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Ann Thorac Surg 2009;88:1632-1637. doi:10.1016/j.athoracsur.2009.07.026
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Solitary Fibrous Tumors of the Pleura: An Analysis of 110 Patients Treated in a Single Institution

Giuseppe Cardillo, MDa,*, Luigi Carbone, MDa, Francesco Carleo, MDa, Nicola Masala, MDa, Paolo Graziano, MDb, Antonio Bray, MDc, Massimo Martelli, MDa

a Unit of Thoracic Surgery, Azienda Ospedaliera San Camillo Forlanini, Rome, Italy
b Unit of Pathology, Azienda Ospedaliera San Camillo Forlanini, Rome, Italy
c Unit of Radiology, Azienda Ospedaliera San Camillo Forlanini, Rome, Italy

Accepted for publication July 21, 2009.

* Address correspondence to Dr Cardillo, Unit of Thoracic Surgery, Azienda Ospedaliera San Camillo Forlanini, Via Portuense 332, Rome, 00149, Italy (Email: gcardillo{at}scamilloforlanini.rm.it).

Presented at the Poster Session of the Forty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Francisco, CA, Jan 26–28, 2009.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Solitary (localized) fibrous tumors of the pleura (SFTP) are rare slow-growing neoplasms that generally have a favorable prognosis. The aim of this paper is to evaluate the predictors of outcome in a series of 110 patients with SFTP.

Methods: The records of 110 patients (63 men; mean age 56.4 years; range, 17 to 79) surgically treated for SFTP from July 1990 to February 2008, were evaluated for demographics, operative procedure, histopathology, morbidity, mortality, postoperative chemotherapy or radiotherapy, and long-term follow-up.

Results: Operative mortality was 0.9% (1 of 110) and the overall morbidity was 10.9% (12 of 110). The main surgical approach was video-assisted thoracoscopic surgery (69 procedures with a conversion rate of 14.5%); 40 patients underwent thoracotomy and 1 had sternotomy. The visceral pleura was the site of origin in 95 tumors, the parietal pleura in 13, the mediastinal pleura in 2 cases. Sixty-three tumors were pedunculated, 35 were sessile, and 12 were inverted fibroma. Tumors were pathologically benign in 95 cases (86.4%), and malignant in 15 (13.6%). Symptomatic patients presented with malignant tumors more often than asymptomatic (19.1% versus 9.5%). Overall 10-year survival rate was 97.5%. The overall disease-free survival rate was 90.8% (95.7% in benign cases and 67.1% in malignant cases; p < 0.05). Eight patients presented with recurrence of disease, 4 cases of which were malignant and 4 were benign.

Conclusions: Solitary fibrous tumor of the pleura is a rare disease that includes both benign and malignant variants.The outcome is mostly benign, with an overall 10-year survival rate of 97.5%. Pathologically benign lesions show a better disease-free survival rate than malignant lesions (95.7% versus 67.1%; p < 0.05). Surgery is the gold standard of treatment as neither radiotherapy nor chemotherapy proved to be effective.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Solitary fibrous tumors of the pleura (SFTP) are rare, slow-growing neoplasms and approximately 800 cases have been reported in the literature [1, 2]. They roughly account for less than 5% of all pleural neoplasms [3–5]. First reported by Lieutaud [6] for 3,000 autopsies in 1767 and described as a different pathologic entity by Wagner [7] in 1870, SFTPs have received different names reflecting their uncertain histogenesis and biological behavior: localized fibrous tumor of the pleura, localized mesothelioma, localized fibrous mesothelioma, localized benign fibroma or submesothelial fibroma. In 1931, Klemper and Rabin [8] first related the existence of the intact layer of cuboidal mesothelial cells on the surface of the localized benign fibromas to the submesothelial origin of this type of neoplasm. This has laid the scientific evidence for the present histogenetic theory recently confirmed by modern immunohistochemical methods [8,9,10] which recognizes SFTP as nonmesothelial in origin. There is still a matter of debate regarding surgical approach (open thoracotomy or video-assisted thoracoscopic [VATS]), surgical technique (wedge resection, anatomic resection, chest wall resection), adjuvant therapy (chemotherapy or radiotherapy), and follow-up of SFTPs mostly related to their localization (parietal or visceral), their hystotype (benign or malignant), and other characteristics (inverted fibromas, redo procedures). The presence of rare malignant types and the rate of recurrence represent variables that also have to be taken into account.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
The study was approved by the Ethics Committee (1024/CE, 2009) of Azienda Ospedaliera San Camillo Forlanini, and individual written informed consent was obtained from all patients or their guardians, as appropriate.

From July 1990 to February 2008, of 22,377 patients admitted to the Unit of Thoracic Surgery, Carlo Forlanini Hospital, in Rome, 110 consecutive patients (0.49%) were treated surgically for SFTPs. Patient characteristics are shown in Table 1.


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  		Table 1 Patient Characteristics (n = 110)
 
According to the histologic criteria published by England and coworkers [11], SFTPs were classified as malignant when one or more of the following criteria was met: (1) mitotic count more than 4 mitosis per 10 high-power fields (HPF), (2) presence of necrosis, (3) presence of nuclear atypia, and (4) hypercellularity. Operative methods are shown in Table 2.


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  		Table 2 Operative Methods (n =110 Patients)
 
Statistical Methods
The {chi}2 test was used to compare discrete variables. Survival and recurrence time were calculated from the date of surgical intervention to the date of death, recurrence, or last follow-up. The actuarial method was used to calculate survival and disease-free survival rates. The log-rank test was used to perform univariate analysis. Results were considered significant if the p value was less than 0.05. All calculations were performed with the Number Cruncher Statistical System (NCSS, Kaysville, UT) 2004 statistical software.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Whole-body 18-fluorodeoxyglucose (FDG) positron emission tomography–computed tomography (PET-CT) scan was performed in 10 cases, and results were negative (standardized uptake value less than 2.5) in 8 patients (7 benign and 1 malignant) and positive in 2 (1 malignant and 1 benign). Preoperative fine-needle aspiration biopsy (FNAB) was performed in 23 cases and provided a generic diagnosis of mesenchymal tumor with no other specifications in 9 cases (39.1%), and failed to provide a result in the remaining 14 (60.9%). Operative methods and type of procedures are shown respectively in Table 2 and Table 3. Ninety-five of the cases (86.4%) originated from the visceral pleura, 13 (11.8%) from the parietal pleura, and 2 (1.8%) from the mediastinal pleura. Sixty-three were pedunculated (61 originated from the visceral pleura, 1 from the parietal, and 1 from the mediastinal pleura), 35 were sessile (22 visceral,12 parietal, and 1 mediastinal), and 12 showed an intrapulmonary growth (also called inverted fibroma). The smallest tumor was 0.4 cm in its greatest diameter and the largest was 28 x 22 x 20 cm, weighting 1.850 g with an average maximum diameter of 8.5 cm. One patient showed three synchronous fibrous tumors located on the visceral pleura of the same lobe (Table 3). Seven patients showed associated diseases (colic cancer in 1 patient, breast cancer in 1 patient, gastric cancer and nonsmall-cell lung cancer in 1 patient, typical lung carcinoid in 2 patients, porphyria acuta intermittens in 1 patient, and myasthenia gravis in 1 patient).


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  		Table 3 Type of Procedures (n = 110 Patients)
 
Surgical resection of the neoplasm with histologically free margins (R0) was accomplished in all patients. Operative (30-day) mortality was 0.9%: 1 patient died in the intensive care unit 12 hours after resection of a giant fibroma arising from the visceral pleura (24 x 18 x 17 cm). Postoperative complications occurred in 12 patients (10.9%) and included 6 atrial fibrillations, 3 persistent pleural effusions that resolved with corticosteroids therapy, and 3 prolonged air leak.

According to England's criteria [9], 95 cases (86.4%) were classified as benign, and 15 (13.6%) as malignant. Symptomatic patients presented malignant tumors (9 of 47) more often than asymptomatic patients (6 of 63) patients (19.1% versus 9.5%, p = 0.1).

The majority of the tumors were well circumscribed, lobulated in appearance and firm in consistency. The cut surface was vaguely nodular storiform, occasionally microcystic and myxoid, white-gray in color. Malignant tumors were generally larger in size, soft in consistency and fleshy in appearance, and focal areas of necrosis and hemorrhage were observed. Most benign tumors showed large areas of collagen production. The mitotic count was low, ranging from 0 to 1 mitosis per 10 HPF, and no abnormal mitoses were observed. All benign tumors showed pushing margins and were generally surrounded by a pseudocapsule. Malignant SFTPs presented high cellularity and infiltrative margins with hemorrhage, necrotic areas, and an increased mitotic activity (more than 4 mitotic figures per 10 HPF) including atypical mitoses (Fig 1). Both benign and malignant SFTs consisted of fusiform or oval cells, sometimes showing prominent nucleoli and low amount of collagen production.


Figure 1
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  		Fig 1. Malignant solitary fibrous tumor of the pleura (SFTP) histology: a hypercellular malignant solitary fibrous tumor showing an high mitotic index. In the inset, the characteristic hemangiopericytoma-like pattern of the neoplasm is observed. (Hematoxylin & eosin [H&E] stain; magnification x20. Inset, H&E, x10.)

 
All patients were included in an outpatient clinic follow-up program that included clinical examination and chest roentgenogram after 1, 3, and 6 months, and then once a year. From 1995 onward, a chest CT scan was performed yearly. The follow-up ended in January 2009 and ranged from 12 to 222 months. Eight patients (4 with malignant tumor and 4 with benign SFTP) presented with a recurrence of disease that required a redo operation, followed by radiotherapy (in 4 patients) or chemotherapy (in 1 patient). One of these patients (a 65-year-old woman with malignant SFTP) died 13 months after redo surgery and radiotherapy; autopsy showed recurrent disease in the surgery lung and pleural effusion. Among 8 patients with recurrences, 1 underwent FNAB before the first operation. Three patients who underwent an operation for a benign fibroma died of causes not related to the SFTPs.

Two patients underwent postoperative chemotherapy because of recurrences, with a survival of 96 and 153 months, respectively. Four patients underwent radiotherapy because of malignant histology and achieved a survival of 13, 27, 42 and 47 months, respectively. The remaining patients were still alive and free from disease at the end of the follow-up. The overall 10-year survival rate was 97.5% (Fig 2). The disease-free survival rate was 90.8% (Fig 3): 95.7% for benign cases and 67.1% for malignant cases (p = 0.0002; Fig 4). Ten-year survival rate was 96.3% for patients treated by VATS and 78.4% for patients treated by open thoracotomy (p = 0.05). Ten-year survival rate was 92.7% and 76.9% (p > 0.05), respectively, for patients with visceral or parietal SFTP. Ten-year survival rate according to tumor size was 96.9% (tumor size less than 3 cm), 83.2 % (tumor size 3 to 10 cm), and 90.9% (tumor size more than 10 cm). The presence of symptoms had no influence on survival (p = 0.4).


Figure 2
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  		Fig 2. Ten-year overall survival curve.

 

Figure 3
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  		Fig 3. Ten-year disease-free survival curve.

 

Figure 4
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  		Fig 4. Ten-year survival curve according to histology.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Primary neoplasms of the pleura were divided in 1931 by Klemperer and Rabin [8] into two categories: diffuse mesothelioma and localized mesothelioma. According to that theory, diffuse tumors were derived from multipotent mesothelial cells and were truly malignant mesotheliomas whereas localized tumors originated from areolar subpleural tissue and were mostly benign. They also claimed the presence of a layer of intact cuboidal mesothelial cells at the surface of localized benign tumors as the proof of the submesothelial origin of the neoplasm. Differently from Klemperer and Rabin, Stout and Murray [12] in 1942 proposed that localized mesothelioma originated from mesothelial cells. More recently, studies based on the immunohistochemical features of the tumoral cells have demonstrated their origin from the submesothelial fibroblasts [9, 10]. Malignant pleural mesotheliomas represent approximately 75% to 90% of all diffuse tumors of the pleura; their relationship with asbestos exposure is now established as is their generally unfavorable prognosis. Conversely, localized mesotheliomas represent approximately 5% of all pleural neoplasms, are not related to asbestos, and generally have a favorable prognosis [3–5]. The SFTPs are equally represented in both sexes and are more frequently diagnosed in the fifth or sixth decade of life [13], being very rare in childhood.

More than 50% of the patients with SFTP are asymptomatic, and the tumor is frequently an incidental finding on a standard chest x-ray film [14]. Symptoms, if any, are more frequently associated with larger and generally malignant tumors. In our series, symptomatic patients presented with malignant tumors more frequently than did asymptomatic patients, respectively 19.1% and 9.5%, even if such data did not show any impact on survival. Intrathoracic symptoms are usually nonspecific and include cough, chest pain, dyspnea, and rarely, hemoptysis. More rarely, patients complain of systemic symptoms such as weakness, night sweats, weight loss, osteoarthropathy, digital clubbing, and hypoglycemia. Hypertrophic pulmonary osteoarthropathy (Pierre-Marie-Bamberg syndrome) has been described in as many as 20% of the cases [15, 16] and appears to be caused by the osteolysis related to the excessive release of hyaluronic acid by the tumor [17].

There is also evidence that the hypoglycemia is related to the tumoral production of insulinlike growth factor II; in fact, it resolves after removal of the tumor [20]. The incidence of hypoglicemia is 2% to 4% in the literature [2, 18, 19] but was only found in 2 patients (1.8%) in our series.

According to England and colleagues [11], pleural effusion affects 16% of the patients, with a higher prevalence among those with malignant fibromas (32%) compared to those with benign tumors (8%). Pleural effusions are generally of a small size, although volumes as great as 3 L have been reported in the literature. We only found a pleural effusion in 5 patients (4.5%).

Solitary fibrous tumors of the pleura are normally first identified on a standard chest roentgenogram as a round, well-defined opacity, rarely calcified or associated with a pleural effusion. Its origin from the pleura can rarely be demonstrated, particularly for those arising from the mediastinal, scissural, or basal pleura.

The CT scan of the chest is currently the gold standard for the diagnosis of pleural lesions because of its high sensitivity and specificity, and it has been perfoprmed in all patients included in the present series. It allows a good visualization of the parietal, visceral, mediastinal, and scissural pleura, although it might be limited in the assessment of the diaphragmatic pleura and the paracardiac regions owing to kinetic artefacts (Figs 5 and 6). Go On a plain CT scan, the tumor appears as a round, well-defined, more or less homogeneous mass if areas of necrosis or calcification are present, with a soft tissue attenuation. A low enhancement (less than 15 HU) after administration of intravenous contrast medium suggests a benign origin of the tumor. The presence of a distinct pedicle and the change in intrathoracic localization of the lesion associated with the changes in position of the patient can be diagnostic. The CT scan can also show areas of localized or diffuse pulmonary collapse due to compression and displacement of bronchi and pulmonary vessels. The CT scan can be of less value in the differential diagnosis between neoplasms originating from the mediastinal or diaphragmatic pleura and mediastinal or diaphragmatic tumors.


Figure 5
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  		Fig 5. Computed tomography scan showing a pedunculated solitary fibrous tumor of the visceral pleura (benign variant).

 

Figure 6
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  		Fig 6. Computed tomography scan showing a sessile giant solitary fibrous tumor of the pleura (malignant variant).

 
Magnetic resonance imaging allows for sagittal and coronal views and is often able to provide a topographic and differential diagnosis, particularly for mediastinal, thoracoabdominal, and cervicothoracic masses. It is also useful in differentiating the tumor from surrounding structures. In our series, it has been performed in 22 patients.

According to the literature, FDG-PET scan has so far found a limited applicability. Kohler and coworkers [21] found whole-body PET-CT scan positive in 3 patients with histologically proven malignant STPF and negative in 3 with a benign lesion. Robinson and colleagues [22], as well as Cortes and associates [23], have reported FDG-PET negativity in patients with benign fibromas. The data from our series confirm the high negative predictive value of PET scan in assessing the malignancy of such lesion, even if the sample is very small (10 cases): 50% (95% confidence interval: 9.4% to 90.5%) of positive predictive value versus 87.5% (95% confidence interval: 52.9% to 97.7%) of negative predictive value.

Preoperative CT-guided transparietal aspiration biopsy (FNAB) has proven of little diagnostic value [13, 24, 25]. Sample variability is a limiting factor for the presence of areas with different cellularity within the neoplasm so that the reported diagnostic accuracy of FNAB is almost invariably low. In our experience, FNAB achieved a generic diagnosis of mesenchymal tumor but no conclusive diagnosis of malignancy in 39% of the cases, in accordance with Magdeleinat and associates [24] (45%) and Kohler and associates [21] (40%). Better results have been reported by Weynand and colleagues [26] with Tru-Cut biopsy: 100% diagnostic accuracy in 5 patients.

As in the literature, a worst prognosis is associated with larger tumors [9, 11, 13]. We grouped our patients into three different categories depending on maximum diameter of the tumor (less than 3 cm, between 3 and 10, and greater than 10 cm). We found that prognosis was not affected either by the site (visceral or parietal) of origin (p = 0.25) or by the size of the tumor (p > 0.05).

Surgical resection represents the treatment of choice for SFTP. The aim of surgery is the complete excision of the mass with clear resection margins and minimal resection of parenchyma. Pedunculated SFTPs originating from the visceral pleura are the most common finding and normally are excised by means of VATS. To ensure radical excision of the tumor, we advocate intraoperative pathology examination of the sample in every case, as spindle cells can invade the pedunculus. In addition, SFTPs affecting the parietal pleura require extrapleural dissection followed by intraoperative examination of the specimen and chest wall resection in case of neoplastic invasion of the parietal pleura. Chest wall resection is also recommended in case of recurrent parietal SFTP. Inverted fibromas require instead an anatomical segmental resection or a lobectomy, which can be performed either by open thoracotomy or by VATS.

Certainly, the treatment of choice for pedunculated tumors of the visceral pleura is VATS resection, but it is also indicated for tumors arising from the parietal pleura as it provides a better view of the margins of excision. Video-assisted thoracoscopic surgery has been the procedure of choice for 62.7% (69 of 110) of our patients. The surgical approach shows a difference in 10-year survival rate favoring VATS (96.3% versus 78.4%; p = 0.05), probably because of a selection bias. Surgical approach (open thoracotomy or VATS) should never compromise the radicality of the procedure. Redo surgery is highly advisable in case of recurrence.

The role of adjuvant treatment in SFTP remains uncertain. After radical surgery, we never recommend either radiotherapy or chemotherapy. Radiotherapy appears to be indicated only when surgical resection is not feasible or is incomplete. The underpowered sample size of patients treated in our series by chemotherapy (2 patients) or radiotherapy (4 patients) gives no data regarding the impact on outcome of adjuvant therapy.

In conclusion, SFTP is a rare disease that includes a benign and a malignant variant. The clinical outcome is benign in the majority of the cases, with an overall 10-year survival rate of 97.5%. Benign lesions have a better disease-free survival rate than do malignant lesions (95.7% versus 67.1%; p = 0.0002). The presence of symptoms (p > 0.05), the origin of the tumor (p > 0.05), and tumor size (p > 0.05) do not influence prognosis. The surgical approach (p = 0.05) shows a difference favoring VATS, probably because of a selection bias. Redo surgery, even iterative, is strongly recommended, because neither chemotherapy nor radiotherapy are effective.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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