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Tumor and tumorlike conditions of the pleura and juxtapleural region: review of imaging findings
Insights into Imaging volume 12, Article number: 97 (2021)
Abstract
Pleural lesions form a diagnostic challenge for the radiologist. Whereas lesions can be initially detected on chest radiographs, CT and MRI imaging are the imaging modalities of choice for further characterization. In a number of cases, imaging findings can be relatively specific. In general unfortunately, imaging findings are rather aspecific. Evolution and extrathoracic imaging findings are important clues toward the diagnosis.
Key points
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CT and MRI are the modalities of choice for imaging (juxta)pleural tumors.
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Imaging findings may be aspecific and diagnostically challenging.
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Patient characteristics and evolution in time are important clues toward the diagnosis.
Introduction
The thoracic space is divided into right and left pleural cavity with a serous membrane, the pleura, contouring both cavities. The pleura is composed of two thin layers of mesothelium: the visceral and parietal pleura. The visceral pleura covers the surface of the lungs and fissures, whereas the parietal pleura covers the thoracic wall and diaphragm. In most cases, the lung does not completely fill the pleural cavity, allowing the parietal pleurae to converge, forming the pleural recess. The visceral pleura is vascularized by arterial branches of the bronchial and pulmonary arterial system, whereas the parietal pleura by intercostal vessels (systemic supply). Due to intercostal nerve innervation, the parietal pleura is sensitive to pain. Both pleurae form a two-layered pleural space containing approximately 5 ml of physiological pleural fluid. Histologically, the pleura is defined as a serous membrane composed of mesothelial cells and loose connective tissue [1, 2].
There is a broad variation in pleural pathologies, with both benign and malignant etiologies. The real prevalence of all pleural pathologies is unclear in the literature. The most common primary malignancy of the pleura is a malignant mesothelioma, with an estimate of 10,000 new cases annually across Western Europe, Scandinavia, North America, Japan, and Australia [3]. Pleural metastases are the most common secondary malignancies often associated with malignant pleural effusion. They are mainly found in primary malignancies of the lung, breast, lymphoma, and ovarian cancer [4]. Primary pleural malignancies, other than mesothelioma, are less frequent and are often a diagnostic challenge for radiologists. According to the 2016 World Health Organization classification of tumors of the pleura, they can be divided into mesothelial tumors, lymphoproliferative disorders, and mesenchymal tumors [5].
This article focuses on primary pleural malignancies, other than mesothelioma, and juxtapleural malignancies. The aim of this pictorial review is to provide a structured overview of the imaging features, with clues for diagnosis and differential diagnosis (Table 1).
Imaging strategy
Conventional radiography (CR) is often the first-line imaging modality for patients with thoracic complaints. One of the signs of an extrapulmonary lesion on chest CR is an incomplete border sign, in which part of the border is invisible. Other signs suggestive of a pleural lesion are displacement of the pulmonary vasculature and respiratory-associated changes in location of the lesion [6]. However, chest CR is often aspecific. Pleural effusion is a common secondary finding that can also be diagnosed by ultrasound. The presence of fibrous septations and/or loculation of the pleural effusion is suggestive of a chronic or malignant effusion. Peripherally located lesions and locoregional chest wall and/or rib invasion may also be visualized using ultrasound [7, 8]. Computed tomography (CT) is used for further visualization and characterization of the pleural lesion, and to define its relationship with the surrounding structures [1]. When comparing to CR and CT, Magnetic resonance imaging (MRI) has a better ability to determine the relationship between the pleural lesion and the surrounding structures, in particular the chest wall and spinal canal. Diffusion-weighted imaging (DWI) on MRI may be helpful in differentiating benign from malignant pleural lesions and in correcting false-positive 18F-Fluorodeoxyglucose positron emission (18-FDG PET) CT findings [9, 10]. The 18F-FDG PET is indicated for the evaluation of distant metastases and other abnormalities that can lead to diagnosis. For complete diagnostic evaluation, ultrasound- or CT-guided biopsy of the lesion and/or pleural effusion may be necessary.
Primary pleural malignancies
Lymphoproliferative disorders
Pleural lymphomas are mainly seen as secondary when in association with other thoracic abnormalities or in cases of aggressive subtypes. They arise from the direct extension from a pulmonary or nodal disease, or through hematogenous or lymphatic dissemination. Patients present with aspecific complaints, including chest pain, dyspnea, or cough. Pleural effusion is one of the main manifestations on imaging. Pleural thickening or solid pleural lesions are less commonly seen with frequently missed pleural lesions due to small size or fluid superposition. Both unilateral and bilateral pleural involvements are possible [11, 12].
Primary pleural lymphomas are rarely diagnosed and consist of two distinct subtypes [13]. The first subtype is the primary effusion lymphoma (PEL), which is a diffuse large B-cell lymphoma (DLBCL) caused by the human herpes virus type 8 or Kaposi sarcoma-associated herpes virus. A unilateral effusion with a homogeneous near-water attenuation is seen on imaging without evidence of solid disease. Therefore, an isolated pleural effusion in a patient with an AIDS-related immune deficiency should alert radiologists and clinicians to the possible diagnosis of PEL (Fig. 1).
The second subtype is the pyothorax-associated lymphoma (PAL). This Epstein-Barr virus (EBV)-positive DLBCL is exclusively seen in patients with chronic pyothorax, usually due to iatrogenic-induced pneumothorax from tuberculosis treatment [3]. The highest incidence of PAL is seen in Japan, as more than 90% of the population is infected with EBV, and lung collapse therapy is widely performed there [12]. Imaging characteristically shows an inhomogeneous solid pleural mass that may extend directly into the lung; locoregional rib destruction has been described in the literature. In contrast to PEL, pleural effusion is not always present. Both PEL and PAL are associated with a poor prognosis [7, 12].
Mesenchymal tumors
The term mesenchymal tumors includes a broad spectrum of various pathologies originating from transformed cells of connective tissue origin. One of the characteristics of these primary malignancies is that most of them are focal.
Solitary fibrous tumors
Solitary fibrous tumors (SFTs) are the second most common primary pleural tumors following mesothelioma, although less than 800 cases have been reported in the literature. Patients from all ages have been described, but predominantly in the age range of 50 to 60 years [14]. Since up to half of patients are usually asymptomatic, SFT is often an incidental finding; however, cough, chest pain, and dyspnea may be presenting symptoms. In 20% of cases, the mass originates from the parietal pleura, predisposing to chest pain. SFTs may be benign or malignant, with approximately 10% to 20% of SFTs being malignant. Malignant SFTs are often associated with clinical symptoms; however, there is no correlation between symptoms and diagnosis of malignancy. SFT is associated with hypertrophic pulmonary osteoarthropathy in 10–30% of cases (Pierre-Marie-Bamberger syndrome). Rarely, patients present with hypoglycemia secondary to tumor-induced production of insulin growth factor (IGF) 2. The IGF-2 leads to activation of IGF-1 and an insulin-like response resulting in hypoglycemia. Doege–Potter syndrome is rare, with an estimated incidence of 3–4% [15].
Standard chest radiography revealed a well-circumscribed pulmonary mass (Fig. 2) with variable size, located adjacent to the pleural surfaces or fissure. A pedunculated tumor may change location on sequential images. As the peduncle itself is not always visible, the change in location is an indirect sign, suggestive of a pedunculated tumor (Fig. 3).
CT is the imaging modality of choice and allows a detailed view of a well-circumscribed mass. SFTs are generally heterogeneous on CT (Fig. 2), with focal hypoattenuating areas due to necrosis, cystic degeneration, or myxoid components. Intralesional hemorrhage and calcifications (2 up to 26%) are seen as hyperdense foci. The focal mass effect leads to displacement of the surrounding structures rather than invading them [16].
MRI can be used to evaluate the relationship between the chest wall and diaphragm. Typically, a low to intermediate signal intensity on T1-weighted images (WI), and low signal intensity (SI) on T2-WI are seen (Fig. 4). After intravenous gadolinium contrast administration, there is a heterogeneous enhancement of the mass.
The most diagnostic challenge in SFTs is the differentiation between benign and malignant tumors [17]. The most important imaging parameter is the size of the lesion; if it is larger than 10 cm, the SFT is malignant until proven otherwise [13, 16]. An increase in size over time, pleural effusion, chest wall invasion, and hypervascularity are other imaging features that may suggest malignancy [14, 17].
Data on the use of 18-F-FDG PET imaging in SFTs are scarce, and FDG-PET seems to be of little value in the diagnosis of benign and malignant tumors and to differentiate between them. Malignant tumors tend to be more hypermetabolic than benign tumors, but there is an overlap in standardized uptake value (SUV) max values between these tumors [18]. 18F-FDG-PET may have a high negative predictive value in assessing the malignancy of SFTs (Fig. 5) [19].
Desmoid-type fibromatosis
Desmoid-type fibromatosis, also known as aggressive fibromatosis, is a benign disease characterized by fibroblast proliferation with an infiltrative character. Although these tumors are not intrinsically malignant, they are often classified as such because of their infiltrative character and high risk of recurrence after surgical resection. Desmoid tumors are predominantly seen in young patients with a female-to-male ratio of 2:1 [20]. An underlying genetic mutation of the adenomatous polyposis of the colon (APC) gene is found in patients with Gardner’s syndrome or familial adenomatous polyposis (FAP). The intrathoracic location is the second most frequent location in addition to the primary intra-abdominal location. In 15% of cases, there is multiplicity of the disease [21]. Most patients are asymptomatic, often with a large sized lesion as a coincidental finding on chest radiographs. On CT, which is the preferred imaging modality, lesions tend to present as well-defined, homogeneous solitary pleural masses that are isodense to muscle (Fig. 6). There are no intralesional hemorrhagic or necrotic foci. MRI shows a signal intensity iso-intense to muscle on T1-WI, whereas on T2 the signal varies depending on the characteristics of the lesion. A high T2-SI is seen in lesions with a high cellularity or myxoid component, whereas low SI is found if lesions predominantly contain collagen. Contrast enhancement is variable in both CT and MRI imaging [22,23,24].
Pleural sarcomas
Pleural sarcomas are most frequently encountered in the context of metastases and rarely as primary pleural sarcomas.
Synovial sarcomas are observed in patients with a wide age range and are mainly found as soft tissue sarcomas of the extremities. Primary pleural presentations are rare. On imaging studies, they manifest as a well-defined heterogeneous mass with intralesional necrosis or hemorrhage (Fig. 7), and lesions may vary in size. After contrast administration, a heterogeneous enhancement is observed. Associated pleural effusion and cortical bone destruction may also occur. Findings on 18-F-FDG PET are aspecific since FDG uptake may be variable [25]. The morphological features of primary and metastatic synovial sarcomas are similar and not differentiable on imaging.
Angiosarcomas are predominantly observed in adult males. They range from low-grade epithelioid hemangioendotheliomas (EHEs) to high-grade angiosarcomas and are typically very aggressive, especially in the high-grade form. EHE is a rare vascular tumor that may present at different sites in the body. Only 200 cases of pulmonary EHE have been reported worldwide, and only 27 have been classified as pleural in origin [26]. Patients are typically male and symptomatic at presentation. Chest pain, dyspnea, and cough are aspecific symptoms, but if persistent, they should be included in the differential diagnosis. Chest imaging shows pleural thickening with a unilateral pleural effusion [27]. This unilateral effusion should raise suspicion if it does not respond to therapy. An angiosarcoma may mimic a mesothelioma on imaging with diffuse pleural thickening (up to 40%) and pleural effusion (up to 70%) (Fig. 8) [28, 29]. Owing to its aggressive course, the prognosis is very poor.
Desmoplastic small round cell tumor
The etiology of desmoplastic small round cell tumor (DSRCT), a rare tumor, is believed to be a genetic alteration of two different tumors (Wilms tumor and Ewing’s tumor). This may explain the young age of the affected population. The clinical presentation is aspecific. DSRCT can present as a single lesion or as diffuse pleural involvement with pleural effusion. This diversity of presentation patterns can be attributed to the dual genetic alterations. Locoregional bone invasion has been described as an associated finding. Imaging findings are aspecific and impose a diagnostic challenge. In general, surgical biopsy is needed for the definite diagnosis of DSRCT [30, 31].
Juxtapleural malignancies
Juxtapleural tumors are closely related to the pleura and chest wall and may originate from osseous structures, cartilage, soft tissue, muscles, nerves, or fat. Although imaging findings may overlap or be aspecific, some tumors may present with a particular imaging feature or specific clinical setting.
Chondrosarcoma and osteosarcoma
Chondrosarcoma is the most common primary tumor of the chest wall and is most commonly seen in elderly patients. Chondrosarcomas are mainly located anteriorly in the chest wall and in the upper five ribs (Fig. 9). Chondrosarcomas produce chondroid matrices, and CT shows the typical imaging features, such as arc-and-ring sign or flocculence appearance (Fig. 10).
Osteosarcomas are primarily found in long bones; chest wall location is rare and is mainly observed in an elderly population. Osteosarcomas contain new neoplastic bone and/or disorganized ossification. Imaging characteristically reveals a heterogeneous mass with associated bone destruction (Fig. 11). Heterogeneity in imaging studies is due to intralesional necrosis, hemorrhage, and ossification. The pathognomonic sunburst sign is less evident in flat bones, thus hampering diagnosis [32].
Extraskeletal Ewing sarcoma
The second most common primary malignant bone tumor in children and adolescents is the Ewing sarcoma, with a slight male predilection (male-to-female ratio of 1.5:1). The primary complaint of patients is pain, which depends on the location, the feeling of a mass, or swelling. Ewing sarcoma can occur in extraskeletal sites in the chest, such as pleural and paravertebral sites. Most lesions have an aggressive appearance with locoregional bone destruction and a large soft-tissue component (Figs. 12, 13) [33].
Leiomyosarcoma
A leiomyosarcoma arises from the smooth muscles and can be located adjacent to the bronchus, pulmonary artery, or peripheral pulmonary parenchyma. Depending on the site, it may evoke dyspnea, chest pain, or hemoptysis. Imaging shows a well-defined smooth or lobular mass with a homogeneous or necrotic aspect (Fig. 14) [32].
Neurogenic tumors
Neurogenic tumors with juxtapleural locations may arise from spinal nerve roots or intercostal nerves (Fig. 15). Benign neurogenic tumors, such as schwannomas and neurofibromas, are commonly diagnosed in younger patients (20–50 years old). Both show iso- to hypointense signal intensity on T1-WI. T2-weighted imaging is more distinctive with a fascicular sign (hypointense foci within the T2 hyperintense area) suggestive of a schwannoma, and a pathognomonic target sign (central hypointense and peripheral hyperintense SI) often seen in cases of neurofibromas. Benign schwannomas may show high uptake on PET, mimicking a malignancy. Malignant peripheral nerve sheath tumors (MPNSTs) are not as common and comprise 5–10% of all soft tissue sarcomas. More than 50% of the cases are associated with neurofibromatosis type 1. Lesions tend to be large (> 5 cm) with ill-defined margins and rapid interval growth on imaging studies. Size is the major discriminant between benign and malignant lesions; the larger the lesion, the more likely it is to be malignant. On MRI, they manifest with an iso- to hyperintense SI on T1-WI and a heterogeneously hyperintense SI on T2-WI due to intralesional necrosis and hemorrhage (Fig. 16) [25, 32, 34]. On 18F-FDG-PET, benign schwannomas may show an elevated FDG uptake [35].
Liposarcomas
Liposarcomas are the malignant counterparts of the frequently found lipomas. Depending on the size, patients may present with thoracic complaints and discomfort. As these lesions grow slowly, patients mostly remain asymptomatic for a long period. [36] The diagnosis is often made on CT with typically a fat-containing lesion with negative Hounsfield units, often inhomogeneous and poorly distinctive from the surrounding structures. Intralesional calcifications may also be observed. On MR imaging, the fatty components have a signal intensity similar to fat on all pulse sequences with intralesional thick septa (> 2 mm) and contrast enhancement [32].
Mimickers
A number of infectious diseases may present as tumors or tumorlike pleural or juxtapleural diseases, mimicking a malignancy, for example, a chest wall cold abscess caused by tuberculosis. This is a rare entity, often simulating a pleural tumor when seen in the chest wall region. Patients may present with thoracic pain, but the pathognomonic clinical symptoms of tuberculosis, such as fever, weight loss, or night sweats, are not always present. Imaging shows a well-defined lobular mass against the pleura (Fig. 17), usually a solitary lesion. The mass may involve the ribs, vertebrae, costochondral junction, or sternum. In most cases, a biopsy is required to confirm the diagnosis [37]. Osteomyelitis (Fig. 18) is another infectious pathology that may mimic a pleural/juxtapleural malignancy. It is mainly seen in young children (< 5 years) and adults (bimodal age distribution). The clinical symptoms are aspecific and include pain, erythema, and edema of the affected body part. Standard radiography is a baseline examination for follow-up and differential diagnosis. MRI is the preferred modality for early detection, whereas CT may be useful in the evaluation of chronic osteomyelitis, particularly in areas with complex anatomy [38]. Tumorlike conditions of the pleura can be focal, but in general, they tend to be multifocal. Conditions such as pleural plaque, thoracic splenosis, thoracic endometriosis, Erdheim-Chester disease, pleural sarcoidosis (Fig. 19), and extramedullary hematopoiesis (Fig. 20) may mimic primary pleural malignancies. Extramedullary hematopoiesis must be in the differential diagnosis when sharply delineated paraspinal masses with a homogeneous signal intensity following bone marrow are encountered on MRI in a patient with a myeloproliferative disorder or hemoglobinopathy [39]. Interpretation of imaging findings in the clinical context is of utmost importance for a correct diagnosis.
Conclusion
Pleural lesions are a diagnostic challenge for radiologists. Patient characteristics, such as age, immune status, hypoglycemia, and previous medical history, can guide the radiologist to the correct diagnosis. Although lesions can be initially detected on chest radiographs, CT and MRI are the imaging modalities of choice for further characterization. Imaging findings can be relatively specific in a number of cases, such as in SFT (presenting as a large well-defined and local non-aggressive mass), osteosarcoma (an aggressive lesion closely related to bone), or chondrosarcoma (location and chondroid matrix). In general, imaging findings are rather aspecific. Evolution is an important clue for the diagnosis. Additional extrathoracic imaging findings such as lymphadenopathies, organomegaly, and polyposis of the colon are important for accurate diagnosis. Discussion on a multidisciplinary thoracic oncology tumor board is vital for different steps in the diagnostic process, from detection on imaging studies to guiding the diagnostic approach (e.g., tissue prelevation), histopathologic diagnosis, and defining the treatment strategy.
Abbreviations
- 18F-FDG PET:
-
18F-Fluorodeoxyglucose positron emission tomography
- APC:
-
Adenomatous polyposis of the colon
- CR:
-
Conventional radiography
- CT:
-
Computed tomography
- DLBCL:
-
Diffuse large B-cell lymphoma
- DSRCT:
-
Desmoplastic small round cell tumor
- DWI:
-
Diffusion-weighted imaging
- EBV:
-
Epstein-Barr virus
- EHE:
-
Epithelioid hemangioendothelioma
- FAP:
-
Familial adenomatous polyposis
- IGF:
-
Insulin growth factor
- MRI:
-
Magnetic resonance imaging
- PAL:
-
Pyothorax-associated lymphoma
- PEL:
-
Primary effusion lymphoma
- SFT:
-
Solitary fibrous tumors
- SI:
-
Signal intensity
- SUV:
-
Standardized uptake value
- WI:
-
Weighted images
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Desimpel, J., Vanhoenacker, F.M., Carp, L. et al. Tumor and tumorlike conditions of the pleura and juxtapleural region: review of imaging findings. Insights Imaging 12, 97 (2021). https://doi.org/10.1186/s13244-021-01038-x
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DOI: https://doi.org/10.1186/s13244-021-01038-x