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Annals of Surgical Oncology 8:290-299 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Gastrointestinal Stromal Tumors and Leiomyosarcoma of the Abdomen and Retroperitoneum: A Clinical Comparison

Bryan M. Clary, MD, Ronald P. DeMatteo, MD, Jonathan J. Lewis, MD, Denis Leung, PhD and Murray F. Brennan, MD

From the Departments of Surgery (BMC, RPD, JJL, MFB) and Biostatistics (DL), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Dr. Murray F. Brennan, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-794-3184; E-mail: brennanm{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Introduction: The present study was undertaken to define the clinical differences between leiomyosarcomas (LMS) occurring within the abdomen and retroperitoneum and gastrointestinal stromal tumors (GIST).

Methods: It was a retrospective, single-institution review of patients treated for intra-abdominal and retroperitoneal GIST and LMS from July 1, 1982 through August 1, 1999.

Results: A total of 561 patients, 239 with GIST and 322 with LMS, were identified. Patients with GIST were older, with a median age of 58 years versus 54 years in the LMS group (P < .01). The majority of patients with GIST were male (58%), whereas 68% of LMS patients (excluding gender-specific sites) were female (P < .01). The 5-year disease-specific survival for GIST and LMS were 28% and 29%, respectively. The presentation status and ability to achieve a complete surgical resection were the main independent predictors of outcome for both GIST and LMS. Local and distant recurrence was common in both. The pattern of distant recurrence differed: 50% of all first-site GIST recurrences involved the liver, whereas 30% of all LMS first-site recurrences involved the lungs.

Conclusions: Although the two patient populations appear to be distinct, their clinical courses are similar. The pattern of distant spread follows the known patterns of hematogenous dissemination. Complete surgical resection is the cornerstone of treatment for primary GIST and LMS and in selected patients with local and distant recurrence.

Key Words: Gastrointestincal stromal tumor • Leiomyosarcoma—Retroperitoneal Sarcoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Gastrointestinal stromal tumors (GIST) and leiomyosarcomas (LMS) of the abdominal cavity and retroperitoneum are unusual malignancies that, until recently, were classified histologically together as leiomyosarcomas because of their similarities on light microscopy. Recent investigations using immunohistochemistry and electron microscopy have provided evidence of not only myogenic features in GIST, but also neural attributes.1–4 The cellular origin of GIST has been proposed to be the interstitial cell of Cajal, an intestinal pacemaker cell.5 This is supported by the finding that GIST and the normal Cajal cell both stain for the myeloid stem cell antigen CD34, and often are marked by the presence of the c-kit proto-oncogene. On ultrastructural examination, the Cajal cell has characteristics of both smooth muscle and neural differentiation that could explain the findings of one or both features in GIST.

The clinical outcome of patients with GIST was recently highlighted in a report from our institution on 200 patients with GIST collected over a span of 16 years.6 In this relatively recent cohort of patients who received a uniform mode of treatment, survival was dependent on the presence of metastases, tumor size, gender, and the ability to achieve a complete resection. Recurrence following a complete resection was common and involved both local (52%) and distant sites (67%). Only one third of patients had recurrence following complete resection that was local only in extent. Hepatic metastases were the predominant site of distant metastases and were a component of 63% of first-site recurrence following resection.

In contrast to the behavior of GIST, small series in the literature suggest that LMS of the abdominal cavity and retroperitoneum (not involving the GI tract) have a different pattern of metastasis, involving pulmonary sites while less commonly spreading to the liver.7,8 A recent report by Rajani et al.9 documented a higher proportion of liver metastases than previous publications, albeit in a small cohort of 17 patients. Retroperitoneal and pelvic sarcomas have been known to reach significant size before detection given their deep location and relatively asymptomatic nature at small sizes, whereas GIST are more often symptomatic at smaller sizes and tend to cause obstruction and GI bleeding. Large series of non-GIST intraabdominal and retroperitoneal leiomyosarcomas do not exist; therefore, it is not known for certain that these tumors behave in a significantly different manner than their intraabdominal GIST counterpart. To address this question, we sought to describe the clinical characteristics and outcome, including the patterns of failure, in a large, consecutive population of patients with GIST and LMS treated over a relatively short period of time at a single institution.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Clinicopathologic Variables:
From July 1982 through June of 1999, 561 patients aged 16 years or older with a diagnosis of GIST or LMS were evaluated and treated at Memorial Sloan-Kettering Cancer Center. Tumors arising within the retroperitoneum for which an intestinal site could be neither confirmed nor excluded were not included in the study. Leiomyosarcoma arising within gastrointestinal sites were classified as GIST. The pathology reports of the first 200 GIST in this series were recently reviewed and confirmed as GIST by the Pathology Department at Memorial Hospital. Patients were followed prospectively and data entered into the Sarcoma Database of the Department of Surgery. Tumor and treatment variables were recorded.

Patient data included age, sex, race, and presentation status. Presentation status was categorized as primary, metastatic, or locally recurrent, and reflected the extent of disease and the history of prior treatment at the time the patient was first seen at Memorial Hospital. Patients classified as having primary disease had a recently discovered intraabdominal tumor without metastasis. All patients with any metastatic disease were considered to have a metastatic presentation, including those with a simultaneous local recurrence.

Tumor size was recorded as the largest diameter in any dimension of the primary tumor and was stratified as <=5 cm, >5 cm to 10 cm, or >10 cm. Margins of resected specimens were analyzed for the presence of microscopic disease.

The treatment philosophy shared by the surgeons at our institution emphasizes complete gross removal of the tumor. Complete resection is defined as the excision of all gross disease, regardless of microscopic margins. Resections are classified as incomplete when the tumor is unresectable at exploration or when gross residual disease is present after resection. Resection of metastases was performed in selected patients in whom the primary tumor was controlled. Systemic chemotherapy and radiotherapy were excluded from the analyses in this report, because they were used infrequently and in a sporadic fashion.

Statistics
Patient, tumor, and treatment variables were analyzed for their relation to outcome. Survival and recurrence were the end points in this study. Only deaths confirmed to be the result of disease were counted as events; other deaths were censored at the time of death. Local recurrence was defined as the reappearance of tumor at the initial site of the primary tumor. Metastasis was recorded when the tumor spread to the liver, lymph nodes, or extra-abdominal sites. All times were calculated from the date of first admission to Memorial Hospital to the last day of follow-up or death. Survival was determined by the Kaplan-Meier method. The relations of patient, tumor, and treatment characteristics to outcome were tested by univariate analysis using the log-rank test. P < .05 was considered statistically significant. Multivariate analysis was performed with the Cox proportional hazards model.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patient Characteristics
From a total of 3968 patients with any type of sarcoma admitted for treatment to Memorial Hospital between July 1982 and June 1999, 561 patients were identified as having GIST (n = 239) or LMS arising in nongastrointestinal sites within the abdomen and retroperitoneum (Fig. 1). Of these, 293 (52%) patients presented with the primary tumor in place, of whom 63 had synchronous presentations of metastases in association with their primary. Fifty-nine patients presented with local recurrences at varying time intervals following resection at outside institutions, and an additional 209 presented with metastases following resection.



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  		FIG. 1. Presentation status of GIST and LMS patients included in study.

 
The characteristics of the entire population are depicted in Table 1. The median age of all patients was 55 years. Patients with GIST were older, with a median age of 58 years versus 54 years for the LMS group. A unimodal distribution of ages was noted in both groups (Fig. 2). Patients older than 60 years accounted for 42% of the GIST population and 32% of the LMS population (P < .01). After excluding gender-specific sites (e.g., uterus, seminal vesicle), there remained a significant difference in gender distribution. Women accounted for 58% of the GIST patients and 31% of the LMS patients (P < .01). Overall, there was no difference in the distribution of primary tumor size within the three categories: <=5 cm, >5 cm to <=10 cm, and >10 cm (P = .3). Only a minority (14%) of patients presented at the time of their original diagnosis with a tumor size of 5 cm or smaller. On presentation to our institution, 230 patients (41%) had a recent diagnosis of a localized primary, and an additional 63 patients (11%) had synchronous metastatic disease in association with their primary. Local recurrence was the sole mode of presentation in 59 patients (11%), whereas 39 (7%) patients presented with both local recurrence and metastases. Metastatic disease only was present in 170 patients (30%) on presentation to our institution.


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  		TABLE 1. Overall patient characteristics (N = 561)
 


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  		FIG. 2. Age distributions of GIST and LMS populations.

 
The characteristics of patients presenting with newly diagnosed primary tumors (n = 293) are presented in Table 2. As with the entire population, the age and gender distributions were significantly different in the two groups, as was the difference in the distribution within size categories. A greater proportion of GIST were 10 cm or smaller (58%), compared to LMS (41%, P = .03). An equivalent proportion (21%) of patients presented with synchronous metastases in association with their primary tumor. At the time of their presentation to Memorial Hospital, none of the patients with synchronous metastases had prior interventions with respect to the primary tumor. The majority of patients with localized primaries had either no prior intervention or biopsy only (190 of 230 patients). Twenty-two patients presented with a prior incomplete resection, whereas 18 had a prior complete resection. The mean follow-up for survivors was 23 months.


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  		TABLE 2. Characteristics of patients with primary presentation (N = 293)
 
The site of tumor origin in the GIST population was most commonly gastric (39%), followed by small intestine (31%) and colon/rectum (16%; Table 3). A gastric site was present in 47% of patients presenting with a primary tumor. The uterus was the most common site of origin in the LMS group (48%), although it accounted for only 33% of patients presenting with a primary tumor. The retroperitoneum was the second most common location for LMS across all types of presentation (42%), but it was more common in patients presenting with a primary tumor.


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  		TABLE 3. Site of tumor origin in patients with primary presentation of GIST and LMS
 
Treatment and Outcome
For the entire population, the mode of presentation, size of the primary tumor, and the ability to achieve a complete resection were all significant prognostic factors of disease-specific survival on univariate and multivariate analyses (Table 4). Age, gender, and histology (GIST vs. LMS) did not predict outcome on univariate analysis. The 5-year disease-specific survivals for all GIST and LMS patients, inclusive of all modes of presentation, were 28% and 29%, respectively. Tumor size, gender, presentation status, and the completeness of resection were significant prognostic indicators of disease-specific survival in patients with GIST, whereas only presentation status and the completeness of resection were significant predictors in patients with LMS (Table 5). Although we do not assign tumor grades to GIST, tumor grade was a significant predictor on univariate analysis for LMS (P < .01). It did not, however, reach significance on multivariate analysis for the entire population of LMS patients. In patients with localized primary LMS, tumor grade (high vs. low) was an independent negative predictor of disease-specific survival on multivariate analysis. Of 12 patients with low-grade, localized, primary LMS who underwent resection, none have recurred at a median follow-up of 36 months. Tumor size and gender were not predictive for patients with LMS.


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  		TABLE 4. Factors of overall disease-specific survival in all patients
 

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  		TABLE 5. Multivariate analysis of factors predictive of disease-specific survival by presenting status (primary only, any metastases)
 

The overall disease-specific survivals according to histology and stratified by presentation status are depicted in Fig. 3. Within each type of presentation (primary only, local recurrence only, any metastases) there were no differences in disease-specific survival when comparing the GIST and LMS populations. Overall, patients with any metastases did poorly, with a median survival of 17.7 months, compared to patients with local recurrence only (23 months, P = .13) and localized primaries (53.5 months, P<.01).



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  		FIG. 3. Disease-specific survival according to presentation status and histology.

 
Complete gross resection of all disease was achieved surgically in 276 of 561 patients (49%) (Table 6). Patients with localized primary GIST were more likely to have a complete resection (84%) compared to patients with localized primary LMS (65%, P < .01). Complete resection was achieved in 52% of patients presenting with local recurrence only and was not affected by the histology. In patients presenting with metastases, complete resection of all gross disease was achieved in 34%. Unlike localized primary tumors and local recurrences in the absence of metastases, where aggressive attempts at complete gross resection usually are undertaken, this approach is used selectively in patients with metastases.


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  		TABLE 6. Surgical treatment according to histology and presentation status
 
Complete resection was associated with an improved median survival across all types of presentations (Table 7, Fig. 4). No significant difference was seen when patients with completely resected GIST and LMS were compared, regardless of presentation. In GIST and LMS patients with incomplete resection, there was a statistical difference in survival in patients with local recurrence (P = .01), whereas in patients with a localized primary and metastatic presentations, there were no differences. The difference in the incompletely resected GIST and LMS patients with local recurrence is secondary to a markedly decreased survival in the small GIST population. Patients with primary localized disease who had complete resection had a median survival of 96 months. The presence of a positive microscopic margin was not a negative predictive factor of outcome in patients undergoing complete resection of localized primary tumors (P = .2), nor was it predictive of outcome in patients undergoing complete resection of locally recurrent and metastases (P = .45).


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  		TABLE 7. Median survival (months) according to treatment
 


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  		FIG. 4. Disease-specific survival according to histology and extent of resection.

 
Tumor size was not a significant predictor of outcome in any group of patients with LMS. In patients with GIST, the size of the primary was not predictive in patients presenting with primary disease (either alone or with metastases). For the entire population of patients with GIST, increasing tumor size was associated with a decrease in disease-specific survival. Anatomic location did not exert any influence on outcome within the GIST and LMS populations. Patients with gastric GIST had a similar disease-specific survival, both in the general population of GIST patients and in patients presenting with localized primary GIST. Similarly, patients with uterine LMS had a similar disease-specific survival regardless of presentation status (Fig. 5).



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  		FIG. 5. Disease-specific survival according to primary site of origin for all presentations (all patients) and patients with localizedprimaries (primary).

 
Male gender was a significant negative prognostic factor for patients with GIST on univariate and multivariate analyses. The magnitude of this effect was quite small: the 5-year survival was 27% and 31% in male and female patients, respectively (all presentations). In patients presenting with a localized primary GIST, the 5-year survivals were 43% and 50% in male and female patients, respectively.

Patterns of Failure
Complete resection of localized primary tumors was achieved in 92 patients with GIST tumors and an additional 72 patients with LMS. These 164 patients were followed prospectively, and the patterns of failure were determined. Recurrence has developed in 64 (37%) patients, with an 5-year relapse-free survival of 48%. There are 13 actual 10-year survivors, 8 of whom are free of disease. The sites of first recurrence (n = 68) occurring in 63 of these 64 patients are listed in Table 8. (In the remaining patient, the site of first recurrence was not known.) Local recurrence as a component of first recurrence occurred in 36% of GIST and 40% of LMS patients. Local recurrence was the sole site of first recurrence in 9 patients with GIST (24%) and in 10 patients with LMS (33%). The site of metastasis was significantly different between the GIST and LMS populations (P < .01). Pulmonary metastases constituted 30% of first recurrences in the LMS group, but were uncommon in the GIST patients (5%). Conversely, hepatic metastases accounted for 50% of first recurrences in the GIST group (39% as the sole site), but only 20% of LMS first recurrences. Other sites of metastases (e.g., soft tissue, bone) were uncommon in both groups.


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  		TABLE 8. Pattern of first-site recurrence following complete resection of localized primary GIST and LMS
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
GIST and LMS involving the abdomen cavity and retroperitoneum are uncommon malignancies that, before the publication of recent reports suggesting a distinct ontogeny, were commonly classified together as leiomyosarcomas. A number of recent reports, including one by us, have better defined the clinical outcome of patients with GIST.6,10,11 It is clear from these studies that survival depends most heavily on the presentation status and the ability to achieve a complete resection. Tumor size appears to be less important, although significant, whereas gender and the site of tumor origin are less important. The importance of complete resection and tumor size as predictors of outcome in localized sarcoma is similar to the experiences previously published with sarcomas involving other sites, including the extremities and the retroperitoneum.12 Only a few reports exist detailing the clinical characteristics and outcome of patients with intraabdominal and retroperitoneal leiomyosarcomas.9,13–17 Although these reports involve small numbers of patients, the poor prognosis of patients with these tumors is evident in all. The overwhelming majority of patients develop local recurrence or metastases. It is not clear from these limited studies what the factors are that are predictive of survival for patients with LMS, although there is some suggestion that tumor grade is important.9 In light of the recently reported differences in histogenesis and the relative paucity of clinical information regarding retroperitoneal and other intraabdominal leiomyosarcomas, the present study was undertaken to define the differences between GIST and LMS, with an emphasis on the patient characteristics and outcome.

We first defined the respective patient populations in these two groups. Even after excluding patients with gender-exclusive primary tumor sites (e.g., uterus), there was a significant difference in the gender distribution, with a preponderance of women in the LMS group (69%) compared to the GIST group (58%). The gender distribution in our GIST population is identical to that reported by Ng18 in 191 patients with GIST. There also was a significant age discrepancy between the two populations. The median ages were 62 years and 54 years, respectively, for patients with primary presentations of GIST and LMS. Half of all patients with a primary mode of GIST presentation were older than 60, compared to 33% of patients with LMS (P < .01). Because the GIST were more likely to present at a smaller size than LMS (P = .03), this age discrepancy is not related to a delay in presentation, but instead may reflect a biologically relevant phenomenon in the pathogenesis of these tumors. Site of tumor origin is by nature histology-specific. The distribution of GIST primary tumor sites, as previously reported,6 is similar to that in other large reported studies, with 40% arising from the stomach, followed by the small intestine (31%) and colon/rectum (16%).18,19 As in other large studies, we did not see an effect on outcome with respect to the site of GIST origin. The uterus was the most common site of LMS in the overall population (48%), followed by the retroperitoneum (42%) and the kidney and bladder (5%). The inclusion of uterine LMS with other LMS of the abdomen is supported by their similar histology as well as their similar survival across all presentations and in patients with localized primaries (Fig. 5).

The clinical outcome of patients with GIST and LMS was then compared. Including all types of presentation, there was no overall difference in 5-year disease-specific survival between the GIST (28%) and LMS (29%) populations. Tumor size, gender, presentation status, and the completeness of resection were significant prognostic indicators of disease-specific survival in patients with GIST, whereas only presentation status and the completeness of resection were significant predictors in patients with LMS (Table 5). There was no difference in disease-specific survival between patients with GIST and LMS when stratified by presentation status (Fig. 3). The ability to achieve a complete resection was a significant predictor of improved survival in both GIST and LMS groups and was true for patients with local recurrence, any metastases, and localized primaries (Fig. 4). When stratified according to presentation status and the ability to achieve a complete resection, disease-specific survival was similar across all groups except for those with incompletely resected or unresectable locally recurrent disease where, in a small number of GIST patients, the median survival was only 2 months. In patients with localized primary tumors, there was a significantly greater rate of complete resection in patients with GIST (84%) compared to patients with LMS (65%, P < .01). Because 66% of unresectable primaries were > 10 cm in size, this discrepancy in resectability was related to the greater proportion of patients with large tumor sizes in the LMS group. In both the LMS and GIST groups, complete resection of local recurrences and metastases was associated with long median survivals of 30 to 50 months, as opposed to 2 to 12 months in patients with incompletely resected or unresectable tumors.

Local recurrence following curative resection of localized primary tumors was a significant problem for both patients with GIST and those with LMS, accounting for 36% and 40%, respectively, of first-site recurrences. Given the different anatomical location and subsequent venous drainage routes, it was not surprising to find that the pattern of systemic failure was different in patients with GIST compared to patients with LMS. Hepatic metastases were a component of recurrences in 50% of all first-site recurrences in patients with GIST, whereas 20% of patients with LMS had liver involvement. Conversely, pulmonary metastases were uncommon in the patients with recurrent GIST following complete resection of localized primary tumors. Pulmonary metastases occurred in 30% of LMS patients with a recurrence.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Both GIST and LMS are uncommon malignancies with a propensity for both local recurrence and systemic dissemination. Complete surgical resection is the cornerstone of treatment for primary GIST and LMS. Carefully selected patients with resectable, locally recurrent or metastatic disease also may benefit from surgical resection. Although the recently described differences in histogenesis are supported by the finding that these two patient populations appear to be distinct, their clinical courses are quite similar. The pattern of distant spread follows the known patterns of hematogenous dissemination, thus accounting for the preponderance of hepatic and pulmonary metastases in GIST and LMS, respectively. Although regional forms of investigational therapy that address intraabdominal sites of recurrence may be appropriate for GIST, a more systemic approach is indicated in patients with LMS.

Received for publication March 18, 2000. Accepted for publication November 9, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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