Skip to main content

Advertisement

SpringerLink
Log in

Complete mesocolic excision and extended (D3) lymphadenectomy for colonic cancer: is it worth that extra effort? A review of the literature

  • Review
  • Published:
International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Purpose

Recent interest in complete mesocolic excision (CME) with central vascular ligation (CVL) or extended (D3) lymphadenectomy (EL) for curative resection of colon cancer has been driven by published series from experienced practitioners showing excellent survival outcomes and low recurrence rates. In this article, we attempt to clarify the role of CME or EL in modern colorectal surgery.

Methods

A narrative review of the evidence for CME and EL in the curative treatment of colon cancer.

Results

The principal of CME surgery, similar to total mesorectal excision (TME) for rectal cancer, is the removal of all lymphatic, vascular, and neural tissue in the drainage area of the tumour in a complete mesocolic envelope with intact mesentery, peritoneum and encasing fascia. Extended (D3) lymphadenectomy (EL) is based on similar principles. Sound anatomical and oncological arguments are made to support the principles of removing the tumor contained within an intact mesocolic facial envelope together with an extended lymph node harvest. Excellent oncological outcomes with minimal morbidity and mortality have been reported. This has led to calls for the standardisation of surgery for colon cancer using CME. However, there is conflicting evidence regarding the prognostic benefit of greater lymph node harvests and the evidence for an oncological benefit of CME is limited by methodology flaws and several potential confounding factors.

Conclusions

Although there is a reasonable anatomical and oncological basis for these techniques, there are no randomised controlled trials from which to draw confident conclusions and there is insufficient consistent high quality evidence to recommend widespread adoption of CME.

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

Similar content being viewed by others

References

  1. Martling AL, Holm T, Rutqvist LE, Moran BJ, Heald RJ, Cedemark B (2000) Effect of a surgical training programme on outcome of rectal cancer in the County of Stockholm. Stockholm Colorectal Cancer Study Group, Basingstoke Bowel Cancer Research Project. Lancet 356:93–96

    Article  CAS  PubMed  Google Scholar 

  2. Kapiteijn E, Putter H, van de Velde CJ, Cooperative investigators of the Dutch ColoRectal Cancer Group, (2000) Impact of the introduction and training of total mesorectal excision on recurrence and survival in rectal cancer in The Netherlands. Br J Surg 89:1142–1149

    Article  Google Scholar 

  3. Wibe A, Møller B, Norstein J, Carlsen E, Wiig JN, Heald RJ, Langmark F, Myrvold HE, Søreide O, Norwegian Rectal Cancer Group (2002) A national strategic change in treatment policy for rectal cancer—implementation of total mesorectal excision as routine treatment in Norway. A national audit. Dis Colon Rectum 45(7):857–866

    Article  PubMed  Google Scholar 

  4. Sondenaa K, Quirke P, Hohenberger W 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  PubMed  Google Scholar 

  5. Kessler H, Hohenberger W (2013) Extended lymphadenectomy in colon cancer is crucial. World J Surg 37(8):1789–1798

    Article  PubMed  Google Scholar 

  6. West NP, Kobayashi H, Takahashi K et al (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 

  7. Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ et al (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21(15):2912–2919

    Article  PubMed  Google Scholar 

  8. Tsai H-L, Lu C-H, Hsieh J-S et al (2007) The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg 11:660–665

    Article  PubMed  Google Scholar 

  9. 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 

  10. West NP, Morris EJA, Rotimi O, Cairns A, Finan PJ, Quirke P (2008) Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study. Lancet Oncol 9(9):857–865

    Article  PubMed  Google Scholar 

  11. 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 364-355

    Article  CAS  PubMed  Google Scholar 

  12. West NP, Sutton KM, Ingeholm P, Hagemann-Madsen RH, Hohenberger W, Quirke P (2010) Improving the quality of colon cancer surgery through a surgical education program. Dis Colon Rectum 53(12):1594–1603

    Article  PubMed  Google Scholar 

  13. Willaert W, Ceelen W (2015) Extent of surgery in cancer of the colon: is more better? World J Gastroenterol 21(1):132–138

    Article  PubMed  PubMed Central  Google Scholar 

  14. Willaert W, Mareel M, Van De Putte D, Van Nieuwenhove Y, Pattyn P, Ceelen W (2014) Lymphatic spread, nodal count and the extent of lymphadenectomy in cancer of the colon. Cancer Treat Rev 40(3):405–413

    Article  PubMed  Google Scholar 

  15. Liang J, Fazio V, Lavery I, Remzi F, Hull T, Strong S, Church J (2015) Primacy of surgery for colorectal cancer. Br J Surg 102(7):847–852

    Article  CAS  PubMed  Google Scholar 

  16. Rosenberg J, Fischer A, Haglind E (2011) Current controversies in colorectal surgery: the way to resolve uncertainty and move forward. Colorectal Dis 14:266–269

    Article  Google Scholar 

  17. Bertelsen CA, Neuenschwander AU, Jansen JE et al (2015) Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 16(2):161–168

    Article  PubMed  Google Scholar 

  18. Siani LM, Pulica C (2014) 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 57:1169–1175

    Google Scholar 

  19. Kotake K, Mizuguchi T, Moritani K et al (2014) Impact of D3 lymph node dissection on survival for patients with T3 and T4 colon cancer. Int J Colorectal Dis 29(7):847–852

    Article  PubMed  Google Scholar 

  20. Storli KE, Sondenaa K, Furnes B et al (2014) 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 18(6):557–564

    Article  CAS  PubMed  Google Scholar 

  21. Galizia G, Lieto E, De Vita F et al (2014) Is complete mesocolic excision with central vascular ligation safe and effective in the surgical treatment of right-sided colon cancers? A prospective study. Int J Colorectal Dis 29(1):89–97

    Article  PubMed  Google Scholar 

  22. Ovesen SH (2010) Total mesocolic excision versus traditional resection in right-sided colon cancer—method and increased lymph node harvest. Dan Med Bull 57(12):A4224

    PubMed  Google Scholar 

  23. Mukai M, Ito I, Mukoyama S et al (2003) Improvement of 10-year survival by Japanese radical lymph node dissection in patients with Dukes’ B and C colorectal cancer: a 17-year retrospective study. Oncol Rep 10(4):927–934

    PubMed  Google Scholar 

  24. Tagliacozzo S, Accordino M, Tocchi A (1994) Extended lymphadenectomy during resection of cancer of the right colon. Eur J Surg 160(3):179–181

    CAS  PubMed  Google Scholar 

  25. Bokey EL, Chapuis PH, Dent OF, Mander BJ, Bissett IP, Newland RC (2003) Surgical technique and survival in patients having a curative resection for colon cancer. Dis Colon Rectum 46(7):860–866

    Article  CAS  PubMed  Google Scholar 

  26. Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99(6):433–441

    Article  PubMed  Google Scholar 

  27. Liang JT, Lai HS, Huang J, Sun CT (2014) Long-term oncologic results of laparoscopic D3 lymphadenectomy with complete mesocolic excision for right-sided colon cancer with clinically positive lymph nodes. Surg Endosc 29:2394–2401

    Article  PubMed  Google Scholar 

  28. Cho MS, Baek SJ, Hur H, Soh Min B, Baik SH, Kyu KN (2015) Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg 261(4):708–715

    Article  PubMed  Google Scholar 

  29. Shin JW, Amar AH, Kim SH et al (2014) 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 18(9):795–803

    Article  CAS  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. Hashiguchi Y, Hase K, Ueno H, Mochizuki H, Shinto E, Yamamoto J (2011) Optimal margins and lymphadenectomy in colonic cancer surgery. Br J Surg 98(8):1171–1178

    Article  CAS  PubMed  Google Scholar 

  32. Pramateftakis MG (2010) Optimizing colonic cancer surgery: high ligation and complete mesocolic excision during right hemicolectomy. Tech Coloproctol 14(Suppl 1):S49–S51

    Article  PubMed  Google Scholar 

  33. Yao HW, Liu YH (2013) Re-examination of the standardization of colon cancer surgery. Gastroenterol Rep (Oxf) 1(2):113–118

    Article  Google Scholar 

  34. Chow CF, Kim SH (2014) Laparoscopic complete mesocolic excision: west meets east. World J Gastroenterol 20(39):14301–14307

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sehgal R, Coffey JC (2014) Historical development of mesenteric anatomy provides a universally applicable anatomic paradigm for complete/total mesocolic excision. Gastroenterol Rep (Oxf) 2(4):245–250

    Article  Google Scholar 

  36. Culligan K, Coffey JC, Kiran RP, Kalady M, Lavery IC, Remzi FH (2012) The mesocolon: a prospective observational study. Colorectal Dis 14(4):421–428, discussion 428-430

    Article  CAS  PubMed  Google Scholar 

  37. Culligan K, Sehgal R, Mulligan D et al (2014) A detailed appraisal of mesocolic lymphangiology—an immunohistochemical and stereological analysis. J Anat 225(4):463–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Watanabe T, Itabashi M, Shimada Y et al (2012) Japanese Society for Cancer of the Colon and Rectum. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol 17(1):1–29

    Article  PubMed  Google Scholar 

  39. Chen SL, Bilchik AJ (2006) More extensive nodal dissection improves survival for stages I to III of colon cancer: a population-based study. Ann Surg 244(4):602–610

    PubMed  PubMed Central  Google Scholar 

  40. Johnson PM, Porter GA, Ricciardi R, Baxter NN (2006) Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol 24(22):3570–3575

    Article  PubMed  Google Scholar 

  41. Parnaby CN, Scott NW, Ramsay G, MacKay C, Samuel L, Murray GI, Loudon MA (2015) Prognostic value of lymph node ratio and extramural vascular invasion on survival for patients undergoing curative colon cancer resection. Br J Cancer. doi:10.1038/bjc.2015.211

    PubMed  PubMed Central  Google Scholar 

  42. Lykke J, Roikjaer O, Jess P, Danish Colorectal Cancer Group (2013) The relation between lymph node status and survival in Stage I-III colon cancer: results from a prospective nationwide cohort study. Colorectal Dis 15(5):559–565

    Article  CAS  PubMed  Google Scholar 

  43. Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H, Siewert JR (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3,026 patients over a 25-year time period. Ann Surg 248(6):968–978

    Article  PubMed  Google Scholar 

  44. Liang JT, Huang KC, Lai HS, Lee PH, Sun CT (2007) Oncologic results of laparoscopic D3 lymphadenectomy for male sigmoid and upper rectal cancer with clinically positive lymph nodes. Ann Surg Oncol 14(7):1980–1990

    Article  PubMed  Google Scholar 

  45. Toyota S, Ohta H, Anazawa S (1995) Rationale for extent of lymph node dissection for right colon cancer. Dis Colon Rectum 38(7):705–711

    Article  CAS  PubMed  Google Scholar 

  46. Færden AE, Sjo OH, Bukholm IR, Andersen SN, Svindland A, Nesbakken A, Bakka A (2011) Lymph node micrometastases and isolated tumor cells influence survival in stage I and II colon cancer. Dis Colon Rectum 54(2):200–206

    Article  PubMed  Google Scholar 

  47. Murphy J, Young-Fadok T (2013) Extended lymphadenectomy in colon cancer is debatable. World J Surg 37(8):1799–1807

    Article  PubMed  Google Scholar 

  48. 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 

  49. Nash GM, Row D, Weiss A et al (2011) A predictive model for lymph node yield in colon cancer resection specimens. Ann Surg 253(2):318–322

  50. Bläker H, Hildebrandt B, Riess H, von Winterfeld M et al (2015) Lymph node count and prognosis in colorectal cancer: the influence of examination quality. Int J Cancer 136(8):1957–1966

    Article  PubMed  Google Scholar 

  51. Moro-Valdezate D, Pla-Martí V, Martín-Arévalo J et al (2013) Factors related to lymph node harvest: does a recovery of more than 12 improve the outcome of colorectal cancer? Colorectal Dis 15(10):1257–1266

    Article  CAS  PubMed  Google Scholar 

  52. Tsikitis VL, Larson DL, Wolff BG, Kennedy G, Diehl N, Qin R, Dozois EJ, Cima RR (2009) Survival in stage III colon cancer is independent of the total number of lymph nodes retrieved. J Am Coll Surg 208(1):42–47

    Article  PubMed  Google Scholar 

  53. Gleisner AL, Mogal H, Dodson R et al (2013) Nodal status, number of lymph nodes examined, and lymph node ratio: what defines prognosis after resection of colon adenocarcinoma? J Am Coll Surg 217(6):1090–1100

    Article  PubMed  Google Scholar 

  54. Cirocchi R, Trastulli S, Farinella E et al (2012) High tie versus low tie of the inferior mesenteric artery in colorectal cancer: a RCT is needed. Surg Oncol 21(3):e111–e123

    Article  PubMed  Google Scholar 

  55. Titu LV, Tweedle E, Rooney PS (2008) High tie of the inferior mesenteric artery in curative surgery for left colonic and rectal cancers: a systematic review. Dig Surg 25(2):148–157

    Article  CAS  PubMed  Google Scholar 

  56. Hida J, Okuno K (2013) High ligation of the inferior mesenteric artery in rectal cancer surgery. Surg Today 43(1):8–19

    Article  PubMed  Google Scholar 

  57. Hida J, Okuno K, Yasutomi M, Yoshifuji T, Uchida T, Tokoro T, Shiozaki H (2005) Optimal ligation level of the primary feeding artery and bowel resection margin in colon cancer surgery: the influence of the site of the primary feeding artery. Dis Colon Rectum 48(12):2232–2237

    Article  PubMed  Google Scholar 

  58. Chen H, Wang Y, Liu H et al (2015) Factors influencing apical node metastasis in colorectal cancer patients treated with laparoscopic radical resection with D3 lymphadenectomy: results from two centers in China. Surg Today 45(5):569–575

    Article  CAS  PubMed  Google Scholar 

  59. Lan YT, Lin JK, Jiang JK (2011) Significance of lymph node retrieval from the terminal ileum for patients with cecal and ascending colonic cancers. Ann Surg Oncol 18(1):146–152

    Article  PubMed  Google Scholar 

  60. Ang CW, Tweedle EM, Campbell F, Rooney PS (2011) Apical node metastasis independently predicts poor survival in Dukes C colorectal cancer. Colorectal Dis 13:526–531

    Article  CAS  PubMed  Google Scholar 

  61. Monga DK, O’Connell MJ (2006) Surgical adjuvant therapy for colorectal cancer: current approaches and future directions. Ann Surg Oncol 13(8):1021–1034

    Article  PubMed  Google Scholar 

  62. Killeen S, Mannion M, Devaney A, Winter DC (2014) Complete mesocolic resection and extended lymphadenectomy for colon cancer: a systematic review. Colorectal Dis 16(8):577–594

    Article  CAS  PubMed  Google Scholar 

  63. Siani LM, Pulica C (2014) Stage I-IIIC right colonic cancer treated with complete mesocolic excision and central vascular ligation: quality of surgical specimen and long term oncologic outcome according to the plane of surgery. Minerva Chir 69(4):199–208

    CAS  PubMed  Google Scholar 

  64. West NP, Kennedy RH, Magro T 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  PubMed  Google Scholar 

  65. Gouvas N, Pechlivanides G, Zervakis N, Kafousi M, Xynos E (2012) Complete mesocolic excision in colon cancer surgery: a comparison between open and laparoscopic approach. Colorectal Dis 14(11):1357–1364

    Article  CAS  PubMed  Google Scholar 

  66. Yamamoto S, Inomata M, Katayama H et al (2014) 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 260(1):23–30

    Article  PubMed  Google Scholar 

  67. Storli KE, Sondenaa K, Furnes B, Eide GE (2013) Outcome after introduction of complete mesocolic excision for colon cancer is similar for open and laparoscopic surgical treatments. Dig Surg 30(4-6):317–327

    Article  PubMed  Google Scholar 

  68. Han DP, Lu AG, Feng H et al (2014) Long-term outcome of laparoscopic-assisted right-hemicolectomy with D3 lymphadenectomy versus open surgery for colon carcinoma. Surg Today 44(5):868–874

    Article  PubMed  Google Scholar 

  69. Zhao LY, Liu H, Wang YN, Deng HJ, Xue Q, Li GX (2014) Techniques and feasibility of laparoscopic extended right hemicolectomy with D3 lymphadenectomy. World J Gastroenterol 20(30):10531–10536

    Article  PubMed  PubMed Central  Google Scholar 

  70. Bae SU, Saklani AP, Lim DR 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  PubMed  Google Scholar 

  71. Han DP, Lu AG, Feng H et al (2013) Long-term results of laparoscopy-assisted radical right hemicolectomy with D3 lymphadenectomy: clinical analysis with 177 cases. Int J Colorectal Dis 28(5):623–629

    Article  PubMed  Google Scholar 

  72. Mori S, Baba K, Yanagi M 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  PubMed  Google Scholar 

  73. Takemasa I, Uemura M, Nishimura J 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  PubMed  Google Scholar 

  74. Munkedal DL, West NP, Iversen LH, Hagemann-Madsen R, Quirke P, Laurberg S (2014) Implementation of complete mesocolic excision at a university hospital in Denmark: an audit of consecutive, prospectively collected colon cancer specimens. Eur J Surg Oncol 40(11):1494–1501

    Article  CAS  PubMed  Google Scholar 

  75. Nakajima K, Inomata M, Akagi T et al (2014) Quality control by photo documentation for evaluation of laparoscopic and open colectomy with D3 resection for stage II/III colorectal cancer: Japan Clinical Oncology Group Study JCOG 0404. Jpn J Clin Oncol 44(9):799–806

    Article  PubMed  Google Scholar 

  76. Kobayashi H, West NP, Takahashi K et al (2014) Quality of surgery for stage III colon cancer: comparison between England, Germany, and Japan. Ann Surg Oncol 21(Suppl 3):S398–S404

    Article  PubMed  Google Scholar 

  77. Kontovounisios C, Kinross J, Tan E, Brown G, Rasheed S, Tekkis P (2015) Complete mesocolic excision in colorectal cancer: a systematic review. Colorectal Dis 17(1):7–16

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Colorectal Surgery, King’s College Hospital, King’s College Hospital NHS Foundation Trust, 2nd Floor Hambelden Wing, Denmark Hill, London, SE5 9RS, UK

    Andrew Emmanuel & Amyn Haji

Authors
  1. Andrew Emmanuel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amyn Haji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew Emmanuel.

Ethics declarations

Author contributions

A. Emmanuel and A. Haji were involved in the concept and design of the review. A. Emmanuel performed the literature review and wrote the text. A. Haji reviewed the manuscript and made corrections and revisions.

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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 31, 797–804 (2016). https://doi.org/10.1007/s00384-016-2502-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00384-016-2502-0

Keywords

Search

Navigation