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1 Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales
College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
2 Present address: Department of Radiology, The Royal Marsden NHS Trust, Downs
Rd., Sutton, Surrey SM2 5PT, England.
3 Department of Imaging, The Middlesex Hospital, Mortimer St., London W1T 3AA,
England.
4 Cardiff School of Biosciences, Biomedical Bldg., Cardiff University, Cardiff
CF10 3US, Wales.
5 Department of Anatomy, The Royal College of Surgeons of England, 35/43
Lincoln's Inn Fields, London WC2A 3PE, England.
6 Department of Colorectal Surgery, The Pelican Centre, North Hampshire
Hospital, Aldermaston Rd., Basingstoke, Hampshire RG24 9NA, England.
Received March 6, 2003;
accepted after revision August 19, 2003.
Address correspondence to G. Brown
(gina.brown{at}rmh.nthames.nhs.uk).
Abstract
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SUBJECTS AND METHODS. High-spatial-resolution T2-weighted MRI was performed using a 1.5-T system in cadaveric sections and in patients before they underwent total mesorectal excision surgery. Anatomic dissections of sagitally sectioned hemipelves were compared with MRIs obtained in vivo to establish criteria for visualization of the structures relevant to anterior resection of the rectum.
RESULTS. High-spatial-resolution MRI depicted a number of structures of importance in total mesorectal excision surgery. The mesorectal fascia, which forms the boundary of the surgical excision plane in total mesorectal excision, was identified, and the presacral fascia, peritoneal reflection, and Denonvilliers' fascia were also shown. Structures 1–2 mm in diameter were visualized because the contrast resolution afforded by T2-weighted fast spin-echo imaging permitted depiction of the inferior hypogastric nerve plexus and the fascial planes within the posterior pelvis.
CONCLUSION. Anatomic landmarks important to the performance of rectal cancer surgery, in particular the mesorectal fascia, may be defined on MRI and are of potential importance in the staging of tumors, assessing resectability, planning surgery, and selecting patients for preoperative neoadjuvant therapy.
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The proximal dissection involves dividing the inferior mesenteric artery close to its origin and mobilizing the vascular pedicle of the sigmoid mesocolon, while carefully preserving the superior hypogastric nerve plexus. The dissection then continues in the relatively avascular areolar tissue plane posterior to the mesorectum, thereby separating the visceral fascia on the surface of the mesorectum from the presacral parietal fascia. As the dissection proceeds inferiorly, the variable rectosacral fascia is divided at the level of the fourth sacral vertebra. The lateral surfaces of the mesorectum are then dissected, separating the mesorectal fascia from the parietal fascia of the pelvic sidewall while preserving the hypogastric nerves and the inferior hypogastric plexus. Further lateral dissection separates the mesorectum from the neurovascular bundles that run forward and medially toward the urogenital structures. The anterior dissection divides the peritoneum anteriorly relative to the rectovesical (in males) or rectovaginal (in females) pouches. The dissection continues in front of Denonvilliers' fascia, posteriorly relative to the seminal vesicles and the prostate gland in the male. In the female, there is a corresponding, but thinner, rectovaginal septum. Thus, the total mesorectal excision specimen comprises the rectum surrounded by a complete mesorectum containing draining lymph nodes within an intact mesorectal fascial envelope with a smooth glistening surface and including Denonvilliers' fascia anteriorly. Preservation of the intact superior and inferior hypogastric plexuses and hypogastric nerves safeguards sexual and bladder function.
Preoperative knowledge of the precise extent of tumor spread in relation to anatomic structures is of critical importance in planning surgery. Furthermore, because this information is used to determine the use of preoperative therapy, surgical planning itself may be altered. The aim of our study, therefore, was to compare axial MRIs of the cadaveric pelvis with axial histologic sections of the same cadaver and to compare MRIs of selected patients obtained before they underwent total mesorectal excision surgery with whole-mount histologic sections obtained after surgery. In addition, anatomic dissections of sagittally sectioned hemipelves were compared with MRIs obtained in vivo to establish criteria for visualization of the structures relevant to anterior resection of the rectum.
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Axial whole-mount histologic sections were obtained from a cadaveric pelvis. Thin axial slices were fixed in formalin and decalcified in 5% hydrochloric acid solution for 6 weeks. Histologic sections were cut and stained with H and E, so that the whole of the mesorectum and surrounding structures could be mounted onto large glass slides. These were then compared with corresponding high-resolution MRIs obtained in the cadaver. Anatomic landmarks visualized on total mesorectal excision whole-mount sections were compared with in vivo MRIs. In addition, cadaveric pelvic hemisections dissected in the parasagittal plane to show the nerve plexuses were compared with in vivo sagittal high-resolution MRIs of the pelvis.
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The Retrorectal Space
When the rectum in the sagittally hemisected cadaveric pelvis is pulled
forward, the retrorectal space is clearly visible
(Fig. 2A). This space is
limited posteriorly by the presacral parietal fascia and anteriorly by the
mesorectal fascia. The presacral fascia is shown on sagittal MRI as a
low-signal-intensity linear structure overlying the presacral vessels
(Fig. 2B). The mesorectal
fascia is seen immediately anterior to this structure, and the potential space
between these two fascial layers forms the retrorectal space. In two patients,
abnormal collections of fluid had accumulated in the retrorectal space as a
result of the perforation of the rectum
(Fig. 3).
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The Rectosacral Fascia
At examination of cadaveric specimens, we found the rectosacral fascia
(Fig. 4A) to be a fascial band
of variable thickness running from the sacrum to the mesorectal fascia at the
level of the fourth sacral vertebra that could be visualized on MRI
(Fig. 4B).
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The Peritoneal Reflection
From the uppermost part of the posterior surface of the bladder, the
peritoneum extends posteriorly to the junction of the upper two thirds and
lower one third of the rectum in males (Fig.
5A,
5B). In females, the site of
attachment in the lower third of the rectum is more varied. The
peritoneum-lined recess between the rectum and the posterior aspect of the
bladder is the rectovesical pouch. On sagittal MRI of histologic sections
obtained after surgery, the peritoneal reflection appears as a
low-signal-intensity linear structure that extends over the surface of the
bladder and can be traced posteriorly to its point of attachment onto the
rectum (Fig. 6). The peritoneum
attaches in a V-shaped manner onto the anterior aspect of the rectum, an
appearance we characterized as the "seagull" sign (Fig.
7A,
7B).
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Denonvilliers' Fascia and the Urogenital Neurovascular Bundle
This well-developed fascia forms a distinctive shiny anterior surface of
the mesorectum. It is visible on MRI as a low-signal layer that can be traced
up to the peritoneum superiorly (Fig.
8A,
8B).
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The Lateral Ligaments
Contralateral rectal traction, or cadaveric dissection (Fig.
9A,
9B), of the fascia around the
neurovascular branches as they run medially to the rectum creates the lateral
ligaments of the rectum. Although not shown as ligamentous structures on MRI,
the lateral ligaments may be indicated by middle rectal vessels when these are
present (Fig. 10A,
10B).
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The Pelvic Nerve Plexuses
In cadaveric sections, the superior hypogastric plexus is seen as
bifurcating like a wishbone into a pair of hypogastric nerves that descend to
join the inferior hypogastric plexuses. Each inferior hypogastric plexus lies
in a parasagittal plane on the sidewall of the pelvis. In males, the inferior
hypogastric plexus lies posterolaterally relative to the seminal vesicle; and
in females, its anterior half lies against the upper third of the vagina.
Thus, the inferior hypogastric plexus is shown on MRI in a plane inside and
medial to the vessels on the pelvic sidewall. The inferior hypogastric plexus
is a rectangular, fenestrated structure that is 3–4 cm in its
anteroposterior length (Fig.
11A,
11B) in the parasagittal plane
and is easily identified on MRI. The dissected inferior hypogastric plexus in
a cadaveric hemipelvis can be correlated with sagittal T2-weighted MRIs
(Fig. 11B), on which it is
depicted as a high-signal-intensity meshlike structure. We found that the
inferior hypogastric plexuses consistently appear on axial
(Fig. 12) and coronal oblique
(Fig. 13) MRIs as linear,
somewhat beaded structures. On coronal oblique images, these structures could
be traced to their sacral nerve origins.
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The Mesorectal Fascia and Mesorectum
We found that the mesorectal fascia seen on axial MRIs of the cadaveric
sections and correlated with the corresponding whole-mount histologic sections
to be a distinct thin layer encompassing the mesorectum and surrounded by
loose areolar tissue (Fig.
14A,
14B,
14C). The mesorectal fascia is
best seen on axial images and appears as a low-signal-intensity linear
structure surrounding the mesorectum. It was consistently visualized on
thin-slice MRI.
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The mesorectum is shown on axial MRIs of the cadaveric sections as a high-signal-intensity (similar to the signal intensity of fat) package surrounding the rectum, containing vessels and lymphatic tissue (Fig. 15A, 15B). Lymph nodes within the mesorectum are shown as high-signal-intensity ovoid structures.
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The Rectal Wall
In cross-section, the rectal wall comprises the mucosal layer, muscularis
mucosae, submucosa, and muscularis propria (Fig.
16A,
16B). On MRIs obtained in
cadavers and in vivo, the mucosal layer of the bowel wall appears as a fine,
low-signal-intensity line with the thicker, higher-signal-intensity submucosal
layer beneath. The muscularis propria is sometimes depicted on MRI as two
distinct layers—the inner circular layer and the outer longitudinal
layer. The outer layer has an irregular corrugated appearance and numerous
surface interruptions caused by vessels entering the rectal wall. The
perirectal fat displays high signal intensity and is surrounded by the low
signal intensity of the muscularis propria.
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The detailed anatomy of the mesorectal fascia (fascia propria of the rectum) and MRI depiction of this structure have been described [3, 4]. Bissett et al. [4] dissected the mesorectal fascia from the mesorectum and showed that this fascia is a continuous structure that encircles the rectum and mesorectum, fusing with the peritoneum at its reflection off the rectum. At the level of the anorectal junction, the mesorectum thins out. The mesorectal fascia is clearly shown on MRI and thus permits an assessment of the distance between the tumor and the potential circumferential margin of total mesorectal excision. Depiction of tumor extending to this margin could influence the type of surgical procedure chosen and alter the plane of surgical excision; it could also result in having the patients undergo preoperative therapy in an attempt to induce the tumor to regress from the margin of the mesorectum.
Van Ophoven and Roth [5] reviewed the conflicting theories concerning the anatomy and embryologic derivation of Denonvilliers' fascia since its first description in 1836 [6]. The consensus is that this fascia represents the fusion of the walls of the peritoneal cul-de-sac that extends down to the pelvic floor in the fetus [7]. This fascia forms the glistening white surface of the anterior aspect of the mesorectum and is removed as an integral component of the resected package in total mesorectal excision. Denonvilliers' fascia is seen on MRI as a low-signal layer, and its visualization in relation to an anterior tumor of the rectum provides valuable preoperative information.
The rectosacral fascia, often referred to as Waldeyer's fascia (although Waldeyer did not describe it as such in his anatomic report published in 1899), was characterized by Crapp and Cuthbertson [8]. The thickness of this fascia varies from a thin transparent membrane to a thick, tough, opaque fascia. In the latter instance, unless the rectosacral fascia is deliberately divided, the surgical plane of dissection may erroneously extend anteriorly into the mesorectum, resulting in its incomplete excision, or stray posteriorly through the presacral fascia with consequent troublesome bleeding from presacral veins. We do not believe that the depiction of this ligament on MRI has been previously described.
The anatomy of the autonomic nerves that must be safeguarded during total mesorectal excision have been described in detail by Havenga et al. [9] and Kirkham et al. [10]. The preservation of these nerves is crucial to the maintenance of urologic and sexual function, and clear depiction of these structures in relation to tumor is of value in surgical planning. To our knowledge, the depiction of the inferior hypogastric plexus on MRI has not previously been described. As reported in MRI studies of the brachial plexus, the high spatial and contrast resolution of MRI enables neural structures to be separately defined from surrounding muscle and vascular structures. High-resolution T2-weighted images show the inferior hypogastric plexuses as high-signal structures that can be distinguished from vessels by their lack of blood-flow-related signal void. Our observations concur with findings of Liu et al. [11] that T2-weighted pulse sequences are the most useful for anatomic definition of nerve plexuses.
The inferior hypogastric plexus also provides branches to the rectum, which may be accompanied by a middle rectal artery, but this artery is often absent or very small. Traction on this neurovascular bundle produces the so-called lateral ligament, the size of which depends on the presence or absence of the middle rectal vessels. Previous studies have shown that the middle rectal vessels are not consistently shown either in cadaveric dissections or on angiography [12, 13].
Although our study defined a number of anatomic structures on high-spatial-resolution MRI, a potential limitation is that we were unable to document the frequency and variation in appearances of these structures because correlation of imaging appearances with anatomic structures had been performed in selected patients. Therefore, a future study evaluating frequency and variation of the structures seen on MRI as well as the usefulness of this information in the clinical setting in a large population would be of value.
The MRI appearances of the peritoneal cavity and the peritoneal folds that subdivide the cavity have been well described in the abdomen [14, 15]. However, the MRI appearances of the attachment of the peritoneum to the anterior rectal wall and the subperitoneal pelvic compartments have not been described, to our knowledge. We have reported the MRI appearance of the pelvic peritoneum and the site of its reflection off the anterior aspect of the rectum. The rectosacral space has also been imaged, and the presacral fascia that limits it has been visualized posteriorly. The preoperative imaging of perirectal structures and compartments and the elucidation of their relation to location and extent of tumor provide valuable information for the overall planning and delivery of best-practices surgery and neoadjuvant therapy.
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