DOI:10.2214/AJR.06.0476
AJR 2007; 188:785-791
© American Roentgen Ray Society
CT Differentiation of Mucinous and Nonmucinous Colorectal Carcinoma
Eun Young Ko1,2,
Hyun Kwon Ha1,
Ah Young Kim1,
Kwon Ha Yoon3,
Chang Sick Yoo4,
Hee Cheol Kim4 and
Jin Cheon Kim4
1 Department of Diagnostic Radiology, Asan Medical Center, University of Ulsan
College of Medicine, 388-1 Poongnap-dong, Songpa-gu, Seoul 138-736,
Korea.
2 Present address: Department of Radiology and Center for Imaging Science,
Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul,
Korea.
3 Department of Radiology, Hospital of Wonkwang University, Iksan, Jeonbuk,
Korea.
4 Department of Surgery, Asan Medical Center, University of Ulsan College of
Medicine, Seoul, Korea.
Received April 4, 2006;
accepted after revision August 18, 2006.
Address correspondence to H. K. Ha
(hkha{at}amc.seoul.kr).
Abstract
OBJECTIVE. The purpose of this study was to evaluate the CT findings
that can help differentiate mucinous from nonmucinous colorectal
carcinoma.
MATERIALS AND METHODS. CT scans of 86 patients with pathologically
proven mucinous colorectal carcinoma were analyzed, and 105 consecutive
patients with nonmucinous colorectal carcinoma were also included as a control
group. CT findings were compared between the two groups with regard to the
bowel involvement patterns; patterns of contrast enhancement; and presence or
absence of bowel obstruction, intratumoral calcification, pericolic fat
infiltration, and local tumor extension to adjacent organs. Statistical
analyses were performed using the Student's t test and Pearson's
chi-square test.
RESULTS. Compared with nonmucinous carcinoma, mucinous carcinoma
showed more severe (2.41 ± 1.19 cm vs 1.94 ± 0.92 cm)
(p = 0.004) and more eccentric (22% vs 8%) (p = 0.025)
bowel-wall thickening. Heterogeneous contrast enhancement was more common in
mucinous than in nonmucinous carcinoma (83% vs 53%) (p = 0.001).
Mucinous carcinoma showed more areas with hypoattenuation (p =
0.001), and the solid portion of mucinous carcinoma showed less enhancement
than that of nonmucinous carcinoma (p = 0.001). Presence of
intratumoral calcification was more frequent in mucinous carcinoma (21% vs 5%)
(p = 0.001). Heterogeneous enhancement showed the highest sensitivity
(82.6%) but moderate specificity (55.9%) in diagnosing mucinous carcinoma.
Tumors with four or more CT findings with a statistically significant
difference were mostly mucinous carcinoma, and the specificity was 87%.
CONCLUSION. CT is useful in the differentiation of mucinous from
nonmucinous colorectal carcinoma.
Keywords: cancer • colon • CT
Introduction
Mucinous colorectal carcinoma is a histologic subtype of
adenocarcinoma characterized by abundant extracellular mucin production
[1,
2]. Although clearly not
established yet, some variations exist in the amount of extracellular mucin
for the definition of mucinous colorectal carcinoma, which range between 50%
and 80%
[3-8].
Compared with nonmucinous carcinoma, mucinous carcinoma has been known to have
a propensity for higher incidence of lymph node metastasis, venous and
lymphatic invasions, local recurrence, and distant metastasis. Consequently,
the prognosis is worse
[5-10].
Therefore, mucinous carcinomas require more aggressive surgical excision, with
wide margins, extensive lymph node dissection, and complete dissection of
tumor extending into adjacent structures, than do nonmucinous carcinomas
[11,
12].
In standard daily practice, a biopsy is required to determine mucinous or
nonmucinous tumors, and CT or MRI is usually performed for tumor staging.
Because mucinous carcinomas have somewhat different tumor behaviors from the
nonmucinous type, imaging interpretation with knowledge of the tumor type may
improve tumor staging. Despite the importance of biopsy to determine tumor
type, sometimes pathologic reports on biopsy specimens lack an exact
description of the tumor type in colorectal carcinomas, although after
resection these tumors may be proved to be mucinous. In other words, imaging
diagnosis can be more useful than biopsy in certain instances to determine the
tumor type.
In fact, there have been some efforts to differentiate mucinous from
nonmucinous carcinoma with MRI
[3,
4]. On T2-weighted images,
mucinous colorectal carcinomas show high signal intensity due to the presence
of abundant extracellular mucin. Although MRI appears to be useful for the
differentiation of both types of carcinomas, in general CT is much more widely
used as the initial technique of choice for patients with colorectal cancer in
many institutions. Unfortunately, to our knowledge, there has been no report
regarding CT differentiation between colorectal mucinous and nonmucinous
carcinoma. Thus, the aim of this study is to differentiate mucinous from
nonmucinous colorectal carcinoma on CT.
Materials and Methods
Ninety-one patients with mucinous adenocarcinoma of the colon and rectum
were selected at two institutions (Ulsan University Hospital and Hospital of
Wonkwang University) during an 8-year period; and as a control group, 171
consecutive patients with nonmucinous adenocarcinoma of the colon and rectum
during a 3-month period in one institution (Ulsan University Hospital) were
included in this retrospective study. CT was performed in 87 patients with
mucinous and 122 patients with nonmucinous carcinomas. We excluded 18 patients
who showed negative CT findings due to small sizes of the tumors (one case of
mucinous and 14 cases of nonmucinous carcinoma) and who underwent CT without
enhancement (three cases of nonmucinous carcinoma). Therefore, a total of 86
cases of mucinous and 105 cases of nonmucinous colorectal carcinomas
constituted the basis of our study. All patients were pathologically confirmed
by surgery (n = 173) or colonoscopic biopsy (n = 18). The
study population (n = 191) consisted of 116 men and 75 women, and the
mean age was 58 years with an age range of 23-85 years. The pathologic
diagnosis of mucinous carcinoma was made according to the criteria that at
least 50% of the tumor was composed of extracellular mucin.
CT examinations were performed with a Somatom Plus-S scanner (Siemens
Medical Solutions), HiSpeed CT/i (GE Healthcare), or LightSpeed QX/i (GE
Healthcare). Images were obtained with a helical acquisition from the top of
the diaphragm to the anal verge in a craniocaudal direction by using 7- to
8-mm collimation, 10-13 mm/s table speed during a single breath-hold, and a 7-
to 8-mm reconstruction interval. Conventional IV contrast enhancement was
performed with scanning 60 seconds after injection of 120-130 mL of nonionic
contrast material (iopromide [Ultravist 370, Schering]) through the
antecubital vein at a rate of 3 mL/s at the first institution and with
scanning at 65-70 seconds after injection of 120-150 mL of nonionic contrast
agent (iopamidol [Iopamiro 300, Bracco]) at a rate of 2.5-3.0 mL/s with 10-mm
slice thickness at the second institution.
Retrospective review of CT images was performed in consensus by two
radiologists who were blinded to the pathologic results. Site and length of
involved segment; types of morphologic features (bowel-wall thickening or
protruding mass); size of the mass or thickness of involved bowel wall;
patterns of bowel-wall thickening (even or uneven, concentric or eccentric);
patterns of contrast enhancement (homogeneous or heterogeneous) of the lesion;
the degree of pericolic fat infiltration; the presence or absence of
intratumoral calcification, bowel obstruction, and regional lymphadenopathy;
and direct invasion of adjacent organs were evaluated.
The degree of contrast enhancement in the solid portion of the tumor was
compared with that of the normal bowel wall. In cases with a heterogeneous
mass, the extent of hypoattenuated area within the tumor was graded into three
groups: less than one third, equal to or greater than one third but less than
two thirds, and equal to or greater than two thirds of the tumor. Pericolic
fat infiltration was graded according to the extent of infiltration: less than
1 cm around the tumor, grade 1; equal to or greater than 1 cm and less than 3
cm, grade 2; and equal to or greater than 3 cm, grade 3.
We used the Student's t test and Pearson's chisquare test for
statistical analyses. We also investigated the usefulness of CT findings that
had a statistically significant difference between the two types of tumor by
evaluating the sensitivities, specificities, and diagnostic accuracies for
each CT parameter. Institutional review board approval and informed consent
were not required for this retrospective study.
Results
Comparison of CT findings between mucinous and nonmucinous carcinomas is
shown in Table 1. Both tumor
types involved the rectosigmoid area most frequently. There was no difference
in the involved sites between mucinous and nonmucinous carcinomas. Compared
with nonmucinous carcinomas, mucinous carcinomas involved the cecum and
ascending colon to some extent, but the involvement was statistically not
significant (p = 0.117). In morphologic features, the annular
wall-thickening type was more frequently seen than the mass-forming type in
both mucinous and nonmucinous carcinomas. The length of the involved segment
in the annular wall-thickening type was similar in both mucinous and
nonmucinous carcinomas. The size of the masses in the mass-forming type of
mucinous carcinoma was larger than in nonmucinous carcinoma, but there was no
statistically significant difference (p = 0.943).
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Fig. 3 —62-year-old woman with mucinous carcinoma in cecum and
proximal ascending colon. CT scan shows eccentric bowel-wall thickening along
with evidence of exophytic tumor growth posteriorly (asterisk). Large
metastatic lymph node (arrow) is noted in medial side of tumor.
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However, mucinous carcinomas showed more severe (p = 0.004) (Figs.
1 and
2) and more eccentric
(p= 0.025) (Figs. 3
and 4) bowel-wall thickening.
Atypical morphologic features, such as a large polypoid lesion with a broad
base, combined annular wall thickening and a partial polypoid lesion, a large
exophytic mass, or eccentric wall thickening without narrowing of the bowel
lumen, were more commonly seen in mucinous carcinomas (n =6) than in
nonmucinous carcinomas (n =1) (Fig.
5A,
5B). Heterogeneous contrast
enhancement of the tumor was much more commonly seen in mucinous carcinomas
than in nonmucinous carcinomas (p = 0.001). A statistically
significant difference was also noted in the extent of hypoattenuated areas
within tumors (p = 0.001). Nonmucinous carcinomas usually showed a
hypoattenuated area of less than one third of the tumor, whereas mucinous
carcinomas showed a hypoattenuated area equal to or greater than two thirds of
the tumor (Figs. 6A,
6B and
7).
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Fig. 6B —69-year-old woman with mucinous carcinoma in proximal transverse
colon. Hypoattenuated area is greater than two thirds of tumor
(asterisk), and enhancement in solid portion of tumor is less than
that of normal bowel wall (arrow).
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Fig. 7 —34-year-old woman with nonmucinous carcinoma in proximal
ascending colon. CT scan shows bowel-wall thickening is relatively homogeneous
and greater than that of normal bowel wall. Hypoattenuated area is less than
one third of tumor. Pericolic fat infiltrations with small regional lymph
nodes are also noted (arrows).
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The degree of contrast enhancement in the solid portion of the tumor was
equal to or greater than that of the normal bowel wall in nonmucinous
carcinomas, but it was less than that of the normal bowel wall in mucinous
carcinomas (p = 0.001) (Figs.
6A,
6B and
7). The presence of
intratumoral calcification was more frequently seen in mucinous carcinomas
(21% vs 5%); most calcifications were small and punctate (Fig.
8A,
8B). Peritoneal seeding was
more frequent in mucinous carcinomas (7/86) than nonmucinous carcinomas
(1/105) (p =0.014). However, the presence of bowel obstruction (8/86
vs 12/105) (p = 0.203), peritumoral fat infiltrations more than 1 cm
(29/86 vs 37/105) (p = 0.609), lymph node metastasis (34/86 vs
50/105) (p = 0.457), and direct invasion of adjacent organs (4/86 vs
7/105) (p = 0.313) were not significantly different between mucinous
and nonmucinous carcinomas.
In the differential diagnosis on CT, the sensitivities, specificities, and
diagnostic accuracies of CT findings that showed a statistically significant
difference between mucinous and nonmucinous carcinomas are listed on
Table 2. Heterogeneous contrast
enhancement of the tumor showed the highest sensitivity (82.6%) with 55.9%
specificity, and the presence of intratumoral calcification showed the highest
specificity (78.2%) with 20.9% sensitivity. Diagnostic accuracies of CT
parameters, such as bowel-wall thickening greater than 2 cm, eccentric
bowel-wall thickening, heterogeneous contrast enhancement of the tumor, poor
contrast enhancement of the solid component of the tumor, a large area of
hypoattenuation within tumor, and intratumoral calcification, ranged between
58.2% and 62.8%. When the presence of any findings that were shown to be
statistically significant in the current study was considered diagnostic of
mucinous carcinoma, the sensitivity of CT was 93% (80/86), whereas specificity
was 50.6%. When the cases with four or more of these CT findings were
diagnosed as mucinous tumor, the specificity was increased to 87% (20/23),
whereas sensitivity decreased to 23.3% (20/86).
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TABLE 2: Sensitivity, Specificity, and Diagnostic Accuracy of CT Findings in
Differentiating Mucinous from Nonmucinous Colorectal Carcinomas
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Discussion
There have been a few reports about the MRI findings of mucinous colorectal
carcinoma [3,
4,
13-16].
Studies for MRI findings of colorectal mucinous carcinoma, including in vitro
study, revealed that signal intensity of colorectal tumors varied depending on
the histologic components of the tumor, and mucinous colorectal carcinomas
showed high signal intensity on T2-weighted images due to the presence of
abundant extracellular mucin. The proportion of the high signal intensity
within the tumor correlated well with the amount of intratumoral mucin pools
[3,
4,
14,
15]. In addition, colorectal
mucinous carcinomas showed either peripheral or heterogeneous enhancement on
MR images, as has been seen in mucinous tumors at other sites
[3,
13]. Some investigators
considered MRI superior to CT because of its ability to differentiate mucinous
from fibrotic components of tumors; both components showed hypoattenuation on
CT scans [4]. But MRI is not
routinely performed as an initial diagnostic evaluation of colorectal
carcinoma in most institutions.
CT is widely accepted as a basic and accurate method for preoperative
evaluation of colorectal carcinoma. However, to our knowledge, no
investigation has been made regarding the CT findings of colorectal mucinous
carcinoma in comparison with nonmucinous carcinoma. In fact, there have been
some reports about the radiologic findings of mucinous carcinoma in sites
other than the colorectum, such as mucinproducing hepatobiliary, pancreatic,
and gastric carcinomas or metastatic tumors of the liver or ovary from
mucinous colon cancer
[17-19].
According to our results, the presence of CT findings, such as bowel-wall
thickening greater than 2 cm, eccentric bowel wall thickening, heterogeneous
contrast enhancement of the tumor with poor enhancement of the solid portion,
a large area of hypoattenuation, and intratumoral calcification, indicates the
high likelihood of the mucinous type of colorectal carcinoma. Diagnostic
accuracies of these CT parameters in differentiating mucinous from nonmucinous
carcinomas ranged between 58.2% and 62.8%. Depending on the number of these
parameters, the sensitivity of CT ranged from 23.3% to 93% with 50.6% to 87%
specificity.
Both heterogeneous enhancement patterns and large areas (greater than two
thirds of the tumor) of hypoattenuation were more frequently seen in mucinous
colorectal carcinomas, as has been seen in mucinous carcinomas of other sites.
A hypoattenuated area on a single-phase CT scan can also be caused by necrotic
tissue of the tumor, fibrous stroma, or abundant extracellular mucin
components. Delayed enhanced CT scans obtained more than 5 minutes after
contrast injection can be helpful in differentiation of the areas of
extracellular mucin components from fibrous lesions, but large areas of
necrosis in poorly differentiated nonmucinous carcinoma are still difficult to
differentiate [4,
19,
20].
In contrast with the previous report
[3] in which the difference of
mucinous and nonmucinous colorectal carcinoma on MRI was only in the
peripheral contrast enhancement pattern but the tumor-to-tissue
contrast-enhancement ratio was not useful, our study results showed a
statistically significant difference between the degree of contrast
enhancement in the solid portion of mucinous and nonmucinous carcinoma. The
solid portion of mucinous carcinoma was enhanced less than that of the normal
bowel wall, whereas the solid portion of nonmucinous carcinoma was enhanced
equal to or greater than that of the normal bowel wall. The exact reason for
this discrepancy of results [3]
is not clear, but it is probably caused by the different mechanisms of
enhancement between CT and MR contrast agents.
Similar to the MRI findings
[3], on CT scans, mucinous
colorectal carcinomas showed a thicker colonic wall than did nonmucinous
carcinomas, and the thickened wall appeared to be more uneven and eccentric.
Calcifications were more frequently seen in mucinous carcinomas than in
nonmucinous carcinomas—in about one fifth of mucinous carcinomas but in
only one in 20 nonmucinous carcinomas. Because unenhanced scans were not
obtained in most CT studies of patients with colorectal carcinoma, the
frequency of intratumoral calcifications in mucinous carcinomas is expected to
be higher than our result.
Although not statistically significant, atypical morphologic features, such
as a broad-based polypoid lesion, combined partially polypoid and partially
wall-thickening pattern, or a large eccentric mass without significant
narrowing of bowel lumen, were more commonly seen in mucinous carcinomas. Our
observation was in accordance with the results of other investigators in which
the macroscopic characteristics of mucinous colorectal carcinoma tended to be
exophytic, partially polypoid lesions with a broad base, and not pedunculated
[1].
In fact, there has been no sufficient explanation for these unusual gross
features of mucinous carcinomas in the literature. Histopathologically,
nonmucinous carcinomas usually consist of glands combined with solid sheets of
malignant cells, but mucinous carcinomas chiefly consist of large pools of
extracellular mucin lined with columns of malignant cells, cords, and vessels
that give rise to a typical meshlike internal structure
[3,
21]. Furthermore, in contrast
to nonmucinous carcinomas, mucinous carcinomas frequently lack an inflammatory
response around the mucus deposits, have scanty desmoplastic reaction, and
sometimes have various sizes of pericolic tumor nodules of gelatinous
components even larger than the primary tumor or a small mucosal tumor with
extensive submucosal and muscular spread. We presume that such different
histopathologic features might be the primary causes of the high incidence of
atypical CT findings.
One limitation of this study is that the images were acquired using 7- to
10-mm collimation helical CT, and improvements in technology with
thinner-slice MDCT will improve visualization, characterization, and
differentiation of colorectal carcinoma. We conclude that CT is highly useful
in the differentiation of mucinous from nonmucinous colorectal carcinoma.
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Abstract
Introduction
