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10.1245/s10434-006-9043-7
Annals of Surgical Oncology 14:222-229 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Clinicopathologic Prognostic Factors in Myxoid Liposarcoma: A Retrospective Study of 49 Patients With Long-Term Follow-Up

Suzan E. ten Heuvel, MD1, Harald J. Hoekstra, MD, PhD1, Robert J. van Ginkel, MD, PhD1, Esther Bastiaannet, MSc1 and Albert J. H. Suurmeijer, MD, PhD2

1 Department of Surgical Oncology, University Medical Center Groningen, University of Groningen, Hanzeplein 1, P.O. Box 30.0019700 RBGroningen, The Netherlands
2 Department of Pathology, University Medical Center Groningen, University of Groningen, Hanzeplein 1, P.O. Box 30.001 9700 RBGroningen, The Netherlands

Correspondence: Address correspondence and reprint requests to: Albert J. H. Suurmeijer, MD, PhD; E-mail: a.j.h.suurmeijer{at}path.umcg.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The main goal of this retrospective study was to investigate prognostic factors influencing the survival of myxoid liposarcoma (MLS) with emphasis on the role of transitional areas (TLS) and round cell morphology (RCLS).

Methods: From 1977 to 2004, 49 patients—28 men (57%) and 21 women (43%) with a median age of 44 years (range, 7–83 years)—were diagnosed with an MLS. In 42 patients, the histology could be reviewed, and tumors were classified as MLS, TLS, or RCLS. Clinicopathologic factors were analyzed for influence on survival by univariate and multivariate methods.

Results: The median follow-up of 49 patients was 101 months (range, 4–550 months). Of the 42 patients for whom histology was reviewed, 16 tumors were classified as MLS (38%), 19 as TLS (45%), and 7 as RCLS (17%). Sixteen patients (33%) developed a local recurrence after a median follow-up of 21 months (range, 2–108 months). Thirteen patients (27%) developed metastases. The median interval between diagnosis and metastasis was 41 months (range, 0–222 months). Median survival after metastasis was 18 months (range, 1–179 months). The 5- and 10-year disease-specific survival rates were 85% and 72%, whereas the 5- and 10-year overall survival rates were 83% and 68%, respectively. Age at presentation (P = .02), tumor grade (P = .01), and tumor size (P = .005) were significant prognostic factors associated with survival. Tumor grade was the only independent prognostic variable that remained significant with multivariate analysis. A TLS presentation had no negative influence on patient survival.

Conclusions: Age at presentation, tumor grade, and tumor size had a negative influence on survival by univariate analysis, whereas tumor grade was the only independent prognostic factor by multivariate analysis. TLS was not associated with poor outcome.

Key Words: Sarcoma • Treatment • Pathology • Metastases • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Myxoid liposarcoma (MLS) belongs to the group of soft tissue sarcomas with lipomatous differentiation; this group also comprises well-differentiated liposarcoma/atypical lipomatous tumor, pleomorphic liposarcoma, and dedifferentiated liposarcoma. MLS is the second most common type of liposarcoma, representing approximately one third of all liposarcomas and 10% of all adult soft tissue sarcomas.1,2 MLS has a typical clinical presentation and meta-static behavior, quite different from the other liposarcoma histotypes. MLS frequently presents as a slow-growing, deep-seated tumor in the lower extremity of a relatively young adult patient. Metastases are often detected in other deep soft tissue locations, such as the retroperitoneum or extremities.1–6

MLS has a distinct morphology, which is rarely confused with other monomorphic soft tissue tumors with myxoid stroma and lipomatous differentiation.1,2 Moreover, specific chromosomal translocations have been discovered in MLS, which consists of the fusion of the FUS and CHOP genes [(t12;16)(q13;p11)] in 90% of tumors and fusion of the EWS and CHOP genes [(t12;22)(q13;q12)] in >5% of tumors. In difficult cases, detection of these translocations with polymerase chain reaction methods allows the pathologist to make a specific diagnosis of MLS.7–10

In the past, paucicellular MLS and hypercellular round cell liposarcoma (RCLS) were considered separate entities, even though transitions between MLS and RCLS were often recognized. However, with the identification of the specific translocations in both MLS and RCLS, it became clear that these lesions represent the ends of a morphological and biological spectrum of the same tumor entity.1,2 MLS with >5% RCLS has a higher tendency to metastasize, and this is associated with poorer survival.11–13 As a consequence, pure MLS is considered a low-grade sarcoma, and MLS with >5% round cell morphology is considered a high grade sarcoma.14 In addition, transitional morphological phenotypes intermediate between paucicellular MLS and hyper-cellular RCLS have been recognized. The biological significance of this transitional type of MLS with increased cellularity (TLS) is still uncertain.1,11,12

In this retrospective study of MLS, the prognostic effect of myxoid, transitional, and round cell morphology, in addition to other more established clinicopathologic prognostic factors, including age at presentation, tumor localization, tumor size, and tumor grade, was studied. Clinical end points evaluated were times to local recurrence, metastasis, and death of disease. The results of this study are discussed with respect to the limited existing literature.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Forty-nine patients were treated between 1977 and 2004 for an MLS at the University Medical Center Groningen. Clinical and pathologic features were retrieved from the Groningen Sarcoma Database patient files and the pathology database. All patients underwent a surgical resection of the tumor with curative intent. Seven patients received hyperthermic isolated limb perfusion with tumor necrosis factor {alpha} and melphalan before surgery.15 Two patients with a tumor in the thigh received preoperative radiotherapy and neoadjuvant chemotherapy according to the so-called Eilber protocol.16 These two patients also received postoperative radiotherapy. Twenty-four patients (49%) received 60 to 70 Gy of postoperative radiotherapy. Six patients received chemotherapy: five patients for metastatic relapse and one patient for an irresectable local recurrence. Tumor size was recorded at 5- and 10-cm cutoff values, in accordance with the tumor-node-metastasis staging system for soft tissue sarcomas.17

Hematoxylin and eosin–stained sections from tumor resections were available for review in 42 cases. All specimens were reviewed by an experienced sarcoma pathologist (A.J.H.S.). All sections were scored by dividing MLS into paucicellular MLS, TLS, and RCLS according to the criteria described by Smith et al.12 MLS was characterized by the presence of lipoblasts in varying numbers, primitive mesenchymal cells with minimal nuclear pleomorphism deposited in a myxoid stroma, and a distinct plexiform vascular pattern composed of thin-walled capillaries. TLS areas were hypercellular compared with the low cellularity of MLS, but the cells remained spindled, the plexiform vascular pattern remained easily discernible, and the cells were separated by at least some myxoid stroma. RCLS areas were characterized by a marked increase in cellularity in which the cells were round and separated by little or no stroma. In these areas, the mitotic index was generally increased, and a plexiform vascular pattern was difficult to recognize secondary to the overgrowth of primitive round cells.12 In this study, tumors with >5% TLS areas or 5% RCLS areas were categorized as TLS and RCLS, respectively. Tumors with >5% TLS and 5% RCLS were categorized as RCLS. Typical examples of TLS and RCLS are shown in Fig 1Go. All tumors could be classified on histological analysis. Polymerase chain reaction for specific chromosomal translocations was not performed. Tumor grade was determined according to the French sarcoma grading system.14 MLS and TLS were considered low-grade tumors (grade 1), whereas RCLS was considered a high-grade tumor (grade 2). Tumor recurrences and tumor metastases were diagnosed with imaging studies and confirmed with histological analysis. Time to recurrence and metastasis, disease-free survival (DFS), and overall survival (OS) were calculated by using the date of the histological diagnosis as the starting point. Clinical follow-up data were obtained from all patients by using information from our tumor registry and medical records.


Figure 1
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  		FIG. 1. Typical histology of transitional areas (A) and round cell areas (B) in myxoid liposarcoma (stain, hematoxylin and eosin; high-power magnification).

 
OS and disease-specific survival (DSS) curves were generated with the Kaplan-Meier method. Fisher’s exact tests were used to assess associations between factors. Clinical and pathologic prognostic factors in Kaplan-Meier curves were analyzed by the log-rank test, and all univariate significant factors were subsequently analyzed in a multivariate fashion with Cox proportional hazard regression.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient and Tumor Characteristics
There were 28 men (57%) and 21 women (43%) with a median age at presentation of 44 years (range, 7–83 years). All patients in this series presented with localized disease. Forty-one tumors (84%) were located in the lower extremity, with the following distribution: 21 in the thigh, 7 in the lower leg, 5 in the gluteal region, 5 around the knee, and 3 in the inguinal region. Of the 8 remaining tumors, 3 were intrathoracic, 2 were retroperitoneal, 1 was intra-abdominal, 1 was in the lower arm, and 1 was in the head and neck area.

Histological review of the 42 MLS resection specimens resulted in the following subtyping: 16 MLS (38%), 19 TLS (45%), and 7 RCLS (17%). All 7 RCLS cases had areas with >5% round cell morphology, whereas none of the cases showed >25% round cell areas.

Tumor size could be retrieved from the pathology reports in 39 cases. The median tumor size was 12 cm (range, 1–40 cm); 7 tumors (18%) were ≤ 5 cm, 11 tumors (28%) were >5 cm but ≤ 10 cm, and 21 tumors (54%) were >10 cm.

Treatment
In all patients, surgical management of the tumor was with curative intent. Reviewing the specimens, a macroscopic radical (R0) resection with narrow margins of the tumor was documented in 37 cases (76%), and a microscopic involved resection margin (R1 resection) was involved in 12 cases. The 24 patients (49%) who received postoperative radiotherapy consisted of 6 patients with an R1 resection and 18 of 37 patients with a R0 resection (including all 6 patients with preoperative hyperthermic isolated limb perfusion).

Follow-Up Results
The OS, DSS, and DFS with a median follow-up of 101 months (range, 4–550 months) are presented in Fig. 2Go. Differences in OS between patients who developed local recurrence and patients who developed metastasis (with or without local recurrence), as opposed to patients without local recurrence or metastasis, are shown in Fig. 3Go.


Figure 2
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  		FIG. 2. Kaplan-Meier curve showing overall survival (OS), disease-specific survival (DSS), and disease-free survival (DFS) of 49 patients with myxoid liposarcoma.

 

Figure 3
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  		FIG. 3. Kaplan-Meier curves showing survival of 11 patients with local recurrence (and no metastasis) and 12 patients with metastatic relapse as opposed to patients with no evidence of disease (NED) during follow-up. Note the long survival of patients with metastatic relapse.

 
Sixteen patients (33%) developed a local recurrence after a median follow-up of 21 months (range, 2–108 months). Eight patients treated for local recurrence were alive without evidence of disease, one patient was alive with disease, and seven patients had died of disease, of whom five patients had developed meta-static disease, whereas the other two patients had uncontrollable local recurrence in the retroperitoneum and mediastinum.

The risk of local recurrence was associated with tumor location; 6 (86%) of the 7 patients with a nonextremity tumor location developed a local recurrence, compared with 10 (24%) of 42 patients with a tumor in the lower or upper extremity (P = .003). The development of local recurrence was not related to the histological subtype of the primary tumor. The risk of local recurrence for a primary tumor classified as MLS, TLS, or RCLS was 38%, 32%, and 29%, respectively, which was not significant (P = .897). After the development of a local recurrence, the 5-year survival was 81% (Fig. 3Go).

According to current Dutch soft tissue sarcoma guidelines,18 all 42 patients with R1 or marginal R0 resection of a tumor that was located in an extremity were eligible for postoperative radiotherapy. However, only 24 of these 42 patients actually received postoperative radiotherapy. Comparison of these patient groups revealed 8 local recurrences (44%) in the nonirradiated group of 18 patients, compared with 2 local recurrences (8%) in the irradiated group of 24 patients (P = .01).

Of the 34 patients with an R0 tumor that was located in an extremity, 7 (21%) developed a local recurrence. Of the eight patients with an R1 tumor that was located in an extremity, three (38%) developed a local recurrence (P = .369).

Thirteen patients (27%) had a metastatic relapse after a median follow-up of 41 months (range, 0–222 months). Clinical and pathologic features, including treatment and follow-up events of the 13 patients found to have metastatic disease, are listed in Table 1Go. Ten patients (77%) had extrapulmonary metastases, of whom three developed lung metastases during follow-up. The three remaining patients developed lung metastases only. At last contact, 1 patient with metastatic disease was alive without evidence of disease, 2 patients were alive with disease, and 10 patients had died of disease. The 5-, 7-, and 10-year survival rates of patients after development of metastatic disease were 67%, 58%, and 34%, respectively (Fig. 3Go).


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  		TABLE 1. Clinical and pathologic features of the 13 patients with metastatic disease
 
The OS, DFS, and DSS according to Kaplan-Meier analysis are presented in Fig. 2Go and Table 2Go. All seven patients with a tumor ≤5 cm were alive without evidence of disease with a median follow-up of 178 months (range, 5–293 months). In univariate analysis, a worse DSS was significantly associated with tumor size by using >5 cm as a cutoff value (P < .05), age at presentation >45 years as a cutoff value (P < .02), and presence of >5% round cell morphology, defined as grade 2 RCLS (P = .0005). Tumor location (extremity vs. nonextremity), tumor size >10 cm, and tumors with transitional morphology defined as TLS were not significantly associated with survival. Moreover, preoperative hyperthermic isolated limb perfusion and postoperative radiotherapy were not significantly associated with survival. In multivariate analysis of age at presentation, tumor size, and tumor histology, grade 2 RCLS was the only variable that remained significantly associated with DSS (P = .033). A Kaplan-Meier curve of patient survival related to tumor grade is presented in Fig. 4Go.


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  		TABLE 2. Literature review of clinicopathologic features and their relation to prognosis in MLS
 

Figure 4
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  		FIG. 4. Kaplan-Meier curves showing survival of 43 patients by histological type and grade (P = .0004). Myxoid liposarcoma (MLS) is grade 1, and round cell liposarcoma (RCLS) is grade 2.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Researchers at the Memorial Sloan-Kettering Cancer Center (MSKCC) have created a nomogram after statistical analysis of DSS in 2163 adult patients with the most common types of soft tissue sarcoma. This nomogram uses significant and well-established predictors of survival, including histological tumor type, tumor site (e.g., lower extremity), superficial or deep localization, tumor size, tumor grade, and patient age. Although not perfectly accurate, the nomogram can be used to predict the probability that a patient will die of soft tissue sarcoma; it has been calculated that nomogram predictions are within approximately 8% of the actual probability on average.18

Using the calculator on the MSKCC Web site (http://www.mskcc.org/mskcc/html/6181.cfm), we entered the common clinicopathologic features of MLS (a low-grade liposarcoma >10 cm deeply situated in the lower extremity of a 45-year-old patient), and this resulted in an estimated 4-, 8-, and 12-year DSS ranging from 85% to 100%, 78% to 94%, and 74% to 90%, respectively. As might be expected, the actual 5- and 10-year DSS rates of 85% and 72% in our clinicopathologic analysis of 49 patients with MLS are comparable to those obtained with the nomogram.

The MSKCC nomogram can also be used to further gain insight into the relative importance of each separate prognostic variable. For instance, when using the 8-year DSS of 86% ± 8% of the average MLS patient as baseline, the difference in estimated DSS is –25% for a patient with a high-grade tumor (instead of a low-grade tumor), –6% for a patient age of 65 years (instead of 45 years), and +9% for tumor size ≤5 cm (instead of >10 cm). From these calculations, one might conclude that tumor grade is prognostically much more important than patient age and tumor size. However, it should be pointed out that the sarcoma survival odds in the MSKCC nomogram are based on all histological types of liposarcomas and not just on MLS. Therefore, we have compared the results in our MLS study with those of previous retrospective prognostic studies performed by three large cancer centers in the United States, including the MSKCC, as summarized in Table 2Go.11–13

As pointed out by others, direct comparison of results derived from retrospective prognostic studies is hampered by inevitable problems due to differences in patient and tumor characteristics, treatment, and statistical analysis. Clearly, statistical power of significance of prognostic factors depends on the number of cases and follow-up time. In this respect, it is notable that the median follow-up of 101 months in our series is the longest follow-up reported to date. The two largest studies (from MSKCC and Mayo Clinic) have also used Kaplan-Meier methods and multivariate analysis with Cox proportional hazards analysis.11,13 In the comparatively small study performed by the Cleveland Clinic Foundation, only event-free survival could be measured.12 We have chosen cutoff values for grade (5% round cell morphology), age (45 years), and tumor size (5 and 10 cm) to allow optimal comparison with the two larger studies. Moreover, the cutoff values applied for tumor size and tumor grade are well established and already used in the 2002 World Health Organization classification for histological typing and the 2002 American Joint Committee on Cancer classification for staging of soft tissue sarcoma.1,17 In addition, age 45 is the median age at presentation of patients with MLS, as found in the other studies, and is thus likely to provide the strongest statistical power.13 With respect to clinicopathologic features potentially influencing prognosis, important differences between the studies discussed herein are differences in the relative number of tumors presenting in the (lower) extremity, of tumors ≤5 cm or >10 cm, and of grade 2 tumors with >5% round cell morphology (Table 2Go).

The prognostic factors significantly associated with worse DSS by univariate analysis in our study were tumor grade (grade 2 with >5% RCLS vs. grade 1; P = .0004), patient age (>45 vs. ≤45 years; P = .02), and tumor size (>5 vs. ≤5 cm; P = .0475). By multivariate analysis, only 5% RCLS (tumor grade 2) was significantly associated with worse DSS (P = .03), in accordance with the MSKCC study.11 In the study from the Cleveland Clinic, 5% RCLS (tumor grade 2) was significantly associated with event-free survival.12 The higher cutoff value of 25% RCLS was significantly associated with OS by multivariate analysis in the Mayo Clinic series, but not in the MSKCC series.11,13

We were only able to consider 5% round cell morphology as a cutoff value for grade 2 MLS. None of our cases contained areas with >25% round cell morphology. The percentage of RCLS (17%) was lower compared with the other studies (27%–43%), and this may explain why the 5-year OS of 83% and the 5-year DSS of 85% were slightly better than the 5-year OS of 82% found in the Mayo Clinic series and the DSS of 80% observed in the MSKCC subgroup of 70 patients with localized disease.11–13 We and others observed that there is no association between TLS and patient survival. Moreover, in a meta-analysis only considering cases of TLS of the lower extremity in the Cleveland Clinic and University Medical Center Groningen series, TLS was not associated with poorer outcome. 12

The metastatic rate in our patient group was 27%, which is lower than that found by other groups (range, 30%–35%).11–13 This may also be due to the lower percentage of RCLS in our series. Although the median survival of patients with metastatic disease is quite long (Fig. 3Go), their outcome was poor. Of the 13 patients with metastatic relapse in our series, 10 had died of disease (after 5 to 65 months), 2 patients were alive with disease (after 28 and 135 months), and 1 patient had no evidence of disease after 16 months. Most metastases were observed in unusual soft tissue locations, which is a typical feature of MLS, as found in other studies.3–6

The local recurrence rate in this study was 33%, which is higher than that found in the MSKCC (27% in localized disease) and Mayo Clinic (14%) series.11,12 The relative number of tumors located in the extremities in our series was comparable to that in the MSKCC series, whereas most tumors in the Mayo Clinic series were in the extremities.11,12 In our series, 24% of tumors in the extremities recurred, as opposed to 86% of tumors with a nonextremity location.

Surgical margins and postoperative radiotherapy are the main factors that are associated with the development of local recurrence. We were not able to study the significance of surgical margin status in this study, but not surprisingly, in the larger MSKCC and Mayo Clinic series, local recurrence–free survival was significantly related to both negative surgical margins and extremity versus nonextremity location.11,12

In our study, the chance of local recurrence was not related to histological subtype (MLS, TLS, or RCLS), whereas in the MSKCC study, development of local recurrence was related to >5% increased cellularity, defined as TLS in our study (P < .01 by univariate analysis).11 In our series, 42 tumors that were located in an extremity were resected with an R1 or a narrow R0 margin, which is an indication for radiotherapy according to current soft tissue sarcoma guidelines in The Netherlands.15 Patients who did not receive radiotherapy had more recurrences than patients who did not. In the Mayo Clinic study, no significant difference was seen in local recurrence rate between patients treated with marginal resection with radiotherapy versus wide surgical resection alone.13

In summary, this study in 49 patients with MLS showed that tumor size, age at presentation, and tumor grade (grade 2 being defined by 5% RCLS) were associated with worse DSS by univariate analysis, whereas tumor grade was the only independent prognostic factor that remained significant by multivariate analysis. In a meta-analysis of our study and one previous study, TLS of the lower extremity was not associated with a worse outcome.

Received for publication October 17, 2005. Accepted for publication April 17, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  14. Guillou L, Coindre JM, Bonichon F, et al. Comparative study of the National Cancer Institute and French Federation of Cancer Centers Sarcoma Group grading system in a population of 410 adult patients with soft tissue sarcoma. J Clin Oncol 1997; 15:350–62.[Abstract/Free Full Text]
  15. Nijhuis PH, Pras E, Sleijfer DT, Molenaar WM, Koops HS, Hoekstra HJ. Long-term results of preoperative intra-arterial doxorubicin combined with neoadjuvant radiotherapy, followed by extensive surgical resection for locally advanced soft tissue sarcomas of the extremities. Radiother Oncol 1999; 51:15–9.[CrossRef][Medline]
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