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Mesorectum. Implications of an Anatomy and Surgical Concept

Article · January 2008

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Ovidiu Vasile Fabian Valentin Muntean


Iuliu Haţieganu University of Medicine and Pharmacy Iuliu Haţieganu University of Medicine and Pharmacy
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First part of the article - J Clin Anat Embryol 2008 1(4):21-32
Second part - 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 delimitatǎ de fascia proprie a rectului - aşa-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). Cunoa‚terea 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 landmark in rectal cancer surgery is the
the removal of the organ affected by the tumour and of surgical procedure proposed by Miles (3) in 1908,
its lymphatic drainage system. In rectal cancer this named by the author "abdominoperineal excision"; its
means the excision of the rectum and mesorectum rapid acceptance by the surgeons and the abandoning of
together (1). To accomplish this, one needs to identify the local excisions done before led to the significant
the mobility between tissues of different embryological improvement of the local disease control (management).
origin, to perform precise dissection under visual control Miles suggested that the resection of the tumour
(and with proper light) and to do a delicate opening of together with the lymph nodes as applied in breast
anatomical elements by soft traction, avoiding the tarring cancer should be applied in rectal cancer using a
of the anatomical structures (2). Our aim is to give a combine - abdominal and perineal procedure (4).
brief description of the anatomy of the mesorectum and
its surgical significance.
22 Ovidiu Fabian

In 1930, Dukes1 proposed a colo-rectal cancer In 1982 Heald, Husband and Ryall presented a
staging that combined 3 essential criteria: local status, solution to all these problems (how much and how),
local and regional lymphatic dissemination and distant proposing also a new anatomy - the mesorectum- and
dissemination. The importance of Dukes' staging is surgical concept - the total mesorectal excision (7). The
obvious if we consider that its improved version new term mesorectum is slightly confusing, seeing that
(Astler-Coller - 5 modifications) continues to be widely the rectum is partially an extraperitoneal organ and also
used by surgeons - even though the TNM staging (used totally fixed, without a mesentery. The imprecise
in all other digestive cancers) is more exact. character of the term was noticed (14-15), some authors
Both Miles and Dukes proposed in fact a new preferring the term of extrafascial excision of the
concept: rectal cancer has a quantifiable stadium rectum (16-17). Heald proposed this term out of
evolution, as well as the fact that in early, curable practical reasons - the redefinitions of anatomy
stages, rectal cancer is a compartment disease (6). The structures concerning details of surgical technique - and
total removal of the rectal "compartment" is (in local also based on embryology data (18). Even some critics
disease stages, without distant metastases) the premise of the new term acknowledge that the mesorectum can
of local recurrence prevention and of the disease be a structure in itself (19); regardless of this, the term
treatment (7). stands to define the limits of the resection and a better
In 1939, Dixon (8) gave a systematic approach one does not exist.
to the technique of anterior rectal resection. This For the surgeons, the concept of "total
dispensed the patient of the infirmity of carrying a mesorectum excision" combines five fundamental
colostomy. The Dixon resection did not replace the principles (20):
principle of tumour resection together with the lymph - definition of an avascular plane used for dissection,
nodes, but it offered a more physiological solution to which Heald pathetically called "the Holy Plane of
the tumours located at a safe distance from the anal rectal surgery"; using this plane for dissection ensures a
sphincter. Perfecting the technique - especially, after radical resection (oncological result) and also the
Fian introduced the mechanic colorectal anastomosis in protection of perirectal nerve structures (functional
1974 (9) - allowed the surgeons to lower the distal limit result)
of resection up to 3 cm from the pectineal line. - definition of a surgical objective: rectum together with
Miles' concept - the removal of the rectum mesorectum removal without any tarring on the
together with the perirectal fat (with perirectal lymph structures and with intact circumferential (all round)
nodes) as a cylindrical segment - has dominated the limits
surgical thinking for almost 80 years. In time, a - definition of a radical surgery evaluation parameter
revisiting of the concept was needed because of 2 major (circumferential resection limits); radial limits are vital
shortcomings: local recurrence of the disease after rectal for the tumour recurrence, even more important than the
resections, sexual and urinary dysfunctions. Local proximal and distal limits (21)
recurrence of the disease raised awareness that some of - identification (and preservation!) during surgery of the
the resections were insufficient. While analyzing rectal autonomic nerve plexuses responsible for the erectile
resection samples after surgery performed by several and the urinary functions
surgeons, Quirke et al. (10) found inadequate resections - preservation of the anal sphincter function and
in 27% of the cases - resections were made either decreased number of colostomies performed.
through the edge of the tumour or through satellite Since 1982 a series of publications supported
lymph node metastases. With one exception, local the validity and utility of total mesorectal excision
recurrence occurred in these patients. Thus, the concerning both local recurrence and urogenital
definition of how much perirectal tissue must be complications prevention after surgery by protecting
removed in order to prevent local recurrence was autonomic pelvic nerve plexuses (22-30).
needed. On the other hand, the frequent sexual These new rectal surgery concepts led to
dysfunctions that occurred - up to 50% of the patients numerous anatomy studies of the pelvis, as well as to
that suffered rectal amputation and up to 40% of the more precise surgical techniques.
patients with rectal resection (11) - and those of the Numerous postoperative complications that
storage and urine evacuations- 4%-7,7% (12-13) -raised occurred after the introduction of the rectum resection
the problem of possible hypogastric and erection nerves' with total mesorectum excision (31) raised the necessity
injuries during surgery. This showed that an exact that oncology and colo-rectal surgeons master this
definition of the perirectal structures that have to be technique rigorously. Thus, the introduction of training
spared during surgery for rectal cancer was needed {how programs for total mesorectal excision confirmed the
to lead the perirectal dissection). major advantages of the technique, superior oncology

1
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 23

results and less postoperative complications (32-33). mobility of the colon (the rectum is practically a fixed
Although some authors (especially American authors) organ) are no longer present.
are reticent about this new concept, but the experience The lower part of the rectum, the anal canal is
of Norwegian authors (35-37) seems convincing. also considered different by anatomists and surgeons
(38-39). The anatomical (or embryological) anal canal
lies between Hilton's skin line (junction between the
Mesorectum mucous membrane and the skin of the anus) and the
pectineate line; it has 2 cm in length and is of
Rectum - elements of descriptive anatomy ectodermic origin. The surgical anal canal (or the
functional one) goes up to the anal ring (insertion of the
Superior (proximal) limit of the rectum levator ani muscles into the rectum); it has about 4 cm
(rectum-sigmoid joint) is considered by the anatomists in length and corresponds to a region of high internal
to lie at the level of S3 vertebrae. Surgeons consider this pressure (the level of the sphincter ani muscles).
limit to lie at the level of the sacral promontory (38-39). The rectum has 12-15 cm in length and 3
More important than these topography criteria are the lateral curves (flexures): the upper and inferior ones,
descriptive ones that consider the beginning of the with their convexity to the right, and the middle one
rectum in the region where the muscular longitudinal with its convexity to the left. Intralumenal, the flexures
bands (taeniae) of the colon (longitudinal muscular correspond to the Houston valves (transverse folds); the
layer becomes wider and inverts the rectum completely), middle flexure (Kohlrausch) is located where the
the saculation of the colon (taenia coli), the pelvic peritoneum of the anterior surface reflects over the
mesocolon {mesocolon sigmoideum) and the urinary bladder or the uterus (fig. 1).

Fig.l. Descriptive anatomy of the rectum.

Rectal arteries medium rectal arteries and branches from the inferior
bladder artery and from the levator ani muscles arteries
Arterial blood flow for the rectum (fig. 2) is (40-41). Blood flow for the anal canal is provided by the
provided by the superior haemorrhoidal artery and also inferior rectal arteries detached from the iliac artery.
by minor arterial sources: medium sacral artery,
24 Ovidiu Fabian

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

Although they have been described in almost optimal excision of the rectal cancer; one has to assume
all anatomy and surgical technique papers, the medium that along such an artery lymph nodes are positioned.
rectal arteries are variable. Also, the rectal wings Cancer dissemination along this lymphatic path may
(which, according to classic papers, contain these lead to internal iliac, obturator and main iliac arteries
arteries) are considered by some authors as artefacts lymph node metastases (fig. 3). This hypothesis,
produced during surgery. Thus, after 83 pelvic detailed supported by some Japanese authors (42, 46-48)
dissections, Sato and Sato (42) found the medium rectal justifies an extended lymph node excision, including the
arteries in only 18 cases (22,2%). Jones et al. (43), so called lateral lymphatic compartment.
performing 28 pelvic dissections on dead bodies found
in 17 cases (60%) only one medium rectal artery; in all Lymph vessels of the rectum
the cases, a one-sided small size artery was found.
Munteanu (44) found a one-sided medium rectal artery The lymph vessels of the rectum were first
in 76,7% of the hemipelvises dissected (46 out of 60); in described by D. Gerota. Until to-day, five methods were
35% of the cases, the artery had a considerable calibre. used to study them: dye injected into corpses, dissection
A medium rectal artery needing electrocautery or followed by pathology analysis of the surgical samples,
ligature is found in only one fifth of the cases, being necropsy studies, preoperative dye injection into the
more frequently a branch of the internal pudendal artery submucosa of the rectum followed by lymphatic
or of the inferior bladder artery and rarely comes scintigram scan.
directly from the internal iliac artery itself (1). This There are three lymphatic streams classically
medium rectal artery may be important in lymph node described (41, 49-50) - fig. 3a.

Fig.3. Lymph vessels of the rectum.


a. Main lymphatic streams (by Skandalakis, cited by Curti-50);
b. Lymphatic areas (by Ueno-46)
Journal of Clinical Anatomy and Embryology Vol.1 No. 4 25

The main lymphatic stream runs upward mesorectum (abdominoperineal resection, anterior rectal
through collectors and lymph nodes positioned along resection, Hartman's rectal resection or pelvic
the branches and trunk of the superior rectal artery; from exenteration) and dissection of the lateral lymph node
the level where the superior rectal artery is divided area. Out of these 41 patients 10 had only lateral lymph
(Mondor lymphatic hilum), the lymph is drained nodes metastases but no mesorectal ones. Considering
towards the lymph nodes of the inferior mesenteric the high frequency of the metastases, Ueno calls the
artery. This lymphatic path is integrated into the region of the internal pudendal, the internal iliac and the
mesorectum. Total excision of the mesorectum provides obturator arteries the "vulnerable field" of this type of
total removal of tumour cell disseminations at this level. metastasising (88% of the lateral area metastases had
Medium lymphatic stream flows along the medium one of these sites). Lateral lymphatic spreading seems to
rectal artery towards the lateral pelvic lymph nodes. The depend on the distal site of the tumour, on its parietal
inferior lymphatic stream is draining the lymph from the depth, on the dissemination in other lymphatic areas and
anatomical anal canal to the inguinal lymph nodes. The on its low differential grade. 2 days before surgery,
inferior lymphatic path has minor importance for rectal Maeda et al (53) injected dye with carbon particles
cancer dissemination. This path is important only in (CH40) into the rectal submucosa of 19 patients with
inferior tumours that develop under the pectinate line rectal cancer (8 into the intraperitoneal and 11 into the
and already have massive metastases in the lymph nodes extraperitoneal rectum). After surgery
of the main ascending lymphatic stream (51). (abdominoperineal resection or anterior rectal resection
The importance of the medium lymphatic path with total mesorectal and lateral lymph nodes excision),
is still subject to debate. Japanese authors consider four the presence of the carbon particles in the lymph nodes
groups (areas) of rectal lymph vessels (fig. 3b): the was evaluated. In the case of the 8 patients with
mesorectal group (rectal lymph nodes), the superior intraperitoneal rectal tumours, the majority of the axial
rectal artery group (area) and the lateral area (46). The lymph nodes were positive for staining and all of the
mesorectal area is divided into two regions: the lateral lymph nodes were negative.
mesorectum close to the tumour (distal from the tumour In the case of the 11 patients with
and proximal up to 5 cm from the superior edge of the extraperitoneal rectal tumours, most (18-73%) axial
tumour) and the remote mesorectum (over 5 cm from lymph nodes were positive for staining but lateral lymph
the superior edge of the tumour). The area of the inferior nodes were positive as well (9-73%). Kawahara et al
mesenteric artery includes lymph nodes located between (54) used a similar technique, injecting indocyanine
the origin of the artery and the origin of left colic artery; green into the submucosa of 14 patients 30 minutes
distal, the lymph nodes of the superior rectal area are before surgery for rectal cancer. 6 patients had positive
located along the artery. The lateral area is composed of staining in the internal iliac lymph nodes areas. In 4 out
6 lymph node groups: the internal pudendal artery group of these patients lymph node metastases were present.
(lateral to the pelvic plexus), internal iliac artery group Obturator lymph nodes were negative for staining. The
(proximal from the superior vesical artery), the common authors concluded that the first station of lateral
iliac artery group, the external iliac artery group, the lymphatic metastasis path is the internal iliac lymph
obturator group and the sacral group (fig. 3b). nodes area.
The lateral lymphatic drainage is considered Lymphatic scintigram scan studies consider the
minor by European and American authors. First studies lateral lymphatic system of minor importance in rectal
have identified this path by injecting dye into corpses cancer. Sterk et al (55) performed lymphatic scintigram
but they didn't determine its importance. After studying scans on 16 patients one day before surgery for rectal
resection samples, Gilchrist (52) described a case of cancer. 12 patients had exclusively mesorectal positive
extraperitoneal rectal cancer with 2 lateral lymph node lymph nodes. In 4 patients extramesorectal (lateral)
metastases, one of them being located in the lymph positive-staining lymph nodes were found; these lymph
nodes of the ascending stream. This type of nodes were removed during surgery but the pathology
dissemination was found by Grinnell in only 1 out of the examination revealed the absence of metastases.
118 cases he studied, 63 having lymph node metastases. Quadros et al (56) revealed positive scintigram scan
Other authors found as well a very low proportion of lateral lymph nodes in 20% of the patients with rectal
this type of metastasis path. cancer but only in 6,7% of the patients lymph node
Still, the observations of the Japanese authors metastases were present.
suggest that the lateral dissemination might be
important in extraperitoneal rectal cancer. Ueno et al Nerve system of the pelvis
(46) found lymph node metastases in 41 out of 455
(16,8%) patients who underwent various rectal The pelvic nerve system is composed of the
resections of the main tumour together with 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 the male erection. Each inferior hypogastric plexus has a
level of S2, S3 and S4 vertebrae, its fibres innervating rectangular sagittal fenestrated lamina shape. It lies
the pelvic and the genital organs) and the pelvic lateral from the rectum, the prostate, the seminal
autonomic plexuses (the superior and inferior vesicles and the posterior of the urinary bladder in males
hypogastric plexuses). All these plexuses are and lateral from the rectum, the neck of the vagina, the
intertwined. The superior hypogastric plexus is made of fornix of the vagina and the posterior face of the urinary
sympathetic thoracolumbar fibres (responsible for bladder in females (1, 58). The inferior hypogastric
ejaculation). It is located in the extraperitoneal plexus branches provide the innervation for the rectum,
conjunctive tissue, anterior to the aortic bifurcation and the urinary bladder, the prostate, the seminal vesicles, the
the common left iliac vein, at the level of the fifth urethra and the corpa cavernosa. The cavernosa nerves
lumbar vertebra and the promontory (1). The plexus has group into nervous bundles going directly to the
a triangular shape with its top angle pointing cranial; the posterior and lateral surface of the prostate; the bundles'
hypogastric nerves (right and left) originate at its lateral thickness decreases from 12 mm at the origin to 6 mm at
angles (56). The delicate fibromatous network of the the base of the prostate. From this level on, the nerves
areolate tissue provides an avascular plane between the follow the arteries and the veins of the prostate capsule,
hypogastric plexus (posterior) and the mesorectum go upwards to the prostate apex (posterior and lateral to
(anterior). This facilitates the intact dissection of the the urethra) and pass through the urogenital diaphragm.
mesorectum from the plexus. The avascular plane passes Pelvic plexuses are located lateral and posterior to the
between the parietal and the visceral layers of the pelvic seminal vesicles (the middle part of the plexus is located
fascia. The excision of the rectum together with the at the top of the seminal vesicles). This is why the
intact mesorectum is obtained by the surgical separation seminal vesicles are the reference point for the
of these fascial layers along the avascular plane. Each identification of the plexuses during surgery (1, 58).
hypogastric nerve ends in an inferior hypogastric plexus Also, the cavernous nerves can be identified posterior
(right and left). These plexuses are composed of and lateral to the prostate and anterior and lateral to the
sympathetic and parasympathetic fibres originating in rectum as a constant vascular and nerve bundle formed
the S2, S3 and S4 segments on the path of the erigent together with the arteries and the veins of the prostate
nerves. The parasympathetic fibres provide 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)
Journal of Clinical Anatomy and Embryology Vol.INo.4 27

Perirectal fasciae own rectal fascia encloses the rectum, fatty tissue,
nerves, blood vessels and lymph vessels. At this level,
The parietal fascia of the pelvis covers the the fatty tissue is more abundant in the posterior part of
walls and the pelvic diaphragm. It stretches also over the rectum and looks like a "bilobate lipoma" (2, 44).
the pelvic organs, forming the visceral fasciae. Around The pelvic fascia is more evident in the lateral and
the rectum it forms the own rectal sheath, or perirectal posterior parts of the extraperitoneal rectum and thicker
fascia. It was first mentioned by Toma Ionescu in the close to the pelvic diaphragm (44).
anatomy treatise by Poirier and Charpy (17, 57). The

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 The rectogenital septum (rectoprostatic in
pelvic fascia, covering the concavity of the sacrum and males and rectovaginal in females) separates the rectum
the coccyx, also nerves, the medium sacral artery and and the rectal fascia from the seminal vesicles and the
the sacral veins. The posterior sacral (retrosacral) fascia2 prostate, or from the vagina. The strict term of
lies between the presacral fascia and the rectal fascia. It Denonvilliers fascia refers to the rectoprostatic fascia,
is formed by the reflection of the presacral fascia over but it was adopted also for the similar septum of the
the S4 vertebra. It also unites with the rectal fascia 3-5 female.
cm from the ano-rectal ring (38, 44). According to Sato The Dennonvilliers fascia is a fibrous structure
and Sato (45), it holds small veins and nervous branches more evident and consistent than the rectal fascia; it is
from the sacral lymph nodes. more prominent in young patients and it becomes much
2
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.
28 Ovidiu Fabian

thinner with age (59). Urologists describe the fascia as none of the cases bilateral medium rectal arteries were
being attached to the prostate and the seminal vesicles. present, although in 17 of the cases they found a
Colo-rectal surgeons consider it more adherent to the unilateral one; in all of the cases, the artery had a
rectum then to these genital organs (60). From the reduced diameter (never over 2 mm in diameter); in
histology point of view, the fascia is formed of dense none of the cases the fibrous structure of the lateral
collagen fibres, smooth muscles and elastin fibres. The ligaments as described in textbooks was found; only
forming of the Deninvilliers fascia was explained in 2 inconstant fibrous structures and nerve fibres were
ways: by fusion of the 2 membranes of the embryonic found - which cannot be mistaken for the lateral
rectovesical pouch or by compression of the embryonic ligaments. On the other hand and out of caution,
mesenchymal layers. The origin and the forming of the surgeons treat these "dissection artefacts" almost always
Denonvilliers fascia were the source of a surgical with care, seeing them as potential haemorrhage
misunderstanding: the existence of fascial layers sources. This is why the majority of the surgical
separable during surgery (61); handbooks recommend the ligature or electrocautery of
although Richardson3 showed the in these structures. Sato and Sato (42) divide each rectal
existence of two elastin layers in cannot be identified ligament into 2 parts: lateral (containing the medial
the rectogenital septum (59), they The cavernous nerves rectal artery and the pelvic splanechnic nerves) and
during surgical dissection (60). on each side of the medial (containing the hypogastric artery and the
and blood vessels are located vascular and nerves branches of the inferior hypogastric plexus). The 2 parts
Denonvilliers fascia, forming bundles (fig. 8b). are located on each side of the rectangular lamina of the
The lateral ligaments ("the rectal wings") are corresponding inferior hypogastric plexus. In the lateral
described in classic anatomy treatises as fibrous part, the medium rectal artery joins the splanechnic
triangular structures with the base to the lateral pelvic pelvic (erigent) nerves in sharp edge. In the medial part,
wall and the top pointing to the rectum. They include the artery runs parallel to the rectal branches of the
the medium rectal arteries. Their existence is subject to inferior hypogastric plexus (fig. 6). The division
debate because they might be surgical (dissection) proposed by Sato is important for the ligature of the
artefacts. Medium rectal arteries over 1 mm in diameter lateral ligaments: the ligature of the ligament in its
exist inconstantly. When present, they are rarely lateral part is followed by erigent nerve lesions
bilateral. After 28 pelvic dissections, Jones et al. (43), (followed by erectile dysfunctions); medial part ligature
drew several conclusions that contradict classic data: in is practically without urology complications.

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

3
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 29

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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 delimitatǎ de fascia proprie a rectului – aşa-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 ƒi definirea unui parametru pentru evaluarea radicalitatii actului chirurgical (marginea
circumferentiala de rezectie). Cunoasterea anatomiei locale si in special a raporturilor nervoase ƒi 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 During the sixth week of development, a
the embryological intestinal tube: the mouth, mesodermal septum divides the cloaca into an anterior
oesophagus, stomach, duodenum and bile tract originate cavity (the urogenital sinus) and a posterior cavity (the
in die anterior intestine; the small intestine and the colon anal canal). This septum merges in the seventh week
(up to the distal half of the transverse colon) originate in with the cloacal membrane forming the perineal body.
the medium intestine. The descendent colon, the sigma Thus, the cloacal membrane is divided into a urogenital
and the rectum develop from the posterior intestine. Its membrane (the larger anterior part) and an anal
distal segment ends in a pouch (cloaca); the allantois membrane (the smaller posterior part). The anal
opens in the anterior part of this pouch. The pouch is of membrane ends in a depression covered by the ectoderm
endodermic origin and is sealed (closed) by an (anal depression - the origin of the anatomical anal
ectodermic membrane (the cloacal membrane - canal). During the eighth week the anal membrane
proctodeum) (62, 57) (fig. 7). disappears. The location where the anal membrane was
52 Ovidiu Fabian

inserted is called the pectinate line, although there are by branches of the intern iliac artery. The tubercles
no consistent arguments in favour or against its develop on each side of the anal membrane from the
existence (40). Following this development, the rectum somatic mesoderm; these tubercles merge (in
and the superior anal canal are of endodermic origin and "horseshoe" shape) posterior to the rectum and then
their vascularisation is provided by the inferior unite with the perineal body. The external anal sphincter
mesenteric artery; the inferior anal canal (anatomical) is is made of this structure.
of ectodermic origin and its vascularisation is provided

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 53

The primitive (embryological) intestinal tract is Mesorectum


suspended posterior by a primitive mesentery, in which
blood and lymphatic vessels and lymph nodes develop. The mesorectum is not a real mesentery and
At the level of the anterior intestine, this primitive that is why the term must be accepted as a linguistic
mesentery forms the bursa omentalis. At the level of the convention. The term mesorectum defines the adipose
medium intestine, the mesentery of the proximal colon tissue that surrounds the rectum, surrounded by its own
is formed. At the level of the posterior embryological fascia and is the first field of rectal cancer spreading
intestine, the mesentery of the distal colon and the (64)-fig. 8.
mesorectum are formed (63).

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 Ovidiu Fabian

The fascia that circumscribes the rectum offers a small size of the lymph nodes, it is possible (in the
relative avascular dissection plane (a very thin layer of absence of a fat solvent) to see tsome of the rectal
lax tissue located between the parietal and the visceral cancers as being in a lower stage. Referring to this last
layers of the pelvic fascia); respecting this dissection aspect, Andreola etal (67) showed that 45% of the
plane reconciles the oncological imperative of the mesorectal metastasised lymph nodes had less than 5
operation with the genito-urinary function preservation. mm in diameter; 14% of the patients with lymph node
The plane is pathetically called by Heald "the Holy metastases had them only in such small nodes. Wang et
Plane" of surgical dissection (2); Skandalakis proposes al. (68) found lymph nodes smaller than a half
the plane to be called the Heald plane (40). millimetre in 5,8% of the cases; occult lymph node
In what concerns the phylogenetic origin of the metastases were found in 29% of the investigated
mesorectum, an interesting comparative anatomy study patients.
was elaborated by Nano et al (65). By comparing the The imagistic exploration of the mesorectum
observations after the dissection of three animal species can be performed using computed tomography,
(dog, pig and a primate species - Macaca ape) and of intrarectal ultrasound and MRI. Computed tomography
human foetuses, Nano et al concluded that the scan is accurate in evaluating the depth of the tumour's
mesorectum is absent in quadruped mammals, but is invasion into the walls of the rectum, the tumour
present in primates. In primates, perirectal fat is more relations with adjacent organs (especially when the
abundant and is surrounded by a fascia resembling the digital exploration of the rectum raises the suspicion of
perirectal fascia in humans. Similarly, the lateral a proximity invasion of the tumour), as well as the
ligaments are present only in primates and humans. One presence of peritumoral adenopathies. It is also true that
cannot conclude about the evolutive moment of these computed tomography is used for diagnose and
structures' appearance, but it is quite likely that they evaluation of tumour recurrence rather than for the
developed along with the upright walking position. This evaluation of the primary rectal tumour.
was followed by important anatomical and functional Intrarectal ultrasound is used to determine the
modifications (the transformation of a large part of the tumoural invasion of the rectal wall (the mucosa - Tl,
rectum into an extraperitoneal organ, the mechanical the own musculature - T2, the adventitia and the
stress of the rectum in this position, the perirectal fat mesorectal fat - T3, the invasion of adjoining organs -
increased development in order to absorb the T4) as well as the presence and size of peritumoral
mechanical shock waves). The perirectal adipose wrap adenopathies - Nl (69); along with its major advantages
(the mesorectum) reaches the rectal adventitia (64); this (efficiency, non-invasiveness, possibility to repeat it
is not a macroscopically identifiable structure, but it risk free), intrarectal ultrasound accuracy depends on
substitutes the visceral peritoneum in the extraperitoneal the skills and experience of the person performing it
part of the rectum. Posterior, the mesorectum along with (70). It is also true that in common practice intrarectal
perirectal fascia reach the presacral fascia. The posterior ultrasound is the most frequently used method for
face of the mesorectum looks like a "bilobate lipoma", preoperative rectal cancer staging.
due to a median depression (2). Lateral, the presacral MRI seems to be the most sensitive method for
fascia is perforated by several apertures through which the examination of the mesorectum. Fascial planes as
the rectal branches of the inferior hypogastric plexus well as perirectal areas are accurately identified with
and the medium rectal vessels (when present) pass. this method (39) (fig. 9)
Anterior, the mesorectum stretches up to de The mesorectum appears as a structure with
Denonvilliers fascia; actually, the perirectal fascia is high intensity signal. The mesorectal fascia (the own
sometimes mistaken for the so-called "posterior layer" rectal fascia) appears as a straight structure with low
of the Denonvilliers fascia. Inferior, the mesorectum intensity signal. The presacral fascia appears as a
stretches up to the insertion of the levator ani. structure with low signal. The virtual space between the
The distribution of the lymph nodes of the presacral fascia and the rectal fascia is represented by
mesorectum was studied on resection samples and on the retrorectal space. The retrosacral fascia and its
corpses by Topor and Galandiuk (66, 6). After dividing peritoneal reflexion can also be identified by MRI. The
the mesorectum into 4 quadrants (posterior, right lateral, Denonvilliers fascia is shown on MRI scan as a structure
left lateral and anterior) and into 3 parts (corresponding with low signal attached to the recto-vesical recess. The
to the superior, medium and inferior thirds of the lateral ligaments cannot be identified by MRI scanning;
rectum) they concluded: most of the lymph nodes (92%) still, their position is indicated by the medium rectal
are located in the posterior quadrant and in the superior vessels when present. The inferior hypogastric plexuses
2/3 of the mesorectum; the superior third of the rectum can be easily identified on parasagittal sections as
has no mesorectum in the anterior quadrant; most of the rectangular structures of 2-4 cm in length, positioned
lymph nodes are small (0,5-3 mm); considering the 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 can be identified by MRI scanning. The adventitia
mucosa (shown as a fine line with low signal), the cannot be identified, but mesorectal fat (the
submucosa (with high intensity signal) and the muscular mesorectum) is shown as a high intensity structure that
coat as a 2 layer structure (internal layer - regular - encloses the rectum. Lymph nodes are shown as ovoid
corresponding to the circular muscles; external layer - structures with high intensity signal (71).
irregular - corresponding to the longitudinal muscles)

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

Implications of the concept of mesorectum mesorectum appears and the resection becomes
insufficient, with the lateral edge invaded by the
The treatment of rectal cancer has one tumour.
oncological objective (total tumour and lymphatic area Radical resection of the tumoral rectum is
removal) and 2 functional ones (the preservation of the defined by the tumour-free proximal, the distal and the
anal sphincteral function and of the uro-genital lateral (circumferential) edges . The proximal resection
functions). The preservation of the sphincter apparatus edge raises no problems because it is done at the level
depends on the site of the tumour, whereas the total where the vasculature (after the ligature of the superior
removal of the tumour site (rectum and mesorectum) rectal or the inferior mesentery pedicle) assures the
and the prevention of uro-genital sequelae are viability of the tissues. The distal resection depends on
determined by the dissection plane. This plane forms as the tumour site (distance from the pectinate line); the
a result of the embryological development of the rectum initial distance of 5 cm was lowered to 2 cm (4), but a
and mesorectum. diminishing under this limit compromises the radicalism
Heald (2) draws the attention to the dissection of the surgical act. In case of low-sited tumours, proper
in this plane (the cause of local recurrence of the tumour rectum dissection can provide an adequate resection
due to insufficient removal of perirectal tumour edge (Goligher, cited by Yeatman - 4). Still, the
deposits) and also to the dissection outside it (leading to preservation of the sphincter apparatus must not
pelvic nerve plexuses injuries). Another element on compromise the radicalism of the operation.
which Heald insists is that dissection be made sharp, not An important feature of the rectal cancer
blunt, since this latter causes the fibrous adhesions of development is the radial dissemination in the perirectal
the mesorectal fascia to the adjoining structures to tear fat (72). The dissemination can be continuous,
towards the mesorectum or towards these structures; as expansive but also irregular, infiltrative and
a result, the risk of tearing fragments from the 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 adequate, no "cone" shape towards the tumour. In the
resection was studied for the first time as a prognostic case of a dissection performed in the mesorectal plane,
factor and a radical operation parameter by Quirke et al the mesorectum on the resection sample has an irregular
(10). They studied resection samples from 52 patients surface with loss of fatty tissue over 5 mm in depth; the
who underwent surgery for rectal cancer. By performing distal edge of the mesorectum ends in a cone shape. In
transversal sections and morphometric measurements, the third case, the dissection is performed in the
they managed to determine the lateral edge of the muscular plane of the rectum; the mesorectum is thin,
tumour as being the most lateral continuous or with deep defects that go up to the muscular layer; the
discontinuous penetration of the mesorectum. radial edge of resection is irregular with muscular layer
Circumferential invasion was defined as tumoral direct appearing here and there.
infiltration into the resection edge of the sample or as a Pelvic nerves preservation is possible in T1-T3
"safety limit" of less than 1 mm in thickness. According tumoral stages; depending on how this target is met, 4
to this definition, the lateral edge was found to be types of surgical procedures have been described (80-
invaded in 27% of the cases. Their presence - 85% of 81): total preservation of autonomic nerves; unilateral
local tumour recurrence in the case of lateral edge preservation of the autonomic nerves; superior
invasion, as compared to only 3% of tumour-free edges - hypogastric plexus resection and pelvic plexuses
confirmed that insufficient resection is the main cause of preservation; resection of the superior and one of the
local recurrence of the disease. Further studies (73-76) inferior plexuses and preservation of one of the pelvic
had similar results, confirming the importance of lateral plexuses (fig. 11).
resection edge invasion as a prognostic factor. The During surgery, several steps with high risk for
lateral means of invasion (direct, discontinuous, lymph pelvic nerves injuries can be identified: the ligature of
node metastasis, perineural invasion, lymphatic or the inferior mesenteric artery, the posterior dissection,
vascular invasion) has no prognostic significance, but the the lateral dissection and the anterior dissection (59, 82).
invasion itself (76). Some authors (78) consider that the During the ligature of the inferior mesenteric artery
distance between the lateral limit of the tumour and the (especially if this is done at its origin in the aorta), the
resection edge must be minimum 2 mm, whereas others sympathetic fibres of the superior hypogastric plexus are
(76) found no such correlation. vulnerable (59); the lesion of these fibres leads to
For the T1-T3 tumoral stages, Quirke et al (79) retrograde ejaculation. To avoid this complication and
set 3 degrees of rectal resection with mesorectal when no palpable adenopathies along the inferior
excision. When the dissection is performed in the fascial mesenteric artery are present, Phang (83) recommends
plane of the mesorectum, the letter one is thick and that the ligature of the artery is done over or beneath the
smooth (possible defects do not exceed 5 mm in depth), origin of the left colic artery (depending on the segment
without lesions of the fatty tissue; the distal edge is 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 There is agreement regarding the posterior and
located at the level of the posterior dissection plane; lateral dissection plane, but in what concerns the
here, the risk is to injure the hypogastric nerves which anterior dissection plane, opinions diverge. The
have only sympathetic fibres (59, 82). Correct dissection dissection "between" the anterior and posterior layers of
is performed within the lax conjunctive tissue right the Denonvilliers fascia - although mentioned by some
outside the mesorectal fascia. The hypogastric nerves authors - is illusory, because the recto-prostate septum
are located close to the lateral side of this plane. They has in fact no separable layers during surgery (59).
can be easily injured if the plane is not rigorously Lindsey (58) defines 3 planes for the anterior dissection:
followed, if a blunt dissection is performed or if the perirectal, mesorectal and extramesorectal plane (fig.
bleeding is not carefully controlled, which then leads to 12).
poor visibility over the dissection plane. The perirectal plane (perimuscular) - located
The second risk area is at the level of the lateral close to the rectal muscles but within the rectal fascia -is
dissection site. Excessive traction over the rectum brings not an anatomical plane. The mesorectal plane is an
the inferior hypogastric plexus upwards and medial, anatomical one, in which the rectal fascia is separated
exposing it to injuries during the from the Denonvilliers fascia, but not so clear as in the
ligature/electrocauterization of the medium rectal artery lateral and posterior part of the rectum. The extramesorectal
and the corresponding lateral ligament. Extensive lymph plane implies the resection of the Denonvilliers fascia
node excision (including the lymph nodes of the lateral revealing the prostate and the seminal vesicles to the
compartment) recommended by Japanese authors is a anterior plane, but with high risk of injury of the
major risk of injury of these nerves, which at this level cavernous nerves. Because the anterior mesorectum is
include both sympathetic and parasympathetic fibres. thin, and out of oncological reasons, Heald (84) favours
The third major risk area is at the level of systematic dissection anterior to the Denonvilliers fascia.
anterior dissection. The space between the rectum Still, the highest risk of local recurrence is present in
(posterior) and the seminal vesicles and prostate tumours located on the anterior part of the rectum (85).
(anterior) is very narrow. During dissection at this level Thus, the opinion of authors such as Lindsey (86) or
or during haemostasis performed in this difficult area, Flati (87), who recommend that dissection be performed
cavernous nerves are exposed to injuries. These nerves anterior to the Denonvilliers fascia only in anterior
contain especially parasympathetic fibres, their injury cancers, is justified.
leading to impotence.
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 laparoscopic excision of the mesorectum
the lymph nodes of the mesorectal area, but not those of benefits from all the advantages of this type of
the lateral area. The importance of this area in intervention: excellent view, rapid mobilisations of the
extraperitoneal rectal cancers is still subject to debate. patient after surgery, rapid resume of intestinal activity,
Also, the significance of the metastasis' stage in this area of oral food intake and of physical activity, short
is differently interpreted: in the TNM classification, postoperative recovery with the possibility to start
European and American authors integrate these adjuvant therapy early (94-96). Numerous studies have
metastases in category Ml (systemic disease) whereas demonstrated the feasibility of the laparoscopic
Japanese authors integrate them into category N3 procedure (97-100). Still, one must mention that these
(regional dissemination) - a category that doesn't exist in studies have been made on small groups of patients, in
the AJCC classification (81, 88). The Japanese authors specialized departments, with different selection criteria
(42, 46, 53, 89) are in favor of lymph adenectomy, for patients' admittance. All these differences are
which should be extended to the lateral compartment in making the comparison with classic surgery difficult, as
case of extraperitoneal rectal cancers, but this leads to a well as the definition of selection criteria of the patients
high rate of uro-genital sequelae. Analysing a series of who can optimally benefit from this technique (101).
variables and statistically eliminating those irrelevant, The trial conducted and published by Quah (98) shows a
Sugihara et al. (90) conclude that cancers present in surprisingly high rate of sexual and vesical dysfunctions
females, extraperitoneal tumour location, tumour size (4 after the laparoscopic excision of the mesorectum for
cm and over) and the presence of perirectal lymph nodes rectal cancer as compared with the open procedure; this
metastasis are significantly associated with increased is caused by the technically difficult lateral and anterior
incidence of the metastases in the lateral lymph nodes dissection. The laparoscopy technique is an advanced
area. The new techniques of lymph nodes procedure (96). That is why further studies are necessary
micrometastases identification by PCR (Polymerase to determine its role (including the patients' selection
Chain Reaction) (91), as well as those of criteria) in rectal cancer surgery (102).
immunoscintigraphy and radio-immune-guided surgery
(92) will probably contribute to the exact evaluation of Conclusions
this lymphatic path and also to the identification of a
patient subgroup that will benefit from the The mesorectum is an anatomically identifiable
lymphadenectomy of the lateral compartment (93). 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. although technically difficult, is feasible; its oncological
The dissection along the anatomical avascular results are similar to those of open surgery but urinary
mesorectal plane and the total mesorectum excision and genital complications are more frequent.
reconcile the oncological objective (total rectal and The role of extensive pelvic lymphadenectomy
perirectal compartment excision) with the functional (including the radial compartment) is controversial; no
objective (sparing the autonomic innervation). The criteria have yet been established for the identification
degree of mesorectal invasion, but also that of the of the patients who might benefit from these
mesorectal excision, have prognostic value. completions of the standard surgical procedure.
The laparoscopic excision of the mesorectum,

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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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