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AJR 2000; 175:747-749
© American Roentgen Ray Society


Original Report

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
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
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
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
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
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
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 lesions—flat lesions with a reticular surface pattern—were 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
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Abstract
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Materials and Methods
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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.

 

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
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
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.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Muto T, Kamiya J, Sawada T, et al. Small "flat adenoma" of the large bowel with special reference to its clinicopathologic features. Dis Colon Rectum 1985;28:849 -851
  2. Shimoda T, Ikegami M, Fujisaki J, Matsui T, Aizawa S, Ishikawa E. Early colorectal carcinoma with special reference to its development de novo. Cancer 1989;64:1138 -1146[Medline]
  3. Matsumoto T, Iida M, Kohrogi N, et al. Minute nonpolypoid adenomas of the colon depicted with barium enema examination. Radiology 1993;187:377 -380[Abstract/Free Full Text]
  4. Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993;25:455 -461[Medline]
  5. Matsui T, Yao T, Yao K, et al. Natural history of superficial depressed colorectal cancer: retrospective radiographic and histologic analysis. Radiology 1996;201:226 -232[Abstract/Free Full Text]
  6. Fujiya M, Maruyama M. Small depressed neoplasms of the large bowel: radiographic visualization and clinical significance. Abdom Imaging 1997;22:325 -331[Medline]
  7. Watari J, Saitoh Y, Obara T, et al. Early nonpolypoid colorectal cancer: radiographic diagnosis of depth of invasion. Radiology 1997;205:67 -74[Abstract/Free Full Text]
  8. Spjut HJ, Frankel NB, Appel MF. The small carcinoma of the large bowel. Am J Surg Pathol 1979;3:46 -49
  9. Wolber RA, Owen DA. Flat adenomas of the colon. Hum Pathol 1991;22:70 -74[Medline]
  10. Bond JH. Small flat adenomas appear to have little clinical importance in Western countries. Gastrointest Endose 1995;42:184 -186
  11. Muto T, Bussey HJR, Morson BC. The evolution of cancer of the colon and rectum. Cancer 1975;36:2251 -2270[Medline]
  12. Fenoglio-Preiser CM, Noffsinger AE, Franzin G, Zamboni G, Scarpa A, Geboes K. Other tumors of the large intestine. In: Whitehead R, ed. Gastrointestinal and oesophageal pathology. Edinburgh: Churchill-Livingstone, 1995:863 -865
  13. Sobin LH. Inverted hyperplastic polyps of the colon. Am J Surg Pathol 1985;9:265 -272[Medline]
  14. Togashi K, Konishi F, Kashiwagi H, Ishizuka T, Kanazawa K. Inverted hyperplastic polyp: report of three cases. Stomach and Intestine 1999;34:935 -940

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