Imaging and Interventional Radiological Treatment of Hemoptysis

REVIEW ARTICLE

ACTA RADIOLOGICA

Imaging and Interventional Radiological Treatment of Hemoptysis P. E. ANDERSEN Department of Radiology, Cardiovascular Section, Odense University Hospital, Odense, Denmark Andersen PE. Imaging and interventional radiological treatment of hemoptysis. Acta Radiol 2006;47:780–792. Hemoptysis is coughing up blood originating from the lower respiratory tract. There are multiple causes of hemoptysis, from airway diseases, parenchymal diseases, cardiovascular diseases, and other causes. Hemoptysis may cease temporarily, but a possible lifethreatening condition may still be present, requiring complete evaluation and probably treatment. Massive hemoptysis (w300 ml blood in 24 hours) seldom occurs but has high mortality. Diagnostic examinations include patient history, physical examination, bronchoscopy, laboratory tests, chest X-ray, computed tomography (CT) of the chest, pulmonary angiography, aortography, and angiography of the bronchials and other thoracic systemic arteries. Bronchoscopy together with clinical and radiological examinations indicates from which part of the lung the bleeding is occurring, yet the cause of hemoptysis cannot be determined in 20–30% of cases. One of the therapeutic measurements may be embolization of the bleeding vessel such as in pulmonary arteriovenous malformations or in bronchial or other systemic arterial branches supplying the bleeding lung segment. Systemic bronchial and non-bronchial collateral artery anatomy is very complex and variable, and it may be difficult to recognize how the systemic arteries or pulmonary arteries may be involved as a source of bleeding. Interventional treatments are effective and safe therapeutic methods which reduce the need for acute thoracic surgery. Embolization may be life saving, or it may postpone surgery and, in some situations, should be the treatment of choice. Key words: Bronchial arteries; hemoptysis; pulmonary arteriovenous malformations; therapeutic embolization Poul Erik Andersen, Department of Radiology, Cardiovascular Section, Odense University Hospital, Sdr. Boulevard, DK-5000 Odense C, Denmark (tel. +45 6541 2188, fax. +45 6590 7244, e-mail. [email protected]) Accepted for publication 26 May 2006

Hemoptysis is coughing up blood originating from the (lower) respiratory tract. Many patients are referred to chest radiography because of mild hemoptysis, which is a rather common symptom. In these cases, the underlying cause is most often benign. Hemoptysis may, however, indicate a severe life-threatening process and require further evaluation, and major hemoptysis is life threatening in itself, with a high mortality. Etiology There are multiple causes of hemoptysis, such as airway diseases, parenchymal diseases, vascular diseases, and other causes (Table 1) (1, 31). It is important to exclude differential diagnosis such as bleeding from the nose, mouth, and pharynx, hematemesis, and false hemoptysis (aspiration of blood).

The most common cause of hemoptysis is a (mild) bronchitic infection with ruptured small blood vessels caused by coughing, determined by normal chest X-ray. In 60–70% of mild hemoptysis, the underlying disorder is benign and the hemoptysis may cease temporarily or permanently, but a possible life-threatening process may still be present, requiring a complete evaluation. The etiology of hemoptysis cannot be determined in 20–30% of cases (cryptogenic hemoptysis) (23), but should (probably) be monitored for years. In approximately 90% of these individuals, hemoptysis will settle spontaneously within 6 months. When chest radiograph is normal or non-localizing, the prevalence of malignancy is low (v5%). Worldwide, tuberculosis is the most common cause of hemoptysis, while bronchiectasis, bronchitis, and bronchogenic carcinoma account for most cases in the western world (20), with a relative DOI 10.1080/02841850600827577

# 2006 Taylor & Francis

Imaging and Treatment of Hemoptysis Table 1. Causes of hemoptysis Airway diseases N Bronchitis N Bronchiectasis N Pulmonary neoplasm (bronchogenic carcinoma) N Other bronchial tumors (e.g., carcinoid, adenoma) Parenchymal diseases N Tuberculosis N Lung abscess N Pneumonia (e.g., klebsiellae, staphylococci) N Aspergillosis N Sarcoidosis N Cystic fibrosis N Infected sequestration N Goodpasture’s syndrome N Wegener’s granulomatosis N Hemosiderosis N Infected bronchogenic cyst Cardiovascular diseases N Vascular malformations (PAVM) N Pulmonary embolism N Left heart failure N Mitral valve stenosis N Pulmonary hypertension (Eisenmenger) N Thoracic aorta aneurysm/dissection N Pulmonary artery aneurysm N Polyarteritis Others N Bleeding tendencies—coagulopathy N Medication (anticoagulation, acetylsalicylic acid, cocaine, etc.) N Foreign body N Trauma

increase in bronchial carcinoma in recent years. In older patients >60 years, the main cause of hemoptysis is bronchogenic carcinoma (45). The most common cause of massive hemoptysis is benign rather than malignant disease (30). Diagnosis There is no consensus on diagnostic strategy, but patients with newly developed hemoptysis should generally be examined with chest X-ray, bronchoscopy, and probably computed tomography (CT) of the chest (6, 16). In about 25–30% of cases of mild hemoptysis, bronchoscopy fails to locate the source of bleeding (13), and 20–30% of patients have a normal chest radiograph (23). In mild, first-time hemoptysis, a chest X-ray should be performed. If it is normal and the patient is at low risk for malignancy, the patient should be observed without further examinations. If the patient is at risk of malignancy, or if the hemoptysis recurs, CT of the chest and bronchoscopy should be performed. Diagnosis is directed towards the cause, the location, and the extent of bleeding, which may be mild (bloodstained sputum) or massive, i.e. w200– 300 ml/24 hours. Massive hemoptysis is life threatening (23, 24, 30) and has a very high mortality of

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w50% (9, 40). Less than 5% of all cases of hemoptysis are massive. These are, however, of great medical importance as they are emergencies in which the risk to life is asphyxiation (17). In massive hemoptysis, chest film and CT of the thorax may be without diagnostic value because of aspiration of blood to other parts of the lungs. CT plays a major role in imaging the mediastinum, bronchiectasis, and peripheral masses, and a definitive role in the staging of cancers. Multislice CT, compared to conventional angiography, has been shown to provide as good or better depiction and traceability of the bronchial arteries in patients with hemoptysis, and in most patients CT enables detection of the bronchial and non-bronchial arteries causing hemoptysis (34, 48, 49). CT also discloses, with very high sensitivity, pulmonary artery aneurysms and pulmonary arteriovenous malformations. Intravenous contrast is not needed in these cases. Recommendations of the American College of Radiology (ACR) state that ‘‘initial evaluation should include chest X-ray. Patients with less than two risk factors for malignancy (male, w40 years old, w40 pack/year smoking history) and negative chest X-ray can be followed with observation. CT and bronchoscopy are complementary examinations in patients presenting with either two or more risk factors for malignancy or persistent or recurrent hemoptysis and a negative chest X-ray. In patients with two or more risk factors and positive chest X-ray, CT is suggested for initial evaluation.’’ It is also recommended by others that CT should be used as the primary investigation in patients with normal or non-localizing chest radiograph, and CT should be performed prior to bronchoscopy in patients in whom chest radiograph is abnormal or suggestive of malignancy (12, 47). When interventional treatment is indicated, chest X-ray, chest CT angiography, and bronchoscopy will most often indicate from which lung and lung segment the bleeding arises, and whether the bleeding is from a systemic or pulmonary artery. In systemic arterial bleeding, the examination is usually initiated with a thoracic aortography followed by a bronchial angiography. If the bronchial arteries are normal, other systemic arteries which may be the source of bleeding should be examined primarily on the suspected side. If no pathologic arteries are found, a pulmonary angiography should be considered. If the pulmonary arteries, evaluated from patient history and objective examinations, are the most likely bleeding sources, a pulmonary angiography should be performed. If the pulmonary arteries are normal, examination of the systemic arteries on the relevant side should be considered. Acta Radiol 2006 (8)

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Treatment In massive hemoptysis or less-than-massive but socially or physically invalidating recurrent hemoptysis there is indication for treatment. The treatment of hemoptysis in the acute phase aims at localizing and controlling the bleeding and the underlying cause. This can be achieved by therapeutic bronchoscopy (e.g., laser coagulation, fibrinogen or thrombin installation, or treatment with ice), endobronchial balloon occlusion, embolization of the bronchial arteries and other arteries from the systemic circulation or pulmonary arteries (16), aortic endoprosthesis implantation, or surgical repair or pulmonary resection (which in acute cases has a mortality rate of 15–30%, higher in aorta repair) (18, 20). Many patients are not candidates for surgical resection because of bilateral disease, inadequate respiratory reserve (20), or other organ failure. Embolotherapy and endovascular repair are options in these cases. In recurrent hemoptysis, it is an advantage to treat in a non-bleeding, non-acute phase. Treatment of hemoptysis in malignant diseases is controversial and should be considered in each case. The logistic requirements for performing elective or acute embolization include: digital (biplanar) angiographic equipment, an on-call embolizationdedicated radiologist and radiography team, embolization materials and a variety of different catheters in stock, standardized management protocols, and an intensive care unit.

Fig. 1. Aortography showing parenchymal staining in the left apical segment, from where the bleeding came, as demonstrated by bronchoscopy.

flow-stop, avoiding regurgitation of the microparticles to other non-intended arterial branches. It is important to use microparticles, which are sized

Bronchial arteries and other arteries from the systemic circulation Bronchial artery embolization (BAE) was introduced in 1974 as a minimally invasive treatment of hemoptysis when the hemoptysis originated from the bronchial arteries (33). There is indication for BAE when conservative, medical treatment fails, in massive hemoptysis when surgery is not indicated, recurrent hemoptysis in patients with bilateral, widespread disease, or (rarely) to control the bleeding as a temporary measure before operation (24, 35). BAE is often preceded by aortography, which may indicate from which part of the lungs the bleeding comes (Fig. 1). BAE is then performed using coaxial microcatheters, and embolization is performed through end-hole catheters using microparticles, spongostan, or the deployment of microcoils in larger-sized bleeding arteries (11, 39) (Figs. 2–4). Microparticles are injected slowly until Acta Radiol 2006 (8)

Fig. 2. Bronchial angiography: one short main stem dividing into a right and a left bronchial artery.

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Fig. 3. A. Microcatheter in the left bronchial artery (arrow). B. Bronchial angiography after embolization with microparticles: distal flow stop.

according to the terminal arterial branches intended to be embolized. There is great variation in normal bronchial artery anatomy. Most often, the origin of the right bronchial artery is from the posterior or lateral wall of the aorta, while the other bronchial arteries arise from the anterior wall of the descending thoracic aorta at levels Th5–Th6. One right bronchial artery and one or two left arteries is most common. Further, a common bronchial trunk or intercostobronchial trunk are frequently seen (23, 28, 41). All systemic arteries suspected of being bronchial feeders (the source of hemoptysis) should be evaluated, starting with the bronchial arteries on the suspected bleeding side, but also the intercostal arteries, internal thoracic/mammary arteries (Figs. 5 and 6), and other branches from the subclavian and axillary arteries (Figs. 7 and 8C) as well as the inferior phrenic and left gastric arteries (Fig. 8D) (12, 18, 26, 36, 47). In principle, all systemic arteries in the chest may contribute to the bronchial circulation. About one third of patients with hemoptysis have a non-bronchial systemic artery contribution (12). Disclosing the source of hemoptysis may be a challenge and very time consuming. The most important diagnostic signs in pathologic, bleeding systemic arteries are: hypervascularity (hypertrophy, tortousity), (pseudo) aneurysms, capillary stasis, parenchymal staining, systemic-topulmonary vascular shunts, and contrast extravasation (into the airways) (Figs. 1–4) (38). These

findings are also often present without actual bleeding, and it is advantageous to perform embolization electively when acute massive bleeding is not occurring. Technical success in BAE is achieved in about 90% of cases, and it controls the bleeding in 66–90% of cases in the short term (1 month) (10, 38, 42, 50), but late recurrent hemoptysis (after 6–12 months) is seen in 20–40% of cases (10, 11, 23, 25, 32). Persistent hemoptysis or early re-bleeding after technically successful BAE is usually due to a failure to recognize the involvement of other bronchial arteries or of non-bronchial systemic vessels which were not identified and occluded in the first place. Late re-bleeding is generally due to disease progression (24). Bleeding from pulmonary arteries must be suspected if the bronchial and other systemic arteries are angiographically normal or if embolization of the systemic—including bronchial—arteries fails to detain the bleeding (29). In patients with hemoptysis due to aspergilloma, better results may be achieved by combining embolization with percutaneous intracavitary installation of antifungal agents. It is very important to identify spinal arteries and to place the microcatheter distally to their orificia, and to inject the embolization microparticles very slowly to avoid retrograde embolization of the spinal arteries. Knowledge of the anatomy of the bronchial and other systemic arteries in the chest and experience in endovascular techniques are Acta Radiol 2006 (8)

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B Fig. 4. A. Pathologic, bleeding bronchial artery: vascular hypertrophy, tortousity, and shunting to veins (arrow). B. Flow stop after embolization with microparticles.

crucial to avoid and reduce undesired side effects and complications. Complications after BAE are few and seldom. Spinal cord injury—transverse myelitis—is seen in v1% because of accidental occlusion of the intercostal and spinal arteries, and is the most important. Other possible complications are esophageal ulceration, stroke, bronchial infarction, and transient chest pain. BAE has become a Acta Radiol 2006 (8)

well-established, first-line, minimally invasive treatment modality for massive hemoptysis. It is an effective means of controlling hemoptysis in many patients (5, 7, 8, 10–12, 26, 35, 38, 42, 43, 46, 50), with lower mortality and morbidity than after surgery (16, 18, 20) and with significantly better results than after medical treatment alone (37). Further, there may be economic advantages in favor of BAE.


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Fig. 5. Left internal mammary artery with collaterals to the bronchial system (arrow).

Aorta Aortobronchial fistula, as seen in thoracic aorta aneurysm or dissection, is a rare condition that may give rise to hemoptysis. Untreated, it has a mortality rate close to 100% (21) and an operative mortality of about 15%. Endoluminal stent-graft treatment with sealing of the tear is an attractive alternative to surgical repair with lower mortality and complications (Fig. 9) (4, 14). The method was first employed in 1994, and has since been used increasingly with the development of better-designed stent grafts. Pulmonary arteries In about 5–10% of hemoptysis, the cause has a pulmonary arterial source. Most common is false pulmonary artery aneurysm (Rasmussen aneurysm) in association with cavernous tuberculosis. Coil embolization may be a treatment option in these cases (27). Pulmonary arteriovenous malformation (PAVM) is a direct connection between the pulmonary artery and vein through an aneurysm. This functions as a pulmonary capillary bypass, shunting the blood from pulmonary arteries to pulmonary veins, and thus causing a right-to-left shunt. This may give paradoxical cerebral emboli (TCI, stroke, cerebral abscess), decreased oxygenation of the blood (exercise intolerance), and the PAVM may rupture

(pulmonary hemorrhage with hemoptysis or hemothorax) (2, 3, 15, 19, 22, 44). The risk of rupture is increased during pregnancy, and the bleeding may be lethal. Ten to fourteen percent of patients with PAVMs have had hemoptysis. Thus, PAVMs may give corresponding clinical symptoms like those listed in Table 2. The indications to treat are to prevent cerebral stroke and abscess, to reduce the shunt and raise the function level, and to prevent rupture of the PAVM. Seventy-five to ninety percent of PAVMs are associated with hereditary hemorrhagic telangiectasia (HHT) (Table 3). HHT has a prevalence of 10–20/100,000, and about 25– 30% of patients with HHT have PAVM. The PAVM diagnosis is based on history, clinical examination, chest radiograph, arterial blood gases, contrast (bubble) echocardiography, CT (without contrast), and pulmonary angiography. There is a generally accepted indication to treat PAVMs with feeding arteries bigger than 2 mm. The treatment is embolization of the pulmonary artery feeding the PAVM with balloons or coils as close to the PAVM as possible to save the normal vessels as much as possible (Fig. 10). This treatment has now replaced surgery. Technical success is achieved in close to 100% of cases, and clinical improvement is seen immediately after embolization because of increasing oxygenation. Complications and adverse reactions are few and mostly temporary. Most often, pleuritis (15–30%), slight fever, and more rarely angina pectoris are Acta Radiol 2006 (8)

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B Fig. 6. A. Right internal mammary artery with large collaterals to the bronchial system. The vessels are tortous, hypertrophic, and there is venous shunting (arrow). B. After embolization of the right internal mammary artery with microcoils there is flow stop in the collaterals to the bronchial system (arrow).

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B Fig. 7. A. Pathological vessels from the left subclavian artery to mediastinal tumor and the bronchial system. B. After embolization with coils, both via the femoral and the brachial arteries: total flow stop.


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Fig. 8. A. Left internal mammary artery with large systemic collaterals via mainly intercostal arteries to bronchial and pulmonary arteries with venous shunting (arrow). B. Same patient as Fig. 8A. Large left subscapular/lateral thoracic artery with intrapulmonary venous shunting (arrows). C. Same patient as Figs 8A and B. Large left dorsal thoracic artery with intrapulmonary venous shunting (arrow). D. Same patient as Figs. 8A–C. Supply from left gastric artery to same pulmonary segment (arrows).



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Fig. 9. A. Aortobronchial fistula from proximal lateral wall of descending aorta (arrow). B. After deployment of endoluminal stent graft, the fistula is sealed. Table 2. Symptoms in pulmonary arteriovenous malformations (PAVMs) Exertional dyspnea (40–70%) Migraine (40–50%) Cerebrovascular accident (20–35%) Transient ischemic attack (15–40%) Hemoptysis (10–14%) Asymptomatic (10%)

Table 3. Hereditary hemorrhagic telangiectasia (HHT) (OslerWeber-Rendu disease) Telangiectasias (buccal mucosa, palate, tongue, conjunctiva, fingers) Epistaxis (90%) Autosomal dominant Gastrointestinal bleeding (33%) PAVM (25–30%) Cerebral AVM Liver AVM Spinal AVM

seen. No mortality in relation to the embolotherapy of PAVMs has ever been reported. Embolization is a well-established, minimally invasive method for treating PAVMs, and it is a

safe and lung-preserving treatment with relatively few transient complications (2, 3, 15, 19, 22, 44). Embolization of PAVM is considered the first-line treatment in these patients. Patients with HHT should be screened for PAVM. Conclusion In minor first-time hemoptysis in patients with less than two risk factors for pulmonary malignancy, a chest film should be taken. If it is negative, the patient should be followed with observation. In patients with a positive chest film, recurrent hemoptysis, or two or more risk factors for malignancy, CT and bronchoscopy should be performed. Multislice CT angiography and MR angiography are new modalities with great potential to provide more precise diagnostic information about the source of bleeding. Intravascular intervention is an option in many cases of recurrent or massive hemoptysis and in some cases the first-line treatment. Embolization Acta Radiol 2006 (8)

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Fig. 10. A. Pulmonary arteriovenous malformation in the left lower lobe in a patient with severe hemoptysis (arrow). B. Selective catheterization of the feeding artery to the PAVM. C. After embolization of the feeding artery with coils (arrow).

may be life saving in acute massive hemoptysis, and offers better long-term control of recurrent minor bleeding and better quality of life than medical therapy alone. Embolization is an effective, safe, minimally invasive therapeutic approach that reduces the need for high-risk acute thoracic surgery. Knowledge of vascular anatomy and embolization techniques is necessary (26), Acta Radiol 2006 (8)

and logistic requirements need to be further optimized. References 1. Abal AT, Nair PC, Cherian J. Haemoptysis: aetiology, evaluation and outcome – a prospective study in a thirdworld country. Respir Med 2001;95:548–52.

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