Benign localized fibrous tumour of the pleura: CT features with histopathological correlations

Benign localized fibrous tumour of the pleura: CT features with histopathological correlations

Clinical Radiology (2006) 61, 875e882 Benign localized fibrous tumour of the pleura: CT features with histopathological correlations S. Chonga, T.S. ...

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Clinical Radiology (2006) 61, 875e882

Benign localized fibrous tumour of the pleura: CT features with histopathological correlations S. Chonga, T.S. Kima,*, E.Y. Chob, J. Kimc, H. Kimd Departments of aRadiology, bPathology, cThoracic Surgery, and dPulmonary and Critical Care Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea Received 21 December 2005; received in revised form 13 June 2006; accepted 14 June 2006

AIM: To assess the CT features of benign localized fibrous tumour of the pleura, with histopathological correlations. MATERIALS AND METHODS: CT and histopathological findings of 18 patients with surgically resected benign localized fibrous tumour of the pleura were retrospectively assessed. RESULTS: Tumours were pleura or fissure based, semilunar, lentiform or oval in shape, classified according to their homogeneous, slightly heterogeneous or heterogeneous enhancement pattern. Of the 18 tumours, 5 (28%) demonstrated 55 HU increment or higher attenuation than muscles on contrast-enhanced CT, and histopathologically showed a haemangiopericytoma-like pattern with rich vascularity. CONCLUSION: CT analysis of the shape of a mass and the enhancement pattern can be helpful in the diagnosis of benign localized fibrous tumour of the pleura. ª 2006 Published by Elsevier Ltd on behalf of The Royal College of Radiologists.

Introduction

Materials and methods

Localized fibrous tumours of the pleura (LFTPs) are rare primary pleural neoplasms derived from mesenchymal cells in the submesothelial lining of the pleural space.1 On CT these tumours usually manifest as a well-defined, variably-sized, homogeneous or heterogeneous mass abutting a pleural surface adjacent to the chest wall, or sometimes within an interlobar fissure.2e7 Benign and malignant subtypes of LFTP are recognized, and approximately 7% to 13% of tumours are malignant at histological examination.1,8,9 We retrospectively assessed CT features with histopathological correlations in 18 patients who had had surgically resected benign LFTPs, to discover any specific CT findings that might help in the diagnosis of these tumours.

Between January 1997 and March 2005, 18 consecutive patients (10 men and 8 women, age range 25 to 83 years, mean age 53 years), with surgically resected benign LFTP, were enrolled in this study from the file archives of the department of pathology at our institution. Approval from the institutional review board was not needed for review of pathological reports and radiological images. We retrospectively assessed the CT and histopathological findings. Unenhanced and contrast-enhanced helical chest CT images were obtained from all patients, using a helical CT machine (HiSpeed Advantage, General Electric Medical Systems, Milwaukee, WI). The parameters of helical chest CT were 140 kVp, 170 mAs, 5-mm collimation and a 10 mm/s table feed with a 1-s rotation time. Unenhanced highresolution images were obtained using 1-mm collimation at 10-mm intervals with bone algorithm reconstruction. Contrast-enhanced chest CT images were obtained after injection of 30 g of iodinated contrast medium (100 ml Iopamidol at 3 ml/s) with a power injector (OP 100, Medrad, Pittsburgh, PA). Data were displayed directly on four monitors

* Guarantor and correspondent: T.S. Kim, Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Gangnam-gu, Seoul 135710, Korea. Tel.: þ82 2 3410 2518; fax: þ82 2 3410 2559. E-mail address: [email protected] (T.S. Kim).

0009-9260/$ - see front matter ª 2006 Published by Elsevier Ltd on behalf of The Royal College of Radiologists. doi:10.1016/j.crad.2006.06.008

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(with 1,536  2,048 image matrices, 8-bit viewable grey scale and 60-ft Lambert luminescence) of a picture archiving and communication system (Pathspeed, General Electric Medical Systems Integrated Imaging Solutions, Mt. Prospect, IL). Chest CT images were analyzed retrospectively and jointly by two thoracic radiologists (T.S.K. and S.C., with 8 and 3 years of experience in thoracic radiology, respectively). The decisions on the CT findings were reached by consensus. Images were assessed specifically for the location, size and shape (ovoid, semilunar or lentiform) of the tumour, the angle (obtuse or acute) formed between the tumour and the adjacent parietal pleura or interlobar fissure, and the pattern and degree of contrast enhancement. We classified the location of pleural lesions into upper, middle or lower third of the hemithorax according to horizontal lines drawn at the levels of the tracheal carina and the inferior pulmonary vein draining into the left atrium. The tumours were classified as originating from the mediastinal or costal pleura or a fissure, according to surgical reports. The degree of contrast enhancement was measured in 13 cases using a net enhancement between pre- and post-contrast images at the same level. In the remaining five cases, we could not measure the value of net enhancement because their CT had been performed at different institutions, and thus only the hard copy of CT images was available at the time of review. In these cases,

Table 1

the degree of contrast enhancement of the tumour was assessed as higher or similar attenuation when compared with that of the adjacent chest wall muscle. The pattern of contrast enhancement was classified into three groups according to the heterogeneity of attenuation on CT as homogeneous, slightly heterogeneous or heterogeneous. We assessed the relationship between tumour size and tumourepleura or tumourefissure angle by statistical analysis using the ManneWhitney test. We also assessed the difference (Kruskale Wallis test) and tendency (the least significance difference test) of tumour size between homogeneous, slightly heterogeneous and heterogeneous groups. In all, 12 patients underwent wedge resection by video-assisted thoracoscopic surgery and 6 underwent mass excision by open thoracotomy, for either pleural or fissural lesions. The specimens obtained were histopathologically confirmed to be benign LFTP. The pattern of histopathological findings was retrospectively assessed by a pathologist with 5 years’ experience in pulmonary pathology (E.Y.C.).

Results CT findings of benign LFTP in 18 cases, with histopathological correlations, are summarized in Table 1. The tumours were in the right (n ¼ 12) or

CT findings of benign localized fibrous tumour of the pleura in 18 cases

Case

Age/sexa

Laterality

Origin

Locationb

Size (cm)

Shape

Anglec

Enhancement

HU

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

M/69 M/25 F/51 F/52 F/50 M/40 F/56 F/25 M/83 M/63 M/63 M/53 F/60 M/54 F/52 F/54 M/52 M/44

Left Right Left Right Right Right Right Right Left Right Right Left Right Right Right Left Right Left

Pleural Pleural Pleural Pleural Pleural Pleural Pleural Pleural Pleural Pleural Pleural Fissural Fissural Fissural Fissural Fissural Fissural Fissural

Lower Lower Lower Upper Lower Lower Lower Lower Lower Lower Lower Middle Lower Upper Lower Lower Middle Lower

1.3  1.1 2.3  1.3 2.3  1.5 3.5  2.3 3.5  2.3 4.4  3.4 4.7  3.1 4.7  3.9 14.4  9.1 16.4  15.8 17.6  13.4 2.3  2.2 2.6  1.8 2.9  2.0 3.3  2.6 4.9  3.7 7.5  3.4 11.0  7.8

Oval Semilunar Semilunar Semilunar Oval Oval Oval Oval Oval Oval Oval Lentiform Lentiform Lentiform Semilunar Lentiform Semilunar Oval

Acute Obtuse Obtuse Obtuse Acute Acute Acute Acute Acute Acute Acute Obtuse Obtuse Obtuse Obtuse Obtuse Obtuse Acute

Homogeneous Homogeneous Homogeneous Homogeneous Slightly heterogeneous Slightly heterogeneous Slightly heterogeneous Heterogeneous Heterogeneous Heterogeneous Heterogeneous Homogeneous Homogeneous Homogeneous Slightly heterogeneous Slightly heterogeneous Slightly heterogeneous Heterogeneous

40 58d 22 40 63d 20 Iso 55d Higher Iso 26 25 Iso 38 10 17 9 Higher

M, male; F, female Iso, iso-attenuation to the chest wall musculature; Higher, higher attenuation than the chest wall musculature. a Years. b Hemithorax. c Tumour-pleura/fissure angle. d Higher attenuation than the chest wall musculature.

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left (n ¼ 6) hemithorax and in the upper (n ¼ 2), middle (n ¼ 2) or lower (n ¼ 14) third. Of the 18 lesions, 9 were oval, 5 semilunar and 4 lentiform in shape; 9 showed acute and 9 showed obtuse tumourepleura or tumourefissure angles (Figs. 1e5). The longest diameter of tumours ranged from 1.3 to 17.6 cm (mean 6.1 þ 5.2 cm). A small-sized, ipsilateral pleural effusion was seen in only one case (5.6%) (Fig. 3). We assessed the degree of contrast enhancement in 13 cases, which showed 9 to 63 HU (mean 32.5  18.0 HU) of net enhancement. For five patients the measurement of CT attenuation numbers was not possible, but the degree of contrast enhancement of the tumour was estimated as higher in two and similar in three when compared with that of the adjacent chest wall muscle.

Figure 2 A 50-year-old woman with benign localized fibrous tumour of the pleura originating from the costal pleural space (case 5). (a) Contrast-enhanced chest CT shows a 3.5  2.3-cm, ovoid, pleura-based mass with acute tumourepleura angles (arrows) in the right lower hemithorax, demonstrating a slightly heterogeneous enhancement pattern with 63 HU of net enhancement. (b) Photomicrograph of a gross specimen obtained from video-assisted thoracoscopic surgery reveals a welldefined tumour consisting of a hypocellular area (black star) and a hypercellular area with a haemangiopericytoma-like pattern (white star) (haematoxylin and eosin, 1). Figure 1 A 51-year-old woman with benign localized fibrous tumour of the pleura originating from the costal pleural space (case 3). Contrast-enhanced chest CT shows a 2.3  1.5-cm, semilunar, pleura-based nodule with obtuse tumourepleura angles (arrows) in the left lower hemithorax, demonstrating a homogeneous enhancement pattern.

According to surgical reports, 11 tumours originated from the pleural space, (9 from the costal pleura and 2 from the mediastinal pleura) and 7 from the fissural space. Pleural tumours were

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As for the tumourepleura or tumourefissure angle, tumours with acute angles (n ¼ 9, mean 8.7 cm) were much larger than those with obtuse angles (n ¼ 9, mean 3.5 cm) (p ¼ 0.0463, ManneWhitney test). The pattern of contrast enhancement was homogeneous (n ¼ 7, mean 2.5 cm), slightly heterogeneous (n ¼ 6, mean 4.7 cm) or heterogeneous (n ¼ 5, mean 12.8 cm) on contrast-enhanced CT. The heterogeneous enhancement pattern of a mass was characterized by central low-attenuation areas surrounded by areas of homogeneous enhancement. A lobular pattern of strong enhancement was seen in three of five cases in the heterogeneous enhancement group (Fig. 5). There was a statistically significant difference in size of tumour between these three groups of enhancement patterns (p ¼ 0.0011, KruskaleWallis test), and also a statistically significant tendency for a larger tumour to produce a more heterogeneous enhancement pattern (the least significance difference test). The seven fissural tumours showed smooth fissural tails and a sharp interface with adjacent lung parenchyma on lung window images of highresolution CT (1-mm collimation) (Fig. 4); six formed obtuse tumourefissure angles, whereas the remaining largest tumour, 11 cm in diameter, demonstrated an acute angle (Fig. 5). Of the 18 tumours, 3 showed 55 HU increment and 2 higher attenuation than that of chest wall muscles on contrast-enhanced CT; all revealed a haemangiopericytoma-like pattern with rich vascularity on histopathological examination. Intratumoural low-attenuation areas seen on contrastenhanced CT corresponded to hypovascular areas of dense fibrosis or loose myxoid stroma (Figs. 2 and 5). Figure 3 A 63-year-old man with benign localized fibrous tumour of the pleura originating from the costal pleural space (case 11). (a) Contrast-enhanced chest CT shows a 17.6  13.4-cm, ovoid, pleura-based mass with acute tumourepleura angles (arrows) in the right lower hemithorax, demonstrating a heterogeneous enhancement pattern. Note a small-sized, ipsilateral pleural effusion. (b) Photomicrograph of histopathological specimen obtained from video-assisted thoracoscopic surgery shows a hypocellular area of dense collagenous tissue (black star) and a hypercellular area of spindle-cell proliferations (white star) (haematoxylin and eosin, 40).

either semilunar (n ¼ 3, mean diameter 2.7 cm) or oval (n ¼ 8, mean 8.4 cm) in shape, whereas fissural tumours were lentiform (n ¼ 4, mean 3.5 cm), semilunar (n ¼ 2, mean 5.4 cm) or oval (n ¼ 1, 11.0 cm).

Discussion Since the pathological characteristics of primary pleural tumours were first described by Klemperer and Rabin in 1931,10 LFTP has been variously named localized mesothelioma, localized fibrous tumour, fibrous mesothelioma or pleural fibroma.11 However, further studies by electron microscopy and immunohistochemistry have shown that the tumour does not originate from the mesothelial layer but from the submesothelial, non-committed mesenchymal layer.12,13 Thus, these tumours are now designated solitary or localized fibrous tumours of the pleura (LFTP). Histopathologically, LFTPs have been classified according to three patterns: the patternless pattern of Stout (fibroblast-like cells and

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Figure 4 A 52-year-old man with benign localized fibrous tumour of the pleura originating from the interlobar fissural space (case 17). (a) Contrast-enhanced chest CT shows a 7.5  3.4-cm, semilunar mass in the right middle hemithorax, demonstrating a slightly heterogeneous enhancement pattern. (b) High-resolution (1-mm collimation) lung window image obtained at the same level as (a) reveals a fissure-based mass with smooth fissural tails and obtuse tumourefissure angles (arrows).

connective tissue in varying proportions arranged in a disorderly or random pattern); a haemangiopericytoma-like pattern (closely packed tumour cells with amphophilic cytoplasm arranged around open or collapsed, branching capillaries and larger vessels); or a leiomyoma-like pattern.14 On CT, LFTP has been known to manifest as a well-defined, homogeneous or heterogeneous mass usually adjacent to the chest wall, or within a fissure, sometimes mimicking a solitary pulmonary nodule.2e7 Classically, an obtuse angle between a mass and the chest wall had been regarded as having a pleural location.15 The differential diagnoses of primary pleural tumours are relatively limited, consisting of LFTP (the most common), malignant mesothelioma and, rarely, synovial sarcoma and epithelioid haemangioendothelioma.16

As for the relationship of tumour size to shape and angle, tumours with obtuse angles (n ¼ 9, mean 3.5 cm) were much smaller than those with acute angles (n ¼ 9, mean 8.7 cm) in our series. Pleural tumours of semilunar shape (n ¼ 3, mean diameter 2.7 cm) were mostly smaller than those of oval shape (n ¼ 8, mean 8.4 cm). Therefore, we suggest that the tumourepleura or tumoure fissure angle tends to change from obtuse to acute as a semilunar LFTP gradually increases in size, showing polypoid growth from the pleural surface and finally become ovoid in shape. As for the heterogeneous pattern on contrastenhanced CT, areas of low attenuation have been known to correspond histopathologically with haemorrhage, necrosis, cystic degeneration and myxoid change.5e7 In our cases, intra-tumoural

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Figure 5 A 44-year-old man with benign localized fibrous tumour of the pleura originating from the interlobar fissural space (case 18). (a) On contrast-enhanced CT, the mass shows a heterogeneous enhancement pattern, demonstrating a lobular pattern of strong enhancement. (b) Lung window image obtained at a higher level than (a) reveals a fissure-originating mass with smooth fissural tails and an acute tumourefissure angle (arrow). (c) Photomicrograph of histopathological specimen obtained from video-assisted thoracoscopic surgery shows a hypocellular area of collagenous tissue with sparse vascularity (black star) and a hypercellular area of spindle-cell proliferations with a haemangiopericytoma-like pattern (white star) (haematoxylin and eosin, 40). (d) High-power photomicrograph of the hypercellular area in (c) shows a haemangiopericytoma-like pattern containing numerous, open, irregularly branching and anastomosing capillaries and larger vessels (arrows) (haematoxylin and eosin, 200).

Benign localized fibrous tumour of the pleura

low-attenuation areas seen at contrast-enhanced CT corresponded to hypocellular areas of dense fibrosis or loose myxoid stroma with sparse vascularity. Irrespective of the enhancement pattern, 5 (28%) of the 18 cases showed portions of strong enhancement, 3 demonstrating 55 HU increment and 2 producing higher attenuation than adjacent chest wall muscles. Histopathologically, these cases proved to be benign LFTPs exhibiting haemangiopericytoma-like patterns. We think that the rich vascularity of such patterns contributed to strong enhancement of the tumour on contrastenhanced CT. In the present study, small pleura-based LFTPs (3.5 cm) could be easily diagnosed by their semilunar shape with smoothly tapering margins, the chest wall forming an obtuse tumourepleura angle which suggested a pleural origin.3 Medium-sized, pleura-based masses (3.5 to 4.7 cm in our series) were ovoid in shape, with acute angles to the pleura. It was relatively difficult to suggest a pleura-originated LFTP in these cases, which mimicked a subpleural pulmonary mass including a possibility of peripheral lung cancer. In our cases of large LFTP (10 cm), heterogeneous enhancement of a large pleura-based tumour, sometimes associated with a strong lobular enhancement pattern, was the characteristic CT finding. In a study of CT findings of localized fibrous pleural mesothelioma, Mendelson et al.5 reported that the heterogeneous enhancement pattern of the mass was characterized by central areas of decreased attenuation surrounded by a region of homogeneous enhancement. A similar enhancement pattern was noted in large LFTPs in our series, and we also confirmed statistically the probability that a larger tumour would show more heterogeneous enhancement (the least significance difference test). According to the present study, a CT finding of a large, pleural-based mass showing heterogeneous, strong lobular enhancement can suggest an LFTP with a haemangiopericytoma-like pattern containing numerous vessels. On the other hand, fissural LFTPs sometimes can be misinterpreted as a pulmonary mass, because of the surrounding lung parenchyma. However, Spizarny et al.4 reported that visualization of the fissures as linear structures at high-resolution CT (1.5- to 3-mm collimation) made it possible to clarify the relationship between a tumour and a fissure. Likewise, CT findings of fissural tails with obtuse tumourefissure angles and a lentiform shape of tumour could correctly indicate a fissure-originated LFTP. There are some limitations to our study. The first is that the degree of contrast enhancement

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was not measured in all 18 cases by net enhancement between pre- and post-contrast images. In five cases, we could not measure net enhancement because their CT had been performed at different institutions, and thus only the hard copy of CT images was available at the time of review. In these cases, the degree of contrast enhancement of the tumour was assessed as higher or similar when compared with that of adjacent chest wall muscle. Secondly, we did not calculate a cut-off value of CT attenuation to differentiate the haemangiopericytoma-like subtype from the others. This subjective assessment of CT attenuation and the cut-off value may disallow a significant correlation between CT attenuation and histological subtype.

Conclusion In summary, we suggest that the tumourepleura angle of an LFTP changes from obtuse to acute as a semilunar nodule gradually increases in size to become ovoid in shape. We also proved statistically a probabilityy that a larger tumour would show more heterogeneous enhancement. According to the present study, small pleura-based LFTPs (3.5 cm) are readily suggested by their semilunar shape with obtuse tumourepleura angles. However, medium-sized, pleura-based masses (3.5 to 4.7 cm in our series) were ovoid in shape with acute angles, and might mimic a sub-pleural pulmonary mass. In the case of large LFTPs (10 cm), the characteristic CT finding of a large, pleura-based mass showing heterogeneous, strong lobular enhancement could suggest an LFTP with a haemangiopericytoma-like pattern containing numerous vessels. In the case of fissure-based tumours, CT findings of smooth fissural tails with obtuse angles and a lentiform shape of tumour can lead to a correct suggestion of LFTP. Thus, CT analysis of the shape of a mass, tumourepleura angle and pattern of contrast enhancement can be helpful in the diagnosis of benign LFTP.

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3. Dedrick CG, McLoud TC, Shepard JA, et al. Computed tomography of localized pleural mesothelioma. AJR Am J Roentgenol 1985;144:275e80. 4. Spizarny DL, Gross BH, Shepard JA. CT findings in localized fibrous mesothelioma of the pleural fissure. J Comput Assist Tomogr 1986;10:942e4. 5. Mendelson DS, Meary E, Buy JN, et al. Localized fibrous pleural mesothelioma: CT findings. Clin Imaging 1991;15: 105e8. 6. Lee KS, Im JG, Choe KO, et al. CT findings in benign fibrous mesothelioma of the pleura: pathologic correlation in nine patients. AJR Am J Roentgenol 1992;158:983e6. 7. Ferretti GR, Chiles C, Choplin RH, et al. Localized benign fibrous tumors of the pleura. AJR Am J Roentgenol 1997; 169:683e6. 8. Okike N, Bernatz PE, Woolner LB. Localized mesothelioma of the pleura: benign and malignant variants. J Thorac Cardiovasc Surg 1978;75:363e72. 9. Cardillo G, Facciolo F, Cavazzana AO, et al. Localized (solitary) fibrous tumors of the pleura: an analysis of 55 patients. Ann Thorac Surg 2000;70:1808e12.

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10. Klemperer P, Rabin LB. Primary neoplasms of the pleura: a report of five cases. Arch Pathol 1931;11:385e412. 11. de Perrot M, Fischer S, Brundler MA, et al. Solitary fibrous tumors of the pleura. Ann Thorac Surg 2002;74:285e93. 12. Hernandez FJ, Fernandez BB. Localized fibrous tumors of pleura: a light and electron microscopic study. Cancer 1974;34:1667e74. 13. Al-Izzi M, Thurlow NP, Corrin B. Pleural mesothelioma of connective tissue type, localized fibrous tumour of the pleura, and reactive submesothelial hyperplasia. An immunohistochemical comparison. J Pathol 1989;158:41e4. 14. England DM, Hochholzer L, McCarthy MJ. Localized benign and malignant fibrous tumors of the pleura. A clinicopathologic review of 223 cases. Am J Surg Pathol 1989;13: 640e58. 15. Pare JAP, Fraser RG. Synopsis of diseases of the chest. Philadelphia, PA: Saunders; 1983. p. 687. 16. Travis WD, Brambilla E, Muller-Hermelink HK, et al. Tumours of the pleura. WHO classification of tumours: pathology and genetics of tumours of the lung, pleura, thymus and heart. Lyon: IARC Press; 2004. p. 125e44.