(Radiographics. 2001;21:403-417.)
© RSNA, 2001
Atypical Pulmonary Metastases: Spectrum of Radiologic Findings1
Joon Beom Seo, MD,
Jung-Gi Im, MD,
Jin Mo Goo, MD,
Myung Jin Chung, MD and
Mi-Young Kim, MD
1 From the Department of Radiology, Gachon Medical School, Gil Medical Center, Inchon, South Korea (J.B.S.); the Department of Radiology, Seoul National University College of Medicine, and the Institute of Radiation Medicine, Seoul National University Medical Research Center, 28 Yongon-dong, Chongno-gu, Seoul 110-744, South Korea (J.G.I., J.M.G., M.J.C.); and the Department of Radiology, Sejong General Hospital, Kyonggigon-dong, South Korea (M.Y.K.). Recipient of a Certificate of Merit award for a scientific exhibit at the 1999 RSNA scientific assembly. Received March 30, 2000; revision requested May 30 and received August 11; accepted August 18. Address correspondence to J.G.I. (e-mail: imjg@radcom.snu.ac.kr).
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Abstract
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Typical radiologic findings of a pulmonary metastasis include multiple round variable-sized nodules and diffuse thickening of interstitium. In daily practice, however, atypical radiologic features of metastases are often encountered that make distinction of metastases from other nonmalignant pulmonary diseases difficult. A detailed knowledge of the atypical radiologic features of a pulmonary metastasis with a good understanding of the histopathologic background is essential for correct diagnosis. Squamous cell carcinoma is regarded as the most common cell type of a cavitating metastasis, but metastatic nodules from adenocarcinomas and sarcomas also cavitate occasionally. Calcification can occur in a metastatic sarcoma or adenocarcinoma, which makes differentiation from a benign granuloma or hamartoma difficult. Peritumoral hemorrhage results in areas of nodular attenuation surrounded by a halo of ground-glass opacity. Pneumothorax commonly occurs in metastases from an osteosarcoma. Air-space consolidation is often seen in cases of metastases from gastrointestinal tract malignancies. Even though tumor emboli in pulmonary arteries can be seen at computed tomography, diagnosis is difficult because they are located in small or medium arteries. A common radiologic appearance of an endobronchial metastasis is an atelectasis. In cases of an endobronchial or a solitary pulmonary metastasis, differentiation between bronchogenic carcinoma and metastasis is difficult. Dilated vascular structures within the mass can be seen in metastatic sarcomas. A sterilized metastasis after chemotherapy is radiologically indistinguishable from a residual viable tumor. Benign tumors such as uterine leiomyomas and giant cell tumors of the bone rarely metastasize to the lung.
Index Terms: Embolism, pulmonary, 60.7229 • Lung, nodule, 60.281 • Lung neoplasms, secondary, 60.33
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LEARNING OBJECTIVES
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After reading this article and taking the test, the reader will be able to:
- Identify the characteristic radiologic features of a variety of atypical pulmonary metastases.
- Describe the histopathologic background of atypical pulmonary metastases.
- Recognize the common cell types of malignancy that manifest specific patterns of atypical metastases.
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Introduction
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The lung is an extremely common site for metastases. Large autopsy series of patients with extrathoracic malignancies reveal pulmonary metastases in 20%–54% of patients (1)–(3). Among autopsy cases, the breast, colon, kidney, uterus, and head and neck are the most common primary sites with a pulmonary metastasis (3),(4). Choriocarcinoma, osteosarcoma, testicular tumor, melanoma, Ewing tumor, and thyroid carcinoma frequently metastasize to the lung, although the frequency of these primary tumors is relatively low (4),(5). The early diagnosis of pulmonary metastases in patients with a known malignancy may be critical in the planning of effective therapy. Computed tomography (CT) is accepted as the state-of-the-art modality for detection of possible pulmonary metastases.
Typical radiologic findings of a pulmonary metastasis include multiple peripherally located round variable-sized nodules (hematogenous metastasis) and diffuse thickening of the interstitium (lymphangitic carcinomatosis) (5)–(7). Among cases of multiple nodules detected with CT, 73% were reported to be pulmonary metastases (8). In daily practice, however, unusual radiologic features of metastases are frequently encountered that make distinction from other nonmalignant pulmonary diseases difficult. These features include cavitation, calcification, hemorrhage around the metastatic nodules, pneumothorax, air-space pattern, tumor embolism, endobronchial metastasis, solitary mass, dilated vessels within a mass, and sterilized metastasis.
The aim of this essay is to illustrate the various imaging features of atypical pulmonary metastases with a brief discussion of the histopathologic aspects. Benign metastasizing tumors of the lung are also discussed briefly. This article is confined to a description of pulmonary parenchymal metastases and does not include findings for mediastinal, pleural, or chest wall metastases. The key radiologic findings of atypical pulmonary metastases, the common cell types, and differential diagnoses are summarized in the Table.
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Characteristic Radiologic Findings, Mechanism, Common Primary Tumors, and Differential Diagnoses of Atypical Pulmonary Metastases
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Cavitation
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The frequency of cavitation in metastatic nodules detected on a radiograph is approximately 4%, in contrast to the 9% frequency of cavitation in pri-mary bronchogenic carcinoma (9). Squamous cell carcinomas are regarded as the most common type of cavitating metastases observed on radiographs, composing 69% of cavitating metastases (9),(10) (Figs 1, 2).
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Figure 1. Cavitating metastasis in a 72-year-old man with a squamous cell carcinoma in the left main bronchus. Transverse CT scan obtained with lung window settings shows multiple metastatic nodules in both lungs. There are several cavitating nodules (arrows) in both lower lobes. Note the irregular thickening of the cavity walls.
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Figure 2a. Cavitating metastasis in a 51-year-old man who had undergone total laryngectomy due to a laryngeal squamous cell carcinoma 2 years previously. (a) Frontal chest radiograph obtained before chemotherapy shows multiple masses (arrows) in both lungs. Note the small eccentric cavitation (arrowhead) of the mass in the left upper lung. (b) Frontal chest radiograph obtained after two cycles of chemotherapy shows extensive cavitation of nodules with air-fluid levels (arrows). Note the irregular thickening of the cavity walls. Sputum cytologic examination revealed squamous cell carcinoma.
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Figure 2b. Cavitating metastasis in a 51-year-old man who had undergone total laryngectomy due to a laryngeal squamous cell carcinoma 2 years previously. (a) Frontal chest radiograph obtained before chemotherapy shows multiple masses (arrows) in both lungs. Note the small eccentric cavitation (arrowhead) of the mass in the left upper lung. (b) Frontal chest radiograph obtained after two cycles of chemotherapy shows extensive cavitation of nodules with air-fluid levels (arrows). Note the irregular thickening of the cavity walls. Sputum cytologic examination revealed squamous cell carcinoma.
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With CT, however, cavitation in metastatic adenocarcinomas is frequently encountered (Fig 3). The frequency of cavitation of metastatic nodules observed at CT was evaluated in 281 consecutive patients with histologically or clinically confirmed pulmonary metastases. The CT scans showed cavitation of the metastatic nodules in 13 (9.5%) of 137 patients with adenocarcinomas, whereas cavitations were detected in five (10%) of 49 patients with squamous cell carcinomas (J.B.S., unpublished data, 1998). There was no statistically significant difference in the frequency of cavitation between the two histologic types.
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Figure 3. Cavitating metastasis in a 28-year-old man who had undergone resection of the rectum due to an adenocarcinoma 2 years previously. Transverse CT scan of the left lung, obtained with lung window settings, shows multiple areas of nodular attenuation with central cavitations (arrows). The walls of the nodules are relatively thin. Cavitation of the nodules was not seen on the chest radiograph (not shown).
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Metastatic sarcomas can also cavitate, and a pneumothorax can be complicated (5),(11),(12) (Fig 4). Chemotherapy is known to induce cavitation (5),(13) (Fig 2b). The exact mechanism of cavitation is usually difficult to determine, but the cause is presumed to be either tumor necrosis or a check-valve mechanism that develops by means of tumor infiltration into the bronchial structure (5),(7),(9),(10). The wall of a cavitated mass is generally thick and irregular, although thin-walled cavities can be found with metastases from sarcomas and adenocarcinomas (Figs 3, 4).
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Figure 4a. Cavitating metastasis associated with a pneumothorax and hemorrhage from an angiosarcoma of the scalp in an 86-year-old man who experienced abrupt onset of dyspnea and hemoptysis. (a) Frontal chest radiograph shows bilateral pneumothoraces (arrows) and diffuse reticular attenuation of both lungs. A drainage catheter is seen in the left hemithorax. (b) Transverse thin-section (1.0-mm) CT scan shows multiple variable-sized thin-walled cavities and bilateral pneumothoraces. Although most of the cavities appear round, some of them have bizarre shapes, mimicking the cysts of Langerhans cell histiocytosis. A subpleural cavity is ruptured into the pleural space (arrow). Multifocal areas of ground-glass opacity are seen in both lungs. (c) Photograph of the resected specimen shows hemorrhagic nodules (arrows) with central cavitary change. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals the wall of the cavity (*) is composed of large plump tumor cells. Note the freely anastomosing vascular channels (arrows) within the tumor.
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Figure 4b. Cavitating metastasis associated with a pneumothorax and hemorrhage from an angiosarcoma of the scalp in an 86-year-old man who experienced abrupt onset of dyspnea and hemoptysis. (a) Frontal chest radiograph shows bilateral pneumothoraces (arrows) and diffuse reticular attenuation of both lungs. A drainage catheter is seen in the left hemithorax. (b) Transverse thin-section (1.0-mm) CT scan shows multiple variable-sized thin-walled cavities and bilateral pneumothoraces. Although most of the cavities appear round, some of them have bizarre shapes, mimicking the cysts of Langerhans cell histiocytosis. A subpleural cavity is ruptured into the pleural space (arrow). Multifocal areas of ground-glass opacity are seen in both lungs. (c) Photograph of the resected specimen shows hemorrhagic nodules (arrows) with central cavitary change. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals the wall of the cavity (*) is composed of large plump tumor cells. Note the freely anastomosing vascular channels (arrows) within the tumor.
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Figure 4c. Cavitating metastasis associated with a pneumothorax and hemorrhage from an angiosarcoma of the scalp in an 86-year-old man who experienced abrupt onset of dyspnea and hemoptysis. (a) Frontal chest radiograph shows bilateral pneumothoraces (arrows) and diffuse reticular attenuation of both lungs. A drainage catheter is seen in the left hemithorax. (b) Transverse thin-section (1.0-mm) CT scan shows multiple variable-sized thin-walled cavities and bilateral pneumothoraces. Although most of the cavities appear round, some of them have bizarre shapes, mimicking the cysts of Langerhans cell histiocytosis. A subpleural cavity is ruptured into the pleural space (arrow). Multifocal areas of ground-glass opacity are seen in both lungs. (c) Photograph of the resected specimen shows hemorrhagic nodules (arrows) with central cavitary change. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals the wall of the cavity (*) is composed of large plump tumor cells. Note the freely anastomosing vascular channels (arrows) within the tumor.
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Figure 4d. Cavitating metastasis associated with a pneumothorax and hemorrhage from an angiosarcoma of the scalp in an 86-year-old man who experienced abrupt onset of dyspnea and hemoptysis. (a) Frontal chest radiograph shows bilateral pneumothoraces (arrows) and diffuse reticular attenuation of both lungs. A drainage catheter is seen in the left hemithorax. (b) Transverse thin-section (1.0-mm) CT scan shows multiple variable-sized thin-walled cavities and bilateral pneumothoraces. Although most of the cavities appear round, some of them have bizarre shapes, mimicking the cysts of Langerhans cell histiocytosis. A subpleural cavity is ruptured into the pleural space (arrow). Multifocal areas of ground-glass opacity are seen in both lungs. (c) Photograph of the resected specimen shows hemorrhagic nodules (arrows) with central cavitary change. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals the wall of the cavity (*) is composed of large plump tumor cells. Note the freely anastomosing vascular channels (arrows) within the tumor.
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Calcification
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Calcification of a pulmonary nodule is usually suggestive of its benign nature, most commonly a granuloma and less commonly a hamartoma, but calcification or ossification can also occur in metastatic nodules from an osteosarcoma or chondrosarcoma (5) (Fig 5). Metastatic nodules from a synovial sarcoma; giant cell tumor of the bone; and carcinomas of the colon (Fig 6), ovary, breast and thyroid may calcify (5),(14)–(17). Calcification can also be seen in treated metastatic choriocarcinomas (18). Calcification is frequently confirmed only with CT.
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Figure 5a. Calcified metastasis in a 44-year-old woman who had undergone wide excision of a left thigh mass, which proved to be an osteosarcoma, 7 years previously. (a) Frontal chest radiograph shows multiple areas of nodular attenuation in both lungs. A focal calcification (arrow) is suspected in the nodule in the left upper lobe. (b) Transverse contrast-enhanced CT scan obtained at the level of the aortic arch clearly shows calcification (arrow) within the nodule. Histopathologic examination of the resected mass revealed a metastatic osteosarcoma with the foci of ossification.
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Figure 5b. Calcified metastasis in a 44-year-old woman who had undergone wide excision of a left thigh mass, which proved to be an osteosarcoma, 7 years previously. (a) Frontal chest radiograph shows multiple areas of nodular attenuation in both lungs. A focal calcification (arrow) is suspected in the nodule in the left upper lobe. (b) Transverse contrast-enhanced CT scan obtained at the level of the aortic arch clearly shows calcification (arrow) within the nodule. Histopathologic examination of the resected mass revealed a metastatic osteosarcoma with the foci of ossification.
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Figure 6. Calcified metastasis in a 50-year-old woman who had undergone resection of the rectum due to an adenocarcinoma 3 years previously. Transverse nonenhanced CT scan shows a mass (arrow) in the right lower lobe with multiple nodular calcifications, mimicking a hamartoma. Needle biopsy of the mass revealed a metastatic adenocarcinoma.
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Several mechanisms are responsible for calcification: (a) bone formation in an osteosarcoma or chondrosarcoma; (b) dystrophic calcification in a papillary carcinoma of the thyroid, giant cell tumor of the bone, synovial sarcoma, or treated metastatic tumor; and (c) mucoid calcification in a mucinous adenocarcinoma of the gastrointestinal tract and breast (19). CT cannot help differentiate calcifications or ossifications in metastatic nodules from those in granulomas or hamartomas.
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Hemorrhage around Metastatic Nodules
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A pulmonary metastasis accompanied by a peritumoral hemorrhage has relatively characteristic CT findings of nodular attenuation surrounded by a halo of ground-glass opacity (CT halo sign) or ill-defined fuzzy margins (7) (Fig 7). A halo of ground-glass opacity is not a specific finding, however, and may also be found in other diseases, including invasive aspergillosis, candidiasis, Wegener granulomatosis, tuberculoma associated with hemoptysis, bronchioloalveolar carcinoma, and lymphoma (20)–(22). The chest radiograph shows multiple nodules with irregular margins (Fig 7).
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Figure 7a. Hemorrhagic metastasis in a 42-year-old woman with a choriocarcinoma who presented with hemoptysis. Her blood ß-human chorionic gonadotropin level was more than 140,000 U/mL. (a) Frontal chest radiograph shows ill-defined nodular and patchy attenuation in both lungs. (b) Transverse CT scan obtained with modified lung window settings shows multiple areas of nodular attenuation with surrounding areas of ground-glass opacity (arrows). The areas of ground-glass opacity are due to hemorrhage around the metastatic nodules. A small cavitation (arrowhead) is seen within the mass in the right lung.
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Figure 7b. Hemorrhagic metastasis in a 42-year-old woman with a choriocarcinoma who presented with hemoptysis. Her blood ß-human chorionic gonadotropin level was more than 140,000 U/mL. (a) Frontal chest radiograph shows ill-defined nodular and patchy attenuation in both lungs. (b) Transverse CT scan obtained with modified lung window settings shows multiple areas of nodular attenuation with surrounding areas of ground-glass opacity (arrows). The areas of ground-glass opacity are due to hemorrhage around the metastatic nodules. A small cavitation (arrowhead) is seen within the mass in the right lung.
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Angiosarcomas and choriocarcinomas are the most representative causes of hemorrhagic metastases (5),(12) (Figs 4, 7). Fragility of the neovascu-lar tissue that leads to a rupture of the vessel is a probable cause for hemorrhage around the metastasis (7),(12).
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Pneumothorax
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A pneumothorax may be seen as the result of tumor necrosis (11). Pneumothorax occurs most frequently with an osteosarcoma (Fig 8), although it has been described in other sarcomatous tumors and in tumors with an aggressive and necrotic nature (5),(11),(23),(24) (Fig 4). Necrosis of subpleural metastases is thought to produce a bronchopleural fistula that results in a pneumothorax.
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Figure 8. Pneumothorax in a 19-year-old man with a known osteosarcoma of the lower extremity who suddenly developed dyspnea. Frontal chest radiograph shows a pneumothorax (arrows). Note the multiple small metastatic pulmonary nodules (arrowheads).
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The frequency of a pneumothorax in a patient with an osteosarcoma has been reported to be approximately 5%–7% (25). In the general population, however, only 10 of 1,143 cases with a spontaneous pneumothorax have been attributed to a malignancy (26). A spontaneous pneumothorax in a patient with a sarcoma should raise the possibility of occult pulmonary metastases (24). In such instances, CT may help detect occult pulmonary metastatic nodules.
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Air-Space Pattern
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Metastases from an adenocarcinoma may spread into the lung along the intact alveolar walls (lepidic growth), in a fashion similar to a bronchioloal-veolar carcinoma (27). The radio-logic features ofthis tumor growth pattern can mimic pneumonia. In one series, six of 65 patients with pulmonary metastases from an adenocarcinoma of the gastrointestinal tract had this pattern of metastasis (28). The radiologic findings of metastases from an adenocarcinoma include air-space nodules, consolidation containing an air bronchogram, focal or extensive ground-glass opacities, and nodules with CT halo signs (Fig 9).
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Figure 9a. Air-space pattern of metastasis from an adenocarcinoma of the stomach in a 38-year-old man who had undergone radical gastrectomy 4 years previously. (a) Frontal chest radiograph shows air-space consolidation with an air bronchogram in the right upper lobe. A chest radiograph obtained 1 year previously (not shown) revealed small patchy poorly marginated lesions in the right upper lobe that were consistent with tuberculosis and failed to respond to antituberculous therapy. (b) Transverse CT scan shows consolidation in the right upper lobe with surrounding ground-glass opacity and an air bronchogram (arrow). Wedge biopsy of this lesion revealed an adenocarcinoma, which was also the histopathologic finding in the stomach lesion.
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Figure 9b. Air-space pattern of metastasis from an adenocarcinoma of the stomach in a 38-year-old man who had undergone radical gastrectomy 4 years previously. (a) Frontal chest radiograph shows air-space consolidation with an air bronchogram in the right upper lobe. A chest radiograph obtained 1 year previously (not shown) revealed small patchy poorly marginated lesions in the right upper lobe that were consistent with tuberculosis and failed to respond to antituberculous therapy. (b) Transverse CT scan shows consolidation in the right upper lobe with surrounding ground-glass opacity and an air bronchogram (arrow). Wedge biopsy of this lesion revealed an adenocarcinoma, which was also the histopathologic finding in the stomach lesion.
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Adenocarcinomas from the breast and ovary can also show this pattern of metastasis (27),(29). The diagnosis of a bronchioloalveolar carcinoma cannot be made with confidence if an extrapulmonary adenocarcinoma has not been ruled out, because both tumors have identical histologic features (27),(29).
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Tumor Embolism
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A tumor embolism is different from a hematogenous metastasis in that with the former, there is no proliferation of metastases within the extravascular tissue (30),(31). Tumor emboli were observed microscopically at autopsy in 2.4%–26.0% of patients with a solid malignancy (30),(31). Tumor emboli are usually located in small or medium arteries, which makes the diagnosis difficult radiologically, even with CT or pulmonary artery angiography (32). A normal chest radiograph with acute or subacute dyspnea and hypoxemia in a patient with a malignancy suggests the presence of a tumor embolism. Perfusion radionuclide scanning usually shows multiple small peripheral subsegmental defects.
Typical pulmonary angiographic findings include delayed filling of the segmental arteries, pruning and tortuosity of the third- to fifth-order vessels, and occasionally subsegmental filling defects. The CT findings reported for tumor emboli include multifocal dilatation and beading of the peripheral subsegmental arteries and peripheral wedge-shaped areas of attenuation due to infarction (33)–(35) (Fig 10d). In selected cases, large tumor emboli in the main, lobar, or segmental pulmonary arteries can be visualized at CT and pulmonary angiography (30),(36) (Fig 10). Tumors frequently associated with pulmonary tumor emboli are hepatomas, breast and renal cell carcinomas, gastric and prostatic cancers, and choriocarcinomas (30),(32).
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Figure 10a. Massive tumor emboli in a 48-year-old man who had undergone hepatic segmentectomy because of a hepatocellular carcinoma 2 years previously and who suddenly developed dyspnea. (a) Transverse contrast-enhanced CT scan obtained at the subcarinal level shows large thrombi (arrows) in the right main and left descending interlobar artery. The thrombi are thought to have originated from the tumor in the inferior vena cava. (b) Transverse CT scan obtained with lung window settings through the lung bases shows multifocal areas of peripheral wedge-shaped consolidation and ground-glass opacity that are thought to be pulmonary infarction. Subsegmental arteries (arrows) have a dilated and beaded appearance. Because they were not seen on CT scans obtained with lung window settings through the same level 5 days earlier (not shown), associated areas of nodular attenuation (arrowheads) within the areas of ground-glass opacity are thought to be dilated small arteries or arterioles filled with tumor emboli rather than hematogenous metastatic nodules. (c) Transverse contrast-enhanced abdominal CT scans obtained 5 days before a and b show a diffuse hepatoma (arrow) in the right hepatic lobe and a surgical defect in segment 8. Tumor thrombi (arrowheads) are also seen in the right hepatic vein and the inferior vena cava. (d) Transverse contrast-enhanced CT scans of the abdomen, obtained with a and b, show that the extent of the hepatic lesion has not changed, but the tumor thrombi in the inferior vena cava (arrowheads) are not seen. The patient died of respiratory failure 20 days later, despite intensive thrombolytic and supportive therapy.
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Figure 10b. Massive tumor emboli in a 48-year-old man who had undergone hepatic segmentectomy because of a hepatocellular carcinoma 2 years previously and who suddenly developed dyspnea. (a) Transverse contrast-enhanced CT scan obtained at the subcarinal level shows large thrombi (arrows) in the right main and left descending interlobar artery. The thrombi are thought to have originated from the tumor in the inferior vena cava. (b) Transverse CT scan obtained with lung window settings through the lung bases shows multifocal areas of peripheral wedge-shaped consolidation and ground-glass opacity that are thought to be pulmonary infarction. Subsegmental arteries (arrows) have a dilated and beaded appearance. Because they were not seen on CT scans obtained with lung window settings through the same level 5 days earlier (not shown), associated areas of nodular attenuation (arrowheads) within the areas of ground-glass opacity are thought to be dilated small arteries or arterioles filled with tumor emboli rather than hematogenous metastatic nodules. (c) Transverse contrast-enhanced abdominal CT scans obtained 5 days before a and b show a diffuse hepatoma (arrow) in the right hepatic lobe and a surgical defect in segment 8. Tumor thrombi (arrowheads) are also seen in the right hepatic vein and the inferior vena cava. (d) Transverse contrast-enhanced CT scans of the abdomen, obtained with a and b, show that the extent of the hepatic lesion has not changed, but the tumor thrombi in the inferior vena cava (arrowheads) are not seen. The patient died of respiratory failure 20 days later, despite intensive thrombolytic and supportive therapy.
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Figure 10c. Massive tumor emboli in a 48-year-old man who had undergone hepatic segmentectomy because of a hepatocellular carcinoma 2 years previously and who suddenly developed dyspnea. (a) Transverse contrast-enhanced CT scan obtained at the subcarinal level shows large thrombi (arrows) in the right main and left descending interlobar artery. The thrombi are thought to have originated from the tumor in the inferior vena cava. (b) Transverse CT scan obtained with lung window settings through the lung bases shows multifocal areas of peripheral wedge-shaped consolidation and ground-glass opacity that are thought to be pulmonary infarction. Subsegmental arteries (arrows) have a dilated and beaded appearance. Because they were not seen on CT scans obtained with lung window settings through the same level 5 days earlier (not shown), associated areas of nodular attenuation (arrowheads) within the areas of ground-glass opacity are thought to be dilated small arteries or arterioles filled with tumor emboli rather than hematogenous metastatic nodules. (c) Transverse contrast-enhanced abdominal CT scans obtained 5 days before a and b show a diffuse hepatoma (arrow) in the right hepatic lobe and a surgical defect in segment 8. Tumor thrombi (arrowheads) are also seen in the right hepatic vein and the inferior vena cava. (d) Transverse contrast-enhanced CT scans of the abdomen, obtained with a and b, show that the extent of the hepatic lesion has not changed, but the tumor thrombi in the inferior vena cava (arrowheads) are not seen. The patient died of respiratory failure 20 days later, despite intensive thrombolytic and supportive therapy.
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Figure 10d. Massive tumor emboli in a 48-year-old man who had undergone hepatic segmentectomy because of a hepatocellular carcinoma 2 years previously and who suddenly developed dyspnea. (a) Transverse contrast-enhanced CT scan obtained at the subcarinal level shows large thrombi (arrows) in the right main and left descending interlobar artery. The thrombi are thought to have originated from the tumor in the inferior vena cava. (b) Transverse CT scan obtained with lung window settings through the lung bases shows multifocal areas of peripheral wedge-shaped consolidation and ground-glass opacity that are thought to be pulmonary infarction. Subsegmental arteries (arrows) have a dilated and beaded appearance. Because they were not seen on CT scans obtained with lung window settings through the same level 5 days earlier (not shown), associated areas of nodular attenuation (arrowheads) within the areas of ground-glass opacity are thought to be dilated small arteries or arterioles filled with tumor emboli rather than hematogenous metastatic nodules. (c) Transverse contrast-enhanced abdominal CT scans obtained 5 days before a and b show a diffuse hepatoma (arrow) in the right hepatic lobe and a surgical defect in segment 8. Tumor thrombi (arrowheads) are also seen in the right hepatic vein and the inferior vena cava. (d) Transverse contrast-enhanced CT scans of the abdomen, obtained with a and b, show that the extent of the hepatic lesion has not changed, but the tumor thrombi in the inferior vena cava (arrowheads) are not seen. The patient died of respiratory failure 20 days later, despite intensive thrombolytic and supportive therapy.
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Endobronchial Metastasis
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The frequency of an endobronchial metastasis is low; grossly visible endobronchial metastases are found in the major airway in only 2% of cases (37). There are two possible routes for the pathogenesis of an endobronchial metastasis. (a) A metastasis can occur directly on the bronchial wall, by means of aspiration of tumor cells, lymphatic spread, or hematogenous metastasis to the bronchial wall, which results in a polypoid lesion inside the bronchial lumen. (b) Tumor cells in the lymph nodes or lung parenchyma that surround the bronchus grow along the bronchial tree, and some portion of the lesion invades through the bronchial wall, which results in an intraluminal lesion visible at bronchoscopy (38) (Fig 11).
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Figure 11a. Solitary endobronchial metastasis in a 47-year-old man who had undergone right nephrectomy because of a renal cell carcinoma 3 years previously. (a) Transverse CT scan shows a solitary pulmonary nodule (arrow) adjacent to the posterior segmental bronchus of the right upper lobe. Mild dilatation of the peripheral bronchi (arrowheads) is also seen. (b) Bronchoscopic image shows an endobronchial mass (arrow) in the posterior segmental bronchus of the right upper lobe. (c) Photomicrograph (original magnification, x10; hematoxylin-eosin stain) reveals a metastatic tumor ( ) of a renal cell carcinoma invading through the bronchial wall and shows the endobronchial extension (arrow).
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Figure 11b. Solitary endobronchial metastasis in a 47-year-old man who had undergone right nephrectomy because of a renal cell carcinoma 3 years previously. (a) Transverse CT scan shows a solitary pulmonary nodule (arrow) adjacent to the posterior segmental bronchus of the right upper lobe. Mild dilatation of the peripheral bronchi (arrowheads) is also seen. (b) Bronchoscopic image shows an endobronchial mass (arrow) in the posterior segmental bronchus of the right upper lobe. (c) Photomicrograph (original magnification, x10; hematoxylin-eosin stain) reveals a metastatic tumor () of a renal cell carcinoma invading through the bronchial wall and shows the endobronchial extension (arrow).
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Figure 11c. Solitary endobronchial metastasis in a 47-year-old man who had undergone right nephrectomy because of a renal cell carcinoma 3 years previously. (a) Transverse CT scan shows a solitary pulmonary nodule (arrow) adjacent to the posterior segmental bronchus of the right upper lobe. Mild dilatation of the peripheral bronchi (arrowheads) is also seen. (b) Bronchoscopic image shows an endobronchial mass (arrow) in the posterior segmental bronchus of the right upper lobe. (c) Photomicrograph (original magnification, x10; hematoxylin-eosin stain) reveals a metastatic tumor () of a renal cell carcinoma invading through the bronchial wall and shows the endobronchial extension (arrow).
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The common sources of endobronchial metastases are kidney, breast, and colorectal cancers (5),(38),(39). The most common radiologic appear-ance is an atelectasis of a lobe or the entire unilateral lung (Fig 12a). At CT, a round endobronchial lesion may be observed in conjunction with atelectasis of the corresponding lobe (Fig 12b). In many cases, differentiation between a primary bronchogenic carcinoma and an endobronchial metastasis is difficult. CT can also show hilar or mediastinal lymphadenopathy and metastatic pulmonary nodules other than the endobronchial lesion (38).
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Figure 12a. Endobronchial metastasis in a 59-year-old man with renal cell carcinoma who presented with dyspnea. (a) Frontal chest radiograph shows collapse of the left upper lobe with a suggested mass shadow (arrow) in the left hilum. (b) Transverse contrast-enhanced CT scan at the carinal level shows an endobronchial mass (arrowhead) in the orifice of the left upper lobar bronchus with collapse of the left upper lobe (arrow). Biopsy of the endobronchial mass and the right renal mass revealed a renal cell carcinoma. (Case courtesy of Jin Hwan Kim, MD, Department of Radiology, Chungnam National University, Taejeon, Korea.)
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Figure 12b. Endobronchial metastasis in a 59-year-old man with renal cell carcinoma who presented with dyspnea. (a) Frontal chest radiograph shows collapse of the left upper lobe with a suggested mass shadow (arrow) in the left hilum. (b) Transverse contrast-enhanced CT scan at the carinal level shows an endobronchial mass (arrowhead) in the orifice of the left upper lobar bronchus with collapse of the left upper lobe (arrow). Biopsy of the endobronchial mass and the right renal mass revealed a renal cell carcinoma. (Case courtesy of Jin Hwan Kim, MD, Department of Radiology, Chungnam National University, Taejeon, Korea.)
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Solitary Metastasis
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When a solitary pulmonary nodule is detected clinically in patients with a malignancy, determining whether the nodule is a metastasis or a primary bronchogenic carcinoma is difficult. The frequency of a surgically confirmed solitary metastasis in patients without a history of malig-nancy is low (0.4%–9.0%) (40),(41). When a solitary pulmonary nodule is detected on a chest radiograph in patients with an extrathoracic malignancy, the probability of metastasis is approximately 25% (42). More than one additional nodule was identified at CT in 32% of cases when only one nodule was observed on a chest radiograph (43).
With CT, 46% of the solitary pulmonary nodules detected in patients with extrapulmonary malignancies were proved to be a metastasis at histologic examination (44). The likelihood that a solitary nodule represents a pulmonary metastasis varies according to the histologic type of the primary tumor and the patient’s age (4). The most frequent malignancies include melanoma; sarcoma; and cancer of the colon, breast, kidney, bladder, and testicle (40),(41) (Fig 11).
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Dilated Vessels within a Mass
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Sometimes dilated, tortuous, and tubular enhancing structures within the metastatic nodule are observed at contrast material–enhanced CT. These structures are engorged tumor vessels that suggest the hypervascular nature of the metastatic nodule. Such findings are observed in cases of a metastasis from a sarcoma such as an alveolar soft-part sarcoma or a leiomyosarcoma (45),(46) (Fig 13).
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Figure 13a. Dilated vessels within a metastatic mass in a 32-year-old woman who had undergone excision of an alveolar soft-part sarcoma of the left foot 5 years previously. (a) Transverse contrast-enhanced CT scan shows a well-defined enhancing nodule in the left lower lobe. Enhancing tubular structures (arrowheads) in the lesion suggest dilated vessels. (b) Photograph of a resected specimen slide (original magnification, x1; hematoxylin-eosin stain) reveals a well-circumscribed nodule containing a dilated vascular structure (arrow), which corresponds to the enhancing tubular structure seen in a. The black line at the top indicates 1 cm. (Reprinted, with permission, from reference 46.)
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Figure 13b. Dilated vessels within a metastatic mass in a 32-year-old woman who had undergone excision of an alveolar soft-part sarcoma of the left foot 5 years previously. (a) Transverse contrast-enhanced CT scan shows a well-defined enhancing nodule in the left lower lobe. Enhancing tubular structures (arrowheads) in the lesion suggest dilated vessels. (b) Photograph of a resected specimen slide (original magnification, x1; hematoxylin-eosin stain) reveals a well-circumscribed nodule containing a dilated vascular structure (arrow), which corresponds to the enhancing tubular structure seen in a. The black line at the top indicates 1 cm. (Reprinted, with permission, from reference 46.)
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Sterilized Metastasis
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When a metastatic nodule persists after adequate chemotherapy with its size unchanged or slightly diminished, it is occasionally discovered at surgical resection to be only necrotic nodules with or without fibrosis and without viable tumor cells (5),(7),(47). Except for the stable appearance of their size, these "sterilized" nodules are radiologically indistinguishable from a residual viable tumor. Metastases from a choriocarcinoma, testicular cancer, after chemotherapy are common causes of sterilized metastases (47),(48). When biologic markers such as ß–human chorionic gonadotropin and 
-fetoprotein are available, this additional information may help determine the viability or sterility of a pulmonary nodule. Histologic confirmation is necessary when such a problems arises (7). After treatment, positron emission tomography, with its capability to help evaluate biologic activity, may help differentiate between a sterilized metastasis and a viable residual tumor.
Some germ cell tumors convert to a benign mature teratoma after chemotherapy and result in persistence of the masses (49). In patients with nonseminomatous germ cell tumors, enlargement of the masses with negative serum tumor markers after chemotherapy usually represents mature teratomas rather than residual malignancies (50). In some cases of pulmonary metastases from germ cell tumors treated with chemotherapy, thin-walled cavities that arise at the sites of the pulmonary metastases, so-called pulmonary lacunae, persist for years without change (51).
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Benign Metastasizing Tumor
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Benign tumors in an extrapulmonary site rarely metastasize to the lung. Despite their metastatic spread, these tumors are histologically benign. They generally originate from a leiomyoma of the uterus (Fig 14), a hydatidiform mole of the uterus, a giant cell tumor of the bone (Fig 15), a chondroblastoma, a pleomorphic adenoma of the salivary gland, or a meningioma (15),(52)–(57).
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Figure 14a. Benign metastasis from a uterine leiomyoma in a 39-year-old woman who had undergone hysterectomy 10 years previously. (a) Transverse contrast-enhanced CT scan shows a 2-cm-diameter round mass (arrow) adjacent to the left upper lobar bronchus. Two small nodules were seen in the right lower lobe (not shown). (b) Photomicrograph (original magnification, x200; hematoxylin-eosin stain) reveals tumor cells formed by interlacing bundles of smooth muscle cells separated by well-vascularized connective tissue, which is consistent with a metastasizing leiomyoma.
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Figure 14b. Benign metastasis from a uterine leiomyoma in a 39-year-old woman who had undergone hysterectomy 10 years previously. (a) Transverse contrast-enhanced CT scan shows a 2-cm-diameter round mass (arrow) adjacent to the left upper lobar bronchus. Two small nodules were seen in the right lower lobe (not shown). (b) Photomicrograph (original magnification, x200; hematoxylin-eosin stain) reveals tumor cells formed by interlacing bundles of smooth muscle cells separated by well-vascularized connective tissue, which is consistent with a metastasizing leiomyoma.
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Figure 15a. Benign metastasis from a giant cell tumor in a 42-year-old man who had undergone repeated curettage of the left third finger. (a) Transverse contrast-enhanced CT scan shows a round mass in the right lower lobe. Note the central nonenhancing area and the septum-like structure (arrowhead). (b) Transverse CT scan obtained at a distal tracheal level shows another 1-cm-diameter nodule in the left upper lobe (arrow). On a follow-up CT scan obtained 3 months later (not shown), the nodule had grown to 2 cm in diameter. (c) Photograph of the resected specimen demonstrates the cut surface of the mass that was removed from the right lower lobe with video-assisted thoracic surgery. The mass is confined within the visceral pleura and shows areas of hemorrhage (arrows) that correspond to the nonenhancing area in a. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals stromal cells and multinucleated giant cells that were similar to those found in the finger lesion.
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Figure 15b. Benign metastasis from a giant cell tumor in a 42-year-old man who had undergone repeated curettage of the left third finger. (a) Transverse contrast-enhanced CT scan shows a round mass in the right lower lobe. Note the central nonenhancing area and the septum-like structure (arrowhead). (b) Transverse CT scan obtained at a distal tracheal level shows another 1-cm-diameter nodule in the left upper lobe (arrow). On a follow-up CT scan obtained 3 months later (not shown), the nodule had grown to 2 cm in diameter. (c) Photograph of the resected specimen demonstrates the cut surface of the mass that was removed from the right lower lobe with video-assisted thoracic surgery. The mass is confined within the visceral pleura and shows areas of hemorrhage (arrows) that correspond to the nonenhancing area in a. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals stromal cells and multinucleated giant cells that were similar to those found in the finger lesion.
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Figure 15c. Benign metastasis from a giant cell tumor in a 42-year-old man who had undergone repeated curettage of the left third finger. (a) Transverse contrast-enhanced CT scan shows a round mass in the right lower lobe. Note the central nonenhancing area and the septum-like structure (arrowhead). (b) Transverse CT scan obtained at a distal tracheal level shows another 1-cm-diameter nodule in the left upper lobe (arrow). On a follow-up CT scan obtained 3 months later (not shown), the nodule had grown to 2 cm in diameter. (c) Photograph of the resected specimen demonstrates the cut surface of the mass that was removed from the right lower lobe with video-assisted thoracic surgery. The mass is confined within the visceral pleura and shows areas of hemorrhage (arrows) that correspond to the nonenhancing area in a. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals stromal cells and multinucleated giant cells that were similar to those found in the finger lesion.
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Figure 15d. Benign metastasis from a giant cell tumor in a 42-year-old man who had undergone repeated curettage of the left third finger. (a) Transverse contrast-enhanced CT scan shows a round mass in the right lower lobe. Note the central nonenhancing area and the septum-like structure (arrowhead). (b) Transverse CT scan obtained at a distal tracheal level shows another 1-cm-diameter nodule in the left upper lobe (arrow). On a follow-up CT scan obtained 3 months later (not shown), the nodule had grown to 2 cm in diameter. (c) Photograph of the resected specimen demonstrates the cut surface of the mass that was removed from the right lower lobe with video-assisted thoracic surgery. The mass is confined within the visceral pleura and shows areas of hemorrhage (arrows) that correspond to the nonenhancing area in a. (d) Photomicrograph (original magnification, x400; hematoxylin-eosin stain) reveals stromal cells and multinucleated giant cells that were similar to those found in the finger lesion.
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The radiologic findings of metastases from benign tumors are indistinguishable from those of hematogenous metastases from malignant tumors. In contrast to metastases from malignant tumors, however, benign metastasizing tumors usually show very slow growth.
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Conclusions
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Although most cases of pulmonary metastases can be diagnosed radiologically on the basis of typical findings, atypical radiologic manifestations of pulmonary metastases make confident diagnosis difficult. An awareness of the spectrum of radiologic manifestations in atypical pulmonary metastases along with their histopathologic findings allows the distinction of metastases from other nonmalignant pulmonary diseases. When atypical radiologic features of a pulmonary metastasis are seen and aggressive therapy for the primary lesion or metastasis is proposed, tissue diagnosis at bronchoscopy or percutaneous transthoracic needle aspiration biopsy is recommended.
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Abstract
LEARNING OBJECTIVES
