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First part of the article

Second part

- J Clin Anat Embryol 2008 1(4):21-32


- J Clin Anat Embryol 2008 1(5):51-62

Mesorectum. Implications of an Anatomy and Surgical Concept. I.


O. Fabian, V. Muntean, R. Simescu, M. Cazacu
IVth Surgical Clinic, "Iuliu Hatieganu" Medicine and Pharmacy University, Cluj-Napoca

Abstract
Perirectal fat separated by the rectal facia - the so-called mesorectum - is the first area of local rectal cancer
dissemination. Thus, its removal along with the rectum affected by the tumour is essential for preventing local
tumour recurrence. The mesorectum, as an anatomical and surgical concept, reconciles two major objectives of rectal
cancer surgery: the radical surgical act and reduced postoperative urinary and genital complications. Besides these
main targets, the concept of total mesorectal excision is useful in determining an avascular area suitable for rectal
dissection and in setting a new parameter for the evaluation of radical surgery (circumferential resection edge).
Understanding the local anatomy and especially the nerves and vascular relations of this anatomical structure is
essential for optimum rectal cancer surgery. Key words: mezorect; cancer rectal; excizia totala a mezorectului.

Rezumat
Adipozitatea perirectala delimitat de fascia proprie a rectului - aa-numitul mezorect - este zona initiala de
diseminare a cancerului de rect, iar indepartarea acesteia in bloc cu rectul tumoral este o conditie esentiala a
prevenirii recidivei locale. Mezorectul ca sj concept anatomo-chirurgical reconciliaza doua obiective ale operatiei
pentru cancerul de rect: radicalitatea actului chirurgical si limitarea sechelelor uro-genitale ale acestuia. In afara
acestor obiectiv principale, conceptul de excizie totala a mezorectului este util pentru defmirea unui plan avascular
pentru disectie i definirea unui parametral pentru evaluarea radicalitatii actului chirurgical (marginea
circumferentiala de rezectie). Cunoaterea anatomiei locale i in special a raporturilor nervoase i vasculare ale
acestei structuri anatomice este esentiala pentru chirurgia optima a cancerului de rect. Cuvinte cheie: mesorectum;
rectal cancer; total mesorectal excision.

Introduction

The history of the mesorectum concept

Radical surgical procedure for cancer means


the removal of the organ affected by the tumour and of
its lymphatic drainage system. In rectal cancer this
means the excision of the rectum and mesorectum
together (1). To accomplish this, one needs to identify
the mobility between tissues of different embryological
origin, to perform precise dissection under visual control
(and with proper light) and to do a delicate opening of
anatomical elements by soft traction, avoiding the tarring
of the anatomical structures (2). Our aim is to give a
brief description of the anatomy of the mesorectum and
its surgical significance.

The landmark in rectal cancer surgery is the


surgical procedure proposed by Miles (3) in 1908,
named by the author "abdominoperineal excision"; its
rapid acceptance by the surgeons and the abandoning of
the local excisions done before led to the significant
improvement of the local disease control (management).
Miles suggested that the resection of the tumour
together with the lymph nodes as applied in breast
cancer should be applied in rectal cancer using a
combine - abdominal and perineal procedure (4).

22

In 1930, Dukes1 proposed a colo-rectal cancer


staging that combined 3 essential criteria: local status,
local and regional lymphatic dissemination and distant
dissemination. The importance of Dukes' staging is
obvious if we consider that its improved version
(Astler-Coller - 5 modifications) continues to be widely
used by surgeons - even though the TNM staging (used
in all other digestive cancers) is more exact.
Both Miles and Dukes proposed in fact a new
concept: rectal cancer has a quantifiable stadium
evolution, as well as the fact that in early, curable
stages, rectal cancer is a compartment disease (6). The
total removal of the rectal "compartment" is (in local
disease stages, without distant metastases) the premise
of local recurrence prevention and of the disease
treatment (7).
In 1939, Dixon (8) gave a systematic approach
to the technique of anterior rectal resection. This
dispensed the patient of the infirmity of carrying a
colostomy. The Dixon resection did not replace the
principle of tumour resection together with the lymph
nodes, but it offered a more physiological solution to
the tumours located at a safe distance from the anal
sphincter. Perfecting the technique - especially, after
Fian introduced the mechanic colorectal anastomosis in
1974 (9) - allowed the surgeons to lower the distal limit
of resection up to 3 cm from the pectineal line.
Miles' concept - the removal of the rectum
together with the perirectal fat (with perirectal lymph
nodes) as a cylindrical segment - has dominated the
surgical thinking for almost 80 years. In time, a
revisiting of the concept was needed because of 2 major
shortcomings: local recurrence of the disease after rectal
resections, sexual and urinary dysfunctions. Local
recurrence of the disease raised awareness that some of
the resections were insufficient. While analyzing rectal
resection samples after surgery performed by several
surgeons, Quirke et al. (10) found inadequate resections
in 27% of the cases - resections were made either
through the edge of the tumour or through satellite
lymph node metastases. With one exception, local
recurrence occurred in these patients. Thus, the
definition of how much perirectal tissue must be
removed in order to prevent local recurrence was
needed. On the other hand, the frequent sexual
dysfunctions that occurred - up to 50% of the patients
that suffered rectal amputation and up to 40% of the
patients with rectal resection (11) - and those of the
storage and urine evacuations- 4%-7,7% (12-13) -raised
the problem of possible hypogastric and erection nerves'
injuries during surgery. This showed that an exact
definition of the perirectal structures that have to be
spared during surgery for rectal cancer was needed {how
to lead the perirectal dissection).

Ovidiu Fabian

In 1982 Heald, Husband and Ryall presented a


solution to all these problems (how much and how),
proposing also a new anatomy - the mesorectum- and
surgical concept - the total mesorectal excision (7). The
new term mesorectum is slightly confusing, seeing that
the rectum is partially an extraperitoneal organ and also
totally fixed, without a mesentery. The imprecise
character of the term was noticed (14-15), some authors
preferring the term of extrafascial excision of the
rectum (16-17). Heald proposed this term out of
practical reasons - the redefinitions of anatomy
structures concerning details of surgical technique - and
also based on embryology data (18). Even some critics
of the new term acknowledge that the mesorectum can
be a structure in itself (19); regardless of this, the term
stands to define the limits of the resection and a better
one does not exist.
For the surgeons, the concept of "total
mesorectum excision" combines five fundamental
principles (20):
- definition of an avascular plane used for dissection,
which Heald pathetically called "the Holy Plane of
rectal surgery"; using this plane for dissection ensures a
radical resection (oncological result) and also the
protection of perirectal nerve structures (functional
result)
- definition of a surgical objective: rectum together with
mesorectum removal without any tarring on the
structures and with intact circumferential (all round)
limits
- definition of a radical surgery evaluation parameter
(circumferential resection limits); radial limits are vital
for the tumour recurrence, even more important than the
proximal and distal limits (21)
- identification (and preservation!) during surgery of the
autonomic nerve plexuses responsible for the erectile
and the urinary functions
- preservation of the anal sphincter function and
decreased number of colostomies performed.
Since 1982 a series of publications supported
the validity and utility of total mesorectal excision
concerning both local recurrence and urogenital
complications prevention after surgery by protecting
autonomic pelvic nerve plexuses (22-30).
These new rectal surgery concepts led to
numerous anatomy studies of the pelvis, as well as to
more precise surgical techniques.
Numerous postoperative complications that
occurred after the introduction of the rectum resection
with total mesorectum excision (31) raised the necessity
that oncology and colo-rectal surgeons master this
technique rigorously. Thus, the introduction of training
programs for total mesorectal excision confirmed the
major advantages of the technique, superior oncology

Dukes CE - The classification of cancer of the rectum , Journal of Pathology and Bacteriology 1932, 35: 323-331 - cited by Astler and Coller (5)

Journal of Clinical Anatomy and Embryology Vol.1 No. 4

results and less postoperative complications (32-33).


Although some authors (especially American authors)
are reticent about this new concept, but the experience
of Norwegian authors (35-37) seems convincing.

Mesorectum
Rectum - elements of descriptive anatomy
Superior (proximal) limit of the rectum
(rectum-sigmoid joint) is considered by the anatomists
to lie at the level of S3 vertebrae. Surgeons consider this
limit to lie at the level of the sacral promontory (38-39).
More important than these topography criteria are the
descriptive ones that consider the beginning of the
rectum in the region where the muscular longitudinal
bands (taeniae) of the colon (longitudinal muscular
layer becomes wider and inverts the rectum completely),
the saculation of the colon (taenia coli), the pelvic
mesocolon {mesocolon sigmoideum) and the

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mobility of the colon (the rectum is practically a fixed


organ) are no longer present.
The lower part of the rectum, the anal canal is
also considered different by anatomists and surgeons
(38-39). The anatomical (or embryological) anal canal
lies between Hilton's skin line (junction between the
mucous membrane and the skin of the anus) and the
pectineate line; it has 2 cm in length and is of
ectodermic origin. The surgical anal canal (or the
functional one) goes up to the anal ring (insertion of the
levator ani muscles into the rectum); it has about 4 cm
in length and corresponds to a region of high internal
pressure (the level of the sphincter ani muscles).
The rectum has 12-15 cm in length and 3
lateral curves (flexures): the upper and inferior ones,
with their convexity to the right, and the middle one
with its convexity to the left. Intralumenal, the flexures
correspond to the Houston valves (transverse folds); the
middle flexure (Kohlrausch) is located where the
peritoneum of the anterior surface reflects over the
urinary bladder or the uterus (fig. 1).

Fig.l. Descriptive anatomy of the rectum.

Rectal arteries
Arterial blood flow for the rectum (fig. 2) is
provided by the superior haemorrhoidal artery and also
by minor arterial sources: medium sacral artery,

medium rectal arteries and branches from the inferior


bladder artery and from the levator ani muscles arteries
(40-41). Blood flow for the anal canal is provided by the
inferior rectal arteries detached from the iliac artery.

24

Ovidiu Fabian

Fig.2. Rectal arteries - by Mandache and Chiricuta (41).


Although they have been described in almost
all anatomy and surgical technique papers, the medium
rectal arteries are variable. Also, the rectal wings
(which, according to classic papers, contain these
arteries) are considered by some authors as artefacts
produced during surgery. Thus, after 83 pelvic detailed
dissections, Sato and Sato (42) found the medium rectal
arteries in only 18 cases (22,2%). Jones et al. (43),
performing 28 pelvic dissections on dead bodies found
in 17 cases (60%) only one medium rectal artery; in all
the cases, a one-sided small size artery was found.
Munteanu (44) found a one-sided medium rectal artery
in 76,7% of the hemipelvises dissected (46 out of 60); in
35% of the cases, the artery had a considerable calibre.
A medium rectal artery needing electrocautery or
ligature is found in only one fifth of the cases, being
more frequently a branch of the internal pudendal artery
or of the inferior bladder artery and rarely comes
directly from the internal iliac artery itself (1). This
medium rectal artery may be important in lymph node

Fig.3. Lymph vessels of the rectum.


a. Main lymphatic streams (by Skandalakis, cited by Curti-50);
b. Lymphatic areas (by Ueno-46)

optimal excision of the rectal cancer; one has to assume


that along such an artery lymph nodes are positioned.
Cancer dissemination along this lymphatic path may
lead to internal iliac, obturator and main iliac arteries
lymph node metastases (fig. 3). This hypothesis,
supported by some Japanese authors (42, 46-48)
justifies an extended lymph node excision, including the
so called lateral lymphatic compartment.
Lymph vessels of the rectum
The lymph vessels of the rectum were first
described by D. Gerota. Until to-day, five methods were
used to study them: dye injected into corpses, dissection
followed by pathology analysis of the surgical samples,
necropsy studies, preoperative dye injection into the
submucosa of the rectum followed by lymphatic
scintigram scan.
There are three lymphatic streams classically
described (41, 49-50) - fig. 3a.

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Journal of Clinical Anatomy and Embryology Vol.1 No. 4

The main lymphatic stream runs upward


through collectors and lymph nodes positioned along
the branches and trunk of the superior rectal artery; from
the level where the superior rectal artery is divided
(Mondor lymphatic hilum), the lymph is drained
towards the lymph nodes of the inferior mesenteric
artery. This lymphatic path is integrated into the
mesorectum. Total excision of the mesorectum provides
total removal of tumour cell disseminations at this level.
Medium lymphatic stream flows along the medium
rectal artery towards the lateral pelvic lymph nodes. The
inferior lymphatic stream is draining the lymph from the
anatomical anal canal to the inguinal lymph nodes. The
inferior lymphatic path has minor importance for rectal
cancer dissemination. This path is important only in
inferior tumours that develop under the pectinate line
and already have massive metastases in the lymph nodes
of the main ascending lymphatic stream (51).
The importance of the medium lymphatic path
is still subject to debate. Japanese authors consider four
groups (areas) of rectal lymph vessels (fig. 3b): the
mesorectal group (rectal lymph nodes), the superior
rectal artery group (area) and the lateral area (46). The
mesorectal area is divided into two regions: the
mesorectum close to the tumour (distal from the tumour
and proximal up to 5 cm from the superior edge of the
tumour) and the remote mesorectum (over 5 cm from
the superior edge of the tumour). The area of the inferior
mesenteric artery includes lymph nodes located between
the origin of the artery and the origin of left colic artery;
distal, the lymph nodes of the superior rectal area are
located along the artery. The lateral area is composed of
6 lymph node groups: the internal pudendal artery group
(lateral to the pelvic plexus), internal iliac artery group
(proximal from the superior vesical artery), the common
iliac artery group, the external iliac artery group, the
obturator group and the sacral group (fig. 3b).
The lateral lymphatic drainage is considered
minor by European and American authors. First studies
have identified this path by injecting dye into corpses
but they didn't determine its importance. After studying
resection samples, Gilchrist (52) described a case of
extraperitoneal rectal cancer with 2 lateral lymph node
metastases, one of them being located in the lymph
nodes of the ascending stream. This type of
dissemination was found by Grinnell in only 1 out of the
118 cases he studied, 63 having lymph node metastases.
Other authors found as well a very low proportion of
this type of metastasis path.
Still, the observations of the Japanese authors
suggest that the lateral dissemination might be
important in extraperitoneal rectal cancer. Ueno et al
(46) found lymph node metastases in 41 out of 455
(16,8%) patients who underwent various rectal
resections of the main tumour together with the

mesorectum (abdominoperineal resection, anterior rectal


resection, Hartman's rectal resection or pelvic
exenteration) and dissection of the lateral lymph node
area. Out of these 41 patients 10 had only lateral lymph
nodes metastases but no mesorectal ones. Considering
the high frequency of the metastases, Ueno calls the
region of the internal pudendal, the internal iliac and the
obturator arteries the "vulnerable field" of this type of
metastasising (88% of the lateral area metastases had
one of these sites). Lateral lymphatic spreading seems to
depend on the distal site of the tumour, on its parietal
depth, on the dissemination in other lymphatic areas and
on its low differential grade. 2 days before surgery,
Maeda et al (53) injected dye with carbon particles
(CH40) into the rectal submucosa of 19 patients with
rectal cancer (8 into the intraperitoneal and 11 into the
extraperitoneal
rectum).
After
surgery
(abdominoperineal resection or anterior rectal resection
with total mesorectal and lateral lymph nodes excision),
the presence of the carbon particles in the lymph nodes
was evaluated. In the case of the 8 patients with
intraperitoneal rectal tumours, the majority of the axial
lymph nodes were positive for staining and all of the
lateral lymph nodes were negative.
In the case of the 11 patients with
extraperitoneal rectal tumours, most (18-73%) axial
lymph nodes were positive for staining but lateral lymph
nodes were positive as well (9-73%). Kawahara et al
(54) used a similar technique, injecting indocyanine
green into the submucosa of 14 patients 30 minutes
before surgery for rectal cancer. 6 patients had positive
staining in the internal iliac lymph nodes areas. In 4 out
of these patients lymph node metastases were present.
Obturator lymph nodes were negative for staining. The
authors concluded that the first station of lateral
lymphatic metastasis path is the internal iliac lymph
nodes area.
Lymphatic scintigram scan studies consider the
lateral lymphatic system of minor importance in rectal
cancer. Sterk et al (55) performed lymphatic scintigram
scans on 16 patients one day before surgery for rectal
cancer. 12 patients had exclusively mesorectal positive
lymph nodes. In 4 patients extramesorectal (lateral)
positive-staining lymph nodes were found; these lymph
nodes were removed during surgery but the pathology
examination revealed the absence of metastases.
Quadros et al (56) revealed positive scintigram scan
lateral lymph nodes in 20% of the patients with rectal
cancer but only in 6,7% of the patients lymph node
metastases were present.
Nerve system of the pelvis
The pelvic nerve system is composed of the
sacral plexus (originating at the level of L4, L5, SI, S2,
S3 vertebrae and innervating the pelvic and the lower

26

Ovidiu Fabian

limb muscles), the pudendal plexus (originating at the


level of S2, S3 and S4 vertebrae, its fibres innervating
the pelvic and the genital organs) and the pelvic
autonomic plexuses (the superior and inferior
hypogastric plexuses). All these plexuses are
intertwined. The superior hypogastric plexus is made of
sympathetic thoracolumbar fibres (responsible for
ejaculation). It is located in the extraperitoneal
conjunctive tissue, anterior to the aortic bifurcation and
the common left iliac vein, at the level of the fifth
lumbar vertebra and the promontory (1). The plexus has
a triangular shape with its top angle pointing cranial; the
hypogastric nerves (right and left) originate at its lateral
angles (56). The delicate fibromatous network of the
areolate tissue provides an avascular plane between the
hypogastric plexus (posterior) and the mesorectum
(anterior). This facilitates the intact dissection of the
mesorectum from the plexus. The avascular plane passes
between the parietal and the visceral layers of the pelvic
fascia. The excision of the rectum together with the
intact mesorectum is obtained by the surgical separation
of these fascial layers along the avascular plane. Each
hypogastric nerve ends in an inferior hypogastric plexus
(right and left). These plexuses are composed of
sympathetic and parasympathetic fibres originating in
the S2, S3 and S4 segments on the path of the erigent
nerves. The parasympathetic fibres provide

the male erection. Each inferior hypogastric plexus has a


rectangular sagittal fenestrated lamina shape. It lies
lateral from the rectum, the prostate, the seminal
vesicles and the posterior of the urinary bladder in males
and lateral from the rectum, the neck of the vagina, the
fornix of the vagina and the posterior face of the urinary
bladder in females (1, 58). The inferior hypogastric
plexus branches provide the innervation for the rectum,
the urinary bladder, the prostate, the seminal vesicles, the
urethra and the corpa cavernosa. The cavernosa nerves
group into nervous bundles going directly to the
posterior and lateral surface of the prostate; the bundles'
thickness decreases from 12 mm at the origin to 6 mm at
the base of the prostate. From this level on, the nerves
follow the arteries and the veins of the prostate capsule,
go upwards to the prostate apex (posterior and lateral to
the urethra) and pass through the urogenital diaphragm.
Pelvic plexuses are located lateral and posterior to the
seminal vesicles (the middle part of the plexus is located
at the top of the seminal vesicles). This is why the
seminal vesicles are the reference point for the
identification of the plexuses during surgery (1, 58).
Also, the cavernous nerves can be identified posterior
and lateral to the prostate and anterior and lateral to the
rectum as a constant vascular and nerve bundle formed
together with the arteries and the veins of the prostate
capsule (58).

Inferior hypogastric plexus


Pudendal n

Fig. 4 - Nerve relations of the rectum and mesorectum.


a - sympathetic innervation diagram of the urinary bladder and the genital organs - by Netter; b - parasympathetic innervation
diagram of the urinary bladder and the genital organs - by Netter; c and d - hypogastric plexuses - by Retzer, Marcio, Wolf (38)

27

Journal of Clinical Anatomy and Embryology Vol.INo.4

Perirectal fasciae
The parietal fascia of the pelvis covers the
walls and the pelvic diaphragm. It stretches also over
the pelvic organs, forming the visceral fasciae. Around
the rectum it forms the own rectal sheath, or perirectal
fascia. It was first mentioned by Toma Ionescu in the
anatomy treatise by Poirier and Charpy (17, 57). The

own rectal fascia encloses the rectum, fatty tissue,


nerves, blood vessels and lymph vessels. At this level,
the fatty tissue is more abundant in the posterior part of
the rectum and looks like a "bilobate lipoma" (2, 44).
The pelvic fascia is more evident in the lateral and
posterior parts of the extraperitoneal rectum and thicker
close to the pelvic diaphragm (44).

Fig.5. Pelvic fasciae.


a and c - in male; b and d - in female
a and b by by Retzer, Marcio, Wolf (38); c and d - by Muntean (44)
The sacral fascia is the thicker part of the
pelvic fascia, covering the concavity of the sacrum and
the coccyx, also nerves, the medium sacral artery and
the sacral veins. The posterior sacral (retrosacral) fascia2
lies between the presacral fascia and the rectal fascia. It
is formed by the reflection of the presacral fascia over
the S4 vertebra. It also unites with the rectal fascia 3-5
cm from the ano-rectal ring (38, 44). According to Sato
and Sato (45), it holds small veins and nervous branches
from the sacral lymph nodes.
2

The rectogenital septum (rectoprostatic in


males and rectovaginal in females) separates the rectum
and the rectal fascia from the seminal vesicles and the
prostate, or from the vagina. The strict term of
Denonvilliers fascia refers to the rectoprostatic fascia,
but it was adopted also for the similar septum of the
female.
The Dennonvilliers fascia is a fibrous structure
more evident and consistent than the rectal fascia; it is
more prominent in young patients and it becomes much

Rectosacral fascia is called by some authors the Waldeyer fascia; others use the same name for the presacral fascia. In fact, W. Waldeyer
described the presacral fascia, but not its recto-sacral extension.

Ovidiu Fabian

28

thinner with age (59). Urologists describe the fascia as


being attached to the prostate and the seminal vesicles.
Colo-rectal surgeons consider it more adherent to the
rectum then to these genital organs (60). From the
histology point of view, the fascia is formed of dense
collagen fibres, smooth muscles and elastin fibres. The
forming of the Deninvilliers fascia was explained in 2
ways: by fusion of the 2 membranes of the embryonic
rectovesical pouch or by compression of the embryonic
mesenchymal layers. The origin and the forming of the
Denonvilliers fascia were the source of a surgical
misunderstanding: the existence of fascial layers
separable during surgery (61);
in
although Richardson3 showed the
existence of two elastin layers in cannot be identified
the rectogenital septum (59), they The cavernous nerves
during surgical dissection (60). on each side of the
and blood vessels are located vascular and nerves
Denonvilliers fascia, forming bundles (fig. 8b).
The lateral ligaments ("the rectal wings") are
described in classic anatomy treatises as fibrous
triangular structures with the base to the lateral pelvic
wall and the top pointing to the rectum. They include
the medium rectal arteries. Their existence is subject to
debate because they might be surgical (dissection)
artefacts. Medium rectal arteries over 1 mm in diameter
exist inconstantly. When present, they are rarely
bilateral. After 28 pelvic dissections, Jones et al. (43),
drew several conclusions that contradict classic data: in

none of the cases bilateral medium rectal arteries were


present, although in 17 of the cases they found a
unilateral one; in all of the cases, the artery had a
reduced diameter (never over 2 mm in diameter); in
none of the cases the fibrous structure of the lateral
ligaments as described in textbooks was found; only
inconstant fibrous structures and nerve fibres were
found - which cannot be mistaken for the lateral
ligaments.
On the other hand and out of caution,
surgeons treat these "dissection artefacts" almost always
with care, seeing them as potential haemorrhage
sources. This is why the majority of the surgical
handbooks recommend the ligature or electrocautery of
these structures. Sato and Sato (42) divide each rectal
ligament into 2 parts: lateral (containing the medial
rectal artery and the pelvic splanechnic nerves) and
medial (containing the hypogastric artery and the
branches of the inferior hypogastric plexus). The 2 parts
are located on each side of the rectangular lamina of the
corresponding inferior hypogastric plexus. In the lateral
part, the medium rectal artery joins the splanechnic
pelvic (erigent) nerves in sharp edge. In the medial part,
the artery runs parallel to the rectal branches of the
inferior hypogastric plexus (fig. 6). The division
proposed by Sato is important for the ligature of the
lateral ligaments: the ligature of the ligament in its
lateral part is followed by erigent nerve lesions
(followed by erectile dysfunctions); medial part ligature
is practically without urology complications.

Fig.6. Structure of lateral ligament - by Sato (42).

Richardson AC - The rectovaginal septum revisited: its relationship to rectocele and its importance in rectocel repair, Clin Obstet Gynecol 1993,
36: 976-983 - cited by Lindsey (58) and van Ophoven (59).

Journal of Clinical Anatomy and Embryology Vol.1 No. 4

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Address for correspondence:


Ovidiu Fabian
CI. Chirurgie IV, Spitalul CF Cluj-Napoca, str. Republicii nr. 18, 400015
email: fabianovidiu@yahoo.com

Mesorectum. Implications of an Anatomy and Surgical Concept. II.


O. Fabian, V. Muntean, R. Simescu, M. Cazacu
IVth Surgical Clinic, "Iuliu Hatieganu" Medicine and Pharmacy University, Cluj-Napoca

Abstract
Perirectal fat separated by the rectal facia - the so-called mesorectum - is the first area of local rectal cancer
dissemination. Thus, its removal along with the rectum affected by the tumour is essential for preventing local
tumour recurrence. The mesorectum, as an anatomical and surgical concept, reconciles two major objectives of rectal
cancer surgery: the radical surgical act and reduced postoperative urinary and genital complications. Besides these
main targets, the concept of total mesorectal excision is useful in determining an avascular area suitable for rectal
dissection and in setting a new parameter for the evaluation of radical surgery (circumferential resection edge).
Understanding the local anatomy and especially the nerves and vascular relations of this anatomical structure is
essential for optimum rectal cancer surgery. Key words: mesorectum; rectal cancer; total mesorectal excision.
Rezumat
Adipozitatea perirectala delimitat de fascia proprie a rectului aa-numitul mezorect - este zona initiala de
diseminare a cancerului de rect, iar indepartarea acesteia in bloc cu rectul tumoral este o conditie esentiala a
prevenirii recidivei locale. Mezorectul ca si concept anatomo-chirurgical reconciliaza doua obiective ale operatiei
pentru cancerul de rect: radicalitatea actului chirurgical si limitarea sechelelor uro-genitale ale acestuia. In afara
acestor obiectiv principale, conceptul de excizie totala a mezorectului este util pentru definirea unui plan avascular
pentru disectie i definirea unui parametru pentru evaluarea radicalitatii actului chirurgical (marginea
circumferentiala de rezectie). Cunoasterea anatomiei locale si in special a raporturilor nervoase i vasculare ale
acestei structuri anatomice este esentiala pentru chirurgia optima a cancerului de rect. Cuvinte cheie: mezorect;
cancer rectal; excizia totala a mezorectului

Embryology

The gastrointestinal tract develops from the 3 parts of


the embryological intestinal tube: the mouth,
oesophagus, stomach, duodenum and bile tract originate
in die anterior intestine; the small intestine and the colon
(up to the distal half of the transverse colon) originate in
the medium intestine. The descendent colon, the sigma
and the rectum develop from the posterior intestine. Its
distal segment ends in a pouch (cloaca); the allantois
opens in the anterior part of this pouch. The pouch is of
endodermic origin and is sealed (closed) by an
ectodermic membrane (the cloacal membrane proctodeum) (62, 57) (fig. 7).

During the sixth week of development, a


mesodermal septum divides the cloaca into an anterior
cavity (the urogenital sinus) and a posterior cavity (the
anal canal). This septum merges in the seventh week
with the cloacal membrane forming the perineal body.
Thus, the cloacal membrane is divided into a urogenital
membrane (the larger anterior part) and an anal
membrane (the smaller posterior part). The anal
membrane ends in a depression covered by the ectoderm
(anal depression - the origin of the anatomical anal
canal). During the eighth week the anal membrane
disappears. The location where the anal membrane was

52

Ovidiu Fabian

inserted is called the pectinate line, although there are


no consistent arguments in favour or against its
existence (40). Following this development, the rectum
and the superior anal canal are of endodermic origin and
their vascularisation is provided by the inferior
mesenteric artery; the inferior anal canal (anatomical) is
of ectodermic origin and its vascularisation is provided

by branches of the intern iliac artery. The tubercles


develop on each side of the anal membrane from the
somatic mesoderm; these tubercles merge (in
"horseshoe" shape) posterior to the rectum and then
unite with the perineal body. The external anal sphincter
is made of this structure.

Fig.7. The development of the rectum, anal canal and genito-urinary organs,
a - diagram of the digestive tract - by Sadler (62).

Fig.7. The development of the rectum, anal canal and genito-urinary organs, b development of the rectum, anal canal and genito-urinary organs - by Sadler (62).

Journal of Clinical Anatomy and Embryology Vol.1 No. 5

The primitive (embryological) intestinal tract is


suspended posterior by a primitive mesentery, in which
blood and lymphatic vessels and lymph nodes develop.
At the level of the anterior intestine, this primitive
mesentery forms the bursa omentalis. At the level of the
medium intestine, the mesentery of the proximal colon
is formed. At the level of the posterior embryological
intestine, the mesentery of the distal colon and the
mesorectum are formed (63).

53
Mesorectum
The mesorectum is not a real mesentery and
that is why the term must be accepted as a linguistic
convention. The term mesorectum defines the adipose
tissue that surrounds the rectum, surrounded by its own
fascia and is the first field of rectal cancer spreading
(64)-fig. 8.

Fig.8. Mesorectum a - sagittal


section - by Heald (2).

Fig.8. Mesorectum b - transversal section - by Heald (2) representation of the histology sample obtained by Patrick Walsh.

54

The fascia that circumscribes the rectum offers a


relative avascular dissection plane (a very thin layer of
lax tissue located between the parietal and the visceral
layers of the pelvic fascia); respecting this dissection
plane reconciles the oncological imperative of the
operation with the genito-urinary function preservation.
The plane is pathetically called by Heald "the Holy
Plane" of surgical dissection (2); Skandalakis proposes
the plane to be called the Heald plane (40).
In what concerns the phylogenetic origin of the
mesorectum, an interesting comparative anatomy study
was elaborated by Nano et al (65). By comparing the
observations after the dissection of three animal species
(dog, pig and a primate species - Macaca ape) and of
human foetuses, Nano et al concluded that the
mesorectum is absent in quadruped mammals, but is
present in primates. In primates, perirectal fat is more
abundant and is surrounded by a fascia resembling the
perirectal fascia in humans. Similarly, the lateral
ligaments are present only in primates and humans. One
cannot conclude about the evolutive moment of these
structures' appearance, but it is quite likely that they
developed along with the upright walking position. This
was followed by important anatomical and functional
modifications (the transformation of a large part of the
rectum into an extraperitoneal organ, the mechanical
stress of the rectum in this position, the perirectal fat
increased development in order to absorb the
mechanical shock waves). The perirectal adipose wrap
(the mesorectum) reaches the rectal adventitia (64); this
is not a macroscopically identifiable structure, but it
substitutes the visceral peritoneum in the extraperitoneal
part of the rectum. Posterior, the mesorectum along with
perirectal fascia reach the presacral fascia. The posterior
face of the mesorectum looks like a "bilobate lipoma",
due to a median depression (2). Lateral, the presacral
fascia is perforated by several apertures through which
the rectal branches of the inferior hypogastric plexus
and the medium rectal vessels (when present) pass.
Anterior, the mesorectum stretches up to de
Denonvilliers fascia; actually, the perirectal fascia is
sometimes mistaken for the so-called "posterior layer"
of the Denonvilliers fascia. Inferior, the mesorectum
stretches up to the insertion of the levator ani.
The distribution of the lymph nodes of the
mesorectum was studied on resection samples and on
corpses by Topor and Galandiuk (66, 6). After dividing
the mesorectum into 4 quadrants (posterior, right lateral,
left lateral and anterior) and into 3 parts (corresponding
to the superior, medium and inferior thirds of the
rectum) they concluded: most of the lymph nodes (92%)
are located in the posterior quadrant and in the superior
2/3 of the mesorectum; the superior third of the rectum
has no mesorectum in the anterior quadrant; most of the
lymph nodes are small (0,5-3 mm); considering the

Ovidiu Fabian

small size of the lymph nodes, it is possible (in the


absence of a fat solvent) to see tsome of the rectal
cancers as being in a lower stage. Referring to this last
aspect, Andreola etal (67) showed that 45% of the
mesorectal metastasised lymph nodes had less than 5
mm in diameter; 14% of the patients with lymph node
metastases had them only in such small nodes. Wang et
al. (68) found lymph nodes smaller than a half
millimetre in 5,8% of the cases; occult lymph node
metastases were found in 29% of the investigated
patients.
The imagistic exploration of the mesorectum
can be performed using computed tomography,
intrarectal ultrasound and MRI. Computed tomography
scan is accurate in evaluating the depth of the tumour's
invasion into the walls of the rectum, the tumour
relations with adjacent organs (especially when the
digital exploration of the rectum raises the suspicion of
a proximity invasion of the tumour), as well as the
presence of peritumoral adenopathies. It is also true that
computed tomography is used for diagnose and
evaluation of tumour recurrence rather than for the
evaluation of the primary rectal tumour.
Intrarectal ultrasound is used to determine the
tumoural invasion of the rectal wall (the mucosa - Tl,
the own musculature - T2, the adventitia and the
mesorectal fat - T3, the invasion of adjoining organs T4) as well as the presence and size of peritumoral
adenopathies - Nl (69); along with its major advantages
(efficiency, non-invasiveness, possibility to repeat it
risk free), intrarectal ultrasound accuracy depends on
the skills and experience of the person performing it
(70). It is also true that in common practice intrarectal
ultrasound is the most frequently used method for
preoperative rectal cancer staging.
MRI seems to be the most sensitive method for
the examination of the mesorectum. Fascial planes as
well as perirectal areas are accurately identified with
this method (39) (fig. 9)
The mesorectum appears as a structure with
high intensity signal. The mesorectal fascia (the own
rectal fascia) appears as a straight structure with low
intensity signal. The presacral fascia appears as a
structure with low signal. The virtual space between the
presacral fascia and the rectal fascia is represented by
the retrorectal space. The retrosacral fascia and its
peritoneal reflexion can also be identified by MRI. The
Denonvilliers fascia is shown on MRI scan as a structure
with low signal attached to the recto-vesical recess. The
lateral ligaments cannot be identified by MRI scanning;
still, their position is indicated by the medium rectal
vessels when present. The inferior hypogastric plexuses
can be easily identified on parasagittal sections as
rectangular structures of 2-4 cm in length, positioned
medial from the lateral pelvic walls

Journal of Clinical Anatomy and Embryology Vol! No. 5

55

and the iliac vessels. From the rectal coats, only the
mucosa (shown as a fine line with low signal), the
submucosa (with high intensity signal) and the muscular
coat as a 2 layer structure (internal layer - regular corresponding to the circular muscles; external layer irregular - corresponding to the longitudinal muscles)

can be identified by MRI scanning. The adventitia


cannot be identified, but mesorectal fat (the
mesorectum) is shown as a high intensity structure that
encloses the rectum. Lymph nodes are shown as ovoid
structures with high intensity signal (71).

Fig.9. Aspect of the mesorectum in an MRI image (sagittal section) - by Salerno (39).

Implications of the concept of mesorectum


The treatment of rectal cancer has one
oncological objective (total tumour and lymphatic area
removal) and 2 functional ones (the preservation of the
anal sphincteral function and of the uro-genital
functions). The preservation of the sphincter apparatus
depends on the site of the tumour, whereas the total
removal of the tumour site (rectum and mesorectum)
and the prevention of uro-genital sequelae are
determined by the dissection plane. This plane forms as
a result of the embryological development of the rectum
and mesorectum.
Heald (2) draws the attention to the dissection
in this plane (the cause of local recurrence of the tumour
due to insufficient removal of perirectal tumour
deposits) and also to the dissection outside it (leading to
pelvic nerve plexuses injuries). Another element on
which Heald insists is that dissection be made sharp, not
blunt, since this latter causes the fibrous adhesions of
the mesorectal fascia to the adjoining structures to tear
towards the mesorectum or towards these structures; as
a result, the risk of tearing fragments from the

mesorectum appears and the resection becomes


insufficient, with the lateral edge invaded by the
tumour.
Radical resection of the tumoral rectum is
defined by the tumour-free proximal, the distal and the
lateral (circumferential) edges . The proximal resection
edge raises no problems because it is done at the level
where the vasculature (after the ligature of the superior
rectal or the inferior mesentery pedicle) assures the
viability of the tissues. The distal resection depends on
the tumour site (distance from the pectinate line); the
initial distance of 5 cm was lowered to 2 cm (4), but a
diminishing under this limit compromises the radicalism
of the surgical act. In case of low-sited tumours, proper
rectum dissection can provide an adequate resection
edge (Goligher, cited by Yeatman - 4). Still, the
preservation of the sphincter apparatus must not
compromise the radicalism of the operation.
An important feature of the rectal cancer
development is the radial dissemination in the perirectal
fat (72). The dissemination can be continuous,
expansive but also irregular, infiltrative and
discontinuous (10, 72) - fig. 10.

56

Ovidiu Fabian

Fig. 10. Rectal tumour dissemination in the mesorectum - continuous and discontinuous
- according to Quirke (10).

The circumferential (lateral) edge of the


resection was studied for the first time as a prognostic
factor and a radical operation parameter by Quirke et al
(10). They studied resection samples from 52 patients
who underwent surgery for rectal cancer. By performing
transversal sections and morphometric measurements,
they managed to determine the lateral edge of the
tumour as being the most lateral continuous or
discontinuous penetration of the mesorectum.
Circumferential invasion was defined as tumoral direct
infiltration into the resection edge of the sample or as a
"safety limit" of less than 1 mm in thickness. According
to this definition, the lateral edge was found to be
invaded in 27% of the cases. Their presence - 85% of
local tumour recurrence in the case of lateral edge
invasion, as compared to only 3% of tumour-free edges confirmed that insufficient resection is the main cause of
local recurrence of the disease. Further studies (73-76)
had similar results, confirming the importance of lateral
resection edge invasion as a prognostic factor. The
lateral means of invasion (direct, discontinuous, lymph
node metastasis, perineural invasion, lymphatic or
vascular invasion) has no prognostic significance, but the
invasion itself (76). Some authors (78) consider that the
distance between the lateral limit of the tumour and the
resection edge must be minimum 2 mm, whereas others
(76) found no such correlation.
For the T1-T3 tumoral stages, Quirke et al (79)
set 3 degrees of rectal resection with mesorectal
excision. When the dissection is performed in the fascial
plane of the mesorectum, the letter one is thick and
smooth (possible defects do not exceed 5 mm in depth),
without lesions of the fatty tissue; the distal edge is

adequate, no "cone" shape towards the tumour. In the


case of a dissection performed in the mesorectal plane,
the mesorectum on the resection sample has an irregular
surface with loss of fatty tissue over 5 mm in depth; the
distal edge of the mesorectum ends in a cone shape. In
the third case, the dissection is performed in the
muscular plane of the rectum; the mesorectum is thin,
with deep defects that go up to the muscular layer; the
radial edge of resection is irregular with muscular layer
appearing here and there.
Pelvic nerves preservation is possible in T1-T3
tumoral stages; depending on how this target is met, 4
types of surgical procedures have been described (8081): total preservation of autonomic nerves; unilateral
preservation of the autonomic nerves; superior
hypogastric plexus resection and pelvic plexuses
preservation; resection of the superior and one of the
inferior plexuses and preservation of one of the pelvic
plexuses (fig. 11).
During surgery, several steps with high risk for
pelvic nerves injuries can be identified: the ligature of
the inferior mesenteric artery, the posterior dissection,
the lateral dissection and the anterior dissection (59, 82).
During the ligature of the inferior mesenteric artery
(especially if this is done at its origin in the aorta), the
sympathetic fibres of the superior hypogastric plexus are
vulnerable (59); the lesion of these fibres leads to
retrograde ejaculation. To avoid this complication and
when no palpable adenopathies along the inferior
mesenteric artery are present, Phang (83) recommends
that the ligature of the artery is done over or beneath the
origin of the left colic artery (depending on the segment
of the colon that will be used for the anastomosis).

Journal of Clinical Anatomy and Embryology Vol.1 No. 5

57

Fig.l 1. Preservation of the autonomic innervation during rectal resection with mesorectal
excision - by Yano and Moran (81)

The first area of risk within the pelvis is


located at the level of the posterior dissection plane;
here, the risk is to injure the hypogastric nerves which
have only sympathetic fibres (59, 82). Correct dissection
is performed within the lax conjunctive tissue right
outside the mesorectal fascia. The hypogastric nerves
are located close to the lateral side of this plane. They
can be easily injured if the plane is not rigorously
followed, if a blunt dissection is performed or if the
bleeding is not carefully controlled, which then leads to
poor visibility over the dissection plane.
The second risk area is at the level of the lateral
dissection site. Excessive traction over the rectum brings
the inferior hypogastric plexus upwards and medial,
exposing
it
to
injuries
during
the
ligature/electrocauterization of the medium rectal artery
and the corresponding lateral ligament. Extensive lymph
node excision (including the lymph nodes of the lateral
compartment) recommended by Japanese authors is a
major risk of injury of these nerves, which at this level
include both sympathetic and parasympathetic fibres.
The third major risk area is at the level of
anterior dissection. The space between the rectum
(posterior) and the seminal vesicles and prostate
(anterior) is very narrow. During dissection at this level
or during haemostasis performed in this difficult area,
cavernous nerves are exposed to injuries. These nerves
contain especially parasympathetic fibres, their injury
leading to impotence.

There is agreement regarding the posterior and


lateral dissection plane, but in what concerns the
anterior dissection plane, opinions diverge. The
dissection "between" the anterior and posterior layers of
the Denonvilliers fascia - although mentioned by some
authors - is illusory, because the recto-prostate septum
has in fact no separable layers during surgery (59).
Lindsey (58) defines 3 planes for the anterior dissection:
perirectal, mesorectal and extramesorectal plane (fig.
12).
The perirectal plane (perimuscular) - located
close to the rectal muscles but within the rectal fascia -is
not an anatomical plane. The mesorectal plane is an
anatomical one, in which the rectal fascia is separated
from the Denonvilliers fascia, but not so clear as in the
lateral and posterior part of the rectum. The extramesorectal
plane implies the resection of the Denonvilliers fascia
revealing the prostate and the seminal vesicles to the
anterior plane, but with high risk of injury of the
cavernous nerves. Because the anterior mesorectum is
thin, and out of oncological reasons, Heald (84) favours
systematic dissection anterior to the Denonvilliers fascia.
Still, the highest risk of local recurrence is present in
tumours located on the anterior part of the rectum (85).
Thus, the opinion of authors such as Lindsey (86) or
Flati (87), who recommend that dissection be performed
anterior to the Denonvilliers fascia only in anterior
cancers, is justified.

58

Ovidiu Fabian

Fig. 12. Anterior dissection planes - by Lindsey (59)


A - perirectal plane
B - mesorectal plane
C - extramesorectal plane
The total excision of the mesorectum removes
the lymph nodes of the mesorectal area, but not those of
the lateral area. The importance of this area in
extraperitoneal rectal cancers is still subject to debate.
Also, the significance of the metastasis' stage in this area
is differently interpreted: in the TNM classification,
European and American authors integrate these
metastases in category Ml (systemic disease) whereas
Japanese authors integrate them into category N3
(regional dissemination) - a category that doesn't exist in
the AJCC classification (81, 88). The Japanese authors
(42, 46, 53, 89) are in favor of lymph adenectomy,
which should be extended to the lateral compartment in
case of extraperitoneal rectal cancers, but this leads to a
high rate of uro-genital sequelae. Analysing a series of
variables and statistically eliminating those irrelevant,
Sugihara et al. (90) conclude that cancers present in
females, extraperitoneal tumour location, tumour size (4
cm and over) and the presence of perirectal lymph nodes
metastasis are significantly associated with increased
incidence of the metastases in the lateral lymph nodes
area. The new techniques of lymph nodes
micrometastases identification by PCR (Polymerase
Chain Reaction) (91), as well as those of
immunoscintigraphy and radio-immune-guided surgery
(92) will probably contribute to the exact evaluation of
this lymphatic path and also to the identification of a
patient subgroup that will benefit from the
lymphadenectomy of the lateral compartment (93).

The laparoscopic excision of the mesorectum


benefits from all the advantages of this type of
intervention: excellent view, rapid mobilisations of the
patient after surgery, rapid resume of intestinal activity,
of oral food intake and of physical activity, short
postoperative recovery with the possibility to start
adjuvant therapy early (94-96). Numerous studies have
demonstrated the feasibility of the laparoscopic
procedure (97-100). Still, one must mention that these
studies have been made on small groups of patients, in
specialized departments, with different selection criteria
for patients' admittance. All these differences are
making the comparison with classic surgery difficult, as
well as the definition of selection criteria of the patients
who can optimally benefit from this technique (101).
The trial conducted and published by Quah (98) shows a
surprisingly high rate of sexual and vesical dysfunctions
after the laparoscopic excision of the mesorectum for
rectal cancer as compared with the open procedure; this
is caused by the technically difficult lateral and anterior
dissection. The laparoscopy technique is an advanced
procedure (96). That is why further studies are necessary
to determine its role (including the patients' selection
criteria) in rectal cancer surgery (102).
Conclusions
The mesorectum is an anatomically identifiable
structure originating in the primitive dorsal mesentery.
The term is inexact from the anatomy point of view and

Journal of Clinical Anatomy and Embryology Vol.1 No. 5

59

it must be accepted as a linguistic convention.


The dissection along the anatomical avascular
mesorectal plane and the total mesorectum excision
reconcile the oncological objective (total rectal and
perirectal compartment excision) with the functional
objective (sparing the autonomic innervation). The
degree of mesorectal invasion, but also that of the
mesorectal excision, have prognostic value.
The laparoscopic excision of the mesorectum,

although technically difficult, is feasible; its oncological


results are similar to those of open surgery but urinary
and genital complications are more frequent.
The role of extensive pelvic lymphadenectomy
(including the radial compartment) is controversial; no
criteria have yet been established for the identification
of the patients who might benefit from these
completions of the standard surgical procedure.

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Address for correspondence:


Ovidiu Fabian, CI. Chirurgie IV, Spitalul CF Cluj-Napoca, str. Republicii nr. 18, 400015;
email: fabianovidiu@yahoo.com

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