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Journal of Computer Assisted Tomography

27(1):48–55
© 2003 Lippincott Williams & Wilkins, Inc., Philadelphia

Accuracy in Differentiation of Mucinous and Nonmucinous


Rectal Carcinoma on MR Imaging

Myeong-Jin Kim, Jeong Seon Park, Sung Il Park, Nam Kyu Kim, Joo Hee Kim, Hee Jung Moon,
Young Nyun Park, and Won Ho Kim

Purpose: The purpose of this work was to determine the diagnostic accuracy of
MRI for the differentiation of mucinous and nonmucinous carcinomas in patients with
rectal carcinomas.
Method: Seventy-six patients with pathologically proven rectal adenocarcinomas
were evaluated with MRI. Both T2-weighted fast spin echo and T1-weighted spin echo
images were independently reviewed by two radiologists who were blinded for tumor
histology. Of the 76 cases, mucin pools were found in 28 (37%), and 16 had a mucin
pool occupying ⱖ50% of the tumor (mucinous carcinoma). The sensitivity, specificity,
accuracy, and positive and negative predictive values of distinguishing between mu-
cinous and nonmucinous carcinomas were calculated. The interobserver agreement
was estimated using ␬ statistics.
Results: The accuracies of the diagnosis of mucinous carcinoma were 97% for
Radiologist 1 and 96% for Radiologist 2. The sensitivities and specificities for diag-
nosing a mucinous carcinoma were 94 and 98% for Radiologist 1 and 100 and 95% for
Radiologist 2, respectively. Interobserver agreement was good (␬ ⳱ 0.61) for the
identification of a mucin pool and was excellent (␬ ⳱ 0.81) for the diagnosis of a
mucinous carcinoma.
Conclusion: Differentiation of mucinous and nonmucinous rectal carcinoma is
highly accurate on preoperative MRI.
Index Terms: Magnetic resonance imaging—Rectum—Neoplasms, rectal—
Adenocarcinoma, mucinous.

A mucinous carcinoma is a subtype of adenocarci- nosis than nonmucinous carcinomas (4–10) and that they
noma containing abundant extracellular mucin within the are also poor candidates for local excision even if con-
tumor (1–3). The amount of mucin required to warrant a fined to the muscularis propria (11). Preoperative iden-
diagnosis of mucinous carcinoma, as set by the World tification of the mucinous type, therefore, is useful for
Health Organization, is at least ⱖ50% of the mucin pool treatment planning in cases of rectal carcinoma. How-
occupying the tumor mass (1). Previous reports have ever, it is sometimes difficult to locate the mucin or
shown that mucinous carcinomas of the rectum have a estimate its content with a small amount of a biopsy
higher rate of local recurrence and a less favorable prog- specimen (3,12). Therefore, it will be useful if preopera-
tive imaging can accurately predict the histologic type on
a preoperative imaging modality.
Previous reports have demonstrated that a mucinous
carcinoma may show a characteristic high signal inten-
From the Departments of Diagnostic Radiology (M.-J. Kim, J. S. sity on T2-weighted fast spin echo MR images and that
Park, S. I. Park, J. H. Kim, and H. J. Moon), Surgery (N. K. Kim), and the high signal intensity corresponds to the tumor mucin
Pathology (Y. N. Park), Brain Korea 21 Project for Medical Science
(M.-J. Kim), and Division of Gastroenterology, Department of Internal pool (12,13). However, the diagnostic accuracy of MRI
Medicine (W. H. Kim), Yonsei University College of Medicine, Seoul, for distinguishing mucinous carcinomas from nonmuci-
Republic of Korea. Address correspondence and reprint requests to Dr. nous carcinomas has not been assessed in a large series.
M.-J. Kim at Department of Diagnostic Radiology, Severance Hospital, The purpose of this study was to determine the diagnos-
Yonsei University College of Medicine, Seodaemun-ku Shinchon-dong
134, Seoul, Republic of Korea, 120-752. E-mail: kimnex@yumc.yonsei.ac.kr
tic accuracy of MRI for the differentiation of mucinous
This work was supported by the Yonsei University Research Fund of and nonmucinous rectal carcinomas on preoperative
2002. MRI.

48
MRI OF MUCINOUS/NONMUCINOUS RECTAL CARCINOMA 49

TABLE 1. Sensitivity, specificity, and accuracy of diagnosis of mucinous carcinoma


Diagnosis of mucinous carcinoma Identification of mucin pool
(n ⳱ 16) (n ⳱ 28)
Radiologist 1 Radiologist 2 Radiologist 1 Radiologist 2
True positive 15 16 19 28
True negative 59 57 45 39
False negative 1 0 9 0
False positive 1 3 3 9
Total 76 76 76 76
Accuracy 0.97 0.96 0.84 0.88
Sensitivity 0.94 1.00 0.68 1.00
Specificity 0.98 0.95 0.94 0.81
Positive predictive value 0.94 0.84 0.86 0.76
Negative predictive value 0.98 1.00 0.83 1.00

MATERIALS AND METHODS or suspected rectal carcinoma and subsequently under-


went surgery. There were 40 men and 36 women with
This study included 76 patients who were referred for ages ranging from 27 to 80 years (mean 59 years).
MR examination for the preoperative staging of known Two pathologists who had no knowledge of the MR

FIG. 1. A 57-year-old woman with a mucinous carcinoma initially diag-


nosed as nonmucinous adenocarcinoma. A: The axial fast spin echo T2-
weighted image depicts a large area of hyperintensity extending to the
perirectal space, suggestive of a mucin pool (arrow). Both radiologists in-
terpreted the tumor as a mucinous carcinoma. B: On the axial spin echo
T1-weighted image, the tumor shows signal intensity similar to the normal
rectum or muscles. C: Coronal fast spin echo T2-weighted images show the
tumor extending into the perirectal fat plane. D: Review of the pathologic
slide showed a large mucin pool volume (arrows); hence, the diagnosis was
changed to mucinous carcinoma. Hematoxylin/eosin; no magnification.

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50 M.-J. KIM ET AL.

findings jointly reviewed retrospectively the histopatho- viewed the films in a random order and without prior
logic findings in all patients, with a special emphasis on knowledge of the histologic tumor type. Both radiolo-
the mucin content of the mucinous carcinoma. Although gists regarded the areas of high signal intensity within
the original pathologic reports revealed mucin pools the tumor on T2-weighted images as being indicative of
within the tumors of 18 patients, a mucin pool was de- a mucin pool (12,13). A high signal intensity was defined
tected in 10 additional cases upon reexamination. There- as a signal intensity that was similar to or brighter than
fore, 28 patients (37%) were found to have mucin pools the perirectal fat on the fast spin echo T2-weighted im-
within the tumor, and among these, 16 (21%) cases ful- ages. Each observer recorded whether the tumors con-
filled the criterion of mucinous rectal carcinoma, having tained a mucin pool and determined the histologic type
a content of ⱖ50% of extracellular mucin. Of these 16 of the tumor as “mucinous” or “nonmucinous” according
patients, there were 5 women and 11 men between 27 to the same criteria used for histologic diagnosis. Al-
and 79 years old, with a mean age 53 years. though the assessments were made on the T2-weighted
MRI was performed with a 1.5 T system (Horizon; GE image findings, the T1-weighted images were viewed
Medical Systems, Milwaukee, WI, U.S.A.) in all pa- simultaneously.
tients, using a phased-array pelvic coil. The axial, sagit- Sensitivity, specificity, positive predictive value, and
tal, and coronal T2-weighted (4,800–7,500/102 ms) im- negative predictive value for the diagnosis of mucinous
ages were obtained using a fast spin echo sequence with carcinoma and the identification of mucin pools in the
the following parameters: a 20 to 24 × 20 to 24 cm field tumor were separately calculated for each radiologist. ␬
of view, two signals averaged, a 512 × 256 matrix, an statistics were used to estimate the level of agreement
echo train length of 16, a bandwidth of 31.3 kHz, and a between the two radiologists in identification of a mucin
5 mm section thickness with a 1.5 mm gap. Axial T1- pool and diagnosing a mucinous carcinoma. ␬ values of
weighted images were also obtained using a spin echo >0 were considered to indicate a positive correlation.
sequence (400–500/8–10 ms, matrix size 256 × 192) with Values up to 0.4 were considered to indicate a marginal
the same field of view, scan thickness, and gap as used correlation, values of 0.41–0.7 a good correlation, and
for the T2-weighted axial images. Because the tumor was values of >0.7 an excellent correlation.
better defined in the distended rectal lumen, tap water
was administered using a rectal tube, and the rectum was
filled until the patient indicated discomfort. The normal RESULTS
volume used was between 200 and 500 mL. To minimize
peristalsis and to alleviate rectal spasm, 20 mg of sco- The accuracy, sensitivity, specificity, positive predic-
polamine butylbromide (Buscopan; Boehringer Ingel- tive value, and negative predictive value for the identi-
heim, Germany) was injected intravenously. fication of a mucin pool and the diagnosis of a mucinous
Two radiologists with different experience (Radiolo- carcinoma are presented in Table 1. Interobserver agree-
gist 1, 8 years; Radiologist 2, 1 year) independently re- ment was good (␬ ⳱ 0.61) for the detection of a mucin

FIG. 2. False-negative diagnosis of mucinous carcinoma by Radiologist 1 in a 67-year-old man. Axial (A) and sagittal (B) fast spin echo
T2-weighted images depict an area of hyperintense mucin pool (arrows). Both radiologists identified mucin pools in the tumor. Radiologist
2 estimated the volume of the mucin pool as >50% of the tumor, which agreed with the results of the pathologic examinations. Radiologist
1 judged that the mucin pool volume was insufficient for a diagnosis of mucinous carcinoma.

J Comput Assist Tomogr, Vol. 27, No. 1, 2003


MRI OF MUCINOUS/NONMUCINOUS RECTAL CARCINOMA 51

pool and was excellent (␬ ⳱ 0.81) for the diagnosis of a not in the tumor, was regarded as a mucin pool by Ra-
mucinous carcinoma (Fig. 1). diologist 2. Radiologist 1 correctly distinguished the tu-
In the diagnosis of a mucinous carcinoma, false- mor and the peritumoral edema in this case (Fig. 4).
negative diagnosis was rendered in one case by Radiolo- In regard to identifying the mucin pools in the tumors,
gist 1 and none by Radiologist 2. In the case that Radi- there were nine false-negative results for Radiologist 1
ologist 1 rendered a false-negative diagnosis, the pres- and none for Radiologist 2. In all nine cases, the propor-
ence of the mucin pool was correctly identified; tion of the mucin pools in the tumors was insufficient for
however, the estimation of the mucin pool volume was a diagnosis of mucinous carcinoma. Therefore, Radiolo-
discordant with the pathologists’ determination (Fig. 2). gist 1 correctly judged all nine cases as nonmucinous
False-positive diagnoses of mucinous carcinoma were carcinomas, whereas Radiologist 2 falsely judged one of
rendered in three cases: one by Radiologist 1 and three them as mucinous carcinoma. A false-positive result for
by Radiologist 2 (one case for both radiologists). Among the identification of mucin pool was made in 10 cases: 3
the three cases, mucin pools were detected in the patho- for Radiologist 1 and 9 for Radiologist 2 (2 cases for
logic specimens in two cases, but pathologists estimated both). In these cases, intratumoral congestion or abscess,
the mucin pool volume to be <50% of the tumor volume liquefactive necrosis, mural edema in the adjacent rectal
(Fig. 3). Therefore, the estimation of the mucin pool wall, and entrapped fluid between the tumor and the
volume was discordant between the radiologists and pa- adjacent rectal wall were the causes of the false-positive
thologists in these two cases. In the remaining one, sub- identification of mucin pools (Fig. 5). However, the high
mucosal inflammatory edema in the adjacent rectal wall, signal intensity portion that was falsely interpreted as a

FIG. 3. False-positive diagnosis of mucinous carcinoma in a 45-year-old man.


Axial (B), sagittal (B), and coronal (C) fast spin echo T2-weighted images depict an
area of hyperintense mucin pool (arrows) and a relatively hypointense nonmuci-
nous component (arrowheads). Both radiologists interpreted the tumor as mucin-
ous carcinoma. At the pathologic examination (D), foci of the mucin pools were
seen in the tumor (arrows), but pathologists judged that the mucin pool volume
was insufficient to define the tumor as mucinous. Hematoxylin–eosin stain; no
magnification.

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52 M.-J. KIM ET AL.

FIG. 4. A 70-year-old woman with a nonmucinous carcinoma. Sagittal (A) and coronal (B) fast spin echo T2-weighted images. Radiologist
2 considered the areas of the high signal intensity of submucosal edema in the adjacent rectal wall as a mucin pool (arrowheads) and
rendered a false-positive diagnosis of mucinous carcinoma. Radiologist 1 correctly identified the hypointense tumor narrowing a segment
of the rectum (arrows) in the absence of a hyperintense mucin pool. Hence, the tumor was correctly interpreted as a nonmucinous tumor
by Radiologist 1 because the extratumoral location of the high signal intensity was correctly identified.

mucin pool comprised only a small portion of the tumor The MR findings of colorectal mucinous carcinoma of
in most cases. Therefore, for Radiologist 1, a true- colorectum and other organs such as the liver, pancreas,
negative diagnosis was made in determining the histo- and prostate have been previously reported (22–25). Kim
logic type of the tumor in all three cases. For Radiologist et al. (12) studied 12 cases of colorectal carcinoma con-
2, a false-positive diagnosis of mucinous carcinoma was taining various amounts of mucin pools. In that study, all
made in one of them. mucinous carcinomas, containing mucin pools of >50%
of the tumor by definition, showed hyperintense area on
T2-weighted MR images, which correlated well with the
DISCUSSION
area of the mucin pool within the tumor. Hussain et al.
There has been some controversy regarding the prog- (13) also studied 9 mucinous and 17 nonmucinous car-
nostic significance of mucinous carcinomas of colon and cinomas with MRI. They found that the relative signal
rectum (14,15). The different results obtained may be intensity of the tumor was significantly higher in the
explained by inferences made from the site or based mucinous compared with the nonmucinous tumors. With
upon the DNA microsatellite instability of the tumor this finding, they suggested that MRI can help distin-
(16). Mucinous carcinomas of proximal colon are likely guish between mucinous and nonmucinous carcinomas.
to have high microsatellite instability and to be diploid However, this has not been demonstrated yet in a larger
and therefore associated with a good prognosis (17,18). study.
However, mucinous carcinomas of the rectum are likely Our study shows that both experienced and less expe-
to be DNA microsatellite stable and aneuploid. More- rienced radiologists accurately distinguish mucinous car-
over, they tend to show more extensive invasion at the cinoma from nonmucinous carcinoma with MRI. In-
time of presentation and to have a poorer prognosis than terobserver agreement was also excellent in the differen-
the nonmucinous type (19,20). The production of mucus tiation of mucinous and nonmucinous carcinoma. There
under pressure allows the cancers to separate tissue were three false-positive and one false-negative case for
planes in the bowel wall and thus to more frequently gain the diagnosis of mucinous carcinomas. The causes of the
access to the peritoneal cavity. In addition, the fluid pro- false diagnoses in three of the four cases were the dis-
duced by these tumors is taken up by lymphatics, which cordance between the radiologists and the pathologists in
helps propel the tumor into the regional lymph nodes the visual estimates of the mucin pools in the tumors.
(21). Another implication of mucinous rectal carcinomas This was because the criterion of a mucinous carcinoma
is that they may present as a perirectal cystic mass be- is based on the visual estimation of the amount of the
cause of their ability to easily penetrate the outside rectal extracellular mucin in the tumor. Therefore, careful in-
wall. Therefore, knowledge of the imaging features of spection of the whole tumor volume may be required to
these tumors is important for radiologists and surgeons obtain correct diagnosis. In this regard, MRI may have
during treatment planning. an advantage over a pathologic examination because the

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MRI OF MUCINOUS/NONMUCINOUS RECTAL CARCINOMA 53

FIG. 5. A 59-year-old man with a nonmucinous carcinoma. A and B: Axial (A) and coronal (B) fast spin echo T2-weighted images. Both
radiologists considered the high signal intensity area near the outer section of the rectal carcinoma as a mucin pool (arrowheads). C: Axial
T1-weighted spin echo image depicted the area as a hypointensity (arrowhead). D: Upon pathologic examination, areas of intramural
abscess (thick arrow) and congestion in the perirectal vein (thin arrow) were noted. Hematoxylin–eosin; no magnification. Radiologist 1
correctly assessed the tumor as a nonmucinous carcinoma. However, Radiologist 2 interpreted the tumor as a mucinous carcinoma.

whole volume of the tumor can be inspected preopera- most common errors in the identification of the mucin
tively or retrospectively at MRI. Thorough examination pools resulted from neglect of the small areas of high
of the entire volume of the tumor from the resected speci- signal intensity, whereas most of the errors by the radi-
men may be difficult in clinical practice. ologist with less experience resulted from the false-
As compared with the accuracy in diagnosis of a mu- positive interpretation of areas of high signal intensities
cinous carcinoma, the accuracy in the identification of mimicking mucin pools in nonmucinous carcinomas,
the mucin pool was relatively lower. The interobserver such as intratumoral congestion, abscess, necrosis, and
agreement for the identification of a mucin pool was also mural edema in the adjacent rectal wall or entrapped
relatively poorer than that for the histologic diagnosis. fluid between the tumor and the adjacent rectal wall.
For the radiologist with a high degree of experience, the These areas were relatively small and scarce within the

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54 M.-J. KIM ET AL.

tumor or located mainly outside of the tumor. The radi- However, MR examinations are being used increasingly
ologist with more experience showed better ability to for the preoperative evaluation of rectal carcinomas and
differentiate those nonmucinous high signal intensities have been reported to be superior to CT at predicting
from a true mucin pool. However, he showed a tendency tumor infiltration (27–29).
to ignore small mucin pools that were deemed to be In conclusion, our study shows that MRI is accurate in
insignificant. The portion of the mucin pools that was preoperatively distinguishing between mucinous and
missed at MRI or the high signal intensity that was nonmucinous carcinoma by identification of the high sig-
falsely interpreted as a mucin pool usually comprised nal intensity area of the mucin pools in the rectal carci-
only a small portion of the tumors. Therefore, false- nomas on T2-weighted images. Therefore, this ability of
positive or -negative diagnosis of mucinous carcinoma MRI to histologically differentiate between rectal carci-
did not occur in the majority of cases for both radiolo- nomas should be incorporated into the preoperative MR
gists. Additional use of gadolinium-enhanced sequences evaluation of rectal carcinomas.
may improve radiologists’ ability to differentiate be-
tween a mucin pool and edema, necrosis, or abscess be-
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