Complete Mesogastric Excisions Involving Anatomically Based Concepts and Embryological-Based Surgeries: Current Knowledge and Future Challenges

Sergii Girnyi, Marcin Ekman, Luigi Marano, Franco Roviello, Karol Połom, Sergii Girnyi, Marcin Ekman, Luigi Marano, Franco Roviello, Karol Połom

Abstract

Surgeries for gastrointestinal tract malignancies are based on the paradigm that we should remove the tumour together with its lymphatic drainage in one block. This concept was initially proposed in rectal surgery and called a total mesorectal excision. This procedure gained much interest and has improved oncological results in rectal cancer surgery. The same idea for mesogastric and complete mesogastric excisions was proposed but, because of the complexity of the gastric mesentery, it has not become a standard technique. In this review, we analysed anatomical and embryological factors, proposed technical aspects of this operation and incorporated the available initial results of this concept. We also discussed analogies to other gastrointestinal organs, as well as challenges to this concept.

Keywords: anatomical dissection; embryological planes; gastric cancer; mesogastrium.

Conflict of interest statement

The authors declare no potential conflict of interest with respect to the research, authorship, and/or publication of this article.

Figures

Figure 1
Figure 1
Table Model for complete mesogastric excision.

References

    1. Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021;71:209–249. doi: 10.3322/caac.21660.
    1. Martin R.C.G., Jaques D.P., Brennan M.F., Karpeh M. Extended local resection for advanced gastric cancer: Increased survival versus increased morbidity. Ann. Surg. 2002;236:159–165. doi: 10.1097/00000658-200208000-00003.
    1. Japanese Gastric Cancer Association Japanese gastric cancer treatment guidelines 2010 (ver. 3) Gastric Cancer. 2011;14:113–123. doi: 10.1007/s10120-011-0042-4.
    1. Smyth E.C., Verheij M., Allum W., Cunningham D., Cervantes A., Arnold D., ESMO Guidelines Committee Gastric cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2016;27:v38–v49. doi: 10.1093/annonc/mdw350.
    1. NCCN . NCCN Clinical Practice Guidelines in Oncology Gastric Cancer. NCCN; Plymouth Meeting, PA, USA: 2020.
    1. Rohatgi P.R., Yao J.C., Hess K., Schnirer I., Rashid A., Mansfield P.F., Pisters P.W., Ajani J.A. Outcome of gastric cancer patients after successful gastrectomy: Influence of the type of recurrence and histology on survival. Cancer. 2006;107:2576–2580. doi: 10.1002/cncr.22317.
    1. Heald R.J., Ryall R.D.H. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet. 1986;327:1479–1482. doi: 10.1016/S0140-6736(86)91510-2.
    1. Enker W.E., Laffer U.T., Block G.E. Enhanced survival of patients with colon and rectal cancer is based upon wide anatomic resection. Ann. Surg. 1979;190:350–360. doi: 10.1097/00000658-197909000-00010.
    1. Cecil T.D., Sexton R., Moran B.J., Heald R.J. Total mesorectal excision results in low local recurrence rates in lymph node-positive rectal cancer. Dis. Colon Rectum. 2004;47:1145–1150. doi: 10.1007/s10350-004-0086-6.
    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. Color. Dis. 2009;11:354–364. doi: 10.1111/j.1463-1318.2008.01735.x.
    1. Bertelsen C.A., Neuenschwander A.U., Jansen J.E., Wilhelmsen M., Kirkegaard-Klitbo A., Tenma J.R., Bols B., Ingeholm P., Rasmussen L.A., Jepsen L.V., et al. Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: A retrospective, population-based study. Lancet Oncol. 2015;16:161–168. doi: 10.1016/S1470-2045(14)71168-4.
    1. Matsubara T., Ueda M., Nagao N., Takahashi T., Nakajima T., Nishi M. Cervicothoracic approach for total mesoesophageal dissection in cancer of the thoracic esophagus. J. Am. Coll. Surg. 1998;187:238–245. doi: 10.1016/S1072-7515(98)00159-8.
    1. Cuesta M.A. Minimally invasive mesoesophageal resection. J. Thorac. Dis. 2019;11:S728–S734. doi: 10.21037/jtd.2018.12.39.
    1. Adham M., Singhirunnusorn J. Surgical technique and results of total mesopancreas excision (TMpE) in pancreatic tumors. Eur. J. Surg. Oncol. 2012;38:340–345. doi: 10.1016/j.ejso.2011.12.015.
    1. Shyr B.-U., Chen S.-C., Shyr Y.-M., Wang S.-E. Mesopancreas level 3 dissection in robotic pancreaticoduodenectomy. J. Surg. 2021;169:362–368. doi: 10.1016/j.surg.2020.07.042.
    1. Xie D., Osaiweran H., Liu L., Wang X., Yu C., Tong Y., Hu J., Gong J. Mesogastrium: A fifth route of metastasis in gastric cancer? Med. Hypotheses. 2013;80:498–500. doi: 10.1016/j.mehy.2012.12.020.
    1. Xie D., Gao C., Lu A., Liu L., Yu C., Hu J., Gong J. Proximal segmentation of the dorsal mesogastrium reveals new anatomical implications for laparoscopic surgery. Sci. Rep. 2015;5:16287. doi: 10.1038/srep16287.
    1. Xie D., Yu C., Liu L., Osaiweran H., Gao C., Hu J., Gong J. Short-term outcomes of laparoscopic D2 lymphadenectomy with complete mesogastrium excision for advanced gastric cancer. Surg. Endosc. 2016;30:5138–5139. doi: 10.1007/s00464-016-4847-4.
    1. Kumamoto T., Kurahashi Y., Haruta S., Niwa H., Nakanishi Y., Ozawa R., Okumura K., Ishida Y., Shinohara H. Laparoscopic modified lymphadenectomy in gastric cancer surgery using systematic mesogastric excision: A novel technique based on a concept. Langenbeck’s Arch. Surg. 2019;404:369–374. doi: 10.1007/s00423-019-01770-5.
    1. Zheng C.-Y., Dong Z.-Y., Qiu X.-T., Zheng L.-Z., Chen J.-X., Zu B., Lin W. Laparoscopic perigastric mesogastrium excision technique for radical total gastrectomy. Videosurg. Other Miniinvasive Tech. 2019;14:229–236. doi: 10.5114/wiitm.2018.77874.
    1. Kawaguchi Y., Cooper B., Gannon M., Ray M., MacDonald R.J., Wright C.V. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 2002;32:128–134. doi: 10.1038/ng959.
    1. Sadler T.W. Langman Medical Embryology. Lippincott Williams & Wilkins; Philadelphia, PA, USA: 2014.
    1. West N.P., Kobayashi H., Takahashi K., Perrakis A., Weber K., Hohenberger W., Sugihara K., Quirke P. Understanding optimal colonic cancer surgery: Comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J. Clin. Oncol. 2012;30:1763–1769. doi: 10.1200/JCO.2011.38.3992.
    1. Shinohara H., Kurahashi Y., Haruta S., Ishida Y., Sasako M. Universalization of the operative strategy by systematic mesogastric excision for stomach cancer with that for total mesorectal excision and complete mesocolic excision colorectal counterparts. Ann. Gastroenterol. Surg. 2017;2:28–36. doi: 10.1002/ags3.12048.
    1. Sjövall A., Granath F., Cedermark B., Glimelius B., Holm T. Loco-regional recurrence from colon cancer: A population-based study. Ann. Surg. Oncol. 2006;14:432–440. doi: 10.1245/s10434-006-9243-1.
    1. Nakajima T.E., Yamada Y., Hamano T., Furuta K., Gotoda T., Katai H., Kato K., Hamaguchi T., Shimada Y. Adipocytokine levels in gastric cancer patients: Resistin and visfatin as biomarkers of gastric cancer. J. Gastroenterol. 2009;44:685–690. doi: 10.1007/s00535-009-0063-5.
    1. Bi T.-Q., Che X.-M. Nampt/PBEF/visfatin and cancer. Cancer Biol. Ther. 2010;10:119–125. doi: 10.4161/cbt.10.2.12581.
    1. Xie D., Gore C., Zhou J., Pong R.-C., Zhang H., Yu L., Vessella R.L., Min W., Hsieh J.-T. DAB2IP coordinates both PI3K-Akt and ASK1 pathways for cell survival and apoptosis. Proc. Natl. Acad. Sci. USA. 2009;106:19878–19883. doi: 10.1073/pnas.0908458106.
    1. Xie D., Liu L., Osaiweran H., Yu C., Sheng F., Gao C., Hu J., Gong J. Detection and characterization of metastatic cancer cells in the mesogastrium of gastric cancer patients. PLoS ONE. 2015;10:e0142970. doi: 10.1371/journal.pone.0142970.
    1. Shen J., Xie D., Tong Y., Gong J. The length and complexity of mesentery are related to the locoregional recurrence of the carcinoma in gut. Med. Hypotheses. 2017;103:133–135. doi: 10.1016/j.mehy.2017.04.013.
    1. Cao B., Xiao A., Shen J., Xie D., Gong J. An optimal surgical approach for suprapancreatic area dissection in laparoscopic D2 gastrectomy with complete mesogastric excision. J. Gastrointest. Surg. 2020;24:916–917. doi: 10.1007/s11605-019-04467-8.
    1. Schwarz R.E., Smith D. Clinical impact of lymphadenectomy extent in resectable gastric cancer of advanced stage. Ann. Surg. Oncol. 2007;14:317–328. doi: 10.1245/s10434-006-9218-2.
    1. Degiuli M., Sasako M., Ponti A., Calvo F. Survival results of a multicentre phase II study to evaluate D2 gastrectomy for gastric cancer. Br. J. Cancer. 2004;90:1727–1732. doi: 10.1038/sj.bjc.6601761.
    1. Sierra A., Martinez-Regueira F., Pardo F., Cienfuegos J. Role of the extended lymphadenectomy in gastric cancer surgery: Experience in a single institution. Ann. Surg. Oncol. 2003;10:219–226. doi: 10.1245/ASO.2003.07.009.
    1. Enzinger P.C., Benedetti J.K., Meyerhardt J.A., McCoy S., Hundahl S.A., Macdonald J.S., Fuchs C.S. Impact of hospital volume on recurrence and survival after surgery for gastric cancer. Ann. Surg. 2007;245:426–434. doi: 10.1097/01.sla.0000245469.35088.42.
    1. Menges M., Hoehler T. Current strategies in systemic treatment of gastric cancer and cancer of the gastroesophageal junction. J. Cancer Res. Clin. Oncol. 2008;135:29–38. doi: 10.1007/s00432-008-0425-z.
    1. Dickson J.L.B., Cunningham D. Systemic treatment of gastric cancer. Eur. J. Gastroenterol. Hepatol. 2004;16:255–263. doi: 10.1097/00042737-200403000-00003.
    1. Noji T., Miyamoto M., Kubota K.C., Shinohara T., Ambo Y., Matsuno Y., Kashimura N., Hirano S. Evaluation of extra capsular lymph node involvement in patients with extra-hepatic bile duct cancer. World J. Surg. Oncol. 2012;10:106. doi: 10.1186/1477-7819-10-106.
    1. Spolverato G., Ejaz A., Kim Y., Squires M.H., Poultsides G.A., Fields R.C., Schmidt C., Weber S.M., Votanopoulos K., Maithel S.K., et al. Rates and patterns of recurrence after curative intent resection for gastric cancer: A United States multi-institutional analysis. J. Am. Coll. Surg. 2014;219:664–675. doi: 10.1016/j.jamcollsurg.2014.03.062.
    1. Etoh T., Sasako M., Ishikawa K., Katai H., Sano T., Shimoda T. Extranodal metastasis is an indicator of poor prognosis in patients with gastric carcinoma. Br. J. Surg. 2006;93:369–373. doi: 10.1002/bjs.5240.
    1. Maehara Y., Oshiro T., Baba H., Ohno S., Kohnoe S., Sugimachi K. Lymphatic invasion and potential for tumor growth and metastasis in patients with gastric cancer. Surgery. 1995;117:380–385. doi: 10.1016/S0039-6060(05)80056-X.
    1. Sasako M., Sano T., Yamamoto S., Kurokawa Y., Nashimoto A., Kurita A., Hiratsuka M., Tsujinaka T., Kinoshita T., Arai K., et al. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N. Engl. J. Med. 2008;359:453–462. doi: 10.1056/NEJMoa0707035.
    1. Xie D., Wang Y., Shen J., Hu J., Yin P., Gong J. Detection of carcinoembryonic antigen in peritoneal fluid of patients undergoing laparoscopic distal gastrectomy with complete mesogastric excision. Br. J. Surg. 2018;105:1471–1479. doi: 10.1002/bjs.10881.
    1. Schwarz R.E. Recurrence patterns after radical gastrectomy for gastric cancer: Prognostic factors and implications for postoperative adjuvant therapy. Ann. Surg. Oncol. 2002;9:394–400. doi: 10.1007/BF02573875.
    1. Lee H.-J., Kim Y.H., Kim W.H., Lee K.U., Choe K.J., Kim J.-P., Yang H.-K. Clinicopathological analysis for recurrence of early gastric cancer. Jpn. J. Clin. Oncol. 2003;33:209–214. doi: 10.1093/jjco/hyg042.
    1. Ossola P., Mascioli F., Coletta D., Bononi M. Laparoscopic mesogastrium excision for gastric cancer: Only the beginning. J. Laparoendosc. Adv. Surg. Tech. 2020 doi: 10.1089/lap.2020.0743.
    1. Shen J., Dong X., Liu Z., Wang G., Yang J., Zhou F., Lu M., Ma X., Li Y., Tang C., et al. Modularized laparoscopic regional en bloc mesogastrium excision (rEME) based on membrane anatomy for distal gastric cancer. Surg. Endosc. 2018;32:4698–4705. doi: 10.1007/s00464-018-6375-x.
    1. Kumamoto T., Kurahashi Y., Niwa H., Nakanishi Y., Ozawa R., Okumura K., Ishida Y., Shinohara H. Laparoscopic suprapancreatic lymph node dissection using a systematic mesogastric excision concept for gastric cancer. Ann. Surg. Oncol. 2019;27:529–531. doi: 10.1245/s10434-019-07700-5.
    1. Fukuda A., Kawaguchi Y., Furuyama K., Kodama S., Horiguchi M., Kuhara T., Koizumi M., Boyer D.F., Fujimoto K., Doi R., et al. Ectopic pancreas formation in Hes1-knockout mice reveals plasticity of endodermal progenitors of the gut, bile duct, and pancreas. J. Clin. Investig. 2006;116:1484–1493. doi: 10.1172/JCI27704.
    1. Tsujimoto H., Hagiwara A., Shimotsuma M., Sakakura C., Osaki K., Sasaki S., Ohyama T., Ohgaki M., Imanishi T., Yamazaki J., et al. Role of milky spots as selective implantation sites for malignant cells in peritoneal dissemination in mice. J. Cancer Res. Clin. Oncol. 1996;122:590–595. doi: 10.1007/BF01221190.
    1. Kurokawa Y., Doki Y., Mizusawa J., Terashima M., Katai H., Yoshikawa T., Kimura Y., Takiguchi S., Nishida Y., Fukushima N., et al. Bursectomy versus omentectomy alone for resectable gastric cancer (JCOG1001): A phase 3, open-label, randomised controlled trial. Lancet Gastroenterol. Hepatol. 2018;3:460–468. doi: 10.1016/S2468-1253(18)30090-6.
    1. Sakimura Y., Inaki N., Tsuji T., Kadoya S., Bando H. Long-term outcomes of omentum-preserving versus resecting gastrectomy for locally advanced gastric cancer with propensity score analysis. Sci. Rep. 2020;10:1–9. doi: 10.1038/s41598-020-73367-8.
    1. Jongerius E.J., Boerma D., Seldenrijk K.A., Meijer S., Scheepers J.J.G., Smedts F., Lagarde S.M., Ponz O.B., Henegouwen M.I.V.B., van Sandick J.W., et al. Role of omentectomy as part of radical surgery for gastric cancer. Br. J. Surg. 2016;103:1497–1503. doi: 10.1002/bjs.10149.
    1. Ri M., Nunobe S., Honda M., Akimoto E., Kinoshita T., Hori S., Aizawa M., Yabusaki H., Isobe Y., Kawakubo H., et al. Gastrectomy with or without omentectomy for cT3–4 gastric cancer: A multicentre cohort study. Br. J. Surg. 2020;107:1640–1647. doi: 10.1002/bjs.11702.
    1. Marano L., Polom K., Bartoli A., Spaziani A., De Luca R., Lorenzon L., Di Martino N., Marrelli D., Roviello F., Castagnoli G. Oncologic effectiveness and safety of bursectomy in patients with advanced gastric cancer: A systematic review and updated meta-analysis. J. Investig. Surg. 2017;31:529–538. doi: 10.1080/08941939.2017.1355942.
    1. Søndenaa K., Quirke P., Hohenberger W., Sugihara K., Kobayashi H., Kessler H., Brown G., Tudyka V., D’Hoore A., Kennedy R.H., et al. The rationale behind complete mesocolic excision (CME) and a central vascular ligation for colon cancer in open and laparoscopic surgery. Int. J. Color. Dis. 2014;29:419–428. doi: 10.1007/s00384-013-1818-2.
    1. Perrakis A., Weber K., Merkel S., Matzel K., Agaimy A., Gebbert C., Hohenberger W. Lymph node metastasis of carcinomas of transverse colon including flexures. Consideration of the extramesocolic lymph node stations. Int. J. Color. Dis. 2014;29:1223–1229. doi: 10.1007/s00384-014-1971-2.
    1. De Manzoni G., Di Leo A., Roviello F., Marrelli D., Giacopuzzi S., Minicozzi A.M., Verlato G. Tumor site and perigastric nodal status are the most important predictors of para-aortic nodal involvement in advanced gastric cancer. Ann. Surg. Oncol. 2011;18:2273–2280. doi: 10.1245/s10434-010-1547-5.
    1. De Manzoni G., Marrelli D., Baiocchi G.L., Morgagni P., Saragoni L., Degiuli M., Donini A., Fumagalli U., Mazzei M.A., Pacelli F., et al. The Italian research group for gastric cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer. 2017;20:20–30. doi: 10.1007/s10120-016-0615-3.
    1. Polom K., Marrelli D., Pascale V., Ferrara F., Voglino C., Marini M., Roviello F. The pattern of lymph node metastases in microsatellite unstable gastric cancer. Eur. J. Surg. Oncol. 2017;43:2341–2348. doi: 10.1016/j.ejso.2017.09.007.
    1. Roviello F., Pedrazzani C., Marrelli D., Di Leo A., Caruso S., Giacopuzzi S., Corso G., de Manzoni G. Super-extended (D3) lymphadenectomy in advanced gastric cancer. Eur. J. Surg. Oncol. 2010;36:439–446. doi: 10.1016/j.ejso.2010.03.008.
    1. Marrelli D., De Franco L., Iudici L., Polom K., Roviello F. Lymphadenectomy: State of the art. Transl. Gastroenterol. Hepatol. 2017;2:3. doi: 10.21037/tgh.2017.01.01.

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