Computed Tomographic Features of Pneumothorax Secondary to a Bronchopleural Fistula in Two Dogs

Introduction

Spontaneous pneumothorax is a condition in which air accumulates in the pleural space without either a traumatic or iatrogenic etiology.¹ The most common cause of spontaneous pneumothorax in dogs is rupture of bullae and blebs.^1–4 Other causes that have been reported in dogs include pulmonary neoplasia, dirofilariasis, pneumonia, pulmonary thromboembolism, pulmonary abscesses, and migrating foreign bodies. One of the possible ways in which pulmonary pathology can cause pneumothorax is through formation of a bronchopleural fistula (BPF). This is a communication between a bronchus and the pleural surface that allows air leakage into the pleural space.^1–3 This air leakage can result in either a tension or continuous pneumothorax, which occurs when there is continuous, progressive air accumulation in the pleural space. A pneumothorax can apply pressure to thoracic organs and can result in decreased venous return to the heart.^1,5–7 BPFs are reported to have varying etiologies in humans, including pulmonary infarction and neoplasia.

The cause of a pneumothorax is often not identified on thoracic radiographs.² Thoracic computed tomography (CT) can be used preoperatively to help identify the cause of the pneumothorax and to aid surgical planning, but studies on this technique are very limited. A prior study in dogs with ruptured bullae and blebs demonstrated that CT is more sensitive than radiographs for identification of bullae or blebs resulting in pneumothorax, although several lesions were not identified and one lung lobe was misidentified.² In people, CT can also be used to identify BPFs resulting in pneumothorax. To the authors’ knowledge, the appearance of BPF on CT and the use of CT to diagnose BPFs in dogs with pneumothoraces have not been described. The purpose of this study was to describe two dogs with continuous pneumothoraces in which BPFs were identified with CT.

Materials and Methods

Imaging Findings

Radiographs

Thoracic radiographs were obtained after pleural drain placement in both dogs. Case 1 had a persistent, severe, right-sided, tension pneumothorax; a mild left pneumothorax; and a small-volume pleural effusion. A left mediastinal shift was also present. An interstitial pattern in the left caudal lung lobe and alveolar pattern in all other lobes was consistent with atelectasis from the pneumothorax. Additionally, multiple round metal foreign bodies consistent with birdshot shotgun pellets were present along the right thorax and axilla. There was no radiographic evidence of either a right-sided cardiomegaly or pulmonary artery enlargement. Case 2 had a mild bilateral pneumothorax and a small volume pleural effusion. Right-sided cardiomegaly; main pulmonary artery enlargement; and enlarged, tortuous peripheral pulmonary arteries were present, consistent with the dog’s history of dirofilariasis. A diffuse interstitial pattern in case 2 was also seen and may have been due in part to atelectasis secondary to the pneumothorax, but the other primary differential diagnosis was eosinophilic pneumonitis secondary to heartworm disease.⁸

Echocardiography

Echocardiography was performed in case 2 because of the relatively recent diagnosis of heartworm disease and the cardiovascular changes detected radiographically. The right ventricle, right atrium, and main pulmonary artery were mildly, moderately, and severely distended, respectively. Numerous heartworms were present in the main pulmonary artery, mostly extending into the right branch. Due to the heavy worm burden and concern for an anaphylactoid reaction if a pulmonary lobectomy was performed, the patient was anesthetized and percutaneous, fluoroscopic- and echocardiographic-guided, mechanical worm embolectomy was performed. Twenty-one worms were removed. Echocardiography performed the following day prior to the thoracic CT demonstrated multiple persistent heartworms within the main pulmonary arteries.

Computed Tomography

Thoracic CT was performed in both dogs with a 16-slice multidetector CT unit^c. Helical image acquisition was 2.5 mm with a pitch of 1.375 and 0.938 in cases 1 and 2, respectively. Soft-tissue, lung, and high-resolution (bone algorithm with edge enhancement) algorithms were available. Both dogs received IV contrast medium^d (350 mg I/mL) at a dose of 770 mg I/kg. Images were reformatted into dorsal, sagittal, or oblique planes as needed utilizing a dedicated CT workstation^e.

Free air and a small amount of fluid were present in the pleural space of both dogs. The pneumothorax was considered moderate in case 1 and mild in case 2 at the time of CT. A left mediastinal shift was present in both dogs. A BPF was identified in the right caudal lung lobe of both dogs and the appearance was similar. In both dogs, along the caudodorsal aspect of the right caudal lung lobe, there was a focal, concave indentation of the lung margin with a thick, consolidated rim of parenchyma and thickening of the adjacent visceral pleura. A relatively straight, dilated subsegmental bronchus extended to the lung surface at the central aspect of the concavity and communicated with the pleural space, consistent with a peripheral BPF. In case 1, the fistula was not appreciated on transverse images but was clearly seen on dorsal and sagittal reformatted images (Figures 1A, B). In case 2, the fistula was apparent on the transverse images, as well as the dorsal and sagittal reformatted images (Figures 2A, B). Both dogs had additional ectatic bronchi within the area of the BPF. In case 1, several small, ectatic bronchi within the thick, consolidated rim of parenchyma were adjacent to, but not distinctly communicating with, the pleural space (Figure 1A), along with small mineral attenuating regions. Case 2 had a more focal rim of consolidation (peribronchovascular thickening) and a ground-glass opacity around the ectatic bronchus. Additionally, there was at least one other smaller, ectatic bronchus with similar peribronchial lung changes seen extending to the concave defect, but it did not appear to communicate with the pleural space (Figure 2B).

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In case 1, the visceral pleural margins of the right caudal lung lobe were thickened more extensively than in case 2 and were more irregular with a mildly undulating surface. The visceral pleural margins along the caudodorsal aspects of the accessory lung lobe were also affected, but less extensively. There also appeared to be an adhesion between the right caudal lung lobe and the diaphragm. A focal, short segment of the right caudal lobar pulmonary artery proximal to the BPF was mildly dilated. Also in case 1, multiple small, round, metal foreign bodies (shotgun pellets) were present in the superficial right thoracic soft tissues. One was within the right pleural space adjacent to the right middle lung lobe and another was present along the right dorsolateral pleural margin adjacent to the pleural cavity.

In case 2, the pulmonary arteries were enlarged, tortuous, and blunted, consistent with previously reported CT findings in dogs with heartworm disease.^8,9 Right ventricular, atrial, and main pulmonary artery enlargement were evident. A diffuse increase in lung attenuation (ground-glass opacity) was present, with more severe changes in the caudodorsal lung fields. In the left caudal lung lobe, there was a markedly dilated, nonenhancing artery that extended to the apex of a focal, pleural-based, wedge-shaped, nonenhancing region of consolidation, consistent with pulmonary thromboembolism and infarction.¹⁰ The pulmonary thromboembolism and infarction were considered secondary to dirofilariasis, but there was no visible communication with the pleural space in that area.

Discussion

To the authors’ knowledge, this is the first report describing CT findings of a BPF with continuous pneumothorax in dogs. BPFs are communications between a bronchus and the pleural space. In people, BPFs are categorized as either central or peripheral. Central BPFs involve either lobar or main bronchi and are secondary to either trauma or prior lung resection.^5–7 Peripheral BPFs involve more distal airways and result in a large-volume pneumothorax, continuous pneumothorax, or empyema.^5–7 Causes of peripheral BPFs in people include necrotizing infections, trauma (including barotrauma), surgery, bronchiectasis, infarction, malignancy, tuberculosis, and abscessation.^5–7

Confirmation of BPFs in dogs presents a diagnostic challenge, and BPFs are likely under diagnosed. BPFs have not been diagnosed histopathologically at the authors’ facility because a direct communication between bronchioles and the pleura has not been appreciated at a histopathological level. At surgery, a defect may be visible along the lung surface; however, confirming direct communication of the defect with a bronchus may not be possible at surgery given that the communicating bronchus is within the deeper parenchyma and may be small. A previous study (predominantly evaluating dogs postmortem) reported the formation of BPFs secondary to heartworm disease resulting in pneumothorax.¹¹ Histopathologically, cavitations were detected underneath thickened visceral pleura at the sites of pulmonary perforations detected grossly, but bronchial communication with the pleural space was not specifically described and bronchopleural communication may have been presumed due to the presence of pneumothorax.¹¹ That is opposed to bullae, which are histopathologically characterized by dilated alveoli and air-filled spaces (emphysema) and are grossly visible as focal, thin-walled, translucent, air-filled “bubble-like” or “blister-like” lesions.³ The confirmed diagnosis of a BPF therefore appears to be best attained via diagnostic imaging. CT, given the high spatial resolution and tomographic nature of the modality, would be the most appropriate modality to facilitate diagnosis of BPF. In people, CT is the imaging modality of choice for visualizing and characterizing BPFs.^5,6

In people, thin-section CT (i.e., 1–2 mm slice thickness) is more reliable than CT with standard slice thickness (8 mm) for identifying either direct or indirect signs of peripheral BPFs. Direct signs of peripheral BPFs include visualization of a tubular, air-filled fistulous tract consisting of an ectatic peripheral bronchus, communication between the pleural space and an airway, and the presence of air in the pleural space. Indirect signs include either localized pleural air or fluid accumulation with adjacent bronchiectasis, but no definitive communication between either the pleural space and airways or the presence of air bubbles beneath a bronchial stump following lobectomy.^5,7 Multiplanar reconstructions of CT images in a dorsal plane aids in demonstrating fistulas, and some fistulas may only be detected after reconstructions.⁵ Both of the dogs in the current report had CT examinations with thin slice thicknesses and multiplanar reconstruction of the images was performed. Multiplanar reconstructions were helpful in identifying the fistula, particularly the dorsal plane in case 1.

Foreign body migration has been reported as a cause for spontaneous pneumothorax in dogs.^4,12 CT findings of BPFs secondary to foreign body migration, however, is not specifically reported in the literature, except for brief mention in one study regarding diagnostic imaging findings with intrathoracic grass awn migration.¹² In that study describing radiographic, ultrasonographic, and CT findings of intrathoracic grass awn migration, pneumothorax was noted in 6 of 14 cases that had CT examination performed. There is also brief mention of one foreign body tract that could be followed from a peripheral bronchus in the left caudal lung lobe to the pleural surface, but no further description of a BPF was made.¹² In case 1, the histological changes in the affected lung lobe and presence of an adhesion at surgery were most consistent with previous foreign body migration; however, a foreign body was not found in that location at surgery. There were multiple birdshot shotgun pellets in the subcutaneous tissues of case 1 along with the pellet in the pleura near the right middle lung lobe. Potentially, a pellet passing through the right caudal lobe could have been responsible for the pulmonary changes that ultimately led to a BPF.

There are few other case reports of heartworm-associated pneumothorax in dogs (n = 20).^11,13–16 Similar to case 2, all of the dogs from the previously published studies presented in acute respiratory distress with or without collapse. A small volume of exudative pleural effusion was noted in 3 of 20 dogs and was present in case 2.¹¹ Also similar was the presence of a large volume of pleural air, with 18 of 20 dogs reported to have either a tension or continuous pneumothorax, which was worse on the right side in 17 dogs (as described in case 2).^11,13,16 The right caudal lung lobe was most commonly the source of air leakage (16 of 20 dogs).^11,14 The peripheral aspect of the right caudal lung lobe was abnormal in those 16 dogs. More specifically, a BPF was being present along the dorsal, peripheral aspect of that lobe in 15 of 20 dogs (although identification of direct communication between a bronchus and the pleural space was not specifically described).¹¹ The remaining 4 of 20 dogs had lesions in the left caudal lobe, left caudal and accessory lobes, right middle lobe, and the left cranial lobe. One of the two left caudal lobar lesions was also reported to occur in the dorsal peripheral aspect of the lung lobe.¹¹ The other reports (3 of 20 dogs) did not describe lesion localization more specifically than the lobe affected.^13–16 One dog had both left caudal and accessory lung lobectomies, but it was not clear whether lesions in one or both of those lobes contributed to the pneumothorax.³ Given that the pneumothorax was predominantly right-sided in that dog, it is possible that the accessory lobe lesion was the primary (or only) site of air leakage. One dog with a right caudal lobar lesion and the dog with both the left caudal and accessory lobectomies had CT performed. Possible blebs in the cranial lung lobes and multifocal bilateral pulmonary bullae were seen in those two dogs, respectively, but the specific source of air leakage was not identified.^14,16 Case 2 in this report had a ruptured bulla histopathologically identified on the lung surface, which may have contributed to the pneumothorax.

Exploratory thoracotomy with lobectomy was performed in 4 of 20 reported dogs with dirofilariasis-associated pneumothorax, while the remaining dogs either died or were euthanized. Interestingly, similar to case 2, heartworms were reportedly present at the transected end of the pulmonary artery in three of four dogs, and heartworms were extracted from the in situ pulmonary artery stump in one dog.^11,14–16 An anaphylactoid reaction associated with heartworm transection was reported in one dog.¹⁴ Given the high heartworm burden as determined by the severity of findings and the concern for anaphylaxis developing secondary to heartworm transection during lung lobectomy, mechanical worm embolectomy was performed prior to lung lobectomy with the goal of decreasing the risk of anaphylaxis.^11,14–18 Despite performing the worm embolectomy, multiple heartworms were present in the pulmonary artery stump following lobectomy in case 2, and transient hypotension occurred immediately following lobectomy, which may have been due to anaphylaxis from heartworm transection. Three of the four dogs from the prior case reports reported did well long term postoperatively. The fourth dog died 9 mo postoperative due to Dirofilaria-associated pulmonary thromboembolism and caval syndrome.^11,14–16

In dogs with dirofilariasis, the earliest vascular changes are noted in the right caudal lobar pulmonary artery.^8,9,11,18 This is thought to be due to its high blood flow volume and its anatomic conformation, being larger in diameter and longer in length than the left caudal lobar artery, extending from the main pulmonary artery in a relatively smooth arch compared with the relatively more acute angle of the left caudal lobar artery from the main pulmonary trunk.^8,9,11,18,19 Obstruction of the pulmonary arteries secondary to dirofilariasis most commonly initially occurs at the distal aspects of the right caudal lobar artery and may be due to the presence of dead worms, thrombi, or arterial wall thickening from intimal proliferation.^8,9,18,20 Collateral circulation from pulmonary arterial obstruction is from the bronchial arteries.²⁰ The dorsal basal aspect of the caudal lung lobes is farther from the beginning of the bronchial artery than other pulmonary regions, which may result in that region being more prone to ischemia and necrosis if the pulmonary artery is obstructed.¹¹ Additionally, if the obstruction was acute, there would not be enough time for collateral circulation from the bronchial arteries to develop.^11,20 Infarction may result in pulmonary parenchymal necrosis. Pulmonary necrosis may produce communication between either the parenchyma or a bronchus with the pleural space, producing a parenchymal-pleural fistula or BPF, respectively, allowing air leakage into the pleural space.^7,11,21 The predilection of the right caudal pulmonary arteries for increased heartworm burden, the associated increased susceptibility of the basal aspect of the right caudal lobar pulmonary arteries to obstruction, and the potential increased vulnerability of this region to secondary infarction and ischemia are likely contributing causes for BPFs to occur most frequently in the dorsal basal aspect of the right caudal lung lobe with dirofilariasis.

Conclusion

CT can aid in the diagnosis of patients with spontaneous pneumothorax due to peripheral BPFs, such as secondary to dirofilariasis or foreign body migration. Thin-slice acquisition and multiplanar reconstructions seem to be helpful in identifying BPFs.