AJR 2002; 179:3-13
© American Roentgen Ray Society
Imaging in Oncology from
The University of Texas M. D. Anderson
Cancer Center |
Imaging in the Diagnosis, Staging, and Follow-Up of Colorectal Cancer
Revathy B. Iyer1,
Paul M. Silverman,
Ronelle A. DuBrow and
Chusilp Charnsangavej
1 All authors: Department of Diagnostic Radiology, Box 57, The University of
Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX
77030.
Received November 14, 2001;
accepted after revision January 9, 2002.
Address correspondence to R. B. Iyer.
Introduction
Colorectal cancer is a disease that is curable if detected early and
preventable if precursor adenomas are detected and removed. Approximately
130,000 new cases were diagnosed in the United States in 2000, and
approximately 56,000 deaths were attributed to the disease. The typical age at
which most patients are diagnosed is during the sixth and seventh decades of
life [1].
The risk factors for the development of colorectal cancer include dietary,
hereditary, and environmental influences. The activation of protooncogenes and
the inactivation of tumor suppressor genes eventually result in the
development of malignancy [2].
The adenoma—carcinoma sequence has also been well established. Most
colon cancers are thought to develop directly from adenomatous polyps. The
cumulative risk for developing invasive carcinoma in unresected polyps is 2.5%
at 5 years, 8% at 10 years, and 24% at 20 years
[2]. The malignant potential of
a polyp is determined by its size. Polyps greater than 2 cm have a greater
than 40% risk of being cancerous, whereas those less than 0.5 cm are
essentially at no risk for harboring malignancy. Other features of a polyp
that predispose to malignancy are villous architecture and degree of cellular
atypia and dysplasia [2] (Fig.
1A,1B).
Approximately 30% of colorectal cancers occur in the sigmoid, 25% occur in
the rectum, and 25% occur in the cecum and ascending colon
[2]. The remaining 20% of
cancers occur in the transverse and descending colon. Grossly, these tumors
may be large, necrotic, and polypoid or ulcerative, infiltrative lesions that
afford a worse prognosis. More distal cancers tend to infiltrate and have an
apple-core appearance (Fig.
2A,2B).
Tumors of the right colon can grow very large before causing symptoms such as
obstruction. Histologically, colon cancers are adenocarcinomas that form
moderately to well-differentiated glands that secrete varying amounts of mucin
[2]. In this review, we present
the imaging findings that may be encountered in the diagnosis, staging, and
follow-up of colorectal cancer.
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Fig. 2A. —59-year-old woman with colon cancer. Radiograph obtained
during double-contrast barium enema shows apple-core lesion
(arrowheads) in sigmoid colon. Note small filling defect
(arrow) in descending colon.
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Staging
Once a tumor is invasive, it can extend through the layers of the colonic
wall and invade adjacent structures
[2,
3]
(Fig. 3). Lymphatic,
hematogenous, and peritoneal spread may also occur. The overall prognosis and
outcome depend on the stage of the tumor at diagnosis. T1 lesions invade the
submucosa. T2 tumors involve the muscular layers. T3 tumors invade the
subserosa, and T4 lesions extend beyond the colon to involve adjacent
structures. Table 1 summarizes
the TNM classification system, established by the Union International Contre
Le Cancer [4], and
Table 2 lists the stage that
corresponds to the combined TNM classification and the modified Dukes'
classification.
The nodal pathways of spread for colon cancer are illustrated in
Figure 4
[2,
3]. Nodal spread from
carcinomas of the right colon follow along the marginal vessels of the cecum
and ascending colon and then along the ileocolic vessels to the root of the
superior mesenteric artery (Figs.
5A,5B
and
6A,6B).
Tumors of the proximal transverse colon tend to spread along the marginal
vessels on the mesocolic side of the colon (Fig.
7A,7B).
These marginal vessels in turn drain to the right or middle colic vessels and
to the root of the mesocolon, anterior to the head of the pancreas. Lymphatics
from the distal transverse colon and splenic flexure follow the left middle
colic vessels to the inferior mesenteric vein just caudal to the body and tail
of the pancreas. Cancers of the descending colon and sigmoid colon will spread
to nodes along the left ascending colic and sigmoidal vessels that can then be
followed to the origin of the inferior mesenteric artery
[5].
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Fig. 6A. —60-year-old man with colon cancer at hepatic flexure. Axial
CT scan of abdomen shows mass (M) at hepatic flexure and lymphadenopathy
(arrow) anterior to superior mesenteric vessels
(asterisks).
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Fig. 6B. —60-year-old man with colon cancer at hepatic flexure. Axial
CT scan of abdomen shows lymphadenopathy (arrow) followed along
gastrocolic trunk (GC) anterior to superior mesenteric vessels
(asterisks).
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Fig. 7B. —45-year-old man with colon cancer involving transverse colon.
Axial CT scan of abdomen shows lymphadenopathy (arrow) followed along
middle colic vessels (asterisk) in transverse mesocolon.
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Treatment
Complete surgical removal of tumor along with the regional lymphatics
affords the best prognosis. The typical surgical approach for proximal colon
cancers is right radical colectomy or extended right radical colectomy for
tumors involving the hepatic flexure or transverse colon. A left radical
colectomy is typically performed for tumors of the descending colon or
proximal sigmoid. Carcinomas of the rectosigmoid may be treated with anterior
or low anterior resection versus abdominoperineal resection depending on the
size and extent of tumor and the proximity to the anal sphincter
[2].
Neoadjuvant chemotherapy and radiation therapy are increasingly
administered preoperatively to downstage rectal tumors that are classified as
T3 or greater; this approach allows more sphincter-preserving low anterior
resections with a decreasing incidence of recurrence. Local recurrence rates
for stage II rectal cancer were approximately 30% and more than 50% for stage
III disease with surgery alone. The risk of local recurrence has been reduced
by 50% with the use of neoadjuvant therapy
[2,
6]. Most neoadjuvant
chemotherapy protocols use 5-fluorouracil with levamisole hydrochloride or
leucovorin. Preoperative radiation, combined with chemotherapy, for rectal
cancer is administered at doses on the order of 40-50 Gy
[2,
6].
Radiologic Evaluation
Imaging plays a role in determining the stage of disease at diagnosis,
which then dictates the appropriate therapy. Endoscopic sonography shows the
layers of the bowel wall and usually allows differentiation between the
submucosa and the muscularis propria and between the muscularis propria and
the surrounding fat, which provides an opportunity to determine the depth of
tumor penetration with an overall accuracy of 80-85%
[3,
7] (Figs.
8 and
9). Helical CT scans obtained
during the peak phase of mural enhancement using a slice collimation of 5 mm
or less can outline tumor and adjacent spread, and the reported sensitivity
for local invasion ranges from approximately 50% to 70%
[3].
Adequate luminal distention is essential for imaging and may be achieved
with water as a negative contrast agent
[3,
7]
(Fig. 10). For patients with
rectal tumors, T2-weighted MR imaging with an endorectal coil shows the bowel
wall layers and adjacent tissue involvement with an overall accuracy of
approximately 80% [3,
7]. All modalities are limited
in their ability to distinguish tumor from peritumoral edema and from
desmoplastic reaction, and none has a 100% accuracy
[7].
Nodal staging on the basis of imaging findings remains a challenge. On
cross-sectional imaging, size (>1 cm) remains the primary criterion for
predicting nodal metastasis using any modality, although it is well known that
size is not an ideal indicator of disease: Benign nodes may be enlarged, and
subcentimeter nodes may contain metastatic tumor
[3,
7].
Sonography, CT, and MR imaging also play a role in identifying sites of
distant metastatic disease, particularly in the liver because limited disease
spread to the liver can be resected for cure. Transabdominal sonography is the
least sensitive of the three modalities. Although intraoperative sonography
obviously cannot be used for screening, this technique is considered the most
sensitive means of detecting liver lesions, with a reported sensitivity of at
least 95% [3,
7].
Hepatic metastases derive their blood supply from the hepatic artery
system, whereas normal liver parenchyma is primarily supplied by the portal
vein system. CT arterial portography is, therefore, a very sensitive technique
for lesion detection. This procedure requires catheterization of the superior
mesenteric artery and intraarterial injection of contrast material, which
results in intense portal vein enhancement of the normal liver. Metastases
appear as filling defects as do perfusion defects, thus specificity is less
than perfect. Conventional, helical, or multidetector CT performed with IV
contrast material during the portal vein—dominant phase of hepatic
enhancement, approximately 60-70 sec after the start of a bolus administered
at a rate of 2-3 mL/sec, typically shows heterogeneous, ring-enhancing
metastases that are predominantly hypodense with respect to the surrounding
liver parenchyma (Fig. 11). Images obtained after a longer delay may not reveal evidence of disease
because lesions become isodense to the surrounding liver and are thus obscured
[3,
7]. Necrosis and calcification
of lesions may be noted (Fig.
12).
When compared with the surrounding liver parenchyma on MR imaging, hepatic
metastases from colorectal cancer typically show increased signal intensity on
T2-weighted images and decreased signal intensity on T1-weighted images. The
behavior of metastatic lesions after the administration of a contrast agent
such as gadopentetate dimeglumine into the extracellular space parallels the
behavior of lesions on CT after the administration of an iodinated contrast
agent (Fig.
13A,13B,13C).
Tissue-specific hepatobiliary contrast agents such as ferumoxides
(superparamagnetic iron oxide) and managenese dipyridoxyl diphosphate may
further increase the sensitivity of lesion detection by increasing
liver-to-lesion contrast [3,
8]. Ferumoxides are
phagocytized by the reticuloendothelial cells of the liver, which decreases
the signal intensity of the normal liver on T2-weighted images. Metastases
will not take up the agent and will appear relatively hyperintense compared
with the surrounding normal liver on T2-weighted images
[8] (Fig.
14A,14B).
Manganese dipyridoxyl diphosphate is incorporated into the hepatocytes;
therefore, normal liver parenchyma will show increased signal intensity on
T1-weighted images compared with metastatic lesions, which do not incorporate
the agent [8].
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Fig. 14B. —60-year-old man with colon cancer and liver metastasis. Axial
T2-weighted MR image of abdomen after ferumoxide administration shows
increased liver-to-lesion (arrow) contrast compared with
A.
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Follow-Up
The risk of recurrence varies according to the preoperative stage,
histology, and adequacy of tumor removal. Follow-up may include laboratory,
endoscopic, and imaging surveillance. Imaging may show recurrent tumor locally
or distant metastases (Figs.
15A,15B
and 16). Although early
studies suggested that MR imaging would be superior in differentiating
recurrent tumor from scarring in the operative bed, a more recent study has
dispelled this theory [7].
Inflammatory changes related to asymptomatic anastomotic leaks after low
anterior resection should be recognized
[9] (Fig.
17A,17B).
Immunoscintigraphy and positron emission tomography with FDG have shown early
promise in distinguishing recurrence from scar and in depicting distant
metastases [3,
7] (Figs.
18A,18B
and
19A,19B).
In some patients, locally recurrent disease in the pelvis may be resected for
cure. Given the increased soft-tissue resolution and multiplanar capabilities
of MR imaging, tissue planes surrounding a known recurrent tumor become more
apparent, which is especially important when resection is being contemplated
(Fig.
20A,20B,20C,20D).
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Fig. 15A. —67-year-old woman who presented with signs and symptoms of
bowel obstruction after having undergone right hemicolectomy for colon cancer.
Radiograph obtained during barium enema shows complete obstruction at
anastomosis (arrow).
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Fig. 15B. —67-year-old woman who presented with signs and symptoms of
bowel obstruction after having undergone right hemicolectomy for colon cancer.
Axial CT scan of abdomen shows recurrent mass (arrow) is causing
small-bowel obstruction.
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Fig. 17A. —49-year-old man who presented with anastomotic leak after
having undergone low anterior resection for colorectal cancer. Axial CT scans
of pelvis (A) and from barium enema (B) show presacral
collection (arrows), posterior to rectum (R), communicating with
rectosigmoid anastomosis (arrowheads).
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Fig. 17B. —49-year-old man who presented with anastomotic leak after
having undergone low anterior resection for colorectal cancer. Axial CT scans
of pelvis (A) and from barium enema (B) show presacral
collection (arrows), posterior to rectum (R), communicating with
rectosigmoid anastomosis (arrowheads).
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Fig. 18B. —70-year-old man who underwent right hemicolectomy for colon
cancer. Axial CT scan of abdomen shows adenopathy (arrow) in middle
colic nodal group anterior to superior mesenteric vessels
(asterisks), corresponding to findings on A, and subsequently
proven to be recurrent disease.
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Fig. 19A. —71-year-old man who presented for routine follow-up after
having undergone left hemicolectomy for colon cancer. Axial CT scan of abdomen
shows linear soft tissue (arrow) along Gerota's fascia.
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Fig. 19B. —71-year-old man who presented for routine follow-up after
having undergone left hemicolectomy for colon cancer. Positron emission
tomogram shows increased uptake (arrow) corresponding to lesion
revealed on A. Lesion was subsequently biopsied and proven to be
recurrent disease.
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Fig. 20A. —40-year-old man who presented with rising level of
carcino-embryonic antigen after having undergone low anterior resection for
rectosigmoid cancer. SPECT image shows uptake of radiolabeled anti-CEA
monoclonal antibody (arrow) in left side of pelvis.
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Fig. 20B. —40-year-old man who presented with rising level of
carcino-embryonic antigen after having undergone low anterior resection for
rectosigmoid cancer. Unenhanced axial CT scan of pelvis shows normal
findings.
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Fig. 20C. —40-year-old man who presented with rising level of
carcino-embryonic antigen after having undergone low anterior resection for
rectosigmoid cancer. Axial (C) and coronal (D) T2-weighted MR
images of pelvis show mass (arrow) adjacent to prostate.
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Fig. 20D. —40-year-old man who presented with rising level of
carcino-embryonic antigen after having undergone low anterior resection for
rectosigmoid cancer. Axial (C) and coronal (D) T2-weighted MR
images of pelvis show mass (arrow) adjacent to prostate.
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Cancer Screening
Because malignancies of the colon develop slowly over time, most often from
preexisting adenomas, screening is of great importance. The ideal screening
test should be safe, accurate, and inexpensive. Although no single examination
meets all these criteria for screening at this time, the following tests are
presently in use: fecal occult blood testing, flexible sigmoidoscopy, barium
enema, and conventional colonoscopy.
The air—contrast barium enema has been the radiologic means of total
colonic examination, providing a minimally invasive examination that is
inexpensive and requires no sedation. However, the performance and
interpretation of this examination result in wide variations in the reported
detection rate of lesions greater than 1 cm; detection rates range from as low
as 48% to as high as 90% [10,
11].
CT colonography or virtual colonoscopy holds promise as a screening tool
for colorectal adenomas with a reported sensitivity of 90% for polyps greater
than 10 mm [12]. After
insufflation of the colon with air or carbon dioxide has been performed, the
abdomen and pelvis are scanned during a single breath-hold, ideally using a
multidetector helical scanner with a 3- to 5-mm collimation and
reconstructions at 1- to 3-mm intervals. Scans are usually obtained with the
patient in the supine and prone positions. Two-dimensional images can then be
reviewed to identify colonic lesions, and three-dimensional reconstructions
with endoluminal perspective volume rendering can be used for problem-solving
or for fly-through viewing of the colon (Fig.
21A,21B,21C).
The quality of the bowel preparation and the adequacy of luminal distention
limit the effectiveness of the CT colonography technique.
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Fig. 21A. —58-year-old woman with breast cancer who presented for
routine colon screening. Two-dimensional axial CT scan (A) and
three-dimensional CT scan with endoluminal-perspective volume rendering
(B) of colon show 1-cm polyp (arrow) in rectum.
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Fig. 21B. —58-year-old woman with breast cancer who presented for
routine colon screening. Two-dimensional axial CT scan (A) and
three-dimensional CT scan with endoluminal-perspective volume rendering
(B) of colon show 1-cm polyp (arrow) in rectum.
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Fig. 21C. —58-year-old woman with breast cancer who presented for
routine colon screening. Photograph obtained at colonoscopy reveals same polyp
(arrow) as that shown in A and B and proven to be
tubulovillous adenoma with foci of high-grade dysplasia.
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CT colonography requires bowel preparation. Researchers are currently
focusing on the use of contrast agents and computer subtraction techniques to
identify fecal material in the colon
[13]. Fecal-tagging may
decrease the number of false-positive findings that occur when bowel cleansing
is suboptimal. Computer-aided diagnosis to more rapidly evaluate CT images of
the colon is also being studied. These more sophisticated approaches may
obviate colonic cleansing, thereby providing a faster, more palatable,
minimally invasive examination for the early detection of colon cancer and its
precursors.
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Introduction
Staging
