British Journal of Radiology (2005) 78, S117-S127
© 2005 British Institute of Radiology
doi: 10.1259/bjr/15128198
Thin section MRI in multidisciplinary pre-operative decision making for patients with rectal cancer
G Brown, MBBS, MD, MRCP, FRCR
Department of Radiology, The Royal Marsden NHS Foundation Trust, Downs Road, Sutton SM2 5PT, UK
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Abstract
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High spatial resolution MRI of the rectum is an accurate method of staging rectal cancer. The technique requires attention to detail so that correct planes and scan parameters are used to obtain the best images. A detailed understanding of the pathological features of these tumours is required for image interpretation so that prognostic information beyond the basic T and N staging of the tumour can be obtained. Use of standardized criteria for reporting is reproducible in the multicentre setting and pre-operative multidisciplinary discussion of the MRI features increases the number of operations performed with tumour-free resection margins.
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Introduction
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With the increasing availability of pre-operative therapy and the proven ability of thin-section MRI to give accurate prognostic information [1], the radiologists' role in the pre-operative multidisciplinary team (MDT) decision making process has become critical because the information provided by the detailed imaging of the primary tumour guides the team to help achieve better outcomes for patients with rectal cancer [2].
The technique requires highly skilled MRI radiographers to understand the anatomy of the pelvis, rectum and mesorectum in order to appropriately plan the acquisitions and obtain consistently high quality images [3]. In England, the recent provision of multidisciplinary study days and workshops through the NHS Colorectal Multidisciplinary Team development programme [4] has proven invaluable in providing that enough time is set aside to ensure that scans are undertaken with meticulous care.
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MRI technical considerations
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Using thin 3 mm sections in-plane resolution is similar to that obtained with the endorectal probe. A rectal cancer, regardless of bulk, position or stenosis, can be imaged non-invasively. Future developments in phased array coil technology promise to improve the image quality yet further and the ability to obtain even higher quality images with optimal contrast resolution and even higher spatial resolution will undoubtedly improve accuracy. MRI has inherent advantages over multidetector CT despite the higher spatial resolution offered by the latter. This is because CT images fail to provide sufficient contrast resolution to delineate tumours from normal anatomical structures such as muscle coat, levator muscle and sphincter complex (Figure 1
). There is also the major limitation of inability to characterize nodules, to distinguish inflammatory change, fibrosis and desmoplastic reaction within mesorectal tissue from tumour within the mesorectal fat and thus there is the potential to overstage disease.
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Figure 1. CT and MRI images of a primary rectal tumour in the same patient. The primary tumour cannot be clearly delineated and there is insufficient contrast resolution between the primary tumour and the anal sphincter complex on the CT examination. The MR images, however, show tumour clearly in the axial and coronal planes (arrows). The coronal images enable a clear depiction of tumour in relation to the sphincter complex (arrow).
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Standardization of MRI technique
The detailed imaging parameters for currently available machines have been described elsewhere [3]. The initial sagittal T2 weighted scans are used to plan the thin section oblique axials (Figure 2). For tumours arising below the level of the levator origins (<6 cm from the anal verge), it is essential to undertake high resolution coronal or paracoronal imaging (Figure 3) and to evaluate the sagittal images carefully, as well as the standard oblique axial sections, in order to avoid the common pitfall of overestimating tumour spread into the levator muscles. In addition, care must be taken to plan scans orthogonal to the rectal wall in order to avoid problems with partial voluming.
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Figure 2. The sagittal T2 weighted scans are used to plan thin-section axial oblique scans. It is important to ensure the scans are obtained in a plane orthogonal to the tumour to prevent over-estimation of tumour spread.
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Figure 3. For tumours arising below the origin of the levator muscle, scans are obtained in a coronal or paracoronal plane as shown.
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To adequately assess the nodal status, scans must include the mesorectum above the tumour, as nodal spread will be in a cranial direction within the mesorectum. Inadequate coverage will lead to understaging. For the lower third rectal tumours, the rest of the mesorectum can be staged for nodes by planning a block of paracoronal slices that run parallel to the sacrum (Figure 4).
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Figure 4. Scan planes used for assessing mesorectal lymph nodes. The mesorectum can be assessed for lymph nodes by planning a block of coronal slices that run parallel to the sacrum.
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Normal anatomy and relevance to staging
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The sagittal scans allow tumours to be depicted in relation to the important anatomical landmarks, namely the dentate line, the anal verge, the peritoneal reflection, the seminal vesicles, the sacrum and coccyx. For the clinical management of rectal cancer, the rectum is divided into upper, mid and lower thirds.
The upper third of the rectum (at 10–15 cm from the anal verge) lies above the level of the peritoneal reflection. Prognostically these tumours tend to fare better than the mid and lower rectal tumours because the surgical dissection is more straightforward. However, it is still important to identify those tumours with significant posterior extension since they may involve the mesorectal fascia posteriorly and therefore require pre-operative therapy to render them resectable. In addition, extension through the peritoneal reflection may occur and invasion of adjacent structures, e.g. bladder usually requires a different operative approach in order to adequately resect tumour. Mid rectal tumours extend from 5–10 cm from the anal verge and lower third rectal tumours are defined as those arising <5 cm from the anal verge. Both mid and low rectal tumours are a challenge and achieving surgical removal with a clear circumferential margin is the goal for the whole multidisciplinary team.
The peritoneal reflection
This can be seen on sagittal images as a low signal intensity linear structure that can be traced back from the surface of the bladder or after us to the rectal wall anteriorly (Figure 5a), where it is attached to the rectum. On axial section, this point of attachment gives a v-shaped configuration (Figure 5b). The anterior covering of the rectum by peritoneal reflection widens in the cranial direction.
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Figure 5. (a) The peritoneal reflection (arrow) is demonstrated on the sagittal MR image as a low-signal intensity structure, here shown running from the posterior surface of the uterus to the anterior rectal wall. (b) On axial section, the apex of the peritoneal attachment forms a v-shaped configuration, as shown (arrows).
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The pelvic sidewall nerves
The inferior hypogastric plexus forms a densely fenestrated meshwork of nerves of genitourinary function. They lie in the sagittal plane running downwards and forwards from the sacral plexus just lateral to the mesorectal fascia. At the level of the seminal vesicles, the nerves lie very close to the mesorectal fascia (Figure 6).
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Figure 6. (a) The inferior hypogastric plexus can be seen both on sagittal and coronal imaging. This is demonstrated on these paracoronal images as strands (arrows), measuring between 2 mm and 4 mm in diameter and best seen at the level of the seminal vesicles. (b) On the sagittal images, the inferior hypogastric plexus forms a densely fenestrated meshwork of nerves, of high-signal intensity close to the pelvic sidewall (arrow).
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The mesorectal fascia
This is shown as a low signal intensity layer that surrounds the mesorectum (Figure 7). Inferiorly this layer fuses with the endopelvic fascia that lies over the surface of the levator muscles and superiorly the fascia fuses with the peritoneal reflection anteriorly and the parietal fascia posteriorly.
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Figure 7. The mesorectal fascia is demonstrated as a low-signal intensity layer surrounding the fatty envelope of the mesorectum (arrows); the corresponding structure can be seen on total mesorectal excision (TME) specimens as the dissection is performed lateral to the mesorectal fascia.
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Denonvilliers fascia
Anteriorly, at the level of the seminal vesicles, the mesorectal fascia fuses with the remnant of the urogenital septum. This is a dense band of connective tissue in the male and separates the prostate and seminal vesicles from the rectum (Figure 8). During total mesorectal excision (TME) surgery, the anterior dissection occurs in the plane between Denonvilliers fascia and the prostate [5].
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Figure 8. Denonvilliers' fascia is demonstrated on sagittal axial images as low-signal intensity bands, slightly thicker than the mesorectal fascia and is seen over the anterior aspect of the mesorectum behind the seminal vesicles and the prostate (arrowheads).
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The anal canal
The top of the anal canal is anatomically defined as the level at which the puborectalis sling sweeps around the rectum and in so doing creates the anorectal junction resulting in angulation between the rectum and anal canal. The length of the anal canal is highly variable, longer in males than females and on average represents the distal 4 cm of the gastrointestinal tract. On MRI, the sphincter is depicted as an almost complete ring of muscle (Figure 9). The superior margin of the external anal sphincter is defined by the lower edge of the puborectalis sling. Inferiorly, the fibres curve inwards just below the internal sphincter. The internal anal sphincter is formed by a thickened segment of the circular muscle coat in the distal rectum. The upper third of the anal canal is characterized by ridges of mucosal membrane that form the anal columns. Below this the mucosa is smooth surfaced and this point of transition is marked by the dentate line.
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Figure 9. Axial T2 weighted MR image of the anal sphincter complex. The external sphincter (black arrow) is demonstrated as an almost complete ring of low-signal intensity. The intersphincteric plane is of relatively high signal (arrowhead). The internal sphincter (white arrow) lies more medially and is also demonstrated as a low-signal intensity structure but is continuous with the muscularis propria of the rectum.
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The levator muscle
The levator ani complex comprises the puborectalis, pubococcygeus, ileococcygeus, and coccygeus muscles. The muscles collectively form a sheet that supports the pelvic floor. The levator muscle sheet is best visualized by MRI on coronal images which depict the muscle sheet running obliquely toward the anorectal junction (Figure 10).
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Figure 10. Coronal T2 weighted MRI showing the levator muscle (black arrow) running obliquely towards the anorectal junction (arrowheads). The mesorectum is at its most tapered at this point and thus tumours that extend through the muscularis propria are at high risk of circumferential involvement.
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Presacral fascia
The presacral fascia lies behind the mesorectal fascia and is described as a thickened parietal fascial covering that overlies the presacral veins and fat, and fuses with, and directly covers the muscles and vessels of the pelvic sidewall (Figure 11). The nodes of the pelvic sidewall accompany branches of the internal and external iliac vessels and are therefore in a separate compartment from the mesorectum. The pelvic sidewall nodes are therefore not routinely visualized in rectal cancer surgery unless this compartment is opened up by dissecting through the presacral or parietal fascia.
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Figure 11. Sagittal MR image demonstrating the presacral fascia (black arrow). This lies directly behind the mesorectal fascia (arrowhead).
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Assessing prognostic features using pre-operative MRI
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The circumferential resection margin (CRM)
Of the pre-operative prognostic features, CRM has emerged as one of the most powerful predictors of outcome. Regardless of local stage of the tumour, the presence of tumour within 1 mm of the surgical circumferential margin (Figure 12) predicts the development of local recurrence.
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Figure 12. Axial T2 weighted image and corresponding histopathology section. Tumour extends to within 1 mm of the mesorectal fascia (arrow). This corresponds to positive surgical circumferential margin on the corresponding histological section (arrow).
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Definition of circumferential resection margin
The surgical CRM is defined as the surgical cut surface of the connective tissues that encases the rectum. It is important to recognize that the areas of the rectum that have a peritoneal covering do not constitute the surgical CRM following TME surgery. The circumferential margin therefore equates to the mesorectal fascia which forms the plane of dissection in rectal cancer surgery.
Histopathological considerations: preparation of the specimen and quality control
Following the publication of observations of the significance of involved circumferential resection margins and its relationship to prognosis [6, 7] the handling of the specimen following resection was modified to enable a rigorous assessment of circumferential resection margin status. This form of specimen preparation has become the standard of practice for pathologists in the UK.
After fixation of the specimen in buffered Formalin, for a minimum of 3–4 days, the non-peritonealized surface of the specimen is painted, so that the inked margins may be visualized on microscopy. The specimen, now rigid, following Formalin fixation is sectioned axially in 3–4 mm slices and laid out for visual inspection by the pathologist. In many pathology laboratories, it is now possible to prepare megablock sections of at least one to two tissue slices, in order to complete detailed evaluation of extramural spread and closest resection margin (Figure 13).
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Figure 13. Histopathological preparation of the specimen. The specimen is sliced after Formalin fixation and the axial tissue slices can either be sampled or embedded whole into large cassettes. Extent of tumour spread (arrowheads) as well as distance to the closest non-peritonealized circumferential resection margin (double arrow) can then be assessed by the pathologist on the haematoxylin and eosin section.
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Elsewhere, visual inspection enables a selection of blocks of tissue from the tissue slices to be prepared. The tissue blocks sampled are specially selected to show the maximum extent of local tumour spread within the perirectal fat and blocks are also prepared of margins that appear close on macroscopic inspection. Blocks are also taken of other areas of interest, such as apparent extramural venous invasion, nodal and tumour deposits, and if tumour lies close to the peritoneal surface, blocks are taken to evaluate tumour and its relationship to the peritoneal membrane.
Clearly, the accuracy of pathology as the gold standard is dependent on the thoroughness of the sampling process and thus the number of blocks taken, as well as the number of lymph nodes harvested which is said to reflect the quality of histopathological sampling [8].
Assessment of the surgical circumferential resection margin is made by measuring the minimum distance between the tumour and the circumferential margin in millimetres. If this value is less than 1 mm (Figure 14), then the circumferential margin is defined as pathologically involved [9]. An overlaid transparent 1 mm grid, known as a graticule, allows precise measurement of tumour spread of the resected specimen. The pathologist notes whether involvement is through direct continuity with the main tumour, by tumour in veins, lymphatics, lymph nodes or by tumour deposits discontinuous from the main tumour.
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Figure 14. Whole mount histopathology section showing 1 mm graticule overlay, which enables precise measurement of distance to the circumferential margin to be made.
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For all patients undergoing primary surgical resection, including palliative cases, the rate of surgical circumferential margin involvement can be as high as 30% [10]. Of the cases undertaken with curative intent, the circumferential resection margin rate has been reported as between 15% and 18% [7].
MRI assessment of the CRM
MRI has the inherent advantage of being able to consistently depict the mesorectal fascia, which forms the surgical circumferential resection margins in TME surgery. When tumour extends to within 1 mm of this fascia, infiltrates or extends beyond this fascia, this predicts subsequent margin involvement (Figure 15) [1]. Prior to the advent of the technique that can delineate this fascia, identification of such cases was limited to clinical assessment of fixity of the tumour and the widely held view that a clinically fixed tumour would result in positive circumferential resection margins. Very often it is impossible to determine by clinical examination cases with margin involvement as these can be remote from the primary tumour. Tumour deposits extending to the mesorectal margins for example will not be detected by endorectal assessment [11].
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Figure 15. Axial T2 weighted MRI examination and corresponding histopathology section. Multiple tumour deposits are demonstrated (arrow), which lie within 5 mm of the mesorectal fascia, but not within 1 mm of the fascia. Although this tumour distribution indicates a poor prognosis, the circumferential resection margins are predicted as being clear of tumour. The corresponding histopathology section demonstrates clear surgical circumferential resection margins (arrowheads).
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In a prospective study assessing the tumour relationship to the mesorectal fascia, excellent agreement of MRI with histology assessment of margin status was obtained when the definition of predictive margin involvement was tumour within 1 mm of the mesorectal fascia. Increasing this distance to between 1 mm and 5 mm did not improve accuracy and would have resulted in overstaging and overtreatment of patients [12].
Nodal disease
The presence of involved lymph nodes in the resected specimen is an important pathological prognostic indicator for the likelihood of systemic disease and is an indication for post-operative adjuvant chemotherapy [13]. The TME operation produces an anatomically undisturbed specimen, containing the rectum, mesorectum, lymph nodes and tumour deposits, encased by the mesorectal fascia. This has provided us with a unique opportunity to map the tumour and lymph nodes within the mesorectum. Using node for node matching, high resolution MRI predicts nodal status most accurately when the morphological features of the nodes were used rather than measurement of size [14]. For this reason, the use of size as a criterion for determining nodal involvement is not recommended. A node can be predicted as malignant if it displays either mixed signal intensity within the node or irregularity of its borders (Figure 16). To further improve our accuracy in nodal staging we need to: (1) resolve even very small nodes <3 mm in diameter; (2) resolve small tumour deposits <2 mm within nodes; and (3) image the entire vascular pedicle that contains nodes up to the origins of the inferior mesenteric artery. Currently, prolonged scan duration limits our ability to image the mesorectal vascular pedicle above the sacral promontory using thin section MRI. The current spatial and contrast resolution achievable using MRI permits us to identify tumour deposits measuring 3 mm or greater within nodes but not to resolve and characterize nodes <2 mm. Thus, accurate assessment of nodal status remains a challenge. However, it is possible that the new lymph node-specific contrast agents may help us detect these small tumour deposits and preliminary evaluation shows that mesorectal lymph nodes can be characterized by using USPIO (ultra small particles of iron oxide) and T2* weighted MRI. Uniform and central low-signal-intensity patterns are features of non-malignant nodes. Reactive nodes show central low signal intensity at T2* weighted imaging and malignant nodes remain bright (Figure 17) [15]. Thus, the use of this agent could be of value in future.
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Figure 16. Axial thin section T2 weighted image and corresponding histopathology section demonstrating a mixed signal intensity lymph node (arrow), which also has an irregular border. The presence of either one of these features is a good predictor for malignant node involvement shown on the corresponding histopathology slide (arrow).
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Figure 17. Identification of benign and malignant nodes using ultra small iron oxide particles (USPIO). Axial T2* weighted images, before and after administration of USPIO, demonstrates three lymph nodes, that are of high-signal intensity before administration of USPIO. Following administration of USPIO normal lymph nodes darken (white arrows) and malignant lymph nodes which do not take up USPIO remain high signal (black arrow) corresponding to histopathology haematoxylin and eosin stained sections demonstrating fully replaced malignant node.
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Pelvic sidewall disease
The 16 cm field of view use of thin-section MRI enables the pelvic sidewall compartment to be assessed, as well as the mesorectal compartment (Figure 18). This is of particular value in identifying patients at risk of residual disease, despite a successful TME operation, due to pelvic sidewall nodal disease. It is generally thought that pelvic sidewall disease is a feature of aggressive disease and is associated with poor survival [16].
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Figure 18. Malignant lymph node (arrow) demonstrated outside the mesorectal envelope. This represents metastatic disease.
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In the UK and Europe, pelvic sidewall nodal dissection is seldom performed because of the unacceptable morbidity related to this operation, but the finding of malignant nodal disease in the pelvic sidewall would prompt the use of targeted radiotherapy or chemoradiotherapy.
Low rectal tumours
Improving outcomes for low rectal cancers remains a challenge for the Colorectal Multi Disciplinary Team. Low rectal cancer is defined as tumour arising in the lowest 5 cm of the rectum and the majority of published series have shown that tumours arising in the lower third of the rectum have the worst outcome, with local recurrence rates as high as 30%, despite the introduction of TME surgery. On review of the imaging, the lowest 5–6 cm coincides with the point at which the mesorectal fascia fuses with the levator muscle, close to the pelvic sidewall and the mesorectum becomes a narrowed and tapered structure with only a thin covering of perirectal tissue. In conventional TME surgery and abdominoperineal surgery, the resection specimen seldom contains the levator muscle, thus the margins of the specimen below the level of the levator origin can be variable. This is particularly so when abdominoperineal excision is performed, as the perineal dissection does not follow a defined and predictable plane and the distal portion of abdominoperineal specimens usually comprise the muscle tube of the rectum with very little perirectal tissue. Thus, for tumours that have gone through the full thickness of the muscle coat in the lower third of the rectum, tumour perforation and exposure of tumour on the surface of the specimen occurs in up to a third of cases [17]. Thus for tumours of the lower third of the rectum the role of MRI becomes even more important in providing the information necessary to determine whether or not an anteroposterior (AP) excision or anterior resection should be performed and whether it is necessary to remove an extended amount of perirectal tissue in order to prevent positive circumferential resection margins. For many colorectal teams, the preferred option is pre-operative therapy followed by surgery, but this has to be balanced against functional outcome, particularly if sphincter-sparing surgery for a low rectal tumour is being contemplated. The coronal T2 weighted images demonstrate the relationship of tumour to the levator muscle, the internal sphincter, external sphincter and perirectal fat and enable the MDT to determine an individualized treatment plan based upon the detailed imaging findings. One of the most common pitfalls when assessing lower third rectal tumours is to overestimate the spread when evaluating the thin-section axial images. Because the rectal wall is tapering and because of the obliquity of the levator muscle, tumour can very easily be overstaged as invading the levator muscle. However this pitfall can be avoided if the sagittal and coronal images are also reviewed (Figure 19).
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Figure 19. Sagittal and axial images of the low rectal tumour. (a) The axial images show apparent tumour spread through the rectal wall into the levator muscle (arrows). However this is artefactual and due to the obliquity of the scan plane. (b) The sagittal image confirmed that the tumour is confined to the rectal wall. The case illustrates the importance of reviewing both the coronal and sagittal images of low rectal tumours.
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Extramural venous invasion
Venous invasion is defined by the pathologist as the presence of tumour tissue within an endothelium lined space; either surrounded by a rim of smooth muscle or contained red blood cells. Talbot shows that extramural venous invasion was present in 52% of specimens examined. Of these, the specimens showing invasion in "thick-walled veins" (14.6% of all rectal cancers) were significantly associated with distant metastases and death from tumour recurrence [18]. Several studies have shown a very strong relationship between the presence of extramural venous invasion and metastatic disease within the liver. This is a very powerful poor prognostic indicator and occurs with increasing depth of spread of tumour. In multivariate analysis the presence of extramural venous invasion maintains its independent prognostic value for outcome [19–22]. On thin-section MRI, extramural invasion by tumour can be readily identified on imaging and is demonstrated as serpiginous or tubular extension tumour beyond the muscle coat and when this is identified this has a high positive predictive value when compared with histopathological assessment of extramural venous spread (Figure 20).
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Figure 20. MRI and corresponding histopathological section showing the primary mid-rectal tumour with nodular extension of tumour into an extramural vein laterally on the left (arrow). When this feature is demonstrated on pre-operative imaging, there is a high positive prediction for extramural venous invasion on histopathology, which in turn is a poor prognostic feature.
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Depth of extramural spread of tumour
Depth of extramural tumour spread is defined as measured distance of tumour beyond the outer longitudinal muscle coat. In the UK, T3 tumours comprise 80% of rectal tumours presenting to the colorectal surgeons, however survival for these varies widely. Pathology audit of specimens has shown that extensive spread of tumour beyond the bowel wall (>5 mm) predicts for significantly poorer survival than tumours with <5 mm spread despite negative circumferential margins [23].
Pathologists have long recognized that with increasing depth of spread there is an increasing incidence of nodal involvement and extramural venous invasion [24–26]. These tumours represent the poorest end of the prognostic spectrum, with high risk of both local and distant failure. There has been interest in selectively treating these patients with aggressive pre-operative therapy [27]. The efficacy of such an approach has been shown in recent phase II clinical trials [28, 29], but phase III trials are required to determine whether a pre-operative strategy achieves an improvement in survival compared with adjuvant post-operative treatment through the earlier elimination of micrometastatic disease.
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Summary
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An MRI determined pre-operative treatment strategy together with good quality surgery promises to improve outcomes in patients with rectal cancer.- MDT discussion of the MRI scans is essential;
- Standardized proforma and specialist Radiology reporting ensures that the many important factors governing patient outcome are sought;
- We may therefore be able to eliminate local failure and increase survival by appropriate targeting of therapy.
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Abstract
Introduction
