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

G Anania, R J Davies, F Bagolini, N Vettoretto, J Randolph, R Cirocchi, A Donini, G Anania, R J Davies, F Bagolini, N Vettoretto, J Randolph, R Cirocchi, A Donini

Abstract

Background: The introduction of complete mesocolic excision (CME) for right colon cancer has raised an important discussion in relation to the extent of colic and mesenteric resection, and the impact this may have on lymph node yield. As uncertainty remains regarding the usefulness of and indications for right hemicolectomy with CME and the benefits of CME compared with a traditional approach, the purpose of this meta-analysis is to compare the two procedures in terms of safety, lymph node yield and oncological outcome.

Methods: We performed a systematic review of the literature from 2009 up to March 15th, 2020 according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Two hundred eighty-one publications were evaluated, and 17 met the inclusion criteria and were included. Primary endpoints analysed were anastomotic leak rate, blood loss, number of harvested lymph nodes, 3- and 5-year oncologic outcomes. Secondary outcomes were operating time, conversion, intraoperative complications, reoperation rate, overall and Clavien-Dindo grade 3-4 postoperative complications.

Results: In terms of safety, right hemicolectomy with CME is not inferior to the standard procedure when comparing rates of anastomotic leak (RR 0.82, 95% CI 0.38-1.79), blood loss (MD -32.48, 95% CI -98.54 to -33.58), overall postoperative complications (RR 0.82, 95% CI 0.67-1.00), Clavien-Dindo grade III-IV postoperative complications (RR 1.36, 95% CI 0.82-2.28) and reoperation rate (RR 0.65, 95% CI 0.26-1.75). Traditional surgery is associated with a shorter operating time (MD 16.43, 95% CI 4.27-28.60) and lower conversion from laparoscopic to open approach (RR 1.72, 95% CI 1.00-2.96). In terms of oncologic outcomes, right hemicolectomy with CME leads to a higher lymph node yield than traditional surgery (MD 7.05, 95% CI 4.06-10.04). Results of statistical analysis comparing 3-year overall survival and 5-year disease-free survival were better in the CME group, RR 0.42, 95% CI 0.27-0.66 and RR 0.36, 95% CI 0.17-0.56, respectively.

Conclusions: Right hemicolectomy with CME is not inferior to traditional surgery in terms of safety and has a greater lymph node yield when compared with traditional surgery. Moreover, right-sided CME is associated with better overall and disease-free survival.

Keywords: CME; Colon cancer; Complete mesocolic excision; Lymph node yield; Meta-analysis; Safety.

Conflict of interest statement

The authors declare that they have no conflict of interest.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
Prisma flowchart of literature search
Fig. 2
Fig. 2
The risk of bias according to ROBINS-I tool
Fig. 3
Fig. 3
GRADE Working Group grades of evidence
Fig. 4
Fig. 4
Anastomotic leak
Fig. 5
Fig. 5
Blood loss
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Fig. 6
Lymph node yield
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Oncological outcomes: overall survival at 3 years
Fig. 8
Fig. 8
Oncological outcomes: disease-free survival at 5 years

References

    1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi: 10.3322/caac.21492.
    1. Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. Rectal cancer, version 2.2018 clinical practice guidelines in Oncology. J Natl Compr Canc Netw. 2018;16(7):874–901. doi: 10.6004/jnccn.2018.0061.
    1. Garcia-Granero A, Pellino G, Frasson M, Fletcher-Sanfeliu D, Bonilla F, Sánchez-Guillén L, et al. The fusion fascia of Fredet: an important embryological landmark for complete mesocolic excision and D3-lymphadenectomy in right colon cancer. Surg Endosc. 2019;33(11):3842–3850. doi: 10.1007/s00464-019-06869-w.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–1012. doi: 10.1016/j.jclinepi.2009.06.005.
    1. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205–213. doi: 10.1097/.
    1. JPT Higgins S Green (2011) Cochrane handbook for systematic reviews of interventions version5.1.0. The cochrane collaboration. Updated Mar 2011
    1. Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919. doi: 10.1136/bmj.i4919.
    1. McGuinness LA, Higgins JPT. Risk-of-bias visualization (robvis): an R package and Shiny web app for visualizing risk-of-bias assessments. Res Syn Meth. 2020 doi: 10.1002/jrsm.1411.
    1. Schünemann H, Brożek J, Guyatt G, Oxman A (2013) GRADE handbook for grading quality of evidence and strength of recommendations. Updated Oct 2013. The GRADE working group at, . Accessed 17 Apr 2021
    1. Athanasiou CD, Markides GA, Kotb A, Jia X, Gonsalves S, Miskovic D. Open compared with laparoscopic complete mesocolic excision with central lymphadenectomy for colon cancer: a systematic review and meta-analysis. USA: Blackwell Publishing Ltd; 2016. pp. O224–O235.
    1. Bertelsen CA, Neuenschwander AU, Jansen JE, Tenma JR, Wilhelmsen M, Kirkegaard-Klitbo A, et al. 5-year outcome after complete mesocolic excision for right-sided colon cancer: a population-based cohort study. Lancet Oncol. 2019;20(11):1556–1565. doi: 10.1016/S1470-2045(19)30485-1.
    1. Brunner M, Weber GF, Wiesmüller F, Weber K, Maak M, Kersting S, et al. Laparoscopic right hemicolectomy with complete mesocolic excision (CME) Zentralblatt fur Chirurgie - Zeitschrift fur Allgemeine, Viszeral- und Gefasschirurgie. 2020;145(1):17–23. doi: 10.1055/a-1024-4629.
    1. Gouvas N, Agalianos C, Papaparaskeva K, Perrakis A, Hohenberger W, Xynos E. Surgery along the embryological planes for colon cancer: a systematic review of complete mesocolic excision. Int J Colorectal Dis. 2016;31:1577–1594. doi: 10.1007/s00384-016-2626-2.
    1. Lu JY, Xu L, Xue HD, Zhou WX, Xu T, Qiu HZ, et al. 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. 2016;17(1):582. doi: 10.1186/s13063-016-1710-9.
    1. Olofsson F, Buchwald P, Elmståhl S, Syk I. No benefit of extended mesenteric resection with central vascular ligation in right-sided colon cancer. Colorectal Dis. 2016;18(8):773–778. doi: 10.1111/codi.13305.
    1. Rinne JK, Ehrlich A, Ward J, Väyrynen V, Laine M, Kellokumpu IH, et al. Laparoscopic colectomy vs laparoscopic CME: a retrospective study of two hospitals with comparable laparoscopic experience. J Gastroint Surg. 2020 doi: 10.1007/s11605-019-04502-8.
    1. Schulte Am Esch J, Iosivan SI, Steinfurth F, Mahdi A, Förster C, Wilkens L, et al. A standardized suprapubic bottom-to-up approach in robotic right colectomy: Technical and oncological advances for complete mesocolic excision (CME) BMC Surg. 2019;19(1):72. doi: 10.1186/s12893-019-0544-2.
    1. Siani LM, Garulli G. Laparoscopic complete mesocolic excision with central vascular ligation in right colon cancer: a comprehensive review. WJGS. 2016;8(2):106. doi: 10.4240/wjgs.v8.i2.106.
    1. 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(4):219–226. doi: 10.1177/1457496914557017.
    1. Tagliacozzo S, Tocchi A. Extended mesenteric excision in right hemicolectomy for carcinoma of the colon. Int J Colorectal Dis. 1997;12(5):272–275. doi: 10.1007/s003840050104.
    1. Thorsen Y, Stimec B, Andersen SN, Lindstrom JC, Pfeffer F, Oresland T, et al. Bowel function and quality of life after superior mesenteric nerve plexus transection in right colectomy with D3 extended mesenterectomy. Tech Coloproctol. 2016;20(7):445–453. doi: 10.1007/s10151-016-1466-y.
    1. Wang C, Gao Z, Shen K, Shen Z, Jiang K, Liang B, et al. Safety, quality and effect of complete mesocolic excision vs non-complete mesocolic excision in patients with colon cancer: a systemic review and meta-analysis. Blackwell Publishing Ltd; 2017. pp. 962–972.
    1. Yang X, Wu Q, Jin C, He W, Wang M, Yang T, et al. A novel hand-assisted laparoscopic versus conventional laparoscopic right hemicolectomy for right colon cancer: Study protocol for a randomized controlled trial. Trials. 2017;18(1):355. doi: 10.1186/s13063-017-2084-3.
    1. Zenger S, Balik E, Bugra D. Complete mesocolic excision for right colon cancer. Ann Laparoscopic Endoscopic Surg. 2019;4:70. doi: 10.21037/ales.2019.07.08.
    1. Merkel S, Weber K, Matzel KE, Agaimy A, Göhl J, Hohenberger W. Prognosis of patients with colonic carcinoma before, during and after implementation of complete mesocolic excision. Br J Surg. 2016;103(9):1220–1229. doi: 10.1002/bjs.10183.
    1. Feng H, Zhao XW, Zhang Z, Han DP, Mao ZH, Lu AG, et al. Laparoscopic complete mesocolic excision for stage II/III left-sided colon cancers: a prospective study and comparison with D3 lymph node dissection. J Laparoendosc Adv Surg Tech A. 2016;26(8):606–613. doi: 10.1089/lap.2016.0120.
    1. Bertelsen CA, Neuenschwander AU, Jansen JE, Kirkegaard-Klitbo A, Tenma JR, Wilhelmsen M, et al. Short-term outcomes after complete mesocolic excision compared with 'conventional' colonic cancer surgery. Br J Surg. 2016;103(5):581–589. doi: 10.1002/bjs.10083.
    1. Storli KE, Søndenaa K, Furnes B, Nesvik I, Gudlaugsson E, Bukholm I, 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(6):557–564. doi: 10.1007/s10151-013-1100-1.
    1. Bertelsen CA, Bols B, Ingeholm P, Jansen JE, Neuenschwander AU, Vilandt J. Can the quality of colonic surgery be improved by standardization of surgical technique with complete mesocolic excision? Colorectal Dis. 2011;13(10):1123–1129. doi: 10.1111/j.1463-1318.2010.02474.x.
    1. Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol. 2015;16(2):161–168. doi: 10.1016/S1470-2045(14)71168-4.
    1. Kobayashi H, West NP, Takahashi K, Perrakis A, Weber K, Hohenberger W, et al. Quality of surgery for stage III colon cancer: comparison between England, Germany, and Japan. Ann Surg Oncol. 2014;21(Suppl 3):S398–404. doi: 10.1245/s10434-014-3578-9.
    1. West NP, Hohenberger W, Weber K, Perrakis A, Finan PJ, Quirke P. 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(2):272–278. doi: 10.1200/JCO.2009.24.1448.
    1. Vajda K, Horti I, Cserni G, Bori R, Sikorszki L. Laparoscopic and open complete mesocolic excision in right-sided colon cancer compared with open and laparoscopic surgery. Magy Seb. 2020;73(1):23–28. doi: 10.1556/1046.73.2020.1.3.
    1. An MS, Baik HJ, Oh SH, Park YH, Seo SH, Kim KH, et al. Oncological outcomes of complete versus conventional mesocolic excision in laparoscopic right hemicolectomy. ANZ J Surg. 2018;88(10):E698–E702. doi: 10.1111/ans.14493.
    1. Bertelsen CA, Larsen HM, Neuenschwander AU, Laurberg S, Kristensen B, Emmertsen KJ. Long-term functional outcome after right-sided complete mesocolic excision compared with conventional colon cancer surgery: a population-based questionnaire study. Dis Colon Rectum. 2018;61(9):1063–1072. doi: 10.1097/DCR.0000000000001154.
    1. Cao J, Ji Y, Yang P, et al. A study on laparoscopic complete mesocolic excision for elderly patients with right-sided colon cancer. J Laparosc Surg. 2018;23(10):778–781.
    1. Galizia G, Lieto E, De Vita F, Ferraraccio F, Zamboli A, Mabilia A, et al. 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. 2014;29(1):89–97. doi: 10.1007/s00384-013-1766-x.
    1. Gao ZD, Ye YJ, Wang S, Yang XD, Yin MJ, Liang B, et al. Complete mesocolic excision versus traditional radical resection in colon cancer. Chin J Gastrointest Surg. 2012;15(1):19–23.
    1. Ho ML, Chong C, Yeo SA, Ng CY, Shen Ann EY. Initial experience of laparoscopic right hemicolectomy with complete mesocolic excision in Singapore: a case series. Singapore Med J. 2019;60(5):247–252. doi: 10.11622/smedj.2019008.
    1. Lieto E, Abdelkhalek M, Orditura M, Denewer A, Castellano P, Youssef TF, et al. Propensity score-matched comparison between complete mesocolic excision and classic right hemicolectomy for colon cancer. Minerva Chir. 2018;73(1):1–12.
    1. Liu SQ, Zhao XW, Liang ZH, Hua W, Han YF, Surgery G, et al. Comparison of lymph node dissection and short-term efficacy between laparoscopic complete mesocolic excision and laparoscopic traditional radical resection for colon cancer. China J Endoscopy. 2015;21(8):794.
    1. Ouyang M, Luo Z, Wu J, Zhang W, Tang S, Lu Y, et al. Comparison of outcomes of complete mesocolic excision with conventional radical resection performed by laparoscopic approach for right colon cancer. Cancer Manage Res. 2019;11:8647–8656. doi: 10.2147/CMAR.S203150.
    1. Pedrazzani C, Lazzarini E, Turri G, Conti C, Secci F, Tripepi M, et al. Complete mesocolic excision versus standard laparoscopic colectomy in right-sided colon cancer: analysis of short-term results from a single italian center. Eur J Surg Oncol. 2020;46(2):e95.
    1. Prevost GA, Odermatt M, Furrer M, Villiger P. Postoperative morbidity of complete mesocolic excision and central vascular ligation in right colectomy: a retrospective comparative cohort study. World J Surg Oncol. 2018;16(1):214. doi: 10.1186/s12957-018-1514-3.
    1. Procházka V, Zetelová A, Grolich T, Frola L, Kala Z. Kompletní mezokolická excize u pravostranné hemikolektomie. Rozhledy v chirurgii : mesicnik Ceskoslovenske chirurgicke spolecnosti. 2016;95(10):359–364.
    1. Qin S, Yu M, Mu Y, Qi Y, Qiu Y, Luo Y, et al. Efficacy of complete mesocolic excision in radical operation for right colon cancer. Chin J Gastrointest Surg. 2016;19(10):1101–1106.
    1. Yang Y, Wang J, Jin L, Li J, Chen G, Wang K, et al. Surgical and pathological outcomes of complete mesocolic excision compared with conventional surgery in right colon cancers. Int J Clin Exp Med. 2017;10(8):11616–11625.
    1. Yozgatli TK, Aytac E, Ozben V, Bayram O, Gurbuz B, Baca B, et al. Robotic complete mesocolic excision versus conventional laparoscopic hemicolectomy for right-sided colon cancer. J Laparoendosc Adv Surg Tech. 2019;29(5):671–676. doi: 10.1089/lap.2018.0348.
    1. Zhao H, Zhou Y, Jin D, Jia Y, L W (2017) Application of laparoscopic comeplete mesocolic excision with a medical-to-lateral approach for right colonic cancer. Journal of Hebei Medical University 38 (11):1279–82
    1. Zurleni T, Cassiano A, Gjoni E, Ballabio A, Serio G, Marzoli L, et al. Correction to: surgical and oncological outcomes after complete mesocolic excision in right-sided colon cancer compared with conventional surgery: a retrospective, single-institution study. Int J Colorectal Dis. 2018;33(1):113–114. doi: 10.1007/s00384-017-2936-z.
    1. J C, J J, P Y, al. et al (2018) A study on laparoscopic complete mesocolic excision for elderly patients with right-sided colon cancer. J Laparosc Surg 23(10): 778–781
    1. Ridgway PF, Darzi AW. The role of total mesorectal excision in the management of rectal cancer. Cancer Control. 2003;10(3):205–211. doi: 10.1177/107327480301000303.
    1. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation—technical notes and outcome. Colorectal Dis. 2009;11(4):354–364. doi: 10.1111/j.1463-1318.2008.01735.x.
    1. Rausa E, Kelly ME, Asti E, Aiolfi A, Bonitta G, Bonavina L. Right hemicolectomy: a network meta-analysis comparing open, laparoscopic-assisted, total laparoscopic, and robotic approach. New York: Springer; 2019. pp. 1020–1032.
    1. Kim NK, Kim YW, Han YD, Cho MS, Hur H, Min BS, et al. Complete mesocolic excision and central vascular ligation for colon cancer: principle, anatomy, surgical technique, and outcomes. Surg Oncol. 2016;25(3):252–262. doi: 10.1016/j.suronc.2016.05.009.
    1. Wu C, Ye K, Wu Y, Chen Q, Xu J, Lin J, et al. Variations in right colic vascular anatomy observed during laparoscopic right colectomy. World J Surg Oncol. 2019;17(1):1–13. doi: 10.1186/s12957-018-1541-0.
    1. Xie D, Yu C, Gao C, Osaiweran H, Hu J, Gong J. An optimal approach for laparoscopic D3 lymphadenectomy plus complete mesocolic excision (D3+CME) for right-sided colon cancer. Ann Surg Oncol. 2017;24(5):1312–1313. doi: 10.1245/s10434-016-5722-1.
    1. Ow ZGW, Sim W, Nistala KRY, Ng CH, Koh FH, Wong NW, et al. Comparing complete mesocolic excision versus conventional colectomy for colon cancer: a systematic review and meta-analysis. Eur J Surg Oncol. 2021;47(4):732–737. doi: 10.1016/j.ejso.2020.09.007.
    1. Baran B, Mert Ozupek N, Yerli Tetik N, Acar E, Bekcioglu O, Baskin Y. Difference between left-sided and right-sided colorectal cancer: a focused review of literature. Gastroenterology Res. 2018;11(4):264–273. doi: 10.14740/gr1062w.
    1. Masoomi H, Buchberg B, Dang P, Carmichael JC, Mills S, Stamos MJ. Outcomes of right vs. left colectomy for colon cancer. J Gastrointest Surg. 2011;15(11):2023–2028. doi: 10.1007/s11605-011-1655-y.
    1. Kataoka K, Beppu N, Shiozawa M, Ikeda M, Tomita N, Kobayashi H, et al. Colorectal cancer treated by resection and extended lymphadenectomy: patterns of spread in left- and right-sided tumours. Br J Surg. 2020 doi: 10.1002/bjs.11517.
    1. Strey CW, Wullstein C, Adamina M, Agha A, Aselmann H, Becker T, et al. Laparoscopic right hemicolectomy with CME: standardization using the “critical view” concept. Surg Endosc. 2018;32(12):5021–5030. doi: 10.1007/s00464-018-6267-0.
    1. Benz S, Tannapfel A, Tam Y, Grünenwald A, Vollmer S, Stricker I. Proposal of a new classification system for complete mesocolic excison in right-sided colon cancer. Tech Coloproctol. 2019;23(3):251–257. doi: 10.1007/s10151-019-01949-4.

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