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Imaging findings in 14 dogs and 3 cats with lobar emphysema

Abstract Background Lobar emphysema in dogs and cats is caused by bronchial collapse during expiration and subsequent air trapping. Congenital causes such as bronchial cartilage defects or acquired causes such as compressive neoplastic lesions have been reported. Morbidity results from hyperinflation of the affected lung lobe and compression of adjacent thoracic structures. Objective To describe patient characteristics and imaging findings in dogs and cats with lobar emphysema. Animals Fourteen dogs and 3 cats with lobar emphysema diagnosed by imaging findings were retrospectively identified from veterinary referral hospital populations over a 10‐year period. Methods Cases that included thoracic radiography, thoracic computed tomography (CT), or both were included. All images were reviewed by a European College of Veterinary Diagnostic Imaging diplomate. Relevant case information included signalment, clinical findings, treatment, and histopathology where available. Results Ten of 17 (59%) patients were presented for evaluation of dyspnea and 6 (35%) for coughing. Eleven (65%) patients were <3 years of age. The right middle lung lobe was affected in 12 cases (71%) and multiple lobes were affected in 7 cases (41%). Congenital lobar emphysema was suspected in 14 cases (82%). Conclusion and Clinical Importance Lung lobe hyperinflation, atelectasis of nonaffected lung lobes, mediastinal shift, and thoracic wall and diaphragmatic wall deformation were common findings. Lobar or multilobar emphysema should be considered in patients with dyspnea or coughing, particularly younger patients. Although radiography is useful, CT provides better detail. In older patients, acquired causes of bronchial compression should be considered.


| INTRODUCTION
Pulmonary lobar emphysema is rare in dogs and cats, and uncommon in humans, where it is most frequently identified during infancy and therefore often suspected to be congenital in nature. [1][2][3] Lobar emphysema is characterized by hyperinflation of ≥1 lung lobe because of bronchial obstruction and air trapping. During inspiration, negative airway pressure allows the affected bronchus to remain open. However, during expiration, the affected bronchus collapses, resulting in a 1way valve effect, with distension of the affected lobe because of accumulation of trapped air and subsequent compression of the adjacent lung lobes, heart, and mediastinal structures. 1 Progressive compression of these structures may result in rapid clinical deterioration because of cardiovascular and respiratory compromise or both.
Several cases of congenital lobar emphysema (CLE) are reported in the veterinary literature. Affected dogs and cats typically present as young animals with acute dyspnea. However, animals presenting with more chronic respiratory signs such as a cough, tachypnea, and exercise intolerance also have been reported. [4][5][6][7][8][9][10][11][12][13][14][15][16] In animals, antemortem diagnosis is achieved using radiography, computed tomography (CT) or a combination of these techniques. Lung lobectomy has been described for management of CLE, with a good outcome reported in 8 of 8 cases reported. [4][5][6][9][10][11]14,15 Congenital defects of bronchial cartilage commonly are associated with development of CLE in human infants. 2 Extramural bronchial obstructions, including vascular developmental abnormalities such as a pulmonary artery sling anomaly, also have been reported as causes of CLE. 1 In addition, lesions such as bronchogenic cysts or lymphadenopathy have been reported as causes of acquired lobar emphysema in human medicine. 3 Bronchial cartilage defects have been described histologically in dogs with CLE, similar to human patients. [4][5][6][7][8][9][10] Histopathology is helpful in determining the etiology of CLE secondary to bronchial cartilage hypoplasia or aplasia. [4][5][6][7][8][9]17 Previous information about cases of lobar emphysema in dogs and cats is limited to single case reports. The purpose of our study was to complement the existing literature in terms of patient characteristics, pathophysiological causes, and diagnostic imaging findings. Patients with thoracic radiography, thoracic CT, or both were included. Information regarding species, age, sex, body weight, breed, and presenting clinical signs were obtained from the medical records.

| MATERIAL AND METHODS
A diagnosis of lobar emphysema was based on imaging findings including diffuse enlargement of ≥1 lung lobe with rounded margins, generalized hypoattenuation or radiolucency and any consequent compressive effect on surrounding structures using either thoracic radiography or CT. Absence of surgical treatment or pathological confirmation were not considered exclusion criteria. Other forms of emphysematous lung disease such as asthma in cats were excluded after review of the images if findings were not consistent with lobar emphysema. Additional information including clinicopathological findings, additional diagnostic imaging, surgical intervention, and histopathological diagnosis also were reported where available.

| IMAGING STUDIES
Imaging studies were performed with the animal under sedation or general anesthesia. Diagnosis was based on radiography, CT, or a combination of both. Computed tomography was performed using All images were reviewed by a European College of Veterinary Diagnostic Imaging (ECVDI) board-certified radiologist (J. M.) and an ECVDI resident in diagnostic imaging (J. G.) using digital imaging and communications in medicine viewer software, RadiAnt. Lung and soft tissue reconstructions were reviewed and multiplanar reconstruction was used when beneficial. Reviewers were not blinded to the final diagnosis of lobar emphysema (as part of the inclusion criteria) but were blinded to the surgical and pathological diagnosis when these were available. Imaging findings were recorded directly into descriptive sheets that were specifically designed by the investigators for both radiography and CT images.
On radiographs, the affected lobe or lobes were identified and the severity of the radiolucency of the emphysematous lobe was subjectively scored as mild, moderate, or severe. The bronchus supplying the affected lobe was identified and abnormalities (collapse, bronchial wall thickening, bronchiectasis) were noted where visible. In addition, the size of the pulmonary vessels of the affected lobe was subjectively assessed. Where CT was used, the affected lobe or lobes were identified and the number of Hounsfield units (HU) of the abnormal lung tissue was estimated on precontrast images by calculating the mean score from 3 regions of interest placed over the emphysematous lung lobe, taking care to avoid bronchovascular structures. These results then were compared with the average attenuation HU of an adjacent unaffected lobe that had no evidence of hyperinflation or atelectasis. The affected area of the emphysematous lobe was subjectively scored for the severity of hyperinflation (mild, moderate, or severe). Additional changes in the affected lobe such as soft tissue or cavitatory lesions were recorded. The affected bronchus was identified and recorded and presence of collapse, obstruction, bronchial wall thickening, or bronchiectasis was noted.
For both radiography and CT studies, changes in other lobes then were described, including the presence of abnormal lung patterns or atelectasis. Atelectasis was suspected when decreased volume and concurrent increased soft tissue opacity of the lung lobe were present. Mediastinal shift, tracheal compression, diaphragmatic deformation, thoracic wall deformation, cardiac silhouette compression, pleural effusion, and pneumothorax were subjectively graded on a 0 (absent) to 4 (severe) scale. Other congenital abnormalities, lymphadenomegaly, and any additional abnormalities also were noted if identified.  Table 1. In 1 case, lobar emphysema was identified as an incidental finding during investigation of comorbid conditions. The duration of clinical signs ranged from 1 day to 10 years.

| Radiographic findings
Radiography of the thorax was performed in 7 patients (5 dogs and 2 cats) and the findings are summarized in Table 2. The affected lobe was readily identified in 3 cases. In the remaining 4 cases, it was more challenging to determine with certainty the affected lobe. In 3 of these cases, it was difficult to determine whether the right middle lobe, right cranial lobe, or both were affected ( Figure 4).
The radiolucency of the emphysematous lobe was graded as moderate in 6 cases and mild in 1 case. The affected lobe enlargement was scored as moderate in 6 cases and mild in 1 case. Cavitary lesions or soft tissue lesions within the affected lobes were not visualized on radiography. Collapse of the affected bronchus was visualized radiographically in  (3 dogs).
An unstructured interstitial lung pattern was identified in the nonemphysematous caudo-dorsal lung fields in 4 cases (2 dogs and 2 cats).
Atelectasis of nonemphysematous lung lobes was visible in 6 cases
The mean attenuations of the emphysematous lung and nonemphysematous normal lung are presented in Table 3.   Effects on the remaining thoracic structures were readily identified by CT and notable changes included flattening of the diaphragm, thoracic wall deformation and mediastinal shift (Figure 2). In addition, pleural effusion and pneumothorax were identified in several dogs. Pneumothorax is recognized as a possible complication of lobar emphysema in people and previously has been reported in a dog. 6,18 The potential for development of tension pneumothorax because of the valve effect of the collapsed bronchus may result in rapid decompensation.
Differentiating between pneumothorax and lobar emphysema is important clinically. In previous studies, cases of CLE in human infants initially have been mistaken for pneumothorax. 3,19,20 Cases with CLE were likely to show hyperlucency of the affected lobe with concurrent mediastinal shift, flattening of the diaphragm, widening of the rib space and atelectasis of the remaining lobes, features that may be misdiagnosed as tension pneumothorax. 19 The presence of bronchovesicular markings in the region of hyperlucency, however, is highly suggestive of CLE rather than tension pneumothorax, where no such markings are present. 19 These findings consistently were identified in our cases with superior accuracy using CT.
Images obtained using radiography allowed a diagnosis of lobar emphysema to be made in all cases, but specific lobe identification was inconsistent. In addition, it was not possible in most cases to identify the collapsed or obstructed bronchus leading into the emphysematous lung lobe. Atelectasis of an adjacent lung lobe was identified in most cases using radiography. Mediastinal shift, thoracic wall deformation, and flattening of the diaphragm also were readily identified using radiography. In the 16 individual cases previously reported in the veterinary literature, the right middle lung lobe was most frequently affected. [4][5][6][7][8][9][10][11][12] Right middle lung lobe involvement also was a consistent finding in our study (Figure 3, Figure 5)  Histopathology, including both the emphysematous lobes and nonaffected bronchi, would be required to establish the validity of this hypothesis. It is unknown why the right middle lung lobe is the most commonly affected lobe. The right middle lung lobe, however, is also commonly affected by lung lobe torsion, which is thought to be caused by the narrow shape and high mobility of this lobe. 23 The increased mobility of the right middle lobe combined with cartilage hypoplasia may contribute to the predilection for CLE in this lobe.
Unsurprisingly, no specific clinicopathological findings were associated with the presence of lobar emphysema. Complete hematology, biochemistry, and urinalysis results, however, were not available for all patients, which limits the assessment of their utility.
In previous case reports, several patients underwent surgical treatment with lobectomy of the affected lobe. 5,[9][10][11] Postoperative follow-up of 15 months in a dog and 36 months in a cat without recurrence of clinical signs were reported. 3,8 However, in cases where surgery was not performed, the condition resulted in rapid deterioration and death or euthanasia. 5,7,8,12,13,22 Although long-term outcomes were not available in our study, a similar proportion underwent surgical lobectomy with 80% (8/10) survival to discharge.
Limitations of our study include its retrospective design leading to bias in the recruitment of cases. Many cases had incomplete records with inconsistent availability of clinicopathological or histopathological information. Information regarding clinician selection of F I G U R E 3 Transverse computed tomographic image in lung window (WL À500, WW 1400) of two dogs, A,B, and a cat, C, with congenital lobar emphysema (CLE) of the right middle lung lobe. Note the collapsed right middle bronchus (black arrows) and atelectasis of the remainder of the lung lobes (*) F I G U R E 4 Dorsoventral radiograph of the thorax of a dog with congenital lobar emphysema (CLE) of the right middle lung lobe. Note the enlarged and hyperlucent lung lobe (*), expanded right side of the rib cage (black arrowheads) and compressed right diaphragmatic crus (black arrow). It was not possible to determine which lobe was emphysematous based on the radiographs alone either radiography or CT was not available. Information regarding the use of breath holding during CT image acquisition was not available in most patients, and this technique may affect the severity of lung lobe hyperinflation and HU values. Only a small number of cases underwent both radiography and CT and therefore direct comparison of these modalities was not possible. A diagnosis of lobar emphysema was based on the imaging findings and where available was confirmed on histopathology. In some cases, however, histopathology was not available, and therefore the underlying pathology could not be determined. This factor may be particularly relevant in cases that underwent thoracic radiography, where more subtle lesions may not be identifiable.

| CONCLUSION
Lobar or multilobar emphysema is a rare disease in both dogs and cats and should be considered as a differential diagnosis in patients presenting with dypsnea and or coughing, particularly young patients.
Radiography is useful in diagnosing most cases, but CT is likely to provide additional details and allow for better surgical planning. In older patients with lobar emphysema, secondary extramural compressive causes should be considered, and CT should be favored over radiography whenever feasible. Although long-term follow-up was not possible in our study, it is likely that surgical treatment, where indicated, will be associated with a favorable outcome.

ACKNOWLEDGMENT
No funding was received for this study. An abstract poster presentation of data from this study was presented at the European College of Veterinary Internal Medicine-Companion Animals Congress, September 2020, Virtual Congress.

CONFLICT OF INTEREST DECLARATION
Authors declare no conflict of interest.

OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.

INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE (IACUC) OR OTHER APPROVAL DECLARATION
Retrospective collection and analysis of cases was approved by the Veterinary Research Ethics Committee of the Institute of Veterinary Science, Leahurst Campus, Neston, South Wirral, United Kingdom (reference VREC766).

HUMAN ETHICS APPROVAL DECLARATION
Authors declare human ethics approval was not needed for this study.