Imaging diagnosis analysis and literature review of intrapulmonary solitary fibrous tumor

Introduction

Solitary fibrous tumor (SFT) is a rare mesenchymal neoplasm, features hyperplasia of spindle cells and small staghorn-like branching blood vessels, and accounts for less than 2% of all soft tissue tumors. It is presently defined by the existence of NAB2-STAT6 fusion. Most cases are low risk, but approximately 10–30% of SFTs demonstrate features of aggressive behavior, such as localized invasion, recurrence, and distant metastasis (1-6). The 2013 World Health Organization (WHO) classification integrates the former denomination of hemangiopericytoma under the SFT nomenclature; the later 2020 WHO classification avoids the terms typical or malignant, as typical SFT is not necessarily synonymous with benign disease (7,8). Thus far, SFTs have been reported in numerous sites, including peritoneum, parotid gland, paranasal sinuses, orbit, skin, and intracranial areas, a fact which supports a mesenchymal rather than a mesothelial origin. Intrapulmonary SFT is quite rare and mostly limited to a few case reports (9). Intrapulmonary SFT, which is seen on imaging as an intrapulmonary lesion with no correlation to the pleura, is histopathology consistent with the pathological diagnosis of SFT, and the pathological findings do not indicate a primary SFT of the lung. Therefore, SFT originating from the pleura cannot be completely excluded. Computed tomography (CT) is presently the first choice for the clinical examination of SFT. The main treatment is resection through radical surgery, which provides patients with relatively good prognosis. This disease lacks clinical specificity and is therefore commonly misdiagnosed. The information of 4 intrapulmonary SFT cases confirmed by operation and pathology in our hospital (The First Medical Center of Chinese PLA General Hospital) and 61 intrapulmonary SFT cases identified by a Chinese- and English-language literature search of the PubMed database were selected for review. We analyzed and summarized the data of these cases in order to provide a helpful reference for doctors to improve their understanding of the disease and its preoperative diagnosis.

Methods

Clinical data

This study retrospectively analyzed information from 65 patients diagnosed with intrapulmonary SFT, with 4 of these cases being confirmed by operation and pathology at our hospital (Table 1) and 61 being identified via a search of the Chinese- and English-language literature of the PubMed database. The group of 65 patients consisted of 30 female and 35 male patients, with a mean age of 58 years (range, 7–83 years) (refer to Table 2 for information on clinical manifestations). The 4 cases were diagnosed before surgery as benign nodules in 2 cases, neurogenic tumor in 1 case, and lung cancer in 1 case. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the ethics committee of The First Medical Center of Chinese PLA General Hospital. Individual consent for this retrospective analysis was waived.

Metastatic risk assessment

Metastatic risk scores were calculated using a 4-variable model reported by Demicco et al. in 2017 (1). Patient age was scored as 0 if <55 years and 1 if ≥55 years; tumor size was scored as 0 if <5 cm, 1 if 5 to <10 cm, 2 if 10 to <15 cm, and 3 if ≥15 cm; mitotic activity was scored as 0 if <1 mitotic figure/10 high-power field (HPF), 1 if 1–3 mitotic figures/10 HPF, or 2 if ≥4/10 HPF; and tumor necrosis was scored 0 if <10% and 1 if ≥10%. Total scores were summed, and scores of 0–3 were considered low risk, 4–5 as intermediate risk, and 6–7 as high risk.

Research methods

Three patients received nonenhanced and enhanced 64-slice chest scans preoperatively using a LightSpeed CT (GE HealthCare, Waukesha, USA) and a Brilliance 256 iCT (Philips, Amsterdam, The Netherlands) scanners. Lying in a supine position, the patient was scanned from the apex of the lung to 3 centimeters below the diaphragm, with the whole procedure completed under a breath-hold at the end of inspiration. The scan parameters were as follows: tube voltage, 120 kVp; automatic tube current modulation; and thin layer reconstruction layer thickness, 1.0–1.5 mm. The lung window width and level were 1,600 Hounsfield units (HU) and −600 HU, respectively; the mediastinum window width and level were 400 HU and 40 HU, respectively. The enhanced scan used nonionic contrast medium [70–90 mL of iohexol or iopromide (300 mgI/mL); velocity 3.5 mL/s], and scans for the arterial phase and the venous phase were performed at 25–30 s and 60–65 s, respectively, after injection of the contrast medium.

One patient underwent chest magnetic resonance imaging (MRI) plain and enhanced scanning in a GE HealthCare Signal HDX 3.0T MR scanner with torso coils. Before the procedure, the patient was trained to breathe calmly. The scanning range was from the superior aperture of the thorax to cover the whole diaphragm. The scanning sequences included the following: (I) real time coronal respiratory gating (COR RT) fast spin echo (FSE) T2 [repetition time (TR): 6,000 ms; time to echo (TE): 85 ms]; (II) sagittal single shot FSE (SAG SSFSE; TR: 1,400 ms; TE: 85 ms); (III) axial spoiled gradient echo (AX SPGR) T1 (TR: 200 ms; TE: 2.6 ms); (IV) AX RT IDEAL (Iterative Dixon water-fat separation with Echo Asymmetry and Leastsquares estimation) T2 [TR: 5,000–8,000 ms; TE: 85 ms; echo train length (ETL): 18]; (V) and single-shot AX diffusion-weighted (DW) spin-echo echo planar imaging [SE-EPI; TR: 6,600 ms, TE: 58 ms; fat-suppressed T2-weight imaging (T2WI): TR: 10,000 ms, TE: 74 ms]. Except for the breath-holding scanning of AX SPGR T1, all the other sequences used free breathing and respiratory gating techniques.

Subsequently, dynamic-enhanced scanning was performed in the cross-sectional, sagittal and coronal planes after injection of a gadolinium-diethylenetriamine-pentaacetic acid (Gd-DTPA) contrast agent bolus in a vein of the elbow at a flow rate of 2.0 mL/s.

Results

Imaging findings

Of the 4 patients with intrapulmonary SFT, 3 tumors were located in the right lower lobe and 1 in the left lower lobe. One patient presented with a broad-based tumor growing close to the pleura. In terms of size and the morphology and density of the lesion, 4 patients with SFT showed quasicircular or oval lesions, with the largest lesion being 29 mm × 23 mm in size; 3 cases showed soft tissue shadows of even density but no calcification; 2 cases showed no obvious enhancement in the arterial phase; and 1 case showed geographic enhancement. One case showed a long T1, slightly long T2 signal, and slightly high diffusion-weighted imaging (DWI) signal intensity, without significant signal diminution during the positive and negative phases; dynamic-enhanced scanning revealed uneven continuous enhancement and a fat pad between the tumor and the adjacent pleura. In terms of peripheral changes, 4 cases had lesions with a clear boundary, and 1 case had a tumor growing adjacent to the visceral pleura. In all cases, the tumor did not invade the visceral pleura, and an obvious, normal, and uninvolved lung parenchyma edge was observed to be separating the tumor mass from the surface of the pleura covering it (Figures 1,2).

Figure 1 Images from Cases 1 (A-D: chest CT scan) and 2 (E,F: chest CT scan). Case 1: A 42-year-old female with nodules in right lower lobe identified in physical examination. (A-D) Chest CT nonenhanced and enhanced scans. (A) Lung window: quasicircular nodules, approximately 19 mm in diameter, observed in the posterior basal segment of the right lower lobe. (B) Mediastinum window: nodules of even density, with a CT attenuation value of about 26 HU. (C,D) Enhanced scan: mild enhancement during the arterial phase, with a CT attenuation value of about 37 HU; uneven enhancement during the venous phase, with a CT attenuation value of about 4–133 HU and a blood vessel running along the margin of the lesion. Case 2: A 23-year-old male with nodules in the right lower lobe identified in physical examination. (E,F) Chest CT scans. (E) Lung window: quasicircular nodules, approximately 15 mm in diameter, observed in the dorsal segment of the right lower lobe. (F) Mediastinum window: nodules of even density, and a CT attenuation value about 27 HU. CT, computed tomography; HU, Hounsfield units.

Figure 2 Images from Cases 3 (A-I: chest MRI scan) and 4 (J-L: chest CT scan). Case 3: A 31-year-old male with nodules beside the posterior mediastinum discovered in physical examination. (A-I) Chest MRI nonenhanced and enhanced scans. (A) Axial T2WI: a quasicircular smooth-edged shadow about 29 mm × 17 mm × 23 mm beside the posterior mediastinum of the right lower lobe and long T1 and T2 signals. (B) DWI: hyperintensity. (C,D) No signal diminution in positive or negative phase signals. (E-G) Enhanced scanning: dynamic-enhanced scans showing continuous uneven enhancement. (H) Coronary scan and (I) sagittal scan: lesions distinctly separated from surrounding tissues. Case 4: A 56-year-old male with nodules in left lower lobe identified in physical examination. (J-L) Chest CT nonenhanced and enhanced scans. (J) Lung window: quasicircular nodules, approximately 13 mm in diameter, observed in the posterior basal segment of the left lower lobe. (K) Mediastinum window: nodules of even density, with a CT attenuation value of about 28 HU. (L) Enhanced scan: mild enhancement during the arterial-venous phase, with a blood vessel running along the margin of the lesion. MRI, magnetic resonance imaging; CT, computed tomography; T2WI, T2-weight imaging; DWI, diffusion-weighted imaging; HU, Hounsfield units.

Pathologic results

In the 4 cases from our hospital, the solitary nodules were all located in the lung parenchyma. In 1 case, the nodule was quasicircular, had a distinct border, and showed no obvious cytologic atypia. Images indicated a mitotic rate at 2/10 HPF. The tumor cells were fusiform, and the tumor stroma contained rich collagen and observable staghorn-like blood vessels. No necrosis was found, and the lesion was lobulated focally and accompanied by alveolar epithelial lining. All the features indicated the benignity of the tumor, and when combined with the immunophenotype, pointed to SFT. Immunohistochemical (IHC) staining of the tumor cells indicated the following: vimentin (+), Bcl-2 (+), Ki-67 (+<10%), CD99 (−), CD34 (−), vessel disease (+), and S-100 (−). In the other 3 cases, the lesions were quasicircular or oval, with a clear border but no obvious cytologic atypia. The mitotic rate was 2/10 HPF, substantial stromal collagen accumulation was evident, staghorn-like blood vessels were observable in the stroma, and no necrosis was found. IHC staining results indicated the following: SMA (smooth muscle antigen) (−), S-100 (−), h-caldesmon (partially weak+), CD34 (+), Bcl-2 (+), STAT6 (signal transducer and activator of transcription 6) (nuclear+), Ki-67 (+8%), and cytokeratin (−) (Figure 3). All 4 cases were low risk (see Table 1).

Figure 3 Pathology results. (A) (HE ×100) Spindle cell tumor with a clear border, no obvious cytologic atypia, conspicuous stromal collagen accumulation, staghorn-like blood vessels visible in the stroma, and no necrosis, indicating SFT. IHC test results (×100): (B) STAT6 (nuclear+), (C) CD34 (+), and (D) Bcl-2 (+). HE, hematoxylin and eosin; SFT, solitary fibrous tumor; IHC, immunohistochemical.

Discussion

SFT originates from a rare mesenchymal tumor differentiating from dendritic mesenchymal cells expressing the CD34 antigen. Its incidence rate is 1.4 per million people, with 13–37% of cases being malignant (10). The tumor mainly consists of a large number of spindle cells, which contain abundant mature blood vessels and mature fibrillar collagen (10,11). Spindle cells are widely distributed in the connective tissue of human body, so SFT can occur in any part of the human body, most often in the chest. Typically, SFT first arises in the pleura and can grow along the mediastinal space. However, reports of extrapleural SFTs have gradually increased in number in recent years, with other sites including the peritoneum, kidney, pancreas, thyroid gland, liver, gall bladder, head and face, mediastinum, breast, and the lung (12-17). There have also been sporadic reports of SFT in the lung parenchyma (18-29). According to the literature, intrapulmonary SFT can occur at all ages but tends to affect young adults and older adults, with most malignant cases occurring in those 50 to 70 years of age, with no sex-specific predominance (1,3,4,7,30-33). Generally, the literature indicates that SFT most often occurs in the left lower lobe, without specific clinical manifestations at onset. As the tumor grows gradually in size and compresses surrounding lung tissue and bronchi, patients experience chest tightness, shortness of breath, dyspnea, and other secondary symptoms, as well as paraneoplastic syndromes (PNS), including Doege-Potter syndrome (recurrent hypoglycemia) and Pierre-Marie-Bamberger syndrome (hypertrophic pulmonary osteoarthropathy, long bone periostitis, and arthritis accompanied by clubbed fingers). These syndromes can be relieved after complete resection of the tumor (34-36). For the 4 cases in this study, the tumors were all less than 30 mm in diameter and triggered no symptoms.

As far back as 1942, Stout and Murray described the intrapulmonary location of these tumors, but it seems that in these early descriptions, the tumors originated from the visceral pleura with a “growth pattern” (37). In this study, the imaging findings of 1 case showed that the disease was closely related to the visceral pleura, and the postoperative pathological findings indicated an intrapulmonary origin. Under most circumstances, intrapulmonary SFTs grow slowly, are asymptomatic at onset and during the course of progression, and are often found during routine physical examination. The intrapulmonary origination of SFT might be attributable to (I) the direct continuity between the mesenchyme and subpleural intralobular septa, (II) parenchymal lung fibroblasts, or (III) indentation of visceral pleura. This topic stems from two assumptions (26). First, the direct continuity of the subpleural mesenchyme and interlobular septa or indentation of visceral pleura can cause pulmonary SFT. Second, these tumors originate from the facultative fibroblast elements in the subcutaneous area of the normal pulmonary parenchyma. It was reported that these elements have ultrastructural and IHC characteristics similar to those of subpleural connective tissue (38). All 4 cases in this study occurred in the lungs, were found on routine physical examination, and demonstrated no clinical or radiological characteristics, which hindered preoperative diagnosis. Excisional biopsy and histopathological examination are usually required (39). Fine needle aspiration or bronchoscopic biopsy is often inadequate for providing reliable therapeutic guidance (40).

Imaging findings of intrapulmonary SFT is usually benign and with a low risk of potential tumor (41). Its imaging features include slow growth, clear border, possible lobulation, absence of spicule sign and satellite lesions, uniform density in most cases, and calcification (about 7–26%) and necrosis in a few cases. The presence of calcification has no obvious correlation with low risk or high risk of malignancy in tumors, but may be related to necrosis (42). Alghamdi et al. reported calcification (in 1 case) (36). The 4 cases in this study did not show specific calcification, and since the tumors were small, there was no necrosis. Some cases with lesion located in the posterior thoracic cavity can also have manifestations similar to those of neurogenic tumors, which is why 1 case in this study was diagnosed as neurogenic tumor before operation. Under enhanced scanning, SFT showed enhancement in a variety of ways. Low-risk SFTs are well supplied, mainly by the internal thoracic artery and bronchial artery. High-risk SFTs have an unclear boundary, uneven density, rough edge, and signs of invasion of the surrounding tissue. The possibility of high-risk SFTs should be considered if the mass grows rapidly, is large (>10 cm), and invades adjacent tissue or has distant metastasis. Under enhanced scanning, most of the SFT cases showed moderate-to-severe uneven enhancement, and the enhancement level was about 45–100 HU (43). Wu et al. reported a case of SFT being diagnosed as central lung cancer preoperatively, where the right main bronchus and the middle segmental bronchus were obstructed, with secondary atelectasis of all lobes; the mass showed relatively even density under plain scan but uneven enhancement under scanning with contrast (31). Two cases in this study presented with no obvious enhancement in the arterial phase, and mild enhancement in the delayed phase; in contrast-enhanced scanning, obviously enhanced linear and strip vascular shadows were seen in part of the lesion in on case, and uneven continuous enhancement was seen in the other case. The CT findings of SFT are related to the size of the lesion. A small lesion has even density and clear boundary, with few accompanying signs. A comparatively large lesion has uneven density, an unclear boundary, and many accompanying signs. As the tumor grows bigger, the probability of the sign of pleural effusion also grows. The 4 cases of this study all showed pathological features of benign tumor, and imaging findings indicated no malignant signs.

Pathological findings of intrapulmonary SFT

There is no significant difference in the clinical, histopathological, or IHC features between intrapulmonary SFT and pleural SFT (30). SFT is generally a quasicircular or lobulated solid mass with a complete capsule or fibrous pseudocapsule, having a well-defined border. Observed under a microscope, the tumor tissue is rich in collagenous fibers and spindle tumor cells, which are mixed in different proportions to form dense and sparse areas of cells, with the spindle cells being arranged without a fixed pattern; these are the pathological features of SFT. A large number of collagenous fibers can be seen in the tumor stroma. Some parts demonstrate mucoid or cystic changes, while some parts contain abundant blood vessels, dilated vascular lumens, hyaline degeneration of vascular walls, and focal hemangiopericytoma-like structures. The positive markers on IHC tests mainly include CD34, vimentin, CD99, and Bcl-2. The majority of SFT cases are CD34 positive, which is specific for the diagnosis of SFT. When the expression of CD34 is negative, the positive expression of Bcl-2 can still be used to diagnose SFT (44). In this study, 1 of the 4 patients showed CD34 (−). Negative markers mainly include S-100, CK, Desmin, SMA, and EMA (epithelial membrane antigen). A large number of studies have shown that STAT6 is the most sensitive and specific marker for diagnosing SFT, which is consistent with a study showing a 96% positive rate of STAT6 expression in all SFT cases examined (45). In our study, we found that the positive rate of vimentin among confirmed SFT cases was 100%. Therefore, the above markers can be used in combination to diagnose SFT. In addition, except with respect to the Ki-67 index, low-risk and high-risk SFTs showed no difference in the IHC test results. Therefore, CT scanning, especially the high-resolution multislice mode, is a reliable method for differentiating high-risk and low-risk SFTs. As a general rule, it is suggested that (I) the lesion be completely resected and that (II) all patients be monitored with long-term follow-up (46).

Intrapulmonary SFT is mainly a low-risk tumor, and typical imaging findings are benign. High-risk intrapulmonary SFT is also rare tumor and need not essential to differentiate from intrapulmonary malignant SFTs; instead, it should be differentiated from other intrapulmonary malignant tumors. Intrapulmonary SFT generally needs to be differentiated from the following diseases, among others: benign intrapulmonary tumors, such as pulmonary sclerosing pneumocytoma (PSP), hamartoma, and granulomatous nodules; neurogenic tumors, more often than not found in the posterior mediastinum; intrapulmonary single metastatic tumor; peripheral lung cancer; Castleman disease; and sarcomatoid carcinoma. Without specific imaging findings, intrapulmonary SFT is easily misdiagnosed as another disease, and preoperative diagnosis and differential diagnosis mainly relies on pathological and IHC test results obtained from tumor biopsy via needle puncture and aspiration.

Intrapulmonary SFT is mainly treated by complete surgical resection. Even when the disease is pathologically diagnosed as low risk, SFT still has the potential for malignancy, and the possibility of relapse or deterioration after complete resection cannot be ruled out. Inoue et al. reported a local relapse of SFT 2 years after nonanatomic wedge resection performed on the left upper lobe and emphasized the importance of long-term postoperative follow-up for benign tumors (47). Wu et al. reported metastasis to the diaphragm and abdominal cavity 5 months after operation in 1 high-risk SFT case (31). As for the 4 cases treated by our hospital, 1 case showed no abnormalities in chest CT scans during the 24-month follow-up, while the other 3 cases were not followed up. The study had several limitations related to its retrospective nature and small sample size.

Conclusions

Since intrapulmonary SFT is clinically nonspecific, the discovery of lesions mainly depends on imaging. Multislice CT has high spatial and temporal resolution, which can not only display the small and microstructures of the lesion but can also enable the observation of the periphery and supplying blood vessels of the lesion from various angles via the multiplanar reconstruction technique. Although intrapulmonary SFTs are often low risk, existing data demonstrate that these tumors necessitate the extension of close clinical follow-up (48).

Acknowledgments

Funding: None.

Footnote

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-22-1328/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the ethics committee of The First Medical Center of Chinese PLA General Hospital. Individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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