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Ann Thorac Surg 2003;75:1998-2006
© 2003 The Society of Thoracic Surgeons

Review

Postoperative aortic fistulas into the airways: etiology, pathogenesis, presentation, diagnosis, and management

Marco Picichè, MDa, Ruggero De Paulisb, Alessandro Fabbri, MDa, Luigi Chiariello, MDb*

a Cardiac Surgery Department, San Bortolo Hospital, Vicenza, Italy
b Chair of Cardiac Surgery, "Tor Vergata" University of Rome, Rome, Italy

* Address reprint requests to Dr Chiariello, Cattedra di Cardiochirurgia, Università di Roma "Tor Vergata," European Hospital, Via Portuense 700, 00149, Rome, Italy


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 References
 
Postoperative aortobronchial and aortopulmonary fistulas are rare and late complications of cardiac surgery. They mostly complicate descending thoracic aortic procedures. Hemoptysis is the main symptom, and may be massive or intermittent. The reported interval between the time of operation and the onset of hemoptysis ranges from 3 weeks to 25 years. Diagnostic examinations are often unable to directly visualize a fistula. Indication for surgical or endovascular repair mostly relies on clinical suspicion and nonspecific diagnostic features. Urgent treatment is based on the association of the following elements: (1) hemoptysis, (2) history of previous cardiac or aortic operation, (3) presence of lung infiltrates on the chest roentgenogram, (4) lung hemorrage on the computed tomographic scan, and (5) and visualization of a pseudoaneurysm. Aortobronchopulmonary fistulas are uniformly fatal if untreated. The overall surgical mortality rate is 15.3%. There is no procedure-related mortality after endovascular stent grafting. A review of the English-language literature from 1947 to October 2002 is presented.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 References
 
Aortic fistulas into the bronchial tree and lung parenchyma may develop after unpredictable periods after surgery and are often the consequence of pseudo-aneurysms. Hemoptysis, whether massive or intermittent, represents the most common symptom [1, 2]. Following our case report describing an aortic pseudoaneurysm (PSA) fistulizating into the right bronchial tree [3], we completed the study on postoperative aortobronchopulmonary fistulas (ABPFs) through a collective review of the literature.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
References
 
We performed a MEDLINE search with the terms "aortobronchial fistula," "aortopulmonary," "aortobronchopulmonary," "aortotracheal," "pseudoaneurysm," "postoperative," and "hemoptysis." References in each article were screened to look for any article not reported on MEDLINE. All case reports and reviews from 1947 to October 2002 have been included. A total of 76 patients and 79 fistulas (3 patients were affected by two fistulas) were found. The etiology, pathogenesis, and anatomical, clinical, diagnostic, and surgical features, as well as the outcomes, were examined.

Historical marks
The first ABPF was described by Girardet [4] in 1914 in a patient affected by pulmonary tuberculosis. In 1934 Keefer and Mallory [5] reported the first series of chronic aortic aneurysms with six autopsy cases of ABPFs. The first case of postsurgical fistula was observed by Jones [6] in 1947 in an 11-year-old girl who had undergone patent ductus arteriosus ligation 2 years previously.

In the 1960s Davey [7] identified the cause of fistulas in the material used for aortic replacement, namely, Ivalon grafts. The first of three existing cases of double ABPF in the same patient was reported by Grillo and colleagues [8] in 1968. In 1993, Ramakantan and Shah [9] first described a communication into the right bronchial tree. In 1996 Campagna and colleagues [10] and Chuter and associates [11] separately reported successful treatment with endovascular stenting.

Etiology and pathogenesis
Aortic fistulas into the airways are more common after descending thoracic aorta (DTA) procedures. During infancy they can be seen after patent ductus arteriosus or aortic coartaction repair [6, 7, 10–35]. In adults they prevail after resection of DTA chronic aneurysms [36–48]. Aortic fistulas have also been reported after surgical repair of aortic arch [49, 50, 51] and thoracoabdominal aneurysms [52], DTA traumatic rupture [51, 53], types A [3, 22, 54, 55] and B [35, 56, 57] dissection, Takayasu arteritis [58], and aortic sarcoma (Table 1) . [59]. The ABPFs encountered after surgery for tetralogy of Fallot [23], aortic and mitral valves [9, 60, 61], and tumor of thoracic vertebrae represent unique cases [62]. Finally, endobronchial expandable metal stents caused fistulas in a patient with pediatric bronchomalacia [63], after lung transplantation [64], aortic dissection [55], or tracheal resection [65] (Table 2).


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  		Table 1. Aortic Diseases and Correlate Procedures Developing Aortobronchopulmonary Fistulas: Population, Type of Procedure, Presentation, and Diagnostic Modalities

 

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  		Table 2. Nonaortic Diseases and Correlate Procedures Developing Aortobronchopulmonary Fistulas: Population, Type of Procedure, Presentation, and Diagnostic Modalities

 
Postoperative aortic PSAs may arise from disruption of one or more arterial wall layers with extravasation of blood into the surrounding spaces. The hematoma is then held by the remaining vascular layers, fibrous tissue, and sometimes the parietal pericardium. A neointima may develop [3]. Disruption may be related to different sites depending on the type of operation. The cannulation site for cardiopulmonary bypass is the most common in a review by Sullivan and associates [66]. Graft-to-graft anastomosis [3], saphenous vein anastomosis [67], aortic and needle vent sites [68], patch suture lines, and distal or proximal suture lines in aortic replacement [69] have also been reported.

Inappropriately tight sutures, fragility of the host tissue, or inappropriate material each play a role in pseudoanaurysm development [6]. Merrill and coworkers [70] have reported PSAs caused by silk suture fragmentation and dissolution in patients with Teflon grafts. A suture line may also be disrupted by adjacent arteriosclerosis [53]. Bacterial or fungal infection of a prosthetic graft may play a role [16, 24, 25, 38, 54, 62]. As with true aneurysms, but at a faster rate, the PSA progressively enlarges and causes compression of the airways. This results in a local inflammatory response and the phenomenon of pressure necrosis, which increases the inflammatory process. Stable adhesions may occur [66]. The lung undergoes chronic pulsate erosion exerted by the vascular mass. When the wall tension of the PSA becomes critical, it ruptures into the airways [3].

A PSA is not the only possible cause of bronchopulmonary damage, which may also be due to neoaneurysms involving the native aortic wall next to suture lines [23, 36–38, 43, 48, 56, 58]. In other cases slow but continuous damage to lung parenchyma is caused by strictly adjacent foreign material such as graft substance [7, 57], remnant of temporary bypass [50, 51], silk knots and suture material [6, 17, 37, 46], endobronchial expandable metal stents [55, 63–65], or kinking of an aortic stent-graft [52] (Table 3).


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  		Table 3. Mechanical Causes of Bronchopulmonary Damage

 
The left lung is much more involved than the right one. This may be explained by the short distance from the DTA. Conversely, communications between the ascending aorta and the right lung are rare, and only 7 cases have been reported so far [3, 9, 22, 51, 54, 60, 61]. Reported sites of aortic and bronchopulmonary ends of fistulas are listed in Table 4.


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  		Table 4. Anatomy of the Fistulous Pathway

 
Presentation
Hemoptysis is the first (and often the only) symptom of ABPFs. It may be massive or intermittent, depending on the size of the opening. The fistula is usually small and it is easily occluded by clots. It then stays closed for weeks or months; when clots lese or dislodge, the communication opens again and a new bleeding ensues [6, 7, 10, 11, 14, 15, 17–23, 36, 37, 40, 41, 43–46, 50–54, 56–59, 62, 71]. This process recurs several times, increasing at each episode until the fistula becomes large enough to cause massive passage of blood. The reported interval between the time of operation and the onset of hemoptysis is variable, ranging from 10 weeks [13] to 25 years [11, 23, 72] after cardiac or aortic procedures. The interval even decreases to 3 weeks after endobronchial expandable metal stents implant [63]. Less frequently, massive bleeding appears abruptly at the first episode, representing an imminent threat to life (Tables 1 and 2) [3, 49, 10, 18, 13, 16, 23, 26, 38, 39, 43, 55, 58, 60, 63–65].

Other symptoms and signs are inconstant. Dyspnea and cough [15, 16, 18, 36, 45, 48, 60, 65], chest or back pain [23, 36, 48, 65], pulmonary rales [15, 18], hypoxemia [11, 45, 47], dysphonia [28], hoarseness [48], tachypnea [45], fever [15], sepsis [11], or respiratory alcalosis [45], failure [78], or arrest [39, 58] have been reported. The patient may be unstable hemodynamically, with hypotension [56], shock [13, 36], and cardiac arrest (Tables 1 and 2) [36].

Diagnosis
Hemoptysis may be present in many pathologic conditions. For this reason, anamnesis is extremely important for differential diagnosis. A history of previous cardiac or aortic operations is highly suggestive of ABPF, especially if DTA was involved [3].

Chest roentgenography is the first means of examination (Fig 1). It may disclose a mediastinal mass or intraparenchymal hemorrage, although imaging of lung infiltrate is nonspecific and a radiogram may even be normal [46]. Thus, additional investigations are required (Tables 1 and 2).



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  		Fig 1. Chest roentgenogram showing opacification of the right lung field due to massive hemorrhage.

 
Aortography has been widely used in the past. The contrast fluid may be seen directly in the fistula [31]. If the contrast medium is seen only in the bronchus it represents an indirect sign; however, more often the fistula is occluded by clots and aortography is nondiagnostic [37]. Dislodgment of clots with fatal hemoptysis during injection of contrast material has been reported [9].

Conventional computed tomography (CT) was first used for diagnosis of ABPF in 1986 [41]. It is easily performed in emergency conditions. With a low dose of contrast material it reveals lung consolidation due to parenchymal hemorrage, the diameter and contours of a mass, and eventual compression of surrounding structures (Fig 2). However, it is quite unlikely to yield a scan that directly visualizes the passage of contrast from the aorta into the airways. To our knowledge, this has only been reported by Riancho and colleagues [18] and by Ninan and associates [61].



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  		Fig 2. Computed tomogram of the chest showing an ascending aorta pseudoaneurysm compressing both the superior vena cava (thin arrow) and the aortic graft (thick arrowhead). Hemorrhage in the right lung is also visible. (Reprinted with permission from The Society of Thoracic Surgeons [Ann Thorac Surg 1999, 68, 1406–7] [3].)

 
Bronchoscopy is able to detect the source of hemoptysis, as it may visualize the bronchial tear [43]. However, dislodgment of occluding clots and traumatic rupture of an adherent vascular mass are potential serious complications [49, 43, 50]. As with aortography [49], some authors recommend that a surgical team be ready for emergency operation during the procedure [49, 45].

Transesophageal echocardiography and magnetic resonance imaging have been used less often. Magnetic resonance imaging is not practical in emergency conditions, and it was able to visualize the fistula tract in one case only [21]. Transesophageal echocardiography is helpful, as it may reveal a compressive mass along the aortic graft [3]. Doppler imaging may reveal an abnormal jet from the aorta into the surrounding spaces. Recently Thompson and associates [47] have visualized the fistula tract in 4 patients.

Recently the technique of computed tomographic angiography has become increasingly popular, and it has been used in some cases of ABPF starting from 1996 [72]. It allows tridimensional view angles, visualizes a PSA and its surrounding structures, shows both the thrombosed and contrast-filled portion, and is less invasive than conventional angiography [10, 27, 59]. For these reasons we agree with Ferretti and colleagues [72], who underline the importance of this technique also when a fistula per se is not demonstrable. We favor this means of examination every time an episode of hemoptysis is reported in a patient with previous aortic surgery.

In conclusion, different diagnostic modalities are potentially able to directly visualize a fistula tract; however, our review discloses that only in exceedingly rare cases was this visualization practically achieved. Thus, indication for surgical or endovascular repair mostly relies on clinical suspicion and nonspecific diagnostic features.

We advise urgent treatment based on the association of the following elements: (1) hemoptysis, (2) history of previous cardiac or aortic operation, (3) presence of lung infiltrates on a chest roentgenogram, (4) lung hemorrage on a computed tomographic scan, and (5) visualization of a PSA.

Management
If left untreated, ABPFs are uniformly fatal [1]. In our review, all 8 untreated patients died due to massive hemoptysis (Table 5). Thus, management of the airways must be immediate and must first include bleeding control by selective endotracheal intubation. The inflated cuff of a Carlens tube [73] or a Fogarty embolectomy catheter [17] may be positioned into the bleeding side of bronchial tree to protect the contralateral side from hemorrage. Otherwise a single-lumen endotracheal tube may be positioned in the healthy main stem bronchus [58]. Some authors recommend using a rigid bronchoscope as an airway and suction conduit while waiting for surgery [2].


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  		Table 5. Overall Mortality in Patients Affected by Postoperative Aortobronchopulmonary Fistulas

 
The patient is often in critical condition at the moment of diagnosis, requiring emergency surgery. Rapid institution of CPB through the femoral vessels is indicated before starting thoracotomy or sternotomy if resuscitation is executed during transport into the operating theater [32]. Nevertheless we deem that, even in stable patients, surgical or endovascular treatment should be performed without delay to prevent clot dislodgment and massive bleeding.

Various surgical approaches have been described. The DTA may be approached through a single [29, 32, 37] or double left posterolateral thoracotomy. The latter is rarely used; it has been carried out at the fourth [21, 32] intercostal space proximally and at the seventh [21] or ninth [32] distally. Although excessively invasive, the association of left thoracotomy and median sternotomy achieves optimal exposition of the supradiaphragmatic aorta [16, 22]. A simple aortic cross-clamping can be used in case of limited extension of a PSA [17, 28, 60], but left atrial–femoral [21, 37, 46] and femoral–femoral [24, 32, 36] bypass, instead of the traditional Gott shunt [41, 65], are more often used to ensure distal perfusion.

When the fistula is located in the ascending aorta, femoral–femoral cannulation should be established before opening the sternum, as the false aneurysm may potentially rupture during sternotomy. In the only reported case of successful off-pump repair the femoral artery had been preventively cannulated [3].

The aortic end of the fistula may be treated by direct [3, 6, 49, 8, 13, 14, 17, 23, 36, 65] or patch [49, 19, 20, 40, 50, 61] closure, subclavian artery flap repair [15], extraanatomic bypass grafting [16, 22, 26, 27, 31, 62], homograft implantation [25], and, more often, prosthetic graft insertion [19, 21, 23, 28, 29, 32, 34, 37, 38, 41, 44, 46, 51, 53, 57, 60, 72] (Table 6).


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  		Table 6. Management of the Aortic End of 71 Aortobronchopulmonary Fistulasa

 
Surgical repair of the bronchial or pulmonary ends may consist of primary closure [3, 6, 49, 13, 22, 46, 50, 53, 56, 60, 61], partial lobe resection [49, 15, 23, 28, 29, 41, 43, 44, 72], lobectomy [14, 51], or pneumonectomy [32, 40, 63] (Table 7). It is not carried out when exclusion of the fistula at the aortic end (as with endovascular treatment) is considered to be adequate [37].


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  		Table 7. Management of the Bronchopulmonary End of 71 Aortobronchopulmonary Fistulas

 
The pseudoaneurysm, if present, should be removed along with all prosthetic material if infection is suspected [57]. Cryopreserved vascular homografts may help to eradicate the infection [25]. Specimens for microbiological investigation should always be taken during operation. We agree with others who advise preventive antibiotic therapy for 3 to 6 weeks postoperatively in case of no evidence of infection [25, 30, 57].

Direct contact between the vascular reconstruction and the pulmonary tissue should be avoided to prevent further erosive damage. The repaired aorta should be covered by the remains of the pseudoaneurysmal wall [51, 60] or by surrounding viable tissue such as thoracic wall muscles [49, 65], pleural [49, 20, 62] or pericardial [49, 19, 20, 28, 65] flaps, thymic fat [23], or omental pedicle [46, 50]. Otherwise bovine pericardium may be used [28].

Since 1996 endovascular procedures have been used by Campagna and colleagues [10] and by Chuter and associates [11] to treat ABPFs. So far 10 groups of investigators have described endovascular stenting in 15 patients [10, 11, 30, 33, 35, 47, 48, 58, 59, 71]. There was no mortality rate associated with these procedures. These data contrast with the high mortality rate of open surgical repair. We found that 8 (16%) of 50 patients who had undergone surgical treatment of DTA fistulas died intraoperatively or early after surgery [18, 19, 24, 39, 43, 45, 52, 63] (Table 8). Surgical mortality is due to complexity of procedures. A challenge is presented by coexistence of emergency conditions and difficulties of redo operations. Hemorrage, prolonged ventilatory compromise, kidney failure, paralysis, or graft infection may easily worsen the prognosis [47].


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  		Table 8. Management of the Aortic End: Procedure-Type–Related Results

 
On the other hand possible complications of an aortic stent graft are migration [52], interruption of spinal chord intercostal blood supply [10], structural defects [30], arterial injury [33], infection (if it is located in a septic environment) [35], and even ABPF [52]. In our review only 1 patient had complications requiring ileofemoral bypass and embolectomy [33]. With the latest generation of devices, which are considered easier to deploy, more suitble to the aortic contour, and less likely to migrate [47], stent grafting appears very promising. With future generations of devices, one may expect that complications will be even less likely. Among patients who underwent endovascular treatment there was one death due to unrelated causes [71]. The overall mortality rate is reported in Table 5.

Finally, in July 2002 Hiraki and colleagues [74] reported the successful treatment of a postoperative ABPF by injecting into the pathway n-butyl-cyanoacrylate material using a microcatheter tip. Rapid, strong solidification of this substance permitted immediate occlusion. Embolization of fistulas has already been adopted in other contexts; however, application to ABPFs, although worthy of interest, requires accurate case selection and further experimentation.

In conclusion, our review disclosed several aspects of postoperative ABPFs. Among them, operative deaths were exclusively related to fistulas of the DTA; 5 patients with fistulas of the ascending aorta successfully underwent surgery [3, 22, 51, 60, 61] and 2 died before treatment [9, 54]. The overall surgical mortality rate was 15.3%.

Although in this setting more experience with endovascular repair and long-term follow-up would be desirable, our review suggests that stent grafting represents the tool of choice to treat postoperative ABPFs involving the DTA[69].


   References
Top
 Abstract
 Introduction
 Patients and methods
 References
 

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