This study was supported in part by the Center for Imaging Sciences, UC Davis, School of Veterinary Medicine.
QUANTITATIVE AND QUALITATIVE COMPUTED TOMOGRAPHIC CHARACTERISTICS OF BRONCHIECTASIS IN 12 DOGS
Article first published online: 11 APR 2013
© 2013 Veterinary Radiology & Ultrasound
Veterinary Radiology & Ultrasound
Volume 54, Issue 4, pages 351–357, July/August 2013
How to Cite
Cannon, M. S., Johnson, L. R., Pesavento, P. A., Kass, P. H. and Wisner, E. R. (2013), QUANTITATIVE AND QUALITATIVE COMPUTED TOMOGRAPHIC CHARACTERISTICS OF BRONCHIECTASIS IN 12 DOGS. Veterinary Radiology & Ultrasound, 54: 351–357. doi: 10.1111/vru.12036
- Issue published online: 17 JUL 2013
- Article first published online: 11 APR 2013
- Manuscript Accepted: 24 FEB 2013
- Manuscript Received: 16 JUL 2012
- Center for Imaging Sciences
- UC Davis
- School of Veterinary Medicine
- bronchoarterial ratio;
Bronchiectasis is an irreversible dilatation of the bronchi resulting from chronic airway inflammation. In people, computed tomography (CT) has been described as the noninvasive gold standard for diagnosing bronchiectasis. In dogs, normal CT bronchoarterial ratios have been described as <2.0. The purpose of this retrospective study was to describe quantitative and qualitative CT characteristics of bronchiectasis in a cohort of dogs with confirmed disease. Inclusion criteria for the study were thoracic radiography, thoracic CT, and a diagnosis of bronchiectasis based on bronchoscopy and/or histopathology. For each included dog, a single observer measured CT bronchoarterial ratios at 6 lobar locations. Qualitative thoracic radiography and CT characteristics were recorded by consensus opinion of two board-certified veterinary radiologists. Twelve dogs met inclusion criteria. The mean bronchoarterial ratio from 28 bronchiectatic lung lobes was 2.71 ± 0.80 (range 1.4 to 4.33), and 23/28 measurements were >2.0. Averaged bronchoarterial ratios from bronchiectatic lung lobes were significantly larger (P < 0.01) than averaged ratios from nonbronchiectatic lung lobes. Qualitative CT characteristics of bronchiectasis included lack of peripheral airway tapering (12/12), lobar consolidation (11/12), bronchial wall thickening (7/12), and bronchial lumen occlusion (4/12). Radiographs detected lack of airway tapering in 7/12 dogs. In conclusion, the most common CT characteristics of bronchiectasis were dilatation, a lack of peripheral airway tapering, and lobar consolidation. Lack of peripheral airway tapering was not visible in thoracic radiographs for some dogs. For some affected dogs, bronchoarterial ratios were less than published normal values.
Bronchiectasis is an irreversible dilatation of the bronchi resulting from chronic airway inflammation that damages elastic components of the bronchi leading to bronchial wall destruction and impaired clearance of respiratory secretions.[1-4] It is considered a unique disease entity though certain developmental and acquired conditions are associated with and likely cause bronchiectasis.[2-4] Congenital disorders predisposing to bronchiectasis in dogs include primary ciliary dyskinesia (PCD)[5-10] and Kartagener's syndrome.[11, 12] Acquired disorders include chronic bronchitis, chronic infectious pneumonia, eosinophilic bronchopneumopathy, and bronchial obstruction.[13-18] Chronic bronchial inflammatory disease has been suggested as the most common etiology associated with bronchiectasis in cats.[15, 17] Recognition of bronchiectasis as a component of, or a sequelum to, underlying pulmonary disease is important because dogs with this condition are at increased risk for developing recurrent pulmonary infections due to decreased mucociliary clearance.[18, 19]
Primary CT features of bronchiectasis in people have been extensively characterized and include abnormal bronchial dilation, lack of peripheral bronchial tapering, and identification of distinct airways within 1 cm of the pleural surface. Secondary features of bronchiectasis include bronchial wall thickening, mucus plugging within the bronchial lumen, and peripheral air trapping as reflected by measurable reduced pulmonary density in affected regions.[2, 3] In people, the most widely used CT criterion for quantifying abnormal bronchial dilation is a bronchoarterial ratio (BA, ratio of the cross-sectional bronchial luminal diameter to accompanying pulmonary artery diameter) >1. [2, 3, 20] In contrast, a recent study revealed that dogs without clinical pulmonary disease can have a bronchoarterial ratio up to 2.0.
Radiographic and bronchographic characteristics of bronchiectasis in dogs have been described previously [13, 14, 17, 19] and there is a single case report describing CT diagnosis of bronchiectasis. However, to our knowledge, there are no larger clinical studies devoted to the CT features of the disorder. The purpose of this retrospective study was to describe quantitative and qualitative CT imaging features in a group of dogs with confirmed bronchiectasis based on histopathology and/or bronchoscopy. Our hypotheses were that the bronchoarterial ratios of bronchiectatic airways would be larger than those of normal bronchi and that these abnormal bronchi would have a bronchoarterial ratio ≥2.0.
Materials and Methods
The University of California Davis Veterinary Medical Teaching Hospital medical records database was searched for dogs with a clinical diagnosis of bronchiectasis between 2002 and 2010. Retrieved records were further screened for dogs meeting inclusion criteria of contemporaneous thoracic radiographs, CT examinations and confirmation of bronchiectasis by histopathology and/or bronchoscopy. Breed, body weight, gender, age, and underlying/associated disease processes were recorded for all included dogs.
Bronchoscopy reports and images were retrieved and reviewed by two of the authors (MSC, LRJ). All bronchoscopic exams had been performed by, or under the direct supervision of, an experienced bronchoscopist (LRJ) according to a standardized institutional protocol. Bronchoscopy was performed using a flexible fiberoptic endoscope with fourway flexion.(Pentax FG16X or V 5.5 mm × 85 cm fiberoptic endoscope, Montvale, NJ) All airways were evaluated in sequence and static images and video recordings were obtained. The presence, location, and severity of abnormal airway diameter (dilation or narrowing/collapse), mucus plugging, and intraluminal masses were recorded based on a consensus opinion. Bronchiectasis was defined as a subjective increase in space within the airways in relationship to airway walls and thinning of airway bifurcations indicative of gross airway dilation.
Histopathologic specimens were retrieved and systematically reviewed by a board certified pathologist (PAP) for evidence of bronchial dilatation, thickness and character of bronchial wall, epithelial, and goblet cell hyperplasia and subepithelial inflammation. Lung samples were obtained based on lesions observed during surgical exploration or necropsy and fixed by immersion in 10% neutral buffered formalin. Fixed samples were dehydrated, embedded in paraffin wax, sectioned at 4 μm, and stained with haematoxylin and eosin (HE). Histopathology sample sites and sizes were not standardized and samples were not matched with CT lesions at the time of collection. In those dogs for which only alveolar parenchyma or pleura samples were available, the cause of pneumonia was characterized but not the histological features of bronchiectasis.
Thoracic radiographic examinations were obtained using a minimum of two views, including dorsal-ventral and right-lateral projections. Radiographs were taken at end inspiration, with the neck extended and the legs extended forward and with standard high kVp and low mAS thoracic exposure factors. Radiographic studies included a mix of conventional film radiographs and DICOM digital images. Pulmonary CT studies had been acquired with a helical CT scanner (fx/I helical CT scanner General Electric Co., Milwaukee, WI) using a standardized institutional protocol. Briefly, examinations were performed with dogs in sternal recumbency under general inhalational anesthesia using a single forced breath-hold technique, with airway pressure held at 15 cm of water and scan times of 60 seconds or less. All examinations consisted of contiguous, 5–7 mm collimated axial images (depending on patient size) using a moderately edge-enhancing (lung) reconstruction algorithm.
Quantitative CT Image Analysis
A single observer (MSC) retrieved DICOM CT images for each dog and reviewed them on a dedicated image viewing station using commercially available viewing and analysis software. (efilm 2.0, Milwaukee, WI) Bronchoarterial (BA) ratio measurements were obtained for each dog using the technique previously described in a report on clinically normal dogs. Transverse CT images were used for all measurements. Window width and level settings used for the measurements were operator controlled and varied depending on whether lung was regionally aerated or consolidated. The six locations measured were the lobar bronchi for the right cranial middle, and caudal lung lobes; and lobar bronchi for the cranial and caudal parts of the left cranial lobe and the left caudal lung lobe. When measuring bronchoarterial ratios from bronchiectatic lung lobes, histopathology and bronchoscopy results were reviewed and used to guide selection of locations for CT measurement of bronchiectatic airways.
Qualitative Thoracic Radiography and CT Image Analysis
Thoracic radiography and CT examinations for each dog were retrieved and reviewed by two board certified radiologists (MSC, ERW). Readers were aware of the clinical diagnosis of bronchiectasis at the time of interpretation. Qualitative imaging features of bronchiectasis were defined by consensus. The following parameters were recorded: lack of peripheral airway tapering, lobar consolidation, bronchial wall thickening, and bronchial lumen occlusion. For CT images, lack of peripheral airway tapering was determined subjectively and based on a single transverse CT image for bronchi visible in a long-axis orientation or based on multiple consecutive transverse images for bronchi visible in a short-axis orientation. Lobar consolidation was defined as alveolar infiltration of a lung lobe. Bronchial wall thickening was defined by subjective comparison with the bronchial wall thickness in other unaffected lobes. Bronchial lumen occlusion was defined as the presence of intraluminal soft tissue dense debris or fluid accumulation. The distribution of disease was designated as either focal (one lung lobe) or multifocal (more than one lobe) in each dog, and the bronchiectatic airways were described as either cylindrical or saccular. Other imaging features such as pleural disease, intrathoracic lymphadenopathy, or pulmonary nodules/masses were also recorded. For thoracic radiographic images, the following characteristics were recorded by consensus: saccular bronchiectasis, nontapering airways, bronchial wall thickening, bronchial lumen occlusion, and pulmonary consolidation. Observers were unaware of CT findings at the time of radiographic interpretation.
Statistical tests were selected and performed by one of the authors (PHK) using commercially available statistical analysis software (Graphpad Prism 5.0, San Diego, CA). Range, mean, and standard deviation values were calculated for all bronchoarterial ratio measurements, both by lung lobe and in aggregate. The average bronchoarterial ratio measurements from each lung lobe were compared using a Friedman's analysis of variance test to determine whether differences existed between anatomic sites. The average bronchoarterial ratio of bronchiectatic and nonbronchiectatic lung lobes was calculated for each subject and the resulting data from all subjects were compared using an unpaired t-test. Significance was set at P < 0.01 for both analyses.
A total of 12 dogs met the inclusion criteria. The diagnosis of bronchiectasis was confirmed based on bronchoscopy in eight dogs and histopathology in four dogs. Median age of affected dogs was 9 years (range 3 to 13). Body weight ranged from 8.3 to 46 kg, with a median weight of 31.3 kg. Breeds included were German Shepherd Dog (two); and one each of Golden Retriever, Labrador, Rottweiler, Cocker Spaniel, Rough Coated Collie, Australian Shepherd, Husky, Malamute, Fox Terrier, and Bernese Mountain Dog. Seven dogs were spayed females, and 5 were neutered males. Based on available clinical data, the cause of bronchiectasis was ascribed to chronic unresolved pneumonia (likely aspiration related) in 6 dogs; eosinophilic bronchopulmonary disease in three dogs (two with granuloma formation); and foreign body pneumonia, chronic bronchitis, and neoplasia in one dog each.
Bronchoscopy was performed in 10 dogs. In two of these dogs, significant mucus plugging precluded evaluation of some of the affected airways, thus preventing a visual diagnosis of the full extent of bronchiectasis. Airway obstruction with mucus or inspissated material was present in seven dogs (marked in three, mild in two, and of unknown degree in two) (Fig. 1). Changes were multilobar in these 7 dogs (Fig. 2). An intraluminal mass was detected in the right middle lobar bronchus of one dog and this was diagnosed as an eosinophilic granuloma based on histopathology of an endoscopic biopsy. Extraluminal compression of bronchi was noted in two dogs. In one of these dogs, eosinophilic bronchopulmonary disease was diagnosed, and an adjacent pulmonary soft tissue nodule causing extramural compression was identified on CT images. In the other dog, diagnosed with eosinophilic granuloma and chronic foreign body pneumonia, adjacent pulmonary consolidation was present at two sites of extraluminal compression. Bronchial collapse in nonbronchiectatic lung lobes was noted in four dogs (multilobar in three, unilobar in one).
Entire excised lung lobes from four dogs were available for histopathologic review and showed marked bronchial dilation with mild to marked hyperplasia of bronchoepithelial cells, and the presence of subepithelial (peribronchial) inflammation (Figs. 3-5). In all four samples, the lumina of mainstem bronchi or their primary divisions contained mucus in combination with either neutrophils or eosinophils. Peribronchial and interstitial inflammation was present in all cases but varied in intensity. Inflammation was chronic (lymphocytes, plasma cells, and macrophages) and ongoing with 4/4 dogs additionally neutrophilic and 1/4 eosinophilic. There was uniform dilation of the bronchi and the peribronchial stroma was edematous with small vessels within this region prominent in both number and diameter (hypertrophied). In two lungs there was loss or displacement of cartilage, and in one lung each there was hypertrophy of the bronchial wall smooth muscle, and granulation tissue (scarring) that extended into the bronchial lumen.
A total of 71 bronchoarterial ratios were measured. One measurement from the cranial portion of the left cranial lobe could not be acquired due to previous lobectomy. One measurement (BA = 8.0) was discarded because the bronchus was not verified as bronchiectatic either by bronchoscopy or histopathology. The mean bronchoarterial ratio for all remaining 70 measurements was 2.08 ± 0.78 (median = 1.80, range = 1.0–4.33). There were no significant differences in average bronchoarterial ratio estimates among the six anatomic sites (P = 0.36). Averaged bronchoarterial ratios from confirmed bronchiectatic lung lobes were significantly larger (P < 0.01) than averaged ratios not documented as bronchiectatic (Fig. 6). The mean bronchoarterial ratio for the 28 confirmed bronchiectatic lung lobes was 2.71 ± 0.80 and ≥2.0 in 23/28 lobes. The mean bronchoarterial ratio for the 42 lobes not designated as bronchiectatic was 1.66 ± 0.39 and ≥2.0 in 11/42 lobes. In this latter group, 7 of the 11 bronchoarterial ratios measured exactly 2.0.
Qualitative CT features of bronchiectasis were present in all dogs and are summarized in Table 1. Nontapering airways were identified in 12/12 dogs. Eleven dogs had CT evidence of pulmonary consolidation (Fig. 7). Seven dogs were diagnosed with bronchial wall thickening and four with intraluminal bronchial fluid or soft tissue dense debris accumulation (Fig 8). Distribution of disease was multifocal in 11 dogs and focal in one dog. Bronchiectasis was classified as cylindrical in 10 dogs, saccular in one dog, and a combination of the two patterns in the remaining dog. Ancillary thoracic changes identified on CT images included pleural thickening (two dogs), peribronchial infiltrates (two), pneumothorax (one), airway-associated pulmonary nodules (one), pulmonary mass (one), and bullae (one).
|(n = 12)||(n = 12)|
|Nontapering airways||12 (100%)||7 (58%)|
|Pulmonary consolidation||11 (92%)||9 (75%)|
|Bronchial wall thickening||7 (58%)||5 (42%)|
|Bronchial lumen occlusion||4 (33%)||0 (0%)|
|Saccular bronchiectasis||2 (17%)||1 (8%)|
Radiographic studies were available for review in 12/12 dogs. Thoracic radiographs revealed nontapering airways in 7/12 dogs (Table 1). Bronchiectasis was classified as cylindrical in six dogs, and saccular in one dog. The apparent distribution of bronchiectatic changes was multifocal in five dogs and focal in two dogs. Alveolar infiltrates were identified in nine dogs. A bronchial pattern characterized by increased bronchial wall thickness was identified in five dogs. Bronchial occlusion was not identified in any dogs radiographically. Ancillary radiographic findings were similar to the corresponding CT findings. No radiographic evidence of tracheal or mainstem bronchial collapse was noted although no fluoroscopic studies were performed to evaluate dynamic airway change. Irregular margination of lobar bronchi was noted in one dog, suggestive of bronchomalacia.
The mean bronchoarterial ratio from confirmed bronchiectatic lung lobes (2.71 ± 0.80) was significantly higher in the dogs of this study than previously reported bronchoarterial ratios from dogs without clinical pulmonary disease (1.45 ± 0.21) and from unaffected lung lobes in dogs with bronchiectasis examined in the current study (1.66 ± 0.39). While most bronchoarterial ratios from affected lobes were ≥2.0, a few (5/28) were <2.0. Thus even though a bronchoarterial ratio ≥2.0 implies CT evidence of bronchiectasis, a ratio of less than 2.0 does not necessarily exclude the diagnosis, and the bronchoarterial ratio serves as one of several criteria for an imaging diagnosis. Some (11/42) bronchoarterial ratios from lungs not verified as being bronchiectatic had a bronchoarterial ratio ≥2.0. It is possible that most or all of these were bronchiectatic but could not be confirmed here due to lack of histopathology or inability to visualize these airways on bronchoscopy due to broncho-occlusion or dilatation beyond the limit of the endoscope. Thus, this study likely underestimated the detection of bronchiectasis using CT bronchoarterial ratios.
Qualitative CT findings of bronchiectasis in this study were similar to those seen in people and included lack of airway tapering, lobar consolidation, bronchial wall thickening, and bronchial lumen occlusion.[24, 25] In people, certain patterns and distributions of CT lesions have been associated with specific underlying causes of bronchiectasis. This study was not large enough to draw any conclusions about the character of bronchiectasis associated with specific diseases, although this may warrant investigation in the future. Two CT findings of bronchiectasis in people, the presence of visible airways within 1 cm of the pleura and peripheral air trapping, were not evaluated in this study for several reasons. These included the presence of severe underlying lung disease preventing accurate measurement in the periphery, inability to confirm small airway bronchiectasis with bronchoscopy or histopathology, and the presence of relatively thick (5–7 mm) CT collimation in some patients. For these reasons, our investigation focused primarily on dilatation of lobar bronchi and larger bronchioles.
As expected, bronchiectatic airway characteristics were detected more frequently using CT than with radiography (12/12 dogs with CT versus 7/12 dogs with radiography). Additionally, CT was more useful for detecting bronchial lumen occlusion and subtle bronchial wall thickening. Interestingly, bronchial occlusion with debris was found most commonly during bronchoscopy (7/12) followed by CT (4/12) and was radiographically silent in all affected dogs. This is likely a reflection of improved direct visualization and documentation with bronchoscopy. The character and distribution of CT findings were similar to a previous study describing radiographic features of the disease. For example, bronchiectasis in most dogs in the present study was classified as cylindrical, and the distribution was more likely to be multilobar than unilobar, similar to a previous description of radiographic features of the disease. Additionally, the causes of bronchiectasis or associated disease processes reported in this study are similar to those reported previously, with chronic inflammatory conditions of the airways being the most commonly identified cause.[14, 17]
Most dogs in this study were diagnosed with underlying chronic bronchopneumonia or airway inflammation. However, one dog was diagnosed with bronchoalveolar carcinoma with adjacent lobar bronchiectasis. Lobar histopathology and thoracic CT in this dog revealed a large solitary mass of the right cranial lung lobe with adjacent bronchiectasis and bulla formation. Multiple pulmonary bullae were identified throughout multiple lung lobes in this dog. In people, mechanical obstruction from a pulmonary mass is a reported cause of bronchiectasis, but is apparently uncommon in dogs. It is not clear if this patient is an example of mechanical obstruction or if an underlying congenital airway abnormality may have been present given the presence of multiple bullae in this dog. Regardless, airway inflammation does not appear to have been a prominent component of disease in this dog.
One limitation encountered in the current study was the presence of underlying pulmonary disease obscuring visualization of the bronchus and pulmonary artery on CT. In all patients, adequate measurement locations could be found, but sometimes at a level slightly cranial or caudal to the previously reported standardized measurement sites. Additionally, measurement of bronchoarterial ratios assumed a normal associated pulmonary artery. It is possible that pulmonary arterial blood flow may have been decreased in diseased lung lobes (and subsequently increased in unaffected lobes) due to redirected flow from altered regional ventilation. This change could have resulted in higher bronchoarterial ratios in diseased lobes and lower bronchoarterial ratios in unaffected lobes. Alternately, chronic lung disease could have caused pulmonary hypertension and an associated increase in pulmonary artery size that would alter the bronchoarterial ratio. Although no pulmonary artery abnormalities were identified on imaging and no clinical evidence of pulmonary hypertension was reported in this population of dogs, occult pulmonary hypertension cannot be entirely excluded as a factor in artificially lowering bronchoarterial ratios. Out of necessity, bronchoarterial ratio measurements in this study were performed by a nonblinded reviewer in order to ensure measurements of confirmed bronchiectatic airways. However, particular care was taken to avoid altering measurement protocol defined previously. In this retrospective study, CT image collimation was variable and in most instances was thicker than is recommended for thin-section, high-resolution pulmonary imaging in people. This may have had a minor effect on subjective assessment of bronchial wall thickening. All measurements were done using transverse CT images and no reformatted images were made. It is therefore possible that some measurements could have been affected by oblique orientation of bronchi or vessels in transverse images. Lobar histopathology can contribute to the diagnosis and underlying cause of bronchiectasis, but some histopathology samples did not include bronchi and not all dogs were evaluated using histopathology. Bronchoscopy was used in many cases to confirm diagnosis. Bronchoscopy can be limited in its ability to evaluate smaller airways and airways occluded by mucus, foreign material, or a mass.
In conclusion, the most common CT characteristics of bronchiectasis in dogs of this study were quantitative airway dilation and qualitative lack of distal airway tapering. Lack of airway tapering was not detected using thoracic radiography for some dogs. The mean bronchoarterial ratio from 28 bronchiectatic lobes was 2.71 ± 0.80, with a ratio ≥2.0 in 23/28 lobes. Since some affected dogs of our study had a bronchoarterial ratio of less than 2.0, this finding may not necessarily rule out a diagnosis of bronchiectasis. Common secondary CT findings included alveolar consolidation, bronchial wall thickening, and exudative airway occlusion.
- 5Chronic bronchitis, bronchiectasis, bronchiolitis, bronchiolitis obliterans, and bronchopneumonia in a rottweiler with primary ciliary dyskinesia. J Am Anim Hosp Assoc 1989;25:297–304., .
- 18Bronchiectasis. In: Textbook of veterinary internal medicine. SJ Ettinger, EC Feldman, (eds): St. Louis: Elsevier Saunders, 2005..
- 19Lower airway and pulmonary parenchymal diseases. In: PF S, (ed): Thoracic diseases of the dog and cat. Wettswil, Switzerland: Peter F. Suter, 1984:533–537..