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Thoracic Imaging |
1 From the Departments of Diagnostic Radiology (W.Y., Y.H.K., J.K.K., J.G.P., H.K.K.) and Internal Medicine (Y.C.K.), Chonnam National University Medical School, Chonnam National University Hospital, 8 Hak-1-dong, Dong-gu, Gwangju 501-757, South Korea. From the 2001 RSNA scientific assembly. Received March 21, 2002; revision requested June 6; revision received July 8; accepted August 8. Address correspondence to W.Y. (e-mail: radyoon@cnuh.com).
| ABSTRACT |
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MATERIALS AND METHODS: Forty consecutive patients with massive hemoptysis underwent contrast materialenhanced CT. Massive hemoptysis was defined as the expectoration of 300600 mL of blood per day. Two CT features were considered to be suggestive of a nonbronchial systemic arterial supply: (a) pleural thickness of more than 3 mm adjacent to the parenchymal lesion and (b) enhancing vascular structures within the extrapleural fat layer. Conventional angiography was used as the standard of reference. CT scans were evaluated by two radiologists in consensus. The CT findings were compared with those of conventional angiography. The sensitivity, specificity, predictive values, and accuracy of CT for predicting the presence of a nonbronchial systemic arterial supply were assessed.
RESULTS: In the determination of a nonbronchial systemic arterial supply, CT had a sensitivity of 80%, specificity of 84%, positive predictive value of 73%, negative predictive value of 91%, and accuracy of 84%. Sensitivity was highest for predicting the branches of subclavian and axillary arterial supply and was lowest for predicting the internal mammary arterial supply. Specificity and accuracy were highest for predicting the intercostal arterial supply.
CONCLUSION: CT demonstrates acceptable sensitivity, specificity, and accuracy in the prediction of a nonbronchial systemic arterial supply in patients with massive hemoptysis.
© RSNA, 2003
Index terms: Arteries, bronchial Lung, CT, 60.1211 Lung, hemorrhage Lung, systemic blood supply, 60.20, 66.20 Pleura, diseases, 66.2056, 66.234
| INTRODUCTION |
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Immediate nonrecurrence rates after bronchial artery embolization have been reported to be 73%98% (4,12,15). The long-term success rate of bronchial artery embolization, however, is unfavorable. Delayed recurrence of hemoptysis after successful embolization of the bronchial artery may be caused by incomplete embolization of vessels, recanalization of previously embolized vessels, revascularization of the collateral circulation, or progression of basic lung disease (3,9,16,17). In addition, systemic arteries other than the bronchial artery can be a major source of bleeding in 41%88% of patients with massive hemoptysis (13,14). Failure to recognize the presence of a nonbronchial systemic arterial supply in patients with massive hemoptysis may result in recurrent bleeding after successful bronchial artery embolization (6,13,14,1821).
Chest radiography is initially used in the assessment of patients with massive hemoptysis. Several investigators have noted that the presence of pleural thickening at radiography is highly associated with the presence of a nonbronchial systemic arterial supply andcan be used as a predictor of that supply (6,13,14,20). Computed tomography (CT) of the chest is now considered a primary noninvasive imaging modality in the evaluation of patients with massive hemoptysis (1,22). The identification of nonbronchial systemic arteries at emergent chest CT and their subsequent embolization in patients with massive hemoptysis would considerably improve patient treatment because persistent or recurrent hemoptysis after successful embolization of the bronchial arteries would be avoided. To our knowledge, however, the role of chest CT in the prediction of a nonbronchial systemic arterial supply in patients with massive hemoptysis has not been reported previously. The purpose of this study was to evaluate the diagnostic accuracy of chest CT in the prediction of a nonbronchial systemic arterial supply in patients with massive hemoptysis.
| MATERIALS AND METHODS |
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CT Examination
All patients underwent contrast materialenhanced CT. CT was performed with a helical scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis) with patients in the supine position. Unenhanced scans were obtained to detect hemorrhage or calcifications in the parenchymal lesions and to determine a more precise scan range for the subsequent contrast-enhanced CT examinations. These unenhanced scans were obtained with a section thickness of 10 mm; the scan range was from the lung apex to the lung base.
Contrast-enhanced scans were obtained to determine the presence or absence of findings associated with a nonbronchial systemic arterial supply to the parenchymal lesions. All patients received 120 mL of contrast material with 300 mg of iodine per milliliter (iohexol, Omnipaque 350; Nycomed-Amersham, Princeton, NJ), which was administered intravenously by means of a power injector (CT 9,000 Digital Injection System; Liebel-Flarsheim, Cincinnati, Ohio) at an injection rate of 2.53.0 mL/sec. We used a cubital vein as the access route and 20- and 18-guage intravenous systems. The CT examination started with a delay of 15, 18, or 20 seconds, depending on the location of the venous access and the cardiac state of the patient. Scans were obtained with 10-mL collimation at 10-mm intervals from the lung apices to the level of the adrenal glands with use of a conventional algorithm (window level, 1,750 HU; window width, -750 HU). CT scans were printed at window settings that are optimal for lung parenchyma and soft tissue (window level, 400 HU; window width, 20 HU).
Additional thin-section CT scans were obtained in all patients and reconstructed by means of a high-spatial-resolution algorithm. Thin-section CT scans were obtained to evaluate the pulmonary abnormality responsible for the massive hemoptysis. These scans were obtained at full inspiration with 1-mm collimation at 2-cm intervals throughout the lungs with the patients in a supine position. A high-spatial-frequency reconstruction algorithm was used, and scans were reviewed with soft-tissue and lung window settings.
On the basis of previous reports (2325) and our preliminary experiences, the following CT features are considered to be suggestive of a nonbronchial systemic arterial supply as a source of massive hemoptysis: (a) pleural thickening of more than 3 mm that abuts the pulmonary abnormality and (b) enhancing vascular structures within the extrapleural fat layer. We classified nonbronchial systemic arteries into three groups according to anatomic location: superolateral, anteromedial, and posterior. The superolateral group of nonbronchial systemic arteries included the branches of the subclavian and axillary arteries, the anteromedial group included the internal mammary artery and its branches, and the posterior group included the intercostal arteries. When the CT features suggestive of a nonbronchial systemic arterial supply were noted at the apex of the chest above the level of the aortic arch, we recorded this as evidence of the presence of the superolateral group of nonbronchial systemic vessels. When CT features were noted along the anterior and mediastinal pleura below the level of the aortic arch, we recorded this as evidence of the presence of the anteromedial group of nonbronchial systemic vessels. When CT features were noted along the posterior pleura, we recorded this as evidence of the presence of the posterior group of nonbronchial systemic vessels.
The presence or absence of CT features suggestive of a nonbronchial systemic arterial supply was recorded for each anatomic location in each hemithorax in each patient. Two radiologists (W.Y., Y.H.K.), who have served as thoracic radiologists for 2 and 5 years, respectively, and who were blinded to angiographic results, retrospectively reviewed the CT scans for each patient. They scored the CT scans together, and conclusions were reached by consensus. CT images were reviewed as hard-copy images.
Conventional Angiography
Conventional angiography and concomitant bronchial artery embolization were performed within 1 week after CT in all patients. Angiography was used as the standard of reference for diagnosis of a nonbronchial arterial supply to the lung parenchymal lesion. The mean interval between CT and angiography was 2 days. In all patients, conventional angiography was performed with a digital subtraction technique (Angiostar; Siemens Medical Systems, Erlangen, Germany).
Thoracic aortograms, selective bronchial angiograms, subclavian angiograms, intercostal angiograms, and internal mammary angiograms were obtained in all patients. The intercostal arteries to be studied were determined on the basis of the findings at thoracic aortography; that is, we studied the intercostal arteries that were enlarged at thoracic aortography. Angiography was performed with a transfemoral approach and the Seldinger technique. Various types of angiographic catheters were used to selectively inject different arteries. The following angiographic findings were considered to be responsible for massive hemoptysis: (a) tortuous enlargement of systemic vessels that supplied the hypervascular parenchymal staining and (b) a shunt into pulmonary vessels. All conventional angiographic studies and embolization procedures were performed by one interventional radiologist (J.K.K.). Two radiologists (J.K.K., J.G.P.) retrospectively reviewed all angiograms and noted whether the angiographic findings were present or absent; conclusions were reached with consensus. The findings at diagnostic angiography were used to determine whether embolization of bronchial arteries and nonbronchial systemic arteries should be performed.
Statistical Analysis
End points of the study were the sensitivity, specificity, positive and negative predictive values, and overall accuracy of CT. Conventional angiography was used as the standard of reference. Sensitivity was defined as the percentage of nonbronchial systemic arterial supplies identified correctly at CT. Specificity was defined as the percentage of cases identified correctly at CT as showing an absence of a nonbronchial systemic arterial supply. Accuracy was defined as the percentage of correct diagnoses (true-positive and true-negative diagnoses). A false-negative finding occurred when CT depicted the absence of a nonbronchial systemic arterial supply that was seen at angiography. False-positive findings occurred when CT depicted the presence of a nonbronchial systemic arterial supply that was not seen at angiography.
| RESULTS |
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| DISCUSSION |
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Nonbronchial systemic arteries can be a major source of massive hemoptysis. In a recent study (13) of 103 patients who underwent bronchial artery embolization, 42 (41%) had nonbronchial systemic contributions and 12 (11.7%) had abnormal nonbronchial systemic arteries but normal bronchial arteries. Michelle et al (14) found that nonbronchial collateral vessels supplied the bleeding area in 14 of 16 patients (88%) with life-threatening hemoptysis. In three of those 16 patients (19%), bleeding from systemic vessels other than the bronchial arteries was the only source of hemoptysis. Vujic et al (28) controlled hemoptysis in three patients by embolizing only the intercostal arteries. Jardin and Remy (19) reported that the internal mammary artery was an important feeder vessel in 11 of 23 patients with hemoptysis. In the study by Hashimoto et al (21), massive hemoptysis was caused by internal mammary artery contributions to the perfusion of lesions in five of 13 patients.
If nonbronchial systemic arteries are not seen at the initial angiographic examination, bleeding may recur soon after successful embolization of the bronchial artery. Many investigators have shown that a concerted search for a nonbronchial systemic arterial supply should be performed (6,9,13,14,19,21,28). Therefore, the prediction of a nonbronchial systemic arterial supply before bronchial artery embolization may be useful for treating patients because the angiographic and embolization procedures can be performed in a focused and efficient manner. In addition, the prediction and embolization of nonbronchial systemic arterial supply can lower the immediate recurrence rate after successful embolization.
It is well known that pleural disease is necessary for the development of a nonbronchial systemic arterial supply to the parenchymal lesion (6,27,29). Anatomically, the parietal pleura is supplied by systemic capillary vessels, whereas the visceral pleura derives its arterial supply from the bronchial arteries. Nonbronchial systemic arteries supply systemic blood to the lungs in pathologic conditions via pleural adhesions, and these transpleural nonbronchial systemic arteries are more likely to occur with diseases that involve the pleura than with those confined to the pulmonary parenchyma (6). In patients with chronic pulmonary inflammation, large anastomoses can develop between systemic and pulmonary arteries in the presence of pleural adhesions (27,30). Therefore, the presence of pleural thickening on an imaging study can be indicative of a nonbronchial systemic arterial supply in patients with massive hemoptysis.
Several investigators have found that pleural thickening at chest radiography can be used as a predictor of nonbronchial systemic vessels in patients with massive hemoptysis. Michelle et al (14) documented that 10 of 13 patients with pleural thickening adjacent to a radiologically abnormal area of lung parenchyma at chest radiography had nonbronchial systemic vessels. Tamura et al (20) reported that long-term complete hemostasis after embolization therapy was achieved in 78% of procedures in patients without pleural thickening at radiography and in 29% of procedures in patients with pleural thickening.
Although chest radiography is usually used in the initial assessment of patients with pleural abnormalities, radiographic findings cannot help differentiate benign from malignant disease and pleural from parenchymal lesions (eg, subpleural consolidations). It is possible that pleural disease as an indicator of nonbronchial systemic vessels may have been detected more easily and accurately in patients with massive hemoptysis if a more sensitive radiologic technique, such as CT, had been used. It is well known that CT is the best modality with which to examine the pleura, and it has been used to evaluate the various pleural diseases (3134).
To our knowledge, however, no studies have been performed to evaluate the usefulness of CT in the prediction of nonbronchial systemic vessels as a cause of bleeding in patients with massive hemoptysis. CT has been used increasingly in the assessment of patients with massive hemoptysis (6,13,14,20). In the literature (1,22), it is recommended that CT should be performed before bronchoscopy in all cases of massive hemoptysis. CT may help the diagnosis of the cause of massive hemoptysis and the localization of bleeding lobes before bronchial artery embolization.
In general, a pleural thickness of more than 3 mm at CT is considered to be an abnormal finding (2325). The extrapleural fat layer usually contains a few systemic vessels that supply the parietal pleura (24). These vessels can be visualized with contrast material. In patients with chronic pleural inflammation, this extrapleural fat layer can become markedly thickened, and systemic vessels may be enlarged, which enables them to be easily identified at contrast-enhanced CT as tortuous tubular enhancing structures (24). On the basis of previous reports (2325) and our preliminary experience, a pleural thickness of more than 3 mm and the presence of systemic vessels within an extrapleural fat layer should be considered CT criteria for the presence of a nonbronchial systemic arterial supply.
Findings in the present study indicate that chest CT can help predict the presence of a nonbronchial systemic arterial supply in patients with massive hemoptysis. CT had an overall sensitivity of 80% and a specificity of 86% in the detection of a nonbronchial systemic arterial supply in 40 patients. There were nine false-negative and 14 false-positive diagnoses with CT. The false-negative cases were relatively evenly distributed; four were in the anteromedial group, three were in the posterior group, and two were in the superolateral group. In nine false-negative cases (eight patients), the cause of massive hemoptysis was active tuberculosis in four cases, acute pneumonia in three cases, bronchiectasis in one case, and chronic tuberculosis in one case. Thus, most false-negative findings (78%) occurred with acute conditions rather than with chronic pulmonary diseases. We believe that CT has a limited sensitivity in the detection of a nonbronchial systemic supply in patients with acute pulmonary disease and massive hemoptysis, because acute pulmonary disease that causes massive hemoptysis does not have enough time to result in pleural adhesion and pleural thickening that would be depicted at CT.
In the present study, the largest proportion of false-positive findings (n = 8) occurred in the superolateral group. False-positive findings were made in four cases in the anteromedial group and in two cases in the posterior group. All false-positive findings of superolateral nonbronchial systemic supply were observed in patients with chronic tuberculosis (24). It is well known that apical pleural thickening is common in patients with chronic parenchymal disease that involves the lung apex, especially in those with chronic tuberculosis. These factors may be responsible for the large proportion of false-positive findings in the superolateral group.
Our study has several limitations. First, the population was inhomogeneous. Although most of our patients had chronic pulmonary disease, 25% (10 of 40) had acute pulmonary disease. As indicated earlier, a nonbronchial systemic arterial supply may develop without pleural adhesion and thickening in cases of acute pulmonary disease. Another limitation is that lung zones supplied by one nonbronchial systemic arterial supply group may overlap with another. It is impossible to divide the lung zones according to vascular territories supplied by specific systemic arteries. Although we classified nonbronchial systemic arteries into three groups according to vascular territories, the areas may overlap. Another limitation of our study is that the angiographic criteria used as a standard of reference are not perfect. Although extravasation of contrast material is considered a specific sign of massive hemoptysis, it is rarely seen. Thus, we strictly applied the positive angiographic sign of hypervascular parenchymal staining, which is supplied by enlarged systemic arteries that are associated with a systemic-pulmonary shunt.
In conclusion, chest CT demonstrates acceptable sensitivity, specificity, positive and negative predictive values, and accuracy in the prediction of a nonbronchial systemic arterial supply in patients with massive hemoptysis. At CT, pleural thickness of more than 3 mm and enlarged vascular structures within extrapleural fat are good indicators that a nonbronchial systemic arterial supply is the cause of bleeding in patients with massive hemoptysis. Identification of a nonbronchial systemic arterial supply at CT before bronchial artery embolization is important because it is helpful for selecting systemic vessels to be studied and embolized.
| FOOTNOTES |
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| REFERENCES |
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