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Peritoneal Leiomyosarcomatosis Originating from Gastrointestinal Leiomyosarcomas: CT Features¹

¹ From the Departments of Diagnostic Radiology (S.E.R., H.K.H., A.Y.K., T.K.K.) and Internal Medicine (S.J.M., S.K.Y.), Asan Medical Center, University of Ulsan College of Medicine, 388-1 Poongnap-Dong, Songpa-Ku, Seoul 138-736, South Korea; and Department of Diagnostic Radiology, Kangnam St Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, South Korea (S.E.R., B.G.C., J.Y.B.). Received January 4, 2002; revision requested February 28; final revision received October 4; accepted October 14. Address correspondence to H.K.H. (e-mail: hkha@amc.seoul.kr).

	ABSTRACT

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PURPOSE: To evaluate the computed tomographic (CT) features of peritoneal leiomyosarcomatosis (PL) originating from gastrointestinal leiomyosarcoma and compare the CT features of primary gastrointestinal leiomyosarcomas between patients with and those without PL.

MATERIALS AND METHODS: The authors reviewed the medical and surgical-pathology records and the CT scans of 89 patients with gastrointestinal leiomyosarcoma to determine the prevalence of PL. Also, the CT scans of the patients with PL were evaluated for the morphologic appearance of peritoneal lesions. The CT features of the primary tumors were compared between the patients with and those without PL. Student t and Fisher exact tests were performed.

RESULTS: Metastases were present in 39 patients. PL was seen in 25 patients. Other metastatic sites included liver in 26 patients, lymph nodes in 11, lungs in three, and bone in one. In the 25 patients with PL, CT findings included multiple discrete peritoneal nodules in 22 patients and massive peritoneal lesions in three. Smudged omental infiltration was combined with other findings in 10 patients. The sites of the peritoneal masses were mesentery in 18 patients, omentum in 11, paracolic gutters in 11, pelvic cavity in eight, perihepatic space in three, and perisplenic space in one. Four patients had ascites. There were statistically significant differences in size of primary tumor (mean diameter, 12.5 cm vs 9.2 cm) (P = .01) and prevalence of exophytic growth of primary tumor (P = .02) between the patients with and those without PL.

CONCLUSION: CT findings can indicate PL in the differential diagnosis. The prevalence of PL appears to be higher when it originates from large primary tumors.

© RSNA, 2003

Index terms: Gastrointestinal tract, CT, 70.12112 • Gastrointestinal tract, neoplasms, 70.322, 70.33 • Leiomyosarcoma, 70.322, 70.33 • Peritoneum, CT, 70.12112 • Peritoneum, neoplasms, 70.322, 70.33

	INTRODUCTION

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Peritoneal leiomyosarcomatosis (PL) is defined as a peritoneal dissemination of leiomyosarcomas (1). Although various sites, such as the mesentery, retroperitoneum, genitourinary tract, and soft tissue, may be involved, the gastrointestinal tract is the most common site of the primary tumor (2). The prevalence of PL in patients with gastrointestinal leiomyosarcoma has ranged from 15% to 21% (2,3), but it may have been influenced by the length of the follow-up period or the location or lesion characteristics of the primary tumor in these previous reports. Among the malignant peritoneal neoplasms, PL has a much lower prevalence compared with peritoneal carcinomatosis: Villanueva et al (1) reported that only six of the 115 patients with peritoneal dissemination of malignant neoplasms in their study had associated PL. Therefore, if a patient does not have a known history of primary gastrointestinal leiomyosarcoma, the presence of multiple disseminated peritoneal masses may be misdiagnosed as peritoneal carcinomatosis (4), tuberculous peritonitis (5), peritoneal lymphomatosis (6), mesothelioma (7), or neurofibromatosis (8). Although leiomyomatosis peritonealis disseminata, a benign condition commonly associated with uterine leiomyoma, is rare, it also closely mimics PL (9).

In patients suspected of having malignant peritoneal neoplasms, computed tomographic (CT) scans may be useful not only in detecting peritoneal nodules but also in determining the primary tumor site. Despite the fact that gastrointestinal leiomyosarcoma is not a rarely encountered disease in the clinical setting, the literature describing the CT features of PL has been limited (1,10,11). Moreover, most previous reports have been those of small patient populations (1,10,11). To improve the early detection of PL in patients with gastrointestinal leiomyosarcoma and to evaluate the factors associated with a high risk of PL, further investigation with a large patient series will be necessary.

The purpose of this study was to evaluate the CT features of PL originating from gastrointestinal leiomyosarcomas and to compare the CT features of primary gastrointestinal leiomyosarcoma between patients with and those without PL.

	MATERIALS AND METHODS

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Patients
By performing a computerized search of the March 1990 to March 2000 medical records of two institutions (Asan Medical Center and The Catholic University of Korea), we identified 103 patients with pathologically proven diagnoses of gastrointestinal leiomyosarcoma. Fourteen of these patients were excluded from analysis because their CT scans were not available. Therefore, the surgical-pathology records and CT scans of the remaining 89 patients (45 men, 44 women; age range, 25–77 years; mean age, 55 years) were retrospectively reviewed. Our institutional review board did not require its approval or patient informed consent for this retrospective study.

The diagnoses of the primary tumors were made on the basis of histopathologic results obtained after surgical resection in 81 patients, endoscopic biopsy results in four patients, and the results of percutaneous needle biopsy of hepatic metastatic lesions in four patients. The following surgical procedures were performed in the 81 patients: segmental resection in 46 (small bowel in 36, rectum in six, stomach in two, and colon in two), total or subtotal gastrectomy in 24, extended total gastrectomy with splenectomy in five, Whipple operation in four, and Mile operation in two patients.

The diagnoses of PL in 25 patients were based on surgical findings in 14 patients and follow-up CT findings in 11 patients. Six patients had PL at the time of surgery for treatment of the primary tumor. The mean interval between the time of surgical removal of the primary tumor and the time of detection of PL was 15 months (range, 1–72 months). A second surgery was performed in nine patients with PL owing to bowel obstruction (five patients) and to remove the tumor burden (four patients).

CT Scanning
All patients underwent abdominal CT (Somatom Plus-S, Somatom Plus-4, and Somatom Plus-40; Siemens, Erlangen, Germany or 9800 Quick System; GE Medical Systems, Milwaukee, Wis) with continuous 8- or 10-mm-thick sections at 8- or 10-mm intervals from the diaphragm to the symphysis pubis. The patients routinely received oral and intravenous contrast materials. In all patients, an automated dedicated CT injector (Medrad MK-IV; Medrad, Pittsburgh, Pa) was used to administer 100–120 mL of either iopamidol (Iopamiro 300; Bracco Diagnostics, Milan, Italy) or iopromide (Ultravist; Schering, Berlin, Germany) by means of bolus injection through an antecubital vein at 3 mL/sec. In 75 of the 89 patients, approximately 600–900 mL of oral contrast material (barium sulfate, E-Z-CAT; E-Z-EM, Westbury, NY) was administered 1 hour before CT scanning; the remaining 14 patients refused to take an oral agent. Follow-up CT scans were obtained in 56 of the 89 patients. The mean total number of CT examinations performed was three (range, two to nine), and the mean interval between examinations was 15 months (range, 1 month to 6 years).

CT Scan Analysis
Two radiologists (S.E.R., H.K.H.), who were unaware of the final diagnoses, reviewed the CT scans independently. When their interpretations differed, they reached a consensus. The CT scans obtained in the 25 patients with PL were evaluated for the site, number, and morphologic appearance of the peritoneal lesions and the presence or absence of ascites, lymphadenopathy, and metastatic lesions at other sites. The peritoneal involvement patterns were classified as peritoneal nodules, omental infiltration, or massive peritoneal lesions. Peritoneal nodules were defined as well-defined soft-tissue nodular lesions in the peritoneal cavity. Omental infiltration was considered to be present when the omentum showed granular infiltration or miliary nodules. Massive peritoneal lesions were defined as masses larger than 10 cm in greatest diameter in the peritoneal cavity. We determined the presence or absence of internal necrosis in the peritoneal mass on the basis of the size of the mass. Lymphadenopathy was considered to be present when soft-tissue nodular lesions larger than 1 cm in short-axis diameter could be seen on transverse CT scans.

Thereafter, in the patients with and those without PL we compared the sites and the CT-depicted morphologic features of the primary tumors—specifically, size, margin (smooth or lobulated), growth pattern, and presence or absence of internal necrosis, calcification, local invasion, lymphadenopathy, and ascites. Growth patterns were classified as endophytic, exophytic, or combined—that is, endophytic and exophytic. Tumor growth was considered to be endophytic when the mass attached to the bowel wall was completely confined to the bowel lumen and not bulging into the extraluminal space. Conversely, tumor growth was considered to be exophytic when the mass was confined to the extraluminal space and partially attached to the bowel wall. The combined growth pattern had the typical dumbbell appearance on CT scans.

Statistical Analyses
Statistical analyses were performed to compare differences in CT findings of the primary tumor between the patients with and those without PL. The Student t test was used to assess differences in the mean size of the primary tumors in the patients with and without PL. The differences between the two groups with regard to CT findings of the primary tumors—specifically, lobulated contour, exophytic growth, and presence or absence of necrosis, calcification, local invasion, lymphadenopathy, and ascites—were compared by using the Fisher exact test. P < .05 was considered to indicate a significant difference. All analyses were performed by using a computer software program (SAS 6.01 for Windows; SAS Institute, Cary, NC).

	RESULTS

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Metastases were present in 39 (44%) of the 89 patients (Table 1). PL was detected in 25 (28%) of the 89 patients. Other metastatic sites included the liver in 26 (29%) patients, the lymph nodes in 11 (12%) patients, the lungs in three (3%) patients, and bone in one (1%) patient. The CT findings in the 25 patients with PL included multiple peritoneal nodules in 22 (88%) (Fig 1), omental infiltration in 10 (40%) (Fig 2), and massive peritoneal lesions in three (12%) (Fig 3) patients. Omental infiltration was not the sole peritoneal manifestation in the 10 patients with this finding: It was detected in combination with multiple peritoneal nodules in eight patients and in combination with massive peritoneal lesions in two.

View larger version (133K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. PL originating from gastric leiomyosarcoma in a 54-year-old woman. (a) Preoperative transverse contrast material-enhanced CT scan shows a large exogastric leiomyosarcoma (arrows) with extensive central necrosis. (b) Follow-up transverse contrast-enhanced CT scan obtained 16 months after surgical resection shows two well-defined, discrete soft-tissue peritoneal nodules (thick white arrows) at the previous tumor site, a finding that represents PL. Multiple hepatic metastases (black arrows) and a small amount of ascites (thin white arrows) in the left subphrenic space also are seen.

View larger version (129K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. PL originating from gastric leiomyosarcoma in a 54-year-old woman. (a) Preoperative transverse contrast material-enhanced CT scan shows a large exogastric leiomyosarcoma (arrows) with extensive central necrosis. (b) Follow-up transverse contrast-enhanced CT scan obtained 16 months after surgical resection shows two well-defined, discrete soft-tissue peritoneal nodules (thick white arrows) at the previous tumor site, a finding that represents PL. Multiple hepatic metastases (black arrows) and a small amount of ascites (thin white arrows) in the left subphrenic space also are seen.

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Transverse contrast-enhanced CT scan obtained in a 69-year-old woman with PL originating from gastric leiomyosarcoma shows a large well-defined mesenteric mass (M) with extensive central necrosis combined with adjacent infiltrative omental thickening (arrows).

View larger version (112K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Transverse contrast-enhanced CT scan obtained in a 43-year-old woman with PL originating from gastric leiomyosarcoma shows a massive omental lesion (arrows) containing irregular areas of low attenuation.

View larger version (139K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Transverse contrast-enhanced CT scan obtained in a 65-year-old man with PL originating from rectal leiomyosarcoma shows multiple well-defined discrete masses (arrows) larger than 3 cm with central necrosis in the peritoneal cavity.

Student t test results indicated that there was a statistically significant difference in the sizes of the primary tumors between the patients with and those without PL (P = .01). Fisher exact test results showed a statistically significant difference in the prevalence of exophytic tumor growth between the patients with and those without PL (P = .02). There was no statistically significant difference in the following features between the patients with and those without PL: lobulated contour (P = .211), presence of internal necrosis (P = .055), presence of calcification (P = .085), presence of lymphadenopathy (P = .664), presence of ascites (P = .075), and presence of local tumor invasion (P = .304). Although a statistically significant difference in lobulated contour or internal necrosis was not noted between the two patient groups, the prevalences of these features were higher in the patients with PL than in those without PL (Table 2). However, focal or stippled calcification was noted in only seven of the 64 patients without PL.

	DISCUSSION

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The principal mode of tumor spread from gastrointestinal leiomyosarcoma is hematogenous, with the liver and the lungs being the most common sites (12). However, PL is not uncommon. In the study with, to our knowledge, the largest population of patients with primary gastrointestinal leiomyosarcoma (3), PL was found at initial surgical exploration in 23 (21%) of the 108 cases of primary leiomyosarcoma of the small and large bowels. McLeod et al (2) reported that the prevalence of CT-depicted PL originating from a variety of primary sites, including the gastrointestinal tract, mesentery, retroperitoneum, genitourinary tract, and soft tissue, was about 12%. In the McLeod et al study, when the primary tumor site was limited to the gastrointestinal tract the prevalence of PL increased to 15% (seven of the 48 patients examined). The prevalence of PL in our study, 28%, was higher than that in previous reports. Such a higher prevalence may have been due to our inclusion of cases that were diagnosed as PL at initial surgical exploration as well as at follow-up CT. Therefore, the comparison of the prevalence of PL in our study with those in the two other reports (2,3) is not reasonable because different diagnostic methods were applied.

Although the stomach was the most common primary site of gastrointestinal leiomyosarcoma in our study and in other investigations (13), it is interesting that in our study the most common primary site of developing PL was the small bowel. We believe that the higher prevalence of PL among the small-bowel tumors might have been due to either a wider range of bowel movement in or the relatively thin wall of the small intestine compared with the range of bowel movement in and the wall thickness of the stomach. The intraperitoneal spread of leiomyosarcomas is thought to occur by means of invasion through the serosa or by means of embolic metastases (14,15).

Our finding that all of the patients with PL showed an exophytic tumor growth pattern favors the hypothesis that there is direct tumor spreading from the serosa into the peritoneal cavity. In our study, the most common sites of PL in the peritoneal cavity were the mesentery, omentum, and paracolic gutters. The pelvic cavity was another common site of PL and thus should be included among the regions scanned at CT in patients suspected of having gastrointestinal leiomyosarcoma.

At comparison of the patients who had PL with those who did not, the primary tumor sizes were significantly larger and the prevalence of exophytic tumor growth was significantly higher in the patients with PL compared with these features in the patients without PL. However, other CT findings, including lobulated contour and presence of necrosis, calcification, local tumor invasion, and ascites, were not significantly different between the two groups.

We believe that among a group of reports describing the CT features of PL (1,10,11), including our present investigation, our study comprises the largest patient population with leiomyosarcomas originating from the gastrointestinal tract. We found, as did other observers (1,10,11), that the most common form of peritoneal involvement in PL was multiple well-defined peritoneal nodules or masses. Most of the peritoneal nodules appeared as homogeneously solid lesions, but the neoplasms larger than 3 cm commonly manifested as heterogeneous masses with central necrosis. In previous studies (1,10), diffuse peritoneal or mesenteric involvement was not observed with PL. However, we noted a smudged pattern of diffuse tumor spread, or omental infiltration, in 10 patients in our study, but this pattern was usually combined with that of multiple peritoneal nodules or massive peritoneal lesions. Furthermore, three patients in our study had an extensive mass that was replacing the peritoneal cavity.

We also believe that it is interesting that PL did not occur in leiomyosarcomas with calcification. Although further investigation is necessary because of the limited number of patients with such findings in our study, the hard consistency of calcified tumors, as well as differences in degree of primary tumor necrosis, vascularity, level of immune response, and growth rate, may account for the lower prevalence of PL in association with calcified tumors.

As the results of both our study and other investigations (1,10,11) have demonstrated, the rarity of ascites and lymphadenopathy was another important CT feature of PL. There have been some differences in the prevalence of ascites among studies, however. In one series (2) ascites was seen in 50% of the patients with PL, whereas in other reports it was minimal or absent (1,10,11). In our study, ascites occurred in only four (16%) patients with PL, and the amount was small and limited to the pelvic cavity or subphrenic space. Lymphatic spread also is rare in patients with gastrointestinal leiomyosarcoma, but it has been reported occasionally, especially in cases of poorly differentiated tumors (12).

The CT findings of PL may simulate those of other peritoneal abnormalities such as peritoneal carcinomatosis. The well-known and common CT features of typical peritoneal carcinomatosis, which occur frequently in association with gastrointestinal, pancreatic, and ovarian carcinomas, are ascites, peritoneal thickening with enhancement, omental changes such as enhancing nodules and omental cakes, and mesenteric infiltration (4). The prevalence of peritoneal nodules in peritoneal carcinomatosis is not as high as might be expected. In one series (5), peritoneal nodules larger than 5 mm in diameter were seen in only 11 of 93 patients with peritoneal carcinomatosis. The CT findings of PL appear to more closely resemble those of intraperitoneal drop metastases from hepatocellular carcinoma (16) or the apparently benign condition of leiomyomatosis peritonealis disseminata (9) rather than the CT findings of peritoneal carcinomatosis.

The pathway of peritoneal seeding from hepatocellular carcinoma is similar to the pathway of PL: the rupture of an exophytic hepatocellular carcinoma into the peritoneal cavity and the subsequent seeding of metastatic deposits with single or multiple discrete hypervascular intraperitoneal masses with or without central necrosis and engorgement of adjacent omental vessels (16,17). In leiomyomatosis peritonealis disseminata, a rare condition that occurs in women of reproductive age, uterine leiomyomas in the form of multiple small nodules of smooth muscle cells develop throughout the subperitoneal surfaces. These tumors have a strong association with pregnancy (18). Such peritoneal lesions regress during the postpartum period or following surgical castration.

There were limitations to our study. First, it was a retrospective analysis. Second, we recognize that there was not proof of metastatic leiomyosarcomas for all of the peritoneal lesions. However, in a patient who has known leiomyosarcoma and no other primary tumor, the development of a new lesion or the interval increase in size of previously noted peritoneal lesions strongly suggests metastatic lesions. These criteria for metastatic disease are also used by oncologists and surgeons. Third, the prevalence of PL in our study was not the true prevalence of this neoplasm at the time of the diagnosis because we included cases that were diagnosed as PL at follow-up CT and only 56 of the 89 patients underwent follow-up CT. We cannot determine what happened to the other patients who did not undergo follow-up CT.

In conclusion, CT is useful for determining the presence or absence of PL and evaluating the morphologic features of this tumor dissemination. The CT findings of multiple peritoneal nodules either with or without central necrosis, hepatic metastases, and/or minimal or nonexistent ascites should lead one to consider PL in the differential diagnosis. Also, the prevalence of PL is thought to be greater when the primary gastrointestinal leiomyosarcoma is large in diameter, has exophytic growth, and originates in the small bowel. In addition, because peritoneal seeding is one of the most common modes of metastasis in gastrointestinal leiomyosarcoma, the entire peritoneal cavity, including the pelvic cavity, should be examined on the initial and follow-up CT scans.

	ACKNOWLEDGMENTS

 
We thank Bonnie Hami of the Department of Radiology, University Hospitals of Cleveland, Ohio for her editorial assistance in the preparation of the manuscript.

	FOOTNOTES

 
Abbreviation: PL = peritoneal leiomyosarcomatosis

Author contributions: Guarantor of integrity of entire study, H.K.H.; study concepts and design, S.E.R., H.K.H.; literature research, S.E.R.; clinical studies, S.J.M., S.K.Y.; data acquisition, S.E.R., A.Y.K.; data analysis/interpretation, S.E.R., H.K.H.; statistical analysis, S.E.R., B.G.C.; manuscript preparation, S.E.R.; manuscript definition of intellectual content, H.K.H., T.K.K., J.Y.B.; manuscript editing and revision/review, H.K.H., T.K.K., J.Y.B., S.K.Y.; manuscript final version approval, H.K.H.

	REFERENCES

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2272012126v1 227/2/385    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Rha, S. E. Articles by Yang, S.-k. Search for Related Content PubMed PubMed Citation Articles by Rha, S. E. Articles by Yang, S.-k.