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1 Department of Radiology, Georges Pompidou Hospital, 20 rue Leblanc, 75015
Paris, France.
2 Department of Pneumology, Georges Pompidou Hospital, 75015 Paris,
France.
Received December 14, 2001;
accepted after revision April 17, 2002.
Presented at the annual meeting of the Radiological Society of North
America, Chicago, November 2000.
Abstract
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MATERIALS AND METHODS. We reviewed the chest radiographs, CT scans, and bronchoscopic findings in 80 patients with either large or massive hemoptysis who were admitted to our intensive care unit between January 1995 and June 1999.
RESULTS. Findings on chest radiography were normal in only 13% of patients, of whom 70% had bronchiectasis. The chest radiographs revealed the site of bleeding in 46% of the patients and the cause in 35%, most of whom had tuberculosis or tumors. CT was more efficient than bronchoscopy for identifying the cause of bleeding (77% vs 8%, respectively; p < 0.001), whereas the two methods were comparable for identifying the site of bleeding (70% vs 73%, respectively; p = not significant).
CONCLUSION. These data suggest that CT could replace bronchoscopy as the first-line procedure for screening patients with large and those with massive hemoptysis. However, these results must be confirmed in a prospective multicenter study.
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The severity of hemoptysis is based on the amount of blood expectorated. According to Coss-Bu et al. [10], major hemoptysis comprises large and massive bleeding, which correspond to blood expectoration of 150-400 mL per day and to more than 400 mL per day, respectively. Other definitions of massive hemoptysis range from 400 to 1000 mL per day [2, 3, 11]. Regardless of the exact amount of blood loss for each category of major hemoptysis, large and massive hemoptysis are both life-threatening. Patients must be hospitalized immediately and must undergo urgent investigations including fiberoptic bronchoscopy, chest radiography, and, in most cases, CT. Bronchial arteriography is often required also and can be coupled with bronchial embolization.
There is no consensus about the optimal examinations for patients who present with hemoptysis [12, 13]. CT and bronchoscopy have been evaluated in this setting [14,15,16], but studies about the specific contribution of each in enabling the diagnosis of major hemoptysis have not, to our knowledge, been performed.
We reviewed the files of all consecutive patients with large or massive hemoptysis admitted to the intensive care unit of our institution from January 1995 to June 1999. The aim of the study was to assess the capacity of chest radiography and CT to determine the cause and site of bleeding relative to bronchoscopy.
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Expectoration of 300 mL or more of blood in 24 hr was defined as massive hemoptysis and of less than 300 mL/24 hr, as large hemoptysis. We excluded from this analysis patients who required admission to the intensive care unit despite the fact that these patients had a small volume of bleeding.
Chest radiographs and CT scans were reviewed by observers who focused on the site and cause of bleeding. These images were considered to show the site of bleeding when at least the side of bleeding could be identified. Radiologic abnormalities were classified as nonspecific for the cause when they simply revealed bleeding and specific when they indicated the cause of bleeding.
We considered that bleeding could create three types of nonspecific radiologic abnormalities: alveolar consolidations (on chest radiography and CT) and ground-glass opacities (on CT), both resulting from the alveolar lumen filling with blood; and atelectasis, induced by clots obstructing the bronchi. These findings were considered to show the site of bleeding if they were unilateral and affected the entire lung, a lobe, or a segment. Nonspecific bilateral abnormalities were also considered to show the site of bleeding when they predominated on one side.
Disease-specific abnormalities were considered to show the cause of bleeding. They were also considered to reveal the site of bleeding if they were strictly unilateral on chest radiography or bilateral but were associated with focal ground-glass opacities on CT. Bronchiectasis was diagnosed when chest radiographs showed tubular or ring opacities or when CT showed bronchi twice the diameter of the neighboring arteries. Large irregular opacities on chest radiographs and CT scans were considered indicative of tumors. Aspergilloma was diagnosed only when a typical fungus ball was visible on chest radiographs (round mass of soft-tissue density with an air-crescent sign) or CT scans. Extensive areas of consolidation associated with focal excavation were considered to indicate acute tuberculosis. Diagnosis of lesions caused by previous tuberculosis infections (i.e., posttuberculous lesions) was based on a combination of the following findings: calcified granulomas, retractile linear opacities, bronchiectasis, and pleural thickening, mainly of the upper lobes. Bronchiectasis with other sequelae of tuberculosis was classified as a posttuberculous lesion, contrary to isolated bronchiectasis.
Radiographic findings were also interpreted in light of available pathologic or microbiologic data. Patient files were reviewed independently by two observers, and a consensus was reached in cases of disagreement. The results of bronchial arteriography and embolization procedures and surgical findings were also assessed if available.
The different approaches for the diagnosis of the site and cause of hemoptysis were compared using the chi-square test or Fisher's exact test.
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The remaining 80 patients had massive (n = 23) or large hemoptysis (n = 57). There were 23 women and 57 men who ranged in age from 20 to 93 years (mean, 58 years). Hemoptysis revealed an underlying disease in 71 patients and complicated a known disease in nine patients (bronchiectasis, n = 7; lung cancer, n = 2).
All 80 patients underwent chest radiography, 73 underwent fiberoptic bronchoscopy, and 57 underwent CT. CT was performed within 48 hr of bleeding onset in 56 patients and 15 days later in one. Forty-two patients underwent bronchial arteriography. Three patients underwent emergency surgery, and 14 underwent surgery between 2 weeks and 3 months after the onset of hemoptysis.
Chest Radiography
The chest radiographs revealed normal findings in only 10 patients (13%)
(Table 1). Seven of 10 these
patients had bronchiectasis; one, an inflammatory tracheal tumor; and one, an
aortic false aneurysm with a bedside radiograph that showed normal findings.
The remaining patient with normal radiologic findings also had normal findings
on a CT examination performed 15 days after the onset of hemoptysis; this
patient did not undergo any further investigations.
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Chest radiographs depicted abnormal findings in 70 patients (87%). The radiographs showed the site of bleeding alone in 20 patients (Fig. 1A,1B,1C) and the cause of bleeding alone in 11 patients who had specific abnormalities that were bilateral so we could not determine which side was bleeding (diffuse bronchiectasis, n = 3; acute tuberculosis with bilateral extensive lesions, n = 3; bilateral posttuberculous lesions, n = 4; and bilateral aspergillomas, n = 1). Both the site and the cause of bleeding could be seen in 17 patients, most of whom had lung cancer (n = 6) or unilateral tuberculous lesions (n = 6). Despite revealing abnormal findings, chest radiographs showed neither the site nor the cause of bleeding in 22 patients.
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CT
CT scans were available for 57 patients
(Table 2). Slices ranging from
6 to 10 mm in thickness were obtained. In 46 patients, the thick slices were
considered inadequate, so high-resolution CT immediately followed. Contrast
medium was not routinely used.
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CT findings were normal in only one patient. However, CT was performed 15 days after the onset of bleeding in this patient, whereas CT was performed within 48 after the onset of bleeding in the remaining 56 patients.
CT revealed the site of bleeding alone in 10 patients. In seven of these patients, CT revealed nonspecific abnormalities considered to be associated with the bleeding: localized groundglass opacities in five patients, alveolar opacities in one patient, and inferior lobar atelectasis in one patient. A nonspecific cavitary lesion and an abscess were each found in one patient (surgical diagnoses of aspergillosis and actinomycosis, respectively). In the last patient, CT revealed a pseudotumoral nodular lesion surrounded by ground-glass opacities that corresponded to a mucoid impaction in distal bronchiectasis at pathologic examination.
CT showed the cause of bleeding alone in 14 patients. Nine had diffuse bronchiectasis; four, bilateral tuberculous lesions; and one, bilateral aspergillomas.
CT showed neither the site nor the cause of bleeding in two patients. One had isolated bilateral ground-glass opacities, and the other had bilateral cavitary lesions due to actinomycosis (surgical diagnosis).
Both the site and the cause of bleeding were revealed on CT in the remaining 30 patients (Figs. 2A,2B,3A,3B,3C,4). The lesions were localized or associated with localized ground-glass opacities.
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In total, CT located the bleeding site in 40 (70%) of the 57 patients examined and showed the cause of bleeding in 44 patients (77%).
Fiberoptic Bronchoscopy
Fiberoptic bronchoscopy was performed in 73 (91%) of the 80 patients
(Table 3). It revealed normal
findings or only showed mild inflammation of the bronchial mucosa in five
patients (7%).
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Fiberoptic bronchoscopy identified the site of bleeding alone in 47 patients (64%), showing the involved segment in four, the involved side in 12 patients, and the involved lobe in 31.
Fiberoptic bronchoscopy identified both the site and the cause of bleeding in six of the nine patients with tracheal or bronchial tumors, of whom two already had a diagnosis of lung cancer.
Fiberoptic bronchoscopy failed to show either the site or the cause of bleeding in 15 patients. It only revealed blood throughout the bronchial tree.
In total, the site of bleeding was identified on bronchoscopy in 73% of the patients and on CT in 70% of the patients (p, not significant; chi-square test). In contrast, bronchoscopy only identified the cause of bleeding in 8% of the patients (six of the nine patients with tumors), whereas CT findings revealed the cause and enabled diagnosis in 77% of the patients (p < 0.001). Peripheral tumors were identified in three patients on CT, whereas fiberoptic bronchoscopy only showed the site of bleeding in two of these patients and failed to identify either the site or the cause of bleeding in the last patient. In this patient, bronchoscopy only revealed the presence of blood throughout the bronchial tree.
Bronchial Arteriography and Embolization
Forty-six patients were referred for bronchial arteriography either to
control bleeding or to prevent recurrence in those admitted for recent massive
hemoptysis on the basis of the assumption that another episode could be fatal.
Bronchial arteriography was never performed for diagnostic purposes only. CT
identified a fissured aortic false aneurysm
(Fig. 4) in a patient scheduled
for bronchial arteriography because of a recurrence of massive bleeding. Thus,
this patient was able to undergo emergency surgery instead of being referred
for embolization.
Embolization was performed in 34 patients and controlled the bleeding in 28. Of the remaining six patients, four needed reembolization, one died, and one underwent surgery.
Surgical Findings
Seventeen patients underwent surgery. Three patients underwent emergency
surgery, one after embolization failed and two after CT revealed an aortic
false aneurysm or a chest-wall hematoma fistulized into the bronchial tree.
The other 14 patients underwent surgery between 2 weeks and 3 months after the
episode of hemoptysis because all had localized lesions and were at risk for
recurrent bleeding.
Mortality
The overall mortality rate was 10%. It was higher among patients with
massive hemoptysis (26%, 6/23) than among those with large hemoptysis (4%,
2/57) (p < 0.05). The two deaths in the latter group both resulted
from surgical complications.
Of the six patients with massive bleeding who died, two had acute tuberculosis, one had postradiation sequelae, and one had a clotting disorder. In the remaining two patients, the cause of hemoptysis was unexplained.
Cause of Hemoptysis
In nine patients, the cause of hemoptysis was known at admission: seven
patients had bronchiectasis and two had cancer. The cause of hemoptysis was
subsequently identified in 63 patients (79%) and remained unknown in eight
patients (10%) either because death occurred before additional investigations
could be performed or because more than one potential cause was
identified.
Among the patients in whom the cause of bleeding was known or identified, 25 (31%) had bronchiectasis, 15 (19%) had acute tuberculosis (n = 4) or sequelae of tuberculosis (n = 11), and nine (11%) had tracheal or bronchial tumors. Eight patients (10%) had nontuberculous lung infection (six aspergillomas and two actinomycosis). Bleeding in the remaining 15 patients (19%) had various causes comprising clotting disorders (n = 6), postradiation lesions (n = 4), iatrogenic causes (n = 3), and vascular lesions (n = 2) (Table 4).
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Most of the patients with no known history of bronchiectasis had no obvious imaging signs even on CT (Fig. 2A,2B). Ten patients had minor bronchiectasis with localized ground-glass opacities. Two others had isolated ground-glass opacities with arteriographic hypervascularity at the same site. These two patients underwent surgery to prevent hemoptysis from recurring. Pathologic examination revealed bronchiectasis; however, bronchiectasis could not be identified on high-resolution CT even retrospectively. The last patient had a nodular lesion on CT with surrounding ground-glass opacities. In this patient, pathologic examination revealed the CT findings to be a mucoid impaction in a distal area affected by bronchiectasis.
None of the 15 patients with tuberculosis had normal findings on chest radiography. CT was performed in nine of these patients and showed only the cause of bleeding or both the site and the cause (Fig. 3A,3B,3C).
Chest radiography revealed abnormal findings in five of the seven patients with previously undiagnosed tumors and in the two patients with known bronchial carcinoma. CT identified all nine tumors, whereas bronchoscopy failed to identify three unknown peripheral tumors.
Chest radiography and CT revealed aspergilloma with abnormalities typical of fungus balls in one and four patients, respectively.
Patients with actinomycosis had nonspecific abnormalities, and the diagnosis was only obtained at surgery.
Of the 15 patients with miscellaneous causes of hemoptysis, six had clotting disorders. Chest radiography failed to show either the site or the cause of bleeding in four of these six patients, none of whom underwent CT. One of the three patients with bleeding of iatrogenic origin had a chest-wall hematoma that appeared after surgical resection of lung cancer. The chest-wall hematoma was depicted on CT and required further surgery. Hemoptysis occurred after fiberoptic bronchoscopy was performed to obtain a biopsy sample in the other two patients. Of these patients, CT showed the site of bleeding in one patient but not in the second patient.
Chest radiography revealed the bleeding site in three of the four patients with postradiation lesions. CT was performed only in the fourth patient. In this patient, CT scans showed traction bronchiectasis in the left upper lobe.
One of the two patients with vascular lesions had a pulmonary arteriovenous fistula. Chest radiography and CT only showed atelectasis, which was probably associated with a clot obstructing the bronchus, in the right lower lobe, and the vascular malformation was only diagnosed after surgical resection of the right lower lobe. Thus, imaging depicted only the site of bleeding in this patient. The second patient had a fissured aortic false aneurysm (Fig. 4) that was not seen on the bedside chest radiograph but was found on unenhanced and contrast-enhanced CT examinations. This patient successfully underwent surgery after CT instead of being referred for bronchial arteriography as initially planned.
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There are few recent published series in this setting, and none that focuses specifically on major hemoptysis [1,2,3,4,5,6]. We therefore reviewed the files of all patients admitted to our intensive care unit with large or massive hemoptysis during the last 5 years. The precise amount of expectorated blood was difficult to determine, but we confidently excluded patients with minor hemoptysis including those with alveolar hemorrhage or pulmonary embolism.
We separately analyzed the images and reports for patients with hemoptysis (n = 80). We arbitrarily defined large hemoptysis as less than 300 mL blood (n = 57) and massive hemoptysis as 300 mL or more of blood (n = 23).
The distribution of causes was similar in the two groups (Table 4). The mortality rate was higher among patients with massive hemoptysis (26%) and was comparable to that reported in another series [12]. Only two patients with large hemoptysis died; both died as a result of postoperative complications.
Bronchiectasis was the main cause of hemoptysis, accounting for 31% of the cases. We adopted a restrictive definition of bronchiectasis. We excluded forms of bronchiectasis that are associated with lesions resulting from tuberculosis or radiation. The frequency of bronchiectasis is probably underestimated in series that do not include diagnostic CT. For example, in a series that did not include CT [4], a high proportion of cases of bronchiectasis were attributed to bronchitis, but these cases probably in fact corresponded to bronchiectasis.
Tuberculosis and tumors were the second and third causes of hemoptysis, respectively, in our series, and nontuberculous infection (mainly aspergillomas in preexisting cavities) was the fourth cause. This hierarchy is similar to that reported in other series [12, 20].
Vascular lesions were observed in two of our patients. One patient had an arteriovenous fistula, which is associated with massive hemoptysis in 4% of the published cases [21]. The lesion in the other patient was caused by fissure of an aortic false aneurysm. Hemoptysis originating in the aorta is not rare; more than 150 cases have been reported during the last 10 years [22,23,24,25]. Hemoptysis that originates from the aorta is mainly seen in patients with a history of cardiovascular surgery and is fatal if untreated. Bronchial arteriography should not be performed in these patients given the extrabronchial bleeding source and the danger of selectively catheterizing a fragile aorta.
The cause of hemoptysis was not identified in eight (10%) of our 80 patients, a proportion similar to that previously reported [12]. Some of these cases in which CT showed only ground-glass opacities may in fact have corresponded to infraradiologic bronchiectasis.
The main objective of this retrospective study was to compare the contributions of chest radiography, CT, and bronchoscopy for identifying the site and cause of hemoptysis. The patients underwent a combination of chest radiography, fiberoptic bronchoscopy, bronchial arteriography, and chest CT.
Chest radiography was performed in every patient and showed normal findings in only 10 patients, seven of whom had bronchiectasis. Normal findings on chest radiography may therefore suggest bronchiectasis as the cause of bleeding. Chest radiography showed the cause of bleeding or both the site and the cause of bleeding in most of the patients with tuberculosis; however, chest radiography had a low diagnostic yield in patients with aspergillomas, a finding for which the superiority of CT is well established [26]. Thus, chest radiographs showing posttuberculous lesions in patients with severe hemoptysis should be followed by high-resolution CT to detect aspergillomas, which require specific treatment. Chest radiography also suggested the cause of hemoptysis in six of the nine patients with lung cancer. The value of chest radiography in this setting has already been reported and is explained by the fact that most tumors are advanced by the time they start to bleed [27].
Chest radiography located the site of bleeding in only 46% of our patients compared with 82% in the series of Hsiao et al. [28]. However, that series probably included cases that were more severe than ours because they studied patients who had been referred for embolization, whereas only 56% of our patients required this procedure. Inclusion of more severe cases could explain the discrepancy between our result and that of Hsiao et al. because abundant bleeding is more likely to produce alveolar abnormalities on chest radiographs. Another possible explanation for this difference is that we considered that chest radiographs had failed to reveal the bleeding site when the radiologic abnormalities due to the causal disease (specific abnormalities) were bilateral (e.g., sequelae of bilateral tuberculosis) even when they predominated on one side. Indeed, we believe that a lateral predominance of specific abnormalities does not show that bleeding originates from the affected side, contrary to nonspecific abnormalities.
CT was performed in 57 (71%) of our 80 patients and had the highest diagnostic yield. To the best of our knowledge, ours is the largest series of CT in patients with major hemoptysis. CT findings showed the cause of bleeding in 44 patients and only the site of bleeding in 10 patients. CT findings were normal in one patient and failed to show either the site or the cause of bleeding in only two patients.
Bronchoscopy is generally considered the first-line screening procedure for patients with severe hemoptysis. Bleeding can also be controlled when a rigid bronchoscope is used [29], but the use of this instrument makes the bleeding site more difficult to identify (43% of patients in the series of Knott-Craig et al. [20]). Immediate control of bleeding is better achieved with embolization [30].
CT and bronchoscopy located the site of bleeding in 70% and 73%, respectively, of the patients in this series. However, CT depicted the cause of bleeding more frequently than bronchoscopy (77% vs 8%, p < 0.001). CT successfully showed all previously unidentified lung tumors, whereas bronchoscopy failed to reveal three peripheral tumors. CT also enabled us to identify four of the five patients with aspergillomas and detected mild bronchiectasis in 10 patients with no previous diagnosis (we found that even minor bronchiectasis could induce severe bleeding). Furthermore, in one of our patients, bronchiectasis was found only at pathologic examination after surgery. It is well known that normal findings on high-resolution CT do not exclude bronchiectasis [31]. Our results suggest that apparently normal CT findings in a patient with major hemoptysis are suggestive of bronchiectasis because this imaging modality depicts most other lesions.
Because bronchiectasis, posttuberculous lesions, and aspergillomas accounted for more than half the causes of hemoptysis in our series, high-resolution CT appears to be the most appropriate imaging method for patients with major hemoptysis. Multidetector CT can obtain images of the entire thorax with millimetric slices in one apnea. Another major advantage of high-resolution CT is that it can reveal focal ground-glass opacities. These findings indicate the side of bleeding and are particularly valuable in patients with bilateral lesions. However, CT must be performed soon after the episode. One patient in this series was examined on CT 15 days after the bleeding episode, and the findings were normal.
Contrast enhancement seems unnecessary for the initial screening of patients with hemoptysis because even the aortic false aneurysm was visible on unenhanced images in this series. In addition, bronchial arteriography was subsequently required for 56% of our patients.
The limitations of this study are mainly related to its retrospective nature. In particular, the investigations were not standardized. Furthermore, some patients died shortly after admission and could not be fully examined. CT was not performed routinely, and high-resolution CT was not always available. However, millimetric slices were obtained whenever thick slices failed to depict the cause or the site of bleeding.
Pathologic confirmation of imaging findings was not systematically obtained. However, cancer, tuberculosis, aspergilloma, and postradiation lesions are well-known causes of hemoptysis. When observed, isolated bronchiectasis was assumed to be the cause of bleeding.
Because this study is retrospective, assessing the effect of the imaging modality on patient treatment is difficult. CT revealed previously undiagnosed bronchiectasis in 17 patients; 11 cases were localized and potentially resectable. CT also revealed three unknown peripheral tumors that were not detected on bronchoscopy and three aspergillomas that were not detected on standard chest radiography. Two patients underwent emergency surgery on the basis of CT findings: one for an aortic false aneurysm and the other for a chest-wall hematoma. CT obviated potentially dangerous bronchial arteriography in the patient with the aortic aneurysm. Thus, the CT findings directly influenced the treatment of at least 25 patients.
As in previous studies, the two main causes of major hemoptysis in this series were bronchiectasis and tuberculosis. The cause was not found in 10% of the patients. Chest radiographs rarely revealed normal findings, but normal radiographic findings suggested bronchiectasis as the cause of bleeding. Most of the tuberculous and tumoral lesions in this series were apparent on chest radiographs. Chest radiography was less useful than bronchoscopy for localizing the bleeding, whereas CT was as efficient as bronchoscopy, showing focal ground-glass opacities, localized lesions, or both. The site of ground-glass opacities and bronchial hypervascularity on arteriography correlated well, particularly in patients with bronchiectasis. As previously shown in series dealing with nonmassive hemoptysis, bronchoscopy was less efficient than CT in detecting lung cancer as the cause of bleeding, and the global diagnostic value of bronchoscopy was lower than that of CT.
Our results indicate that emergency highresolution CT can help in the treatment of patients with major hemoptysis because CT yielded the cause in 77% of our patients and located the bleeding as efficiently as bronchoscopy. Locating the bleeding site using CT can assist with embolization, which is the best procedure for immediate control of bleeding in most patients. Moreover, CT obviates bronchial arteriography when it shows an extrapulmonary site of bleeding (twice in our series).
In conclusion, the results of this retrospective study suggest that CT can replace bronchoscopy as the first-line investigation for patients with large or massive hemoptysis, but these results need to be confirmed in a prospective multicenter study.
Acknowledgments
We thank G. Chatellier for his help with the statistical analysis,
Christelle Largenton and Joelle Bauvillard for their help in preparing the
manuscript, and David Young for editorial assistance.
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