Zhang L, Zheng M, Feng B (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  PubMed  Google Scholar 

  28. Spinoglio G, Marano A, Bianchi PP, Priora F, Lenti LM, Ravazzoni F, Formisano G (2016) Robotic right colectomy with modified complete mesocolic excision: long-term oncologic outcomes. Ann Surg Oncol 23(Suppl 5):684–691

    Article  PubMed  Google Scholar 

  29. 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  PubMed  Google Scholar 

  30. Kanemitsu Y, Komori K, Kimura K, Kato T (2013) D3 lymph node dissection in right hemicolectomy with a no-touch isolation technique in patients with colon cancer. Dis Colon Rectum 56(7):815–824

    Article  PubMed  Google Scholar 

  31. Bae SU, Saklani AP, Lim DR, Kim DW, Hur H, Min BS, Baik SH, Lee KY, Kim NK (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  PubMed  Google Scholar 

  32. 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  PubMed  Google Scholar 

  33. Feng B, Sun J, Ling TL, Lu AG, Wang ML, Chen XY, Ma JJ, Li JW, Zang L, Han DP, Zheng MH (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  PubMed  Google Scholar 

  34. Feng B, Ling TL, Lu AG, Wang ML, Ma JJ, Li JW, Zang L, Sun J, Zheng MH (2014) Completely medial versus hybrid medial approach for laparoscopic complete mesocolic excision in right hemicolon cancer. Surg Endosc 28(2):477–483

    Article  PubMed  Google Scholar 

  35. 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  PubMed  Google Scholar 

  36. Lee SD, Lim SB (2009) D3 lymphadenectomy using a medial to lateral approach for curable right-sided colon cancer. Int J Colorectal Dis 24(3):295–300

    Article  PubMed  Google Scholar 

  37. 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  PubMed  Google Scholar 

  38. Subbiah R, Bansal S, Jain M, Ramakrishnan P, Palanisamy S, Palanivelu PR, Chinusamy P (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  PubMed  Google Scholar 

  39. Trastulli S, Coratti A, Guarino S, Piagnerelli R, Annecchiarico M, Coratti F, Di Marino M, Ricci F, Desiderio J, Cirocchi R, Parisi A (2015) Robotic right colectomy with intracorporeal anastomosis compared with laparoscopic right colectomy with extracorporeal and intracorporeal anastomosis: a retrospective multicentre study. Surg Endosc 29(6):1512–1521

    Article  PubMed  Google Scholar 

  40. Paquette IM, Madoff RD, Sigurdson ER, Chang GJ (2018) Impact of Proximal Vascular Ligation on Survival of Patients with Colon Cancer. Ann Surg Oncol 25(1):38–45

    Article  PubMed  Google Scholar 

  41. Toyota S, Ohta H, Anazawa S (1995) Rationale for extent of lymph node dissection for right colon cancer. Dis Colon Rectum 38:705–711

    Article  CAS  PubMed  Google Scholar 

  42. Hohenberger W, Merkel S, Weber K (2007) Lymphadenektomie bei Tumoren des unteren Gastrointestinaltrakts. Chirurg 78:217–225

    Article  CAS  PubMed  Google Scholar 

  43. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108

    Article  PubMed  Google Scholar 

  44. Alhassan N, Yang M, Wong-Chong N, Liberman AS, Charlebois P, Stein B, Fried GM, Lee L (2019) Comparison between conventional colectomy and complete mesocolic excision for colon cancer: a systematic review and pooled analysis: a review of CME versus conventional colectomies. Surg Endosc 33(1):8–18

    Article  PubMed  Google Scholar 

  45. Kim NK, Kim YW, Han YD, Cho MS, Hur H, Min BS, Lee KY (2016) Complete mesocolic excision and central vascular ligation for colon cancer: Principle, anatomy, surgical technique, and outcomes. Surg Oncol 25(3):252–262

    Article  PubMed  Google Scholar 

  46. Croner RS, Ptok H, Merkel S, Hohenberger W (2018) Implementing complete mesocolic excision for colon cancer—mission completed. Innov Surg Sci 3(1):17–29

    PubMed  PubMed Central  Google Scholar 

  47. Wang C, Gao Z, Shen K, Shen Z, Jiang K, Liang B, Yin M, Yang X, Wang S, Ye Y (2017) Safety, quality and effect of complete mesocolic excision vs non-complete mesocolic excision in patients with colon cancer: a systemic review and meta-analysis. Colorectal Dis 19(11):962–972. https://doi.org/10.1111/codi.13900

    Article  CAS  PubMed  Google Scholar 

  48. Ow ZGW, Sim W, Nistala KRY, Ng CH, Koh FH, Wong NW, Foo FJ, Tan KK, Chong CS (2020) Comparing complete mesocolic excision versus conventional colectomy for colon cancer: A systematic review and meta-analysis. Eur J Surg Oncol 12:S0748-S7983. https://doi.org/10.1016/j.ejso.2020.09.007

    Article  Google Scholar 

  49. Kong JC, Prabhakaran S, Choy KT, Larach JT, Heriot A, Warrier SK (2021) Oncological reasons for performing a complete mesocolic excision: a systematic review and meta-analysis. ANZ J Surg 91(1–2):124–131. https://doi.org/10.1111/ans.16518

    Article  PubMed  Google Scholar 

  50. Dai Q, Tu S, Dong Q, Chen B (2020) Laparoscopic complete mesocolic excision versus noncomplete mesocolic excision: a systematic review and meta-analysis. Surg Laparosc Endosc Percutan Tech 31(1):96–103. https://doi.org/10.1097/SLE.0000000000000845

    Article  PubMed  Google Scholar 

  51. De Simoni O, Barina A, Sommariva A, Tonello M, Gruppo M, Mattara G, Toniato A, Pilati P, Franzato B (2020) 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  PubMed  Google Scholar 

  52. Scarborough JE, Schumacher J, Kent KC, Heise CP, Greenberg CC (2017) Associations of specific postoperative complications with outcomes after elective colon resection: a procedure-targeted approach toward surgical quality improvement. JAMA Surg 152(2):e164681. https://doi.org/10.1001/jamasurg.2016.4681

    Article  PubMed  Google Scholar 

  53. Chapman SJ, EuroSurg Collaborative (2018) Ileus management international (IMAGINE): protocol for a multicentre, observational study of ileus after colorectal surgery. Colorectal Dis 20(1):O17–O25. https://doi.org/10.1111/codi.13976

    Article  CAS  PubMed  Google Scholar 

  54. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213

    Article  PubMed  PubMed Central  Google Scholar 

  55. Strey CW, Wullstein C, Adamina M, Agha A, Aselmann H, Becker T, Grützmann R, Kneist W, Maak M, Mann B, Moesta KT, Runkel N, Schafmayer C, Türler A, Wedel T, Benz S (2018) Laparoscopic right hemicolectomy with CME: standardization using the “critical view” concept. Surg Endosc 32(12):5021–5030

    Article  PubMed  PubMed Central  Google Scholar 

  56. Lu JY, Xu L, Xue HD, Zhou WX, Xu T, Qiu HZ, Wu B, Lin GL, Xiao Y (2016) The radical extent of lymphadenectomy—D2 dissection versus complete mesocolic excision of laparoscopic right colectomy for right-sided colon cancer (RELARC) trial: study protocol for a randomized controlled trial. Trials 17:582

    Article  PubMed  PubMed Central  Google Scholar 

  57. Karachun A, Petrov A, Panaiotti L, Voschinin Y, Ovchinnikova T (2019) Protocol for a multicentre randomized clinical trial comparing oncological outcomes of D2 versus D3 lymph node dissection in colonic cancer (COLD trial). BJS Open 3(3):288–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Neither funds nor grants were received for this research.

Author information

Authors and Affiliations

  1. Department of General and Emergency Surgery, San Filippo Neri Hospital, Rome, Italy

    Gennaro Mazzarella, Edoardo Maria Muttillo, Biagio Picardi, Stefano Rossi & Irnerio Angelo Muttillo

  2. Sapienza University of Rome, Viale del Policlinico 155, 00161, Rome, Italy

    Gennaro Mazzarella & Edoardo Maria Muttillo

Authors
  1. Gennaro Mazzarella
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edoardo Maria Muttillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Biagio Picardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefano Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Irnerio Angelo Muttillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gennaro Mazzarella.

Ethics declarations

Disclosures

Drs. Gennaro Mazzarella, Edoardo Maria Muttillo, Biagio Picardi, Stefano Rossi and Irnerio Angelo Muttillo have no conflicts of interest or financial ties to disclose.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mazzarella, G., Muttillo, E.M., Picardi, B. et al. Complete mesocolic excision and D3 lymphadenectomy with central vascular ligation in right-sided colon cancer: a systematic review of postoperative outcomes, tumor recurrence and overall survival. Surg Endosc 35, 4945–4955 (2021). https://doi.org/10.1007/s00464-021-08529-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-021-08529-4

Keywords

Search

Navigation