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CT Features of Metastatic Linitis Plastica to the Rectum in Patients with Peritoneal Carcinomatosis

¹ Department of Diagnostic Radiology, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Poongnap Dong Songpa Ku, Seoul, 138-040, Korea.
² Department of Pathology, Asan Medical Center, Seoul, 138-040 Korea.
³ Department of Surgery, Asan Medical Center, Seoul, 138-040 Korea.

Received May 14, 1999; accepted after revision July 2, 1999.

 
Address correspondence to H. K. Ha.

Abstract

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OBJECTIVE. We examined the CT features of 22 patients with metastatic linitis plastica to the rectum.

CONCLUSION. Metastatic linitis plastica to the rectum should be considered when CT shows a long segment of circumferential rectal wall thickening, especially in patients with peritoneal carcinomatosis from gastric cancer. In such patients, CT helps avoid unnecessary extensive surgery.

Introduction

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Linitis plastica refers to the diffuse proliferation of the connective tissue of a hollow organ, resulting in tissue thickening so that the organ is constricted, inelastic, and rigid. Although it is commonly seen in the stomach, other organs such as the small intestine, colon, and rectum are sometimes involved. The stomach is the most common primary site [1, 2] of metastatic linitis plastica; however, other sites include the breast [3], gallbladder, bladder, and prostate gland [1]. The disease is characterized by an increase in connective tissue with scanty malignant epithelial cells [4, 5]. As a result, researchers stress the difficulties associated with correct diagnosis using endoscopic rectal biopsy [6].

When the rectal wall is circumferentially involved with metastatic linitis plastica, the rectal lesion might be mistaken for primary rectal cancer, other inflammatory or ischemic processes, or changes after radiation therapy. Misdiagnosis may occur even with a knowledge of the patient's history of primary tumor or prior surgery for tumor.

According to researchers [1, 2, 6], metastatic linitis plastica to the rectum is frequently associated with peritoneal carcinomatosis. However, the incidence and routes for this type of rectal involvement are not well understood. Moreover, most reports of such patients describe radiologic findings on double-contrast barium enema results [7, 8] but, to our knowledge, no analysis of the CT features of this condition. We examined the CT features of metastatic linitis plastica to the rectum in 22 patients.

Materials and Methods

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A computerized search of medical records at our institution found 514 patients with peritoneal carcinomatosis between January 1992 and August 1997. All patients underwent CT, and their scans were retrospectively reviewed. Of these patients, 37 showed circumferential rectal wall thickness greater than 1 cm. Fifteen patients were excluded from the study because 11 records included no confirmation of rectal abnormality and four patients had a history of pelvic radiation therapy. Therefore, we based our study on the images of 22 patients, 11 men and 11 women (age range, 25-75 years; mean, 50 years). Diagnosis of metastatic linitis plastica to the rectum was made with surgery in 14 patients, proctosigmoidoscopic biopsy in seven, and cystoscopic biopsy in one.

CT was performed using a GE 9800 Quick System (General Electric Medical Systems, Milwaukee, WI) and Somatom Plus-S, Plus-4, and Plus-40 scanners (Siemens, Erlangen, Germany) with 8- or 10-mm slice thickness at 8- or 10-mm intervals from the diaphragm to the pubis. Approximately 600-900 ml of oral contrast material (2% barium sulfate suspension; E-Z-CAT, E-Z-EM, Westbury, NY) was given 1 hr before scanning. Approximately 100-120 ml of IV iopamidol (Iopamiro 300; Bracco, Milan, Italy) or iopromide (Ultravist; Schering, Berlin, Germany) was given as a bolus (rate, 3.0 ml/sec) to 15 patients. Scanning was started 40-60 sec after IV infusion with a scanning time of 0.8-2.0 sec and an interscan delay of 1.8-3.5 sec. A traditional bolus rapid-drip infusion technique was used for the remaining seven patients. Rectal contrast material was not administered to all patients.

CT images were analyzed for the length and thickness of the rectum, patterns of rectal wall thickening (even or uneven), contrast enhancement (homogeneous, heterogeneous, or target sign), degree of infiltration in the perirectal fat plane (not visible; grade I, confined to the perirectal space but not reaching the perirectal fascia; grade II, beyond the perirectal fascia but not reaching the pelvic side wall; and grade III, reaching the pelvic side wall), and changes in other abdominal organs and sites. CT images were independently reviewed by two radiologists. If interpretations differed, consensus findings were used for a final decision.

Results

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Patients' symptoms included chronic constipation in six, defecation difficulty in five, tenesmus in four, abdominal pain and distention in three, watery diarrhea in two, and hematochezia in two (symptom duration, 5 days-6 months). Primary tumors included gastric cancer in 18 patients, transitional cell carcinoma of the bladder in one, serous cystadenocarcinoma of the ovary in one, squamous cell carcinoma of the cervix in one, and ascending colon carcinoma (poorly differentiated type) in one. The tumor cell types of the 18 gastric cancers included poorly differentiated in 11 patients, signet ring cell in four, well differentiated in one, moderately differentiated in one, and mucinous in one. Before the diagnosis of metastatic linitis plastica to the rectum was made, 20 of the 22 patients underwent surgery for primary tumors at other sites at various intervals (range, 7-45 months; mean, 22 months). In the remaining two patients, the diagnosis of primary tumor was made at endoscopic biopsy.

Thirteen of the 22 patients underwent proctosigmoidoscopic examination to confirm rectal abnormality. Biopsy specimens yielded tumor cells in seven patients. In six patients, biopsy indicated chronic proctitis without tumor cells. Surgery for rectal lesions was attempted in 14 of 22 patients: low anterior resection in one, palliative colostomy in eight, palliative ileostomy in one, right hemicolectomy with ileostomy in one, and exploratory laparotomy in three. In 22 patients, the tumor cells obtained were identical to those found during histopathologic examination.

Table 1 summarizes the CT features of 22 patients with linitis plastica to the rectum. On CT, rectal wall thickening (range, 1.0-2.2 cm; mean, 1.6 cm) appeared to extend downward to the lower rectum nearly to the level of the anal verge in 19 patients (86%) (Fig. 1A, 1B). In 12 patients (55%), rectal wall thickening appeared to extend upward to the sigmoid colon. In six patients (27%), the thickened rectal wall showed three zones (target sign): a hyperattenuated inner zone, a hyperattenuated outer zone, and a hypoattenuated middle zone (Figs. 1A, 1B and 2). Of the 16 patients without the target sign, three showed marked contrast enhancement in the rectum.

View larger version (145K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —55-year-old man with metastatic linitis plastica of rectum. Patient underwent subtotal gastrectomy for gastric cancer (poorly differentiated type) 43 months previously and then underwent palliative sigmoid loop colostomy. Contrast-enhanced CT scan shows concentric rectal wall thickening (arrowheads) with target sign. Images revealed 3-cm mass (not shown) in rectovesical pouch. Bladder wall is thickened (arrows). Proctoscopy and cystoscopy confirmed tumor infiltration to rectum and bladder.

View larger version (159K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —55-year-old man with metastatic linitis plastica of rectum. Patient underwent subtotal gastrectomy for gastric cancer (poorly differentiated type) 43 months previously and then underwent palliative sigmoid loop colostomy. Contrast-enhanced CT scan 4 cm caudad to A shows downward extension of tumor invasion (arrows) to lower rectum and level of anal verge. Note minimal infiltration (arrowheads) in perirectal fat plane.

View larger version (178K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2. —65-year-old woman with metastatic linitis plastica of rectum and Krukenberg's tumor of ovary. Patient underwent total gastrectomy for gastric cancer (signet ring cell type). Contrast-enhanced CT scan shows concentric thickening (arrows) of rectal wall with target sign. Images reveal irregular uterine (U) surface. Note left ovarian mass (K), ascites (asterisk), and focal thickening of peritoneum (arrowhead).

Table 2 summarizes changes in other abdominal organs and sites. Masses were present in the pelvic cavity of 11 patients (50%) (Figs. 3A, 3B, 3C and 4). Except for two patients who had a recurrent ovarian or bladder tumor (10.0 and 10.5 cm, respectively), the masses in the remaining nine patients ranged from 1.8 to 5.0 cm in diameter (mean, 3.1 cm). In these patients, the masses were directly contiguous with the involved rectum. The bladder wall was thickened in five patients (23%) (Fig. 1A), and cystoscopic confirmation of tumor infiltration was made in two patients.

View larger version (147K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —61-year-old woman with metastatic linitis plastica of rectum. Patient underwent total gastrectomy for gastric cancer (poorly differentiated type) 45 months previously and then underwent palliative sigmoid loop colostomy for rectal obstruction. Contrast-enhanced CT scan shows concentric thickening of rectal wall without target sign. Note ill-defined mass (arrow) in cul-de-sac.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —61-year-old woman with metastatic linitis plastica of rectum. Patient underwent total gastrectomy for gastric cancer (poorly differentiated type) 45 months previously and then underwent palliative sigmoid loop colostomy for rectal obstruction. Double-contrast barium enema shows narrowing of rectum and thickened mucosal folds with irregular contour (arrows). Note concentric luminal narrowing (asterisk) in transverse colon caused by peritoneal tumor seeding.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —61-year-old woman with metastatic linitis plastica of rectum. Patient underwent total gastrectomy for gastric cancer (poorly differentiated type) 45 months previously and then underwent palliative sigmoid loop colostomy for rectal obstruction. Photomicrograph shows diffuse involvement of entire wall by poorly differentiated adenocarcinoma. Mucosa is eroded (arrowheads) and submucosa (SM) and subserosa (SS) are significantly thickened because of tumor infiltration and reactive fibrosis. Compared with healthy corresponding layer (arrows), proper muscularis (PM) is considerably thickened because of hypertrophic changes of muscle fiber and tumor infiltration. (H and E, x5)

View larger version (167K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4. —59-year-old woman with metastatic linitis plastica to rectum. Patient underwent total hysterectomy with bilateral salpingo-oophorectomy for cervical cancer (squamous cell type) 21 months previously and then underwent palliative transverse colon colostomy. Contrast-enhanced CT scan shows heterogeneous rectal wall thickening with recurrent pelvic mass (black arrows) in area of vaginal stump. Posterior bladder wall is thickened because of tumor invasion. Note minimal perirectal lymphadenopathy (arrowheads), fluid collection in presacral space, and thickening of both ureteral walls (white arrows). Cystoscopic examination confirmed tumor invasion to bladder.

In nine (41%) of the 22 patients, bowel wall thickening similar to that of the rectum was seen in the gastrointestinal tract; a total of 19 intestinal segments were involved including transverse colon in seven patients, ascending colon in four, terminal ileum in three, descending colon in two, proximal ileum in two, and jejunum in one. Intestinal obstruction developed in 11 patients (50%) and included the rectum in five patients, sigmoid colon in one, transverse colon in one, ascending colon in one, ileum in one, and jejunum in two.

Resected surgical specimens of the rectum were available for five patients. On histopathologic examination, the mucosa was focally involved and eroded in most instances and the submucosa or subserosa was thickened by reactive fibrosis and tumor cell infiltration (Fig. 3C). The muscularis propria layer was thickened to a lesser degree, probably because of tumor infiltration and mild hypertrophic change of the muscle fiber; in this layer, reactive fibrosis was unidentified. Histopathologic examination showed similar findings for all surgical specimens. For patients with the target sign on rectal images, CT-histopathologic correlation was impossible because these patients did not undergo surgical resection.

Discussion

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Rectal invasion routes appear to differ according to the type of primary tumor. In a study examining 75 patients with breast cancer, 12 patients showed colorectal involvement [3]; therefore, the main route was hematogenous. Alternatively, tumors may spread intramurally through lymphatic channels. Fernet el al. [1] described five cases of the linitis plastica type of intramural tumor that spread along the alimentary tract among 150 patients with gastric cancer. In one of their five patients, the rectum was involved. These researchers reported that such intramural spread was caused by the milking of tumor cells via small longitudinal lymphatic channels, especially along the submucosa resulting from peristalsis and antiperistalsis. Although these hematogenous or lymphatic routes have a role in some instances, most primary abdominal tumors that manifest from the stomach, pancreas, or ovary usually spread to the large intestine by direct invasion along mesenteric reflections, the gastrocolic ligament, or an immediately contiguous site [9]. In our study, pelvic masses (recurrent tumor or rectal shelf) were directly contiguous with rectal lesions favoring the route of direct tumor invasion from the drop-off metastasis or pelvic tumor. Even in patients without pelvic masses, the rectal tumor invasion probably developed from tiny implanted lesions.

In our study, the most common CT feature in patients with metastatic linitis plastica to the rectum was concentric bowel wall thickening in a long segment (>10 cm). However, because we could not obtain biopsy specimens, we might have overestimated the extent of segment involvement in which ischemic colitis coexisted proximal to rectal cancer [10]. Furthermore, other conditions such as fluid overload, heart failure, or postoperative state may contribute to rectal wall thickening. Additionally, the same finding can be seen in neoplastic, inflammatory, and vascular disorders; therefore, a pattern of bowel wall involvement may be nonspecific for diagnosis. The perirectal changes in patients with linitis plastica did not differ from those of other diseases. Rectal wall thickening extended downward to the lower rectum nearly to the level of the anal verge in 19 (86%) of our 22 patients. As Fernet et al. [1] speculated, this occurrence probably results from the milking force associated with peristalsis and antiperistalsis.

An important pathologic characteristic of linitis plastica is the exuberant desmoplastic response that the tumor cells or their products elicit in the stroma, especially in the submucosa and subserosa. In reviewing the literature [1, 2, 11], we found similar histopathologic findings. The target sign seen on CT reflected these pathologic findings. Although the target sign is an important indicator of benign gastrointestinal tract diseases [12], our study shows that this sign can be seen in malignant conditions as well. Moreover, the hypoattenuated middle zone of the target sign represents the muscularis propria. This result differs from the usual understanding of target signs in that hypoattenuated zone (submucosa).

Many conditions appear on CT with a long length of rectal wall thickening; these include primary linitis plastica without primary tumors at other sites, primary rectal cancer with proximal obstructing colitis [10], ulcerative colitis, Crohn's disease, pseudomembranous and ischemic colitis, and endometriosis. Use of only the rectal wall thickening pattern in diagnosis might cause difficulties in differentiating metastatic linitis plastica from other conditions. Therefore, knowledge of a patient's history of primary cancer at other sites and the ancillary findings in abdominal organs may help to suggest the possibility of metastatic linitis plastica to the rectum. In conclusion, metastatic linitis plastica to the rectum should be considered when CT shows a long segment of circumferential rectal wall thickening, especially for patients with peritoneal carcinomatosis from gastric cancer. In such patients, CT helps avoid unnecessary extensive surgery.

Acknowledgments
 
We thank Bonnie Hami for her editorial assistance in preparing this manuscript.

References

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