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Japanese Journal of Clinical Oncology Pages 86-91

Frequent Expression of bcl-2 Protein in Solitary Fibrous Tumors
Introduction
Materials and methods
Results
   Clinicopathological Findings
   Histological Findings
   Immunohistochemical Findings
Discussion
References
Frequent Expression of bcl-2 Protein in Solitary Fibrous Tumors

Frequent Expression of bcl-2 Protein in Solitary Fibrous Tumors

Tadashi Hasegawa1, Yoshihiro Matsuno1, Tadakazu Shimoda2, Setsuo Hirohashi1, Takanori Hirose3, Toshiaki Sano3

1Pathology Division and 2Clinical Laboratory Division, National Cancer Center Research Institute, Tokyo and 3First Department of Pathology, University of Tokushima School of Medicine, Tokushima, Japan

The distinction of solitary fibrous tumors from histologically similar neoplasms is often difficult because they rarely occur at a variety of extrapleural sites. CD34 immunoreactivity has recently been recognized to be an adjunct for the diagnosis of solitary fibrous tumors. However, it is now known that CD34 staining is not entirely specific for this entity. We evaluated 23 solitary fibrous tumors and 54 other spindle cell tumors often considered in the differential diagnosis for immunoreactivity using monoclonal antibodies directed against bcl-2 protein, which protects cells from apoptosis and CD34. The patients with solitary fibrous tumors comprised 11 men and 12 women, ranging in age from 35 to 85 years (mean, 57.6 years). Fourteen tumors arose in the pleura, four in the retroperitoneum, three in the superficial soft tissue and one each in the mediastinum and uterine cervix. Nineteen of 23 solitary fibrous tumors (83%), irrespective of tumor site, demonstrated diffuse cytoplasmic staining for bcl-2 protein. bcl-2 immunoreactivity was also observed in five of seven neurofibromas (71%), eight of 10 synovial sarcomas (80%) and one of three spindle cell lipomas (33%). CD34 immunoreactivity was present in all but one solitary fibrous tumor (96%), seven of seven neurofibromas (100%), three of three spindle cell lipomas (100%), five of five dermatofibrosarcomas (100%), three of three hemangiopericytomas (100%) and two of seven malignant fibrous histiocytomas (29%). To date, most of the pleural and extrapleural cases have not shown aggressive features. We suggest that bcl-2 protein can be used together with CD34 in the diagnosis of solitary fibrous tumor to distinguish this entity from other spindle cell neoplasms.

Key words: bcl-2 - CD34 - soft tissue tumor - solitary fibrous tumor - immunohistochemistry

INTRODUCTION

The B-cell leukemia/lymphoma-2 (bcl-2) oncogene was first identified at the breakpoint of the t(14;18)(q32;q21) translocation, a chromosomal abnormality found in a majority of follicular lymphomas (1). Juxtaposition of the immunoglobulin heavy-chain gene on chromosome 14 with bcl-2 causes deregulated expression of high levels of the bcl-2 protein that has been shown to prolong survival of cells by preventing programmed cell death (apoptosis) (2). Subsequently, the bcl-2 protein has been discovered in a wide range of lymphoproliferative disorders without this chromosomal abnormality (3).

In adult normal tissues, bcl-2 expression seems to be confined to cell populations characterized by terminally differentiated (nonproliferative) elements, including peripheral nerve and brain, self-renewing tissues, such as hematopoietic lineages, epidermis and intestinal epithelia and hormone- or growth factor-dependent glandular epithelium, e.g. breast, prostate, endometrium and thyroid (4,5). The bcl-2 protein is also expressed in a variety of non-hematological epithelial malignancies and some neural and melanocytic tumors (6-10), but there have been few data on its expression and exact role in soft tissue tumors (11-13).

Solitary fibrous tumors are rare spindle cell neoplasms in adults that usually arise in the pleura. Because of a variegation of morphological patterns seen in these tumors, often overlapping with those of other spindle cell neoplasms, the aggressive clinical course in a minority of cases and their occurrence at a variety of extrapleural sites, the distinction of solitary fibrous tumors from other neoplastic lesions may be difficult. The CD34 antigen has recently been found to be a helpful marker for diagnosis of solitary fibrous tumors (13-23). bcl-2 expression in solitary fibrous tumors was initially reported by other investigators (13). In this study, we characterized the expression of bcl-2 protein and CD34 immunohistochemically in 23 solitary fibrous tumors and 54 other spindle cell neoplasms and also assessed their utility for differential diagnosis.

Materials and methods

We evaluated 77 formalin-fixed, paraffin-embedded tissue samples that were collected from the pathology files of the National Cancer Center and the First Department of Pathology, University of Tokushima School of Medicine, and the consultation files of the authors. These samples included 23 solitary fibrous tumors (Table 1), six leiomyosarcomas, seven neurofibromas, 10 synovial sarcomas, three spindle cell lipomas, eight fibromatoses, five dermatofibrosarcomas, three hemangiopericytomas, seven malignant fibrous histiocytomas, four fibrosarcomas and one sarcomatoid mesothelioma. Hematoxylin- and eosin-stained slides were reviewed to confirm the diagnosis. The clinicopathological, immunohistochemical and ultrastructural features (except for bcl-2 reactivity and recent follow-up data) of cases 6-8 of solitary fibrous tumors have been reported previously (22).

For immunohistochemical examination, 4 µm thick sections from the paraffin blocks were stained with monoclonal antibodies against bcl-2 protein (clone 124, 1:100, Dako, Carpinteria, CA) and CD34 (clone My10, 1:25, Becton Dickinson, San Jose, CA) by the labeled streptavidin-biotin (LSAB) method using an LSAB kit (Dako). To evaluate the proliferative activity of neoplastic cells in solitary fibrous tumors, a formalin-resistant epitope of Ki-67 was detected by immunostaining for MIB-1 (1:100, Immunotech, Marseille, France). As an antigen retrieval method, the tissue sections with bcl-2 and MIB-1 antibodies were preheated in a microwave oven in 10 mM citrate buffer, pH 6.0, for 15 min at 95°C.

Table 1. Clinicopathological findings and immunohistochemical results of solitary fibrous tumors
Case
No.		 Age (yr)/
sex		 Site Size (cm) Histological
grade		 Follow-up bcl-2 CD34 MIB-1
labeling (%)
1 38/M Retroperitoneum: bladder-pelvic space 12 Benign NED, 17 years + + 0.5
2 69/M Retroperitoneum: liver-retroperitoneal space 15 Benign NED, 3 years + + 1
3 47/M Retroperitoneum: ureter-pelvic space 12 Benign NED, 2 years 6 months + + 0.5
4 76/M Retroperitoneum: bladder-pelvic space 7 Benign NED, 6 months + + 1
5 78/F Uterine cervix: cervix-vaginal wall 6 Benign NED, 11 years + + 0.5
6 85/F Superficial soft tissue: upper arm 4 Benign NED, 5 years 9 months + + 1
7 50/M Superficial soft tissue: back 4 Benign NED, 1 year 6 months - + 1
8 50/F Superficial soft tissue: abdomen 3 Benign NED, 1 year 2 months + + 1
9 53/F Mediastinum 6.3 Benign NED, 6 years + + 10
10 45/M Pleura: visceral pleura 4.5 Benign NED, 19 years - + 0.5
11 43/F Pleura: visceral pleura 6 Benign NED, 11 years + + 0.5
12 46/F Pleura: visceral pleura 12 Benign NED, 10 years - - 0.5
13 59/F Pleura: visceral pleura 28 Benign NED, 6 years + + 2
14 54/M Pleura: mediastinal pleura 17 Benign NED, 3 years 8 months + + 0.5
15 63/F Pleura: parietal pleura 29 Benign NED, 3 years + + 1
16 36/F Pleura: visceral pleura 3 Benign NED, 2 years 8 months + + 0.5
17 67/M Pleura: visceral pleura-lung 2 Benign NED, 2 years 5 months + + 0.5
18 65/M Pleura: visceral pleura 2.8 Benign NED, 2 years 2 months + + 5
19 35/F Pleura: visceral pleura 2.2 Benign NED, 1 year 8 months + + 1
20 74/M Pleura: visceral pleura 15.5 Benign NED, 10 months + + 0.5
21 78/M Pleura: visceral pleura-lung 11 Benign NED, 4 months + + 10
22 39/F Pleura: visceral pleura 7.5 Benign NED, 3 months + + 0.5
23 74/F Pleura: parietal pleura-lung 18.5 Malignant REC, 9 months;
NED, 1 year 3 months		 - + 20
M, male; F, female; NED, no evidence of disease; REC, recurrence; +, positive; -, negative.

Results

Clinicopathological Findings

The clinicopathological features of the 23 solitary fibrous tumors are summarized in Table 1. The patients consisted of 11 men and 12 women, ranging in age from 35 to 85 years (mean 57.6 years). Of the 23 tumors, 14 involved the pleura; the remaining nine were from extrapleural sites. The majority of the tumors appeared as localized, well circumscribed, encapsulated masses. Most of the pleural tumors originated in the visceral pleura as a polypoid mass and seven had short pedicles attached to the pleura. Two tumors grew from the visceral pleura, compressing the lung parenchyma inward and one (case 23) arose from the parietal pleura and adhered to the lung. Four tumors were located in the retroperitoneum, two were situated in the posterior wall of the bladder, one was attached to the ureter and one to the liver. One tumor arose in the uterine cervix and extended into the vaginal wall. Three tumors were located in the superficial soft tissue of the upper arm, back and abdomen. The size of the tumors ranged from 2 to 29 cm (mean 9.9 cm) in greatest diameter.

Thirteen patients were asymptomatic at the time of presentation, the lesions being discovered on either routine chest radiographs or computed tomograms taken for unrelated conditions. Two patients with plural tumors complained of cough and dyspnea. Of the four patients with retroperitoneal tumors, two had abdominal pain and a lower abdominal mass. Three soft tissue lesions were found as painless masses. One patient with a tumor of the uterine cervix presented with genital bleeding. A history of hypoglycemia was reported in two patients.

All cases were treated by surgical excision. One tumor was considered histologically malignant on the basis of previous criteria (24). Follow-up was possible in all patients and ranged from 3 months to 19 years (mean 4 years 11 months). All patients whose tumors were classified as benign by light microscopy showed no recurrence and were subseqently free of disease. One patient with a malignant tumor developed local recurrence 9 months later, but was alive and well at the latest follow-up.

Histological Findings

The solitary fibrous tumors were composed of relatively uniform, bipolar spindle or oval cells in a heavily collagenized stroma, often showing abundant blood vessels in a hemangiopericytoma-like pattern (Fig. 1). The degree of cellularity varied a great deal from area to area and in less cellular areas the intercellular collagen was often thick and keloid-like. The other growth patterns included fascicular areas, storiform and herringbone formations and wavy neurofibroma-like and monophasic synovial sarcoma-like areas in the solid spindle cell component, thus simulating a variety of soft tissue neoplasms. Some tumors showed compact clusters of polygonal cells with a rather epithelioid appearance. Mitotic activity was generally low, ranging from 0 to 2/10 HPFs. Focal areas of necrosis were identified in five cases. Stromal cystic degeneration and myxoid change were also present in three and two instances, respectively.


Figure 1. Solitary fibrous tumor showing haphazard proliferation of spindle cells in a fibrocollagenous background. The prominent vascularity is reminiscent of hemangiopericytomas (HE).

One tumor was highly cellular and mitotically active, showing histologically malignant features, but otherwise resembled the patterns decribed above. This lesion showed highly cellular spindle cell areas resembling fibrosarcoma, made up of plump spindle or round cells with hyperchromatic nuclei, more frequent mitoses (>4 mitotic figures/10 HPFs) and extensive necrosis (Fig. 2).


Figure 2. Histologically malignant solitary fibrous tumor having areas of increased cellularity characterized by interlacing fascicles of spindle cells with hyperchromatic nuclei and mitotic figures (HE).

Table 2. Immunoreactivity for bcl-2 and CD34 in solitary fibrous tumors and other spindle cell tumors
Tumor No. of cases bcl-2 positivity (%) CD34 positivity (%)
Solitary fibrous tumor 23 19/23 (83) 22/23 (96)
Leiomyosarcoma 6 0/6 (0) 0/6 (0)
Neurofibroma 7 5/7 (71) 7/7 (100)
Synovial sarcoma 10 8/10 (80) 0/10 (0)
Spindle cell lipoma 3 1/3 (33) 3/3 (100)
Fibromatosis 8 0/8 (0) 0/8 (0)
DFSP 5 0/5 (0) 5/5 (100)
Hemangiopericytoma 3 0/3 (0) 3/3 (100)
MFH 7 0/7 (0) 2/7 (29)
Fibrosarcoma 4 0/4 (0) 0/4 (0)
Sarcomatoid mesothelioma 1 0/1 (0) 0/1 (0)
DFSP, dermatofibrosarcoma protuberans; MFH, malignant fibrous histiocytoma.

Immunohistochemical Findings

The results of immunostaining for bcl-2 and CD34 in solitary fibrous tumors and other spindle cell tumors are shown in Tables 1 and 2. Expression of bcl-2 protein was detected in 19 (83%) of the 23 solitary fibrous tumors (Fig. 3). In each case, staining for bcl-2 protein was distributed diffusely throughout the cytoplasm with perinuclear enhancement of the spindle cell component. Tumor site had little influence on the frequency of bcl-2 immunoreactivity. Regardless of positivity or negativity for bcl-2 protein in the solitary fibrous tumors, scattered lymphocytes expressed the bcl-2 protein and thus served as internal controls.


Figure 3. bcl-2 immunoreactivity of solitary fibrous tumor displaying diffuse cytoplasmic staining with perinuclear enhancement in many tumor cells (immunoperoxidase stain, hematoxylin counterstain).


bcl-2 immunoreactivity was also observed in five of seven neurofibromas (71%), eight of 10 synovial sarcomas (80%) and one of three spindle cell lipomas (33%). Schwann cells having wavy hyperchromatic nuclei in neurofibromas and both spindle and epithelioid cells in synovial sarcomas showed diffuse bcl-2 immunoreactivity, whereas spindle cells in spindle cell lipomas exhibited diffusely weak bcl-2 reactivity. No expression was found in leiomyosarcomas, fibromatoses, dermatofibrosarcomas, hemangiopericytomas, malignant fibrous histiocytomas, fibrosarcomas or sarcomatoid mesothelioma.

CD34 immunoreactivity was present in all but one solitary fibrous tumor (96%). CD34 reactivity was characterized by diffuse cytoplasmic and fibrillar staining (Fig. 4). The staining was nearly uniform in the histologically benign cases and patchy in the malignant case. The histological features of the cases negative for bcl-2 and/or CD34 did not differ significantly from those of the positive cases.


Figure 4. Numerous spindle cells of solitary fibrous tumor showing fibrillar positive staining for CD34 (immunoperoxidase stain, methyl green counterstain).

CD34 immunoreactivity was observed in seven of seven neurofibromas (100%), three of three spindle cell lipomas (100%), five of five dermatofibrosarcomas (100%), three of three hemangiopericytomas (100%) and two of seven malignant fibrous histiocytomas (29%). The CD34-positive cells in neurofibromas had delicate dendritic processes with oval or rounded nuclei, distinct from the Schwann cells. Similarly to the staining seen in solitary fibrous tumors, spindle cell lipomas and dermatofibrosarcomas showed diffuse, strong positivity for CD34 in the spindle cells. Hemangiopericytomas exhibited CD34 positivity in a large number of perivascular spindle cells. Malignant fibrous histiocytomas showed heterogeneous reactivity for CD34.

The numbers of MIB-1-positive nuclei were low in all histologically benign cases, ranging from 0.5 to 10% (mean 1.8%). The MIB-1 labeling was higher (20%) in the malignant tumor.

Discussion

Approximately 83% of solitary fibrous tumors that we evaluated, irrespective of tumor site, demonstrated diffuse cytoplasmic staining with an anti-bcl-2 antibody. In keeping with previous studies (13-23), 96% of evaluated solitary fibrous tumors were CD34-positive.

When solitary fibrous tumors occur at extrapleural sites, such as the retroperitoneum and soft tissue, they may be confused histologically with other spindle cell neoplasms (19,23,25). Solitary fibrous tumors usually show negative immunoreactions for cytokeratin, smooth-muscle actin and S-100, but are positive for CD34 (13-23). CD34 is a 110 kDa transmembrane glycoprotein present on human hematopoietic progenitor cells and vascular endothelial cells (26). Although originally described as a marker specific for vascular lesions, it is now clear that CD34 has a much broader reactivity in non-vascular mesenchymal tumors of diverse types. Similarly to previous studies (16,27-31), we found that dermatofibrosarcoma protuberans and hemangiopericytomas demonstrated diffuse CD34 immunoreactivity. In contrast to the occasional staining described in non-gastrointestinal smooth muscle tumors (16,28,32,33), leiomyosarcomas in our series failed to stain for CD34. Malignant fibrous histiocytomas have been reported to show areas of tumor cells with distinctive CD34 reactivity in sporadic cases (31,32).

CD34 positivity observed in neurofibromas was confined to a dendritic spindle cell population, similar to the findings reported by others (30). Likewise, strong CD34 positivity has recently been described in the spindle cells of spindle cell lipomas (34). It was postulated that the morphological similarities of the spindle cells and the strong CD34 positivity in both spindle cell lipomas and solitary fibrous tumors suggested a close kinship of their cell lineages. The exact histogenesis of solitary fibrous tumors remains controversial. Common CD34 immunoreactivity in solitary fibrous tumors seems to indicate that these tumors could be derived from certain specific populations of CD34-positive dendritic interstitial cells (35).

We found diffuse bcl-2 positivity in the majority of neurofibromas and synovial sarcomas as well as solitary fibrous tumors. Cytogenetic abnormalities involving 18q21, where the bcl-2 gene is located, are not associated with solitary fibrous tumors (36). The expression of bcl-2 protein in neural crest-derived tumors such as primitive neuroectodermal tumors, melanomas and peripheral nerve sheath tumors appears to reflect the phenotype of its normal counterpart rather than an anomaly of chromosome 18 (6-8). About 80-100% cases of Kaposi's sarcoma and synovial sarcoma have also been reported to exhibit bcl-2 immunoreactivity (11,12). It has been speculated that viral infection may upregulate high levels of bcl-2 in Kaposi's sarcoma, in which the etiological agent for Kaposi's sarcoma is now termed human herpes virus type 8 (HHV8). The possibility of a correlation between the bcl-2 expression in synovial sarcoma and the characteristic chromosomal translocation t(X;18) has been proposed (12). Another mechanism might be involved in the deregulation of bcl-2 gene in solitary fibrous tumors. It is of interest that weak but diffuse reactivity for bcl-2 protein was observed in the spindle cells of one case of spindle cell lipomas.

The principal differential diagnoses of solitary fibrous tumor are monophasic fibrous synovial sarcomas, commonly bcl-2 positive and nerve sheath tumors, sometimes bcl-2 positive. Demonstration of S-100 positivity will help in differentiating between the nerve sheath tumor and solitary fibrous tumor. An immunohistochemical absence of CD34 in synovial sarcomas, as found in our study, serves to separate them from solitary fibrous tumor. In addition, demonstrating positivity of the spindle cells with cytokeratin and epithelial membrane antigen in synovial sarcoma and negative labeling with these antibodies in solitary fibrous tumor should be of aid in the diagnosis (13-15,17-23).

Recently, a majority of solitary fibrous tumors have been reported to show bcl-2 immunoreactivity (13), similar to our results. Among these studies, many gastrointestinal stromal tumors, that are peculiar mesenchymal neoplasms of uncertain histogenesis arising in the muscular wall of the gastrointestinal tract, coexpressed CD34 and bcl-2 protein.

A variety of other entities, such as leiomyosarcoma, fibromatosis, dermatofibrosarcoma protuberans, hemangiopericytoma, malignant fibrous histiocytoma, fibrosarcoma and sarcomatoid mesothelioma, which are frequently considered in the differential diagnosis of solitary fibrous tumor, were uniformly bcl-2 negative. bcl-2 protein may play a role in rescuing of neoplastic cells from apoptotic cell death, leading to slower tumor growth. However, it is obscure how the prevention of apoptosis by bcl-2 protein is related to a variety of other tumors, such as leiomyosarcoma and fibromatosis, because apoptotic tumor cell death does not always occur in these bcl-2-negative tumors.

It has been reported that almost 90% of solitary fibrous tumors are cured by surgical excision. Briselliet al. (37), in a thorough review of the literature, found that 12% of pleural tumors had caused death because of extensive intrathoracic growth. Indicators of good prognosis were the presence of a pedicle, good circumscription and absence of nuclear pleomorphism or mitotic activity. The outlook for extrapleural lesions is uncertain largely because of the small number of reported cases (23,25,38). Most of the pleural and extrapleural cases in our study, despite their large size, did not show local recurrence for periods of up to 19 years. This non-aggressive behavior appeared to be supported by their low mitotic rate and MIB-1 labeling.

In summary, this study has shown that abnormal expression of bcl-2 protein is frequently found in solitary fibrous tumors. bcl-2 protein is potentially useful in the diagnosis of this entity and for distinguishing solitary fibrous tumors from other spindle cell tumors, especially those arising at unusual sites.

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Received July 16, 1997; accepted September 8, 1997
For reprints and all correspondence: Tadashi Hasegawa, Pathology Division, National Cancer Center Research Institute, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104, Japan
Abbreviations: HHV8, human herpes virus type 8; M, male; F, female; NED, no evidence of disease; REC, recurrence; DFSP, dermatofibrosarcoma protuberans; MFH, malignant fibrous histiocytoma

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