Introduction

Brachycephalic obstructive airway syndrome (BOAS) in brachycephalic dogs has been well described in the veterinary literature.^1–7 Aberrant nasal turbinates, a thickened and elongated soft palate, everted laryngeal saccules and tonsils, a hypoplastic trachea, and bronchial collapse are some of the anatomic anomalies that have been commonly identified in these patients.^1,2,4–11

Diagnostic imaging is commonly performed on patients with BOAS prior to corrective airway surgery to identify any comorbidities or anatomic variants that may impact the outcome^7,12 or influence surgical planning.¹³ CT allows for 3-D evaluation of the upper and lower airways and other structures of the cranium and thoracic cavity without the superimposition of organs. In our institutions, we have observed that bronchial wall thickening (BWT) is commonly seen on CT images of brachycephalic dogs presented for upper airway corrective surgery and that many of these patients have no obvious clinical signs related to lower airway disease, such as coughing or expiratory wheezing.¹⁴

In humans, BWT is often associated with pulmonary diseases such as chronic obstructive pulmonary disease¹⁵ and asthma.^16,17 There is also a correlation between obstructive sleep apnea and BWT in patients with no history of respiratory disease. This is believed to be due to an alteration of the oxidative balance secondary to repeated hypoxic episodes, which causes inflammation of the bronchial wall.¹⁸ BWT in dogs is often associated with chronic inflammatory airway diseases such as chronic bronchitis.^19,20 However, these patients typically present with a history of persistent cough.¹⁴ To the authors’ knowledge, there has been no published assessment of a potential relationship between BWT and brachycephalic conformation in dogs with or without clinical signs of BOAS.

Bronchial collapse is associated with brachycephalic conformation, with the Pug being the most commonly affected breed.¹¹ Bronchial collapse has also been observed on CT images of healthy Beagles during the expiratory phase and is considered to be a normal variant.²¹ However, in a recent study²² of CT bronchial collapsibility ratio, healthy brachycephalic dogs had higher collapsibility ratios than did Beagles.

The objectives of the study reported here were to assess the prevalences of BWT and bronchial collapse in brachycephalic dogs with and without BOAS that did not have evidence of pulmonary disease and to compare those prevalences with prevalences in nonbrachycephalic (ie, mesocephalic and dolichocephalic) dogs.

Materials and Methods

The study protocol was approved by the Veterinary School Research Ethics Committee of the University of Liverpool (approval No. RETH 000765 and RETH 1438). The clinical records of the University of Liverpool Small Animal Teaching Hospital were reviewed to identify brachycephalic dogs examined between March 2011 and August 2019 that underwent CT imaging of the thorax prior to BOAS surgery or as part of a medical workup.

The history of dogs considered for inclusion in the study was checked for any mention of clinical signs of upper respiratory disease. Brachycephalic dogs with BOAS (BOAS group) were eligible for inclusion in the study if they had a history of clinical signs of upper airway obstruction (eg, dyspnea, exercise intolerance, cyanosis, stridor or stertor, collapsing episodes, nasal discharge, reverse sneezing, episodes of syncope, and snoring) and had undergone thoracic CT (with or without CT of the head) as a diagnostic test or as part of the surgical planning. Patients with any history of BOAS surgery were excluded from the study. Brachycephalic dogs without BOAS (BDWB group) were eligible for inclusion in the study if they did not have any recorded clinical signs of BOAS in their history and had undergone CT of the thorax (with or without CT of the head) for staging of diseases unrelated to the respiratory tract. From the same database and time period, we selected a control group of nonbrachycephalic dogs with no clinical or CT findings of upper or lower respiratory tract disease that weighed between 5 and 27 kg (ie, similar to the typical weight of brachycephalic breeds chosen for the study).

Data collection and review of CT images

For each dog included in the study, information was collected on signalment, clinical signs, and duration of the clinical signs. Head (when available) and thoracic CT images had been acquired with a 4-slice CT scanner (Somatom; Siemens Healthcare Diagnostics) or an 80-slice CT scanner (Aquilon Prime 80; Toshiba Medical Systems Corp) through the use of a standardized institutional protocol. For imaging, all patients were placed in sternal recumbency and anesthetized or heavily sedated. The decision of whether to anesthetize or sedate each individual dog was made by the attending anesthetist or clinician. No manual lung inflation was performed during image acquisition.

Slice thickness, pitch, and collimation varied among scanning sessions. Images were reconstructed with lung and soft tissue reconstruction algorithms for the thorax and bone and soft tissue reconstruction algorithms for the head. In some patients, images were acquired before and after IV administration of iodinated contrast medium (Xenetix; Guebert Laboratories Ltd; Optiray; Guebert Laboratories Ltd) at a dose of 2 mL/kg via a cephalic vein. Bronchi and the trachea were assessed on precontrast images with a lung reconstruction algorithm. The remaining structures were assessed on pre- and postcontrast images with soft tissue reconstruction algorithms.

Images were anonymized and assessed with medical imaging software (RadiAnt; Medixant) by a veterinary radiologist board certified by the European College of Veterinary Diagnostic Imaging (FS) who was blinded to the group category, history, signalment, and final diagnosis. A subjective CT scoring system was used to assess the presence and severity (mild, moderate, or marked) of BWT (Figure 1). The distribution was classified as focal, multifocal, or generalized. Affected lobes and the total number of affected lobes were also recorded. Bronchial collapse was assessed subjectively as present or absent (Figure 2). The presence of bronchiectasis was documented, with bronchiectasis defined as a lack of peripheral airway tapering.²³ Lymphadenomegaly was defined as a short-axis diameter on transverse images > 12 mm.²⁴ Enlargement of the pulmonary lobar vessels was subjectively assessed by comparison with the corresponding bronchial diameter. Main pulmonary artery enlargement was assessed by calculating the pulmonary trunk-to-aorta (PT:Ao) ratio as previously described.²⁵ Whether pulmonary atelectasis was present and, if so, the affected lobes were recorded, and its severity was subjectively graded as mild (occasional small areas of ground glass attenuation or a parenchymal band with mild loss of volume), moderate (several areas of ground glass or soft tissue attenuation, moderate loss of volume, and parenchymal bands), or severe (partial collapse and soft tissue attenuation of several lung lobes). Bronchial plugging, tracheal collapse, tracheal exudate, thymic remnant, and the number of malformed vertebrae were also recorded when present. The tracheal diameter-to-thoracic inlet ratio was calculated as previously described.²⁶

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Transverse thoracic CT images of bronchi (arrows) in dogs with normal bronchial wall thickness (A) and with mild (B), moderate (C), and marked (D) bronchial wall thickening of a dog. Images are displayed in a lung window (window level, –500 HU; window width, 1,400 HU).

Citation: Journal of the American Veterinary Medical Association 261, 1; 10.2460/javma.21.10.0448

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Transverse (A), sagittal (B), and dorsal (C) CT images of a brachycephalic dog. Bronchial collapse can be observed in the cranial portion of the left cranial lung lobe (arrows). There is also generalized bronchial wall thickening (dashed arrows). Images are displayed in a lung window (window level, –500 HU; window width, 1,400 HU).

Citation: Journal of the American Veterinary Medical Association 261, 1; 10.2460/javma.21.10.0448

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The thoracic width-to-height ratio was calculated by dividing the maximum height (from the inner margin of T11 to the inner margin of the sternum at the same level) by the maximum width (from the inner margin of one costophrenic recess to the inner margin of the other costophrenic recess) of the thoracic cavity. The skull index was calculated as previously described.²⁷ Aberrant turbinates were identified and graded as described by Vilaplana Grosso et al.⁶

Results

A total of 85 dogs were included in the study. Fifty-six brachycephalic patients (30 with BOAS [BOAS group] and 26 without BOAS [BDWB group]) met the inclusion criteria. Breeds of dogs in the BOAS group consisted of French Bulldog (n = 22), English Bulldog (4), Pug (3), and Shih Tzu (1). Breeds of dogs in the BDWB group consisted of Shih Tzu (n = 11), English Bulldog (6), French Bulldog (4), Pug (3), Boston Terrier (1), and Lhasa Apso (1). For dogs in the BOAS group, sexually intact males were most common (n = 15), followed by neutered males, sexually intact females, and neutered females (5 each). For dogs in the BDWB group, neutered females were most common (n = 11), followed by neutered males (8), sexually intact males (6), and sexually intact females (1). Median age for dogs in the BOAS group was 2.5 years (IQR, 0.75 to 7.9 years), median body weight was 12.2 kg (IQR, 5 to 36 kg), and median BCS was 4 (IQR, 2 to 7). Median age for dogs in the BDWB group was 7.8 years (IQR, 0.7 to 13.7 years), median body weight was 13.6 kg (IQR, 3.7 to 49 kg), and median BCS was 5 (IQR, 3 to 9).

Twenty-eight control dogs met the inclusion criteria. Breeds of control dogs consisted of English Springer Spaniel (n = 4), Schnauzer (3), Cocker Spaniel (3), and Border Collie (3), with the remaining dogs representing a variety of breeds. Neutered males were the most common (n = 10), followed by neutered females (9), sexually intact males (7), and sexually intact females (2). Median age was 6 years (IQR, 0.6 to 13 years), median weight was 15.4 kg (IQR, 7 to 26 kg), and median BCS was 5 (IQR, 3 to 8).

There was a significant (P < 0.001) difference in age among groups, with dogs in the BOAS group being the youngest. There were no significant differences in weight (P = 0.13) or sex (P = 0.067) among groups.

Discussion

To the authors’ knowledge, the present study is the first to describe BWT as a common CT finding in brachycephalic dogs. BWT is typically related to inflammatory bronchial disease, with chronic bronchitis being the most common cause.^19,20 However, Mortier et al²⁰ demonstrated that BWT is not always present on CT images of patients with chronic bronchitis; therefore, chronic bronchitis remains a diagnosis of exclusion. Chronic bronchitis was considered unlikely in our brachycephalic population, because one of the exclusion criteria was a history or presence of clinical signs suggestive of lower respiratory tract disease. However, subclinical chronic bronchitis could not be excluded in our population.

A relationship between obstructive sleep apnea and BWT has been reported in people.¹⁸ Human patients with sleep apnea have been compared to English Bulldogs in the past, establishing similar findings and physiologic changes between human and canine patients.²⁸ BWT in humans with obstructive sleep apnea is believed to be due to an alteration of the oxidative balance secondary to repeated hypoxic episodes, which leads to the development of inflammation of the bronchial wall.¹⁸ However, further investigations are warranted to explain these bronchial changes. In our study, the cause of BWT was not investigated. A histopathologic and comparative analysis between groups would have offered further information. However, owing to the study design and ethical considerations, this was not feasible.

In our control group, 10 of 28 (35.7%) dogs had mild BWT, but none of the control dogs had moderate or marked thickening. This was an unexpected finding because BWT was not identified in the reports that were initially issued at the time CT was performed. Considering that the mean age of dogs in the control group was higher than that for dogs in the BOAS group and that chronic bronchitis is often diagnosed in older patients, it is possible that some patients in the control group could have had subclinical chronic bronchitis. CT changes in the lungs associated with aging in dogs have been described; however, BWT was not reported as an aging change.²⁹

There was a significant correlation between body weight and the presence of BWT on multivariable analysis in the present study. It is interesting to note that dogs with a higher BCS also have a higher chance of manifesting BOAS than do dogs with a lower BCS, and we could hypothesize that these correlations may be interrelated.¹

In previous publications^19,20 in which the bronchial wall-to-pulmonary artery ratio was used to identify BWT in patients with chronic bronchitis, a negative correlation was identified between the ratio and patient body weight. It was suggested by Mortier et al²⁰ that as the size of the patient increases, the pulmonary artery diameter increases proportionally more than the bronchial wall thickness. Contrasting these results, in the present study, a positive correlation was noted between BWT and patient body weight. The possible explanation for this finding is that larger patients are likely to have proportional thicker bronchial walls in comparison to smaller patients. It is also interesting to note that dogs in our BOAS group had a median BCS of 4, compared with a median BCS of 5 for both the BDWB and control groups. In the study by Liu et al,³⁰ the authors concluded that young age and a normal BCS were some of the factors that would indicate a poor prognosis after BOAS surgery. The population of the BOAS group in our study presented these 2 factors. However, outcome of the patients was not assessed in our study; therefore, a possible relationship between bronchial changes and prognosis would require further studies.

BWT was more frequently identified in French Bulldogs (24/56) than in the other brachycephalic breeds in the present study, suggesting that BWT may be more common in French Bulldogs than other brachycephalic breeds. However, breed was only identified as significant on univariable analysis and not on multivariable analysis.

Bronchial collapse was mainly observed in the BOAS (17/30) and BDWB (17/26) groups in the present study, with the control group having only a small number of cases (3/28). In the study by De Lorenzi et al,¹¹ the authors suggested that bronchial collapse is a common finding in brachycephalic breeds, with 87.5% of cases presenting some degree of bronchial collapse. They also identified that the left cranial bronchus with its respective subdivisions was most commonly affected and that Pugs were the most frequently affected breed. In the same study,¹¹ the authors suggested that as a result of BOAS, there is an increase in transmural pressures during exhalation, which leads to chronic airway compression and should be considered bronchial stenosis rather than bronchial collapse. Another publication³¹ suggests that the barrel-chest conformation of this breed predisposes the left mainstem bronchus to be embedded between the aorta and left atrium, which causes chronic compression of the bronchus. In the present study, the left cranial bronchus was the most commonly affected in both the BOAS and BDWB groups, which agrees with the past literature.^11,31 Our data also showed a significant (P < 0.01) relationship between bronchial collapse and brachycephalic conformation. In both the BOAS (17/30 [56.7%]) and BDWB (17/26 [65.4%]) groups, there were similar proportions of patients with bronchial collapse. This would suggest that it is unlikely that the severity of BOAS is directly associated with bronchial collapse.²² There was also no significant association between bronchial collapse and the thoracic width-to-height ratio, which could indicate that thoracic conformation may not be related with bronchial collapse. However, further studies are needed to confirm these findings.

There were several limitations to the present study. Owing to the retrospective nature of the data acquisition, CT images of the head were not available for several cases, which could have affected the statistical analyses. However, we believe that the number of patients with CT images of the head was sufficient to warrant its inclusion in the statistical analysis. Another limitation attributable to the retrospective nature of the study was that classification of dogs in the BOAS and BDWB groups relied on the history and clinical signs of the dogs. Owners may not identify some of the clinical signs of BOAS; therefore, it is less likely that these would be discussed with the clinician and recorded in the history, especially if the dog was presented with a complaint unrelated to the respiratory tract.³² Classifying patients with some of the published methods would have increased the accuracy and improved patient selection for the brachycephalic groups.^33,34 Clinical grading would have also aided establishing a potential relationship between bronchial changes and severity of BOAS. However, it is very likely that most dogs in the BOAS group were more severely affected than those in the BDWB group. Further studies, more likely of a prospective nature, would be interesting to confirm our findings and to try to find associations between clinical grade of BOAS and bronchial changes.

In the present study, only a single observer evaluated and graded the CT images, and interobserver agreement in the detection of BWT is only moderate, as previously reported by Mortier et al.²⁰ However, the purpose of our study was not to assess the reliability of CT in detecting bronchial changes, as this was a descriptive study. We also chose a subjective assessment of BWT because previous publications have suggested that objective methods of measuring BWT are unreliable.²⁰

There was a difference in age between the BOAS group and the BDWB and control groups in the present study. Median age for the BOAS group was 2.5 years, compared with 7.8 and 6 years for the BDWB and control groups, respectively. However, patient age was not significantly associated with BWT or bronchial collapse. In the study by Hornby and Lamb,²⁹ the authors concluded that older dogs were more likely to have heterotopic bone and may have been more prone to lung lobe collapse than young dogs, but this should not contribute to misdiagnosis of pulmonary disease.

Our initial study design planned to include patients of similar weight and size for all 3 groups, which should have aided in homogenizing the population. However, thoracic CT images of dogs with no respiratory signs were much more common for older dogs.

Owing to the retrospective nature of the study, an anesthesia or sedation protocol was not established. Placement of an endotracheal tube may have affected the results of our study. A higher proportion of dogs in the BOAS group were anesthetized, rather than sedated, in comparison to the other groups. However, no significant relationship was established between type of anesthesia and either BWT or bronchial collapse.

A histopathologic or cytologic comparison of bronchial walls between groups would have been useful to confirm the hypothesis that BWT and bronchial collapse are more common in brachycephalic dogs, especially dogs with BOAS, and to understand the pathologic process. However, sampling of the bronchial wall or bronchoalveolar lavage was not available in these patients owing to the retrospective nature of the study. Further studies are needed to understand the nature of some of these changes.

In conclusion, BWT and bronchial collapse should be considered common findings in brachycephalic dogs with or without clinical signs of BOAS. BWT was also more frequent in the BOAS group.