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DOI: 10.1148/radiol.2241010654
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(Radiology 2002;224:124-130.)
© RSNA, 2002

Pediatric Imaging

Bronchial Artery Embolization for Hemoptysis in Young Patients with Cystic Fibrosis1

Juerg Barben, MD, David Robertson, FRACR, Anthony Olinsky, FCPSA, FRACP and Michael Ditchfield, FRACR

1 From the Departments of Respiratory Medicine (J.B., A.O.) and Radiology (D.R., M.D.), Royal Children’s Hospital, Flemington Rd, Parkville 3052, Victoria, Australia. Received March 21, 2001; revision requested April 27; final revision received December 14; accepted January 16, 2002. Address correspondence to M.D. (e-mail: ditchfim@cryptic.rch.unimelb.edu.au).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To review the authors’ 15-year experience with bronchial artery embolization (BAE) for treatment of hemoptysis in young patients with cystic fibrosis.

MATERIALS AND METHODS: By searching the 1985–1999 radiology database, the authors identified 23 young patients who had been referred to the radiology department for angiography. Twenty of these patients underwent BAE. The 23 medical records were retrospectively reviewed with regard to embolization agents used, embolization success rates, number of repeat embolizations, survival times, and causes of death.

RESULTS: BAE was performed on 38 occasions in 20 patients. The mean age of patients at first BAE was 15 years (age range, 7–19 years). The majority (n = 34 [89%]) of BAEs were performed by using polyvinyl alcohol. The immediate success rate after BAE (ie, no recurrent bleeding within 24 hours) was 95% (36 of 38 BAEs). Eleven (55%) patients required more than one BAE, and the median time between first and second embolizations was 4 months (range, 5 days to 61 months). Three patients died as a consequence of severe hemoptysis during induction of anesthesia with intermittent positive pressure ventilation in preparation for BAE. The median survival duration after the first BAE (Kaplan-Meier estimate) was 84 months (average follow-up, 61 months; range, 5 days to 169 months).

CONCLUSION: BAE had a high success rate for short-term control of bleeding; however, more than half the patients required repeat embolization during the long-term follow-up.

© RSNA, 2002

Index terms: Angiography, 948.122 • Arteries, therapeutic embolization, 943.1264, 943.1266 • Fibrosis, cystic, 60.252 • Lung, hemorrhage, 60.4123, 60.4128


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Major hemoptysis occurs in approximately 1% of all patients with cystic fibrosis (CF) and is more frequent in those with more severe lung disease (1). Major hemoptysis is rarely seen in children younger than 10 years; however, it occurs in up to 1.5% of individuals aged 16–20 years (1). Minor hemoptysis—that is, blood streaking in sputum—such as that seen with bronchiectasis is relatively common and has been reported in up to 60% of adults with CF (2). In patients with CF, hemoptysis occurs as a complication of lung disease and is believed to result from erosion of abnormal bronchial vessels (1). These vessels may be thin walled, tortuous, or newly developed and are found in areas of bronchiectasis secondary to chronic infection (3–6). A second reason for hemoptysis in individuals with CF is coagulopathy secondary to vitamin K deficiency (7).

The commonly used definition of major hemoptysis is acute massive bleeding of greater than 240 mL/d or recurrent bleeding of substantial volume (>100 mL/d) for a few days or weeks (8–10). Chronic recurrent small-volume hemoptysis (<100 mL/d) that interferes with a patient’s lifestyle and/or prevents effective physical therapy also may be considered to be major hemoptysis (10,11). In many patients with major hemoptysis, the bleeding stops spontaneously within a few days (8). At times, conservative treatment, such as bed rest, intensive intravenous antibiotic treatment, vitamin K therapy, blood transfusion if necessary, and temporary discontinuation of physical therapy, is sufficient to control the symptoms (3,8,12,13). Percutaneous bronchial artery embolization (BAE) has been shown to be a safe and effective method of controlling hemoptysis in patients with (4,6,10,11,14–17) and in those without (18,19) CF. However, the superiority of BAE over conservative therapy in reducing the rate of long-term recurrence of major hemoptysis and in improving survival has not yet been proven (17,20).

The purpose of our study was to review our 15-year experience with BAE for treatment of hemoptysis in young patients with CF at Royal Children’s Hospital in Melbourne, Australia.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
The CF unit at Royal Children’s Hospital manages the care of 320–340 young patients with CF, who represent more than 90% of the young patients with this disease in the state of Victoria (population, approximately 5 million). Prior to 1985, all young patients who required BAE were referred to an adult hospital. A search of the radiology database for January 1985 to December 1999 resulted in the identification of 23 young patients with CF and major hemoptysis who were referred for angiography and BAE by a pediatric respiratory physician after consultation with pediatric radiologists. These 23 medical records were retrospectively reviewed with regard to type of embolization agents used, embolization success rate, number of repeat embolizations, time between embolization and recurrent bleeding, surgery performed, survival time, and cause of death. Our institutional review board did not require its approval or patient informed consent for this study.

The diagnosis of CF was made in all patients on the basis of clinical presentation and a positive sweat test result (21) before neonatal screening was introduced in 1989. The severity of lung disease was classified as mild (forced expiratory volume in 1 second [FEV1] > 75% of that predicted), moderate (FEV1 = 50%–75% of that predicted), or severe (FEV1 < 50% of that predicted). The results of lung function examinations (ie, forced vital capacity and FEV1) that were performed by using standardized criteria for pediatric lung function testing (22) were obtained from the laboratory database of the CF unit.

Twenty-three patients (11 [48%] female, 12 [52%] male) were referred for BAE. Their mean age at referral for BAE was 15 years (median age, 16.8 years; age range, 7–19 years); four children were younger than 10 years. Overall, the male patients were older than the female patients (mean age, 16.1 vs 14.0 years). The mean FEV1 at first embolization was 56% of that predicted (range, 25%–94%), with a lower FEV1 in the female patients (46% of that predicted; range, 25%–81%) compared with that in the male patients (64% of that predicted; range, 40%–94%).

Hemoptysis was considered to be major on the basis of the following criteria: (a) major hemoptysis as a single event (>240 mL/d), (b) moderate hemoptysis in the form of recurrent bleeding of substantial volume (>100 mL/d) for a few days, or (c) chronic recurrent hemoptysis in the form of small hemoptyses (<100 mL) that interfered with the patient’s lifestyle (eg, sporting activities) or prevented effective physical therapy for a few weeks.

BAE Procedure
The sizes of the catheters used ranged from 5.0 to 6.5 F. The catheters typically used were either 5-F (HNK; Cook, Brisbane, Queensland, Australia) or 5-F visceral (Cobra C1; Cook) types. For the past 7 years, microcatheters have been used when there is difficulty securing or advancing the catheter to a safe position; typically an infusion catheter (Tracker 18; Boston Scientific/Target Therapeutics, Boston, Mass) is used in these cases. Catheters were introduced into the femoral artery through an introducer sheath by using the Seldinger technique. As a routine procedure, the descending thoracic aorta and intercostal arteries were angiographically examined for the identification of bronchial arteries. All abnormal vessels and their origins seen at each bleeding episode were evaluated and counted. Vessels that were enlarged and/or abnormally tortuous were embolized. Embolization with particulate matter was continued until the flow into the embolized vessel almost ceased. If catheter placement could not be secured, embolization was not performed. The presence of a spinal artery circulation arising from a bronchial artery was an absolute contraindication to embolization if the origin was distal to the farthest reach of the catheter tip. The ability to access abnormal bronchial arteries improved as catheter technology improved during the series.

The embolic materials used were polyvinyl alcohol (Ivalon; Pacific Medical Industries, La Mesa, Calif), which contained particles that ranged in size from 150 to 550 µm; gelatin pledgets (Gelfoam; Upjohn, Kalamazoo, Mich); Gianturco coils (Cook); or a combination of two or more of these materials.

BAE was considered to be successful when the patient’s hemoptysis stopped within 24 hours after embolization. If major hemoptysis persisted or recurred, the procedure was repeated (or surgery was performed) and considered as a separate procedure in the results.

Statistical Analyses
Statistical analyses were performed by using computer software (STATA 6.0; STATA, College Station, Tex). Median survival times were estimated by using the Kaplan-Meier method, and comparisons between the sexes were performed with the log-rank test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Of a total of 46 bleeding episodes, which led to a referral for BAE, 22 (48%) were massive (>240 mL/d); 10 (22%), moderate (>100 mL/d); and 14 (30%), chronic recurrent (<100 mL/d). Coagulation was abnormal (international normalized ratio > 1.4) in six patients, who had eight episodes of hemoptysis that led to BAE, and was treated on each occasion with intravenously administered vitamin K. Thirteen patients required blood transfusions on 18 occasions prior to BAE.

BAE Findings and Results
BAE was performed 38 times in 20 patients (Figure; Tables 1, 2). BAE was planned but not performed in three other patients (Table 3). In the 46 bleeding episodes, 69 abnormal vessels could be identified. There was one abnormal vessel in 25 episodes, two in 16 episodes, and three in four episodes. One patient (patient 23) died before angiography could be performed. The majority of abnormal vessels (n = 65 [94%]) arose directly from the descending aorta, two abnormal vessels arose from the internal thoracic artery, and one abnormal vessel each arose from the thyrocervical trunk and lateral thoracic artery. Fourteen of the bronchial arteries identified were not embolized: Three had a connection to a spinal artery, and 11 did not have hypertrophy that was substantial enough to warrant embolization. The majority (n = 34 [89%]) of BAEs were performed by using polyvinyl alcohol. Gelatin pledgets were used only a few times and usually in combination with polyvinyl alcohol. Coils were used only five times and have not been used at our institution since 1988.



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  		Flow chart of BAE performed in young patients with CF and major hemoptysis. CRF = cardiorespiratory failure, MPH = massive pulmonary hemorrhage during induction of anesthesia with intermittent positive pressure in preparation for BAE. ventilation. All numbers are numbers of patients.

 

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  		TABLE 1. Patients Who Underwent One BAE

 

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  		TABLE 2. Patients Who Underwent More Than One BAE

 

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  		TABLE 3. Patients Who Were Selected for BAE but Did Not Undergo Embolization

 
With regard to the procedure itself, the immediate success rate after BAE, defined as no recurrence of bleeding within 24 hours, was 95% (36 of 38 BAEs). In the intention-to-treat analysis, this rate dropped to 92% (35 BAEs) because one patient (patient 23) died as a result of respiratory arrest following major hemoptysis at induction of general anesthesia just before BAE could be performed. Two additional patients had further major hemoptysis within 1 week.

Long-term Follow-up
The average follow-up time was 61 months (range, 5 days to 169 months). The median survival time after BAE (Kaplan-Meier estimate) was 84 months for all patients; the male patients had significantly longer survivals than the female patients (relative risk, 6.6; 95% CI: 1.4, 31.0; P = .006, log-rank test). BAE was performed only once in nine patients, and 11 (55%) patients required more than one embolization (Table 2). The median time between the first and second embolizations was 4 months (mean, 14.6 months; range, 5 days to 61 months). Six patients required repeat BAE within 6 months; one patient, between 6 and 12 months; and two patients, between 12 and 18 months. Two patients did not require repeat BAE until 55 and 61 months after the initial embolization.

In two patients, bleeding could not be controlled with BAE and lobectomy was performed: One child (patient 17) continued to have massive hemoptysis, which led to repeat BAE 6 days after the first embolization. This patient continued to have recurrent moderate hemoptysis and then massive hemoptysis, which led to further bronchial angiography 7 weeks following the initial BAE. An abnormal left bronchial artery supplying the lower lobe but also giving rise to a spinal artery was depicted but not embolized. Further massive hemoptysis occurred, and left lower lobectomy was performed 52 days after the initial BAE.

The other child (patient 14) who eventually required surgical intervention had no major hemoptysis for 2 months after the initial BAE. He was shown to have multiple abnormal bronchial arteries. Because of a recurrence of massive hemoptysis, another embolization of a right upper lobe bronchial artery arising from the descending thoracic aorta was performed. The hemoptysis was not controlled, and repeat angiography depicted a tortuous aberrant vessel arising from the proximal right subclavian artery. This vessel could not be cannulated and was clipped at thoracotomy. The patient presented with major hemoptysis 4 months later, and angiography depicted an aberrant bronchial artery arising from the right internal thoracic artery that supplied the right upper lobe. This vessel was embolized. Multiple systemic to bronchial artery collateral vessels had developed following the thoracotomy and could not be embolized. Recurrent mild hemoptysis was controlled with tranexamic acid, but 5 months later major hemoptysis recurred and right upper lobe lobectomy was performed (13).

Fourteen of the 23 patients died during the study period. Eleven patients, nine of whom were female, died of cardiorespiratory failure as a consequence of progressing CF, and three died of severe hemoptysis. As already mentioned, one patient died immediately as a result of massive pulmonary bleeding during induction of anesthesia just prior to BAE. Two other patients died 14 and 52 days after major hemoptysis during induction of anesthesia for BAE. Apart from these anesthesia-related complications, which have been described in detail elsewhere (23), no substantial adverse events relating to the BAE procedure were recorded.

Patients Who Were Selected for BAE but Did Not Undergo Embolization
In three patients who were referred for BAE, vessels were not embolized (Table 3). Patient 21 presented with chronic recurrent hemoptysis, and an abnormally enlarged and tortuous right bronchial artery was seen at angiography. However, this vessel gave rise to a spinal artery distal to the farther point of cannulation and therefore was not embolized. The patient did not have further major hemoptysis but died 2 months later as a result of cardiorespiratory failure. Patient 22 presented with moderate hemoptysis, and an abnormally enlarged and tortuous left bronchial artery was seen at angiography. However, this vessel could not be selectively cannulated and therefore was not embolized. Eight months later, this patient had another episode of major hemoptysis, which was treated conservatively. She died of cardiorespiratory failure 2 months later. Patient 23 died during induction of anesthesia just prior to BAE, as mentioned herein earlier.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
BAE, which to our knowledge was first reported on by Remy and colleagues (14) in 1974, is an effective method for controlling major hemoptysis. Many reports (4,10,11,16,17) describing this technique, including those describing its use in adult patients with CF, have been published. Catheter embolization of bronchial arteries was first performed in our hospital in 1985. Since then, BAE has had an important role in controlling major hemoptysis in patients with CF, as described in this review article.

Our immediate success rate (no bleeding within 24 hours) of 95% is similar to other published data (16,19,24). However, 55% of the patients required repeat embolization at some point. This repeat embolization rate is similar to the risk of recurrence of major hemoptysis treated conservatively during longer term follow-up (24) and is slightly higher than the repeat embolization rate reported in other published studies. However, these studies had much shorter follow-up durations (Table 4), which would account for the difference.


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  		TABLE 4. Long-term Follow-up after BAE in Previous Studies

 
Different embolic materials have been used in previous studies; these include polyvinyl alcohol particles used alone or with gelatin pledgets and coils. Polyvinyl alcohol has been reported to be superior to gelatin pledgets for permanent occlusion, but recurrence of hemoptysis and repeat BAE have been noted with the use of both of these materials (10,11,16). At our institution, the majority of BAEs were performed by using polyvinyl alcohol. Gelatin pledgets were rarely used, but when they were, they usually were used with polyvinyl alcohol. Coils were used only five times and have not been used at our institution since 1988, because on subsequent occasions coil placement hampered attempts to embolize distal vessels.

BAE, as performed by experienced interventional physicians, has been shown to be a safe and effective method for treatment of major hemoptysis with CF (4,16,17). However, serious adverse events have been reported; these include transverse myelitis (25), bronchial infarction (26), esophagobronchial fistula (27), and ischemic colitis (28). The most feared complication is spinal infarction and paraplegia resulting from embolization of a spinal artery (10,11,29). Minor adverse events include transient chest pain, fever, and dysphagia (10,17). In our series, three patients died following massive pulmonary hemorrhage during induction of anesthesia with intermittent positive pressure ventilation in preparation for BAE. This complication has been reported in detail elsewhere (23). As a result of these events, the procedure used to induce anesthesia for BAE is now a combination of intravenous sedation and local anesthesia with spontaneous respiration instead of intermittent positive pressure ventilation, whenever possible. With regard to the embolization procedure itself, BAE was well tolerated and no other major adverse events were recorded.

In two patients, pulmonary bleeding could not be controlled with BAE, and surgical intervention in the form of bronchial artery ligation and local pulmonary resection was necessary. This embolization failure rate is in accordance with that in previously published, predominantly adult, studies in the literature (9,30–34).

Some authors (37) recommend performing emergency bronchoscopy during active bleeding in an attempt to localize and identify the specific site of hemorrhage. In our experience, there was no need for routine bronchoscopy, and we performed only a few emergency bronchoscopies.

Major hemoptysis with CF is believed to occur in patients with diffuse severe lung disease (35); however, it can also be associated with moderate or mild pulmonary disease (36), in which it possibly arises in a localized area of more severe inflammation or as a result of aberrant arteries (13). These possible causes of hemoptysis emphasize the need to identify each bronchial artery and to search for any aberrant arteries by means of angiography before performing selective catheterization (11).

In summary, the results of this retrospective study show that BAE is a safe and efficient treatment for major hemoptysis in young patients with CF. Despite the effectiveness of BAE, its superiority over conservative therapy in reducing recurrent bleeding and long-term morbidity remains unproven, as illustrated by the cases in which vessels were not embolized in this study. Only a prospective randomized trial can address this issue. Some patients will undergo only conservative treatment (eg, bed rest, intensive intravenous antibiotic therapy, vitamin K therapy, blood replacement, tranexamic acid therapy, and temporary discontinuation of physiotherapy) (8). However, we believe that BAE should always be considered for treatment of moderate to major hemoptysis.


   ACKNOWLEDGMENTS
 
The authors are grateful to John B. Carlin, PhD, of the Clinical Epidemiology and Biostatistics Unit of Royal Children’s Hospital for statistical advice.


   FOOTNOTES
 
Abbreviations: BAE = bronchial artery embolization, CF = cystic fibrosis, FEV1 = forced expiratory volume in 1 second

Author contributions: Guarantors of integrity of entire study, J.B., M.D.; study concepts, J.B., D.R., M.D.; study design, J.B., M.D.; literature research, J.B.; data acquisition and analysis/interpretation, D.R., J.B., M.D.; manuscript preparation, J.B.; manuscript definition of intellectual content, J.B., M.D., A.O.; manuscript editing, J.B.; manuscript revision/review, M.D., A.O.; manuscript final version approval, J.B., M.D., A.O.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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