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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.09.005 on April 12, 2004

Annals of Surgical Oncology 11:483-490 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Evaluation of a Clinically Applicable Post-Surgical Classification System for Primary Retroperitoneal Soft-Tissue Sarcoma

Thijs van Dalen, MD, Adriaan Hennipman, MD, Frits van Coevorden, MD, Harald J. Hoekstra, MD, Bert N. van Geel, MD, Piet Slootweg, MD, Cherry F. Albus Lutter, MD, Murray F. Brennan, MD and Samuel Singer, MD

From the Dutch Soft Tissue Sarcoma Group, Vereniging van Integrale Kanker Centra (TvD, AH, FvC, HJH, BNvG, PS, CFAL), Utrecht, The Netherlands; and the Sarcoma Disease Management Team, Department of Surgery, Memorial Sloan-Kettering Cancer Center (MFB, SS), New York, NY.

Correspondence: Address correspondence and reprint requests to: Samuel Singer, MD, Memorial Sloan-Kettering Cancer Center, Department Of Surgery, H1210, 1275 York Avenue, New York, NY; e-mail: Singers{at}Mskcc.Org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The present AJCC/TNM staging system is of limited value for prediction of prognosis for patients with retroperitoneal sarcoma. The objective of the present study was to develop a postsurgical classification system that would enable comparison of outcomes for patients with primary retroperitoneal soft-tissue sarcoma.

Methods: Four classes were defined: I, low-grade/complete resection/no metastasis; II, high-grade/complete resection/no metastasis; III, any-grade/incomplete resection/no metastasis; and IV, any-grade/any resection/distant metastasis. The prognostic value of this classification system was analyzed in a population-based multicenter group(MCG) of patients with primary retroperitoneal soft-tissue sarcoma (n = 124) and in a cohort of patients treated in a single tertiary referral center (SCG; n = 107).

Results: Overall 5-year survival rates were 55% in the SCG and 43% in the MCG (P = 0.02). Class III (incomplete resection) was more frequent in the MCG than in the SCG (33% vs. 16%; P = 0.02). In the SCG, stage-specific 5-year survival rates were 89%, 40%, 26%, and 17% for classes I, II, III, and IV, respectively (P < 0.001), in comparison with 68%, 46%, 24%, and 0% in the MCG (P < 0.001). In a comparison of class-specific survival between the groups, only class I patients in the SCG had significantly better survival than class I patients in the MCG (P = 0.048).

Conclusions: Classification based on grade, completeness of resection, and distant metastasis offers a reproducible prognostic tool that can be used to evaluate treatment strategies for primary retroperitoneal soft-tissue sarcoma. The probability of complete resection was significantly higher in the SCG than in the MCG. In patients with low-grade, completely resected sarcoma, there is a significant survival benefit with treatment in a high-volume tertiary center of excellence.

Key Words: Classification • Outcomes • Prognostic factors • Retroperitoneal • Sarcoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Surgery is the primary treatment modality for patients with retroperitoneal soft-tissue sarcoma (RSTS). Sarcoma grade and completeness of surgical resection are the two most important prognostic factors for survival.1–3 Despite extensive retroperitoneal resections, obtaining locoregional control remains difficult even in the most experienced hands.2,4 A prognostic tool enabling comparison of outcomes for patients with RSTS would be useful for designing clinical trials, comparing results from different institutions, and evaluating the efficacy of new treatment modalities.

The recently revised UICC-TNM staging system for soft-tissue sarcoma, incorporating information about malignancy grade, tumor size, deep versus superficial location, lymph node status, and metastasis has been designed and validated for soft-tissue sarcoma arising in the extremities.5,6 For RSTS, the applicability of the TNM staging system seems limited, because apart from malignancy grade and metastasis, all other factors in this classification are less important predictors for survival. This is largely a result of the large size and deep location of most retroperitoneal sarcomas at the time of initial diagnosis.

In the present study, a simple postsurgical classification system based on well documented predictors of survival for retroperitoneal sarcoma is evaluated. The prognostic value of this classification/staging is analyzed in a population-based multicenter group (MCG) of patients with primary RSTS and in a cohort of patients treated in a tertiary referral center, a single-center group (SCG).


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A classification was developed with use of malignancy grade (high vs. low), completeness of resection (complete vs. incomplete), and distant metastasis (no metastasis vs. metastasis), and this classification was analyzed in two cohorts of patients who underwent surgery for primary RSTS: a population-based multicenter group (MCG) of 124 patients from the Netherlands and a group of 107 consecutive patients treated at a single tertiary referral center (SCG) in the United States. The median follow-up time from diagnosis for surviving patients was more than 5 years in both groups.

The Dutch Multicenter Group
In the Dutch group, information about patients was obtained with help from the Dutch Network and National Database for Pathology (PALGA). All patients who were registered in the Netherlands between 1989 and 1994 as having a newly diagnosed primary RSTS were selected by this registry (n = 301). Through PALGA, a questionnaire about the histopathology of the tumor (histologic type, malignancy grade) was sent to the involved pathology laboratories (n = 58), including a request for the original slides and pathology report. A second questionnaire regarding the clinical course of the patient was forwarded to the consultant involved in the treatment of the patient, including a request for the operative notes.

Data were returned on 202 patients (67% response), but 51 patients did not have primary RSTS: 33 patients were first treated before the study period, while 18 patients had conditions other than RSTS. Of the 151 patients with primary RSTS, 17 were not offered surgery, and 8 patients were excluded from the study because of grossly incomplete data. Thus, complete data was available on 124 patients. These 124 patients were treated by 87 different attending clinicians, and this patient cohort was considered a multicenter group (MCG).

The following clinical factors were recorded: date of birth and gender of the patient, tumor size, result of surgery (complete vs. incomplete resection), the presence of metastasis, defined as lymphatic spread and/or hematogenous dissemination to the liver or lungs at the time of surgery, and the date of death. A complete resection was defined as a complete gross resection of the sarcoma, independent of the microscopic resection margin. Slides of the original specimens were reviewed by two pathologists (P. S. and Ch. A-L) for histologic type7 and grade.8,9 The degree of malignancy was scored as low, intermediate, or high grade on the basis of the classification of Trojani an Coindre. Follow-up data were obtained from the clinical questionnaire and by annually consulting the attending clinician and/or the patient’s general practitioner (until January 2000). Survival was measured from the date of operation. At least a 5-year follow-up was completed for all patients, whereas median follow-up was 84 months for patients alive at the end of the study.

The Memorial-Sloan Kettering Cancer Center Single-Center Group
The second group consisted of 107 consecutive patients referred to the Memorial-Sloan Kettering Cancer Center (MSKCC) and operatively treated for primary RSTS between 1992 and 1997. This cohort of patients was considered to as the single-center group (SCG). For these patients, the aforementioned clinicopathological data had been collected prospectively. Histologic type was determined according to the same guidelines as in the Dutch group, whereas grade was defined as high or low, on the basis of the classification proposed by Hajdu.10 Postoperatively, patients were monitored in a soft-tissue sarcoma clinic until January 2002. Follow-up was complete, and median follow-up time from the operation was 64 months for those alive at the end of the study (Table 1).


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  		TABLE 1. Comparison of patient- and tumor characteristics in the Dutch- and the MSKCC-study group
 
The Postsurgical Classification System
Based on malignancy grade (low vs. high), completeness of resection (complete vs. incomplete), and distant metastasis (no metastasis vs. metastasis), four classes were defined:

The discrepancy between the three degrees of malignancy in the Trojani classification as used in the Dutch group and the low- versus high-grade classification in the MSKCC cohort was overcome by combining the patients with intermediate and high-grade sarcomas in the Dutch group into a single high-grade group, as proposed in the latest UICC-TNM staging classification (2002) and illustrated in Figure 1.5



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  		FIG. 1. TNM-staging of soft tissue sarcomas (2002).

 
The prognostic value of this classification was assessed separately in the MCG and in the SCG. Subsequently, class-specific outcome was compared between the two groups.

In addition, patients were also classified according to the UICC-TNM staging classification (2002) for STS,5 and stage-specific outcome was assessed in the MCG and the MCG.

Statistical analysis
The proportion of patients who underwent a complete resection of the retroperitoneal sarcoma and the frequencies of the consecutive stages for the two groups were compared with the {chi}2 test. Overall sarcoma-specific survival was estimated with the Kaplan-Meier method,11 and curves were plotted for graphic display of differences in outcome. The log-rank test of survival analysis12 was used to compare the overall sarcoma-specific survival distributions of the various classes and patient groups (MCG and the SCG).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The median ages were 58 years and 61 years in the Dutch MCG and the MSKCC SCG, respectively. There was a 23% difference in gender distribution between the two patient groups, with women accounting for 59% of the MCG and only 36% of the SCG (P = 0.001; Table 1). Liposarcomas were more common in the SCG, accounting for 50% of the histologic types, compared with 42% of the histologic types in the MCG (P = 0.002). However, the frequency of low-grade sarcomas was similar in both groups (45%). The frequency of T-, G-, N-, and M-stage criteria and subsequent TNM stage classification was also similar in both groups (Table 2). Complete resection of the tumor was achieved in 77 of 124 patients (62%) treated by the MCG, compared with 88 of 107 patients (82%) in the SCG (P = 0.002). The 5-year overall sarcoma-specific survival rates were 43% and 55% in the MCG and SCG, respectively (P = 0.015; Fig. 2).


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  		TABLE 2. Comparison of T, N, M and G-stage determining factors and stage groups of retroperitoneal sarcomas according to the TNM staging of STS 20025
 


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  		FIG. 2. Overall survival for patients with retroperitoneal sarcoma in a single-center and multicenter group (n = 231).

 
On the basis of the proposed classification criteria, class I disease (low-grade/complete resection/no metastasis) accounted for 30% (n = 37) and 37% (n = 40) of the MCG and SCG, respectively. Class II disease(high-grade/complete resection/no metastasis) accounted for 31% (n = 39) and 41% (n = 44) of the MCG and SCG, respectively. Class III disease (any grade/incomplete resection/no metastasis) accounted for 33% (n = 42) and 16% (n = 17) of the MCG and SCG, respectively (P = 0.02). Class IV disease (any grade/any resection/distant metastasis) accounted for 5% (n = 6) and 6%(n = 6) of the MCG and SCG, respectively.

Figure 3 shows class-specific overall survival in both cohorts. In the MCG (Fig. 3A), the overall class-specific 5 year survival rates were 68%, 46%, 24%, and 0% for classes I to IV. These survival differences were statistically significant (P < 0.001). In the SCG (Fig. 3B), class-specific 5-year survival rates were 89%, 40%, 26%, and 17%, respectively (P < 0.001). When comparing class-specific survival between the two populations by class, we noted that patients in the MSKCC SCG (Fig. 4A) who had class I disease (low-grade, complete resection, no metastasis) had significantly better survival than those in the Dutch MCG (P = 0.048). In contrast, no survival differences between the MCG and the SCG were observed for patients with high grade/completely resected tumors (class II; Fig. 4B), patients with incompletely resected tumors (class III; Fig. 4C), and patients with synchronous metastasis (class IV; Fig. 4D).



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  		FIG. 3. Overall survival for (A) patients with retroperitoneal sarcoma in the multicenter group, by class (n = 124), and (B) patients with retroperitoneal sarcoma in the single-center group, by class (n = 107).

 


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  		FIG. 4. Overall survival for patients with (A) class I (low grade/complete resection) retroperitoneal sarcoma in a single-center group and a multicenter group (n = 77); (B) stage II (high grade/complete resection) retroperitoneal sarcoma in a single-center group and a multicenter group (n = 83); (C) stage III (incomplete resection) retroperitoneal sarcoma in a single-center group and a multicenter group (n = 59); and (D) stage IV (metastasis) retroperitoneal sarcoma in a single-center group and a multicenter group (n = 12).

 
Based on the T-, G-, N-, and M-stage criteria of the TNM-staging classification (Table 2), stage I disease accounted for 43% (n = 54) and 45% (n = 48) of the MCG and SCG, respectively, and stage II disease for 2% (n = 2) and 1% (n = 1) of the MCG and SCG, respectively. Stage III disease accounted for 48% (n = 60) and 47% (n = 48) of the MCG and SCG, respectively, and stage IV disease accounted for 5% (n = 6) and 6%(n = 6) of the MCG and SCG, respectively. Figure 5 shows TNM-stage-specific overall survival in both cohorts. In the MCG (Fig. 5A), the overall TNM-stage-specific 5-year survival rates were 61%, 0%, 33%, and 0% for stages I to IV (P < 0.001). In the SCG (Fig. 5B), TNM-stage-specific 5-year survival rates were 83%, 100%, 31%, and 17%, respectively (P < 0.001). The rarity of TNM stage II disease precludes any statistical statement regarding prognosis. The only patient in the SCG did well in the 5-year follow-up. In contrast, the two patients with TNM stage II disease in the MCG had both died 1 year following operative treatment.



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  		FIG. 5. Overall survival for patients with (A) retroperitoneal sarcoma in the multicenter group, by TNM stage (n = 122), and (B) retroperitoneal sarcoma in the single-center group, by TNM stage (n = 106).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study a clinicopathologic classification system for primary RSTS based on malignancy grade, completeness of resection, and distant metastasis was evaluated. Conventionally the extent of resection is not included in a staging/classification system, but in the absence of an appropriate system we classified patients post-resection that were R0 and R1 as complete resection. Between the four defined consecutive classes, significant survival differences were observed, in a population-based multicenter group as well as in a single-center patient cohort from a tertiary referral center. The classification system proposed is simple to apply, is reproducible, and may enable comparison of outcomes between groups of patients with primary RSTS.

Because of the rarity of this tumor, evidence-based data regarding best treatment for these patients is and will remain difficult to obtain, and current treatment is based on data from individual institutional case series. Many authors advocate extensive surgical procedures, including en-bloc resections,1,2,4,13 and some support the additional use of radiotherapy,14–16 arguing that soft-tissue sarcomas in the retroperitoneal space should be treated in a fashion similar to extremity sarcomas. The advocated beneficial effect of aggressive treatment strategies is not supported by a control group for comparison, and a good classification system that stratifies survival through assessment of key clinicopathological factors for a given patient’s sarcoma may be one way to overcome this problem. A standardized classification system would enable comparison of results from different institutions and thereby facilitate the evaluation of treatment modalities.

The present, recently revised UICC-TNM classification for soft-tissue sarcoma is designed to be applicable to soft-tissue sarcoma in all locations.5 However, this is an elaborate classification, as illustrated in Figure 1. Furthermore, although it is designed to be applicable to STS in all body areas, it has been validated only for extremity sarcomas, where the consecutive stages reflect the relative risk of death, usually heralded by the occurrence of distant metastasis.6 For retroperitoneal STS, locoregional recurrence instead of distant metastasis determines prognosis for the majority of tumors.17 In the case of retroperitoneal sarcomas, the TNM staging classification reflects merely malignancy grade, because of the uniform classification of retroperitoneal tumors as deep tumors and the rare presence of tumors <=5 cm (2% in the Dutch group; 3% in the MSKCC group), lymph node metastases (0% and 1%, respectively), and distant metastases (5% in both groups). TNM stage II retroperitoneal sarcomas (high-grade sarcomas <=5 cm) are practically nonexistent. Therefore, staging of RSTS according to the current TNM classification of soft-tissue tumors adds little to malignancy grade in determining prognosis.

In the present classification, we used malignancy grade, completeness of resection, and distant metastasis to define four stages. For this postsurgical classification the microscopic margin status is not distinguished because both R1 and R0 resections are considered complete. Accurate assessment of microscopic margin status for retroperitoneal resections is difficult, given the large size and complex three-dimensional orientation of these tumors. Malignancy grade and completeness of resection have been identified as independent prognostic factors by many authors.1,2,13,18,19 In the SCG the rate of complete resections was significantly higher (82%) than in the MCG (62%), but even in the SCG almost 20% of patients did not have a complete resection of tumor, and this figure compares favorably to resection rates from other tertiary referral centers.3,4,20 We therefore consider completeness of resection as a reflection of the biological behavior of the tumor as well as a surgeon-related factor.

Applying our "simple" classification criteria to the population-based MCG from the Netherlands and the SCG from MSKCC resulted in considerable numbers of patients in the four consecutive classes. Class III (incomplete resection) was significantly less common in the MSKCC group, which seems the likely result of the higher level of experience in this SCG or of the referral pattern and case selection for operation. In both groups the number of patients with class IV (metastatic) disease was small (5%), representing the low incidence of synchronous metastasis in patients with primary RSTS. Applying the proposed classification criteria also led in both groups to significant survival differences between the four consecutive classes.

The proposed retroperitoneal sarcoma classification system allows for comparison of survival results between the MCG and SCG and demonstrates for stage I disease (low-grade/completely resected tumors) a significant improvement in sarcoma-specific survival for the group treated in a tertiary single center of excellence for sarcoma. For patients with high-grade or incompletely resected tumors, as well as for patients with synchronous metastases, survival was not influenced by center type or expertise. Thus, the advantage of treatment in a tertiary referral center appears twofold: the chances of attaining a complete resection are better, and survival from completely resected low-grade sarcomas is improved. The higher resection rate and improved survival with completely resected, low-grade sarcoma supports the notion that patients with retroperitoneal sarcoma should be referred to a tertiary center of excellence prior to any intervention (other than radiological imaging). The fact that an improvement in outcome is not observed for the high-grade/incompletely resected patients treated at a high-volume center suggests that aggressive tumor biology is the most important determinant of outcome rather than quality of surgery for this high-risk group of patients. The simple classification system proposed will enable future efforts evaluating the efficacy of neoadjuvant/adjuvant radiotherapy, chemotherapy, or immunotherapy in addition to surgery for clinical trials in retroperitoneal sarcoma.

In conclusion, our retroperitoneal classification system based on malignancy grade, completeness of surgical resection, and distant metastasis appears to be a reproducible prognostic tool. As such, it can be used to evaluate treatment strategies for primary RSTS and may be helpful in designing clinical trials.


   ACKNOWLEDGMENTS
 
This study was supported in part by grant T32 CA 09501 from the National Institutes of Health.


   FOOTNOTES
 
A simple post-surgical classification for retroperitoneal sarcoma is proposed and validated in a single-center and multicenter group. The classification demonstrates the benefit of surgical treatment in a specialized center for low-grade/completely resected tumors.

Received for publication September 5, 2003. Accepted for publication January 23, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  3. Jenkins MP, Alvaranga JC, Thomas JM, et al. The management of retroperitoneal soft tissue sarcomas. Eur J Cancer 1996; 32A: 622–6.
  4. Stoeckle E, Coindre JM, Bonvalot S, et al. Prognostic factors in retroperitoneal sarcoma: a multivariate analysis of a series of 165 patients of the French Cancer Center Federation Sarcoma Group. Cancer 2001; 92: 359–68.[CrossRef][Medline]
  5. TNM Classification of Malignant Tumours. 6th ed. New York: Wiley, 2002.
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  7. Enzinger and Weis’s Soft Tissue Tumors. 4th ed. St. Louis: Mosby, 2001.
  8. Trojani M, Contesso G, Coindre JM, et al. Soft-tissue sarcomas of adults; study of pathological prognostic variables and definition of a histopathological grading system. Int J Cancer 1984; 33: 37–42.[Medline]
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  14. Jones JJ, Catton CN, O’Sullivan B, et al. Initial results of a trial of preoperative external-beam radiation therapy and postoperative brachytherapy for retroperitoneal sarcoma. Ann Surg Oncol 2002; 9: 346–54.[Abstract/Free Full Text]
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  16. Petersen IA, Haddock MG, Donohue JH, et al. Use of intraoperative electron beam radiotherapy in the management of retroperitoneal soft tissue sarcomas. Int J Radiat Oncol Biol Phys 2002; 52: 469–75.[CrossRef][Medline]
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