You are on page 1of 27

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/255744726

Mesorectum. Implications of an Anatomy and Surgical Concept

Article · January 2008

CITATION READS

1 446

4 authors, including:

Ovidiu Vasile Fabian Valentin Muntean


Iuliu Haţieganu University of Medicine and Pharmacy Iuliu Haţieganu University of Medicine and Pharmacy
22 PUBLICATIONS   101 CITATIONS    42 PUBLICATIONS   257 CITATIONS   

SEE PROFILE SEE PROFILE

All content following this page was uploaded by Ovidiu Vasile Fabian on 03 June 2014.

The user has requested enhancement of the downloaded file.


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

References 16. Bissett IP, Hill GL - Extrafascial excision of the


rectum for cancer: A technique for the avoidance of
1. Sinnatamby CS - Anatomical aspects of total the complications of rectal mobilization, Semin
mesorectal excision, The TME Workshop 2003, Surg Oncol 2000, 18:207-215
Pelican Cancer Foundation, http://tycohealth-ece. 17. Giuly J, Nguyen-Cat R, Francois GF - Resection
com/files/dOOO 1 /ty_lcxqto .pdf extrafasciale du rectum ou excision mesorectale
2. Heald RJ - The 'Holy Plane' of rectal surgery, J R totale ? Etude anatomochirurgicale, Annales de
Soc Med 1988, 81:503-508 Chirurgie 2004, 129: 68-72
3. Miles EW - A method of performing abdomino- 18. Heald RJ - The surgical aspects of total mesorectal
perineal excision for carcinoma of the rectum and excision, The TME Workshop 2003, Pelican
of the terminal portion of the pelvic colon, Lancet Cancer Foundation, http://tycohealth-
1908, 2: 1812-1813, republicat in CA Cancer J Clin ece.com/files/d000 1/tyzakwia.pdf
1971;21:361-364 19. Marchal F, Bresler L, Marchal C, Brunaud L,
4. Yeatman TJ, Kirby IB - Sphincter-saving Sebbag H, Guillemin F, Tortuyaux JM, Boissel P,
procedures for distal carcinoma of the rectum, Ann Braun M - Le mesorectum: mise au point et
Surg 1988, 209: 1-18 anatomie d'une erreur semantique, Morphologie
5. Astler VB, Coller FA- The prognostic significance 2000,84(266): 13-18
of direct extension of carcinoma of the colon and 20. Heald RJ, Daniels I - Rectal cancer management:
rectum, Ann Surg 1954, 139: 846-851 Europe is ahead, in Buchler MW, Heald RJ, Ulrich
6. Galandiuk S, Charurvedi K, Topor B - Rectal B, Weitz J- Rectal Cancer Treatment, Springer-
cancer: a compartmental disease. The mesorectum Verlag, Berlin-Heidelberg, 2005 (Recent results in
and mesorectal lymph nodes, in Buchler MW, cancer research 2005, 165: 75-81)
Heald RJ, Ulrich B, Weitz J- Rectal Cancer 21. Zinner MJ, Ashley SW - Maingot's abdominal
Treatment, Springer-Verlag, Berlin-Heidelberg, operations, 11-th Edition, 2006
2005 (Recent results in cancer research 2005, 165: 22. MacFarlane JK, Ryall RDH, Heald RJ -Mesorectal
21-29 excision for rectal cancer, The Lancet 1993,341
7. Heald RJ, Husband EM, Ryall RDH - The (8843): 457-460
mesorectum in rectal cancer surgery—the clue to 23. Kinn AC, Ulf Ohman U - Bladder and Sexual
pelvic recurrence?, Br J Surg, 1982 69: 613-616 Function after Surgery for Rectal Cancer, Dis Col
8. Dixon CF - Surgical removal of lesions occur in the Rect 1996, 29(1): 43-48
sigmoid and rectosigmoid, Am J Surg 1939, 46: 12- 24. Paty PB, Enker WE, Cohen AM, Lauwers GY -
17 Treatment of rectal cancer by low anterior resection
9. Fain N, Patin CS, Morgenstern L - Use of a with coloanal anastomosis, Ann Surg 1994, 219 (4):
mechanical suturing apparatus in low colorectal 365-373
anastomosis, Arch Surg 1975, 110: 1079-1082 25. Arbman G, Nilsson E, Hallbook O, Sjodahl R -
10. Quirke P, M. Dixon F, Durdey P, Williams NS - Local recurrence following total mesorectal
Local recurrence of rectal adenocarcinoma due to excision for rectal cancer, Br J Surg 1996, 83 (3):
inadequate surgical resection. Histopathological 375-379
study of lateral tumor spread and surgical excision, 26. Arenas RB, Fichera A, Mhoon D, Michelassi F -
Lancet 1986, 8514:996-999 Total mezenteric excision in the surgical treatment
11. Fazio V, Fletcher J, Montague D - Prospective of rectal cancer, Arch Surg 1998, 133: 608-612
study of the effect of resection of the rectum on 27. Leo E, Belli F, Andreola S, Gallino G, Bonfanti G,
male sexual function, World J. Surg. 1980, 4: 149- Ferro F, Zingaro E, Sirizzotti G, Civelli E, Valvo F,
151 Gios M, Brunelli C - Total rectal resection and
12. - Beahrs JR, Bearhrs OH, Beahrs MM, Leary FJ - complete mesorectum excision followed by
urinary tract complications with rectal surgery, Ann coloendoanal anastomosis as the optimal treatment
Surg 1978, 187:542-547 for low rectal cancer: The experience of the
13. Gerstenberg TC, Nielsen ML, Clausen S, Blaabjerg National Cancer Institute of Milano, Ann Surg One,
J, Lindenberg J - Bladder function after 7(2): 125-132
abdominoperineal resection of the rectum for 28. Ridgway PF, Darzi AW - The role of total
anorectal cancer, Ann Surg 1980, 191: 81-86 mesorectal excision in the management of rectal
14. Morgado PJ - Total mesorectal excision: a cancer, Cancer Control 2003, 10 (3): 205-211
misnomer for a sound surgical approach, Dis Colon 29. Del Rio C, Sanchez-Santos R, Oreja V, De Oca J,
Rectum 1998; 41: 120-121 Biondo S, Pares D, Osorio A, Marty-Rague J,
15. *** (anonymous) - Breaching the Mesorectum, Jaurrieta E - Long-term urinary dysfunction after
Lancet 1990,335 (8697): 1067 rectal cancer surgery, Colorect Dis 2004, 6: 198-
30 Ovidiu Fabian

202 44. Muntean V- The surgical anatomy of the fasciae


30. Law WL, Chu KW - Anterior resection for rectal and the fascial spaces related to the rectum, Surg
cancer with mesorectal excision, a prospective Radiol Anat 1999, 21:319-324
evaluation of 622 patients, Ann Surg 2004, 240 (2): 45. Sato H, K. Maeda K, Maruta M, Masumori K
260-268 Koide Y - Who can get the beneficial effect from
31. Carlsen, E Schlichting, Guldvog, Johnson, Heald - lateral lymph node dissection for dukes c rectal
Effect of the introduction of total mesorectal carcinoma below the peritoneal reflection?, Dis
excision for the treatment of rectal cancer, Br J Colon Rectum 2006, 49(Suppl 10):S3-12
Surg 1998, 85 (4): 526-529. 46. Ueno H, Mochizuki H, Hashiguchi Y, Ishiguro M,
32. Wibe A, Mfoller B, Norstein J, Carlsen E, Wiig JN, Miyoshi M, Kajiwara Y, Sato T, Shimazaki H,
Heald RJ, Langmark F, Myrvold HE, Soreide O - A Hase K - Potential Prognostic Benefit of Lateral
national strategic change in treatment policy for Pelvic Node Dissection for Rectal Cancer Located
rectal cancer - implementation of total mesorectal Below the Peritoneal Reflection, Ann Surg 2007,
excision as routine treatment in Norway. A 245: 80-87
National audit, Dis Colon Rectum 2002, 45 (7): 47. - Lateral ligament: Its anatomy and clinical
857-866 importance, Semin. Surg. Oncol. 2000, 19:386-395,
33. Wibe A, Eriksen MT, Syse A, Myrvold HE - Total 2000
mesorectal excision for rectal cancer - what can be 48. Takahashi T, Ueno M, Azekura K, Ohta H - Lateral
achieved by a national audit?, Colorect Dis 2003, 5 node dissection and total mesorectal excision for
(5): 471-477 rectal cancer, Dis Colon Rectum 2000, 43 (Suppl.
34. Goldberg S, Klas JV - Total mesorectal excision in 10): S59-S68
the treatment of rectal cancer: a view from the 49. Testut L - Traite d'anatomie humane, tome
USA, Semin Surg Oncol 1998, 15(2): 87-90 quatrieme Appareil de la digestion, Huitieme
35. Wiig JN, Carlsen E, Soreide O - Mesorectal edition (revue par A Latarjet), Gaston Doin, Paris,
excision for rectal cancer: A view from Europe, 1931
Semin Surg Oncol 1998, 15 (2): 78-86 50. Curti G, Maurer CA, Buchler MW - Colorectal
36. Bernardshawa SV, Ovrebob K, Eidec GE, carcinoma: is lymphadenectomy useful?, Dig Surg
Skarsteinb A, Rtfkked O - Treatment of rectal 1998; 15:193-208
cancer: reduction of local recurrence after the 51. Grinnell RS - The lymphatic and venous spread of
introduction of TME - Experience from one carcinoma of the rectum, Ann Surg 1942, 116(2):
university hospital, Dig Surg 2006, (1-2): 51-59 200-216
37. Soreide O, Norstein J - Local recurrence after 52. Gilchrist RK, David VC - Lymphatic spread of
operative treatment of rectal carcinoma: a strategy carcinoma of the rectum, Ann Surg 1938, 108(4):
for change, J Am Col Surg 1997, 184: 84-92 621-642
38. Marcio J, Jorge N, Habr-Gama A - Anatomy and 53. Maeda K, Maruta M, Utsumi T, Hosoda Y, Horibe
embryology of the colon, rectum, and anus, in Y - Does perifascial rectal excision (i.e. TME)
Wolff BG, Fleshman JW, Beck DE, Pemberton JH, when combined with the autonomic nerve-sparing
Wexner SD - The ASCRS textbook of colon and technique interfere with operative radicality?,
rectal surgery, Springer, New-York, 2007 - cpt. 1 Colorect Dis 2004, 4(4): 233-239
39. Salerno G, Sinnatamby C, Branagan G, Daniels IR, 54. Kawahara H, Nimura H, Watanabe K, Kobayashi T,
Heald RJ, Moran BJ - Defining the rectum: Kashiwagi H, YanagaK - Where does the first
surgically, radiologically and anatomically, lateral pelvic lymph node receive drainage from?,
Colorect Dis 2006, 8 (Suppl. 3), 5-9 Dig Surg 2007; 24: 413-417
40. Skandalakis JE - Surgical anatomy: the 55. Sterk P, Keller L, Jochims H, Klein P, Stelzner F,
embryologic and anatomic basis of modern surgery, Bruch HP, Marker U - Lymphoscintigraphy in
McGraw-Hill Professional Publishing, 2004, cpt. 18 patients with primary rectal cancer: the role of total
- Large intestine and anorectum mesorectal excision for primary rectal cancer - a
41. Mandache F, ChiricuJ)a I - Chirurgia rectului, Ed. lymphoscintigraphic study, Int J Colorectal Dis
Medicala, Bucure°ti 1957 2002, 17:137-142
42. Sato T, Sato K - The vascular and neuronal 56. Quadros CA, Lopes A, Araujo I, Fahel F, Bacellar
composition of the lateral ligament of the rectum MS, Dias CS - Retroperitoneal and lateral pelvic
and the rectosacral fascia, Surg Radiol Anat 1991, lymphadenectomy mapped by lymphoscintigraphy
13: 17-22 and blue dye for rectal adenocarcinoma staging:
43. Jones OM, Smeulers N, Wiseman O, Miller R - preliminary results, Ann Surg Oncol 2006,
Lateral ligaments of the rectum: an anatomical 13(12):1617-1621
study, Br J Surg 1999, 86: 487-489 57. Faucheron JL - Pelvic anatomy for colorectal
Journal of Clinical Anatomy and Embryology Vol.1 No. 4 31

surgeons, Acta Chir Belg 2005, 105:471-474 results in cancer research 2005, 165: 30-439
58. Walsh PC, Schlegel PN - Radical pelvic surgery 73. Shepherd NA, Baxter KJ, Love SB - Influence of
with preservation of sexual function, Ann Surg local peritoneal involvement on pelvic recurrence
1988, 208(4): 391-400 and prognosis in rectal cancer, J Clin Pathol 1995,
59. Lindsey I, Guy RG, Warren BF, Moretensen NJ - 48:849-855
Anatomy of Denonvilliers' fascia and pelvic nerves, 74. de Haas-Kock DFM, Baeten CGMI, Jager JJ,
impotence and implications for the colorectal Langendijk JA, Schoutent LJ, Volovicss A,
surgeon, Br J Surg 2000, 87:1288-1299 Arendsd JW - Prognostic significance of radial
60. van Ophoven A, Roth S - The anatomy and margins of clearance in rectal cancer, Br J Surg
embryological origins of the fascia of Denovilliers: 1996,83:781-785
a medico-historical debate, J Urol 1997, 157: 3-9 75. Marks CG, Lewis CE, Jackson PA, Cook MG -
61. Secin FP, Karanikolas N, Gopalan A, Bianco FJ, What determines the outcome after total mesorectal
Shayegan B, Touijer K, Olgac S, Myers RP, excision for rectal carcinoma - 15 years experience
Dalbagni G, Guillonneau B - The anterior layer of of a specialist surgical unit, Colorectal Disease
Denonvilliers' fascia, a common misconception in 2000, 2: 270-276
the laparoscopic prostatectomy literature, J Urol 76. Birbeck KF, Macklin CP, Tiffin NJ, Parsons W,
2007, 177: 521-525 Dixon MF, Mapstone NP, Abbott CR, Scott N,
62. Sadler TW - Lagman's medical embryology, 10 Finan PJ, Johnston D, Quirke P - Rates of
edition, Lippincott Williams & Wilkins, 2006 circumferential resection margin involvement vary
63. Heald RJ, Moran BJ- Embryology and anatomy of between surgeons and predict outcomes in rectal
the rectum, Semin Surg Oncol 1998, 15(2):66-71 cancer surgery, Ann Surg 2002, 235 (4): 449^57
64. Diop M, Parratte B, Tatu L, Vuillier F, Brunelle S, 77. Nagtegaal ID, van de Velde CJH, van der Worp E,
Monnier G - Mesorectum: the surgical value of an Kapiteijn E, Quirke P, van Krieken JHJM -
anatomical approach, Surg Radiol Anat 2003, 25: Macroscopic evaluation of rectal cancer resection
290-304 specimen: clinical significance of the pathologist in
65. Nano M, Prunotto M, Ferronato M, Solej M, quality control, J Clin Oncol 2002, 20(7): 1729-
Galloni M - The mesorectum: hypothesis on its 1734
evolution, Tech Coloproctol 2006, 10:323-328 78. Nagtegaal ID, Marijnen CAM, Klein Kranenbarg E,
66. Topor B, Acland R, Kolodko V, Galandiuk S - van de Velde CJH, van Krieken JHJM -
Mesorectal lymph nodes: their location and Circumferential margin involvement is still an
distribution within the mesorectum, Dis Colon important predictor of local recurrence in rectal
Rectum 2003, 46:779-785 carcinoma. Not one millimeter but two millimeters
67. Andreola S, Leo E, Belli F, Gallino G, Sirizzotti G, is the limit, Am J Surg Pathol 2002, 26(3): 350-357
Sampietro G - Adenocarcinoma of the lower third 79. Quirke P, Morris E - Reporting colorectal cancer,
of the rectum, Ann Surg Oncol 2000, 8(5):413-417 Histopathology 2007, 50: 103-112
68. Wang C, Zhou ZG, Wang Z, Chen DY, Zheng YC, 80. Moriya Y, Sugihara K, Akasu T, Fujita S - Nerve-
Zhao GP - Nodal spread and micrometastasis sparing surgery with lateral node dissection for
within mesorectum, World J Gastroenterol 2005, advanced lower rectal cancer, Eur J Cancer 1995,
ll(23):3586-3590 31A (7/8). 1229-1232
69. Badea G, Badea R, Valeanu A, Mircea P, Dudea S - 81. Yano H, Moran BJ - The incidence of lateral pelvic
Ecografie gastrointestinala, in Bazele ecografiei side-wall nodal involvement in low rectal cancer
clinice, Ed. Medicala 1995, cap. 15 may be similar in Japan and the West, Br J Surg
70. Cazacu M, Simon I, Badea R, Petrica A, 2008;95:33-49
Constantinescu D, Rednic N, Galatar N - Pre- 82. Keighley MRB, Williams NS - Surgery of the anus,
treatment staging of colorectal cancer. The value of rectum and colon, W. B. Saunders Company,
endosonography, RJGE 1998, 4 London-Philadelphia-Toronto-Sydney-Tokyo 1999,
71. Brown G, Kirkham A, Williams GT, Bourne M, cpt. 11 - Impaired sexual function after rectal
Radcliffe AG, Sayman J, Newell R, Sinnatamby C, surgery
Heald RJ - High resolution MRI of the anatomy 83. Phang TI - Total mesorectal excision: technical
important in total mesorectal excision of the rectum, aspects, Can J Surg 2004, 47(2): 130-137
AJR 2004, 182:431-439 84. Heald RJ, Moran BJ, Brown G, Daniels IR -
72. Autschbach F - The pathological assessment of total Optimal total mesorectal excision for rectal cancer
mesorectal excision: what are the relevant resection is by dissection in front of Denonvilliers' fascia, Br
margins?, in Biichler MW, Heald RJ, J Surg 2004,91: 121-123
- Ulrich B, Weitz J- Rectal cancer treatment, 85. Chan CLH, Bokey EL, Chapuis PH, Renwick AA,
Springer-Verlag, Berlin-Heidelberg, 2005 (Recent Dent OF - Local recurrence after curative resection
32 Ovidiu Fabian

for rectal cancer is associated with anterior position mesorectum excision, JSLS 2002, 6: 163-167
of the tumour, Br J Surg 2006; 93: 105-112 95. Morino M, Giraudo G - Laparoscopic total
86. Lindsey I, Warren B, Mortensen N - Optimal total mesorectal excision - The Turin experience, in
mesorectal excision for rectal cancer is by Buchler MW, Heald RJ, Ulrich B, Weitz J- Rectal
dissection in front of Denonvilliers' fascia, Br J cancer treatment, Springer-Verlag, Berlin-
Surg 2004, 91: 897 Heidelberg, 2005 (Recent results in cancer research
87. Flati G, Porowska B, Procacciante F - Optimal total 2005, 165: 167-179)
mesorectal excision for rectal cancer is by 96. Copaescu C - Excizia totala a mezorectului prin
dissection in front of Denonvilliers' fascia, Br J abord laparoscopic, Chirurgia 2008, 103(1): 87-94
Surg 2004, 91: 1202-1203 97. Leo E, Belli F, Andreola S, Gallino G, Bonfanti G,
88. Greene FL, Compton CC, Fritz AG, Shah JP, Ferro F, Zingaro E, Sirizzotti G, Civelli E, Valvo F,
Winchester DP - AJCC Cancer staging atlas, Gios M, Brunelli C - Total rectal resection and
Springer 2006 complete mesorectum excision followed by
89. Matsumoto T, Ohue M, Sekimoto M, Yamamoto coloendoanal anastomosis as the optimal treatment
H, Ikeda M, Monden M - Feasibility of autonomic for low rectal cancer: The experience of the
nerve-preserving surgery for advanced rectal cancer National Cancer Institute of Milano, Ann Surg
based on analysis of micrometastases, Br J Surg Oncol 2000, 7(2): 125-132
2005, 92: 1444-1448 98. Quah HM, Jayne DG, Eu KW, Seow-Choen F -
90. Sugihara K, Kobayashi H, Kato T, Mori T, Bladder and sexual dysfunction following
Mochizuki H, Kameoka S, Shirouzu K, Muto T - laparoscopically assisted and conventional open
Indication and benefit of pelvic sidewall dissection mesorectal resection for cancer, Br J Surg 2002, 89:
for rectal cancer, Dis Colon Rectum 2006; 49: 1551-1556
1663-1672 99. Polliand C, Barrat C, Champault G - Laparoscopic
91. Mori M, Mimori K, Inoue H, Barnard GF, Tsuji K, resection of low rectal cancer with a mean follow-
Nanbara S, Ueo H, Akiyoshi T - Detection of up of seven years, Surg Laparosc Endosc Percutan
Cancer Micrometastases in Lymph Nodes by Tech 2005, 15:144-148
Reverse Transcriptase-Polymerase Chain Reaction, lOO.Kienle P, Weitz J, Koch M, Buchler MW -
Cancer Res 1995, 55: 3417-3420 Laparoscopic surgery for colorectal cancer,
92. Hladik P, Vizda J, Bedrna J, Simkovic D, Strnada Colorect Dis 2006, 8 (Suppl. 3), 33-36
L, Smejkal K, Voboril Z - Immunoscintigraphy and lOl.Gohl J, Merkel S, Hohenberger W -
intra-operative radio immunodetection in the LaparoscopicTME -The surgeon's or the patient's
treatment of colorectal carcinoma, Colorect Dis preference, in Buchler MW, Heald RJ, Ulrich B,
2001,3:380-386 Weitz J - Rectal cancer treatment, Springer-Verlag,
93. Koch M, Kienle P, Antolovic D, Buchler MW, Berlin-Heidelberg, 2005 (Recent results in cancer
Weitz J - Is the lateral lymph node compartment research 2005, 165: 158-166)
relevant?, in Buchler MW, Heald RJ, Ulrich B, 102.Schiedeck THK, Fischer F, Gondeck C, Roblick
Weitz J- Rectal cancer treatment, Springer-Verlag, UJ, Bruch HP - Laparoscopic TME: better vision,
Berlin-Heidelberg, 2005 (Recent results in cancer better results?, in Buchler MW, Heald RJ, Ulrich B,
research 2005, 165:40-45) Weitz J - Rectal Cancer Treatment, Springer-
94. Reis Neto JA, Quilici FA, Cordeiro F, Reis JA Jr., Verlag, Berlin-Heidelberg, 2005 (Recent results in
Kagohara O, Neto S, - Laparoscopic total cancer research 2005, 165: 148-157)

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,

References urinary tract complications with rectal surgery, Ann


Surg 1978, 187:542-547
1. l.Sinnatamby CS - Anatomical aspects of total 13. Gerstenberg TC, Nielsen ML, Clausen S, Blaabj erg
mesorectal excision, The TME Workshop 2003, J, Lindenberg J - Bladder function after
Pelican Cancer Foundation, http://tycohealth- abdominoperineal resection of the rectum for
ece.com/files/d000 l/tylcxqto.pdf anorectal cancer, Ann Surg 1980, 191: 81-86
2. Heald RJ - The 'Holy Plane' of rectal surgery, J R 14. Morgado PJ - Total mesorectal excision: a
Soc Med 1988, 81:503-508 misnomer for a sound surgical approach, Dis Colon
3. Miles EW - A method of performing abdomino- Rectum 1998; 41: 120-121
perineal excision for carcinoma of the rectum and 15. *** (anonymous) - Breaching the Mesorectum,
of the terminal portion of the pelvic colon, Lancet Lancet 1990, 335 (8697): 1067
1908, 2: 1812-1813, republicat in CA Cancer J Clin 16. Bissett IP, Hill GL - Extrafascial excision of the
1971;21:361-364 rectum for cancer: A technique for the avoidance of
4. Yeatman TJ, Kirby IB - Sphincter-saving the complications of rectal mobilization, Semin
procedures for distal carcinoma of the rectum, Ann Surg Oncol 2000, 18:207-215
Surg 1988, 209: 1-18 17. Giuly J, Nguyen-Cat R, Francois GF - Resection
5. Astler VB, Coller FA- The prognostic significance extrafasciale du rectum ou excision mesorectale
of direct extension of carcinoma of the colon and totale ? Etude anatomochirurgicale, Annales de
rectum, Ann Surg 1954, 139: 846-851 Chirurgie 2004, 129: 68-72
6. Galandiuk S, Chaturvedi K, Topor B - Rectal 18. Heald RJ - The surgical aspects of total mesorectal
cancer: a compartmental disease. The mesorectum excision, The TME Workshop 2003, Pelican
and mesorectal lymph nodes, in Biichler MW, Cancer Foundation, http://tycohealth-
Heald RJ, Ulrich B, Weitz J- Rectal Cancer ece.com/files/d0001/ty_zakwia.pdf
Treatment, Springer-Verlag, Berlin-Heidelberg, 19. Marchal F, Bresler L, Marchal C, Brunaud L,
2005 (Recent results in cancer research 2005, 165: Sebbag H, Guillemin F, Tortuyaux JM, Boissel P,
21-29 Braun M - Le mesorectum: mise au point et
7. Heald RJ, Husband EM, Ryall RDH - The anatomie d'une erreur semantique, Morphologie
mesorectum in rectal cancer surgery—the clue to 2000,84(266): 13-18
pelvic recurrence?, Br J Surg, 1982 69: 613-616 20. Heald RJ, Daniels I - Rectal cancer management:
8. Dixon CF - Surgical removal of lesions occur in the Europe is ahead, in Biichler MW, Heald RJ, Ulrich
sigmoid and rectosigmoid, Am J Surg 1939, 46: 12- B, Weitz J- Rectal Cancer Treatment, Springer-
17 Verlag, Berlin-Heidelberg, 2005 (Recent results in
9. Fain N, Patin CS, Morgenstern L - Use of a cancer research 2005, 165: 75-81)
mechanical suturing apparatus in low colorectal 21. Zinner MJ, Ashley SW - Maingot's abdominal
anastomosis, Arch Surg 1975, 110: 1079-1082 operations, 11-th Edition, 2006
10. Quirke P, M. Dixon F, Durdey P, Williams NS - 22. MacFarlane JK, Ryall RDH, Heald RJ -Mesorectal
Local recurrence of rectal adenocarcinoma due to excision for rectal cancer, The Lancet 1993, 341
inadequate surgical resection. Histopathological (8843): 457-460
study of lateral tumor spread and surgical excision, 23. Kinn AC, Ulf Ohman U - Bladder and Sexual
Lancet 1986, 8514:996-999 Function after Surgery for Rectal Cancer, Dis Col
11. Fazio V, Fletcher J, Montague D - Prospective Rect 1996, 29 (1): 43-48
study of the effect of resection of the rectum on 24. Paty PB, Enker WE, Cohen AM, Lauwers GY -
male sexual function, World J. Surg. 1980, 4: 149- Treatment of rectal cancer by low anterior resection
151 with coloanal anastomosis, Ann Surg 1994, 219 (4):
12. - Beahrs JR, Bearhrs OH, Beahrs MM, Leary FJ - 365-373
60 Ovidiu Fabian

25. Arbman G, Nilsson E, Hallbook O, Sjodahl R - 38. Marcio J, Jorge N, Habr-Gama A - Anatomy and
Local recurrence following total mesorectal embryology of the colon, rectum, and anus, in
excision for rectal cancer, Br J Surg 1996, 83 (3): Wolff BG, Fleshman JW, Beck DE, Pemberton JH,
375-379 Wexner SD - The ASCRS textbook of colon and
26. Arenas RB, Fichera A, Mhoon D, Michelassi F - rectal surgery, Springer, New-York, 2007 - cpt. 1
Total mezenteric excision in the surgical treatment 39. Salerno G, Sinnatamby C, Branagan G, Daniels IR,
of rectal cancer, Arch Surg 1998, 133: 608-612 Heald RJ, Moran BJ - Defining the rectum:
27. Leo E, Belli F, Andreola S, Gallino G, Bonfanti G, surgically, radiologically and anatomically,
Ferro F, Zingaro E, Sirizzotti G, Civelli E, Valvo F, Colorect Dis 2006, 8 (Suppl. 3), 5-9
Gios M, Brunelli C - Total rectal resection and 40. Skandalakis JE - Surgical anatomy: the
complete mesorectum excision followed by embryologic and anatomic basis of modern surgery,
coloendoanal anastomosis as the optimal treatment McGraw-Hill Professional Publishing, 2004, cpt.
for low rectal cancer: The experience of the 18 - Large intestine and anorectum
National Cancer Institute of Milano, Ann Surg One, 41. Mandache F, ChiricuJ>a I - Chirurgia rectului, Ed.
7(2): 125-132 Medicala, Bucure°ti 1957
28. Ridgway PF, Darzi AW - The role of total 42. Sato T, Sato K - The vascular and neuronal
mesorectal excision in the management of rectal composition of the lateral ligament of the rectum
cancer, Cancer Control 2003, 10 (3): 205-211 and the rectosacral fascia, Surg Radiol Anat 1991,
29. Del Rio C, Sanchez-Santos R, Oreja V, De Oca J, 13: 17-22
Biondo S, Pares D, Osorio A, Marty-Rague J, 43. Jones OM, Smeulers N, Wiseman O, Miller R -
Jaurrieta E - Long-term urinary dysfunction after Lateral ligaments of the rectum: an anatomical
rectal cancer surgery, Colorect Dis 2004, 6: 198- study, Br J Surg 1999, 86: 487-489
202 44. Muntean V- The surgical anatomy of the fasciae
30. Law WL, Chu KW - Anterior resection for rectal and the fascial spaces related to the rectum, Surg
cancer with mesorectal excision, a prospective Radiol Anat 1999, 21:319-324
evaluation of 622 patients, Ann Surg 2004, 240 (2): 45. Sato H, K. Maeda K, Maruta M, Masumori K Koide
260-268 Y - Who can get the beneficial effect from lateral
31. Carlsen, E Schlichting, Guldvog, Johnson, Heald - lymph node dissection for dukes c rectal carcinoma
Effect of the introduction of total mesorectal below the peritoneal reflection?, Dis Colon Rectum
excision for the treatment of rectal cancer, Br J Surg 2006, 49(Suppl 10):S3-12
1998, 85 (4): 526-529. 46. Ueno H, Mochizuki H, Hashiguchi Y, Ishiguro M,
32. Wibe A, IVMler B, Norstein J, Carlsen E, Wiig JN, Miyoshi M, Kajiwara Y, Sato T, Shimazaki H, Hase
Heald RJ, Langmark F, Myrvold HE, S0reide O - A K - Potential Prognostic Benefit of Lateral Pelvic
national strategic change in treatment policy for Node Dissection for Rectal Cancer Located Below
rectal cancer - implementation of total mesorectal the Peritoneal Reflection, Ann Surg 2007, 245: 80-
excision as routine treatment in Norway. A National 87
audit, Dis Colon Rectum 2002, 45 (7): 857-866 47. - Lateral ligament: Its anatomy and clinical
33. Wibe A, Eriksen MT, Syse A, Myrvold HE - Total importance, Semin. Surg. Oncol. 2000, 19:386-395,
mesorectal excision for rectal cancer - what can be 2000
achieved by a national audit?, Colorect Dis 2003, 5 48. Takahashi T, Ueno M, Azekura K, Ohta H - Lateral
(5): 471-477 node dissection and total mesorectal excision for
34. Goldberg S, Klas JV - Total mesorectal excision in rectal cancer, Dis Colon Rectum 2000, 43 (Suppl.
the treatment of rectal cancer: a view from the 10): S59-S68
USA, Semin Surg Oncol 1998, 15(2): 87-90 49. Testut L - Traite d'anatomie humane, tome
35. Wiig JN, Carlsen E, S0reide O - Mesorectal quatrieme Appareil de la digestion, Huitieme
excision for rectal cancer: A view from Europe, edition (revue par A Latarjet), Gaston Doin, Paris,
Semin Surg Oncol 1998, 15 (2): 78-86 1931
36. Bernardshawa SV, Ovrebob K, Eidec GE, 50. Curti G, Maurer CA, Biichler MW - Colorectal
Skarsteinb A, Rakked O - Treatment of rectal carcinoma: is lymphadenectomy useful?, Dig Surg
cancer: reduction of local recurrence after the 1998; 15:193-208
introduction of TME - Experience from one 51. Grinnell RS - The lymphatic and venous spread of
university hospital, Dig Surg 2006, (1-2): 51-59 carcinoma of the rectum, Ann Surg 1942, 116(2):
37. S0reide O, Norstein J - Local recurrence after 200-216
operative treatment of rectal carcinoma: a strategy 52. Gilchrist RK, David VC - Lymphatic spread of
for change, J Am Col Surg 1997, 184: 84-92 carcinoma of the rectum, Ann Surg 1938, 108(4):
621-642
Journal of Clinical Anatomy and Embryology Vol.1 No. 5 61

53. Maeda K, Maruta M, Utsumi T, Hosoda Y, Horibe of the rectum, Ann Surg Oncol 2000, 8(5):413-417
Y - Does perifascial rectal excision (i.e. TME) 68. Wang C, Zhou ZG, Wang Z, Chen DY, Zheng YC,
when combined with the autonomic nerve-sparing Zhao GP - Nodal spread and micrometastasis
technique interfere with operative radicality?, within mesorectum, World J Gastroenterol 2005,
Colorect Dis 2004, 4(4): 233-239 ll(23):3586-3590
54. Kawahara H, Nimura H, Watanabe K, Kobayashi 69. Badea G, Badea R, Valeanu A, Mircea P, Dudea S
T, Kashiwagi H, YanagaK - Where does the first - Ecografie gastrointestinala, in Bazele ecografiei
lateral pelvic lymph node receive drainage from?, clinice, Ed. Medicala 1995, cap. 15
Dig Surg 2007; 24: 413-417 70. Cazacu M, aimon I, Badea R, Petrica A,
55. Sterk P, Keller L, Jochims H, Klein P, Stelzner F, Constantinescu D, Rednic N, Galatar N - Pre-
Bruch HP, Marker U - Lymphoscintigraphy in treatment staging of colorectal cancer. The value of
patients with primary rectal cancer: the role of total endosonography, RJGE 1998, 4
mesorectal excision for primary rectal cancer - a 71. Brown G, Kirkham A, Williams GT, Bourne M,
lymphoscintigraphy study, Int J Colorectal Dis Radcliffe AG, Sayman J, Newell R, Sinnatamby C,
2002, 17:137-142 Heald RJ - High resolution MRJ of the anatomy
56. Quadros CA, Lopes A, Araujo I, Fahel F, Bacellar important in total mesorectal excision of the
MS, Dias CS - Retroperitoneal and lateral pelvic rectum, AJR 2004, 182:431-439
lymphadenectomy mapped by lymphoscintigraphy 72. Autschbach F - The pathological assessment of total
and blue dye for rectal adenocarcinoma staging: mesorectal excision: what are the relevant resection
preliminary results, Ann Surg Oncol 2006, margins?, in Biichler MW, Heald RJ, Ulrich B,
13(12):1617-1621 Weitz J- Rectal cancer treatment, Springer-Verlag,
57. Faucheron JL - Pelvic anatomy for colorectal Berlin-Heidelberg, 2005 (Recent results in cancer
surgeons, Acta Chir Belg 2005, 105:471-474 research 2005, 165: 30-439
58. Walsh PC, Schlegel PN - Radical pelvic surgery 73. Shepherd NA, Baxter KJ, Love SB - Influence of
with preservation of sexual function, Ann Surg local peritoneal involvement on pelvic recurrence
1988, 208(4): 391-400 and prognosis in rectal cancer, J Clin Pathol 1995,
59. Lindsey I, Guy RG, Warren BF, Moretensen NJ - 48:849-855
Anatomy of Denonvilliers' fascia and pelvic nerves, 74. de Haas-Kock DFM, Baeten CGMI, Jager JJ,
impotence and implications for the colorectal Langendijk JA, Schoutent LJ, Volovicss A, Arendsd
surgeon, Br J Surg 2000, 87:1288-1299 JW - Prognostic significance of radial margins of
60. van Ophoven A, Roth S - The anatomy and clearance in rectal cancer, Br J Surg 1996,83:781-
embryological origins of the fascia of Denovilliers: 785
a medico-historical debate, J Urol 1997, 157: 3-9 75. Marks CG, Lewis CE, Jackson PA, Cook MG -
61. Secin FP, Karanikolas N, Gopalan A, Bianco FJ, What determines the outcome after total mesorectal
Shayegan B, Touijer K, Olgac S, Myers RP, excision for rectal carcinoma - 15 years experience
Dalbagni G, Guillonneau B - The anterior layer of of a specialist surgical unit, Colorectal Disease
Denonvilliers' fascia, a common misconception in 2000, 2: 270-276
the laparoscopic prostatectomy literature, J Urol 76. Birbeck KF, Macklin CP, Tiffin NJ, Parsons W,
2007, 177: 521-525 Dixon MF, Mapstone NP, Abbott CR, Scott N,
62. Sadler TW - Lagman's medical embryology, 10 Finan PJ, Johnston D, Quirke P - Rates of
edition, Lippincott Williams & Wilkins, 2006 circumferential resection margin involvement vary
63. Heald RJ, Moran BJ- Embryology and anatomy of between surgeons and predict outcomes in rectal
the rectum, Semin Surg Oncol 1998, 15(2):66-71 cancer surgery, Ann Surg 2002, 235 (4): 449-457
64. Diop M, Parratte B, Tatu L, Vuillier F, Brunelle S, 77. Nagtegaal ID, van de Velde CJH, van der Worp E,
Monnier G - Mesorectum: the surgical value of an Kapiteijn E, Quirke P, van Krieken JHJM -
anatomical approach, Surg Radiol Anat 2003, 25: Macroscopic evaluation of rectal cancer resection
290-304 specimen: clinical significance of the pathologist in
65. Nano M, Prunotto M, Ferronato M, Solej M, quality control, J Clin Oncol 2002, 20(7): 1729-
Galloni M - The mesorectum: hypothesis on its 1734
evolution, Tech Coloproctol 2006, 10:323-328 78. Nagtegaal ID, Marijnen CAM, Klein Kranenbarg E,
66. Topor B, Acland R, Kolodko V, Galandiuk S - van de Velde CJH, van Krieken JHJM -
Mesorectal lymph nodes: their location and Circumferential margin involvement is still an
distribution within the mesorectum, Dis Colon important predictor of local recurrence in rectal
Rectum 2003, 46:779-785 carcinoma. Not one millimeter but two millimeters
67. Andreola S, Leo E, Belli F, Gallino G, Sirizzotti G, is the limit, Am J Surg Pathol 2002, 26(3): 350-357
Sampietro G - Adenocarcinoma of the lower third 79. Quirke P, Morris E - Reporting colorectal cancer,
62 Ovidiu Fabian

Histopathology 2007, 50: 103-112 and intra-operative radioimmunodetection in the


80. Moriya Y, Sugihara K, Akasu T, Fujita S - Nerve- treatment of colorectal carcinoma, Colorect Dis
sparing surgery with lateral node dissection for 2001,3:380-386
advanced lower rectal cancer, Eur J Cancer 1995, 93. Koch M, Kienle P, Antolovic D, Biichler MW,
31A (7/8). 1229-1232 Weitz J - Is the lateral lymph node compartment
81. Yano H, Moran BJ - The incidence of lateral pelvic relevant?, in Biichler MW, Heald RJ, Ulrich B,
side-wall nodal involvement in low rectal cancer Weitz J- Rectal cancer treatment, Springer-Verlag,
may be similar in Japan and the West, Br J Surg Berlin-Heidelberg, 2005 (Recent results in cancer
2008; 95: 33-49 research 2005,165:40-45)
82. Keighley MRB, Williams NS - Surgery of the anus, 94. Reis Neto JA, Quilici FA, Cordeiro F, Reis JA Jr.,
rectum and colon, W. B. Saunders Company, Kagohara O, Neto S, - Laparoscopic total
London-Philadelphia-Toronto-Sydney-Tokyo 1999, mesorectum excision, JSLS 2002, 6: 163-167
cpt. 11 - Impaired sexual function after rectal 95. Morino M, Giraudo G - Laparoscopic total
surgery mesorectal excision - The Turin experience, in
83. Phang TI - Total mesorectal excision: technical Biichler MW, Heald RJ, Ulrich B, Weitz J- Rectal
aspects, Can J Surg 2004, 47(2): 130-137 cancer treatment, Springer-Verlag, Berlin-
84. Heald RJ, Moran BJ, Brown G, Daniels IR - Heidelberg, 2005 (Recent results in cancer research
Optimal total mesorectal excision for rectal cancer 2005, 165: 167-179)
is by dissection in front of Denonvilliers' fascia, Br 96. Copaescu C - Excizia totala a mezorectului prin
J Surg 2004, 91: 121-123 abord laparoscopic, Chirurgia 2008, 103(1): 87-94
85. Chan CLH, Bokey EL, Chapuis PH, Renwick AA, 97. Leo E, Belli F, Andreola S, Gallino G, Bonfanti G,
Dent OF - Local recurrence after curative resection Ferro F, Zingaro E, Sirizzotti G, Civelli E, Valvo F,
for rectal cancer is associated with anterior position Gios M, Brunelli C - Total rectal resection and
of the tumour, Br J Surg 2006; 93: 105-112 complete mesorectum excision followed by
86. Lindsey I, Warren B, Mortensen N - Optimal total coloendoanal anastomosis as the optimal treatment
mesorectal excision for rectal cancer is by for low rectal cancer: The experience of the
dissection in front of Denonvilliers' fascia, Br J National Cancer Institute of Milano, Ann Surg
Surg2004,91:897 Oncol 2000, 7(2):125-132
87. Flati G, Porowska B, Procacciante F - Optimal total 98. Quah HM, Jayne DG, Eu KW, Seow-Choen F -
mesorectal excision for rectal cancer is by Bladder and sexual dysfunction following
dissection in front of Denonvilliers' fascia, Br J laparoscopically assisted and conventional open
Surg 2004, 91: 1202-1203 mesorectal resection for cancer, Br J Surg 2002, 89:
88. Greene FL, Compton CC, Fritz AG, Shah JP, 1551-1556
Winchester DP - AJCC Cancer staging atlas, 99. Polliand C, Barrat C, Champault G - Laparoscopic
Springer 2006 resection of low rectal cancer with a mean follow-
89. Matsumoto T, Ohue M, Sekimoto M, Yamamoto H, up of seven years, Surg Laparosc Endosc Percutan
Ikeda M, Monden M - Feasibility of autonomic Tech 2005, 15:144-148
nerve-preserving surgery for advanced rectal cancer lOO.Kienle P, Weitz J, Koch M, Biichler MW -
based on analysis of micrometastases, Br J Surg Laparoscopic surgery for colorectal cancer,
2005, 92: 1444-1448 Colorect Dis 2006, 8 (Suppl. 3), 33-36
90. Sugihara K, Kobayashi H, Kato T, Mori T, lOl.Gohl J, Merkel S, Hohenberger W -
Mochizuki H, Kameoka S, Shirouzu K, Muto T - LaparoscopicTME -The surgeon's or the patient's
Indication and benefit of pelvic sidewall dissection preference, in Biichler MW, Heald RJ, Ulrich B,
for rectal cancer, Dis Colon Rectum 2006; 49: Weitz J - Rectal cancer treatment, Springer-Verlag,
1663-1672 Berlin-Heidelberg, 2005 (Recent results in cancer
91. Mori M, Mimori K, Inoue H, Barnard GF, Tsuji K, research 2005, 165: 158-166)
Nanbara S, Ueo H, Akiyoshi T - Detection of 102.Schiedeck THK, Fischer F, Gondeck C, Roblick
Cancer Micrometastases in Lymph Nodes by UJ, Bruch HP - Laparoscopic TME: better vision,
Reverse Transcriptase-Polymerase Chain Reaction, better results?, in Biichler MW, Heald RJ, Ulrich B,
Cancer Res 1995, 55: 3417-3420 Weitz J - Rectal Cancer Treatment, Springer-
92. Hladik P, Vizda J, Bedrna J, Simkovic D, Strnada Verlag, Berlin-Heidelberg, 2005 (Recent results in
L, Smejkal K, Voboril Z - Immunoscintigraphy cancer research 2005, 165: 148-157)

Address for correspondence:


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

View publication stats