Orthopaedics & Traumatology: Surgery & Research 101 (2015) 103–107

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Original article

Prognostic factors for the recurrence of myxoid liposarcoma: 20 cases

with up to 8 years follow-up
M. Lemeur a , J.-C. Mattei a,∗ , P. Souteyrand b , C. Chagnaud b , G. Curvale a , A. Rochwerger a
a
Service de chirurgie orthopédique, traumatologique et des tumeurs musculo-squelettiques du Pr Curvale, hôpital Nord, chemin des Bourrely, 13915
Marseille cedex 20, France
b
Service de radiologie du Pr Chagnaud, hôpital de la Conception, 147, boulevard Baille, 13005 Marseille, France

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: Myxoid liposarcomas (MLS) are the second most common type of liposarcoma. Although
Accepted 29 September 2014 some MRI findings are distinctively characteristics of MLS, the diagnosis can be tricky in tumors with
a large portion of round cells (RC). Known predictors of an unfavorable outcome include age, tumor
Keywords: size, high RC content and positive resection margins. The goal of this retrospective study was to define
Myxoid liposarcoma prognostic factors for recurrence, with special emphasis on the percentage of RCs and medical care
Prognostic factors provided in a non-specialized center.
Imaging
Patients and methods: Twenty patients (11 women, 9 men) with a mean age of 44.3 years (18–73) were
Recurrence
Specialized center
reviewed after a mean of 55.9 months. Six of these patients had been operated at a non-specialized center.
Round-cell percentage The diagnostic MRI was read by a specialized radiologist and the resection procedures performed by two
specialized surgeons. Tumors were labeled as either “pure myxoid liposarcoma” or “myxoid/round-cell
liposarcoma”. The local recurrence-free survival rate and mortality rate were calculated.
Results: Fifteen patients had undergone an MRI during the initial assessment. The typical MRI findings
of MLS were present in four of them. The MRI suggested a non-specific lesion in the other 11 patients.
After correlation with pathology findings, these tumors contained more than 5% round cells. The fourteen
patients treated at our facility had undergone a biopsy, while none of the ones treated outside did. Five
patients had R0 resection margins and 15 had R1 margins. Prognostic factors for recurrence consisted
of age, tumor size > 10 cm, R1 resection margins, FNCLCC grade 2 + R1 margins, medical care at a non-
specialized center, and > 5% round cells. There were eight local recurrences and three metastases (15%).
Two patients died (90% overall survival rate).
Discussion: The risk of local recurrence was 3.86 times greater in this study when the tumor contained
more than 5% RCs, which is consistent with published data. The MLS diagnosis was made only four times
based on the initial MRI because misleading nature of high RC tumors. R1 resection margins are a risk
factor for local recurrence. However, cases with R1 margins have a recurrence rate that is similar to R0
cases when the surgery is performed at a specialized cancer center. Treatment of MLS in a non-specialized
center is a key negative prognostic factor. The reported rate of metastasis varies. Atypical extrapulmonary
localizations are common, and often multifocal. MRI has been shown to be superior at detecting secondary
lesions and some have suggested that a full-body MRI should be performed.
Conclusion: Prognostic factors for the recurrence of myxoid liposarcomas have been identified. MRI
analysis is not definitive and must be supplemented by a biopsy.
© 2014 Elsevier Masson SAS. All rights reserved.

1. Introduction population. These tumors make up 17–25% of all sarcomas, which

Liposarcomas are soft-tissue tumors in a broader class of mes-
enchymal tissue neoplasms, which have an adipocyte-derived cell
∗ Corresponding author. Tel.: +33631502927.
E-mail addresses: jeancamille.mattei@gmail.com,
jaicy19@gmail.com (J.-C. Mattei).
have an incidence of 30 cases per million [1,2].
The World Health Organization classification includes five
sub-types, including myxoid liposarcomas (MLS) and round-cell
liposarcomas (RCLS) [3] (Fig. 1). MLS is the second most com-
mon type of liposarcoma. The disease spectrum is consistent with
that of other tumor types, ranging from well-differentiated pure
liposarcoma to dedifferentiated liposarcoma with high round-cell
content [4]. Well-known negative prognostic factor are patient age

http://dx.doi.org/10.1016/j.otsr.2014.09.024
1877-0568/© 2014 Elsevier Masson SAS. All rights reserved.
104 M. Lemeur et al. / Orthopaedics & Traumatology: Surgery & Research 101 (2015) 103–107

meetings: radiation therapy for R1 tumors or FNCLCC grade 2 or 3

tumors; chemotherapy for metastatic lesions.
The data were analyzed statistically using the XLSTAT® software
(Addinsoft SARL, Paris, France). The local recurrence-free survival
time was defined as the period between the initial diagnosis and the
date of the last visit. The mortality rate was calculated. Differences
between the “local recurrence” and “recurrence-free” groups were
analyzed with a Chi2 test for the qualitative variables and Student’s
t-test for quantitative variables. A multivariate analysis was carried
using a Cox proportional hazards model. Statistical tests where the
P-value was below 0.05 were considered as being statistically sig-
nificant. Survival rates were analyzed using Kaplan-Meier curves
to determine the risk of local recurrence, metastasis and death.

3. Results

The series consists of 20 patients (11 women, 9 men) who were

operated for curative purposes between January 2004 and February
2012 (Table 1). The average age was 44.3 years (range 18 to 73).
The average follow-up was 55.9 months. The tumor was located
in the lower limb in all patients: popliteal fossa in five patients
(25%), anterior aspect of thigh and sartorius muscle in four patients
Fig. 1. Section through a myxoid liposarcoma after surgical resection showing typ- (20%), adductor fossa in seven patients (35%) and gluteal area in two
ical features such as myxoid and gelatinous tissue infiltrated by fat (superior pole patients (10%). The tumor was located in the anterior compartment
and center, arrows).
of the tibia in one patient and was located in the infrapatellar fat
pad in one other patient.
Fifteen patients had undergone an MRI during the initial assess-
(> 45 years), tumor size (> 10 cm), sub-aponeurotic location, high ment. The disease-specific MRI finding of a homogeneous mass
histological grade, large percentage of round cells and positive with combined T1 hyposignal and T2 hypersignal and intralesional
resection margins [5–7]. adipose tissue was present in four patients, all of whom had pure
Magnetic resonance imaging (MRI) is essential for the diagnosis myxoid liposarcomas. In the other patients, the MRI report listed
of liposarcoma [4,8–10]. Although there are disease-specific MRI the presence of a non-specific heterogeneous mass with malig-
criteria, the diagnosis can be tricky in tumors containing a large nant appearance. After correlation with pathology results, these
number of round cells [4,10]. Treatment of these lesions requires tumors contained more than 5% round cells. The five patients who
a multidisciplinary team in a specialized cancer center [11–13].
MLS have the ability to metastasize to other soft tissues, including
Table 1
serous ones, which can make patient monitoring more challenging
Summary of study results.
[5,14,15].
The goal of the current study was to define prognostic factors Variable Value Percentage (%)
for local recurrence and metastasis, with special emphasis on the Age
percentage of round cells and treatment at a non-specialized center. Average 44.3
Range 18–73
Gender
Male 9 45
2. Patients and methods Female 11 55
Presentation
A series of 20 patients who were treated surgically for MLS Primary 14 70
between January 2004 and February 2012 were reviewed ret- Post-resection R2 4 20
Post-recurrence 2 10
rospectively. Patients were included if they had been referred
Tumor size
within our hospital network for consultation and treatment of Average 11.675
MLS. Patients who were diagnosed and underwent tumor resection Range 2–26
at our facility were included, as where those who underwent an Biopsy 14 70
unplanned tumor resection at another facility. CT scan 8 57.1
Surgery 5 35.7
All patients were treated and monitored. Patients who experi- Biopsy/excision 1 7
enced a recurrence during the follow-up period were compared to FNCLCC grade
those who did not. The initial MRI analysis was performed by a Grade 1 11 55
single specialized radiologist. All of the surgical procedures were Grade 2 9 45
Grade 3 0 0
performed by two surgeons who were specialized in the care of
“R” Classification
adult sarcomas. R0 5 25
The definitive diagnosis was made by a pathologist who spe- R1 15 75
cializes in sarcomas. The liposarcomas were labeled as either “pure Round cells
myxoid liposarcoma (MLS)” or “myxoid/round-cell liposarcoma 0–5% 5 45
10% 3 27.3
(MRCLS)”. Histological grading was performed based on the FNCLCC 25% 2 18.2
system (French Federation of Comprehensive Cancer Centers). The > 25% 1 9.5
quality of the surgical resection was defined according to the “R” Local recurrence 8 40
classification of the Union for International Cancer Control. The Metastasis 3 15
Death 2 10
need for additional treatment was determined in multidisciplinary
 M. Lemeur et al. / Orthopaedics & Traumatology: Surgery & Research 101 (2015) 103–107
Fig. 2. Specific MRI findings of a pure myxoid tumor, namely T1 hyposignal (isosignal to muscle) and T2 hypersignal in a homogeneous mass with intralesional adipose
tissue.
had sought treatment at non-specialized centers did not initially
undergo an MRI evaluation.
Fourteen patients underwent a biopsy at our facility (8 under CT
control), while none of the ones treated outside had a biopsy. An
analysis of the biopsied tissue led to the final diagnosis of MLS.
Surgical treatment was performed on 14 patients at our facility.
The resection was recorded as marginal in 3 patients (21.4%), wide
in 6 patients (42.8%) and radical in 5 patients (35.7%). The excision
was labeled as “intralesional” when the tumor was opened during
the surgery, thereby contaminating the surgical site, which leads to
a high local recurrence rate. The excision was labeled as “marginal”
when the tumor was removed macroscopically without opening it
but the dissection plane was located near the tumor’s pseudocap-
sule; this leads to a risk of microscopic amounts of residual tumor
tissue, which is also a cause of recurrence. This type of excision is
often performed when the presence of nerve and vascular elements
prevents a more extensive excision from being performed. The exci-
sion was labeled as “wide” when the entire tumor was removed
with its pseudocapsule and a sleeve of healthy tissue around it from
the same compartment. This however does not prevent the pos-
sibility of “skip” metastasis in cases of highly malignant tumors.
The excision was labeled as “radical” or compartmental when the
entire compartment containing the tumor and its pseudocapsule
were removed, including fascia, muscle insertions and septa. The
risk of recurrence is very low (< 2%) in such cases [16].
The tumor resection surgery had been performed at a non-
specialized center in the six other patients. Four were referred to
us for consultation after a type R2 resection and two after local
recurrence.
The pathology evaluation identified tumors that were 2 to 26 cm
in size. Nine were pure myxoid liposarcomas and 11 were classi-
fied as myxoid/round-cell liposarcomas, 6 of which had >5% round
cells. There were 11 grade 1 tumors and 9 grade 2 tumors (FNCLCC
scale). The resection margins were graded as R0 in 5 cases and R1 in
15 cases, 10 of which were from “planned” surgical procedures. The
diagnosis was confirmed by the detection of t(12;16) chromosome
translocation, specifically TLS-CHOP fusion [5]. Adjuvant radiation
therapy was carried out in the 15 patients with R1 resection mar-
gins or grade 2 tumors. The lesions were subfascial in all of these
cases; a small tumor size did not exclude the patient from adjuvant
radiation therapy. Adjuvant chemotherapy was prescribed in the
three patients with metastasis.
There were eight cases of local recurrence. Negative progno-
stic factors consisted of higher age (mean of 52.25 in those with
105
recurrence), tumor size (> 10 cm) in combination with age, R1
resection margins, FNCLCC grade 2 tumor with R1 margins, treat-
ment carried out in non-specialized center and > 5% round-cell
content. Only the latter component was a statistically significant
predictor of recurrence (P = 0.047).
Three patients had a metastasis; all had tumors with a large
portion of round cells. Secondary lesions were found in extrapul-
monary locations such as bone, muscle and the retroperitoneal
space. The estimated metastasis risk was 15%. Two of these patients
died. The survival rate for the patient cohort was 90% with a maxi-
mum follow-up of 8 years.
4. Discussion
This was a retrospective study of a rare disease with short inclu-
sion and follow-up periods; all of these factors combine to reduce
the statistical power of this study. There are only seven published
studies on myxoid/round-cell liposarcoma [5,6,17–21]. The small
number of patients also limits the interpretation of any statistical
tests for prognostic factors.
The percentage of round cells was the strongest prognostic
factor, as it negatively impacted local recurrence, metastasis and
survival. Grading of the round-cell content of tumors is based on
three levels and a 5% threshold. The lowest grade corresponds to
pure MLS; intermediate-grade tumors contain 0 to 5% RCs and the
highest-grade tumors contain more than 5% RCs. In this study, 11
of the 20 patients (55%) had RCs in their tumor; 6 of them had
more than 5%. Among these 6 patients, 5 had a local recurrence.
This resulted in an 83% rate of recurrence for tumors with > 5% RCs
and 21.5% rate for tumors with < 5% RCs.
In this study, the risk of local recurrence was 3.86 times greater
if the tumor contained more than 5% RCs; this is consistent with the
3.4 fold increase in risk found in a recent study [17]. There is also
evidence that the “low-grade” nature of pure myxoid liposarcomas
results in a 77% recurrence-free survival rate at 10 years [22].
Imaging findings are not definitive; many pitfalls have been
described [4,8–10]. Disease-specific MRI findings only occur with
pure myxoid liposarcoma or tumors with a low percentage of RCs
(Fig. 2). Tumors with a high percentage of RCs have an atypical
appearance (Fig. 3). In the current study, the MLS diagnosis was
strongly suggestive in only 4 of 20 patients based on the initial
MRI.
R1 resection margins are an important risk factor for local recur-
rence [5,6,17–21,23]. However, a local recurrence rate similar to R0
106 M. Lemeur et al. / Orthopaedics & Traumatology: Surgery & Research 101 (2015) 103–107
Fig. 3. Tumors containing a large percentage of round cells are more heterogeneous,
making them trickier to diagnose using MRI.
surgery can be obtained when the excision procedure is planned by
a specialized surgeon who has decided before the surgery to accept
narrow margins in high-risk areas or areas in close proximity to
vascular, nerve or bone structures [12,23–25]. The local recurrence
rate was 23% in the current study when the surgery was planned
accordingly, which is comparable to published rates [5,6,17–21].
Treatment of MLS at a facility that is not specialized in cancer
care is an important risk factor for local recurrence. Engström et al.
[12] found a 47% recurrence rate for tumors operated in this setting.
Chandrasekhar et al. [11] found a 59% rate of residual tumors out
of 363 cases. In the current study, six patients were initially treated
in a non-specialized center. Four of them had a recurrence; four
had an “intralesional” excision; only one had a preoperative MRI;
none of the patients had a preoperative biopsy; two experienced
a metastasis and one died. The French National Cancer Institute
(INCa) has set up an accredited network of facilities in 2010 that
includes three specialized centers and 25 expert centers through-
out France. Patients with a suspected sarcoma must be referred
to one of these centers so they can benefit from care given by a
specialized team.
The published rate of MLS metastasis ranges from 14 to 32%
[5,6,17–21]. Atypical extrapulmonary localizations are common,
and often multifocal [5,14–16,21,26]. MRI has been shown to be
superior at detecting secondary lesions [27,28]. It has also been
suggested that patients undergo a whole-body MRI [29]. This exam-
ination was shown to be feasible in a small series of patients and
has good sensitivity and specificity. Nevertheless, it cannot be per-
formed in all patients and should be limited to those who have the
highest risk of an unfavorable outcome based on the prognostic
factors.
MLS are atypical when it comes to adjunct treatments. They
are more sensitive to radiation therapy [30–32] and chemotherapy
[33,34] than other soft-tissue sarcomas. Trabectedin is a promis-
ing therapeutic candidate [35]. The relatively high recurrence rate
when compared to other centers (28% vs. 10%) highlights the ben-
efit of treatment in a specialized center and also points to a benefit
of neoadjuvant radiation therapy [18,19,36]. This could be partic-
ularly relevant for large tumors with a high risk of recurrence, as
it may be possible to reduce the tumor’s volume before it is surgi-
cally resected. Radiation therapy was used as an adjuvant in certain
patients in the current study. The studies reporting a better sur-
vival rate were performed on patients who received neoadjuvant
chemotherapy [6,17]. Nevertheless, the treatment protocols are not
well defined and have not been standardized.
5. Conclusion
The goal of this study was to define prognostic factors for myx-
oid liposarcomas. The risk factors for local recurrence found in this
study were consistent with the ones outlined in previously pub-
lished studies: patient above 45 years of age, tumor size greater
than 10 cm, positive resection margins with or without FNCLCC
grade 2, more than 5% round-cell content and treatment carried
out at a facility that is not specialized in sarcoma care.
Non-planned surgery was a predictor of unfavorable outcomes.
Based on these findings, sarcoma patients should only be treated in
specialized centers, especially since MRI and biopsy examinations
can be tricky and misleading. Sarcoma patients who are referred
after being treated in non-specialized centers have a greater risk of
local recurrence.
MLS are atypical tumors that are very sensitive to radiation
therapy and chemotherapy, and have an unusual ability to metas-
tasize in locations other than the lungs. The threshold between
intermediate-grade and high-grade corresponds to a 5% round-cell
content. High-grade tumors (> 5% round cells) have a higher risk of
metastasis. The potential benefit of neoadjuvant radiation therapy
and adjuvant chemotherapy must be evaluated in these patients.
This subset of patients is also a candidate group for research into
new treatments.
Disclosure of interest
The authors declare that they have no conflicts of interest con-
cerning this article.
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