REVIEW ARTICLE
The Clinical Respiratory Journal
Successful embolization in childhood hemoptysis due to abnormal systemic arterial bleeding of the lung and review of the literature Tugba Sismanlar1, Ayse T. Aslan1, Koray Akkan2, Emetullah Cindil2, Baran Onal2 and Beyza Ozcan3 1 Department of Pediatric Pulmonology, Gazi University Hospital, Ankara, Turkey 2 Department of Radiology, Gazi University Hospital, Ankara, Turkey 3 Department of Neonatology, Etlik Zubeyde Hanım Eg˘itim ve Aras¸tırma Hospital, Ankara, Turkey
Abstract Background and Aims: Hemoptysis in children is a rare but potentially lifethreatening symptom of an underlying respiratory tract abnormality. Hemoptysis, when massive and untreated, has a mortality rate of more than 50%. With interventional radiological procedures and surgery, this rate has dropped to 7%–18%. The experience with bronchial arterial embolization in childhood is very limited; only a few case reports with short-term follow-up have been reported. Methods: We report herein two patients with massive hemoptysis due to abnormal systemic arterial bleeding of the lung; neither patient had any lung or systemic disease. In both cases, the bleeding was controlled with endovascular embolization. The first case had bronchopulmonary arterial anastomosis and represents the first reported case with this anomaly. The second case had recurrent massive hemoptysis due to bronchial artery bleeding, and repeat embolization was performed. Results: Both of these children had rare vascular anomalies without parenchymal lung disease and were treated successfully with bronchial arterial embolization. Conclusion: Massive hemoptysis due to abnormal systemic bleeding of the lung in the absence of parenchymal disease is an uncommon and severe symptom in childhood. Embolization can be a treatment option in children with abnormal vasculature bleeding and can be repeated safely when needed. Please cite this paper as: Sismanlar T, Aslan AT, Akkan K, Cindil E, Onal B and Ozcan B. Successful embolization in childhood hemoptysis due to abnormal systemic arterial bleeding of the lung and review of the literature. Clin Respir J 2015; ••: ••–••. DOI:10.1111/crj.12289.
Key words bronchial artery embolization – children – hemoptysis – treatment Correspondence Tugba Sismanlar, MD, Department of Pediatric Pulmonology, Gazi University Hospital, Bes¸evler, Çankaya, 06500 Ankara, Turkey. Tel: +90312 2027597 Fax: +903122150143 email: [email protected] Received: 18 August 2014 Revision requested: 23 January 2015 Accepted: 01 March 2015 DOI:10.1111/crj.12289 Authorship and contributorship TS designed the study and wrote the paper. ATA analysed and interpreted the data and wrote the paper. KA, EC and B Ozcan contributed important reagents and performed the study. B Onal performed the study and analysed and interpreted the data. Ethics Written consents were obtained from the parents. Conflict of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
Introduction Hemoptysis in children is a rare but potentially life-threatening symptom of an underlying respiratory tract abnormality. Hemoptysis, when massive and untreated, has a mortality rate of more than 50% (1).
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
With interventional radiological procedures and surgery, this rate has dropped to 7%–18% (2). The lungs have a dual blood supply. They receive deoxygenated blood from the right ventricle via the pulmonary arteries. The blood is oxygenated and returned back to the heart via the pulmonary veins.
1
Embolization in childhood hemoptysis
Sismanlar et al.
The other source of blood supply is from the systemic circulation via the bronchial arteries. As a rule, there is one bronchial artery to the right lung that arises as a branch of the first intercostal artery. On the left, there are usually two arteries, arising directly from the descending thoracic aorta. They drain mostly via the pulmonary veins to the left atrium (3). The presence of anomalous arterial collateral supply to normal lung segments is well-reported in adults, but is much less common in children (4). We report herein two patients with massive hemoptysis due to abnormal systemic arterial bleeding of the lung; neither patient had any lung or systemic disease. Bleeding was controlled with bronchial arterial embolization (BAE).
Case 1 An 8-year-old boy was admitted with massive hemoptysis after coughing. His physical examination was normal. He had no prior history of pulmonary or cardiac disorders. He had normal complete blood count (CBC) and clotting studies. He had a normal rhinoscopy, upper airway examination and gastrointestinal tract endoscopy. He had negative serology for antinuclear cytoplasmic antibody (ANCA), antiglomerular basement membrane antibody (AGBMA), antinuclear antibody (ANA), anti-DNA, and rheumatoid factor (RF), and negative tuberculin skin test (TST). His chest X-ray was normal. Computed tomog-
(A)
(B)
raphy (CT)-angiography scan of the chest showed parenchymal consolidation in the right lower lobe, which was thought to be secondary to parenchymal hemorrhage. Selective right bronchial angiogram demonstrated a dilated lower bronchial artery and hypervascularity in the localization of lesions, compatible with the thoracic CT angiography, and common bronchopulmonary arterial anastomosis was detected. After catheterization with a 5Fr Cobra catheter, a 2.8Fr microcatheter was advanced into the right bronchial artery. Embolization was performed with polyvinyl alcohol (PVA) particles (250–355 μm in diameter). After the procedure, filling of the fistula disappeared, and pruning of bronchial artery branches was observed (Fig. 1). No complication was observed after the procedure. The patient has been followed for 26 months without hemoptysis.
Case 2 A 7-year-old girl presented after coughing up approximately 500 mL of fresh blood. She had been coughing up blood intermittently for 2 months. She had tachycardia and was pale. Her breath sounds were decreased in the right hemithorax. She had normal CBC, clotting tests and normal serology for ANA, RF, ANCA, AGBMA and anti-DNA. The rhinoscopy and upper airway examination were normal. On her chest roentgenogram, infiltration was seen in the right lower lobe. Descending thoracic aortogram and
(C)
Figure 1. (A) Selective right bronchial arteriogram shows hypervascularity, neovascularity and shunting into the pulmonary artery (arrows) in the paracardiac region. (B) Microcatheterization stage (arrow) through diagnostic catheter to prevent involuntary embolization. (C) Post-embolization arteriography demonstrates early cessation of the right bronchial artery and devascularization of the right paracardiac region (arrows). Note the disappearance of the right pulmonary artery filling through shunting.
2
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Sismanlar et al.
Embolization in childhood hemoptysis
(A)
(B)
(C)
(D)
Figure 2. (A) Initial selective right bronchial arteriogram shows hypervascularity and neovascularity in the paracardiac region (arrow). (B) Rebleeding bronchial arteriogram at the 14th month. Note the prominent pulmonary artery shunting (arrow). (C) Glue cast after embolization with N-butylcyanoacrylate-lipiodol mixture (black arrows). (D) Devascularized right paracardiac region after embolization (black arrows).
selective right bronchial angiogram demonstrated a hypertrophied tortuous bronchial artery with an area of hypervascularity and neovascularity. After catheterization with a 5Fr Cobra catheter, a 2.8Fr microcatheter was advanced into the right bronchial artery. Embolization was performed with PVA particles (355–500 μm in diameter). The follow-up angiogram demonstrated devascularization of the right bronchial artery. No complication was observed after the procedure. She was followed without hemoptysis for an extended period; however, she was admitted with massive hemoptysis 14 months later. Right bronchial artery angiography revealed revascularization with shunting into the pulmonary artery. For embolization, 0.5 mL of N-butyl-cyanoacrylate (NBCA) (Histoacryl, B. Braun Aesculap, Tuttlingen, Germany) was mixed with iodized oil (Lipiodol Ultra-Fluide, Guerbet, Aulnay-Sous-Bois, France) in a 1:2 ratio to make it fluoroscopically visible and to delay the polymeriza-
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
tion of the metal coils. Embolization with that mixture produced an immediate devascularization with the cessation of shunting into the pulmonary artery (Fig. 2). She has been followed for 42 months without hemoptysis.
Discussion Our first case had dilated bronchial artery and bronchopulmonary arterial anastomosis. To our knowledge, he represents the first case with massive hemoptysis due to bronchopulmonary arterial anastomosis that was treated successfully with embolization. The second patient had recurrent massive hemoptysis, attributed to bleeding from a normal bronchial artery that supplied a normal lung. There was no shunting into the pulmonary artery or vein or bronchial artery aneurysm. Only two patients with hemoptysis with normal bronchial artery supplying a normal lung have 3
Embolization in childhood hemoptysis
been reported (5, 6). Neither of our cases had any lung or systemic disease, and their anomalies are rare and unique. According to the literature, there have been only a few patients with hemoptysis due to abnormal systemic arterial bleeding, in the absence of lung or systemic disease, who were treated successfully with embolization. Both Sharifi et al. (7) and Chung et al. (8) described an 11-year-old girl with pulmonary and bronchial arteriovenous malformation supplied by the bronchial artery. Sheikh et al. (5) reported an 11-yearold boy with abnormal ‘blushing’ from the bronchial artery, and Arranz Arana et al. (6) reported an 11-yearold girl with bleeding from a hypertrophied bronchial artery. Abdulhamid and Forbes (4) reported five patients aged 7–15 years with aberrant systemic arteries from the aorta, right iliac artery, and left/right internal mammary artery. The longest follow-up time after BAE without complication was reported as 2 years. These cases and our cases are summarized in Table 1. Massive hemoptysis, also known as life-threatening hemoptysis, is a serious, critical condition that necessitates urgent assessment and treatment of the patient. Despite advances in the treatment of massive hemoptysis, it continues to represent a high-risk condition. Conservative medical treatment of patients with expectoration of 300–600 mL of blood per day is associated with mortality in 50%–100% of the patients affected (9), with asphyxia rather than hemorrhage commonly being the cause of death (10). Although surgical treatment of massive hemoptysis is associated with mortality rates ranging from 7.1% to 18.2%, the rate can reach 40% when surgery is performed urgently (2).
Sismanlar et al.
BAE has become a well-established vascular interventional technique in the management of massive and recurrent hemoptysis (11). The mode of action is the occlusion of systemic arterial inflow to the fragile vessels within inflammatory tissue, reducing the perfusion pressure and the likelihood of further bleeding (12). A number of embolic materials such as absorbable gelatin sponge, PVA, metal coils and NBCA are available for BAE. It is important to avoid embolic material that can pass through abnormal bronchopulmonary anastomoses, as there is a risk of pulmonary infarction via bronchial artery–pulmonary artery shunts or systemic artery embolization via bronchial artery pulmonary vein shunts. Bronchopulmonary anastomoses of up to 325 μm have been demonstrated in an anatomical study (13), and thus embolic materials with less than this diameter should not be used in BAE in adults. The smaller materials are reported to be used in selected patients and children (14–17). Our patients were 7 and 8 year olds, because of diameters of bronchial arteries were smaller than adults, smaller sized embolic materials were used. Otherwise, with the use of larger materials, it would cause the proximal embolization. Superselective embolization has been shown to reduce the risk of inadvertent embolization of the anterior medullary artery by embolization of more terminal branches of the bronchial artery beyond the origin of the spinal arteries (18). When performing embolization with NBCA, as in our second case, special care must be taken to avoid inadvertent embolization. NBCA has the ability to pass through an anastomosis of any size. Thus, the presence of an anterior medullary artery anastomosis must be searched carefully, and
Table 1. Clinical features of patients with abnormal systemic arterial bleeding of the lung treated with embolization
Case 1 Case 2 Sharifi et al. (7) Chung et al. (8) Sheikh et al. (5) Abdulhamid and Forbes (4)
Arranz Arana et al. (6)
Age
Sex
Anomaly
Procedure
Recurrence
Follow-up
8 7 11 11 11 7
M F F F M F
BAE BAE BAE BAE BAE BAE
No Yes (after 14 months) – – No Yes (after 5 years)
26 42 – – 18 15
13 15
M F
BAE BAE
No No
18 months 18 months
7 10 11
M F F
Bronchopulmonary arterial anastomosis Bronchial artery Bronchial AVM supplied by bronchial artery Pulmonary AVM supplied by bronchial artery Bronchial artery Aberrant systemic arteries from aorta and subclavian junction Aberrant systemic arteries from LIMA Aberrant systemic arteries from RIA, aorta, RIMA Aberrant systemic arteries from aorta Aberrant systemic arteries from aorta Aberrant bronchial artery from aorta
BAE BAE BAE
No Yes (after 5 months) –
2 years 4 months –
months months
months months
AVM, arteriovenous malformation; BAE, bronchial arterial embolization; LIMA/RIMA, left/right internal mammary artery; RIA, right iliac artery.
4
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Sismanlar et al.
transcatheter embolization must be performed by experienced operators who are familiar with the use of NBCA. BAE appears to be effective, although there may be some side effects, the most common of which are pleuritic chest pain, fever, leukocytosis, dysphagia, post-embolism syndrome (lasting 5–7 days), and treatment with analgesics and narcotics, if necessary. Bronchoesophageal fistula as a complication resulting in more severe stenosis or bronchial wall necrosis may develop, but it has been reported very rarely (19, 20). However, we did not observe any complications in the two cases presented herein. Embolization can be repeated if needed. Abdulhamid and Forbes (4) repeated embolization in their two patients. In one case, embolization was repeated 5 years later and in the other case 5 months later. Our second case experienced repeat massive hemoptysis, and embolization was repeated 14 months after the first procedure. She has had no complaints in the 42 months of follow-up since the second embolization. This case represents the longest follow-up after repeat embolization reported in the literature. Massive hemoptysis due to abnormal systemic bleeding of the lung in the absence of parenchymal disease is an uncommon and severe symptom in childhood. Although there may be some complications, embolization can be a treatment option in children with abnormal vasculature bleeding. It is a safe procedure when performed by experienced operators and can be repeated safely when needed.
References 1. Samara KD, Tsetis D, Antoniou KM, Protopapadakis C, Maltezakis G, Siafakas NM. Bronchial artery embolization for management of massive cryptogenic hemoptysis: a case series. J Med Case Rep. 2011;5: 58–63. 2. Fernando HC, Stein M, Benfield JR, Link DP. Role of bronchial artery embolization in the management of hemoptysis. Arch Surg. 1998;133: 862–86. 3. Hubail Z, Eapen R, Lemler M. Anomalous systemic arterial supply to the lungs: an unusual etiology for cardiomegaly. Pediatr Cardiol. 2006;27(5): 608–11. 4. Abdulhamid I, Forbes T. Severe hemoptysis from dilated systemic aberrant arteries supplying normal lung segments. Pediatr Pulmonol. 2004;38(6): 477–82. 5. Sheikh S, Sisson B, Senler SO, Eid N. Moderate hemoptysis of unknown etiology. Pediatr Pulmonol. 1999;27(5): 351–5.
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Embolization in childhood hemoptysis
6. Arranz Arana L, Nogués Pérez A, Mendiola Ruiz R, Loyola Echaniz F. Life threatening hemoptysis and aberrant bronchial artery. A case report. An Pediatr (Barc). 2011;74(3): 182–6. 7. Sharifi M, Messersmith R, Newman B, Chung Y, Lakier JB. Bronchial arteriovenous malformation in a child with hemoptysis. A case report. Angiology. 1996;47(2): 203–9. 8. Chung Y, Ahrens WR, Singh J. Massive hemoptysis in a child due to pulmonary arteriovenous malformation. J Emerg Med. 1997;15(3): 317–9. 9. Najarian KE, Morris CS. Arterial embolization in the chest. J Thorac Imaging. 1998;13: 93–104. 10. Remy J, Voisin C, Ribet M, Dupuis C, Beguery P, Tonnel AB, Douay B, Pagniez B, Denies JL. Treatment, by embolization, of severe or repeated hemoptysis associated with systemic hypervascularization. Nouv Presse Med. 1973;2: 2060–8. 11. Chun J-Y, Morgan R, Belli A-M. Radiological management of hemoptysis: a comprehensive review of diagnostic imaging and bronchial arterial embolization. Cardiovasc Intervent Radiol. 2010;33: 240–50. 12. Marshall TJ, Jackson JE. Vascular intervention in the thorax: bronchial artery embolization for haemoptysis. Eur Radiol. 1997;7: 1221–7. 13. Pump K. Distribution of bronchial arteries in human lung. Chest. 1972;62: 447–51. 14. Antonelli M, Midulla F, Tancredi G, Salvatori FM, Bonci E, Cimino G, Flaishman I. Bronchial artery embolization for the management of nonmassive hemoptysis in cystic fibrosis. Chest. 2002;121(3): 796–801. 15. Barben J, Robertson D, Olinsky A, Ditchfield M. Bronchial artery embolization for hemoptysis in young patients with cystic fibrosis. Radiology. 2002;224(1): 124–30. 16. de Gregorio MA, Medrano J, Mainar A, Alfonso ER, Renge M. Endovascular treatment of massive hemoptysis by bronchial artery embolization: short-term and long-term follow-up over a 15-year period. Arch Bronconeumol. 2006;42(2): 49–56. 17. Roebuck DJ, Barnacle AM. Haemoptysis and bronchial artery embolization in children. Paediatr Respir Rev. 2008;9(2): 95–104. 18. Tanaka N, Yamakado K, Murashima S, Takeda K, Matsumura K, Nakagawa T, Takano K, Ono M, Hattori T. Superselective bronchial artery embolization for hemoptysis with a coaxial microcatheter system. J Vasc Interv Radiol. 1997;8: 65–70. 19. Schidlow DV, Taussig LM, Knowles MR. Cystic Fibrosis Foundation consensus conference report on pulmonary complications of cystic fibrosis. Pediatr Pulmonol. 1993;15: 187–98. 20. Saluja S, Henderson KJ, White RI Jr. Embolotherapy in the bronchial and pulmonary circulations. Radiol Clin North Am. 2000;38: 425–48.
5
The Clinical Respiratory Journal
Successful embolization in childhood hemoptysis due to abnormal systemic arterial bleeding of the lung and review of the literature Tugba Sismanlar1, Ayse T. Aslan1, Koray Akkan2, Emetullah Cindil2, Baran Onal2 and Beyza Ozcan3 1 Department of Pediatric Pulmonology, Gazi University Hospital, Ankara, Turkey 2 Department of Radiology, Gazi University Hospital, Ankara, Turkey 3 Department of Neonatology, Etlik Zubeyde Hanım Eg˘itim ve Aras¸tırma Hospital, Ankara, Turkey
Abstract Background and Aims: Hemoptysis in children is a rare but potentially lifethreatening symptom of an underlying respiratory tract abnormality. Hemoptysis, when massive and untreated, has a mortality rate of more than 50%. With interventional radiological procedures and surgery, this rate has dropped to 7%–18%. The experience with bronchial arterial embolization in childhood is very limited; only a few case reports with short-term follow-up have been reported. Methods: We report herein two patients with massive hemoptysis due to abnormal systemic arterial bleeding of the lung; neither patient had any lung or systemic disease. In both cases, the bleeding was controlled with endovascular embolization. The first case had bronchopulmonary arterial anastomosis and represents the first reported case with this anomaly. The second case had recurrent massive hemoptysis due to bronchial artery bleeding, and repeat embolization was performed. Results: Both of these children had rare vascular anomalies without parenchymal lung disease and were treated successfully with bronchial arterial embolization. Conclusion: Massive hemoptysis due to abnormal systemic bleeding of the lung in the absence of parenchymal disease is an uncommon and severe symptom in childhood. Embolization can be a treatment option in children with abnormal vasculature bleeding and can be repeated safely when needed. Please cite this paper as: Sismanlar T, Aslan AT, Akkan K, Cindil E, Onal B and Ozcan B. Successful embolization in childhood hemoptysis due to abnormal systemic arterial bleeding of the lung and review of the literature. Clin Respir J 2015; ••: ••–••. DOI:10.1111/crj.12289.
Key words bronchial artery embolization – children – hemoptysis – treatment Correspondence Tugba Sismanlar, MD, Department of Pediatric Pulmonology, Gazi University Hospital, Bes¸evler, Çankaya, 06500 Ankara, Turkey. Tel: +90312 2027597 Fax: +903122150143 email: [email protected] Received: 18 August 2014 Revision requested: 23 January 2015 Accepted: 01 March 2015 DOI:10.1111/crj.12289 Authorship and contributorship TS designed the study and wrote the paper. ATA analysed and interpreted the data and wrote the paper. KA, EC and B Ozcan contributed important reagents and performed the study. B Onal performed the study and analysed and interpreted the data. Ethics Written consents were obtained from the parents. Conflict of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
Introduction Hemoptysis in children is a rare but potentially life-threatening symptom of an underlying respiratory tract abnormality. Hemoptysis, when massive and untreated, has a mortality rate of more than 50% (1).
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
With interventional radiological procedures and surgery, this rate has dropped to 7%–18% (2). The lungs have a dual blood supply. They receive deoxygenated blood from the right ventricle via the pulmonary arteries. The blood is oxygenated and returned back to the heart via the pulmonary veins.
1
Embolization in childhood hemoptysis
Sismanlar et al.
The other source of blood supply is from the systemic circulation via the bronchial arteries. As a rule, there is one bronchial artery to the right lung that arises as a branch of the first intercostal artery. On the left, there are usually two arteries, arising directly from the descending thoracic aorta. They drain mostly via the pulmonary veins to the left atrium (3). The presence of anomalous arterial collateral supply to normal lung segments is well-reported in adults, but is much less common in children (4). We report herein two patients with massive hemoptysis due to abnormal systemic arterial bleeding of the lung; neither patient had any lung or systemic disease. Bleeding was controlled with bronchial arterial embolization (BAE).
Case 1 An 8-year-old boy was admitted with massive hemoptysis after coughing. His physical examination was normal. He had no prior history of pulmonary or cardiac disorders. He had normal complete blood count (CBC) and clotting studies. He had a normal rhinoscopy, upper airway examination and gastrointestinal tract endoscopy. He had negative serology for antinuclear cytoplasmic antibody (ANCA), antiglomerular basement membrane antibody (AGBMA), antinuclear antibody (ANA), anti-DNA, and rheumatoid factor (RF), and negative tuberculin skin test (TST). His chest X-ray was normal. Computed tomog-
(A)
(B)
raphy (CT)-angiography scan of the chest showed parenchymal consolidation in the right lower lobe, which was thought to be secondary to parenchymal hemorrhage. Selective right bronchial angiogram demonstrated a dilated lower bronchial artery and hypervascularity in the localization of lesions, compatible with the thoracic CT angiography, and common bronchopulmonary arterial anastomosis was detected. After catheterization with a 5Fr Cobra catheter, a 2.8Fr microcatheter was advanced into the right bronchial artery. Embolization was performed with polyvinyl alcohol (PVA) particles (250–355 μm in diameter). After the procedure, filling of the fistula disappeared, and pruning of bronchial artery branches was observed (Fig. 1). No complication was observed after the procedure. The patient has been followed for 26 months without hemoptysis.
Case 2 A 7-year-old girl presented after coughing up approximately 500 mL of fresh blood. She had been coughing up blood intermittently for 2 months. She had tachycardia and was pale. Her breath sounds were decreased in the right hemithorax. She had normal CBC, clotting tests and normal serology for ANA, RF, ANCA, AGBMA and anti-DNA. The rhinoscopy and upper airway examination were normal. On her chest roentgenogram, infiltration was seen in the right lower lobe. Descending thoracic aortogram and
(C)
Figure 1. (A) Selective right bronchial arteriogram shows hypervascularity, neovascularity and shunting into the pulmonary artery (arrows) in the paracardiac region. (B) Microcatheterization stage (arrow) through diagnostic catheter to prevent involuntary embolization. (C) Post-embolization arteriography demonstrates early cessation of the right bronchial artery and devascularization of the right paracardiac region (arrows). Note the disappearance of the right pulmonary artery filling through shunting.
2
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Sismanlar et al.
Embolization in childhood hemoptysis
(A)
(B)
(C)
(D)
Figure 2. (A) Initial selective right bronchial arteriogram shows hypervascularity and neovascularity in the paracardiac region (arrow). (B) Rebleeding bronchial arteriogram at the 14th month. Note the prominent pulmonary artery shunting (arrow). (C) Glue cast after embolization with N-butylcyanoacrylate-lipiodol mixture (black arrows). (D) Devascularized right paracardiac region after embolization (black arrows).
selective right bronchial angiogram demonstrated a hypertrophied tortuous bronchial artery with an area of hypervascularity and neovascularity. After catheterization with a 5Fr Cobra catheter, a 2.8Fr microcatheter was advanced into the right bronchial artery. Embolization was performed with PVA particles (355–500 μm in diameter). The follow-up angiogram demonstrated devascularization of the right bronchial artery. No complication was observed after the procedure. She was followed without hemoptysis for an extended period; however, she was admitted with massive hemoptysis 14 months later. Right bronchial artery angiography revealed revascularization with shunting into the pulmonary artery. For embolization, 0.5 mL of N-butyl-cyanoacrylate (NBCA) (Histoacryl, B. Braun Aesculap, Tuttlingen, Germany) was mixed with iodized oil (Lipiodol Ultra-Fluide, Guerbet, Aulnay-Sous-Bois, France) in a 1:2 ratio to make it fluoroscopically visible and to delay the polymeriza-
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
tion of the metal coils. Embolization with that mixture produced an immediate devascularization with the cessation of shunting into the pulmonary artery (Fig. 2). She has been followed for 42 months without hemoptysis.
Discussion Our first case had dilated bronchial artery and bronchopulmonary arterial anastomosis. To our knowledge, he represents the first case with massive hemoptysis due to bronchopulmonary arterial anastomosis that was treated successfully with embolization. The second patient had recurrent massive hemoptysis, attributed to bleeding from a normal bronchial artery that supplied a normal lung. There was no shunting into the pulmonary artery or vein or bronchial artery aneurysm. Only two patients with hemoptysis with normal bronchial artery supplying a normal lung have 3
Embolization in childhood hemoptysis
been reported (5, 6). Neither of our cases had any lung or systemic disease, and their anomalies are rare and unique. According to the literature, there have been only a few patients with hemoptysis due to abnormal systemic arterial bleeding, in the absence of lung or systemic disease, who were treated successfully with embolization. Both Sharifi et al. (7) and Chung et al. (8) described an 11-year-old girl with pulmonary and bronchial arteriovenous malformation supplied by the bronchial artery. Sheikh et al. (5) reported an 11-yearold boy with abnormal ‘blushing’ from the bronchial artery, and Arranz Arana et al. (6) reported an 11-yearold girl with bleeding from a hypertrophied bronchial artery. Abdulhamid and Forbes (4) reported five patients aged 7–15 years with aberrant systemic arteries from the aorta, right iliac artery, and left/right internal mammary artery. The longest follow-up time after BAE without complication was reported as 2 years. These cases and our cases are summarized in Table 1. Massive hemoptysis, also known as life-threatening hemoptysis, is a serious, critical condition that necessitates urgent assessment and treatment of the patient. Despite advances in the treatment of massive hemoptysis, it continues to represent a high-risk condition. Conservative medical treatment of patients with expectoration of 300–600 mL of blood per day is associated with mortality in 50%–100% of the patients affected (9), with asphyxia rather than hemorrhage commonly being the cause of death (10). Although surgical treatment of massive hemoptysis is associated with mortality rates ranging from 7.1% to 18.2%, the rate can reach 40% when surgery is performed urgently (2).
Sismanlar et al.
BAE has become a well-established vascular interventional technique in the management of massive and recurrent hemoptysis (11). The mode of action is the occlusion of systemic arterial inflow to the fragile vessels within inflammatory tissue, reducing the perfusion pressure and the likelihood of further bleeding (12). A number of embolic materials such as absorbable gelatin sponge, PVA, metal coils and NBCA are available for BAE. It is important to avoid embolic material that can pass through abnormal bronchopulmonary anastomoses, as there is a risk of pulmonary infarction via bronchial artery–pulmonary artery shunts or systemic artery embolization via bronchial artery pulmonary vein shunts. Bronchopulmonary anastomoses of up to 325 μm have been demonstrated in an anatomical study (13), and thus embolic materials with less than this diameter should not be used in BAE in adults. The smaller materials are reported to be used in selected patients and children (14–17). Our patients were 7 and 8 year olds, because of diameters of bronchial arteries were smaller than adults, smaller sized embolic materials were used. Otherwise, with the use of larger materials, it would cause the proximal embolization. Superselective embolization has been shown to reduce the risk of inadvertent embolization of the anterior medullary artery by embolization of more terminal branches of the bronchial artery beyond the origin of the spinal arteries (18). When performing embolization with NBCA, as in our second case, special care must be taken to avoid inadvertent embolization. NBCA has the ability to pass through an anastomosis of any size. Thus, the presence of an anterior medullary artery anastomosis must be searched carefully, and
Table 1. Clinical features of patients with abnormal systemic arterial bleeding of the lung treated with embolization
Case 1 Case 2 Sharifi et al. (7) Chung et al. (8) Sheikh et al. (5) Abdulhamid and Forbes (4)
Arranz Arana et al. (6)
Age
Sex
Anomaly
Procedure
Recurrence
Follow-up
8 7 11 11 11 7
M F F F M F
BAE BAE BAE BAE BAE BAE
No Yes (after 14 months) – – No Yes (after 5 years)
26 42 – – 18 15
13 15
M F
BAE BAE
No No
18 months 18 months
7 10 11
M F F
Bronchopulmonary arterial anastomosis Bronchial artery Bronchial AVM supplied by bronchial artery Pulmonary AVM supplied by bronchial artery Bronchial artery Aberrant systemic arteries from aorta and subclavian junction Aberrant systemic arteries from LIMA Aberrant systemic arteries from RIA, aorta, RIMA Aberrant systemic arteries from aorta Aberrant systemic arteries from aorta Aberrant bronchial artery from aorta
BAE BAE BAE
No Yes (after 5 months) –
2 years 4 months –
months months
months months
AVM, arteriovenous malformation; BAE, bronchial arterial embolization; LIMA/RIMA, left/right internal mammary artery; RIA, right iliac artery.
4
The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Sismanlar et al.
transcatheter embolization must be performed by experienced operators who are familiar with the use of NBCA. BAE appears to be effective, although there may be some side effects, the most common of which are pleuritic chest pain, fever, leukocytosis, dysphagia, post-embolism syndrome (lasting 5–7 days), and treatment with analgesics and narcotics, if necessary. Bronchoesophageal fistula as a complication resulting in more severe stenosis or bronchial wall necrosis may develop, but it has been reported very rarely (19, 20). However, we did not observe any complications in the two cases presented herein. Embolization can be repeated if needed. Abdulhamid and Forbes (4) repeated embolization in their two patients. In one case, embolization was repeated 5 years later and in the other case 5 months later. Our second case experienced repeat massive hemoptysis, and embolization was repeated 14 months after the first procedure. She has had no complaints in the 42 months of follow-up since the second embolization. This case represents the longest follow-up after repeat embolization reported in the literature. Massive hemoptysis due to abnormal systemic bleeding of the lung in the absence of parenchymal disease is an uncommon and severe symptom in childhood. Although there may be some complications, embolization can be a treatment option in children with abnormal vasculature bleeding. It is a safe procedure when performed by experienced operators and can be repeated safely when needed.
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The Clinical Respiratory Journal (2015) • ISSN 1752-6981 © 2015 John Wiley & Sons Ltd
Embolization in childhood hemoptysis
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