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Ann Thorac Surg 2000;70:1808-1812
© 2000 The Society of Thoracic Surgeons

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Original article: general thoracic

Localized (solitary) fibrous tumors of the pleura: an analysis of 55 patients

^a Division of Thoracic Surgery, Azienda Ospedaliera San Camillo-Forlanini, Ospedale Carlo Forlanini, Rome, Italy
^b Unit of Pathology, Azienda Ospedaliera San Camillo-Forlanini, Ospedale Carlo Forlanini, Rome, Italy

Address reprint requests to Dr Giuseppe Cardillo, Divisione Chirurgia Toracica, Ospedale C. Forlanini, Via Portuense 332, 00149 Rome, Italy
e-mail: gcardillo{at}scamilloforlanini.rm.it

Presented at the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments Discussion References

 
Background. Localized (solitary) fibrous tumors (LFTPs) of the pleura are rare, slow-growing neoplasms thought to originate from submesothelial connective issue. The aim of this article is to present 55 new cases of LFTP, and to discuss the treatment of choice and the clinical behavior of such neoplasms.

Methods. From July 1990 to November 1999, 55 patients (32 male, 23 female) with an LFTP were surgically treated at our Institution. Neoplasms were considered to be malignant if one or more of the following histologic features were present: high cellularity with crowding and overlapping of nuclei; high mitotic activity; or mild, moderate, or marked pleomorphism.

Results. No operative mortality was reported. Forty-eight of the cases arose from the visceral pleura and seven arose from the parietal pleura. A local removal of the neoplasm with free surgical margins was accomplished by video-assisted thoracic surgery in 39 patients and by standard thoracotomy in 10 patients. Four patients underwent formal lung resections, 1 had thymectomy, and 1 had en bloc chest wall resection. Four malignant variants were identified. One patient developed local recurrence and underwent redo surgery with chest wall resection. One patient died of unrelated disease. The remaining patients are alive and disease free at a median follow-up of 53.2 months.

Conclusions. LFTPs show a benign outcome in most of the cases. Video-assisted thoracic surgery, with intraoperative assessment of the surgical margins, represents the treatment of choice.

	Introduction

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Localized (or solitary) fibrous tumor of the pleura (LFTP) is a rare, slow-growing neoplasm with about 600 cases reported in the literature to date [1]. LFTP was first described as a distinct clinical entity among primary pleural tumors in 1931 by Klemperer and Rabin [2]. Because of controversy surrounding its histogenesis (mesothelial vs submesothelial), it has received different names, such as "subpleural fibroma" and benign or localized (fibrous) mesothelioma." Nowadays, this tumor is commonly known as localized (or solitary) fibrous tumor of the pleura (LFTP) and widely recognized as nonmesothelial in origin on the basis of immunohistochemical and ultrastructural findings [3, 4].

LFTPs are usually first discovered as asymptomatic lesions on routine chest radiographs, in adult patients, with no gender predilection and with no evidence of a relationship to asbestos exposure. Most of the cases show a benign clinical outcome even if malignant forms may occur up to 37% of the time [5].

The present study describes a series of 55 consecutive cases, surgically treated at our Institution during a 9-year period. The principal anatomo-clinical findings are presented and discussed.

	Material and methods

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From July 1990 to November 1999, 12,633 patients were admitted at the Unit of Thoracic Surgery of our institution. Of these, 55 patients (0.43%) were surgically treated for an LFTP. Our series included 32 males and 23 females with a mean age of 55 years (range 18 to 80 years) (Table 1). Symptoms were present in 23 patients (41.81%) and included chest pain, cough, dyspnea, and hyperthrophic osteoarthropathy; 1 patient had hypoglicemia. Three patients presented with pleural effusion (serous in 2 cases and bloody in 1 case). No history of exposure to asbestos was recorded. All patients underwent chest roentgenogram and computed tomographic (CT) scanning of the chest. Fiberoptic bronchoscopy was done in 32 patients (58.18%); magnetic resonance imaging (MRI) was performed in 10 cases (18.18%). Eleven patients (20%) underwent CT-guided fine needle aspiration biopsy (FNAB).

Immunohistochemistry was performed on formalin-fixed, paraffin-embedded tissue, using the streptavidin-biotin immunoperoxidase method. The following antibodies were used: Cytocheratin (AE1–AE3), CD 34, Vimentin [3].

Flow-cytometric analysis was performed on fresh material. A FACScan (Becton Dickinson & Co, Erembodegem, Belgium) was used to analyze the samples [6].

	Results

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Forty-eight of the cases (87.28%) were based on the visceral pleura and seven (12.72%) arose from the parietal pleura. Thirty-one tumors (56.36%) were pedunculated on visceral pleura-based pedicles. Among tumors arising from the visceral pleura, four showed a prevalent intrapulmonary growth (the so-called inverted fibroma). All tumors arising from the parietal pleura were broad based and not pedunculated.

Chest radiographs demonstrated a sharply marginated globular mass. CT scans showed a tissular mass that is homogenous, although larger tumors may show local areas of low attenuation, representing cystic or hemorrhagic degeneration (Figs 1–3). MRI showed on T1-weighted images an intermediated signal intensity; T2-weighted images demonstrated a variegated pattern depending on the composition of the tumor tissue.

View larger version (100K): [in this window] [in a new window]   Fig 1. Computed tomographic scan showing a broad-based solitary fibrous tumor of the parietal pleura.

View larger version (115K): [in this window] [in a new window]   Fig 2. Computed tomographic scan showing a pedunculated solitary fibrous tumor of the visceral pleura located within the fissure.

View larger version (103K): [in this window] [in a new window]   Fig 3. Computed tomographic scan showing a giant solitary fibrous tumor of the pleura (malignant variant) with focal areas of low attenuation, representing hemorrhagic degeneration.

A local removal of the neoplasm with histologically free surgical margins was accomplished by video-assisted thoracic surgery (VATS) in 39 patients (70.90%) and by standard thoracotomy in 10 patients (18.18%), including the case with three synchronous LFTPs. Two lobectomies and one bilobectomy were performed due to an intraparenchimal extension of the tumor (inverted fibroma), and one pneumonectomy was performed for a heavy bleeding encountered in the removal of a "giant" tumor (20 x 10 x 7 cm) with extensive vascular adhesions. One patient underwent local removal of the tumor plus thymectomy for an associated myasthenia gravis. The last patient affected by a broad-based histologically malignant tumor arising from the parietal pleura underwent en bloc chest wall resection 13 months after local removal by VATS.

Major complications included one atrial fibrillation (after left upper lobectomy) that resolved with amiodarone therapy and one localized pleural effusion (after VATS) that resolved with corticosteroids therapy. No operative mortality was reported. Macroscopically, most tumors were well circumscribed, lobulated in appearance, and firm in consistency. The cut surface was vaguely nodular, occasionally mycrocistic and myxoid, and white-gray in color. The malignant ones were larger in diameter, soft in consistency, and fleshy in appearance. The cut surface was variegated for the presence of large necrotic and hemorrhagic areas. Histologically, 51 cases (92.72%) were classified as benign while four cases (7.28%) were found to be malignant (Table 2). Microscopically, the benign LFTPs were composed of spindle cells arranged in a variety of patterns including hemangioperycitoma-like, neuroid, and storiform. In all cases, collagen production was abundant; in 2 cases the tumor was almost completely collagenized. Scattered mast cells were commonly observed. The mitotic count was low, ranging from zero to one mitosis per 10 HPFs. No abnormal mitoses were observed. All tumors showed pushing margins and were almost completely surrounded by a pseudocapsule. The malignant variants were more cellular with infiltrative margins. Cells were oval with evident nucleoli and little collagen production. Necrotic areas ranging from microscopic to geographic were always observed, and the mitotic count raised to more than four mitoses per 10 HPFs, including atypical mitoses.

Flow-cytometry was performed in 26 cases (47.27%), all belonging to the benign variants; the analysis revealed a diploid DNA content in 24 cases and a bimodal peak in two cases. Immunohistochemical analysis was performed in 23 cases (41.81%). All cases including three malignant cases were positive for CD34 and Vimentin, while none showed reaction to antikeratin antibodies.

All patients were included in a follow-up program that included clinical examination and chest roentgenogram after 1, 3, and 6 months, and every year. From 1995 onward, chest CT scan was performed every year. Follow-up ended January 25, 2000 and ranged from 2 to 114 months, with a median value of 53.2 months. Two patients were lost at follow-up, respectively, 12 and 19 months after surgery. Four malignant variants of LFTP were identified. Of these, 1 patient developed local recurrence 13 months after VATS removal of a malignant fibrous tumor of the parietal pleura: a chest wall resection was performed and 30 Gy of radiotherapy was also administered. Fifty-two months after redo surgery, the patient is alive and disease free. One patient, with a benign variant of LFTP, died from metastatic spread of a metachronous adenocarcinoma of the lung. All the remaining patients are alive and well at a median follow-up of 53.2 months.

	Comment

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The first report of a primary tumor of the pleura is historically traced back to Lieutaud in 1767 [7]. In 1931, Klemperer and Rabin [2] divided primary tumors of the pleura into two categories: diffuse mesothelioma and localized mesothelioma. They also proposed the submesothelial cell as the cell of origin for the latter tumor. In 1942, Stout and Murray [8], on the basis of in vitro cell culture findings, proposed mesothelial cells as the source of the so-called localized mesothelioma. Such controversy regarding the cellular origin of this tumor lasted for more than four decades, creating much confusion in the literature between diffuse and localized mesothelioma.

Recently, localized mesothelioma has been termed LFTP. It is now clear that the tumor cells of LFTP are not mesothelial in origin according to their immunoprofile (CD34⁺, Vimentin⁺, Cytokeratin^-) and ultrastructural features [3]. Furthermore LFTPs are not associated with asbestos exposure and usually show a good prognosis, whereas diffuse mesothelioma are related to asbestos exposure and mostly behave aggressively [4].

LFTP shows no gender predilection. In our series, there was a slight male predilection (32 male and 23 female) and, according to the literature, no cases were observed in childhood. The usual presentation, as described in over 50% of the cases reported in the literature, is an asymptomatic mass discovered incidentally on a chest radiograph [9]. Symptoms, if any, tend to be more common in larger lesions and include either local symptoms (such as chest pain, cough, dyspnea, and more rarely hemoptisis) or systemic symptoms (such as weakness, nocturnal sweating, chills, weight loss, digital clubbing, hypertrophic ostearthropathy, and hypoglicemia). When symptoms are present, they are more often multiple, regressing completely after surgical resection [10], as observed in our patients.

Hypertrophic osteoarthropathy is related to the abnormal production of hyaluronic acid by tumor cells and affects up to 20% of the patients [11, 12]. Hypoglicemia, which is observed in up to 2% to 4% of the cases, is attributed to the production of insulin-like growth factor II (IGF-II), which lowers the blood glucose and impairs the growth hormone counter-regulatory response to hypoglicemia [13]. These patients show symptoms associated with neuroglycopenia, which may be nonspecific, especially in the elderly [14]. Isolated cases of hypoglicemic coma have been reported in the literature [15]. In our series, only 1 patient (1.81%) showed asymptomatic hypoglicemia.

Serous pleural effusion affects fewer than 10% of the patients [10] and was present in two cases of our series (3.63%). One patient showed bloody pleural effusion, which has never been reported up to now; this finding was associated with a malignant variant of LFTP.

As previously noted, the FNAB is not a reliable diagnostic tool [10]; in fact, only 4 out of 11 cases (36.36%) were identified by FNAB.

Chest radiographs and CT scanning are the imaging studies of choice. Pedunculated tumors may show a marked mobility by changing position of the patient at fluoroscopy. A few cases with calcification have been reported [9]. In one of our cases, numerous psammoma bodies were found inside the tumor. The presence of a distinct pedicle at CT is an important diagnostic clue. Intravenous contrast administration may demonstrate a moderate to strong enhancement due to the high vascularity of the tumor. MRI can show the fibrous character of the lesion. The vascular bed of the tumor may be seen as serpigineous signal voids [9].

Multiple tumors are extremely rare [10]. One of our 55 patients (1.81%) showed three synchronous fibrous tumors localized on the visceral pleura of the same lobe.

The great majority of LFTPs have a benign clinical outcome with a long-term disease-free survival in around 90% of the cases [4, 5, 10, 16–18]. The single best predictor of a benign course was the complete excision with microscopically free surgical margins [4, 10, 18]. Intraoperative examination of the surgical margins is therefore mandatory. In parietal pleura broad-based tumor, a minimal extrapleural resection in order to assess the surgical margins is recommended. VATS gives a more precise view of the surgical margins and represents, in our opinion, the technique of choice in all pedunculated tumors and in most of the other cases. Furthermore, histological aspects of the tumor and the size of the lesion may have prognostic implications as well. In the series of 223 cases reported by England and associates [5], 82 (37%) were considered to be malignant and 114 (63%) were considered to be benign. Among 82 malignant tumors, 55% experienced an aggressive course with recurrences and/or metastases. Nevertheless, histologically malignant tumors that were pedunculated and easily excised usually behaved benignly. The malignant tumors ere usually greater than 10 cm in diameter, hemorrhagic, and necrotic. Among 114 benign tumors, 1.4% of the patients had recurrences [5]. In our series of 55 LFTPs, four (7.27%) malignant variants were identified with only one local recurrence, 13 months after the primary surgical treatment; this patient shows no evidence of disease 52 months after redo surgery and radiotherapy (30 Gy). The follow-up of the remaining 3 patients with malignant tumors is too short (3, 7, and 14 months, respectively) to assess a clinical judgment. Among 51 benign LFTPs reported in our series (92.73%), all patients are alive with no evidence of disease at a median follow-up of 53.2 months, except for 1, who died from metastatic spread of a metachronous adenocarcinoma of the lung.

In conclusion, LFTPs show a benign clinical outcome in most patients. Clinical outcome is mainly related to the completeness of the surgical treatment; moreover, important factors are the presence of a benign histological variant, a pedunculus, and a limited size.

The surgical treatment of choice is local removal by VATS with intraoperative assessment of free surgical margins. In parietal-pleura-based lesions, a minimal extrapleural resection to assess the margins is mandatory. If the parietal pleura show signs of tumor invasion, a chest wall resection is recommended. In inverted fibroma, we believe that a wedge resection with free surgical margins or a lobectomy should be performed. In large size lesions, if a VATS resection is technically feasible, it can be done; the surgical specimen must be estracted by means of a retrieval bag (Endoloop EJ 10G; Ethicon Inc, Somerville, NJ).

In the presence of intraoperative evidence of a malignant LFTP, we believe that the surgical approach should be tailored to the peculiar lesion. Broad-based neoplasms require a lobectomy if originating from the visceral pleural and a chest wall resection if originating from the parietal pleura. Pedunculated lesions can be safely treated with a wedge resection if originating from the visceral pleura or with a local resection with extrapleural dissection if originating from the parietal pleura, provided that the surgical margins are negative.

There are no clear data in the world literature regarding the role of adjuvant therapy in malignant LFTP [10, 18]; isolated reports claim the use of postoperative radiotherapy [10].

	Acknowledgments

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We thank Bruno Notargiacomo, MD, for providing data regarding in-hospital admissions and we sincerely acknowledge the skillful technical assistance of Raimondo Panzica. We also appreciate the help of thoracic specialty nurses Daniela Colasanti, Massimiliano Porena, and Alessandro Spano.

	Discussion

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DR PETER GOLDSTRAW (London, England): The one thing I have learned about these tumors is that they are often extremely vascular and have very thin-walled veins running across their surface. You mentioned that one of your cases went to pneumonectomy because of bleeding. Was that a benign case?

DR CARDILLO: The histology showed a benign pattern. We performed pneumonectomy because of a vascular lesion even if this was not a malignant pattern. A malignant tumor does not always predict a bad clinical outcome. The prognosis is related to the complete surgical excision either in benign or in malignant.

DR DOUGLAS E. WOOD (Seattle, WA): Often these tumors are very large, and in spite of your success in excising them with video-assisted techniques, I am interested in your techniques of removing them from the chest cavity using minimally invasive techniques. Have you had any difficulty with that, or do you find that you are needing to do a large utility thoracotomy to remove the bulky tumor after you have successfully excised it thoracoscopically?

DR CARDILLO: That is right. The mean size of these tumors in our experience was around 8 to 9 cm. So they are a little big. At the end of the videothoracoscopic procedure, we put the tumor in a retrieval bag and we performed a small incision. In some patients in which we were able to assess the pedunculus, we fragmentated the tumor inside the bag and then we pulled it away.

DR DANIEL L. MILLER (Rochester, MN): In the last 6 years at Mayo, we have operated on 3 patients for recurrent disease secondary to solid fibrous tumors. Two of these were local recurrence at a thoracoscopic site. In reviewing the operative reports from the other institutions, they had spillage at the time of surgery. They were all of a malignant variety. The other recurrence was a stalk implant, which at the time of surgery resection was across the stalk. The take-home message is that you must be aware of the malignant variety and the possibility of local recurrence as you experienced in your patients.

DR CARDILLO: Yes, we agree. We have to be very careful at the margins of the tumor.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Giuseppe Cardillo Massimo Martelli Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Cardillo, G. Articles by Martelli, M. Search for Related Content PubMed PubMed Citation Articles by Cardillo, G. Articles by Martelli, M.