Acknowledgments
We the authors gratefully acknowledge the insight and advice offered by the following individuals:
Ann Brannigan
Consultant Colorectal Surgeon Mater Misericordiae Hospital University College Dublin Dublin, Ireland
John P. Burke
Consultant Colorectal Surgeon Beaumont Hospital Dublin, Ireland
Manish Chand
Consultant Colorectal Surgeon Department of Surgery and Interventional Sciences University College London London, United Kingdom
Eoghan Condon
Consultant Surgeon Department of Surgery University Hospital Limerick University of Limerick Limerick, Ireland
Peter Dockery Department of Anatomy School of Medicine
National University of Ireland Galway, Ireland
Jonathon Efron Ravitch Division of GI Surgery Department of Surgery
The Mark M Ravitch Professor of Surgery and Urology Johns Hopkins University Baltimore, Maryland
Bill Heald Pelican Cancer Foundation Basingstoke Hospital Basingstoke, United Kingdom
Awad M. Jarrar Department of Cellular and Molecular Medicine Lerner Research Institute Cleveland Clinic Cleveland, Ohio
Mathew Kalady Department of Colorectal Surgery
Digestive Diseases Institute Cleveland Clinic Cleveland, Ohio
Miranda Kiernan Department of Surgery Graduate Entry Medical School University of Limerick Limerick, Ireland
Ravi Kiran Department of Surgery
Columbia University Medical Center Mailman School of Public Health Center for Innovation and Outcomes Research Division of Colorectal Surgery New York Presbyterian Hospital-Columbia New York, New York
Joep Knol Consultant General and Colorectal Surgeon Jessa Hospital Hasselt, Belgium
Ian Lavery Department of Colorectal Surgery
Digestive Diseases Institute Cleveland Clinic Cleveland, Ohio
Jeremy Lipman
Associate Professor of Surgery
Cleveland Clinic Lerner College of Medicine
Case Western Reserve University
Staff Colorectal Surgeon Cleveland Clinic Foundation Cleveland, Ohio
Deirdre McGrath
4i Centre for Interventions in Inflammation, Infection and Immunity
Graduate Entry Medical School
University of Limerick Limerick, Ireland
Manus Moloney
Department of Gastroentrology
University of Limerick Hospitals Group
University Hospital Limerick Limerick, Ireland
Brendan J. Moran
Peritoneal Malignancy Institute
Basingstoke Hospital
Basingstoke, United Kingdom
James W. Ogilvie Jr.
Department of Colorectal Surgery
Spectrum Health/Ferguson Clinic
Michigan State University Grand Rapids, Michigan
D. Peter O’Leary
Department of Surgery
University of Limerick Hospitals Group University Hospital Limerick Limerick, Ireland
James O’Riordan
Department of General and Colorectal Surgery Tallaght Hospital Dublin, Ireland
Nicola O’Riordan
Department of Surgery
University of Limerick Hospitals Group University Hospital Limerick Limerick, Ireland
Colin Peirce
Department of Surgery
University Hospitals Limerick Limerick, Ireland
Feza Remzi
Professor of Surgery
Director, Inflammatory Bowel Disease Center
NYU Langone Medical Center
New York, New York
Jonathon Roddy
Department of Surgery
University of Limerick Hospitals Group
University Hospital Limerick Limerick, Ireland
Shaheel M. Sahebally Department of Surgery
University of Limerick Hospitals Group University Hospital Limerick Limerick, Ireland
Martin Shelly Department of Radiology
University of Limerick Hospitals Group
University Hospital Limerick Limerick, Ireland
Neil J. Smart
Department of Colorectal Surgery
University of Exeter Medical School
Royal Devon & Exeter Hospital Exeter, United Kingdom
Mattias Soop
Department of Colorectal Surgery
University of Manchester
Manchester, United Kingdom
Salford Royal Hospital Salford, United Kingdom
David W. Waldron
Department of Surgery
University of Limerick Hospitals Group University Hospital Limerick Limerick, Ireland
Leon G. Walsh
University of Limerick Hospitals Group University Hospital Limerick Limerick, Ireland
Steven D. Wexner
Digestive Disease Center
Department of Colorectal Surgery
Cleveland Clinic Florida Weston, Florida
Florida Atlantic University College of Medicine
Florida International University College of Medicine Miami, Florida
History
J. CALVIN COFFEY AND NICOLA O’RIORDAN
Two roads diverged in a wood, and I— I took the one less travelled by, And that has made all the difference.
Robert Frost
INTRODUCTION
For centuries, the mesentery and associated peritoneal lining have been regarded as structurally complex. In 1885, Sir Frederick Treves provided the fist comprehensive description of both, emphasizing that while some mesenteric regions persisted in adulthood, others regressed and were lost [1]. For example, the small intestinal mesentery, transverse, and sigmoid mesocolon were consistently identifiable in adults, while the right and leftmesocolon were identifiable in a minority only. Treves’ descriptions were welcome at the time, given the apparent complexity of the topic, and were subsequently indoctrinated in virtually all anatomic, embryologic, clinical, and related literature [1–3]. To the present, the fist chapter of most reference texts on intestinal surgery focuses on anatomy and physiology and is based on Treves’ descriptions. A review of later chapters dealing with techniques in intestinal removal identifiesa remarkable disparity. The right and leftmesocolon are invariably present in the adult and must be resected like any other mesenteric region. Put simply, intestinal surgery has always relied on the persistence of all regions of the mesentery.
Numerous factors contributed to the divergence of anatomic and surgical approaches to the mesentery and peritoneum. Since the time of Treves’ anatomic-based research, surgeons focused increasingly on cellular aspects of disease. With increasing awareness of the molecular basis
of surgical disease, the emphasis of research shi fted away from the anatomic-based craftcomponent. More recently, laparoscopic and robotic surgery have increased focus on the “cra ft” component of surgery. In keeping with this, the fild of surgical anatomy has increased in relative signi ficance and led to the demonstration of continuity of the mesenteric organ from the small intestinal mesentery to the mesorectum [4,5]. The following chapter will demonstrate these shi ft ing trends and clarify the manner in which recent demonstrations allow a reconciliation of anatomic and surgical approaches to this important organ. Th is chapter fi nishes by demonstrating the opportunities that now occur across a broad array of clinical and non-clinical sciences.
CARL TOLDT (1840–1920)
Carl Florian Toldt was born on May 3, 1840, in Bruneck, Austria. A fter spending much of his childhood repairing clocks, he received his doctorate in 1864 at St. Joseph’s University in Vienna and was appointed Professor of Anatomy at the University of Vienna in 1875 (Figure 1.1). He became Professor of Anatomy at the German university in Prague. He subsequently returned to Vienna in 1884 to work with his colleague, Langer, and together they established the Anatomy Institute of Vienna. Carl Toldt’s best-known anatomic work was Anatomischer Atlas für Studierende und Aerzte (An Atlas of Human Anatomy for Students and Physicians) (Figure 1.2), which was translated into English. Despite the superb quality of this work, and its anatomic accuracy, it has been little referenced overall. Toldt died from pneumonia in Vienna in November 1920 [6–9].
Toldt’s descriptions were based on dissection of fresh cadavers that had not been exposed to corrosive preservative
agents. He first observed that intestinal mesenteries did not simply comprise two thin layers of closely apposed cells (i.e., the mesothelia) but rather contained vessels, nerves, and fat. He called the resultant complex of structures the “lamina mesenteria propria” (Figure 1.3). While Treves described disappearance of the right and leftmesocolon as humans matured into adults, Toldt maintained they persisted and attached (i.e., flattened against) to the abdominal wall. Where they attached, Toldt identifid a thin seam of connective tissue (Toldt’s fascia) separating mesentery from abdominal wall, just as two layers of rock might be separated by a seam of rock (see Chapter 2). Toldt suggested that wherever the mesentery attached to the abdominal wall, the cellular layer lining both (i.e., the mesothelium) underwent a “gradual disappearance” to “admit contact and fusion of their connective tissue laminae.” Toldt also suggested that the outer cellular layer of the intestine, the tunica serosa, could undergo a similar process and merge with the covering mesothelium of adjacent mesentery. There is a striking similarity between current descriptions, and those of Toldt, and it is remarkable that his work should have been so infrequently referenced over the past two centuries [6–9].
SIR FREDERICK TREVES
Frederick Treves was born in Dorset, England, in 1853 (Figure 1.4). He received his medical education at the London School of Medicine and became assistant surgeon at the London hospital in 1879. In 1883 he was appointed as surgeon and head of the department of Anatomy. He famously housed Joseph Merrick, “the Elephant Man,” in his attic until Merrick died in 1890 [6,10]. Treves was awarded the Jacksonian prize for dissertations on the pathology, diagnosis, and treatment of obstruction of the intestine and numerous Hunterian lectures on the anatomy of the intestinal canal and the peritoneum. He served in the Boer war in 1899. He was knighted by King Edward VII on whom he performed an appendectomy in 1902. He was a noted travel writer and took up fi nal residence in Geneva (Switzerland) due to poor health. He died of peritonitis in 1923 [6,10,11].
Treves described the human mesentery as fragmented. Accordingly, the right and leftmesocolic components of the mesentery are, according to Treves, mostly absent in the adult human. He described the small intestinal, transverse, and sigmoid mesentery as persisting into adulthood and attaching directly to the abdominal wall (Figure 1.5). At the time, his descriptions provided a welcome rationalization of what was, and still is, regarded as a complex anatomic topic (i.e., mesenteric and peritoneal anatomy in the adult human). Although some aspects of his descriptions of the mesentery and peritoneum are now regarded as inaccurate, he was correct in describing a “mesenteric root” at the origin of the superior mesenteric artery. He was also correct in describing the mesentery of the appendix as arising from the undersurface of the mesentery in the right iliac fossa. Treves’ stunning descriptions were made at a time when signi ficant advances were occurring in anatomic and
Figure 1.1 Carl Toldt (1840–1920).
Figure 1.2 Cover illustration of Anatomischer Atlas Fur Studierende und Aertze
Tunica serosa intestini
Tunica muscularis Stratum longitudinale Stratum circulare
Durchtr itt eines Ar terienzweiges durch die Tunica muscularis
Tela subserosa
Tunica serosa mesenterii
Epithelium
Lamina mesenterii propria Venenzweig Fettgewebe
Einstrahlung des Bindegewebes der Lamina mesenterii propria in die Darmwand
Tunica mucosa
Tela submucosa
9/1
Figure 1.3 The mesentery and adjacent intestine is demonstrated. Toldt drew submesothelial connective tissue as well as a mesenteric connective tissue lattice. He demonstrated a contiguity between these and the connective tissue of the outer layers of the intestine. (Taken from Carl Toldt’s Anatomischer Atlas Fur Studirende und Aertze.)
Figure 1.5 Mesenteric attachments and peritoneal anatomy in the adult human as per Sir Frederick Treves. The mesentery of the small intestine, transverse, and sigmoid colon are depicted by Treves as having linear attachments to the posterior abdominal wall. The attachment of the right and left colon is indicated (arrows). These correspond to the regions where a right or left mesocolon, if present, would be located.
Figure 1.4 Sir Frederick Treves (1853–1923).
Left colic attachment
Right colonic attachment
safe surgery, a factor that is likely to have aided in their indoctrination in mainstream literature. Not surprisingly, they were adopted comprehensively in most anatomic, embryologic, and surgical texts and to the present they form the basis of introductory chapters in reference textbooks. It is remarkable that even today, case reports continue to emerge describing the presence of a right or leftmesocolon (now known to be correct) as anomalous or pathologic [1,5,6].
LIMITED SUPPORT FOR TOLDT’S OBSERVATIONS
Toldt’s findings were supported by the observations of Broesike (1891), Vecchi (1910), Vogt (1926), and Congdon (1942) [12]. Gerota (1895) and Southam (1923) described an “anterior renal fascia” (also referred to as the lateroconal fascia or Gerota’s fascia) as being “fusional in nature,” thereby touching on Toldt’s concept of adhesion [13,14]. In a review of the topic in 1942, Congdon noted that only a single reference anatomic text mentioned Toldt’s fascia, that is, Poirier and Charpy’s text of anatomy [15]. Congdon also noted that at that time, several anatomic texts including that of Waterston, Last, Cunningham, and Grant omitted the fascia from contained illustrations. Toldt’s observations received little if any attention following Congdon’s corroboration of them. It is not known why this occurred. Reference in anatomic texts was, and to this day remains, scant. Although surgical texts can be credited with a little more emphasis, this has also remained limited [16]. The tide may be turning however as the most recent edition of reference anatomic texts such as Gray’s Anatomy acknowledge continuity of the mesentery, as well as the presence of Toldt’s fascia between mesentery and the retroperitoneum [4].
‘The mesocolon extends along the entire length of the colon and is continuous with the small bowel mesentery proximally and the mesorectum distally … Toldt’s fascia lies immediately posterior to the mesocolon, where it is adherent to the retroperitoneum of the posterior abdominal wall’ (Culligan et al. 2014).
In the main, Treves’ arguments supporting discontinuity were adopted in general and specialty literature [5,6]. Mesenteric discontinuity meant that the right and leftmesocolon were, in general, considered absent in the majority of adult humans. If they were present, then they were regarded as abnormal or pathologic. In an attempt to reconcile Treves’ descriptions with theories on the embryologic development of the mesentery, two theories were developed. These were attempts at explaining mesenteric regression or obliteration and were called the sliding and regression theories [17–19].
RADIOLOGY
One of the best ways of appraising living anatomy in its undisturbed format is through radiologic imaging. Radiologists continue to try reconciling the radiologic appearance of the mesentery and associated peritoneum, with Treves’ descriptions. Not surprisingly, many articles on the topic of mesenteric and peritoneal radiology open with a statement asserting the complexity of the fild in general [20,21].
As mentioned earlier, and in keeping with other disciplines, radiologic appraisals of mesenteric anatomy adhere to the descriptions of Treves. Earlier radiologic techniques relied on the injection or consumption of radiopaque contrast to outline the intestinal lumen. These provided limited information on structures outside the intestine, which, for the most part, had to be inferred. The groundbreaking development of computerized axial tomography (CT) and magnetic resonance imaging (MRI) meant that structures outside the intestinal tract could now be visualized. With this development, radiologists attempted to reconcile CT and MRI appearances of the mesentery, with classic anatomic teaching, and di fficulty was again encountered. To address this problem, Oliphant (1982) suggested that the mesentery was continuous with the retroperitoneum (Figure 1.6), leading to the concept of the “subperitoneal space of Oliphant” (Figure 1.6) [22]. In 1986, Dodd indicated that the then current theories of mesenteric anatomy could not be correlated with the shapes observed on CT imaging. He suggested that in order to reconcile both filds (i.e., radiologic and anatomic), the mesentery was best considered as being entirely extra-retroperitoneal
Figure 1.6 Schematic illustration demonstrating Oliphant’s interpretation of the subperitoneal space.
[23]. The theory of Oliphant gained acceptance, while that of Dodd went largely unnoticed until recently (see the “Anatomic continuity: a simpler principle” section).
More recently still, Charnsangavej et al. exploited vascular markings in order to identify mesenteric regions on abdominal CT [20,21,24]. Th is approach is practical and readily adopted, which likely explains its widespread use. However, the sentiment expressed by Dodd (that the CT appearance of the mesentery is di fficult to correlate with prevailing anatomic concepts) still holds.
RENAISSANCE IN FOCUS ON THE MESENTERY
Interest in the mesentery increased with the realization that when the mesentery associated with the rectum (i.e., the mesorectum) was fully excised for rectal cancer, the incidence of recurrent cancer decreased signifiantly. The concept was termed “total mesorectal excision.” Although total mesorectal excision had been conducted worldwide and for decades, the anatomic basis for its success was a recent discovery. In 1982, Heald et al. showed that a plane occurs between the mesorectum and the pelvis and that dissection in this plane, “the holy plane,” enabled a total mesorectal excision (Figure 1.7) [25,26]. Ths was a highly signifiant anatomic description as it provided surgeons with a failsafe anatomic roadmap, which, if adhered to, led to better outcomes for patients with rectal cancer. Initial uptake of the anatomic principle was begrudgingly slow, but it has now gained worldwide acceptance. Surprisingly, Heald and coworkers did not extrapolate the same anatomic basis to the remainder of the colon and mesocolon.
LAPAROSCOPIC AND ROBOTIC SURGERY: THE CRAFT OF COLORECTAL SURGERY
During the 1990s, the development of laparoscopic and minimally invasive surgery (and subsequently robotic techniques) revolutionized intestinal surgery by providing high magnifiation (greater than 20-fold) and high-resolution anatomic imagery. Just as the principles of laparoscopic and robotic intestinal surgery emerged, terminologies such as “mesocolon” and “Toldt’s fascia” were increasingly utilized. For laparoscopic and robotic colorectal surgery to be safe and repeatedly successful, the surgeon must adhere to a universally reproducible anatomic roadmap. Unfortunately, the anatomic basis for laparoscopic and robotic intestinal surgery was also sketchily developed [5,27]. Ths assertion may be considered as unexpected, given surgeons for decades practiced technically superb resections in the open context. It is not surprising, however, when one considers that descriptions of open, laparoscopic and robotic surgical techniques are hallmarked by limited reference to the mesentery, the associated peritoneum and fascia.
A brief illustration of this point is important at this juncture. The mesofascial plane is a key plane throughout colorectal surgery. Access to it is universally gained by division of the overlying peritoneal reflection. Peritonotomy (i.e., division) of the reflection and separation of plane components are core colorectal activities and are universally required for colorectal resection. Despite being centrally important, their anatomic basis has only recently been described.
Focus on the anatomic and surgical importance of the mesentery increased further when Werner Hohenberger described superb results for patients undergoing a “complete mesocolic excision” for colon cancer (Figure 1.8) [28].
Figure 1.7 Professor R.J. (Bill) Heald, OBE, MChir, FRCS(Ed)(Eng).
Figure 1.8 Professor Werner Hohenberger, MD, PhD.
In his 2009 article, he demonstrated that by applying anatomic principles, one could achieve an R0 resection (i.e., clearance of all microscopic disease) in 97% of cases. Around the same time, West et al. demonstrated the effcts of anatomic dissection on colon cancer outcomes. Their fi ndings suggested that by adopting a strictly anatomic approach, one could enhance patients’ survival following surgery for stage three colon cancer [29,30]. These fi ndings went a considerable distance in demonstrating the association between anatomic surgery and better cancer-speci fic outcomes.
Remarkably, however, a unifying anatomic principle that could reconcile anatomic with established surgical approaches to the colon, rectum, and small bowel remained elusive.
ANATOMIC CONTINUITY: A SIMPLER PRINCIPLE
In 2012, a study was performed involving collaboration between the Department of Surgery in University Hospital Limerick, Ireland, and the Department of Colorectal Surgery at the Digestive Diseases Institute at The Cleveland Clinic, in which the anatomic structure of the small and large intestinal mesentery was formally clarifid (Chapter 2) [31]. Crucially, the authors demonstrated that the small intestinal and colonic mesenteries are different regions of the same anatomic structure and that the mesentery itself spans the intestinal tract from the duodenum to the junction between the rectum and anus (Figure 1.9). Ths was a considerable departure from
the classic depictions as it meant that the mesenteric organ is a substantive and continuous structure, and not fragmented or discontinuous as was generally described [32,33]. The newer appraisal was far simpler than the classic description. Recognition of continuity led to similar observations on the peritoneal reflction and Toldt’s fascia. It is now accepted that Toldt’s fascia is continuous from the origin of the mesenteric organ (at the superior mesenteric artery) to its termination at pelvic flor. Similarly, the peritoneum is draped in a contiguous manner over intraperitoneal structures from the root region to the so-called anterior reflction in the pelvis [32,33].
FUTURE DIRECTIONS
Anatomic continuity and contiguity of mesentery, fascia, peritoneal reflection, and gastrointestinal tract has major implications at numerous levels and across multiple specialties (clinical and nonclinical). These form the basis and content of this book. For the surgeon, continuity and contiguity mean that the same anatomic technical elements can be universally used to perform a safe intestinal resection [33]. For the abdominal radiologist, they enable a clearer understanding of the type and extent of intraperitoneal disease [33]. Perhaps most importantly, identification of continuity and clarification of anatomy now permits the systematic (i.e., scientific) study of the mesentery and associated structures [33].
SUMMARY
Transverse colon
Transverse mesocolon
Figure 1.9 (See also QR 1 and 7.) The mesenteric organ. The illustration is of a model of the mesentery generated using a 3D printer. Pan-mesenteric continuity is demonstrated (from the duodenum to the anorectal junction).
There are numerous incidents in the history of medicine where an inaccurate understanding of structure was dogmatically integrated in literature. William Osler wrote that “the greater the ignorance the greater the dogma.” Recent clari fication of mesenteric structure has presented a far simpler structure than heretofore thought. The following chapters will describe the scienti fic opportunities that stem from this clari fication. In addition, it will explain the mesenteric basis of clinical practice.
REFERENCES
1. Treves, F., Lectures on the anatomy of the intestinal canal and peritoneum in man. Br Med J, 1885. 1(1264): 580–583.
2. McConnell, A.A. and T.H. Garratt, Abnormalities of fixation of the ascending colon: The relation of symptoms to anatomical findings. Br J Surg, 1923. 10: 532–557.
3. Netter, F.H., Atlas of Human Anatomy. Elsevier Health Sciences, Philadelphia, PA, 2014, pp. 263–276.
4. Standring, S., Gray’s Anatomy: The Anatomical Basis of Clinical Practice. Elsevier Health Sciences, London, U.K., 2015, Chapter 62, pp. 1098–1111, 1124–1160.
5. Coffey, J.C., Surgical anatomy and anatomic surgery—Clinical and scientific mutualism. Surgeon, 2013. 11(4): 177–182.
Right mesocolon
Right colon
Mesosigmoid
Mesorectum
Sigmoid colon
Rectum
Anorectal junction
Left mesocolon
6. Sehgal, R. and J.C. Coffey, Historical development of mesenteric anatomy provides a universally applicable anatomic paradigm for complete/total mesocolic excision. Gastroenterol Rep, 2014. 2(4): 245–250.
7. Toldt, C., Bau und wachstumsveranterungen der gekrose des menschlischen darmkanales. Denkschrdmathnaturwissensch, 1879. 41: 1–56.
8. Toldt, C., An Atlas of Human Anatomy: For Students and Physicians , Vol. 6: Primary Source Edition. BiblioBazaar, 2013.
9. Toldt, C. and A.D. Rosa, An Atlas of Human Anatomy for Students and Physicians . Macmillan, New York, 1926.
10. Cohen, M.M., Jr., Further diagnostic thoughts about the Elephant Man. Am J Med Genet, 1988. 29(4): 777–782.
11. Treves, F., Discussion on the subsequent course and later history of cases of appendicitis after operation. Med Chir Trans , 1905. 88: 429–610.
12. Congdon, E.D., R. Blumberg, and W. Henry, Fasciae of fusion and elements of the fused enteric mesenteries in the human adult. Am J Anat, 1942. 70: 251–279.
13. Chesbrough, R.M. et al., Gerota versus Zuckerkandl: The renal fascia revisited. Radiology, 1989. 173(3): 845–846.
14. Amin, M., A.T. Blandford, and H.C. Polk, Jr., Renal fascia of Gerota. Urology, 1976. 7(1): 1–3.
15. Poirier, P. and A. Charpy, Traité D’Anatomie Humaine Publié Sous la Direction de P Poirier et a Charpy BiblioBazaar, Charleston, SC, 2010.
16. Goligher, J., Surgery of the Anus Rectum and Colon. All India Traveller Book Seller, 1992.
17. Moore, K.L., T.V.N. Persaud, and M.G. Torchia, The Developing Human: Clinically Oriented Embryology Elsevier Health Sciences, Philadelphia, PA, 2015, pp. 210–239.
18. Sadler, T.W., Langman’s Medical Embryology. Wolters Kluwer Health, Philadelphia, PA, 2011, pp. 208–232.
19. Schoenwolf, G.C. et al., Larsen’s Human Embryology. Elsevier Health Sciences, Philadelphia, PA, 2014, pp. 341–374.
20. Charnsangavej, C. et al., CT of the mesocolon. Part 1. Anatomic considerations. Radiographics , 1993. 13(5): 1035–1045.
21. Charnsangavej, C. et al., CT of the mesocolon. Part 2. Pathologic considerations. Radiographics , 1993. 13(6): 1309–1322.
22. Oliphant, M. and A.S. Berne, Computed tomography of the subperitoneal space: Demonstration of direct spread of intraabdominal disease. J Comput Assist Tomogr, 1982. 6(6): 1127–1137.
23. Dodds, W.J. et al., The retroperitoneal spaces revisited. Am J Roentgenol, 1986. 147(6): 1155–1161.
24. Coffey, J.C. et al., An appraisal of the computed axial tomographic appearance of the human mesentery based on mesenteric contiguity from the duodenojejunal flexure to the mesorectal level. Eur Radiol, 2016. 26(3): 714–721.
25. Heald, R.J., The “Holy Plane” of rectal surgery. J R Soc Med, 1988. 81(9): 503–508.
26. Heald, R.J., E.M. Husband, and R.D. Ryall, The mesorectum in rectal cancer surgery—The clue to pelvic recurrence? Br J Surg , 1982. 69 (10): 613–616.
27. Coffey, J.C. et al., Terminology and nomenclature in colonic surgery: Universal application of a rule-based approach derived from updates on mesenteric anatomy. Tech Coloproctol, 2014. 18 (9): 789–794.
28. Hohenberger, W. et al., Standardized surgery for colonic cancer: Complete mesocolic excision and central ligation—Technical notes and outcome. Colorectal Dis , 2009. 11(4): 354–364; discussion 364–365.
29. West, N.P. et al., Pathology grading of colon cancer surgical resection and its association with survival: A retrospective observational study. Lancet Oncol, 2008. 9(9): 857–865.
30. Coffey, J.C. and P. Dockery, Colorectal cancer: Surgery for colorectal cancer—Standardization required. Nat Rev Gastroenterol Hepatol, 2016. 13(5): 256–257.
31. Culligan, K. et al., The mesocolon: A prospective observational study. Colorectal Dis , 2012. 14 (4): 421–428; discussion 428–430.
32. Coffey, J.C. et al., Mesenteric-based surgery exploits gastrointestinal, peritoneal, mesenteric and fascial continuity from duodenojejunal flexure to the anorectal junction—A review. Dig Surg , 2015. 32(4): 291–300.
33. Coffey, J.C. and D.P. O’Leary, The mesentery: Structure, function, and role in disease. Lancet Gastroenterol Hepatol 1(3): 238–247.
