Eur. Radiol. 9, 55±59 (1999) Ó Springer-Verlag 1999
European Radiology
Pictorial review Radiolucencies and cavitation in bronchioloalveolar carcinoma: CT-pathologic correlation M. Gaeta1, R. Caruso2, A. Blandino3, G. Bartiromo1, E. Scribano3, I. Pandolfo3 1
Service of Diagnostic Imaging, Piemonte Hospital, via Spatafora, I-98124 Messina, Italy Institute of Pathology, University of Messina, I-98100 Messina, Italy 3 Institute of Radiologic Sciences, University of Messina, I-98100 Messina, Italy 2
Received: 31 December 1997; Revision received: 23 March 1998; Accepted: 28 April 1998
Abstract. Bronchioloalveolar carcinoma (BAC) is a polymorphic lung cancer the incidence of which is rising. The presence of intratumoral radiolucencies is an important feature of bronchioloalveolar carcinoma.The aim of this study was to present pictorially the spectrum of intratumoral radiolucencies visible in BAC. In 57 BACs studied with thin-slice CT, we identified six types of radiolucencies: (a) patent intratumoral bronchioles (air bronchiologram); (b) pseudocavitations; (c) cavitation; (d) serpentine radiolucencies; (e) internal alveologram; and (f) multiple cystic lesions. Key words: Lung cancer ± Bronchioloalveolar carcinoma ± Radiolucencies ± Computed tomography
Introduction Bronchioloalveolar carcinoma (BAC) is a well-differentiated adenocarcinoma of the lung which has an extraordinary polymorphism [1±3]. Its growth is characterized by spread of neoplastic cells in the peripheral air space without destroying underlying architecture (lepidic tumor growth) [4]. Recent evidence suggests that BAC has increased dramatically in recent years [5, 6]. Internal radiolucencies are an important feature of BAC [7±9]. Since BAC has to be considered in the radiologic differential diagnosis of a large part of pulmonary disease, accurate knowledge of its CT characteristics is very important. The aim of this paper is to describe the different types of radiolucencies seen with CT in 57 BACs: solitary nodule (n = 29); solitary mass (n = 2); segmental or
Correspondence to: M. Gaeta Present address: co fam. Sciabà, via Sicilia, n. 24, I-98124 Messina, Italy
lobar consolidation (n = 9); and multicentric or diffuse disease (n = 17). Diagnosis was obtained by surgery in 32 cases and by transbronchial or percutaneous biopsy in 25 cases. The following types of radiolucencies have been detected: (a) patent intratumoral bronchioles (air bronchiologram); (b) bubble-like lucencies or pseudocavitations; (c) cavitation; (d) serpentine radiolucencies; (e) internal alveologram; and (f) multiple, thin-walled cystic lesions. Air bronchiologram Lepidic tumor growth accounts for the high frequency of air bronchiolograms in nodular BAC. We found air bronchiolograms in 10 of 29 (34 %) nodular BACs. When air-containing intratumoral bronchioles are cut along their long axis, they appear as linear and branching radiolucencies on thin-section CT (Fig. 1). Frequently, bronchioles are ectatic for desmoplastic reaction (Fig. 2). Kuriyama et al. [10] found patent bronchioles in 14 of 20 adenocarcinomas (70 %) and only in 1 of 20 benign nodules (5 %). This study suggests that the presence of air bronchiologram within a pulmonary nodule may indicate a high likelihood of adenocarcinoma. However, patent intratumoral bronchioles may be detected less commonly in lymphoma, and in benign nodules as focal organizing pneumonia [11], and infarct (Fig. 3). Pseudocavitations The presence of small, oval areas of low attenuation mimicking tiny cavities (pseudocavitations or bubblelike lucencies) within or surrounding the periphery of BAC was first described by Kuhlman et al. [7] (Fig. 4 a). They found pseudocavitations in 18 (60 %) of 30 nodular BACs and correlated them with intratumoral bronchioles and areas of focal emphysema (Fig. 4 b).
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3 According to Zwirewich et al. [9], pseudocavitations also may be due to air-containing cystic spaces within papillary regions of tumor growth (Fig. 4 c). On thin-slice CT sections, pseudocavitations appear as round or, more frequently, oval air-containing spaces with smooth walls. In our series, no pseudocavitation was larger than 4 mm in diameter. Usually, two or more pseudocavitations are seen within a nodule or perinodular halo of lepidic tumor growth. Smaller pseudocavitations can appear as dot-like areas of low attenuation (Fig. 5 A). An attenuation value higher than air can be caused by volume averaging or fluid contained within glandular spaces (Fig. 5 b). A cluster of pseudocavitations can mimic a true cavity (Fig. 6). Rarely, pseudocavitations are seen in non-
Fig. 1. A 2-mm-thick CT scan through middle lobe shows a 2-cm nodule with heterogeneous attenuation, infiltrating a secondary pulmonary lobule. The lobular bronchiole (arrow) can be seen branching (arrowheads) within tumor. The final pathologic diagnosis was bronchioloalveolar carcinoma, nonmucinous type Fig. 2. Thin-section CT shows a nodule containing an ectatic bronchiole (arrowheads). Histologic examination (not shown) demonstrated that bronchiolectasis was caused by desmoplastic reaction within a bronchioloalveolar carcinoma Fig. 3. Targeted, high-resolution CT scan shows a 2.5 2-cm lobular infarct. An air bronchogram (asterisks) is visible within lesion which also contains two 8-mm air-filled spaces (A) representing spared acini
Fig. 4. a High-resolution CT scan through lingula shows a 2-cm bronchioloalveolar carcinoma surrounded by a large halo of ground-glass attenuation (halo sign). An intratumoral bronchus (open arrow), multiple pseudocavitations (arrows), and serpentine radiolucencies (arrowheads) can be seen within halo. (From [8]). b Histologic slide from the surgical specimen shows two cystic areas of focal emphysema (dots and ring) separated by a septum (arrows) and located between neoplastic consolidation and lepidic tumor growth (L). In bronchioloalveolar carcinoma intratumoral areas of emphysema may develop by check-valve bronchiolar obstruction, or desmoplastic traction, or destruction of alveolar walls by neoplastic growth. Neoplastic cells line the emphysematous spaces. c Histologic slide shows two causes of intratumoral aircontaining cystic spaces in bronchioloalveolar carcinoma: a patent bronchus (b) and a cystically dilated neoplastic glandular space (c). The papillary growth of tumor (arrows) projecting into the cystic space is not visible on CT images
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Fig. 5. a Targeted high-resolution CT scan through right upper lobe shows a 1-cm nodule with spiculated edges. Four pseudocavitations, measuring 2±3 mm, are visible in this small bronchioloalveolar carcinoma. Furthermore, dot-like, low-attenuation areas (arrowheads) are seen. (A) artery of the apical segment of the upper lobe. b A photomicrograph shows a 0.8 0.4-mm, mucin-filled glandular space. Such a space correlates with dot-like radiolucencies seen on CT Fig. 6. A thin-section CT through diaphragm (D) shows a subpleural nodule containing three pseudocavitations. Note typical oval shape and smooth walls of pseudocavitations. Thin septa (arrowheads) separate the pseudocavitations. Septa were not visible, both on X-ray film and CT scan viewed at soft tissue window setting, and a frank cavitation could be suspected. Surgery demonstrated a nonmucinous bronchioloalveolar carcinoma Fig. 7. Thin-slice CT scan through left upper lobe demonstrates a nodule with spiculated margins (arrowheads) and two air-containing cystic radiolucencies (arrows) mimicking pseudocavitations. At surgery, a tuberculoma was found. Pathologic examination demonstrated that cystic spaces seen on CT were small, necrotic cavitations
BAC pulmonary malignancies [9, 11]. Small cavitations within a tuberculoma (Fig. 7) as well as aerated acini in a pulmonary infarct (see Fig. 3) can simulate pseudocavitations. Although pseudocavitations are not specific, a peripherally located nodule demonstrating spiculated borders, and pseudocavitations, is characteristic enough to suggest BAC (Fig. 5 a) [7, 9].
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Cavitation Cavitation is caused by tumor necrosis. Usually, cavitation appears as a round, solitary radiolucency with irregular walls, larger than pseudocavitation. However, small cavitations cannot be distinguished from pseudocavitations by CT (Fig. 7). Hill [1] observed overt cavitation in 7 % of BACs. In our series, we found two lesions containing an overt cavitation (3.5 %): a nodule (Fig. 8) and a pneumonic-like BAC (Fig. 9). Serpentine radiolucencies Serpentine radiolucencies have been described in BAC and correspond to air-containing neoplastic glandular spaces (Fig. 8) [8]. Since this CT sign strictly correlates with the glandular tumor structure, it is probably more specific for malignancy than pseudocavitations; however, serpentine radiolucencies are not pathognomonic for BAC. We found them also in patients with lung metastases from gastrointestinal adenocarcinoma (Fig. 10; M. Gaeta, unpublished data). Internal alveologram We classified internal alveologram as an intratumoral heterogeneous attenuation due to thick-walled alveolar spaces (Fig. 11). To the best of our knowledge, this finding has not been previously described in BAC. We ob-
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M. Gaeta et al.: Radiolucencies and cavitation in bronchioloalveolar carcinoma Fig. 8. a Thin-slice CT scan through left lung shows a nodular bronchioloalveolar carcinoma containing a frank cavitation and two serpentine radiolucencies (arrowheads). Note the irregular walls of cavitation. b An air-containing serpentine glandular space (S) is seen in this microphotograph. Lepidic tumor growth (arrows) is present at the periphery of the nodule Fig. 9. Pathologically proved, mucinous bronchioloalveolar carcinoma. A 2-mmthick CT scan shows a pneumonic-like lesion in the lingula. Areas of ground-glass attenuation (open arrows) represent lepidic tumor growth. A frank cavitation with irregular walls (arrowhead) is contained within the neoplastic consolidation. Cavitation in a pneumonic-like bronchioloalveolar carcinoma is an exceedingly rare occurrence Fig. 10. A pulmonary metastasis from gastric adenocarcinoma contains a serpentine radiolucency (arrow)
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Fig. 11. a High-resolution CT scan through right lower lobe shows a lowattenuating mucinous bronchioloalveolar carcinoma containing an enhanced pulmonary vessel (angiogram sign; black arrow). A low-attenuating metastatic adenopathy (white arrow) is seen in the right hilum. At this window setting, the mass seems to contain a large cavitation (asterisk). b At wider window width setting, a fine reticular appearance is seen within the mass. This appearance simulates thickening of intralobular interstitium, but at pathologic examination it correlated with an area of lepidic tumor growth surrounded by a thick ring of neoplastic consolidation (C)
M. Gaeta et al.: Radiolucencies and cavitation in bronchioloalveolar carcinoma
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Fig. 12 a, b. Bronchioloalveolar carcinoma proved by transbronchial biopsy. a A 4-mm-thick CT scan through lower lobes shows a pulmonary mass (M) in the right lung and diffuse nodules, some showing cavitation (arrowheads). b Three types of cavitary nodules can be detected in this scan through the upper lobes: with thin wall (1), with thick wall (2), and with a small papillary tumor projection (3)
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served it in two lesions. Internal alveologram represents an area of lepidic tumor growth surrounded by neoplastic consolidation. Multiple thin-walled cystic lesions Bronchioloalveolar carcinoma may have a widespread multinodular pattern. However, multinodular cavitary BAC is very uncommon (Fig. 12). Weisbrod et al. [13] identified thin-walled cystic lesions in four patients with BAC. The authors suggest three mechanisms to explain formation of cystic lesions: (a) ischemic necrosis; (b) obstructive bronchiectasis by check-valve bronchiolar obstruction; and (c) air-containing neoplastic space. The differential diagnosis includes eosinophilic granuloma, septic emboli, laryngeal papillomatosis, metastases and Wegener's granulomatosis [13]. The suspicion of BAC should arise in the presence of multiple, thin-walled nodules associated with a mass (Fig. 12 a). References 1. Hill CA (1984) Bronchioloalveolar carcinoma: a review. Radiology 150: 15±20 2. Adler B, Padley S, Miller RR, Muller NL (1992) High-resolution CT of bronchioloalveolar carcinoma. AJR 159: 275±277 3. Trigaux JP, Genevois PA, Goncette L, Gouat F, Schumaker A, Weynants P (1996) Bronchioloalveolar carcinoma: computed tomography findings. Eur Respir J 9: 11±16
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4. Liebow AA (1960) Bronchiolo-alveolar carcinoma. Adv Intern Med 10: 329±358 5. Barsky SH, Cameron R, Osann KE, Tomita D, Carmack Holmes E (1994) Rising incidence of bronchioloalveolar carcinoma and its unique clinicopathologic features. Cancer 73: 1163±1170 6. Ikeda T, Kurita Y, Inutsuka S et al. (1991) The changing pattern of lung cancer by histological type: a review of 1151 cases from a university hospital in Japan. Lung Cancer 7: 157±164 7. Kuhlman JE, Fishman EK, Kuhajda FP et al. (1988) Solitary bronchioloalveolar carcinoma: CT criteria. Radiology 167: 379±382 8. Gaeta M, Barone M, Caruso R, Bartiromo G, Pandolfo I (1994) CT-pathologic correlation in nodular bronchioloalveolar carcinoma. J Comput Assist Tomogr 18: 229±232 9. Zwirewich CV, Vedal S, Miller RR, Muller NL (1991) Solitary pulmonary nodule: high-resolution CT and radiologic±pathologic correlation. Radiology 179: 469±476 10. Kuriyama K, Tateishi R, Doi O et al. (1991) Prevalence of air bronchograms in small peripheral carcinomas of the lung on thin-section CT: comparison with benign tumors. AJR 156: 921±924 11. Kuriyama K, Tateishi R, Doi O et al. (1987) CT-pathologic correlation in small peripheral lung cancers. AJR 149: 1139±1143 12. Kohno N, Ikezoe J, Johkoh T et al. (1993) Focal organizing pneumonia: CT appearance. Radiology 189: 119±123 13. Weisbrod GL, Towers MJ, Chamberlain DW, Herman SJ, Matzinger FR (1992) Thin-walled cystic lesions in bronchioloalveolar carcinoma. Radiology 185: 401±405
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