ANTICANCER RESEARCH 35: 2229-2234 (2015)

Prognostic Factors and Survival in Patients Treated Surgically

for Primary and Recurrent Uterine Leiomyosarcoma:
A Single Center Experience
NICOLAE BACALBASA1, IRINA BALESCU2, SIMONA DIMA3,
VLADISLAV BRASOVEANU3 and IRINEL POPESCU1,3

1Carol
Davila U.M.F., Bucharest, Romania;
2Ponderas
Hospital, Bucharest, Romania;
3Dan Setlacec Center of Gastrointestinal Disease and Liver Transplantation,

Fundeni Clinical Institute, Bucharest, Romania

Abstract. Aim: To (i) determine prognostic factors after
initial surgery for uterine leiomyosarcomas (LMS) and their
recurrence and (ii) assess the effectiveness of re-resections.
Patients and Methods: All cases that underwent surgery for
uterine leiomyosarcomas at the Fundeni Clinical Institute,
Bucharest between 2002 and 2013 were reviewed. Twenty-
six patients with primary uterine leiomyosarcomas were
introduced in our study. Sixteen of them were re-addressed
to the same hospital for recurrence. Results: At the moment
of initial surgery the most important prognostic factors
were age <60 years, International Federation of
Gynecology and Obstetrics (FIGO) stage I, tumor
dimension <15 cm and mitotic index <15/10 high-power
fields (HPF). The five-year overall survival was 40%.
Sixteen patients were re-operated for recurrence; the most
important prognostic factors being a late recurrence (>12
months) and initial FIGO stage I. The five-year overall
survival was 12.5%. Conclusion: Uterine leiomyosarcoma
is an aggressive malignancy with a high rate of recurrence.
In selected cases surgery may be attempted for re-
recurrence.
This article is freely accessible online.
Correspondence to: Irinel Popescu, Center of Digestive Diseases
and Liver Transplantation, Dan Setlacec Center of General Surgery
and Liver Transplantation, Fundeni Clinical Institute, Bucharest,
Romania, Sos. Fundeni 258, Bucharest 022328, Romania, Tel/Fax:
+40 213180417, e-mail: irinel.popescu220@gmail.com and Nicolae
Bacalbasa, Carol Davila U.M.F., Bd. Eroii sanitari 8, Bucharest
050471, Romania, Tel: +40 0723540426, e-mail: nicolae_bacalbasa
@yahoo.ro, nicolaebacalbasa@gmail.com
Key Words: Uterine leiomyosarcomas, complete resection, recurrence.
Leiomyosarcomas (LMS) of the uterus is a rare malignancy
accounting for approximately 1% of gynecological cancers
and carries an extremely poor prognosis. (1) Survival is
dependent upon stage at diagnosis (2), but overall results are
poor with a 5-year overall survival ranging between 52 and
75% for stage I and 0-39% for stages II-IV (3, 4).
For early-stage LMS simple hysterectomy is warranted.
The incidence of ovarian metastases is low (3.4-3.9%) (5, 6,
7) and preservation of ovarian tissue does not seem to
increase the risk of recurrence (8, 9, 10). Lymph node
metastases are not common (3.5-11%) (5, 11) and
lymphadenectomy does not seem to affect survival (12). The
major problem with LMS, even in early stages, is relapse.
Radiation therapy, at least when used alone, does not seem
to affect survival; the European Organization for Research
and Treatment of Cancer (EORTC) randomized control trial
for early-stage sarcoma (radiation versus no further
treatment) failed to show improvement of survival or local
control for patients with LMS (13). Several other studies
showed improvement in pelvic control after adjuvant
radiotherapy (5).
The effect of chemotherapy is modest with single-agent
response ranging from 9 to 25% (14, 15); as far as combination
is concerned, the best response is obtained by a combination
of gemcitabine and docetaxel ( 27% response rate) (16).
Treatment of recurrent disease is mainly based on resection
of both local and systemic recurrence with pulmonary
metastasectomy (17, 18, 19), liver metastasectomy (20, 21)
and even re-resection (17, 22).
Due to the rarity of disease, most studies are retrospective,
with a small number of patients making, thus, prospective
randomized studies difficult. We aimed to review cases of
uterine LMS treated at a tertiary referring center (Fundeni
Clinical Institute) between 2002 and 2014 from primary
surgery to quaternary cytoreduction.

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 ANTICANCER RESEARCH 35: 2229-2234 (2015)

Table I. Associated resections at the time of initial surgery. Table II. The main characteristics of patients after initial surgery
influencing survival at univariate analysis.
Resected organ No. of cases
Parameter No. of cases Survival p-Value
Total cystectomy 3 (months)
Total colpectomy 1
Rectosigmoidian resection 3 Age (years)
Right colectomy 1 <60 17 65 0.007
Segmentary enterectomy 2 >60 8 27
Stage
I 13 103 0.0000235 (I vs. IV)
II 9 47 0.00191 (I vs. II)
Patients and Methods IV 3 5 0.00507 ( IV vs. II)
Tumor grade
G1 6 99 0.336 (G1 vs. G2)
We retrospectively reviewed the hospital medical records of Dan G2 12 75 0.143 (G2 vs. G3)
Setlacec Center of General Surgery and Liver Transplantation, G3 7 35 0.0629 (G3 vs. G1)
Fundeni Clinical Institute, Bucharest between January 2002 and Tumor size
April 2014. Twenty-six patients were identified to have <15 cm 15 50 0.015
histopathological findings of primary uterine LMS and sixteen of >15 cm 10 24
them were re-operated for recurrent tumors at the Fundeni Clinical Mitotic count
Institute. Survival curves, overall survival and disease-free survival, <15 15 86 <0.001
were generated using the the Kaplan-Meyer method. A p-value >15 10 23
<0.05 was considered statistically significant.
After approval by the Fundeni Clinical Institute Ethics
Committee, the files of the patients diagnosed with uterine LMS
between January 2002 and April 2014 were retrieved. The diagnosis
of uterine LMS was confirmed by histopathological exam. Date of The median hospitalization stay was 8.5 days (range=6-25
death was confirmed with the National Register of Population.
days). The postoperative mortality was 3.8% (abdominal
Statistical analysis was performed using the application SigmaPlot
version 12.1 (link or supplier with address). sepsis after enteral fistula, 1 case). Postoperative morbidity
was also 3.8%-wound infection in one case .
Six patients (14.28%) with advanced stage and high grade
Results sarcoma underwent adjuvant chemotherapy. In one case
radiotherapy was also associated.
Initial surgery. A total of twenty-six patients with uterine Overall survival after initial surgery was 51 months
sarcomas were eligible for our study. The median age at (range=1-133 months). When classified on FIGO stages,
initial surgery was 53.26 years (range=32-83). Nineteen overall survival was 75 months (range=20-133) for stage I, 36
(73%) of the patients had a post-menopausal status. The months (range=7-98) for stage II and 6.4 months (range=1-22)
most common symptoms were vaginal bleeding, 19 patients for stage IV. The 5-year overall survival was 40%.
(73%); abdominal pain,15 patients (57.6%); and palpable The main characteristics of patients with uterine LMS
abdominal mass, 11 patients (42.3%). Only five patients after initial surgery influencing survival at univariate analysis
(19.3%) were diagnosed preoperatively through bioptic are presented in Table II. Survival analysis was performed
curettage with uterine sarcomas. Associated comorbidities on the remaining lot of twenty-five patients (after excluding
were diabetes mellitus in four cases and arterial hypertension the early postoperative death after enteral fistula).
in ten cases. Thirteen patients were assigned to stage I The most important factors associated with an improved
(50%), nine cases to stage II (34.6%) and four cases to stage overall survival after initial surgery were age <60 years
IV (15.3%), according to the 2009 FIGO classification for (p=0.007), FIGO stage I (p=0.00191 when compared to
uterine sarcomas. None of the patients presented ascites at FIGO stage II and p=0.0000235 when compared to FIGO
the moment of diagnosis. Neo-adjuvant chemo-irradiation stage IV, respectively) (Figure 1), tumor size <15 cm
was associated in three cases. (p=0.015) and mitotic count <15 (p=0.001). Although other
In twenty-five patients, surgical treatment consisted in factors like the tumoral grade of differentiation were not
total hysterectomy with bilateral salpingo-oophorectomy. statistically significant in terms of survival, important
Lymph node dissection was associated in five cases (pelvic differences between the three groups (G1 versus G2 or
lymph node dissection); para-aortic lymph node dissection versus G3) were found. Overall survival in the G1 group
was associated in four cases. In none of the cases lymph was 99 months and significantly decreased in the other
nodes were invaded. Other associated resections are sum- groups (75 months for G2 and 35 months for G3,
marized in Table I. respectively).

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 Bacalbasa et al: Prognostic Factors in Uterine Leiomyosarcoma

Table III. Associated resections at the time of secondary surgery. Table IV. The most important factors influencing survival in cases in
which complete R0 resections were performed.
Resected organ No. of cases
Parameter No. of cases Survival p-Value
Rectosigmoidian resection 9 (months)
Total cystectomy 5
Total colpectomy 4 Time to recurrence
Nephrectomy 1 <12 months 8 65 0.035
Right colectomy 1 >12 months 6 21
Atypical hepatectomy 2 FIGO stage
Appendectomy 1 I 7 66 0.02
Pulmonary resection 1 II-IV 7 20
No. of recurrences
Single 11 61 0.15
Multiple 3 23
Localization of the recurrence
Surgery for recurrence. A total of sixteen patients underwent Pelvic 10 53 0.606
surgery for abdominal or pelvic recurrence. The mean age Distant 4 29
at secondary surgery was 56.6 years (range=38-73). Tumoral grade
Disease-free survival after initial surgery was 35 months G1 4 54 0.213 (G1 vs. G2)
G2 7 36 0.992 (G2 vs. G3)
(range=3-117 months).
G3 3 16 0.117 (G3 vs.G1)
Single-tumor recurrence was found in thirteen patients
(81.25%), while the other three patients had at least two
lesions. Eleven patients were diagnosed solely with pelvic
recurrence, while in other three cases both pelvic and upper Table V. Associated visceral resections at the time of tertiary
cytoreduction.
abdominal recurrence was found. One case presented only
an upper abdominal metastasis and another one presented an Resected organ No. of cases
isolated pulmonary metastasis. The overall survival at two
and five years was 43.75% and 12.5%, respectively. Total cystectomy 1
Complete cytoreduction was performed in 14 cases (87.5%) Segmentary enterectomy 2
Atypical hepatectomy 1
and included abdominal, pelvic and thoracic resections. In two
Total colpectomy 1
cases incomplete R1 resections were performed. Isolated Cephalic duodeno-pancreatectomy 1
resections were performed in one case with pulmonary
metastasis and in another case with isolated liver metastases.
All other patients benefited from extended combined
abdominal and pelvic resections. Associated resections at the gastric ulcer. The postoperative course after re-exploration
time of secondary surgery are noted in Table III. was uneventful, with a reported survival of 12 months.
The mean dimension of resected tumor was 13 cm The overall survival after secondary surgery was 33
(range=2-30 cm). The distribution according the tumoral months (range=7-116 months).
grade revealed: G1 tumor in four cases, G2 in eight cases and After resection for recurrence, the most important factors
G3 in three cases. None of the patients presented changed associated with an improved survival are FIGO stage I at
type of tumor differentiation when compared with primary initial surgery (stage I vs. stages II-IV, p=0.02) (Figure 2)
surgery. and time to recurrence (disease-free interval above twelve
Pelvic lymph node dissection was associated in four cases months is associated with better prognosis, p=0.035)
but nodal involvement was found in a single patient with G3 (Figure 3). There were important differences in terms of
LMS. Para-aortic lymph node dissection was also associated survival when comparing the groups with single versus
in five cases, while two patients with G1 and G2 LMS multiple recurrences (61 months vs. 23 months), pelvic
presented positive lymph nodes, respectively. The median versus abdominal localization of the tumor (53 months vs.
hospital stay was 10 days (between 5 and 21 days). 29 months), association of adjuvant chemo-irradiation (54
Postoperative mortality was (6.25%): one patient died in months in patients with adjuvant chemoirradiation and only
the early postoperative course due to colic necrosis-abdominal 30 months in those with no oncologic treatment) or the
sepsis. Postoperative morbidity was 25%, with four cases different histopathological grades (54 months for G1, 36
presenting postoperative complications: wound infection in 2 months for G2 and 16 months for G3); however, none of
cases and urinary incontinence also in 2 situations. In one these factors proved to be statistically significant. The
case Clavien Dindo grade III complications occurred: surgical overall survival at 2 years was 43.75%, while the 5-year
re-exploration was needed for gastric perforation through overall survival was 12.5%.

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 ANTICANCER RESEARCH 35: 2229-2234 (2015)
The most important factors influencing survival in cases
in which complete R0 resections were performed are shown
in Table IV.
Eight patients recurred after secondary surgery, with mean
age at tertiary surgery being 52.2 years (range=39-61).
Disease-free survival after secondary surgery was 15.3
months (range, 7-42).
Six patients presented pelvic recurrence, while isolated
upper abdominal recurrence was found in two cases: hepatic
recurrence in one case and pancreatic recurrence in the other.
Six of the eight patients (75%) underwent complete
cytoreduction, while in two cases only biopsy was performed.
Associated visceral resections at the time of tertiary
cytoreduction are mentioned in Table V.
The mean hospitalization stay was 14 days (range, 6-30).
No postoperative death was reported. Two of the eight
patients presented postoperative complications: Clavien
Dindo grade I (one case, wound infection) and Clavien
Dindo grade III (one case, enteral fistula), which required
surgical re-exploration and ileostomy. The overall survival
after tertiary surgery was 17 months (range=1-35).
Two patients were diagnosed with abdomino-pelvic
recurrences after tertiary surgery. Their mean age was 60
years (range=55-65). In both patients colic and segmentary
enteral resections were associated. One of the two patients
died in the early postoperative period, two weeks after
surgery, due to neurological disorders, i.e. ischemic vascular
stroke. Survival for the other patient was 14 months.
Discussion
Uterine LMS carries a grim prognosis; the body of evidence
concerning this disease is scarce, mostly consisting of small
retrospective studies. There is a need to better-establish
prognostic factors and principles of management of the
recurrence. Also, benefit of surgery beyond first recurrence
needs to be assessed.
Medical charts of Dan Setlacec Center of General Surgery
and Liver Transplantation, Fundeni Clinical Institute,
Bucharest between 2002 and 2014 (twelve years) were
reviewed; twenty-six patients with uterine LMS were
identified. The vast majority were stage I and II, the rest of
them being assigned to stage IV. Standard procedure at
primary surgery was total hysterectomy with bilateral
oophorectomy. Despite the early stages, most of them (15/25,
60%) realpsed, which is consistent with current literature
indicating a relapse often above 60% (11, 23).
One of the most important factors associated with
outcome after surgery for uterine LMS is stage; the overall
survival for stage I is 103 months, for stage II 47 and only 5
months survival for stage IV. The survival in stage I has
statistical significance when compared to both stage II and
IV. This data is consistent with conclusions of other
2232
investigators; Kapp et al. (24) on a SEER analysis of 1,396
cases of uterine LMS established stage as an independent
prognostic factor for survival.
Age (>60) proved to be a statistically significant factor for
worse prognosis, consistent with already existing evidence
(10, 11, 25, 26).
Tumor size under 15 cm and mitotic count below 15
mitoses proved statistically significant for better survival as
previously described by most investigators (5, 27-30).
Although not reaching statistical significance, a
difference was noted regarding tumor grading with an
overall survival of 99 months for G1 group versus 35
months for G3 group.
Management of recurrent disease is an important matter
in a malignancy that, as pointed above, carries a strong
tendency for relapse even in early stages. Randomised
control prospective studies are lacking due to the rarity of
the disease. Sixteen of the initial 26 patients with uterine
LMS underwent surgery for relapse in the same centre. The
overall survival at two years after secondary cytoreduction
was 43.75% with 12.5% alive subjects at 5 years.
The most important prognostic factors after resection for
recurrence in our study was a disease-free interval of over
12 months after initial surgery that is statistically associated
with better survival; this probably reflects a more indolent
course in tumor biology.
FIGO stage I at initial surgery represents a different subset
of patients with better outcome after surgery for recurrence.
Hoang et al. (31) have made similar observations. Although
not statistically significant, we found a difference in survival
favouring patients with single versus multiple recurrence
(similar to studies by Hoang and Giuntoly) (23, 31) and
pelvic versus upper abdominal recurrence (confirmed by
Giuntoly) (23).
Interestingly, patients who underwent chemo-irradiation
after initial surgery had better prognosis after resection of
recurrence (54 versus 30 months), although statistically
significance has not been reached.
The use of radio-chemotherapy in the recurrence after
LMS brings little survival benefit as reflected by most
studies. On the other hand, there is important evidence to
support extended use of surgery in management of both local
recurrence and distant metastases, including lung (17-19, 32)
and liver (20, 21). It would, thus, seem logical to give the
same credit to surgery beyond the first recurrence, although
existing data is extremely scarce.
Eight patients from the same lot underwent tertiary
surgery in the same centre with a good resecability rate
(75%) and acceptable complication rate (25%). The overall
survival after tertiary surgery was 17 months (range=1-35).
Beyond tertiary surgery, there is a problem of individual
evolution, patient and surgeon’s choice. Nevertheless, one
patient with quaternary surgery survived 14 months.
 Bacalbasa et al: Prognostic Factors in Uterine Leiomyosarcoma
Figure 1. Survival analysis on FIGO stages after the initial surgery.
Figure 2. Survival after resection for recurrence according to FIGO
staging.
Conclusion
Uterine LMS is a rare but very aggressive uterine
malignancy with high risk of recurrence even after complete
initial resections. In our study the most important prognostic
factors after initial surgery were age <60 years, FIGO stage
Figure 3. The influence of the time to recurrence on overall survival.
I and smaller tumors (<15 cm) with a lower mitotic index
(<15/10 high-power fields (HPF)). Although complete R0
resection was performed in all cases at the moment of initial
surgery, in sixteen patients the disease relapsed. Our
retrospective study showed that, at the moment of resection
for recurrent tumors, the most important factors improving
survival were the moment of recurrence (>12 months) and
initial FIGO stage I. In fourteen cases complete resections
were performed. The overall survival after recurrence
resection was 43.75% at 2 years and 12.5% at 5 years,
respectively. These results sustain the role of surgery in
treating recurrent LMS, showing an important benefit in
terms of overall survival when compared with patients who
were only chemotreated and in whom the median survival
reported in literature ranges between 9 and 17.9 months.
Beyond resections for first recurrence, we further identified
patients with secondary and even tertiary relapses who
benefited from complete resection of the re-recurence. We
report an overall survival of 17 months after re-resetion of the
recurrences and a survival of 14 months in the case of a patient
who underwent quaternary cytoreduction. Although improved
survival after resection was obtained in almost all the cases,
our study was limited by the small number of patients who
benefited from tertiary or even quaternary resections.
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Received September 13, 2014
Revised December 17, 2014
Accepted December 23, 2014