AJR 2000; 175:747-749
© American Roentgen Ray Society
Small Flat Umbilicated Tumors of the Colon
Radiographic and Pathologic Findings
Mary E. Cunnane1,
Stephen E. Rubesin1,
Emma E. Furth2,
Marc S. Levine1 and
Igor Laufer1
1
Department of Radiology, University of Pennsylvania Medical Center, MRI Bldg.
1, 3400 Spruce St., Philadelphia, PA 19104.
2
Department of Pathology and Laboratory Medicine, University of Pennsylvania
Medical Center, Philadelphia, PA 19104.
Received January 14, 2000;
accepted after revision February 16, 2000.
Stephen E. Rubesin and Marc S. Levine are consultants for E-Z-EM.
Address correspondence to S. E. Rubesin.
Abstract
OBJECTIVE. We describe the radiographic and pathologic findings of
small flat umbilicated tumors of the colon detected on double-contrast barium
enema examinations performed in a Western population.
CONCLUSION. Unlike those reported by Japanese authors, the small
flat umbilicated tumors of the colon in our patients were usually hyperplastic
polyps, previously called "inverted hyperplastic polyps."
Nevertheless, colonoscopy with excisional biopsy is warranted for such tumors
detected on double-contrast barium enema examinations because of the small
possibility that these tumors represent adenoma or even early
adenocarcinoma.
Introduction
Small (<2 cm) flat adenomas and adenocarcinomas of the colon have been
described on double-contrast barium enema examinations, primarily by Japanese
authors
[1,2,3,4,5,6,7].
These neoplasms are manifested radiographically by a central depression within
a flat or slightly raised mucosal lesion
[6]. In one series, these flat
neoplasms accounted for 3.5% of all adenomatous lesions less than 1 cm in
diameter [6]. Although rare,
these small flat tumors are important because they are adenomatous neoplasms
that may harbor high-grade dysplasia or even invasive adenocarcinoma
[2,
4,5,6,7].
Although small flat adenomas and adenocarcinomas have been reported in
Western patients [8,
9], these tumors are extremely
uncommon [10]. In one series,
flat adenomas accounted for 8.5% of 340 adenomas removed at colonoscopy
[9]. In another series, no flat
adenomas were identified, even using high-resolution video endoscopy
[10]. In Western countries,
most early colorectal carcinomas appear macroscopically as pedunculated or
sessile polypoid lesions. However, adenocarcinoma is rarely discovered in
small adenomatous polyps in Western populations. In one series, only 1.3% of
1479 adenomas less than 1 cm in diameter were found to contain foci of
adenocarcinoma [11]. Over the
last decade, we have diligently searched for small flat tumors when performing
double-contrast barium enemas. This article reports our experience with small
flat umbilicated lesions of the colon.
Materials and Methods
A computerized search of radiology files at our institution during a 9-year
period between January 1990 and March 1999 revealed 15 patients in whom small
flat umbilicated tumors were detected on double-contrast barium enema
examinations. Two additional patients with small umbilicated lesions on
double-contrast barium enema examinations from our affiliated Veterans Affairs
Medical Center were also identified. Seven patients were excluded because of
lack of pathologic follow-up. Five other patients were excluded because they
had undergone colonoscopy and biopsy before the barium enema examination; it
was not possible to determine if the central umbilication was intrinsic to the
lesion or this umbilication represented a biopsy defect. The remaining five
patients comprised our study group.
The spot and overhead radiographs from the double-contrast barium enema
examinations were reviewed retrospectively in these five patients. Lesions
were included in our study group if the polyps were less than 2 cm in greatest
diameter; if they were flat, raised, or depressed less than 1 mm in height; or
if they contained a central depression seen as a contour abnormality in
profile or as a central collection of barium en face. Carpetlike
lesionsflat lesions with a reticular surface patternwere
excluded from our study. Medical records revealed that five lesions were
biopsied at colonoscopy, one lesion was excised at colonoscopy, and one lesion
was removed during surgery for a cecal carcinoma. The pathology reports and
the pathologic slides were reviewed retrospectively by a gastrointestinal
pathologist to determine the pathologic nature of these lesions.
Results
Five patients had a total of seven lesions that appeared on double-contrast
barium enema examinations as small, flat, centrally umbilicated tumors (Figs.
1,2,3).
Three of the patients were men and two were women. The average age was 69
years (age range, 55-84 years). Four patients had one small flat umbilicated
polyp, and one patient had three. Four of the lesions were found in the
sigmoid colon, one in the hepatic flexure, one in the splenic flexure, and one
in the rectum. One patient had a synchronous cecal carcinoma. Another patient
had a synchronous large pedunculated tubular adenoma in the sigmoid colon. A
third patient had a synchronous 4-cm sessile tubulovillous adenoma in the
transverse colon.

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Fig. 1. 55-year-old man with heme-positive stool. Spot radiograph of sigmoid
colon from double-contrast barium enema examination shows flat lesion
(large straight arrow) as 1.0-cm, barium-etched ring shadow with
barium-filled central linear umbilication (small straight arrow).
Forceps biopsy revealed hyperplastic polyp. Note 2.0-cm polyp (curved
arrow) on 2.5-cm stalk. Excisional biopsy of pedunculated polyp revealed
tubular adenoma.
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Fig. 2. 84-year-old woman with palpable mass in right lower quadrant. Spot
radiograph of hepatic flexure from double-contrast barium enema examination
shows 1.2-cm flat lesion as barium-etched ring shadow (white arrow)
with central, linear, barium-filled umbilication (black arrow). Right
hemicolectomy was performed for 7.0-cm cecal adenocarcinoma (not shown). Small
flat umbilicated tumor proved to be hyperplastic polyp of 0.9 cm in
diameter.
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Fig. 3. 60-year-old man without symptoms who was undergoing screening
examination. Spot radiograph of sigmoid colon from double-contrast barium
enema examination reveals 1.2-cm flat umbilicated tumor. One edge of tumor
(white arrow) is etched by barium. Note punctate central barium
collection (black arrow). Excisional biopsy revealed 0.8-cm
adenocarcinoma invading superficial submucosa. Eight days later, sigmoid colon
was removed, and no residual tumor was identified.
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Five (72%) of the seven small, flat, centrally umbilicated lesions were
hyperplastic polyps (Figs. 1
and 2), one (14%) was a tubular
adenoma, and one (14%) was an early carcinoma with invasion of the superficial
portion of the submucosa (Fig.
3). The lesions had an average diameter of 1.2 cm (range, 1.0-1.5
cm), without correction for radiographic magnification. The lesions appeared
as sessile, well-circumscribed, smooth or slightly lobulated, round or oval,
flat alterations of the normally smooth surface of the colon. In all seven
cases, a central umbilication was seen as a central, punctate
(Fig. 3), or linear barium
collection (Figs. 1 and
2) en face or as a
depression in profile.
Five lesions were biopsied, and specimens were submitted in fragments so
that the pathologic size of the lesions could not be determined. The
superficial carcinoma, which measured 1.2 cm in diameter radiographically, was
completely excised at colonoscopy and, after fixation, measured 0.8 cm in
greatest dimension. The hyperplastic polyp in the hepatic flexure, which
measured 1.2 cm radiographically, was found to measure 0.9 cm in diameter
after right hemicolectomy for a synchronous adenocarcinoma of the cecum.
Discussion
Diminutive flat tumors have most often been detected at endoscopy
[7] and barium enema
examinations [3,
6] in Japanese patients.
Matsumoto et al. [3]
prospectively detected 52% of small (3-5 mm) flat adenomas on double-contrast
barium enema examinations. Fujiya and Maruyama
[6] detected 60% of lesions
less than 6 mm in diameter and 80% of lesions between 6 and 10 mm in diameter
on double-contrast barium enema examinations. These small, flat, centrally
depressed lesions of the colon are potentially invasive epithelial tumors
[4,5,6].
Although such small lesions are rarely encountered in Western populations, our
series did include one microinvasive carcinoma
(Fig. 3). In Western
populations, most colorectal carcinomas exceed 2 cm in diameter
[11].
Although most small flat umbilicated tumors reported in Japanese articles
in the English literature have been adenomas or early adenocarcinomas, five of
the seven lesions in our series were hyperplastic polyps. In the colon,
hyperplastic polyps are usually smaller than 5 mm, appearing macroscopically
as smooth-surfaced sessile lesions that are frequently multiple. These lesions
are composed histologically of elongated crypts lined by a serrated epithelium
containing intermediate cells and scattered goblet cells
[12]. Hyperplastic polyps
result from altered maturation of normal colonic epithelium and are not
precancerous [12]. These
lesions are extremely common. They are detected at autopsy in more than 75% of
people over the age of 40 years
[12]. Most hyperplastic polyps
are found in the rectum, and they frequently arise on the crests of mucosal
folds. Almost all hyperplastic polyps are dome-shaped, but these lesions
rarely may contain a central depression; such lesions have been called
"inverted hyperplastic polyps"
[13]. In a recent report from
the Japanese literature, three small flat umbilicated lesions detected and
removed during colonoscopy were found to be inverted hyperplastic polyps on
pathologic examination [14].
Thus, small flat umbilicated hyperplastic polyps similar to those found in our
study have been documented both endoscopically and pathologically.
It remains unclear why the small, flat, centrally umbilicated adenomas and
adenocarcinomas described in the Japanese literature are encountered so
infrequently in Western populations
[10]. One explanation is that
these tumors are more common in Japan. Alternatively, the adult population in
Japan may undergo screening for colonic carcinoma more frequently and at an
earlier age than Western populations. At our institution, less than 10% of
barium enemas are performed on asymptomatic patients who have no risk factors
for the development of colonic carcinoma. Therefore, it is possible that some
of our symptomatic patients with ulcerated plaquelike carcinomas of the colon
might previously have had small flat umbilicated adenomas that were
potentially detectable had screening barium enemas been performed.
Differences in endoscopic or barium enema technique may also account for
the discrepancy in detection of these small flat umbilicated lesions in
Japanese and Western populations. At our institution, we use a barium
suspension of 100% weight per volume, which gives a uniform, relatively thick
mucosal coating despite the presence of intraluminal fluid or epithelial
inflammation. We are able to detect the innominate grooves of the colon
infrequently and, in those infrequent cases, the colon is relatively
collapsed. In contrast, most Japanese authors use a less viscous (70% weight
per volume) barium, which permits visualization of the innominate grooves in
nearly 50% of patients [6].
Thus, in Japan, the use of less viscous barium may be partly responsible for
the increased detection of small flat umbilicated lesions on double-contrast
barium enema examination.
Finally, it is possible that overdistention of the colon with air during
double-contrast barium enema could efface these small flat umbilicated
lesions. In fact, it has previously been shown that these lesions become
flatter and have a shallower central depression when the colon is
overdistended [6].
Nevertheless, comparison of images from our double-contrast barium enema
examinations with Japanese images published in American journals or in the
Japanese journal Stomach and Intestine do not reveal any substantial
differences in the degrees of colonic distention.
In summary, five (72%) of the seven small flat umbilicated colonic lesions
in our series were found to be hyperplastic polyps, previously called
"inverted hyperplastic polyps." However, one lesion was found to
be a microinvasive carcinoma. When small flat umbilicated polyps are detected
on double-contrast barium enema examinations in Western populations, endoscopy
and excision biopsy should be performed to rule out an adenoma or even a
microinvasive carcinoma.
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