International Journal of Colorectal Disease

, Volume 31, Issue 9, pp 1577–1594 | Cite as

Surgery along the embryological planes for colon cancer: a systematic review of complete mesocolic excision

  • Nikolaos Gouvas
  • Christos Agalianos
  • Kleio Papaparaskeva
  • Aristotelis Perrakis
  • Werner Hohenberger
  • Evaghelos Xynos



Complete mesocolic excision (CME) for colonic cancer offers a surgical specimen of higher quality, with higher number of lymph nodes compared to conventional colectomy. However, evidence on oncological outcomes is limited. The aim of the present study is to review recent literature and provide more information regarding the effect of CME colectomy on short- and long-term outcomes.


PubMed and MEDLINE databases were searched, and articles in English reporting data on CME were reviewed. Intraoperative events; postoperative morbidity and mortality; histopathological characteristics, including macroscopic assessment, number, and status of retrieved lymph nodes; and oncological outcomes were the end-points.


Thirty-two studies were analyzed. As regards the macroscopic assessment, a larger specimen (p = 0.02) that contains a higher number of lymph nodes (p < 0.00001) is acquired after CME. Two studies report a higher disease-free survival, in stage I and II and particularly in stage III disease after CME. CME by laparoscopy offers comparable outcomes, as regards intraoperative blood loss and immediate postoperative morbidity and mortality rates. Specimen quality is similar after either approach, for cancers located at the right and left colon, but not at the transverse colon.


There is strong evidence that CME offers a longer central pedicle that contains more lymph nodes than conventional surgery for colon cancer. CME represents the surgical background for the maximum lymph node harvest, an important quality marker for the surgical outcome. However, and according to present data, there is limited evidence that colectomy in terms of CME leads to improved long-term oncological outcomes.


Complete mesocolic excision Central vascular ligation Colon cancer Systematic review Meta-analysis 


  1. 1.
    Heald RJ, Ryall RD (1986) Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1(8496):1479–1482CrossRefPubMedGoogle Scholar
  2. 2.
    Quirke P, Steele R, Monson J, Grieve R, Khanna S, Couture J, O'Callaghan C, Myint AS, Bessell E, Thompson LC, Parmar M, Stephens RJ, Sebag-Montefiore D, Investigators MCN-CCT, Group NCCS (2009) Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG CO16 randomised clinical trial. Lancet 373(9666):821–828. doi: 10.1016/S0140-6736(09)60485-2 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Wibe A, Moller B, Norstein J, Carlsen E, Wiig JN, Heald RJ, Langmark F, Myrvold HE, Soreide O, Norwegian Rectal Cancer G (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):857–866CrossRefPubMedGoogle Scholar
  4. 4.
    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. Color Dis : Off J Assoc Coloproctology Great Britain Ireland 11(4):354–364 . doi: 10.1111/j.1463-1318.2008.01735.xdiscussion 364-355CrossRefGoogle Scholar
  5. 5.
    West NP, Morris EJ, 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. doi: 10.1016/S1470-2045(08)70181-5 CrossRefPubMedGoogle Scholar
  6. 6.
    Chow CF, Kim SH (2014) Laparoscopic complete mesocolic excision: West meets East. World J Gastroenterol : WJG 20(39):14301–14307. doi: 10.3748/wjg.v20.i39.14301 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Culligan K, Remzi FH, Soop M, Coffey JC (2013) Review of nomenclature in colonic surgery—proposal of a standardised nomenclature based on mesocolic anatomy. Surg : J Royal Coll Surg Edinb Ireland 11(1):1–5. doi: 10.1016/j.surge.2012.01.006 Google Scholar
  8. 8.
    Killeen S, Mannion M, Devaney A, Winter DC (2014) Complete mesocolic resection and extended lymphadenectomy for colon cancer: a systematic review. Color Dis : Off J Assoc Coloproctology Great Britain Ireland 16(8):577–594. doi: 10.1111/codi.12616 CrossRefGoogle Scholar
  9. 9.
    Kontovounisios C, Kinross J, Tan E, Brown G, Rasheed S, Tekkis P (2015) Complete mesocolic excision in colorectal cancer: a systematic review. Color Dis : Off J Assoc Coloproctology Great Britain Ireland 17(1):7–16. doi: 10.1111/codi.12793 CrossRefGoogle Scholar
  10. 10.
    Adamina M, Manwaring ML, Park KJ, Delaney CP (2012) Laparoscopic complete mesocolic excision for right colon cancer. Surg Endosc 26(10):2976–2980. doi: 10.1007/s00464-012-2294-4 CrossRefPubMedGoogle Scholar
  11. 11.
    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. doi: 10.1245/s10434-014-3614-9 CrossRefPubMedGoogle Scholar
  12. 12.
    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? Color Dis : Off J Assoc Coloproctology Great Britain Ireland 13(10):1123–1129. doi: 10.1111/j.1463-1318.2010.02474.x CrossRefGoogle Scholar
  13. 13.
    Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Iversen ER, Kristensen B, Gogenur I, Danish Colorectal Cancer G (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. doi: 10.1016/S1470-2045(14)71168-4 CrossRefPubMedGoogle Scholar
  14. 14.
    Cho MS, Baek SJ, Hur H, Soh Min B, Baik SH, Kyu Kim N (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. doi: 10.1097/SLA.0000000000000831 CrossRefPubMedGoogle Scholar
  15. 15.
    Eiholm S, Ovesen H (2010) Total mesocolic excision versus traditional resection in right-sided colon cancer—method and increased lymph node harvest. Dan Med Bull 57(12):A4224PubMedGoogle Scholar
  16. 16.
    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. doi: 10.1007/s00464-013-3225-8 CrossRefPubMedGoogle Scholar
  17. 17.
    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. doi: 10.1007/s00464-012-2435-9 CrossRefPubMedGoogle Scholar
  18. 18.
    Galizia G, Lieto E, De Vita F, Ferraraccio F, Zamboli A, Mabilia A, Auricchio A, Castellano P, Napolitano V, Orditura M (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 Color Dis 29(1):89–97. doi: 10.1007/s00384-013-1766-x CrossRefGoogle Scholar
  19. 19.
    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. Color Dis : Off J Assoc Coloproctology Great Britain Ireland 14(11):1357–1364. doi: 10.1111/j.1463-1318.2012.03019.x CrossRefGoogle Scholar
  20. 20.
    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. doi: 10.1002/bjs.7518 CrossRefPubMedGoogle Scholar
  21. 21.
    Kang J, Kim IK, Kang SI, Sohn SK, Lee KY (2014) Laparoscopic right hemicolectomy with complete mesocolic excision. Surg Endosc 28(9):2747–2751. doi: 10.1007/s00464-014-3521-y CrossRefPubMedGoogle Scholar
  22. 22.
    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(Suppl 3):S398–S404. doi: 10.1245/s10434-014-3578-9 CrossRefPubMedGoogle Scholar
  23. 23.
    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. doi: 10.1007/s00464-014-3940-9 CrossRefPubMedGoogle Scholar
  24. 24.
    Matsuda T, Iwasaki T, Mitsutsuji M, Hirata K, Maekawa Y, Tanaka T, Shimada E, Kakeji Y (2015) Cranial-to-caudal approach for radical lymph node dissection along the surgical trunk in laparoscopic right hemicolectomy. Surg Endosc 29(4):1001. doi: 10.1007/s00464-014-3761-x CrossRefPubMedGoogle Scholar
  25. 25.
    Melich G, Jeong DH, Hur H, Baik SH, Faria J, Kim NK, Min BS (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):331–336CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Mori S, Baba K, Yanagi M, Kita Y, Yanagita S, Uchikado Y, Arigami T, Uenosono Y, Okumura H, Nakajo A, Maemuras K, Ishigami S, Natsugoe S (2015) Laparoscopic complete mesocolic excision with radical lymph node dissection along the surgical trunk for right colon cancer. Surg Endosc 29(1):34–40. doi: 10.1007/s00464-014-3650-3 CrossRefPubMedGoogle Scholar
  27. 27.
    Mori S, Kita Y, Baba K, Yanagi M, Okumura H, Natsugoe S (2015) Laparoscopic complete mesocolic excision via reduced port surgery for treatment of colon cancer. Dig Surg 32(1):45–51. doi: 10.1159/000373895 CrossRefPubMedGoogle Scholar
  28. 28.
    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. doi: 10.1016/j.ejso.2014.04.004 CrossRefPubMedGoogle Scholar
  29. 29.
    Nakajima K, Inomata M, Akagi T, Etoh T, Sugihara K, Watanabe M, Yamamoto S, Katayama H, Moriya Y, Kitano S (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. doi: 10.1093/jjco/hyu083 CrossRefPubMedGoogle Scholar
  30. 30.
    Perrakis A, Weber K, Merkel S, Matzel K, Agaimy A, Gebbert C, Hohenberger W (2014) Lymph node metastasis of carcinomas of transverse colon including flexures. Consideration of the extramesocolic lymph node stations. Int J Color Dis 29(10):1223–1229. doi: 10.1007/s00384-014-1971-2 CrossRefGoogle Scholar
  31. 31.
    Pramateftakis MG (2010) Optimizing colonic cancer surgery: high ligation and complete mesocolic excision during right hemicolectomy. Tech Coloproctol 14(Suppl 1):S49–S51. doi: 10.1007/s10151-010-0609-9 CrossRefPubMedGoogle Scholar
  32. 32.
    Shin JW, Amar AH, Kim SH, Kwak JM, Baek SJ, Cho JS, Kim J (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. doi: 10.1007/s10151-014-1134-z CrossRefPubMedGoogle Scholar
  33. 33.
    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):199–208Google Scholar
  34. 34.
    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. doi: 10.1177/1457496914557017 CrossRefPubMedGoogle Scholar
  35. 35.
    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. doi: 10.1159/000354580 CrossRefPubMedGoogle Scholar
  36. 36.
    Storli KE, Sondenaa K, Furnes B, Nesvik I, Gudlaugsson E, Bukholm I, Eide GE (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. doi: 10.1007/s10151-013-1100-1 CrossRefPubMedGoogle Scholar
  37. 37.
    Takemasa I, Uemura M, Nishimura J, Mizushima T, Yamamoto H, Ikeda M, Sekimoto M, Doki Y, Mori M (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. doi: 10.1007/s00464-013-3284-x CrossRefPubMedGoogle Scholar
  38. 38.
    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. doi: 10.1200/JCO.2009.24.1448 CrossRefPubMedGoogle Scholar
  39. 39.
    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. doi: 10.1200/JCO.2011.38.3992 CrossRefPubMedGoogle Scholar
  40. 40.
    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. doi: 10.1007/DCR.0b013e3181f433e3 CrossRefPubMedGoogle Scholar
  41. 41.
    West NP, Kennedy RH, Magro T, Luglio G, Sala S, Jenkins JT, Quirke P (2014) Morphometric analysis and lymph node yield in laparoscopic complete mesocolic excision performed by supervised trainees. Br J Surg 101(11):1460–1467. doi: 10.1002/bjs.9602 CrossRefPubMedGoogle Scholar
  42. 42.
    Gao Z, Ye Y, Zhang W, Shen D, Zhong Y, Jiang K, Yang X, Yin M, Liang B, Tian L, Wang S (2013) An anatomical, histopathological, and molecular biological function study of the fascias posterior to the interperitoneal colon and its associated mesocolon: their relevance to colonic surgery. J Anat 223(2):123–132. doi: 10.1111/joa.12066 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ, Haller DG (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. doi: 10.1200/JCO.2003.05.062 CrossRefPubMedGoogle Scholar
  44. 44.
    Moore J, Hyman N, Callas P, Littenberg B (2010) Staging error does not explain the relationship between the number of lymph nodes in a colon cancer specimen and survival. Surgery 147(3):358–365. doi: 10.1016/j.surg.2009.10.003 CrossRefPubMedGoogle Scholar
  45. 45.
    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. doi: 10.1245/s10434-007-9368-x CrossRefPubMedGoogle Scholar
  46. 46.
    Ingeholm P (2012) Annual report 2012 of the Danish Colorectal Cancer Group. Danish Colorectal Cancer Group,Google Scholar
  47. 47.
    Rose J, Augestad KM, Cooper GS (2014) Colorectal cancer surveillance: what's new and what's next. World J Gastroenterol: WJG 20(8):1887–1897. doi: 10.3748/wjg.v20.i8.1887 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Nikolaos Gouvas
    • 1
  • Christos Agalianos
    • 2
  • Kleio Papaparaskeva
    • 3
  • Aristotelis Perrakis
    • 4
  • Werner Hohenberger
    • 4
  • Evaghelos Xynos
    • 5
  1. 1.Department of General SurgeryMetropolitan HospitalPireusGreece
  2. 2.Department of General SurgeryNaval & Veterans HospitalAthensGreece
  3. 3.Department of PathologyKonstantopouleio Hospital of AthensAthensGreece
  4. 4.Department of SurgeryUniversity Hospital of ErlangenErlangenGermany
  5. 5.Department of General SurgeryCreta InterClinic HospitalHeraklionGreece

Personalised recommendations