Solitary fibrous tumor of the pleura: An analysis of forty patients
Department of Thoracic Surgery, Chinese PLA General Hospital, Beijing, China
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Original Article
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Abstract
Objective: To study the clinical characteristics, treatment and prognosis of patients with solitary fibrous tumor of the pleura (SFTP) in order to improve the diagnostic accuracy and treatment of SFTP.
Methods: A retrospective analysis of clinical and imaging features, serum biochemical changes, pathological characteristics and treatment follow-up results was conducted for 40 SFTP patients from January 1998 to March 2010.
Results: A chest CT diagnosis was conducted for 63.6% of the patients; the unenhanced and contrast-enhanced CT findings were significantly different among the cohort (P<0.01). Patients lacking a uniform MRI internal signal comprised 88.9% of the group, 66.7% showed T1 isointensity, 33.3% demonstrated T1 hypointensity, 44.4% showed T2 hypointensity and 44.4% had slight hypointensity. The follow-up time was between 2 and 116.9 months, with an average of 35 months; postoperative adjuvant therapy was not administered. Currently, all the studied patients are alive, with no metastasis or recurrence.
Conclusion: Chest CT is a valuable tool for diagnosis and surgical decisions, and the efficacy of MRI examination is comparable to chest CT. The majority of cases originated in the visceral pleural; for these, surgical resection is an effective treatment, and the prognosis is generally favorable.
Key words
Solitary fibrous tumor of the pleura; clinical features; imaging; pathology; treatment
J Thorac Dis 2012;4(2):146-154. DOI: 10.3978/j.issn.2072-1439.2012.01.05
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Introduction
Solitary fibrous tumor (SFT) is a rare type of soft tissue tumor (1). According to a 2006 review by Robinson, only about 800 cases have been reported in the literature since 1931 (2). The histological features of SFT were first described in detail by Wagner in 1870, but it was not until 1931 that Klemperer and Rabin officially classified it as an independent disease (3). Historically, SFT had long been considered a localized pleural mesothelioma, but in 1979, Scharifker and Kaneko showed that SFT originated in subserosal mesenchymal tissue (4); this finding has gradually been accepted by most scholars. In the past, the SFT nomenclature was rather disorganized. Terms such as localized fibroma, localized mesothelioma, solitary fibrous mesothelioma, localized fibrous mesothelioma, subcutaneous fibroma, subserosal fibroids and others have been reported in previous studies and considered to be solitary fibrous tumors (5,6). According to the 2002 publication by the WHO titled “Pathology & Genetics of Tumors of Soft tissue and Bone” (7), SFT is defined as a mesenchymal tumor that may have fibroblastic characteristics and clear peripheral vascular tumor-like branching blood vessels. Those classified as fibroblastic/myofibroblastic tumors may represent an intermediate type (i.e., occasionally metastatic) and intermediate malignancy. SFT is often misdiagnosed because the disease lacks obvious clinical features, imaging findings are often nonspecific and knowledge among medical professionals is lacking (8-11). This study retrospectively analyzed data for 40 SFTP patients admitted to our hospital with the aim of augmenting clinicians’ awareness and improving the diagnostic and therapeutic accuracy for this disease.
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Patients and methods
Case selection and clinical data
Inclusion criteria: clinical and pathological data integrity and a final pathological diagnosis of SFTP. Data for 40 SFT patients treated in the Department of Thoracic Surgery, People’s Liberation Army General Hospital was collected from January 1998 to March 2010. Clinical features, imaging characteristics, serum biochemical changes, surgical procedures and pathology
results were recorded. Imaging and pathological data were
examined and confirmed by radiology or pathology physicians as
well as the deputy director and other experts, and the final data
were reported.
Follow-up
Follow-ups were conducted by telephone. The follow-up times
ranged from 2 to 116.9 months, with a median of 65.5 months.
Follow-up records included the patients’ survival status and
recurrence of notable preoperative physical symptoms found
in the examination after surgery. Other treatment regimens
administered after the operation were recorded, and the patients’
recurrence status after the operation was also noted; if a relapse
occurred, the post-treatment situation was studied in detail.
Statistical analysis
The analyzed data are presented as means ± standard deviations.
The chi-squared test was used for rate comparisons, and average
values for the two groups were compared using a t-test. P<0.05
indicates a statistically significant difference. The above analyses
were conducted with the SPSS Statistics v17.0 software.
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Results
Patient demographics and clinical features
Among the 40 patients, there were 17 males and 23 females,
a male to female ratio of 1:1.35. The patients were aged 17-78 years, with a median age of 48 years, and 30 patients (75%)
were more than 40 years old. Twenty patients in the group did
not have any symptoms, but chest masses were found during an
examination, and these patients subsequently received treatment.
Fourteen patients showed simple chest symptoms. Two cases
had simple joint symptoms. One case had both chest symptoms
(cough) and joint symptoms (right knee joint swelling). One
case showed chest symptoms (chest tightness) and clubbed
fingers. One case showed chest symptoms (chest pain, chest
tightness and cough) and early morning confusion. One case
had long-term right upper-quadrant discomfort and fullness. All
these patients were receiving treatment for the symptoms. Table 1 lists the related conditions of five patients with paraneoplastic
syndrome. There were 17 patients (42.5%) with chest symptoms,
for whom the average value of the maximum tumor diameter was
15.34 cm. The analysis showed that the presence of symptoms
was correlated with the maximum tumor diameter (P<0.01).
Imaging data
Chest X-ray was used to examine 33 cases. In 31 cases, clear
pleural space-occupying signs or nodules (93.9% positive
rate) were found in the posteroanterior chest film, whereas the
other 2 cases showed normal chest X-ray results. Chest CT
scans were used to examine 33 patients (82.5%); 11 patients
(33.3%) were determined to have fibroids, according to the
imaging data. Ten cases (30.3%) were diagnosed as benign
(indeterminate), 5 patients (15.2%) did not receive a diagnosis
and 3 cases (9.1%) had mesothelioma. There was 1 case each
of thymoma, neurogenic tumor, giant lymph node hyperplasia
and lung cancer. Twenty-two cases were definitively diagnosed with a CT scan (66.7%), among which 21 cases showed mild
or greater enhancement (95.5%) and 11 cases showed uneven
enhancement (accounting for 52.4% of the enhanced cases).
Sixteen cases were reported with average unenhanced and
enhanced CT values (Figure 1), as shown in Table 2 Unenhanced
CT values and enhanced CT values were significantly different
(P<0.01). The incidence of maximum tumor diameter less than
10 cm and greater than or equal to 10 cm in the uniformity of
tumor CT density were significantly different (P<0.01).
Figure 1. Plain and contrast-enhanced chest computed tomography (CT) for four patients with SFTP. A1-A3. The patient is a middle-aged
woman. An oval-shaped mass on the right lateral chest wall protrudes into the lung, with its wide base connected to the thoracic wall. The mass has
smooth margin and uniform density, with a size of 5cm x 2cm and a CT value of about 35 HU. The mass was slightly enhanced after contrast material
administration, with a CT value of 43 - 51 HU. B1 - B3. The patient is a young men. A round-like mass is observed on the left upper mediastinum. It
has a size of 4.7cm x 5.5 cm, smooth margin, and a CT value of 31 - 47 HU. Inhomogeneous enhancement was observed following contrast medium
administration, with a CT value of 55 - 90 HU. C1 - C3. The patient is an old man. A large soft tissue mass is visible in the middle and lower portions of
the right side of thoracic cavity. The mass has a size of about 15cm x 9 cm, inhomogeneous density, and punctate calcification, with a mean CT value of
about 25HU. Inhomogeneous enhancement was observed following contrast medium administration, with a CT value of about 40 HU. Compression
atelectasis of the right lower lobe is seen. A curved line of effusion is visible in the right pleural cavity. The mediastinum slightly extends to the left, and
the lymph nodes in mediastinum and behind the trachea and superior vena cava enlarge. D1 - D3. The patient is a young woman. A spindle-shaped
soft-tissue shadow is seen on the right posterior chest wall, with a size of about 5 cm x 10 cm, uneven density, and a CT value of about 34-50 HU.
Calcified plaque is observed inside the lesions, whose margins are surrounded by low-density fluid. Fat lines exist on the mass and chest wall, showing
a tight relationship with the diaphragma. The mass was slightly enhanced after administration of contrast material, with a CT value of about 36 - 59
HU.
Nine patients received a chest MRI examination (both
unenhanced and enhanced scans) (Figure 2). Among the
unenhanced scans, 8 cases lacked internal signal uniformity
(88.9%), whereas 1 case showed a uniform internal signal.
The T1 phase tended to be isointense or hypointense, with 6
isointense cases (66.7%) and 3 hypointense cases (33.3%). For
the T2 phase, 4 cases (44.4%) were hypointense, 4 cases (44.4%)
were slightly hypointense and 1 case (11.1%) was mixed
isointense-hypointense.
Figure 2. Chest MRI findings of a middle-aged female patient. A round-like lesion with long T1 and T2 signals at the upper posterior portion
of the right mediastinum (near the third thoracic vertebra) is observed. The lesion has a size of 2.9cm x 3.1 cm x 3.5 cm, clearly defined margin, and
inhomogeneous internal signal intensity. The lesion shows slightly high signal intensity on DWI. Dynamic enhancement imaging shows that the
lesion is slightly enhanced in the arterial phase, and such enhancement becomes even more obvious in the portal venous phase and delayed phase;
meanwhile, inhomogeneous internal enhancement is also observed.
Related laboratory indices
Among the 39 SFTP cases, blood sugar, potassium, sodium and blood chloride were measured in 33 patients before and after
surgery. The preoperative examinations revealed 1 case of high
blood sugar and 3 cases of low blood sugar. Blood glucose and
serum potassium levels showed no significant difference before
and after surgery (P>0.05), whereas serum sodium and serum
chloride showed significant changes after surgery (P<0.05 and
P<0.01, respectively).
Pathological data
Of the 40 cases in this group, 39 tissue samples underwent a
routine pathological examination and immunohistochemical
analysis. Twenty-seven cases originated in the visceral pleura,
of which 2 were malignant (7.4%). Tumors protruding the lung
surface were found in 25 cases, with 2 cases of cancer growing
inside the lung and below the pleura. Eight cases originated in
the parietal pleura; 4 of these cases (50.0%) were malignant,
and 2 cases originated in the right mediastinal pleura. Four cases
originated in the interstitial cells of the lung parenchyma, and
1 of these (25%) was malignant. The SFTP malignancy rate for
cases originating in the non-visceral pleura was 41.7%, which was
5.6-fold higher than for SFTP originating in the visceral pleural.
Table 3 lists the pulmonary invasion statuses for 5 patients. Table 4 lists the related statuses of 6 wide-base tumor cases. Table 5
lists the features of 8 patients with malignant SFTP. Figure 3
show the typical cytology and immunohistochemical features of
SFTP.
Figure 3. The tumor cells and intercellular collagen fibers proliferated without obvious direction or structure, which corresponded to the socalled
patternless. Immunohistochemical analysis revealed positivity for CD34 (++), bcl-2(+++), and VIMENTIN (++) in tumor cells.
Preoperative biopsy, surgical treatment and prognosis
Fourteen patients received a puncture biopsy (11 cases were
biopsied in this hospital), and 9 cases were confirmed as SFTP.
Three cases biopsied in other hospitals had not undergone
immunohistochemistry analysis; thus, these diagnoses were not
confirmed. The puncture biopsies conducted in this hospital
showed an 81.8% positive rate, and 2 puncture biopsy cases
in this hospital could not be confirmed as SFTP due to an
insufficient biopsy specimen obtained. One case was diagnosed
as benign fibroblastic proliferative lesion, and another case was
diagnosed as spindle cell tumor. Thirty-nine patients received
and completed radical surgical treatment. The surgical resection
rate was 100%, with no serious complications, and these patients
were discharged after 1-2 weeks. Eight patients were determined
to have hypervascular tumors with vascular embolization
from the preoperative imaging studies. Twenty-four patients
(61.5%) received conventional open thoracotomy, 9 cases
(23.1%) underwent simple thoracoscopic surgery and 6 cases
(15.4%) received video-assisted thoracoscopic surgery. Twenty-nine patients (74.4%) underwent simple tumor resection, 6
patients (15.4%) underwent lung cancer resection and a partial
lobectomy and 4 cases (10.3%) received a lobectomy. Among
the lobectomy patients, 1 case showed an extremely large right
pleural tumor (30 cm ×25 cm ×20 cm) pressing on the lower
right lobe and causing compression atelectasis. During the tumor
separation procedure, the lower right lobe was severely damaged,
and the lower right lobe was removed during tumor resection; an
upper lobe resection was performed in 1 case due to the tumor
being located in the parenchyma near the hilum in the right
upper lobe, with a high risk of simple partial tumor resection
and lung resection. One case showed a very large tumor (20
cm ×19 cm ×10 cm) exerting a high degree of pressure, and the
middle lobe of the right lung had consequent atelectasis and
consolidation; the middle lobe of the right lung was therefore
removed for this case. In 1 case, the middle lobe of the right lung
was resected due to the middle lobe vein being located near the
tumor.
Follow-up
The author conducted telephone follow-up interviews with 40
patients; 11 cases (27.5%) were lost, primarily due to changes
in phone number. The specific patient situations are illustrated
in Table 3.18. The follow-up duration was 2-116.9 months, with
a median of 65.5 months. Four patients with malignancy were
followed up for 116.9 months, 34.3 months, 9.5 months and 1.8
months, respectively. Among the 25 patients with benign tumors,
the follow-up duration ranged from 3.3 months to 96.2 months,
with an average of 34.1 months; 9 patients were followed up
for more than 36 months. For 29 cases, no other adjuvant
treatment had been administered after the surgery at the time of
the final follow-up; all these patients are currently alive, with no
metastasis, recurrence or relapse.
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Discussion
Previous studies have reported the age of SFTP patients to be
between 5-87 years (12), and a higher incidence of SFTP among
elderly patients has been reported. This study retrospectively
analyzed 40 SFTP patients aged from 17 to 78 years, with
75% of the cohort being 40 years of age and older. Consistent
with previous reports, SFTP was mostly reported as a benign
tumor. This may be related to its characteristic slow growth and
development, the delayed presence of clinical symptoms and its
atypical nature. The incidence of SFTP is currently thought to be
comparable between men and women. In this study, there were
23 female and 17 male patients, a male to female ratio of 1:1.35.
We reviewed 157 cases of pleural solitary fibrous tumor reported
in the literature between 2000 and 2009, among which 71 cases
were males and 86 cases females, a male to female ratio of 1:1.21.
This demonstrates that the incidence of SFTP was greater in
females than males. SFTP patients are often asymptomatic; most
cases are discovered during a physical examination. Among the
40 cases of this group, 20 patients (50%) showed no symptoms
but were found to have SFTP upon a physical examination,
which is consistent with reports in the literature indicating that
the percent of SFTP patients showing symptoms was between
40-50%. Seventeen cases in this group had chest symptoms.
The average maximum diameter of the tumor specimens was
15.34 cm, and 12 tumors (70.6%) had maximum diameters
larger than or equal to 10 cm. Twenty-four cases had an average
maximum tumor diameter less than 10 cm, and chest symptoms
were reported in 5 of these patients (20.8%). Eight cases had
a maximum tumor diameter of 10-20 cm, and 4 of these cases
(50%) showed symptoms. Of 8 cases with tumor diameters
larger than or equal to 20 cm, 7 (87.5%) showed symptoms.
These data indicate that tumor size and the occurrence of chest
symptoms are closely related: the larger the tumor, the more
prone the patient is to presenting with chest symptoms. The
literature has reported that chest symptoms were often reported
in patients with a maximum tumor diameter greater than 10
cm (13), whereas this study indicates that chest symptoms are
more prevalent in patients with a maximum tumor diameter
greater than 20 cm. Arthritis-like symptoms and clubbing can
occur in SFTP patients, which is considered hypertrophic
osteoarthropathy (HOA). This cohort included 3 patients with
arthritis-like symptoms.
Imaging is essential for SFTP diagnosis and treatment. Benign
tumors have smooth edges and clear boundaries. Interestingly,
after multiple imaging studies, changes in the tumor’s location
can be detected; this is often related to benign SFTP connecting
with pleural tissue through the pedicle. Lewis et al. reported this
phenomenon in 1985 (14); this finding has some significance
for SFTP diagnosis and surgery, but the specific impacts of this
behavior were not well known then. Malignant SFTP mostly
grows in a wide base, spread along the chest wall or with a deep
invasion into lung tissue. It is generally thought that CT and
MRI tests are valuable in distinguishing benign from malignant
SFTP. Benign tumors show encapsulation and a clear boundary
and often have pedunculated growth; in contrast, malignant
tumors tend to show hemorrhaging, necrosis, organ infiltration,
recurrence and metastasis, among other signs. All patients in this
study underwent a routine preoperative chest X-ray examination;
the positive diagnosis rate of the chest X-ray examination in this
hospital was 93.9%. Tumors were not discovered in 2 cases. In
1 of these cases, the tumor was located on the right side of the
chest and had a size of 3.55 cm ×8.76 cm; this tumor appeared
spindle-shaped and was close to the chest wall. In another case,
the tumor was located in the right lower mediastinum. This
tumor was about 5 cm ×4 cm ×3 cm in size and was covered
by the heart shadow. Chest X-ray examinations had a relatively high positive diagnosis rate, and this type of examination is
convenient, inexpensive and suitable for routine screening
and postoperative follow-up tracking. Among 33 patients who
received chest CT examination, 11 (33.3%) were considered
to have fibroids, and 10 cases (30.3%) were considered benign
(indeterminate). The diagnostic accuracy rate of CT imaging
reached 63.6%. de Perrot et al. reported that in an unenhanced
scan, the tumor CT value was usually between 25 and 40 HU
(13). Unenhanced and enhanced CT scans were used for
16 patients in this group. The CT values were significantly
different for different tumor sizes, which is consistent with SFT
histologically being a hypervascular tumor (15).
Inside the tumor, heterogeneous components may be
caused by hemorrhage, necrosis and cystic masses, leading to
heterogeneity in the internal density of the CT scan. An increase
in heterogeneity was observed when the CT values increased,
which is called the “map-like enhancement mode” (16).
CT can be used to make a preliminary judgment about
whether a tumor is benign or malignant, and it is invaluable
for choosing the surgical approach and estimating procedural
difficulty. It was believed in the past that MRI was more valuable
than CT for diagnosing SFTP, but analysis of 9 patients in this
group who received either a chest MRI or CT examination
showed that MRI showed a comparable efficacy to CT in
diagnosing SFTP, and the cost of an MRI examination is higher
than that of CT. Therefore, MRI should not replace CT for
SFTP diagnosis. SFTP patients can occasionally have low blood
sugar, a phenomenon that is seen more often in patients with
malignant SFTP and is known as Doege-Potter syndrome.
Doege-Potter syndrome is believed to be a type of non-insulindependent
hypoglycemia, which can accompany a variety of
interstitial tumors, including SFTP, as well as some epithelial and
hematological tumors (1). We found 3 cases of low blood sugar
that were detected before surgery. However, when statistical tests
were conducted to analyze blood sugar values before and after
surgery, the results showed no significant difference between
the two time points. We speculated that SFTP-related decreased
blood sugar maybe due to a variety of independent factors, such
as the amount of IGF-II production and the consumption of
sugar by the tumor, among others. Most SFTP patients show
normal blood sugar levels, but SFTP patients with hypoglycemia
require clinical attention. Delayed treatment may have serious
and unexpected consequences and can even lead to death. Serum
potassium, sodium and chloride levels showed no abnormalities
before or after surgery. Preoperative and postoperative serum
potassium levels were not significantly different, but preoperative
and postoperative serum sodium and serum chloride levels
were significantly different. No previous studies have reported
that SFTP causes changes in serum electrolytes. We speculate
that the patients’ serum sodium and chloride levels differed
before and after the operation due to postoperative aseptic
inflammation, fasting and fluid intake rather than SFTP-induced
pathophysiological changes.
SFTP specimens are generally spherical, spherical-like or
ellipsoidal. The literature has reported tumor sizes ranging from
several centimeters to tens of centimeters. Whereas benign
tumors mostly have intact membranes, malignant tumors often
show cystic degeneration and necrosis, which are important
indicators of malignancy. Most SFTP cases originate from the
visceral pleura, fewer originate from the parietal pleura and
tumors rarely originate from the lung parenchyma. In this group,
8 cases were found to originate in the parietal pleura, 4 cases
showed wide bases and 3 cases were malignant. Generally, it is
believed that SFTP originating from the visceral pleura is mostly
benign, and these tumors are usually attached to the pleura
by a pedicle, with only a small number of wide bases. Those
originating from the parietal pleura often have wide bases and
a large volume. A substantial proportion of these latter tumors
showed malignant tendency. Cardillo et al. reported that in 55
cases of SFTP, 7 were derived from non-visceral pleura, of which
3 cases were malignant (43%) (17).
In contrast, of 48 cases originating from the visceral pleura,
only 4 were malignant (8%). For the patients in the present study,
among 6 cases of tumors with wide bases, only 2 were malignant.
Of the 7 cases of malignant SFTP, only 3 tumors had wide bases,
which is inconsistent with the previously reported incidence
of tumors with wide bases that were prone to malignancy.
Currently, SFTP is primarily diagnosed with pathological
microscopy and especially using immunohistochemistry. The
immunohistochemical studies reported here did not show
significant differences between the malignant and benign cases.
SFTP is generally difficult to diagnose preoperatively because
its clinical features and imaging findings do not tend to show
abnormalities. Chest X-ray or CT examinations indicate that
when a single large oval shadow is seen in the thoracic cavity,
an SFTP diagnosis should be considered (18). However,
diagnostic confirmation depends on postoperative pathological
and immunohistochemical examinations of the specimens (9-
11). The necessity of a preoperative puncture biopsy remains
controversial. Suter et al. believe that a puncture biopsy cannot
obtain sufficient tissue for cytological analysis and tends to result
in a high false negative rate (19). In addition, for tumors with a
rich blood supply, a puncture biopsy is accompanied by a risk of
bleeding. However, Weynand et al. used immunohistochemistry
to definitively diagnose 5 SFTP patients before surgery (20). In
the present analysis of 40 patients, 14 received a puncture biopsy
(11 cases were biopsied in this hospital), and the puncture
biopsy positive rate in this hospital was 81.8%.
We can conclude that puncture biopsy is a valuable tool for
diagnosing SFTP; the key is to obtain a sufficient amount of
biopsy tissue for successful immunohistochemical staining.
Complete surgical resection is the first-line treatment choice, and it is the only demonstrated effective treatment. Most
patients are cured after a complete surgical resection. Thirty-nine
patients in this study received surgery, with a 100% resection
rate and complete removal of the tumor. There were no serious
postoperative complications, and patients were discharged in
1-2 weeks. For benign SFTP cases, extended resection is not
recommended. Tumors such as those originating from the
pedicle visceral pleura do not typically require further action
or an entire lung lobe wedge resection. For tumors invading
the parenchyma, it is recommended that after the tumor is
removed, a partial or complete lung lobe resection should then
be conducted. For malignant SFTP, local extension of the lung
and pleura removal are necessary. For tumors originating in the
parietal pleura, removal of the thoracic fascia is recommended if
possible, and the surgeon can consider removing the chest wall if
invasion is detected. The choice of surgical approach is primarily
based on tumor size and the difficulty of removal. Standard
open-chest surgery, video-assisted thoracoscopic surgery (VATS)
and thoracoscopic surgery are potential treatment options (21).
If complete resection of SFTP is achieved, further radiotherapy
and chemotherapy are not necessary. According to the followup
results in the present study, 28 patients who underwent
complete tumor removal did not receive adjuvant radiotherapy
or chemotherapy (including those patients with malignancies).
The maximum follow-up duration was 9.6 years. Metastasis and
recurrence have not yet occurred. Postoperative radiotherapy or
chemotherapy should be administered for those patients who
did not receive a complete resection. Some scholars suggest
using doxorubicin and clacarbazin as chemotherapeutic agents,
but the specific effects of these treatment modalities requires
further study.
In conclusion, SFTP occurs more often in the elderly, and
half of the patients are asymptomatic. Chest CT is a valuable
tool for diagnosis and surgical decisions, and the efficacy of MRI
examination is comparable to chest CT. The majority of cases
originated in the visceral pleural; for these, surgical resection is
an effective treatment, and the prognosis is generally favorable.
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References
Cite this article as: Chu X, Zhang L, Xue Z, Ren Z, Sun Y, Wang M, Liu M.
Solitary fibrous tumor of the pleura: An analysis of forty patients. J Thorac
Dis 2012;4(2):146-154. doi: 10.3978/j.issn.2072-1439.2012.01.05
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