The Mesentery—Past, Present, and Future

Abstract

This article summarizes the events that shaped our current understanding of the mesentery and the abdomen. The story of how this evolved is intriguing at several levels. It speaks to considerable personal commitment on the part of the pioneers involved. It explains how scientific and clinical fields went different directions with respect to anatomy and clinical practice. It demonstrates that it is no longer acceptable to adhere unquestioningly to models of abdominal anatomy and surgery. The article concludes with a brief description of the Mesenteric Model of abdominal anatomy, and of how this now presents an opportunity to unify scientific and clinical approaches to the latter.

In 1983, Heald first emphasized and detailed the mesenteric basis of good-quality surgery for rectal cancer. ^{1 2 3} Apparently, this was already known at the time of Heald's description of it. It will seem surprising then that although it was known, it did not seem worth documenting to those who knew. In a similar sequence of events, in 2009, Hohenberger emphasized and demonstrated the mesenteric basis of good-quality outcomes during surgery for colon cancer. ^{3 4} Again, some commentators were compelled to publish on the fact this was not new. More recently, we built on the work of Heald and Hohenberger and clarified the shape of the mesentery, the anatomical foundation, and fundamental order of the abdomen. ⁵ During the journey to those discoveries, we again encountered comments that our findings were not new, and in fact were already well known. The story of the mesentery, and its application to colorectal surgery, is thus one of advancements to some and status quo to others.

A review of the history of our understanding of the mesentery and its application to surgery will demonstrate that colorectal surgeons were long practicing mesenteric-based surgery, but without a formal anatomical basis. It is true to say that good-quality colon and rectal cancer surgery had been standard for many, and for decades, but remarkably this practice lacked an explanatory anatomical model. The work of Heald and Hohenberger returned surgery to its anatomical foundations and led to clarification of the anatomical basis of abdominal anatomy and abdominal surgery. ^{1 3 6} Theirs and the work that followed reconciled science and surgery. This review will describe events during that process and thus explain how we arrived at the current state, and the directions surgery and science are now collectively moving in.

Pre-Heald era

The importance of the mesentery was apparent to Aristotle, Galen, and Mundinus, each of whom described a mesenterium (i.e., a single mesentery). ⁷ Similarly, a mesenterium was apparent during the Renaissance to Vesalius, Aselli, and Eustachii. This idea continued into the 18th century with Haller and others, but changes crept in in the 19th century. ⁷ These were driven mainly by the French surgeon Amussat who claimed the left mesocolic region was an artifact of dissection, and hence not an actual anatomical entity. This was upheld by Henry Gray in his text “ Medicine, Descriptive and Surgical ,” which was the forerunner of Gray's Anatomy. ⁸ Gray's descriptions were further supported by Treves in 1885, when he concluded the left and right mesocolon were apparent in a minority of cadavers only. ⁹ The idea of multiple mesenteries emerged and rationalized by defining the mesenteries as a “duplicature of peritoneum.”

The peritoneal model of abdominal anatomy remained the mainstay of anatomical curricula for over a century. It was the foundation accepted in medicine, surgery, pathology, and later pathology. Accordingly, the abdomen is organized by a network of peritoneal derivatives termed mesenteries, omenta, ligaments, and reflections. ^{10 11} According to this model, the term mesentery could only be applied if a duplicature (i.e., a double layer) of peritoneum was apparent. Given this, the mesorectum, mesogastrium, mesopancreas (or mesoduodenum), and right and left mesocolon were misnomers. ¹²

During the early twentieth century a shift occurred in surgical techniques involved in resection of a tumor of an organ of the digestive system. The lymphatic drainage of the organ in which the tumor arose became a technical focus, and surgical procedures evolved to include lymph-containing tissue adjoining organs of the digestive system. During this period, the peritoneal model of abdominal anatomy continued as the focus of the first chapter of many reference texts in surgery. ^{12 13} In effect, the surgical technique went in one direction; anatomy held fast to the peritoneal model of the abdomen.

The Heald era

In 1983 Bill Heald demonstrated the importance of removal of the mesorectal package adjoining the rectum, in surgery for rectal cancer. ^{1 3 4} He provided an anatomical basis for surgical techniques that were practiced by many, but not by most. This advancement by Heald will be mentioned repeatedly in the following articles as it is the seminal event in the history of the following story.

The findings of Heald gradually took hold and ultimately total mesorectal excision (TME) became the gold standard procedure for rectal surgery. Now, one would hope, it is practiced by most. Despite this being the case the idea of the mesorectum remained (until recently) a misnomer to anatomists. ¹² Indeed it often continues to be described as such in the anatomical chapter of reference texts of colorectal surgery. ^{12 13}

Heald's findings preceded the development of minimally invasive colorectal surgery from 1990 to the present. In minimally invasive surgery, the surgeon no longer handles tissue directly and is compelled to adopt a fail-safe anatomical model by which to conduct surgery. Laparoscopic and robotic telescopes afforded a magnified view of the tissue planes during surgery and hence of the anatomical landscape encountered. As a result, techniques were developed that matched anatomical observations. While these were broadly termed the medial and lateral approach to mobilization of the colon, they were in fact medial and lateral mobilization of the mesentery adjoining an already mobile colon.

The Hohenberger era

During this time Werner Hohenberger was accumulating data regarding a technique termed “complete mesoscopic excision,” in which the central anatomical tenets of TME were replicated and the mesentery resected intact. ⁶ Shortly after, pathologists began publishing on how anatomic-based surgery led to good-quality outcomes for patients undergoing surgery for colon and rectal cancer. The technique of complete mesocolic excision (CME) is now widely practiced, due largely to its having a sound anatomical basis and the association with exemplary oncological outcomes.

Following the introduction of TME and CME, anatomists and surgeons had separated fully. Anatomists maintained that the right and left mesocolon (and mesorectum) were anatomical misnomers as they did not have a duplicature of peritoneum. Surgeons repeatedly described that anatomical position in the first chapter of reference texts, but then went on to routinely ignore this in the chapters that followed. Surgical techniques themselves were firmly grounded in mobilization and resection of the mesocolon and mesorectum. This meant surgeons were operating according to an alternative, albeit yet to be articulated, anatomical model.

The Mesentery Is Continuous

In February 2008, we observed that structures previously regarded as misnomers (i.e., the right and left mesocolon) were always present. ¹⁴ We then argued that if they were always present, then that observation, taken in conjunction with the acceptance of small intestinal mesentery, transverse and rectosigmoid mesentery, collectively pointed to mesenteric continuity. We observed that the mesentery is continuous from the duodenojejunal junction to the mesorectum. To surgeons, this was nothing new, which probably explained why the observation struggled to achieve publication until its acceptance in the journal “Colorectal Disease.” ¹⁴

Shortly after the 2012 publication, there was increased recognition of the importance of mesocolic continuity as reflected in increasing numbers of publications on it. ^{15 16 17} On the whole however, research directly focused on the mesentery was conducted by a limited few. ^{16 18} A change then emerged in anatomical reference texts, i.e., to Gray's Anatomy. The mesentery below the duodenum was described as continuous. Although this was a subtle change, its implications were important. We then published the first reference text to focus on the mesentery, “Mesenteric Principles of Gastrointestinal Surgery: Basic and Applied Principles.”

In 2016 we completed an article on the mesentery in which we described it as an organ. ¹⁹ A related press release was published late in December 2016, and the world's media focused on the mesentery. The term mesentery was published by media outlets such as Time, CNN, the Guinness Book of Records, National Geographic, and many others. The mesentery was receiving increasing attention. Some disagreed openly with the idea that the mesentery is an organ. Some disagreed privately but did not argue openly. The counter argument is that the mesentery is a connector but cannot be considered an organ. ²⁰ According to that argument the mesentery occupied a similar hierarchical level as an organ, but was not an organ. The prevailing debate fuelled further research on the mesentery.

Next, publications emerged that suggested that resection of the mesentery during surgery form Crohn's disease may alter the natural history of the condition. ²¹ These were welcome findings, as patients with Crohn's disease were faced with the likelihood of requiring repeated operations. The debate as to whether the mesentery should be resected in surgery for Crohn's disease is discussed in this issue.

Adherence to “Continuity and Evolution Rather than Radical Change and Revolution”

Still, adherence to the conventional definition of the word “mesentery” persisted. The mesorectum, mesocolon, mesoduodenum, mesojejunum, and mesoileum were not listed in Terminologia Anatomica 2 in 2019. The latter is a list of terms formally accepted by the International Federation of Anatomical Societies, FIPAT. ²² It can be argued the omission of these terms was an opportunity lost by the International Federation of Anatomical Societies.

Since 2019

As can be seen from the above, the argument as to the nature of the mesentery and the peritoneum has been longstanding. Fortunately, recent findings may have brought a closure to it and also reconcile anatomical and surgical approaches to the abdomen. We recently found that the mesentery is the organ in and on which all abdominal digestive organs develop and remain directly connected to. ⁵ As the abdomen develops, it remains composed of two distinct anatomical compartments. The mesenteric compartment or domain includes all abdominal digestive organs positioned on the mesentery. The nonmesenteric domain is that on which all genitourinary organs are positioned and remain. This description is termed the Mesenteric Model of Abdominal Anatomy. ^{5 23} It explains the positional anatomy of all contents of the abdomen. In keeping with this, it explains the position of the peritoneum. The peritoneum is the surface lining of the mesenteric domain (i.e., visceral peritoneum), the surface lining of the nonmesenteric domain (i.e., parietal peritoneum), and the junction between both (the reflection).

The Mesenteric Model of Abdominal Anatomy thus reconciles surgical and anatomical approaches to the abdomen. Regions of the mesentery (like other organs of the mesenteric domain) have peritonealized and nonperitonealized surfaces. The mesentery does not have to be a duplicature of peritoneum to be considered mesentery. The mesogastrium, mesoduodenum, right and left mesocolon, medial mesosigmoid, and mesorectum are part of the mesenteric continuum. The peritoneal canopy covers some surfaces of that continuum, but not all.

Conclusion

Heald and Hohenberger insisted on formalizing the anatomical foundation of surgery for colorectal cancer. Their work prompted reappraisal of abdominal anatomy. That led to clarification of the anatomical foundation of the abdomen, and the order (the fundamental order) at the foundation level. While theirs and the work that followed focused on the mesentery, the findings reconciled surgical and anatomical approaches to the abdomen in general. It is thus fitting and timely to generate a collection of state-of-the-art reviews that summarize the surgical importance of the mesentery.