The last few years have seen advancing surgical techniques and neoadjuvant therapies that have significantly improved outcomes for patients with rectal cancer.1 Prior to the introduction of rectal magnetic resonance imaging (MRI) as routine clinical practice, the pathological staging of rectal cancer postoperatively was the mainstay of predicting outcome and survival, and a combination of digital rectal examination and endoscopic ultrasound was the basis of preoperative assessment.2 However, the Magnetic Resonance Imaging and Rectal Cancer European Equivalence Study (MERCURY) showed that high-resolution rectal MRI can accurately predict both the involvement of the surgical resection margin and the depth of extramural spread.3–5 This ability of rectal MRI to identify those patients with high-risk rectal cancer in a reproducible manner has led to the routine, and for many countries mandatory, adoption of rectal MRI for the preoperative assessment of patients.6–9
The accurate preoperative diagnosis and staging of rectal cancer are increasingly crucial, especially to ensure the appropriate selection of patients for neoadjuvant therapy and sphincter-preserving surgery.1 Accurate staging of rectal cancers enables patients to be advised regarding the risks of local and distant recurrence versus the morbidity of therapy and thus enables optimal and individualized treatment strategies.10
The effective use of rectal MRI relies on high-quality images and a systematic interrogation of the images.11 In this article, we outline key technical considerations along with a practical, systematic approach to the interpretation of rectal MRI.
Excellent patient preparation is obligatory for a high-quality study. Specifically, patients are counselled that individual sequences are lengthy but essential to optimize their treatment plans. To minimize patient discomfort during the examination, which takes 30 to 40 minutes, patients should empty their bladder prior to the scan. If there is concern regarding a patient’s ability to stay still during the study, the appropriate use of analgesia and sedation may be considered prior to their arrival in the magnetic resonance department.11
The advent of the pelvic phased array coil resulted in a change in rectal MRI. Prior to this, some early studies deploying the endorectal coil had shown promise from high-resolution T2-weighted scans of the rectal wall.12–16 As with any endoluminal technique, the disadvantages include severe discomfort for patients, inability to traverse stricturing or obstructing tumors, problems of near-field distortion,17 and incomplete imaging of the entire mesorectum at high resolution due to the limited high-resolution coverage.18 The advent and continued development of multichannel, multiarray pelvic received coils have enabled images to be obtained with resolution that are comparable to endoluminal techniques (Fig. 1). Furthermore, this enables imaging of the entire mesorectum in relative comfort for the patient11; thus, high-quality and high-resolution images can be obtained.
Appropriate positioning of the coil is essential and depends on the position of the tumor within the rectum. Problems are commonly encountered with low-rectal and midrectal tumors where the coil is positioned too high, and therefore there is loss of the detailed anatomy of the low rectum with added noise in the image; therefore, detailed interpretation of the tumor stage becomes needlessly challenging (Fig. 2). For low- and midrectal tumors, the pubic symphysis should be located within the center of the field of view, and for rectosigmoid tumors, the coil should be centered more superiorly.11
High-resolution T2 images are the mainstay of rectal cancer imaging. The magnetic resonance protocol has been published19 and validated by the MERCURY Study group,3 and the numerical parameters are listed in Table 1. Whereas the timing of each sequence has reduced with the introduction of newer magnetic resonance scanners, the sequence parameters remain unchanged.
Initial coronal and sagittal localizers are used to plan the first sagittal sequence, which will then be used to plan the high-resolution oblique axial and oblique coronal images.11 It is these high-resolution images that allow detailed interpretation of the tumor stage. Good communication regarding the site of the rectal tumor will allow appropriate planning of the study, especially considering the coil positioning.
The sagittal image is obtained with a slice thickness of 3 mm, a 25 × 25-cm field of view, and a 512 × 320 matrix size, which results in a higher-resolution sagittal image (a standard sagittal image would be obtained using a 5-mm slice thickness, a 30 × 30-cm field of view, and a 240 × 320 matrix). This higher-resolution sagittal image allows closer scrutiny of the anterior surgical plane in addition to planning of the high-resolution sequences. A large-field-of-view, T2-weighted axial image of the entire pelvis can be performed, while the high-resolution images are being planned, and these images give an overview of the pelvis and provide additional information regarding distant pelvic spread of disease and complications, for example, renal obstruction.
The high-resolution T2 oblique axial and oblique coronal images are performed with a 3-mm slice thickness, small field of view (16 × 16-cm maximum), a 256 × 256 matrix size, and a minimum of 6 signal averages; this results in a voxel size of 1.1 mm3. Any increase in the voxel size by uncompensated alteration of these parameters results in loss of detail and inability to assess the fine details of tumor spread (Fig. 1).
The sagittal image is used to plan the acquisition of the high-resolution T2 images, which need to be performed perpendicular to the rectal tumor.11 For a more tortuous rectum, this may mean smaller stacks of images are required to follow the contour of the rectum, but this is essential as overstaging can result from oblique scans where the normal rectal wall and extension of the tumor through the muscularis propria (MP) can be confused. The oblique coronal images are especially useful to assess the levator plate; this is especially important in the assessment of low-rectal tumors and when considering whether a low anterior resection or an abdominoperineal excision (APE) is more appropriate.20 Scans should always cover a minimum of 5 cm of mesorectum above the superior edge of the tumor to ensure adequate coverage of the lymph node drainage territory.21
T1-weighted images of the pelvis and the use of intravenous (IV) contrast are unhelpful in the assessment of primary rectal cancer and are therefore not indicated. Rather than aiding the diagnosis of rectal cancer, our experience is that IV contrast results in loss of clarity of the pelvic planes and causes the vessels to enhance (Fig. 3), so rather than aiding diagnosis, the use of IV contrast may in fact lead to overstaging of the tumor.11
A large anterior saturation band overlying the anterior abdominal wall should be used to reduce artifact from the movement of the abdominal wall muscles (Fig. 4), and antispasmodics should be used to reduce movement artifact from the bowel.11
Cross-talk artifact should be minimized by interleaving the slices and adding a small gap between each slice (<0.5 mm).11
INTERPRETING THE IMAGES
Each layer of the rectal wall has a distinct imaging appearance on T2-weighted MRI, thus enabling the interpretation of the T stage of the rectal tumor.19 The mucosa, although infrequently seen, is of low signal intensity, whereas the submucosa is of high signal intensity. The MP is formed of 2 layers, which are both of low signal intensity on the T2 images; the 2 layers are separated by the myenteric plexus, which is of intermediate signal intensity. These muscles can be differentiated by the direction of the muscle fibres; the circular muscle fibres are circumferential around the rectal wall, whereas the longitudinal muscles appear as small bundles that are orientated longitudinally around the rectal wall (Fig. 5).
The mesorectal fat appears as high signal surrounding the low signal of the MP; it contains signal voids, which represent vessels within the mesorectum.
The high-resolution oblique axial and coronal T2-weighted images are used for the assessment of the T stage, but the initial identification of the tumor is often best performed on the sagittal images. The location of the tumor should be defined as low, mid, or upper rectum dependent on the height of the tumor. Low-rectal tumors lie with within 6 cm of the anal verge,11,20 midrectal tumors are between 6 and 10 cm from the anal verge, and upper rectal tumors are in the proximal 5 cm of the rectum.11
The location of the tumor is important not only for planning acquisitions and positioning of the surface of the coil (as described above), but also for the planning of surgery. For low-rectal tumors, assessment of the levator plate and sphincter complex is required to assess a patient’s suitability for sphincter conserving surgery.20 Particular care should be taken to ensure that the scan acquisitions are obtained in the correct plane.
Once the tumor has been located, an assessment of the axial location of the tumor (in quadrants—anterior, posterior, right lateral, or left lateral) and tumor morphology will allow identification of the invasive margin of the tumor. Annular and ulcerating tumors present with raised rolled edges and a central invasive portion (Fig. 6). Although the raised rolled areas may be large and may occupy the rectal lumen, they will not infiltrate through the rectal wall. Therefore, the raised rolled edges allow identification of the central invasive portion.
Polypoidal and villous tumors may occupy the rectal lumen but are joined to the rectal wall by a fibrous stalk, which is of low signal intensity (Fig. 7). Rather than having an invasive central infiltrating area, they infiltrate through the base of the fibrous stalk.
Mucinous tumors comprise up to 20% of rectal cancers. They are notoriously difficult to detect on initial biopsy and are defined on MRI as containing more than 50% high-signal-intensity mucin within tumor stroma (Fig. 8). Magnetic resonance imaging has emerged as an effective and accurate means of identifying this poor-prognosis subgroup of patients. In a recent study of 330 patients with rectal cancer, MRI detected mucinous tumors in 18% in rectal cancer patients compared with only 5% detected by preoperative biopsy.22 In the same study, MRI detected mucinous tumor was an independent prognostic factor for poor disease-free survival.22
The final variation is the “signet ring” tumors that diffusely infiltrate the layers of the rectal wall and so produce thickening and accentuation of the rectal wall layers rather than destruction or replacement of individual layers (Fig. 9).
Following identification of the tumor, the tumor morphology, and the infiltrating margin, the T stage of the tumor can be assessed. This is done by systematic assessment of the intermediate signal intensity tumor infiltration through the walls of the rectum. Table 2 outlines the appearance of rectal tumors at each T stage.
With the advent of local excision for early-stage (T1) tumors, the accurate diagnosis of early stage is increasingly important. Endoscopic ultrasound with a high-frequency probe has been shown to detect sm1 tumors, which are suitable for local excision.23 The use of endoscopic ultrasound is limited by its inability to sufficiently resolve tumors with more than 5-mm penetration through the rectal wall. As a result, too few patients with early-stage rectal tumors may be underreferred for local excision.
The use of MRI in early-stage rectal tumors enables objective delineation of the relationship of the base of the tumor to the submucosa and MP layers and enables more appropriate selection of patients for local resection.24 In T1 sm1 and T1 sm2 tumors, the submucosa is visible at the invasive edge, whereas in T1 sm3 tumors and early T2 tumors, the submucosa is not seen at the invasive edge, but the normal thick MP layer is maintained (Fig. 10). For T2 tumors, part of the MP should be visible; however, full-thickness T2 tumors and T3a tumors are seen as tumors that replace the normal MP but where the intermediate tumor signal does not project beyond the normal contour of the bowel wall (Fig. 11).
The MRI diagnosis of a T3 rectal tumor requires the presence of tumor signal through and beyond the MP.11 The depth of penetration of the tumor through the MP allows subclassification of T3 tumors; this has prognostic significance and as such will alter patient management. Patients with T3a and T3b rectal tumors (where the tumor does not extend >5 mm beyond the MP) have equivalent survival to those patients with T2 tumors; therefore, additional treatment is not indicated.25 However, patients with T3c and T3d tumors have significantly worse prognosis, and as such, neoadjuvant treatment is indicated.25 This important distinction can be made by assessment of continuous tumor invasion through the MP, although this should not be confused with the small vessels that normally cross the MP into the mesorectal fat11 (Fig. 12).
T4 tumors are those that invade an adjacent organ or structure; these are seen as intermediate tumor signal intensity that invades into the peritoneum or adjacent pelvic organs. T4 structures are further divided into those that invade the peritoneum (T4a tumors) and those that invade adjacent organs (T4b).11 The location of the invasive edge of the tumor should be noted as it can predict the site of local invasion. Anterior tumors often invade the bladder and uterus, whereas lateral extension will be into the pelvic side wall, and posterior tumors will invade the sacrum (Fig. 13). Low-rectal tumors will also invade the seminal vesicles, vagina, sacrum, and coccyx as well as the levator muscles and the sphincter complex.11
Before the advent of total mesorectal excision (TME), the lymph node status of a rectal tumor predicted for local recurrence following surgery as the mesorectum was not removed in its entirety, and there was a high incidence of positive margins.26 However, in the modern era of TME, the mesorectal lymph nodes are removed en bloc with the rectal tumor, and as such, the incidence of positive margins and local recurrence has reduced.24,27
The presence of positive lymph nodes does not predict for patient outcome—for patients with early-stage disease, there is no increase in the incidence of local or distant recurrence, and for patients with advanced disease, the presence of malignant lymph nodes does not alter treatment plan or prognosis.
An assessment of nodal status by size criteria is inadequate. Histological data have demonstrated that there is a significant size overlap between malignant and benign lymph nodes28 and that there is no useful size cutoff for predicting the nodal status.29 Instead, the nodal morphology should be assessed on the high-resolution images. Normal, benign, or reactive lymph nodes are homogeneous with a preserved capsule, whereas malignant lymph nodes are irregular and heterogeneous and may demonstrate capsular breach (Fig. 14).
Extramural Vascular Invasion
Extramural vascular invasion (EMVI) is the presence of tumor cells beyond the MP in endothelium-lined vessels.30–32 It can be readily identified on high-resolution T2-weighted MRI, where it is identified as low signal intensity, which fills the normal signal void of a vessel (Fig. 15). It should be scored as either present or absent. Once EMVI is identified, it should be located as being within a small, medium, or large vein.
The presence of MRI-defined EMVI in a recognizable large vessel is an independent prognostic factor and defines the presence of a high-risk tumor.31 It is found in approximately 30% to 40% of patients with rectal cancer and is strongly associated with the development of local recurrence and liver metastatic disease.31,33
ASSESSMENT OF MARGINS
The majority of patients with rectal cancer will undergo TME, where the rectum and mesorectum will be removed en bloc by using the mesorectal fascia as the surgical plane; thus, the mesorectal fascia represents the potential circumferential resection margin (CRM).
The mesorectal fascia is clearly demonstrated on high-resolution T2-weighted MRI, and the radiologist report must determine whether the CRM is involved.11 The CRM is involved if there is tumor or EMVI within 1 mm of the mesorectal fascia; this is highly accurate and specific.5 The magnetic resonance CRM has been shown to be the only independent preoperative predictor of local recurrence in patients undergoing TME,34 and there is widespread agreement that all patients with an involved CRM on MRI should be offered preoperative chemoradiotherapy.
MAGNETIC RESONANCE TO GUIDE NEOADJUVANT TREATMENT
In the reporting of MRI, it is important to avoid overstaging tumors, which for low-risk tumors leads to significant added morbidity. In such patients, a low risk of local recurrence needs to be carefully balanced against the added risk of complications from radiotherapy such as impaired sphincter, urinary, and sexual function.1 The MERCURY study group showed that approximately one third of patients present with low-risk features: tumor spread of less than 5 mm, absence of extramural venous invasion, greater than 1-mm distance to CRM, and distal TME plane, and regardless of nodal involvement, such patients were shown to have a local recurrence rate of less than 3% (significantly lower than that achieved by the use of radiotherapy in previous clinical trials). Therefore, objective assessment of T substaging improves the appropriate use of radiotherapy; this can be achieved by a systematic interrogation of high-resolution magnetic resonance as described above.
Historically, pathologists have been able to assess the degree of response to chemoradiotherapy by determining the relative portions of fibrosis and residual tumor, as was described by the Dworak tumor regression grading (TRG) system.11,28 An MRI-based TRG system has been developed and validated to assess response to neoadjuvant therapy. Similar to the pathological system, the MRI-based TRG assesses the degree with which the rectal tumor has been replaced by fibrosis. Magnetic resonance imaging–based TRG been shown to correlate with overall survival27 and is a significant independent predictor of overall survival and disease-free survival.35
Tumor regression grading has 5 stages, as described in Table 3. The posttreatment MRI should be performed using the high-resolution technique described above and should be performed in the same planes as the original pretreatment staging MRI scans.11
In interrogating the images, radiologists should initially decide whether the residual mass is predominantly tumor or predominantly fibrosis. Thereafter, determining the exact TRG depends on the relative degree of fibrosis and residual tumor.27 In the future, MRI following neoadjuvant treatment may be used to decide whether further therapy is required and whether the surgical plane should be modified, an approach currently being tested in clinical trials.
Low-rectal tumors deserve special consideration because the surgical options for these tumors differ from higher-rectal tumors, and conventional staging systems are insufficient in these cases. Furthermore, most patients are anxious to preserve sphincter function if feasible. Low-rectal tumors are those that arise within 6 cm of the anal verge. At this point, the natural downward tapering of the mesorectal envelope means that surgery is more technically challenging, and the incidence of positive resection margins is increased.20 The main surgical options for the treatment of low-rectal cancer are a low anterior resection and an APE.20 Patients who require an APE have previously been shown to be at an increased risk of having an involved CRM, and therefore accurate depiction of the surgical anatomy within the pelvis is required to determine whether neoadjuvant therapy is required, based on the safety of the TME plane versus the need for an extended extralevator approach. The increased incidence of involved CRM associated with low-rectal cancer was due to high rates of perforations at the level of the puborectalis sling and “waisting” of the dissection in the distal TME procedure.20
Preoperative assessment combines an evaluation of the feasibility of sphincter preservation by assessing the distance from the distal edge of the tumor to the top of the puborectalis sling seen on MRI (Fig. 16) and assessment of the radial extent of tumor in relation to the distal TME plane. While patients with tumors that do not encroach the intersphincteric plane can undergo intersphincteric dissection and ultralow coloanal anastomosis, there is general agreement that such an approach needs to be determined preoperatively rather than at the time of surgery. For patients with tumor encroaching the intersphincteric plane, a more radical approach such as the extralevator APE should be performed.
A staging system has since been proposed that considers the relevant anatomy and aids surgical planning by assessing the safety of the distal TME plane. The MERCURY II multicenter Low Rectal Cancer study aims to reduce the incidence of involved margins by better preoperative depiction of the surgical planes.
Following validation by the MERCURY study group,3,4 rectal MRI has become mandatory for the local staging of rectal cancer in the United Kingdom and other countries.9 At diagnosis, MRI can now be used to identify the factors that are predictive of local recurrence to enable the appropriate use of radiotherapy.34 In addition, MRI should be used to identify high-risk patients who may require more intensive follow-up and to aid the planning of surgery. Following initial treatment, MRI can be used for restaging and in clinical trials is being used to select patients who may defer surgery.
Good-quality high-resolution T2-weighted MRI with systematic image interpretation should form the basis for discussing the management of patients with rectal cancer, thus informing confident radiology reporting, which can then guide the appropriate use of neoadjuvant therapy and aid in surgical planning.
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