Mesenteric organ

The human mesentery or mesentery organ is defined as the small intestinal mesentery, the mesocolon, mesosigmoid and mesorectum.^[1] Conventional teaching has dogmatically described the mesocolon as a fragmented structure, i.e. the small intestinal mesentery, transverse and sigmoid mesocolon all ‘terminate’ at their ‘insertion’ into the posterior abdominal wall.^[1] Recent advances in gastrointestinal anatomy have demonstrated that the mesenteric organ is in fact a single continuous structure from the duodenojejunal flexure to the level of the distal mesorectum. This far simpler concept has been shown to have significant implications.^[1,2]

History

The classical anatomical description of the mesocolon is credited to British surgeon Sir Frederick Treves in 1885.^[3] Treves is famously known for performing the first appendectomy in England in 1888 and was surgeon to both Queen Victoria and King Edward VII.^[4] He studied the human mesentery and peritoneal folds in 100 cadavers and described the right and left mesocolon as vestigial or absent in the human adult. Accordingly, the small intestinal mesentery, transverse and sigmoid mesocolon all terminated or attached at their insertions into the posterior abdominal wall.^[3-4] These assertions were indoctrinated into mainstream surgical, anatomical, embryological, and radiologic literature for more than a century and up to the recent present.^[5-6]

Interestingly, almost 10 years prior to Treves, the Austrian anatomist Carl Toldt described the persistence of all portions of the mesocolon into adulthood.^[7] Toldt was professor of anatomy in Prague and Vienna and published his account of the human mesentery in 1879. Furthermore, Toldt identified a fascial plane between the mesocolon and the underlying retroperitoneum formed by the fusion of the visceral peritoneum of the mesocolon with the parietal peritoneum of the retroperitoneum (this later became known as Toldt's fascia).^[7,8]

In 1942, the anatomist also Edward Congdon demonstrated that the right and left mesocolon persisted into adulthood and remained separate from the retroperitoneum (i.e. extra-retroperitoneal).^[9] The radiologist Wylie J. Dodds also described this concept in 1986.^[10] Dodds astutely extrapolated that unless the mesocolon remained an extra-retroperitoneal structure (i.e. separate from the retroperitoneum), only then would the radiologic appearance of the mesentery and peritoneal folds be reconciled with actual anatomy.^[10]

Descriptions of the mesocolon by Carl Toldt, Edward Congdon and W.J. Dodds have largely been ignored in mainstream literature until recently. A formal appraisal of the mesenteric organ anatomy was conducted in 2012 and echoed findings of Toldt, Congdon and Dodds.^[11] The single greatest advance in this regard was the identification of the mesenteric organ as being contiguous as it spans the gastrointestinal tract from duodenojejunal flexure to mesorectal level.^[11]

Embryology

The embryologic forerunner of the gastrointestinal tract (GIT) is suspended from the posterior abdominal wall by the dorsal mesentery. The GIT and associated dorsal mesentery, is subdivided into foregut, midgut and hindgut regions based on the respective blood supply; the foregut is supplied by the celiac trunk, the midgut is supplied by the superior mesenteric artery (SMA) and the hindgut is supplied by the inferior mesenteric artery (IMA). This division is established by the 4th week of intrauterine life. Following this the midgut undergoes a period of rapid elongation, which forces it to herniate through the umbilicus. During herniation, the midgut loop undergoes a 90^o anti-clockwise rotation around the axis of the SMA, with the cranial portion of the loop moving to the right and the caudal portion of the loop moving toward the left. This rotation occurs at approximately the 8th week of development. The cranial portion of the loop will develop into the jejunum, most of the ileum while the caudal part of the loop eventually forms the terminal portion of the ileum, the ascending colon and the initial 2/3 of the transverse colon. As the foetus develops in size, the mid-gut loop is drawn back through the umbilicus and undergoes a further 180^o rotation, completing a total of 270^o rotation. At this point, approximately 10 weeks, the caecum lies in close approximation to the liver. From here it moves in a cranial to caudal direction to eventually lie in the lower right portion of the abdominal cavity. This process brings the ascending colon to lie vertically in the lateral right portion of the abdominal cavity apposed to the posterior abdominal wall. The descending colon occupies a similar position on the left hand side.^[12,13]

During all these topographic changes, the dorsal mesentery undergoes corresponding changes. Most anatomical and embryological textbooks suggest that, after adoption of a final position, the ascending and descending mesocolon disappear during embryogenesis. “Embryology - An Illustrated Colour Text” states that “most of the mid-gut retains the original dorsal mesentery, though parts of the duodenum derived from the mid-gut do not. The mesentery associated with the ascending colon and descending colon is resorbed, bringing these parts of the colon into close contact with the body wall.”^[13] In “The Developing Human” the author states that “the mesentery of the ascending colon fuses with the parietal peritoneum on this wall and disappears; consequently the ascending colon also becomes retroperitoneal”.^[14] To reconcile these suggestions several theories of embryologic mesenteric development (including the “regression” and “sliding” theories) have been proposed however none widely accepted.^[13,14]

Anatomy

Contemporary characterizations of meseteric anatomy revealed several novel anatomical findings not previously documented. In 2012, the first prospective observational study of the mesocolon was undertaken.^[11] A total of 109 patients undergoing open, elective total abdominal colectomy were studied. Anatomical observations were recorded during the surgery and on the postoperative specimens. These observations included: (i) the mesocolon is continuous from ileocaecal to rectosigmoid level; (ii) a mesenteric confluence occurs at the ileocaecal and rectosigmoid junction as well as at the hepatic and splenic flexures; (iii) each flexure (and ileocaecal junction) is a complex of peritoneal and omental attachments to the colon centred on a mesenteric confluence (discussed below); (iv) the proximal rectum originates at the confluence of the mesorectum and mesosigmoid; and (v) a plane occupied by Toldt’s fascia separates the entire apposed small intestinal mesentery and mesocolon from the retroperitoneum. Deep in the pelvis, this fascia coalesces to give rise to Waldeyer’s fascia.^[11]

Flexural Anatomy

Frequently described as a difficult area, flexural anatomy is also simplified when each flexure is considering as being centered on a mesenteric contiguity. The ileocaecal flexure arises at the point where the ileum is continuous with the caecum around the ileocaecal mesenteric flexure. Similarly, the hepatic flexure is formed between the right mesocolon and transverse mesocolon, at the mesenteric confluence. The colonic component of the hepatic flexure is draped around this mesenteric confluence. Furthermore, the splenic flexure is formed by the mesenteric confluence between the transverse and left mesocolon. The colonic component of the splenic flexure occurs lateral to the mesenteric confluence. At every flexure, a continuous peritoneal fold lies outside the colonic/mesocolic complex tethering this to the posterior abdominal wall.^[1,11]

Peritoneal fold anatomy

Understanding the macroscopic structure of the mesenteric organ meant that associated structures (i.e. peritoneal folds and congenital as well as omental adhesions) could be better appraised. The small intestinal mesenteric fold occurs where the small intestinal mesentery folds onto the posterior abdominal wall and continues laterally as the right mesocolon. During mobilization of the small intestinal mesentery from the posterior abdominal wall, this fold is incised, thus allowing access to the interface between the small intestinal mesentery and the retroperitoneum. The fold continues at the inferolateral boundary of the ileocaecal junction and turns cephalad as the right paracolic peritoneal fold. During lateral to medial mobilization this fold is divided permitting the surgeon to serially lift the right colon and associated mesentery off the underlying fascia and retroperitoneum. At the hepatic flexure the right lateral peritoneal fold turns and continues medially as the hepatocolic peritoneal fold. Division of the fold in this location permits separation of the colonic component of the hepatic flexure and mesocolon off the retroperitoneum.^[1,11]

Interposed between the hepatic and splenic flexures the greater omentum adheres to the transverse colon along a further band or fold of peritoneum. Dissection through this allows access to the cephalad (top) surface of the transverse mesocolon. Focal adhesions frequently tether the greater omentum to the cephalad aspect of the transverse mesocolon. The left colon is associated with a similar anatomic configuration of peritoneal folds in that the splenic peritoneal fold is contiguous with the left lateral paracolic peritoneal fold at the splenic flexure. Division of the latter similarly allows for the separation of the left colon and associated mesentery off the underlying fascia and hence frees it from the retroperitoneum. The left lateral paracolic peritoneal fold continues distally at the lateral aspect of the mobile component of the mesosigmoid.^[1,11]

Histology

Determination of the macroscopic structure of the mesenteric organ permitted a recent characterisation of the histological and electron microscopic properties.^[15] The microscopic structure of the mesocolon and associated fascia is consistent from ileocecal to mesorectal levels. A surface mesothelium and underlying connective tissue is universally apparent. Adipocytes lobules within the body of the mesocolon are separated by fibrous septae arising from submesothelial connective tissue. Where apposed to the retroperitoneum, two mesothelial layers separate the mesocolon and underlying retroperitoneum. Between these, a discrete layer of connective tissue, i.e. Toldt’s fascia, occurs. Lymphatic channels are evident in mesocolic connective tissue and in Toldt’s fascia.^[15]

Lymphangiology

An improved understanding of mesenteric structure and histology has enabled a formal characterisation of mesenteric lymphangiology.^[16] Stereologic assessments of the lymphatic vessels demonstrate a rich lymphatic network embedded within the mesenteric connective tissue lattice. On average, vessels occur every 0.14mm, and within 0.1mm from the mesocolic surfaces (anterior and posterior). Lymphatic channels have also been identified in Toldt’s fascia, though the significance of this is unknown.^[16]

Patho-physiology

Clarifications of the mesenteric anatomy have a clearer understanding of diseases involving the mesentery (examples of which include malrotation and Crohn’s disease (CD)). In CD, the mesentery is frequently thickened rendering haemostasis challenging. In addition, fat wrapping (i.e. creeping fat) involves extension of mesenteric fat over the circumference of contiguous gastrointestinal tract and has been suggested to reflect increased mesothelial plasticity. The relationship between mesenteric derangements and mucosal manifestations in CD points to a pathobiologic overlap with some suggesting that CD is primarily a mesenteric disorder that secondarily affects the GIT and systemic circulation.^[17]

Furthermore, the rationalization of mesenteric and peritoneal fold anatomy permits the surgeon to differentiate both from intraperitoneal adhesions (aka ‘congenital adhesions’). These are highly variable amongst patients and occur in several locations. Congenital adhesions occur between the lateral aspect of the peritoneum overlying the mobile component of the mesosigmoid, and the parietal peritoneum in the left iliac fossa. During lateral to medial approach of mobilizing of the mesosigmoid, these must be divided first before the peritoneum proper can be accessed. Similarly, focal adhesions occur between the undersurface of the greater omentum and the cephalad aspect of the transverse mesocolon. These can be accessed after dividing the peritoneal fold that links the greater omentum and transverse colon. Adhesions here must be divided in order to separate the greater omentum off the transverse mesocolon thus allowing access to the lesser sac proper.^[1,2]

Treatment

Surgery

While the total mesocolic excision (TME) operation has become the surgical gold standard for the management of rectal cancer, this is not so for colon cancer.^{[1,2,11,18-20]} Recently, the surgical principles underpinning TME in rectal cancer have been extrapolated to colonic surgery.^[21-27] Total or Complete mesocolic excision (CME), utilize planar surgery and extensive mesenterectomy (i.e. high tie) to minimise breach of the mesentery and maximise lymph nodes yield. Application of this T/CME reduces local 5-year recurrence rates in colon cancer from 6.5% to 3.6%, while cancer related 5-year survival rates, in patients resected for cure, increased from 82.1% to 89.1%.^[27]

Radiology

Recent radiologic appraisals of the mesenteric organ have been conducted in the light of the contemporary understanding of mesenteric organ anatomy. When this organ is divided into non-flexural and flexural regions, these can readily be differentiated in the majority of patients, on CT imaging. Clarification of the radiological appearance of the human mesentery resonates with the suggestions of Dodd, and enables a clearer conceptualisation of mesenteric derangements in disease states.^[10] This is of immediate relevance in the cancer of spread from colon cancer, perforated diverticular disease and in pancreatitis, where fluid collections in the lesser sac dissect the mesocolon from the retroperitoneum, and thereby extend distally within the latter.^[28]

References

1. Coffey JC (2013) Surgical anatomy and anatomic surgery: clinical and scientific mutualism. Surgeon 11:177–182

2. Coffey JC, Sehgal R, Culligan K, Dunne C, McGrath D, Lawes N, Walsh D. (2014) Terminology and nomenclature in colonic surgery – universal application of a rule-based approach derived from updates on mesenteric anatomy. Tech Coloproctol. IN PRESS

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4. Mirilas P, Skandalakis JE. Not just an appendix: Sir Frederick Treves. Arch Dis Child. 2003 Jun;88(6):549-52.

5. Ellis H. The abdomen and pelvis. In: Ellis H, editor. Clinical anatomy: applied anatomy for students and junior doctors. 12th ed. Blackwell Science; 2010. p. 86.

6. McMinn RH. The gastrointestinal tract. In: McMinn RH, editor. Last’s anatomy: regional and applied. 9th ed. London: Langman Group Ltd; 1994. p. 331e42.

7. Toldt C. Bau und wachstumsveranterungen der gekrose des menschlischen darmkanales. Denkschrdmathnaturwissensch 1879;41:1-56.

8. Toldt C. Splanchology – general considerations. In : Toldt C & Della Rossa A (Eds.), An atlas of human anatomy for students and physicians. New York: Rebman Company 1919. vol. 4. 408.

9. Congdon ED, Blumberg R, Henry W. Fasciae of fusion and elements of the fused enteric mesenteries in the human adult. Am J Anat 1942:251-279.

10. Dodds WJ, Darweesh RM, Lawson TL, et al. The retroperitoneal spaces revisited. AJR Am J Roentgenol 1986;147:1155-1161.

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

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14. Moore KL, TPersaud TVN, Torchia MG. The Developing Human: Clinically Oriented Embryology with Student Consult Online Assess, 9th Edition. Saunders; ISBN 978-1437720020<

15. Culligan K, Walsh S, Dunne C, Walsh M, Ryan S, Quondamatteo F, Dockery P, Coffey JC (2014) The mesocolon: a histological and electron microscopic characterization of the mesenteric attachment of the colon prior to and after surgical mobilization. Ann Surg [Epub ahead of print]

16. Culligan K, Sehgal R, Mulligan D, Dunne C, Walsh S, Quondamatteo F, Dockery P, Coffey JC. A detailed appraisal of mesocolic lymphangiology – an immunohistochemical and stereological analysis. Journal of Anatomy. [IN PRESS]

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19. Sehgal R, Coffey JC. Comprehensive standardization of complete mesenteric surgery is now possible. Tech Coloproctol. 2014 Mar 6.

20. Sehgal R, Coffey JC. Standardization of the nomenclature based on contemporary mesentericanatomy is paramount prior to performing a complete mesentericexcision. Int J Colorectal Dis. 2014 Apr;29(4):543-4.

21. 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 2008;9:857–65.

22. Jagoditsch M, Lisborg PH, Jatzko GR, et al. (2000) Long-term prognosis for colon cancer related to consistent radical surgery: Multivariate analysis of clinical, surgical, and pathologic variables. World J Surg 24:1264–1270.

23. Bokey EL, Chapuis PH, Dent OF, et al. (2003) Surgical technique and survival in patients having a curative resection for colon cancer. Dis Colon Rectum 46:860–866.

24. Søndenaa K, Quirke P, Hohenberger W, Sugihara K, Kobayashi H, Kessler H, Brown G, Tudyka V, D'Hoore A, Kennedy RH, West NP, Kim SH, Heald R, Storli KE, Nesbakken A, Moran B. 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. 2014 Apr;29(4):419-28.

25. Storli KE, Søndenaa K, Furnes B, Nesvik I, Gudlaugsson E, Bukholm I, Eide GE. 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. 2013 Dec 20.

26. Galizia G, Lieto E, De Vita F, Ferraraccio F, Zamboli A, Mabilia A, Auricchio A, Castellano P, Napolitano V, Orditura M. 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 Jan;29(1):89-97.

27. Hohenberger W, Weber K, Matzel K et al. Standardized surgery for colonic cancer: complete mesenteric excision and central ligation–technical notes and outcome. Colorectal Dis 2009;11:354–65.

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