Primary pleural tumors occur uncommonly in both children
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1 Review and Update of Uncommon Primary Pleural Tumors A Practical Approach to Diagnosis Laura Granville, MD; Alvaro C. Laga, MD; Timothy Craig Allen, MD, JD; Megan Dishop, MD; Victor L. Roggli, MD; Andrew Churg, MD, PhD; Dani S. Zander, MD; Philip T. Cagle, MD Objective. We address the current classifications and new changes regarding uncommon primary pleural tumors. Primary pleural tumors are divided according to their behavior and are discussed separately as benign tumors, tumors of low malignant potential, and malignant neoplasms. Data Sources. Current literature concerning primary pleural neoplasms was collected and reviewed. Study Selection. Studies emphasizing clinical, radiological, or pathologic findings of primary pleural neoplasms were obtained. Data Extraction. Data deemed helpful to the general surgical pathologist when confronted with an uncommon primary pleural tumor was included in this review. Data Synthesis. Tumors are discussed in 3 broad categories: (1) benign, (2) low malignant potential, and (3) malignant. A practical approach to the diagnosis of these neoplasms in surgical pathology specimens is offered. The differential diagnosis, including metastatic pleural neoplasms, is also briefly addressed. Conclusions. Uncommon primary pleural neoplasms may mimic each other, as well as mimic metastatic cancers to the pleura and diffuse malignant mesothelioma. Correct diagnosis is important because of different prognosis and treatment implications for the various neoplasms. (Arch Pathol Lab Med. 2005;129: ) Primary pleural tumors occur uncommonly in both children and adults. Metastatic cancers are by far the most common neoplasms of the pleura, greatly outnumbering the most common primary neoplasm of the pleura, diffuse malignant mesothelioma. There are a wide variety of much more uncommon tumors, both malignant and benign, that the surgical pathologist will infrequently be called on to diagnose. Although rare, it is important to recognize these uncommon pleural neoplasms and differentiate them from the more common metastatic cancers and diffuse malignant mesothelioma, as well as from each other, because of potentially significant differences in prognosis and therapy. In this article, a number of primary pleural lesions, both Accepted for publication July 14, From the Department of Pathology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (Dr Granville); Department of Pathology, Baylor College of Medicine, Houston, Tex (Dr Laga); Department of Pathology, University of Texas Health Center at Tyler (Dr Allen); Department of Pathology, Texas Children s Hospital, Houston (Dr Dishop); Department of Pathology, Duke University Medical Center, Durham, NC (Dr Roggli); Department of Laboratory Medicine, Health Sciences Centre Hospital, Vancouver, British Columbia (Dr Churg); Department of Pathology and Laboratory Medicine, University of Texas Health Science Center at Houston Medical School (Dr Zander); and Department of Pathology, The Methodist Hospital, Houston, Tex (Dr Cagle). The authors have no relevant financial interest in the products or companies described in this article. Reprints: Philip T. Cagle, MD, Department of Pathology, The Methodist Hospital, 6565 Fannin St Main Building, Room 227, Houston, TX ( pcagle@tmh.tmc.edu). benign and malignant, are reviewed. First, the uncommon entities that may present as primary tumors in the pleura are briefly defined. Second, a practical approach to the diagnosis of these uncommon neoplasms is presented, emphasizing the histopathologic features that may cause these tumors to mimic each other, as well as mimic metastatic cancers and diffuse malignant mesothelioma. We divide these primary pleural tumors into 4 major histologic patterns that may be encountered on biopsies or surgical specimens: (1) spindle cell, (2) epithelioid cell, (3) biphasic (at least 2 cell types), and (4) small blue cell. Four minor histologic patterns are also recognized, including papillary pattern, discohesive pattern, angiomatoid pattern, and lipomatous/clear cell pattern. We compare and contrast those pleural lesions with similar histologic appearances in order to facilitate accurate diagnosis of these rare pleural tumors. For additional information on pleural tumors, including rare primary neoplasms of the pleura, the reader is referred to several recent texts to which the authors of this review have contributed and edited. These include Pathology of Occupational Lung Disease, 1 Pathology of Asbestos-Associated Diseases, 2 Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart (World Health Organization Classification of Tumours), 3 Color Atlas and Text of Pulmonary Pathology, 4 and The Armed Forces Institute of Pathology s Tumors of the Serosal Membranes (Atlas of Tumor Pathology, 4th series). 5 BENIGN TUMORS Primary benign pleural tumors are much less common than metastatic cancers or diffuse malignant mesothelio Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
2 ma. However, because of their better prognosis and potential for successful treatment, including complete resection, benign pleural neoplasms must be recognized and differentiated from pleural malignancies. Eight primary benign pleural lesions are discussed: (1) solitary fibrous tumor, (2) nodular pleural plaque, (3) lipomatous tumors, (4) adenomatoid tumor, (5) calcifying fibrous tumor, (6) simple mesothelial cysts, (7) multicystic mesothelioma, and (8) schwannoma. Solitary Fibrous Tumor Although previously given a variety of names, such as submesothelial fibroma, localized mesothelioma, fibrous mesothelioma, and benign mesothelioma, the preferred term for this entity is now solitary fibrous tumor (SFT). The term localized fibrous tumor is also widely accepted, because these tumors may rarely be multiple. Solitary fibrous tumor is the most common benign neoplasm of the pleura. 6,7 The tumor usually is discovered in asymptomatic middleaged adults (occasionally in children) and affects men and women equally. Imaging studies usually disclose a welldemarcated, pleural-based mass. Approximately 50% of cases are pedunculated and most are solitary, although, as noted, rare patients with multiple SFTs have been reported. 8 Solitary fibrous tumors usually range from 5 to 10 cm in diameter, but giant SFTs up to 40 cm in greatest dimension do occur and can produce symptoms due to compression of surrounding structures. 9 Dyspnea, cough, and chest pain are the most common presenting symptoms, and pleural effusion may occur. Sometimes the tumor may produce insulin-like growth factor resulting in hypoglycemia, known as Doege-Potter syndrome. 10 The cut surface of an SFT is generally off-white, firm, and whorled. Necrosis suggests the possibility of malignant SFT, and adequate sampling is necessary to evaluate for malignant features. Histologically, SFTs are characteristically sharply circumscribed lesions with pushing borders composed of bland spindle cells in a collagenous stroma. Three patterns have been described: (a) patternless pattern of Stout, which has a hypocellular appearance with thick ropey collagen and inconspicuous spindle cells within slitlike spaces (Figure 1); (b) hemangiopericytoma-like pattern, which displays increased cellularity and classic staghorn vessels (Figure 2); and (c) cellular pattern, the most cellular, although variable from field to field and sometimes containing a storiform spindle cell arrangement (Figure 3). Although the cell of origin of SFT is unknown, the spindle cells appear primitive and resemble fibroblasts. Immunohistochemistry is usually helpful for confirming the diagnosis. Solitary fibrous tumor typically stain with CD34, CD99, Bcl-2, and vimentin, but not with keratin, desmin, smooth muscle actin, muscle-specific actin, S100 protein, CD31, or factor VIII. 6,11,12 Most SFTs are benign lesions that are cured by excision. 13,14 Absence of necrosis, cytologic atypia, and mitoses helps rule out a malignant SFT. 15 It is especially important to distinguish SFT from sarcomatous or desmoplastic malignant mesothelioma, which has an extremely poor prognosis. 16 This distinction is generally not a problem if the localized nature of the lesion is known, but pure reliance on histologic patterns in the absence of information about the gross distribution of tumor can easily lead to confusion. Other neoplasms that may be considered in the differential diagnosis of SFT include monophasic synovial sarcoma, peripheral nerve sheath tumor, desmoid tumor, undifferentiated sarcoma, and thymoma. Most tumors previously designated primary hemangiopericytomas of the pleura are now believed to be SFTs. Currently, molecular studies do not contribute to the diagnosis of SFT. Nodular Pleural Plaque Although nonneoplastic, nodular pleural plaque is included here because it may mimic both primary and metastatic pleural neoplasms. Pleural plaques can be nodular, mimicking pleural-based neoplasms on imaging, and are usually found in patients with a history of asbestos exposure. 17 The lesions are often bilateral and can be multiple. The pathologist may receive a biopsy to rule out malignant mesothelioma or other lesions of the pleura. Histologically, the pleural plaque is composed of virtually acellular collagen arranged in a basket-weave pattern (Figure 4). Metaplastic bone or calcification may be present. Nodular pleural plaques can be seen in association with mesothelioma, and rare cases have been associated with primary lung carcinoma. 18,19 The differential diagnosis includes desmoplastic mesothelioma and other spindle cell pleural neoplasms, but the hypocellular appearance of this lesion is distinctive and should enable its separation from these neoplasms. Lipomatous Tumors Lipomas and lipoblastomas of the visceral pleura may occur in children and are rare incidental findings. 20,21 Chest wall lipoma protruding into the pleural cavity is a more common incidental finding, seen in about 0.1% of all computed tomographic scans of the chest. 22 Magnetic resonance imaging may also be useful to better characterize these lesions. 23 These lesions are typically asymptomatic and detected incidentally. Only 1 case of a symptomatic subpleural lipoma has been reported, due to torsion of the pedunculated lesion that resulted in infarction and chest pain. 24 Histologically, lipomas consist of mature adipose tissue (Figure 5), and lipoblastomas are composed of lobules of immature fat cells. Surgical excision establishes the diagnosis and is curative. Adenomatoid Tumor Virtually always incidental findings, adenomatoid tumors typically arise in the genital tract, but rarely occur in extragenital locations such as the pleura. They appear as solitary, small, circumscribed nodules on imaging studies. 25,26 Histologically, adenomatoid tumors of the pleura are composed of vacuolated epithelioid mesothelial cells forming tubular spaces, identical to adenomatoid tumors in other locations (Figure 6). Keratin and mesothelial markers are generally immunoreactive. 27 Although the histology and immunohistochemical staining pattern of diffuse malignant mesothelioma can resemble the adenomatoid tumors, a lack of diffuse growth and invasion favors an adenomatoid tumor. Localized malignant mesothelioma must also be considered in the differential diagnosis. The characteristic adenomatoid pattern helps differentiate adenomatoid tumor from localized malignant mesothelioma. A case of localized malignant mesothelioma arising from an adenomatoid tumor has been reported. 28 Calcifying Fibrous Tumor Calcifying fibrous tumor, or childhood fibrous tumor with psammoma bodies, is typically found within sub- Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1429
3 Figure 1. Solitary fibrous tumor with characteristic hypocellular appearance; there are inconspicuous cells within slitlike spaces separated by thick bands of ropey collagen (hematoxylin-eosin, original magnification 200) Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
4 cutaneous and deep soft tissues, but rare cases have been reported in the pleura. 29 Usually presenting with chest pain or found incidentally, calcifying fibrous tumor is seen in young adults and shows no sex predilection. 30 The lesions can be solitary or multiple and range from a few millimeters up to 12 cm. 31 An unusual clinical presentation of a detached nodule that moved on imaging was attributed to necrosis of the pedicle and subsequent free mobility of the calcifying fibrous tumor within the pleural cavity. 32 Imaging studies may demonstrate calcification. Histologically, calcifying fibrous tumors have dystrophic calcification, which may be psammomatous, within a dense collagenous stroma with rare scattered fibroblasts and a variable lymphoplasmacytic infiltrate (Figure 7). The fibroblasts are generally immunoreactive with vimentin, CD68, and factor XIIIa and are usually immunonegative with cytokeratin and CD34, distinguishing calcifying fibrous tumor from diffuse malignant mesothelioma and SFT, respectively. Immunostaining for actin, desmin, S100 protein, and CD31 is also usually negative Other differential diagnostic considerations include calcified pleural plaque, calcified or hyalinizing granuloma, chronic fibrous pleuritis, amyloid deposition, and inflammatory pseudotumor. Calcifying fibrous tumor has rarely recurred after surgical excision. Simple Mesothelial Cysts Most simple mesothelial cysts are found incidentally in the peritoneum in women, but rare cases have been described in the pleura. 36,37 Usually measuring only a few centimeters, they can be multiple and can be free-floating. 38 Rarely, patients may present with pneumothoraxlike symptoms. 39 The simple cysts are fluid-filled with translucent fibrous walls lined by a single layer of flat to cuboidal mesothelial cells. Generally thought to represent hyperplastic reactive lesions or inclusion cysts rather than true neoplasms, they may or may not be related to multicystic mesotheliomas. Multicystic Mesothelioma Multicystic mesothelioma, also referred to as multicystic inclusion cyst, multilocular inclusion cyst, and benign multicystic mesothelial proliferation, arises most frequently in young or middle-aged premenopausal women. These lesions are most commonly found in the pelvic peritoneum. 40 Rare cases in other locations, including the pleura, have been reported. 41,42 Grossly, multiple or multilocular fluid-filled cysts with thin translucent walls spread along the serosal surface forming a multilocular mass. There may be associated unilocular cysts, including free-floating cysts. The cyst fluid is clear, serous, or gelatinous, and cytologic examination shows sheets of uniform mesothelial cells without significant atypia. Histologically, cysts of varying sizes are lined by flat to cuboidal mesothelial cells, sometimes with a picket-fence or hobnail appearance (Figure 8). Metaplastic change is not uncommon. Considered benign or indolent neoplasms by some authors and hyperplastic reactive lesions by others, they typically behave benignly. However, reports of recurrence and later development of diffuse malignant mesothelioma in some patients suggest that various authors may have included more than 1 entity in this category or, alternatively, that there is a true spectrum of behavior in this disease. 43 Schwannoma Schwannomas can radiographically resemble pleural neoplasms if they occur in a paraspinal thoracic location. These mediastinal schwannomas have the same histopathologic and immunohistochemical features of schwannomas in other locations (Figure 9). The rare melanotic variant of schwannoma, containing brown cytoplasmic pigment, most commonly occurs in the paraspinal region. One case report showed epithelioid cells with a signetring appearance mimicking adenocarcinoma in a pleural effusion associated with a paraspinal melanotic schwannoma. 44 Additionally, recurrent pleural effusions and hemothorax have been associated with rare schwannomas. 45,46 Rarely, malignant schwannomas, now called malignant peripheral nerve sheath tumors, may involve the pleura. 47,48 PRIMARY PLEURAL NEOPLASMS OF LOW MALIGNANT POTENTIAL There are 3 entities that are typically benign, but occasionally aggressive lesions: (1) pleural thymoma, (2) welldifferentiated papillary mesothelioma, and (3) desmoid tumor. These tumors are similar in that potential aggressive behavior can be unpredictable based on gross evaluation and histology alone in some cases. Pleural Thymoma Thymomas, both localized and diffuse, can arise in the pleura. Most patients are adults without myasthenia gravis symptoms. Rarely, patients experience acute chest pain after rupture of cystic thymomas. 49 On imaging and gross examination, the diffuse variant may mimic diffuse malignant mesothelioma. 50 Histologically, pleural thymomas are similar to mediastinal thymomas. Most have characteristic dual cell populations composed of epithelial cells and lymphocytes. 51 Some cases may have spindle cell morphology, expanding the differential diagnosis to include sarcomatoid malignant mesothelioma and SFT (Figure 10). 52 Occasional pleural thymomas may be sclerosing, mimicking desmoplastic mesothelioma and other desmoplastic neoplasms (Figure 11). Keratin immunostains may help highlight the epithelial component (Figure 12). Complete surgical resection for localized tumors is usually cu- Figure 2. Solitary fibrous tumor with characteristic hemangiopericytoma pattern containing branching blood vessels (hematoxylin-eosin, original magnification 150). Figure 3. Solitary fibrous tumor with characteristic cellular area with abundant spindle cells (hematoxylin-eosin, original magnification 300). Figure 4. Pleural plaque consists of virtually acellular, thick collagen in a basket-weave pattern (hematoxylin-eosin, original magnification 200). Figure 5. Pleural lipoma consists of mature adipose tissue (hematoxylin-eosin, original magnification 150). Figure 6. Adenomatoid tumor composed of vacuolated epithelioid mesothelial cells forming tubular spaces (hematoxylin-eosin, original magnification 300). Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1431
5 Figure 7. Calcifying fibrous tumor of the pleura showing dense, hyalinized stroma and scattered calcification (hematoxylin-eosin, original magnification 200). Figure 8. Benign multicystic mesothelioma shows multiple cysts of variable size containing serous fluid and lined by flat to cuboidal mesothelial cells (hematoxylin-eosin, original magnification 200) Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
6 rative, but diffuse variants or incompletely resected tumors may require radiation therapy. 53 Well-Differentiated Papillary Mesothelioma Well-differentiated papillary mesothelioma (WDPM) most commonly arises in the peritoneal cavity in women, but can also arise in the visceral or parietal pleura. 54 Although asbestos exposure has been reported in some cases (up to 46% in the latest series), there is currently no established epidemiologic correlation between WDPM and asbestos exposure. 55 Pleural WDPM occurs with similar frequencies in men and women, with a mean age of 60 years. Although often found incidentally at surgery, some patients with pleural WDPM have symptoms such as dyspnea, pleural effusion, chest pain, and/or pneumothorax. In WDPM, the symptoms tend to be milder and present more insidiously, often several years prior to diagnosis, in contrast to diffuse malignant mesothelioma, which typically presents with rapidly progressive symptoms. 55 Well-differentiated papillary mesothelioma usually has diffuse nodular growth, but can rarely form a localized mass. The nodules may be several centimeters in diameter, or the involved serosa may have a velvety appearance imparted by numerous small tumor nodules only a few millimeters in diameter (Figure 13). Histologically, WDPM has short broad papillae with definitive fibrovascular cores lined by a single layer of flat to cuboidal, uniformly bland mesothelial cells (Figure 14). Tumor cells do not show an increase in mitotic figures or large nucleoli. Although the growth pattern may be diffuse, the spread is superficial and deep invasion does not occur, except occasionally in recurrent or longstanding lesions. Myxoid degeneration of the papilla is a common finding, but necrosis should not be present. Psammoma bodies may be found. Solid and/or tubular growth may arise focally, and the localized variant often has a central scar. Immunohistochemical staining and electron microscopy confirm the mesothelial origin of the lining cells. The differential diagnosis includes diffuse malignant mesothelioma with focal WDPM-like pattern. Diagnosing WDPM by cytology or in a small biopsy specimen may be misleading because these specimens may not include an invasive component that could have important prognostic implications. However, if no frank invasion is seen in a completely excised lesion, localized WDPM is considered cured. 56 Generally, WDPMs with multiple small nodules have an indolent course with prolonged survival and in most instances do not shorten life expectancy. In contrast, recent data suggest that rare fatal WDPM can occasionally occur, and superficial invasive foci within WDPM may suggest a more aggressive clinical course. 54,55 However, rapidly progressive disease is not seen in true cases of WDPM. Desmoid Tumor Desmoid tumors, also called aggressive fibromatosis or musculoaponeurotic fibromatosis, most commonly arise in soft tissue but have been described in numerous anatomic locations and rarely may arise in the pleura. 57 The tumors are generally large with broad-based attachments to either the visceral or parietal pleura. The cut surface is typically firm, glistening, trabeculated, and white. Histologically, desmoid tumors are similar to desmoid tumors arising in other locations and contain a hypocellular, collagenous, or myxoid stroma with bland fibroblasts, fibrocytes, and myofibroblasts arranged in long fascicles with parallel, slitlike vessels (Figures 15 and 16). Immunostains with vimentin and muscle markers are usually positive, and immunostains with CD34 and keratin are usually negative. Immunostains may help exclude other spindle cell lesions of the pleura, such as SFT and solitary neurofibroma. 58,59 Molecular analysis has shown these proliferations to be clonal, and they often show strong expression of -catenin, either related to mutations in the adenomatous polyposis coli (APC) gene or to activating mutations in the -catenin gene The APC gene, located on the long arm of chromosome 5, indirectly induces the degradation of -catenin and leads to inhibition of the Wnt signaling pathway, which is important in tumor suppression. Desmoid tumors with a mutation in the APC gene often are found in patients with familial adenomatous polyposis syndromes, such as Gardner syndrome. The mutations are less common in sporadic cases. 63 These genetic mutations have not been correlated with prognosis. However, trisomy 8 may be correlated with a higher recurrence rate. 64 Desmoid tumors may recur, but adequate surgical resection is usually curative; these tumors have no propensity to metastasize. RARE PRIMARY MALIGNANT PLEURAL NEOPLASMS Diffuse malignant mesothelioma is the most common primary neoplasm arising in the pleura. Other rare primary malignant pleural neoplasms can occur and must be distinguished from diffuse malignant mesothelioma and metastatic cancers, owing to their varying treatment and prognosis. Metastatic pleural neoplasms are much more common than rare primary malignant neoplasms and, like diffuse malignant mesothelioma, generally have a poor prognosis. Eight rare malignant pleural neoplasms are discussed: (1) malignant solitary fibrous tumor, (2) localized malignant mesothelioma, (3) desmoplastic small round cell tumor, (4) primitive neuroectodermal tumor, (5) pleuropulmonary blastoma, (6) liposarcoma, (7) synovial sarcoma, and (8) vascular sarcoma. Malignant Solitary Fibrous Tumor Patients with malignant solitary fibrous tumor (MSFT) are more likely to present with chest pain, shortness of Figure 9. Schwannoma with spindle cells showing nuclear palisading (hematoxylin-eosin, original magnification 300). Figure 10. Pleural thymoma with prominent areas of spindled epithelial cells (hematoxylin-eosin, original magnification 350). Figure 11. Sclerosing pleural thymoma with islands of epithelial cells within abundant fibrous tissue (hematoxylin-eosin, original magnification 150). Figure 12. Keratin immunostain highlights the epithelial cells in a sclerosing pleural thymoma (keratin, original magnification 250). Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1433
7 Figure 13. Gross photograph of a well-differentiated papillary mesothelioma (WDPM) on the pleural surface. Fronds of WDPM rise above the visceral pleural surface in this wedge biopsy of lung tissue. Figure 14. Well-differentiated papillary mesothelioma shows fibrovascular cores lined by bland cuboidal mesothelial cells (hematoxylin-eosin, original magnification 150). Figure 15. Pleural desmoid tumor composed of hypocellular collagenous tissue with blood vessels (hematoxylin-eosin, original magnification 250) Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
8 breath, and pleural effusion than are patients with SFT. 60 While some similarities with SFT exist, MSFTs usually measure more than 10 cm in diameter and histologically have increased numbers of mitoses ( 4/10 high-power fields), increased cellularity with overlapping nuclei, cytological atypia, pleomorphism, and necrosis (Figure 17). 65 The tumor may have an invasive growth pattern and may involve adjacent structures, such as the parietal pleura, the pulmonary fissure, mediastinal structures, or pulmonary parenchyma. Some MSFTs may have areas histologically indistinguishable from high-grade sarcoma, abutting areas of typical-appearing SFT. 16 Immunohistochemical staining patterns for MSFT are similar to those of SFT. However, lack of expression of CD34 and high expression of CD31, p53, and Ki-67 are reported to be poor prognostic indicators. 15,66 Also, incomplete resection appears to predict a poorer outcome. Malignant solitary fibrous tumors can recur, metastasize, and be fatal in some cases. 8,14 Localized Malignant Mesothelioma A very rare lesion, localized malignant mesothelioma, has been reported in men and women with equal frequencies, between 40 and 70 years of age, and its association with asbestos exposure, if any, is unknown. 67,68 Some tumors are small and incidental, but size ranges to 10 cm in diameter. There may be an associated pleural effusion. The lesion is well-circumscribed by definition and may be either sessile or pedunculated, arising from the visceral or parietal pleura. Lack of diffuse spread over the pleural surface differentiates localized malignant mesothelioma from diffuse malignant mesothelioma. Localized malignant mesothelioma may be epithelial, biphasic, or sarcomatous, and is identical to diffuse malignant mesothelioma histologically and immunohistochemically. 69 Because of its localized nature, the lesion can often be successfully excised; however, some cases recur and it may metastasize, causing death. 70 Desmoplastic Small Round Cell Tumor A rare tumor classified as one of the pediatric small round blue cell tumors, desmoplastic small round cell tumor usually occurs in the peritoneal cavity of teenage boys. Six cases of primary thoracic desmoplastic small round cell tumor have been reported, however, in teenagers or young adults (4 males and 2 females), some of whom had pleural effusions. 71,72 Neoplastic growth was sometimes localized, but was more commonly diffuse. The histologic pattern is distinctive, with nests and cords of primitive-appearing small round cells, often showing nuclear molding, surrounded by dense, fibrous, desmoplastic stroma (Figure 18). Occasional cells with rhabdoid features can be seen with the primitive cell component. Unusual variants, such as the signet ring and anaplastic types, also occur. Immunohistochemical studies generally show staining with desmin (dotlike perinuclear location), vimentin, epithelial membrane antigen, Wilms tumor protein (WT-1), neuron-specific enolase, CD15, and keratins. Molecular studies demonstrating a specific translocation, t(11;22)(p13;q12), usually detected by reverse transcriptase polymerase chain reaction, can confirm the diagnosis This translocation results in a characteristic fusion transcript between the Ewing sarcoma gene on chromosome 22 and the Wilms tumor gene on chromosome 11. The fusion results in a unique chimeric protein that may play an important role in the pathogenesis of desmoplastic small round cell tumor. Some investigators have proposed that these tumors may arise from primitive mesothelial cells, but that has not been confirmed. Overall, desmoplastic small round cell tumor is relatively resistant to chemotherapy, with an aggressive course leading to death within 2 years in most patients, although 1 patient was reportedly alive at 5 years. 76 Primitive Neuroectodermal Tumor of Thoracopulmonary Region (Askin Tumor) The peripheral primitive neuroectodermal tumor, also referred to as Askin tumor when it involves the thoracopulmonary region, is a rare, small, round blue cell tumor and a member of the Ewing sarcoma tumor family. The tumor predominantly occurs in children and young adults, and often presents as a single lesion or multiple nodules involving the pleura. 77 Histologically, the primitive cells are nested and may form rosettes (Figure 19). Tumor cells are typically immunoreactive with S100 protein and synaptophysin, but do not stain with chromogranin. Ultrastructurally, peripheral primitive neuroectodermal tumor cells contain few neurosecretory granules. Cytogenetic studies show t(11;22)(q12,q24), which results in a fusion transcript between EWS and FLI-1, or molecular studies can demonstrate gene fusions of the Ewing sarcoma gene on chromosome 22 with a member of the ETS family of transcription factors. Generally, the tumor is aggressive with a poor prognosis. 78 Pleuropulmonary Blastoma Pleuropulmonary blastomas are tumors of childhood that can arise in the pleura, the lung parenchyma, and mediastinum. 79 Two cases have also been reported in adults. 80,81 The tumors can be associated with cystic lesions of the lung and should be distinguished from cystic adenomatoid malformation, particularly the peripheral cyst type (Stocker type 4). Symptoms of respiratory distress are often present, and imaging studies commonly show a unilateral mass, although rare bilateral cases have been reported. Some patients present with symptoms and imaging mimicking an empyema, and others may have associated pneumothorax Grossly, the tumors can be divided into 3 types: purely cystic (type 1), both cystic and solid (type 2), and purely solid (type 3). Histologically, the tumor is biphasic and consists of small blastemal cells that have scant cytoplasm and hyperchromatic nuclei, with spindled mesenchymal Figure 16. Pleural desmoid tumor consisting of fascicles of bland fibroblasts (hematoxylin-eosin, original magnification 250). Figure 17. Malignant solitary fibrous tumor shows extensive necrosis with pleomorphic spindle cells surrounding the necrosis (hematoxylin-eosin, original magnification 100). Figure 18. Pleural desmoplastic small round cell tumor demonstrating cords of small, round cells with minimal cytoplasm surrounded by a dense desmoplastic stroma (hematoxylin-eosin, original magnification 300). Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1435
9 Figure 19. Primitive neuroectodermal tumor of the chest wall (Askin tumor) is a highly cellular tumor of small, round cells with minimal cytoplasm (hematoxylin-eosin, original magnification 300). Figure 20. Pleuropulmonary blastoma demonstrates cystic spaces bounded by bands of mixed blastemal and spindle cells (hematoxylin-eosin, original magnification 150). Figure 21. Myxoid liposarcoma involving the pleura is composed of lipoblasts within a myxoid stroma (hematoxylin-eosin, original magnification 300) Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
10 cells sometimes containing primitive cartilage and frankly sarcomatous areas (Figure 20). The sarcomatous areas may include chondrosarcoma, liposarcoma, or rhabdomyosarcoma. Importantly, there is not a malignant epithelial component. Pleuropulmonary blastomas are uniformly immunoreactive with vimentin and may demonstrate other mesenchymal markers, depending on the type of sarcomatous differentiation. Tumor cells generally do not stain with cytokeratin and epithelial membrane antigen. Cytogenetic and molecular studies have found mutations in p53 and gains of chromosome Overall, pleuropulmonary blastoma is an aggressive neoplasm with variable long-term survival. 89 Liposarcoma Liposarcomas of the pleura are rare and usually present in adult men, but can occur in women and affect a wide age range. 90 The tumor often shows myxoid liposarcoma morphology and must be distinguished from diffuse malignant mesothelioma and MSFT with liposarcomatous differentiation (Figure 21). The treatment involves surgical excision and may be combined with chemotherapy, resulting in a variable prognosis. Synovial Sarcoma Synovial sarcoma may arise rarely as a primary pleural neoplasm, or more commonly, as a pleural metastasis from another location. 91,92 Pleural synovial sarcoma has only been widely recognized since Usually, the patient is a young or middle-aged adult, but a wide age range (9 72 years) has been reported and no gender predilection is recognized. The chief complaint is often chest pain, but some patients also have dyspnea, cough, hemoptysis, low-grade fever, and weight loss. The prognosis is generally poor. The tumor can recur and metastasizes to liver, bone, lung, and brain in approximately 20% of patients. Lymph node metastases are rare. The tumor can show a wide variety of growth patterns, from a localized well-circumscribed lesion to an invasive or diffuse growth pattern mimicking diffuse malignant mesothelioma. Grossly, necrosis and cystic degeneration may be evident. Histologically, the tumor can be either biphasic or monophasic, with the biphasic type being more common in the pleura. The spindle cell component has a monomorphic appearance and consists of spindled cells with carrot-shaped nuclei, sparse cytoplasm, variable mitoses, and fascicular arrangement within a variably collagenous to myxoid stroma. The epithelial component, if present, generally merges imperceptibly with the spindle cells and is composed of moderately sized polygonal cells, often forming glandular structures (Figure 22). 94 Mast cells may be present. Synovial sarcoma typically expresses cytokeratin, epithelial membrane antigen, CD56, Bcl-2, S100, calretinin, and CD99. The tumor cells generally do not stain with CD34, desmin, or smooth muscle actin. 95 Important differential diagnostic considerations include metastatic synovial sarcoma, spindle cell carcinoma, and sarcomatous diffuse malignant mesothelioma. 96,97 The majority of tumors studied, primarily from the extremities of young patients, show characteristic chromosomal translocations in greater than 90% of cases (t[x; 18][p11;q11]), which may be demonstrated by reverse transcriptase polymerase chain reaction, fluorescence in situ hybridization, or real-time polymerase chain reaction; these translocations confirm the diagnosis. 98,99 Monophasic synovial sarcomas commonly have fusion of the SYT gene to the SSX2 gene, while biphasic synovial sarcomas usually show a fusion between SYT and SSX Most primary intrathoracic synovial sarcomas demonstrate t(x;18) involving either the SSX2 gene or the SSX1 gene. 101 Vascular Sarcoma Vascular sarcomas arising in the pleura range from lowgrade epithelioid hemangioendotheliomas to high-grade angiosarcomas. 102 These neoplasms often present in adults and occur more commonly in men. There may be an association with chronic pyothorax in Japanese patients with pleural or pulmonary tuberculosis; this association has not been demonstrated in patients elsewhere. 103 The tumor may have a diffuse growth pattern, mimicking diffuse malignant mesothelioma in some cases. 104 Histologically, the epithelioid hemangioendothelioma-like tumors are composed of polygonal or spindle cells with bland nuclei and infrequent mitoses, arranged in cords or strands within a hyaline or myxoid stroma (Figure 23). The cells characteristically have intracytoplasmic lumina containing red blood cells, which can be highlighted by factor VIII staining. Metaplastic bone and osteoclast-like giant cells may be present. Angiosarcoma is histologically a high-grade neoplasm, with extensive hemorrhage and epithelioid or spindle cells forming cords, sheets, nests, and rudimentary vascular channels (Figure 24). The neoplastic cells have large pleomorphic nuclei and a high mitotic rate, and they line the vascular spaces and protrude into the vascular lumina. It may occasionally histologically mimic diffuse malignant mesothelioma. 105,106 Both epithelioid hemangioendotheliomas and angiosarcomas are typically strongly immunopositive with CD31 and CD34, and variably immunopositive with von Willebrand factor (factor VIII). Epithelioid angiosarcoma may stain with keratin, contributing to confusion with diffuse malignant mesothelioma. 107,108 Tumor cells do not usually stain with human herpesvirus 8. The prognosis for pleural vascular sarcomas is poor. 109 DIFFERENTIAL DIAGNOSIS General Considerations Pleural metastases, many of which have associated pleural effusions, are far more common than primary pleural neoplasms. The most common neoplasms metastasizing to Figure 22. Biphasic synovial sarcoma of the pleura shows spindle cells and glandlike spaces lined by epithelioid cells (hematoxylin-eosin, original magnification 150). Figure 23. Epithelioid hemangioendothelioma composed of relatively bland epithelioid cells in a hyaline stroma (hematoxylin-eosin, original magnification 350). Figure 24. Epithelioid cells form rudimentary vascular structures in a case of pleural angiosarcoma (hematoxylin-eosin, original magnification 300). Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1437
11 Table 1. Neoplasms With a Spindle Cell Histologic Pattern* Entity Age Growth Cytokeratin Vimentin Calretinin CD34 CD99 EMA Muscle Markers Bcl-2 S100 Treatment Prognosis Sarcomatoid DMM Adults Diffuse ( ) E E ND ( ) ND ( ) ND ( ) None Poor LMM Adults Localized ( ) E E ND ( ) ND ( ) ND ( ) Excision Good SFT All ages Localized ( ) E ( ) ( ) ( ) ( ) ( ) ( ) ( ) Excision Good MSFT All ages Localized ( ) E ( ) ( / ) ( ) ( ) ( ) ( ) ( ) Excision Variable Schwannoma Adults Localized ( ) ( ) ND ( ) ND E ( ) ( ) ( ) Excision Good CFT Young adults Localized ( ) ND ND ( ) ND ND ( ) ( ) ( ) Excision Good Desmoid tumor All ages Variable ( ) ( ) ( ) ( ) ( ) ( ) E or ( ) E ( ) Excision Variable Synovial sarcoma All ages Variable ( ) ( ) E ( ) E ( ) ( ) ( ) ( ) Excision Poor * EMA indicates epithelial membrane antigen; DMM, diffuse malignant mesothelioma; LMM, localized malignant mesothelioma; SFT, solitary fibrous tumor; MSFT, malignant solitary fibrous tumor; CFT, calcifying fibrous tumor; plus sign ( ), 70% to 100% of cases stained; minus sign ( ), 0% to 30% of cases stained; E, equivocal, 31% to 69% of cases stained; and ND, no data available. Rare cases may benefit from triple-modality therapy (excision, chemotherapy, and radiation). the pleura include lung carcinoma, breast carcinoma, lymphoma, gastrointestinal carcinoma, and genitourinary carcinoma. The most common histologic type of carcinoma metastatic to the pleura is adenocarcinoma. Prognosis is generally poor. 4,5 Diffuse malignant mesothelioma is the most common primary tumor of the pleura. Early lesions may show multiple pleural nodules that coalesce in later stages. The histopathologic appearance of diffuse malignant mesothelioma is highly variable. Major subtypes include (1) epithelioid, (2) sarcomatoid (which includes the desmoplastic subtype), and (3) biphasic (composed of mixed epithelial and sarcomatous elements). These tumors are often associated with asbestos exposure and are uniformly fatal. Therefore, it is of paramount importance to distinguish diffuse malignant mesothelioma, metastatic disease, and other rare primary pleural neoplasms, owing to the varying prognostic implications. 1 5 Practical Approach to Interpretation of Biopsy Specimens For differential diagnosis purposes, we can divide pleural neoplasms into 4 major histologic categories: (1) spindle cell, (2) epithelioid cell, (3) biphasic pattern (neoplasms composed of both spindle and epithelioid cells), and (4) small blue cell (neoplasms composed of cells with scant cytoplasm such that the predominant cytologic feature is that of a dark-staining nucleus on hematoxylin-eosin). There are also 4 minor patterns that are helpful to recognize: (a) papillary pattern, (b) discohesive pattern (the neoplastic cells lack cohesiveness), (c) angiomatoid pattern (neoplastic cells are arranged as vascular structures), and (d) lipomatous/clear cell pattern (clear or vacuolated cytoplasm predominates). Some neoplasms may show features of more than 1 pattern, and occasional lesions may not be classifiable within this system. Pleural neoplasms that resemble each other histologically may sometimes, but not always, be differentiated on the basis of gross, clinical, and radiologic findings; on the basis of histologic fields that permit a specific diagnosis; or on the basis of special studies, such as immunostains, molecular pathology, or electron microscopy. The clinical history and gross and radiologic distribution of the neoplasm should generally be compatible with the histologic diagnosis. Different types of pleural neoplasms, in addition to similar histologic features, can have overlapping clinical, radiologic, and gross findings; for example, several types of malignant neoplasms may present with pleural effusion and shortness of breath, as well as a widespread distribution over the pleural surface. Tables 1 through 4 list the major diagnostic considerations in the histologic categories discussed, including characteristic immunostains that may assist in diagnosis. Neoplasms With a Spindle Cell Pattern Spindle cell neoplasms can be divided into those that are hypocellular and those that are cellular. Those included in the hypocellular category include the patternless pattern of SFTs, nodular pleural plaque (which is not a true neoplasm, as noted previously), desmoplastic diffuse malignant mesothelioma, desmoid tumor, and calcifying fibrous tumor. 1 5 The patternless pattern of SFT has a hypocellular appearance with small cells within slitlike spaces, surrounded by thick ropey collagen (Figure 1). In contrast, a pleural plaque consists of virtually acellular collagen in a characteristic basket-weave pattern (Figure 4). Additionally, desmoplastic diffuse malignant mesothelioma may be deceptively hypocellular and may be difficult to distinguish from a benign pleural plaque (Figure 25). However, the extreme sparse cellularity of the nodular pleural plaque and the lack of significant cytological atypia should help differentiate these 2 lesions. Most importantly, desmoplastic diffuse malignant mesothelioma may show invasion of the underlying fat (a definitive feature for diagnosis), bland necrosis, or focal areas of overtly sarcomatous tumor. 5, Sarcomatoid diffuse malignant mesothelioma, including desmoplastic diffuse malignant mesothelioma, may not stain with calretinin or other markers of mesothelial differentiation. Negative staining in those cases does not indicate benignity. 114,115 Dense fibrous tissue with calcifications should raise the possibility of calcifying fibrous tumor of the pleura (Figure 7). Pleural desmoid tumor is another consideration when abundant collagen is seen in a biopsy specimen. Abundant collagen surrounds uniform spindle cells, often arranged in sweeping bundles (Figures 15 and 16). One or more muscle markers will usually be expressed by desmoid tumors, which, unlike SFTs, will not express CD ,116 Pleural thymoma may have abundant sclerosis, and the cellular component may be sparse (Figure 11). In these cases, immunostaining may assist differentiation of sclerosing pleural thymoma from a desmoplastic diffuse malignant mesothelioma (calretin Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
12 Table 2. Neoplasms With an Epithelioid Histologic Pattern* Entity Age Growth Cytokeratin Vimentin Calretinin CD34 EMA Treatment Prognosis Epithelioid DMM Adults Diffuse ( ) E ( ) ( ) ( ) None Poor LMM Adults Localized ( ) E ( ) ( ) ( ) Excision Good Epithelioid angiosarcoma Adults Variable E ( ) ( ) ( ) ( ) No effective Poor therapy Adenomatoid tumors Adults Localized ( ) E ( ) ND ( ) Excision Good Benign mesothelial Adults Localized ( ) ( ) ( ) ND E Excision Good proliferation Thymoma Adults Variable ( ) ( ) ( ) ( ) E Excision Variable and/or XRT Adenocarcinoma Adults Variable ( ) ( ) ( ) ( ) ( ) Chemo/XRT Poor Epithelioid synovial sarcoma All ages Variable ( ) ( ) E ( ) ( ) Excision Poor * EMA indicates epithelial membrane antigen; DMM, diffuse malignant mesothelioma; LMM, localized malignant mesothelioma; plus sign ( ), 70% to 100% of cases stained; E, equivocal, 31% to 69% of cases stained; minus sign ( ), 0% to 30% of cases stained; ND, no data available; chemo, chemotherapy; and XRT, radiation therapy. Rare cases may benefit from triple-modality therapy (excision, chemotherapy, and radiation). Table 3. Neoplasms With a Biphasic Histologic Pattern* Entity Age Growth Cytokeratin Vimentin Calretinin CD99 EMA Desmin Bcl-2 Treatment Prognosis Biphasic DMM Adults Diffuse ( ) E ( ) ( ) ( ) ( ) ND None Poor Biphasic synovial Adults Variable ( ) ( ) E E ( ) ( ) ( ) Excision Poor sarcoma Thymoma Adults Variable ( ) ( ) ( ) ( ) ND ( ) ( ) Excision and/or Variable XRT DSRCT Children Variable ( ) ( ) ( ) ND ( ) ( ) ( ) Chemo Poor PPB Children Localized ( ) ( ) ND ND ND E ND Excision/chemo/XRT Poor * EMA indicates epithelial membrane antigen; DMM, diffuse malignant mesothelioma; DSRCT, desmoplastic small round cell tumor; PPB, pleuropulmonary blastoma; plus sign ( ), 70% to 100% of cases stained; E, equivocal, 31% to 69% of cases stained; minus sign ( ), 0% to 30% of cases stained; ND, no data available; chemo, chemotherapy; and XRT, radiation therapy. Rare cases may benefit from triple-modality therapy (excision, chemotherapy, and radiation). Table 4. Neoplasms With a Small Blue Cell Histologic Pattern* Entity Age Growth Cytokeratin Vimentin CD45 CD99 EMA Desmin S100 Treatment Prognosis Small cell carcinoma Adults Diffuse ( ) ( ) ( ) ND ( ) ND ( ) Chemo Poor Askin tumor Children Variable ( ) ( ) ( ) ND ( ) ND ( ) Chemo Poor PPB Children Localized ( ) ( ) ND ND ND E ND Chemo/excision/XRT Poor DSRCT Children Diffuse (+) (+) ( ) ( ) (+) (+) ( ) Chemo Poor Lymphoma All ages Diffuse ( ) ( ) ( ) E ( ) ( ) ( ) Chemo Variable Melanoma Adults Variable ( ) ( ) ( ) ( ) ( ) ( ) ( ) Chemo Poor Small cell synovial All ages Variable ( ) ( ) ( ) ( ) ( ) ( ) ( ) Excision Poor sarcoma PNET/Ewings Children Variable ( ) ( ) ( ) ( ) ( ) ( ) ( ) Chemo Poor * EMA indicates epithelial membrane antigen; PPB, pleuropulmonary blastoma; DSRCT, desmoplastic small round cell tumor; PNET, peripheral neuroectodermal tumor; plus sign ( ), 70% to 100% of cases stained; minus sign ( ), 0% to 30% of cases stained; ND, no data available; E, equivocal, 31% to 69% of cases stained; chemo, chemotherapy; and XRT, radiation therapy. in positive), desmoplastic small round cell tumor, and the hypocellular spindle cell neoplasms mentioned previously. A biopsy specimen showing a cellular spindle cell neoplasm also has a broad differential diagnosis, including metastatic sarcomas, metastatic spindle cell carcinoma, other metastatic spindle cell malignancies, and sarcomatoid diffuse malignant mesothelioma. Sarcomatoid localized malignant mesotheliomas are histologically and immunohistochemically indistinguishable from sarcomatoid diffuse malignant mesothelioma, and their diagnosis requires correlation with clinical, radiologic, and gross findings. Schwannomas show palisading nuclei and variation in cellularity (Antoni A and Antoni B areas) (Figure 9). Positive staining with S100 protein can help confirm a diagnosis of schwannoma, but metastatic spindle cell melanoma (Figure 26) is also usually positive with S100 protein. Malignant solitary fibrous tumor exhibits increased cellularity, pleomorphism, and necrosis (Figure 17). On a small biopsy, MSFT can be histologically indistinguishable from high-grade sarcoma. Immunostaining with CD34 may be helpful in identifying both malignant and benign SFTs. 4,5,7 Additionally, monophasic synovial sarcoma shows hypercellularity with carrot-shaped nuclei and abundant mitoses. Immunostaining may be helpful, but not entirely specific for synovial sarcoma. Reverse transcriptase polymerase chain reaction for the characteristic Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al 1439
13 Figure 25. Desmoplastic diffuse malignant mesothelioma with hypocellular area and dense collagen resembling pleural plaque (hematoxylineosin, original magnification 300). Figure 26. Melanoma composed of spindle cells metastatic to the pleura (hematoxylin-eosin, original magnification 300). Figure 27. Epithelioid cells of a melanoma metastatic to the pleura (hematoxylin-eosin, original magnification 350). Figure 28. Clear cell renal cell carcinoma metastatic to the pleura. Note relatively bland nuclei and delicate capillaries (hematoxylin-eosin, original magnification 350). translocation, t(x;18), can be performed on paraffin-embedded tissue to assist in its diagnosis. 3 5,100,101, However, this molecular test does not distinguish a primary synovial sarcoma from metastatic synovial sarcoma, and clinical correlation is required. Rarely, other types of sarcoma may occur as primary pleural neoplasms, including liposarcoma, angiosarcoma, and leiomyosarcoma. Ultimately, clinical presentation, growth pattern, specific histologic features, and immunostaining patterns may all be required to differentiate spindle cell neoplasms presenting in the pleura (Table 1). Neoplasms With an Epithelioid Histologic Pattern Epithelioid neoplasms include metastatic carcinoma, metastatic melanoma, epithelioid diffuse malignant mesothelioma, epithelioid localized malignant mesothelioma, epithelioid angiosarcoma, adenomatoid tumor, benign mesothelial proliferations (including simple mesothelial cysts and multicystic mesothelioma), thymoma, and epithelioid synovial sarcoma. Epithelioid angiosarcoma may histologically resemble metastatic carcinomas and epithelioid diffuse malignant mesothelioma. Imaging studies may show localized growth or diffuse spread suggestive of diffuse malignant mesothelioma. However, recognition of the rudimentary vascular structures histologically is helpful in making the diagnosis of vascular sarcomas (Figures 23 and 24). Angiosarcoma may show immunopositivity with keratin. CD31 is positive in epithelioid angiosarcoma in nearly 100% of cases and is considered more sensitive than CD , In some cases of pleural thymoma the epithelial component may predominate, requiring differentiation from metastatic carcinoma and epithelioid diffuse malignant mesothelioma. Epithelioid synovial sarcoma may also be 1440 Arch Pathol Lab Med Vol 129, November 2005 Uncommon Primary Pleural Tumors Granville et al
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