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4 J. C. Coffey and P. O’Leary
Fig. 1.1 Classic model depicting multiple mesenteries and a complex peritoneal landscape
continuous mesentery but they did not textually describe it as such. In general,
textual descriptions of the mesentery were remarkably limited. In 1858 Henry Gray
described the “root” of the small intestinal mesentery as attaching along a particular
trajectory across the posterior abdominal wall. He described multiple mesenteries,
as opposed to one continuous mesentery (Fig. 1.1). This concept was supported by
observations of numerous surgeons including Sir Frederick Treves.
The Gray model was indoctrinated in reference texts for a number of reasons,
until recently when it was noted that the mesentery is in fact continuous and that all
abdominal digestive organs are continuous with it. The last point is particularly
important as it means that our understanding of how all digestive organs are connected to the rest of the body, must change.
It is now recognized that the mesentery is centrally positioned within the
abdominal digestive system, linking all digestive organs, and connecting these
collectively to the posterior abdominal wall (Fig. 1.2). Moreover, the mesentery,
and digestive organs, determine and explain the peritoneal landscape. As the latter
determines the shape of the peritoneal cavity, it follows the anatomy of the peritoneal cavity is primarily determined and explained by the mesentery and associated digestive system organs (Fig. 1.3).
1 Redefining the Mesentery as an Organ 5
Fig. 1.2 Current model depicting a single continuous mesentery. Mesenteric continuity has major
implications for our understanding of the anatomical organization of the abdomen
Fig. 1.3 3D digital sculpture
demonstrating the peritoneal
reflection and the position of
the peritoneum in the
mesenteric-based model of
abdominal anatomy
The Science of the Mesentery
The proposal that the mesentery is an organ was surprising in that many held that all
human anatomy was well established. The proposal generated considerable media
attention and argument. Whether the mesentery is an organ or not is a point for
discussion, and as with any discussion there are for and against sides.
6 J. C. Coffey and P. O’Leary
Arguing against the concept that it is an organ, one commentator argued that
whilst the mesentery is not an organ, it does occupy the same “hierarchical level” as
an organ. The argument was based on multiple points but chief amongst these was
the concept the mesentery does not serve an essential and unique function. Others
commentated that more information was required in order to make a definitive
decision on the matter.More recently, anatomists have moved towards arguing that
anatomical terminology such as “organ” requires updating, and that classification
systems need updating.
Apart from these points, there appears to be little else in formal literature arguing
against the concept of the mesenteric organ. Indeed, many scientists are using the
definition as an opportunity to further characterize and explore the mesentery. It is
not possible to reference all articles of relevance as these are continuing to emerge
in numerous languages and across multiple scientific and clinical disciplines. In
many respects this book, reflects that movement.
If we are to consider the mesentery as an organ, then we must challenge it in the
same way we would any organ. In keeping with this, the current text summarizes
diseases of the mesentery and is the first reference text that explains how these may
be diagnosed and treated. Yi Li et al. recently published a comprehensive review of
lymphatics of the mesenteric organ. Britta Siegmund’s group described the
importance of the mesenteric organ in the context of intestinal and systemic
immunity. Rivera et al. elegantly summarized the role of mesenteric events in
multiple diseases, in multi-organ dysfunction syndrome and the systemic inflammatory response. Argikar et al. characterized the pharamacobiology of the
mesenteric organ demonstrating several opportunities for further scientific exploration. Several authors have characterized mesenteric-organ inputs into hepatic,
pancreatic, splenic and intestinal development. These are the subject of a focused
issue of Seminars in Cell and Developmental Biology. The title of the issue, currently in press, is “Mesenteric Organogenesis.” Indeed, several authors have even
linked the mesentery to correlates in numerous traditional medicines.
Conclusion
The mesenteric organ is being given increased attention in the forthcoming reference text Gray’s Surgical Anatomy, in the upcoming edition of Gray’s Anatomy
and in reference textbooks on human embryology (including the most recent edition
of Langmans Embryology). These are important developments that signify
increasing acceptance of the importance of the mesentery in scientific and clinical
practice.
It is imperative that we now exploit developments in order to enhance our ability
to diagnose and treat human disease. In that regard, there is no more fitting place to
start, than with diseases of the mesentery itself.
1 Redefining the Mesentery as an Organ 7
Suggested Reading
1. Coffey JC, Sehgal R, Culligan K, Dunne C, McGrath D, Lawes N, Walsh D. Terminology and
nomenclature in colonic surgery: universal application of a rule-based approach derived from
updates on mesenteric anatomy. Tech Coloproctol. 2014;18:789– 94.
2. Sehgal R, Coffey JC. Standardization of the nomenclature based on contemporary mesocolic
anatomy is paramount prior to performing a complete mesocolic excision. Int J Colorectal
Dis. 2014;29:543–4.
3. Coffey JC, O’Leary DP. The mesentery: structure, function, and role in disease. Lancet
Gastroenterol Hepatol. 2016;1(3):238–47.
4. Culligan K, Walsh S, Dunne C, Walsh M, Ryan S, Quondamatteo F, Dockery P, Coffey JC.
The mesocolon: a histological and electron microscopic characterization of the mesenteric
attachment of the colon prior to and after surgical mobilization. Ann Surg. 2014;260
(6):1048–56.
5. Hikspoors JPJM, Kruepunga N, Mommen GMC, Peeters JPWU, Hülsman CJM, Eleonore
Köhler S, Lamers WH. The development of the dorsal mesentery in human embryos and
fetuses. Semin Cell Dev Biol. 2018.
6. Byrnes KG, Walsh D, Lewton-Brain P, McDermott K, Coffey JC. Anatomy of the mesentery:
historical development and recent advances. Semin Cell Dev Biol. 2018. pii: S1084–9521(18)
30204–0.
7. Kumar A, Kishan V, Jacob TG, Kant K, Faiq MA. Evidence of continuity of mesentery from
duodenum to rectum from human cadaveric dissection—a video vignette. Colorectal Dis.
2017;19(12):1119–20.
8. Coffey JC, Dillon M, Sehgal R, Dockery P, Quondamatteo F, Walsh D, Walsh L.
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.
9. Coffey JC, Culligan K, Walsh LG, Sehgal R, Dunne C, McGrath D, Walsh D, Moore M,
taunton M, Scanlon T, Dewhurst C, Kenny B, O'Riordan C, O'Brien JM, Quondamatteo F,
Dockery P. 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):714–21.
10. Coffey JC, O’leary DP. Defining the mesentery as an organ and what this means for
understanding its roles in digestive disorders. Expert Rev Gastroenterol Hepatol. 2017;11
(8):703–5.
11. Byrnes KG, McDermott K, Coffey JC. Development of mesenteric tissues. Semin Cell Dev
Biol. 2018. pii: S1084–9521(18)30234–9.
12. Gray, H. Anatomy, descriptive and surgical. New York;1858.
13. Treves F. Lectures on the anatomy of the intestinal canal and peritoneum in man. Br
Med J. 1885;1:470–4.
14. Culligan K, Coffey JC, Kiran RP, Kalady M, Lavery IC, Remzi FH. The mesocolon: a
prospective observational study. Colorectal Dis. 2012;14(4):421–8; discussion 428–30.
15. Neumann PE. Another new organ! is this a golden age of discovery in anatomy? Clin Anat.
2018;31(5):648–9. https://doi.org/10.1002/ca.23184 Epub 2018 May 25.
16. Kumar A, Ghosh SK, Faiq MA, Deshmukh VR, Kumari C, Pareek V.: A brief review of recent discoveries in human anatomy. QJM. 2018.
17. Neumann PE. Organ or not? Prolegomenon to organology. Clin Anat. 2017;30(3):288–9.
18. Argikar AA, Argikar UA. The mesentery: an ADME perspective on a ‘new’ organ. Drug
Metab Rev. 2018;50(3):398–405.
19. Li Y, Ge Y, Gong J, Zhu W, Cao L, Guo Z, Gu L, Li J. Mesenteric lymphatic vessel density is
associated with disease behavior and postoperative recurrence in Crohn’s disease.
J Gastrointest Surg. 2018;22(12):2125–32.
8 J. C. Coffey and P. O’Leary
20. Siegmund B. Mesenteric fat in Crohn’s disease: the hot spot of inflammation? Gut. 2012;61
(1):3–5.
21. Rivera ED, Coffey JC, Walsh D, Ehrenpreis ED. The mesentery, systemic inflammation, and
Crohn’s disease. Inflamm Bowel Dis. 2019;25(2):226–34.
22. Byrnes KG, McDermott KW, Coffey JC. Mesenteric organogenesis. Semin Cell Dev Biol.
2018.
23. Gong CZ, Liu W. Convergence of medicines: west meets east in newly-discovered organs and
functions. Chin J Integr Med. 2018.
Embryology of the Mesentery
Kevin G. Byrnes and J. Calvin Coffey
Introduction
Past appraisals of embryonic development of the mesentery aimed to reconcile
observations with the concept of multiple mesenteries. As it is now accepted that
there is one, single and continuous mesentery, this prompts a re-appraisal of
mesenteric embryology. That process is currently underway, and as such, it is
somewhat premature to provide a detailed descri ption of mesenteric embryology.
It is, however, possible to mention some points that hold, irrespective of recent
advancements in our understanding of anatomy. Previously, the mesentery was
regarded as an inert scaffold that structurally supported digestive organ development, but with little direct contributions to the latter. Clarification of mesenteric
structure permitted systematical investigation of the mesentery and with this came
the realization that the mesentery is far more active in digestive organ and related
organogenesis, than previously though t. This led to the development of the field of
mesenteric organogenesis, the study of organ development related to the mesentery.
2
Embryological Development of the Mesentery and Related Organs
The Ventral and Dorsal Mesentery
The mesentery develops early during development, as a membrane that spans the
developing coelom which is the forerunner of the peritoneal cavity (Fig. 2.1). The
following discussion will focus on the upper region of the abdominal mesentery,
K. G. Byrnes J. C. Coffey (&)
School of Medicine and Department of Surgery, University of Limerick Hospital Group, Raheen,
Dooradoyle, Limerick, Ireland
e-mail: calvin.coffey@ul.ie
© Springer Nature Switzerland AG 2021
E. D. Ehrenpreis et al. (eds.), The Mesenteric Organ in Health and Disease,
https://doi.org/10.1007/978-3-030-71963-0_2
9
10 K. G. Byrnes and J. C. Coffey
Fig. 2.1 Mesenteric continuity extending throughout abdominal digestive system
which extends from anterior to the posterior wall of the coelom, It is arbitrarily
divided into two regions, based on the presence of endoderm (from which the
intestine will derive). The region of the mesentery anterior to the developing intestine
is the ventral mesentery, and posterior is the dorsal mesentery. The ventral mesentery
has a lower limit extending from the developing diaphragm to the umbilicus. The
dorsal mesentery extends beyond this to the region of the anorectal junction.
Development of the Upper Region of Mesentery and Associated Organs
All abdominal digestive organs develop in and remain continuous with, the
mesentery (Fig. 2.2 ). In the upper region, the liver develops in the ventral
mesentery and quickly outgrows the boundaries of this. At full term and in the
adult, the ventral mesentery in which the liver developed is retained as a mesenteric
brace, the front region of which corresponds to the falciform ligament a nd the back
region corresponds to the ventral mesentery. Both falciform ligament and ventral
mesentery converge and meet at the oesophagogastric mesenteric pedicle (see
chapter on Anatomy).
A region of the upper mesentery invaginates to give rise to a mesenteric bubble
or diverticulum that is oriented to the left. The spleen develops in the left-most
corner of this bubble of mesentery. The stomach will develop as a region of
developing endoderm, in the anterior leaf of the bubble. The mesentery between the
stomach and spleen will extend inferiorly into the coelom, and give rise to the
greater omentum.
2 Embryology of the Mesentery 11
Fig. 2.2 Abdominal digestive organs centered on a mesenteric frame. a Anterior view of
mesentery with contiguous abdominal digestive organs in situ b Posterior view of mesentery with
contiguous abdominal digestive organs in situ c Anterior view of mesenteric frame extending from
mesogastrium to mesorectum d Posterior view of mesenteric frame extending from mesogastrium
to mesorectum
12 K. G. Byrnes and J. C. Coffey
Development of the Lower Region of Mesentery and Associated Organs
At present the precise morphological changes the mesentery undergoes during
development, are unknown. Data is emerging, following the application of a
number of techniques, pointing to several processes, but these remain to be validated. For example, our group has examined individual stages of embryological
development, reconstructed the shape of the mesentery at each stage (in the context
of mesenteric continuity), then merged each stage in animation to depict the processes involved. A second approach involved reverse engineering the development
of the mesentery, working from the adult shape, in reverse, back to the stage at
which the mesentery was a sheet like structure spanning the coelom. The shape
changes identified using both these techniques are complex, due to the presence of
the ventral mesentery in the upper region, and evolvi ng relationships with digestive
organs as these develop in tandem. Although these findings are preliminary several
statements can be made about mesenteric development.
Firstly, most development of the mid and lower intestine-mesenteric complex
occurs, as mentioned, at the periphery of the mesentery. The developing gut tube
elongates faster than the mesentery causing the mesentery and gut tube to form a
coil. A fixed set of coils arises early in development, and these are the platform on
which the remainder of development occurs. At this point in development, the
duodenal region forms a coil to the right of the midline. The developing hindgut has
already lateralised to the left of the midline. Between left and right lateralized
regions, the gut tube has a hairpin-like conformation and the mesentery occupies
the space between limbs of the hairpin.
The intestine of the proximal limb of hairpin elongates substantially, generating
multiple additional coils. These events are not replicated in the distal limb of
hairpin. Instead, the distal limb of developing gut tube and mesentery, elongate in
tandem. As a result of in-tandem development, they take up a position first in the
upper region of the developing abdominal cavity, and thereafter in the right flank of
the cavity. The last change is important is at causes the highly coiled region of
intestine and mesentery (the forerunner of the ileum and jejunum) to take up a
position in the central region of the abdomen.
Development of the Peritoneum and Peritoneal Cavity
Most mesenteric organogenesis occurs at the periphery of the mesentery. By
full-term, the mesentery and digestive organs have acquired their final conformation
and topographical organization in the coelom. In tandem with this, mechanisms of
mesenteric attachment (see chapter on Anatomy) develop and assist in maintaining
the mesentery and abdominal digestive system in position . The peritoneal reflection
is a major mecha nism by which the mesentery is held in position (Fig. 2.3).
However, the reflection appears to continue to develop after birth. As the peritoneal
landscape determines the shape of the peritoneal cavity, it follows that the
2 Embryology of the Mesentery 13
Fig. 2.3 Topography of
lateral peritoneal reflection
following completion of
mesenteric development. Red
broken line indicates
reflection
peritoneal cavity develops both before and after birth. In fact, changes in the
peritoneal landscape occur throughout life, under the influence of several natural
and artificial (i.e. surgical interruption) factors.
Migration Across the Mesentery
Several cell types use the mesentery as a platform across which to migrate. These
include cells that migrate from the neural crest to the developing intestine where
they will contribute to the enteric nervous system. Primordial germ cells migrate
from the developing hindgut, across the mesentery to the genital ridges where they
will ultimately give rise to adult germ cell.
Regenerative Capacity of the Mesentery and Bioengineering of Abdominal Digestive Organs
The field of mesenteric organogenesis received a considerable boost with the
identification of mesenteric continuity. Prior to this development, multiple groups
had been working separately on the embryological development of digestive system
organs in humans and other species. For example, the sea cucumber and related
species expel its gut tube under the influence of certain stimuli. This is followed by
the regeneration of a new gut tube at the mesenteric margin once occupied by the
previous intestine.
With clarification of mesenteric shape, it became apparent that previously
divergent fields shared a common element in mesenteric inputs. These and other
events have prompted renewed interest and focus on recapitulating the mesenteric
milieu, in bioengineering of liver, pancreatic and intestinal tissue. It is likely that
advances in this area of human embryology could assist in addressing the current
deficit in digestive organs available for transplantation.