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Imaging, 22 (2013), 20110078

GASTROINTESTINAL IMAGING

Staging of colorectal cancer


M J STEWARD,

MRCP, FRCR

and D MURRAY,

MRCP, FRCR

Department of Imaging, Whittington Hospital, London, UK


Summary
Colonic cancer should be routinely staged with multidetector CT of the chest,

abdomen and pelvis to assess complications, metastatic disease and high-risk


patients.
MRI should be offered to rectal cancer patients, unless contra-indicated, to guide
selective use of neoadjuvant chemoradiotherapy and optimise delayed surgical
treatment.
Optimised MRI technique and interpretation allows assessment of tumour and lymph
node staging, and investigation of the potential circumferential resection margin.
Restaging with MRI after neoadjuvant therapy aids MDT decisions.
Developments in diffusion-weighted imaging may have a role in assessing local disease.

doi: 10.1259/imaging.
20110078
2013 The British Institute of
Radiology

Cite this article as: Steward MJ, Murray D. Staging of colorectal cancer. Imaging 2013;22:20110078.

Abstract. Colorectal cancer requires different modalities for


accurate staging. Pre-operative staging with multidetector CT
(MDCT) for colonic cancer and MRI to assess local disease in
rectal cancer are central to multidisciplinary meetings to plan
treatment strategy. MRI has shown increased relevance for
neoadjuvant chemoradiotherapy in order to optimise delayed
surgical treatment. A systematic approach to reporting helps
define high-risk patients, particularly those with potential for
local recurrence or curative total mesorectal excision. This
review highlights the use of MDCT and MRI, including their
techniques in pre-operative, post-operative or post-neoadjuvant
treatments. Illustrated examples of TNM staging and
complications of disease are used. Future developments with
the use of diffusion-weighted imaging are also discussed.
Colorectal cancer is the third most common cancer in
the UK after breast and lung. In 2009 there were 32 751
new cases of colorectal cancer registered in the UK [1]
(approximately two-thirds in the colon and one-third in
the rectum). Tumours in the sigmoid colon, rectosigmoid
junction and the rectum account for over half of the cases.
After consultation, the National Institute for Health
and Clinical Excellence (NICE) recently published clinical
guidelines for the diagnosis and management of colorectal
cancer [2]. Diagnostic imaging investigations including CT
and MRI have been highlighted as central to the staging
process and discussion encouraged via colorectal MDTs.
The findings of a digital rectal examination should not be
used as part of the staging assessment. The use of specialist
Address correspondence to: Dr Michael Steward, Department of
Imaging, Whittington Hospital, Magdala Avenue, London N19 5NF,
UK. E-mail: Michael.Steward@nhs.net

imaging.birjournals.org

hepatobiliary MDTs, if CT demonstrates metastatic disease


only in the liver, should also be accessible.
This review will summarise the modalities used to
stage colorectal cancer, including techniques and image
interpretation. The staging of colon and rectal tumours
will be reviewed separately below.

Staging of colonic carcinoma


Multidetector CT (MDCT) has been the principal investigation for the staging of colonic carcinomas, and
contrast-enhanced MDCT of the chest, abdomen and
pelvis should be offered as routine staging. This provides
information regarding the site and size of the tumour,
infiltration into surrounding structures and metastatic
spread. The technique has been standardised by the
Royal College of Radiologists. It involves the oral administration of 1 l water for the delineation of the small
and large bowel followed by 100150 ml intravenous
iodinated contrast medium injected at 24 ml s21. The
chest is imaged 2025 s and the abdomen and pelvis
7080 s post contrast injection. Sections are acquired at
1.252.5 mm thickness with reformatting at 5 mm for
interpretation. Three-dimensional reconstruction allows
analysis in the coronal and sagittal planes as well.
While demonstration of metastatic disease traditionally
alters management and should be commented upon,
there has been significant attention recently to improve
interpretation of CT examinations in order to accurately
identify poor prognostic indicators of the primary tumour [3]. These indicators determine high-risk patients
and include depth of extramural spread, lymph node involvement, extramural venous invasion (Figures 1 and 2)
and peritoneal infiltration. The process of differentiating
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Figure 1. Axial multidetector CT with a thickened, irregular

M0: no distant metastasis


M1: distant metastasis
M1a: metastasis confined to one organ or site
(e.g. liver, lung, ovary)
M1b: metastasis in more than one organ/site or
the peritoneum

Distant metastases (M)

M J Steward and D Murray

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Classifications according to American Joint Committee for Cancer staging manual, 7th edition [4].

T3: tumour invades the muscularis propria into


pericolorectal tissues
T4a: tumour penetrates the surface of visceral
peritoneum
T4b: tumour directly invades other organs or
structures

NX: cannot be assessed


N0: no regional lymph node metastasis
N1: metastasis in 13 regional lymph nodes
N2: metastasis in 4 or more regional lymph nodes
TX: cannot be assessed
T0: no evidence of primary tumour
T1: tumour invades submucosa
T2: tumour invades muscularis propria

nous invasion (arrow) from the corresponding resection


tumour of Figure 1.

Regional lymph nodes (N)

Figure 2. Histopathological correlation of extramural ve-

Primary tumour (T)

high-risk patients from low-risk patients based on MDCT


will help identify a cohort of patients that could benefit
from neoadjuvant therapies.
The TNM staging system classifies the extent of cancer
based on anatomical information about the size and extent
of the primary tumour (T), the regional lymph node status
(N) and the distant metastases (M). Revisions are made
periodically and currently it is the most widely used
staging system worldwide. The 7th edition of TNM staging was recently published by the UICC (International
Union for Cancer Control) and AJCC [4] (American Joint
Committee for Cancer) at the beginning of 2010 (Table 1).
It recognised the fact that anatomical imaging has a crucial
prognostic role for neoplastic disease.
Colonic cancers are staged as T1 if the tumour invades
the submucosa and T2 if the tumour invades the muscularis propria. With regard to MDCT, T1 lesions are
depicted with intraluminal projection of the tumour
without any distortion of the bowel wall layers. T2
lesions present with asymmetrical thickening projecting
intraluminally but with preservation of the smooth
muscle coat and clear adjacent pericolonic fat. T3 lesions
infiltrate beyond the muscularis propria and features

Table 1. TNM classification for colon and rectum cancer staging

vessel (arrow) illustrating extramural venous invasion adjacent to a stenosing splenic flexure colonic tumour.

Imaging 2013, 22, 20110078

Staging of colorectal cancer

identifiable on MDCT include smooth or nodular extension of a discrete mass of tumour tissue beyond the
contour of the bowel wall with extension into pericolic
fat. Use of coronal or sagittal imaging can improve detection of this extramural invasion for more accurate
staging.
T4 lesions include tumours that penetrate the surface of
the visceral peritoneum, directly invade or are adherent
to other organs or structures, or tumours where there is
evidence of perforation. The identification of peritoneal
infiltration has been used to classify patients as high risk
by recent groups [5, 6].
MDCT has limited accuracy for the detection of nodal
stage, largely because of its inability to detect micrometastases. The criterion of a nodal mass larger than 1 cm
in diameter or a group of three or more nodes is used for
positivity. Accuracy rates are still poor and range from
60% to 80%. Some advocate the use of enhancement
characteristics and suggest an enhancement greater than
100 HU, representing malignancy [6, 7].
Extramural venous invasion as an independent prognostic factor has been evaluated by MDCT, and classified
[6, 7]. The appearances of nodular spread into small vessels or definite enhancing tumour spread along a large
vein are considered to define positivity. The accuracy of
these observations is currently an area of active research.
MDCT pre-operatively can alter management by
demonstrating T4 invasion that will modify the surgical
approach. In addition it may identify a complication related to the primary tumour. Examples include intestinal
obstruction, pericolic abscess, intussusception (Figure 3)
and acute appendicitis. Local tumour perforation through
the peritoneal membrane carries an unfavourable prognosis, and risks dissemination of malignant cells via
transcoelomic spread and peritoneal involvement.
After curative resection patients with colorectal cancer
should also have regular surveillance. Current guidance
suggests a minimum of two MDCTs of the chest,

Figure 4. Axial multidetector CT with a right-sided anterior


subcutaneous nodule (arrow), subsequently biopsied and
found to be the site of recurrence.

abdomen and pelvis in the first 3 years and regular serum


carcinoembryonic antigen tests, at least every 6 months
in the first 3 years [8]. Assessment of the anastomosis
should be included for recurrence and for extracolonic
disease (Figure 4). The presence of operable hepatic metastasis should also be discussed at local hepatobiliary
MDTs. If intracranial disease is suspected, contrastenhanced MRI of the brain should be offered.

Staging of rectal carcinoma


The current NICE guidance is to offer MRI to all
patients with rectal cancer to assess the risk of local recurrence, determined by anticipated resection margin,
tumour and lymph node staging. MRI can therefore guide
the selective use of neoadjuvant chemoradiotherapy to
optimise delayed surgical intervention after discussion
within the multidisciplinary cancer management teams.

MRI technique

Figure 3. Coronal multidetector CT demonstrating an ascending colon tumour with intussusception (arrow) as a complication
causing obstruction.
imaging.birjournals.org

As with all MRI examinations, patient preparation is


key. Patients should be fully informed and are positioned
supine on the scanner. Coronal and sagittal localisation
images are used to plan the high-resolution images.
Sagittal T2 weighted, fast spin-echo sequences enable
detection of the primary tumour. Large-field-of-view axial sections of the whole pelvis are also acquired. Highresolution T2 weighted axial sections through the rectal
cancer can then be acquired, but these must be carefully
aligned perpendicular to the long axis of the rectum and
at the level of the tumour in order to avoid partial volume
effects. While the referring clinician should indicate the
site of tumour, for low rectal cancers coronal imaging
should be employed to accurately depict the levators and
sphincter complex (Table 2).
The technique for image acquisition may vary, but
many centres recommend no bowel preparation or filling
of the rectum [9]. The use of contrast enhancement with
gadolinium is also not currently advocated [10]. Although the use of antispasmodic agents may sometimes
improve image quality, their use is not mandatory.
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M J Steward and D Murray


Table 2. MRI parameters for rectal cancer staging
Parameter

5 mm sagittal and axial

High-resolution oblique axial and coronal

TR sagittal (ms)
TR axial (ms)
TE sagittal (ms)
TE axial (ms)
Slices sagittal
Slices axial
Echo-train length
Field of view (mm)
Acquisitions sagittal
Acquisitions axial
Phase-encoding

5080
4018
132
80
23
20
23
250
3
2
Anteroposterior

5362
100
16
16
160
6
Inferosuperior

TE, echo time; TR, repetition time.


Parameters according to Brown et al, 2005 [9].

Interpretation of rectal MRI


A systematic approach to image interpretation aids accurate staging for rectal cancer. Classification of tumours
into ulcerating lesions, polypoid tumours or mucinous
tumours may help. Ulcerating lesions tend to grow circumferentially and may cause annular stenosis of the
bowel wall. Polypoid tumours tend to protrude into the
lumen and may be associated with a lower malignant
potential [1113]. Mucinous tumours (Figure 5) are associated with a worse prognosis in the rectum and can be
identified by their high T2 signal intensity mucin pools
within the tumour [14].
Patterns of invasion should also be noted. Poorly defined borders and an infiltrative pattern of growth are
associated with a worse prognosis, whereas an inflammatory response at the margin is more indicative of
a better prognosis [15].
The site of the tumour should be clearly stated: upper
third (more than 10 cm from the anal verge), middle third
(510 cm from the anal verge) and lower third (less than
5 cm from the anal verge). Measurement regarding its distal
edge to the puborectalis sling, its length over a craniocaudal
extent and its relation to the peritoneal reflection should be
documented. The invading edge of the tumour using circumference margins (from oclock to oclock) are also
useful.
The important distinction of a T3 lesion is based on the
presence of the tumour signal extending into the perirectal

fat. This broad-based or pushing nodular configuration of


an advancing T3 tumour margin is in continuity with the
intramural portion of the tumour. This needs to be distinguished from spiculation associated with the lower
signal intensity of fibrosis in order to avoid the overstaging
of T2 tumours.
T4 lesions involve invasion into an adjacent organ or
structure and those that have perforated the peritoneum
(Figures 6 and 7). Anterior invasion into the bladder or
uterus, lateral extension to the pelvic sidewall and posterior invasion to the sacrum should be evaluated. If the
tumour is in the lower third of rectum, infiltration of the
pelvic floor structures needs to be determined, although
invasion of the levator alone does not constitute T4
disease.
Extramural vascular invasion (Figure 8) is more easily
identified on MRI for rectal tumours than MDCT for colonic tumours. As the tumour grows into or along a recognisable vessel, this vessel should be identified (for example

Figure 6. High-resolution T2 weighted axial MRI with


Figure 5. Large-field-of-view T2 weighted axial MRI with
mucinous tumour. Note the high T2 signal (arrow).

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tumour recurrence invading prostate gland and right pelvic


sidewall (arrow).

Imaging 2013, 22, 20110078

Staging of colorectal cancer

Figure 7. Large-field-of-view T2 weighted axial MRI with T4


rectal tumour invading posterior bladder wall (arrow).

superior rectal vein) as well as whether the tumour


threatens the mesorectal fascia (within 1 mm of the fascia).
Lymph node staging with MRI is not solely reliant on
the size of the nodes. Criteria based on the outline of the
node and feature of signal intensity are more reliable
[16, 17]. The use of high-resolution imaging can help
classification. Lymph nodes with a smooth outline and
uniform signal intensity are considered to be benign. By
using these criteria, Brown and colleagues [16] reported
a sensitivity of 85% and specificity of 97%. This was
a retrospective study that achieved results that were
significantly better than using size criteria alone. When
the criteria were applied in a prospective study, agreement with histological stage was 85% [18]. More suspicious nodes have irregular outlines and mixed signal
intensities. The distinction between N1 and N2 is numerical: N1 includes one to three nodes, N2 includes four
or more nodes (Figure 9). Any lymph node within 1 mm
of the circumferential resection margin should also be
documented and also evaluated for malignant potential.
Similarly a record of the location and size of pelvic

Figure 9. High-resolution T2 weighted axial MRI of rectal


tumour with mesorectal lymph nodes (arrows), staged as N2.
Note the poorly defined borders and mixed signal characteristics.

sidewall lymph nodes, and whether they have any suspicious features, should be noted.
With the use of total mesorectal excision for complete
surgical excision of the primary tumour, the circumferential resection margin (CRM) needs to be identified
during interpretation (Figure 10). The CRM is formed by
the mesorectal fascia, which envelops the mesorectum
and constitutes the dissection plane in total mesorectal
excision. The MR images need to be obtained in a plane
perpendicular to the rectum and mesorectum, and these
oblique axial images will then correspond precisely with
the specimen resected [19].
Measurements are taken of the distance from the tumour to the mesorectal fascia, the potential CRM. If the
tumour lies within 1 mm of the mesorectal fascia, then
this is a potentially positive margin (Figure 11) [20]. The
risk of local recurrence can also be stratified according to
the characteristics of rectal tumours predicted by MRI
(Table 3).

Figure 8. High-resolution T2 weighted coronal MRI of mid/

Figure 10. High-resolution T2 weighted coronal MRI depicting

lower rectal tumour with extramural venous invasion (arrow).

the surgical approach (arrows) for total mesorectal excision.

imaging.birjournals.org

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M J Steward and D Murray

Figure 11. High-resolution T2 weighted axial MRI of a T3


rectal tumour extending anterior to the mesorectal fascia
below the level of the peritoneal reflection and involving the
circumferential resection margin (arrow).

The staging of low rectal tumours will involve assessment of the sphincter complex, and the ability to achieve
clear radial and distal margins is key to success. For these
low rectal tumours at or below the puborectalis sling, it
should be noted whether there is full-thickness invasion
of muscularis propria, invasion into the intersphincteric
plane or external sphincter [21]. If this is present extralevator abdominoperineal excision is indicated instead of
low anterior resection. Pelvic exenteration is reserved for
invasion beyond the external sphincter into ischiorectal
tissue.

Post-treatment MRI staging of rectal tumours


Pre-operative concurrent chemotherapy and radiation
therapy (CCRT) is now widely used in locally advanced
rectal cancer, as it has been shown to reduce the rate of
local recurrence and may permit sphincter-preserving
surgery [22, 23].
Poor pre-operative prognostic factors include infiltration into the mesorectal fat of more than 5 mm (T3b
disease) and mesorectal fascial involvement (within 1 mm
of the mesorectal fascia) [24, 25].

MRI has developed a role in assessing the response to


CCRT and restaging the tumour to plan further management. The restaging of the tumour by MRI aids the
multidisciplinary decision of whether to proceed to waitand-see policy (if there is a complete response), local excision including transanal endoscopic microsurgery
(TEMS; if it is now confined to the rectal wall), sphincter saving surgery (if the tumour has retracted from the
sphincter), total mesorectal excision (if the tumour has
regressed from the mesorectal fascia) or to withhold
radical surgery (if the tumour has progressed on CCRT).
Histologically the response is determined by the ratio
of viable tumour to fibrotic tissue in the specimen, with
treated tumours demonstrating replacement of tumour
cells by fibrous or fibroinflammatory tissue. Lack of active tumour necrosis but increased mucin production and
stromal mucin pools also determine response [26]. There
are various methods to assess tumour regression grade
(TRG), which are modifications of the Mandard scoring
system for oesophageal cancer [27]:
TRG 1
TRG 2
TRG 3
TRG 4
TRG 5

complete regression: low-signal fibrosis only; no


intermediate tumour signal
rare residual cancer cells scattered throughout
the fibrosis; greater than 75% fibrosis
50% tumour/fibrosis
residual cancer outgrowing fibrosis; less than
25% fibrosis
absence of regressive change; treated tumour
shows no fibrosis.

At MRI, tumour response manifests as a reduction in


tumour size and signal.
The signal characteristics of the main tumour mass as
well as the invading most peripheral part of the tumour
should be assessed relative to the pre-treatment scan and
relative to gluteal muscle signal. A reduction in the T2
signal indicates a fibrotic response (Figures 12 and 13) or

Table 3. Risk of local recurrence for rectal tumours as predicted


by MRI [2]
Risk of local
recurrence

Characteristics of rectal tumours predicted by


MRI

High

Threatened (,1 mm) or breached


resection margin OR
Low tumours encroaching onto
intersphincteric plane or with levator
involvement
Any T3b (.5 mm) or greater, in which the
potential surgical margin is not
threatened OR
Any suspicious lymph node not
threatening the surgical margin OR
Presence of extramural venous invasion
T1, T2 or T3a (,5 mm) involvement AND
No lymph node involvement

Medium

Low

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Figure 12. High-resolution T2 weighted axial MRI of T3


rectal tumour prior to neoadjuvant therapy. Note discontinuity of muscularis propria (arrow).

Imaging 2013, 22, 20110078

Staging of colorectal cancer

Figure 13. High-resolution T2 weighted axial MRI of rectal


tumour in Figure 12 with low-signal fibrosis (arrow) post
neoadjuvant therapy. This was a resected and pathologically
T3 tumour with 12 mm infiltration beyond the muscularis
propria.

a very high increased T2 signal can indicate a mucinous


response. These changes are listed below [28]:
Active tumour: intermediate signal intensity (higher than
that of muscle)
Tumour response: decreased signal intensity relative to
pre-CCRT findings, increased signal intensity relative
to pre-CCRT findings (higher than that of fat)
T0T2: complete disappearance of tumour (normal rectal
wall) or hypointense thickened rectal wall with or
without hypointense spiculations that extend to the
perirectal fat
T3: broad-based pushing or nodular configuration of
lateral tumour margin with signal intensity greater
than that of muscle extending into perirectal fat
T4: broad-based pushing or nodular configuration of
lateral tumour margin with signal intensity greater than
that of muscle extending into an adjacent structure or
viscus [28].
Tumour size can be assessed with Response Evaluation
Criteria In Solid Tumors (RECIST) (a reduction of at least
30% in the maximum diameter), although consistent
measurements are difficult in irregular rectal tumours.
Volumetric analysis is more reliable, with a reduction in
volume of 65% representing a partial response. A further
study suggested that a volume reduction of 70% had a
high positive predictive value and low negative predictive
value for distinguishing between responding and nonresponding tumours [29].
MRI staging following CCRT is complicated by the
superimposed changes due to the therapy, and accuracy
rates of 4754% for T stage, 6468% for N stage and 66%
for CRM assessment. The rectal wall often becomes
thickened, obscuring the individual layers, which prevents differentiation of T0, T1 and T2 tumours (classified
as yT0T2). MRI may overstage the desmoplastic inflammatory reaction produced by the CCRT, or may
misinterpret post-treatment rectal proctitis or ulceration.
MRI may understage tumours when active tumour cells
are present in a fibrotic scar. It is also difficult to
imaging.birjournals.org

Figure 14. Recurrent rectal tumour post chemotherapy and


radiation therapy with poor response with high apparent
diffusion coefficient values (arrow).

characterise an irradiated lymph node by conventional


morphological criteria, leading to overstaging.
There has been recent interest in diffusion-weighted
imaging to assess response by highlighting cellular density and integrity of the cellular membranes within the
treated tumour. The apparent diffusion coefficient (ADC)
values have been shown to initially rise, and then reduce
at the end of the treatment as the treatment-induced fibrosis causes a reduction in water mobility. Conversely,
high ADC values are related to a poor response (Figures
14 and 15) [30]. Contrast-enhanced MRI is also currently
under investigation, relying on demonstrating the increased microcirculation and angiogenic activity of
a more aggressive tumour.
Positron emission tomography (PET) has also been
used to assess disease response, relying on the metabolic
activity of malignant tissue rather than tumour shrinkage.
A reduction in the standardised uptake value of 66.2% has

Figure 15. Corresponding axial diffusion weighted image


(b-value, 1000 s mm22) demonstrating tumour (arrow).

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M J Steward and D Murray

been shown to be related to tumour response [31]. Its use is


limited by poor spatial resolution and also its inability to
differentiate post-therapy inflammatory change. However,
its other potential role is to detect unknown metastatic
lesions, which are potentially resectable.

Endorectal ultrasound and positron emission


tomography/CT in rectal tumours
Endorectal ultrasound (EUS) can be used as a modality
to stage rectal cancer if there is disease amenable to local
excision or if MRI is contraindicated. Two systematic
reviews [32, 33] have shown high sensitivity, specificity
and accuracy. There are some limitations in its use. Stenotic tumours or high rectal cancers situated 10 cm from
the anal verge are almost impossible to evaluate. The
presence of inflammatory reactions and desmoplastic
changes around tumours can also cause overstaging as
the changes cannot be differentiated from cancer infiltration [34, 35]. Endorectal sonogaphy is also limited in
the detection and characterisation of lymph nodes and is
unable to visualise the total extent of nodal disease within
the pelvis. There is significant interobserver variation in
the performance of EUS, and as a technique it is inherently
operator dependent.
The combination of metabolic activity with anatomical
localisation that can be achieved with PET/CT has had
some role in colorectal cancer management, including the
detection of small lesions up to 1 cm [36, 37]. In rectal
cancer subsequent examinations after neoadjuvant therapy have been used to assess residual disease [38]. Most
recently it is suggested PET/CT should be considered if
the CT scan shows possible extrahepatic metastases that
could be amenable to further radical surgery [2, 8].
Fluoro-2-deoxy-D-glucose (FDG) PET has several limitations in the assessment of colorectal cancer. It has a low
sensitivity for mucinous adenocarcinomas where the
metabolic activity is low. Partial volume averaging and
necrotic lesions may also cause false-negative results, and
incidental physiological bowel FDG uptake or inflammation
will produce increased tracer uptake. This can cause falsepositive findings that can mimic a tumour.

Conclusions
Advances in colorectal tumour staging are now established beyond just the detection of metastases. The use of
MDCT and MRI are central to multidisciplinary meetings
to plan treatment strategy and assess tumour response to
these treatments.

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