Aspiration-related respiratory disorders in dogs

Laura A. Nafe Department of Veterinary Clinical Sciences, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

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Megan E. Grobman Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Isabelle Masseau Département de Sciences Cliniques, Faculté de Médecine Vétérinaire, Université de Montréal, St Hyacinthe, QC J2S 7C6, Canada.

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Carol R. Reinero Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211.

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Aspiration is defined as the intake of solid or liquid materials into the airways and pulmonary parenchyma.1 The content of the aspirated material may be food particles, blood, secretions, liquids, or other accidentally inhaled foreign material.2 In veterinary medicine, the term aspiration is often used interchangeably with aspiration pneumonia, which is a common condition in canine patients.3 Although aspiration pneumonia is well documented in the small animal medical literature,3–5 other aspiration-related respiratory disorders exist that are less common, poorly described, or to date unrecognized in dogs but have been characterized in humans. Ultimately, the consequence of aspiration is dependent on both the underlying health of the individual and the content and volume of the aspirated substance. The distribution of lesions within the lungs reflects the sites with which the aspirated material has had contact and is therefore generally, but not always, gravity dependent.

Aspiration-related respiratory disorders should be expected in dogs as they are in humans, given that dogs are susceptible to many of the health conditions that put humans at risk for aspiration-related disease. Such conditions in humans include dysphagia, regurgitation, vomiting, impaired gag reflex (secondary to medication or underlying neurologic disease), GER, compromised airway defenses (eg, laryngeal dysfunction), and obesity.1,2 In veterinary medicine, aspiration is perceived as a pathological event, with the potential to result in considerable adverse effects, including death.4 Interestingly, studies6,7 have shown that over half of healthy humans aspirate during sleep without clinical consequence (ie, silent aspiration). In situations of silent aspiration, pneumonia is prevented by host defense mechanisms (mechanical and immunologic), such as cough, mucociliary clearance, immunoglobulins, and respiratory phagocytic cells,7 thereby demonstrating the importance of these defense mechanisms and the amount and type of substance aspirated when considering the risk of clinical consequences from aspiration. Although this has not been fully investigated in veterinary medicine, it is reasonable to suspect that healthy dogs could have silent aspiration without clinical respiratory disease.

In dogs with aspiration-related respiratory disease, the location and severity of lesions are presumed to be dependent on the substance aspirated, volume and pH of aspirate, host defense mechanisms, and whether concurrent respiratory disorders exist. Research into risk factors associated with aspiration in dogs and cats has primarily focused on aspiration pneumonia or pneumonitis specifically.3,8,9 A retrospective study4 revealed that 16% of dogs with aspiration pneumonia had undergone general anesthesia within 24 hours prior to diagnosis and that 64% had a history of vomiting. Because aspiration has consequences other than pneumonia, clinicians should recognize that these risk factors may apply to all aspiration-related respiratory conditions.

The purpose of the present report is to provide a general overview of aspiration-related respiratory disorders recognized in human medicine, followed by a literature review and parallel examples (when applicable) involving canine patients specifically. In human medicine, recognized aspiration-related respiratory disorders are subdivided into airway and parenchymal disorders. The airway diseases include upper airway disorders (ie, involving the pharynx, larynx, and extra-thoracic portion of the trachea), lower airway disorders (ie, involving the intrathoracic portion of the trachea and mainstem bronchi and midsize bronchi), bronchiectasis, and DAB; the parenchymal subdivision includes aspiration pneumonitis and ARDS, aspiration pneumonia, exogenous lipid pneumonia, and interstitial lung diseases such as pulmonary fibrosis. Importantly, even in humans (for which these disorders have been well described), aspiration is often not initially suspected for patients with clinical signs caused by aspiration-related respiratory disease. Recognition of parallel disorders in dogs may ultimately lead to novel therapeutic approaches focused on reducing aspiration events or minimizing their detrimental effects on the respiratory tract.

Description and Proposed Classification of Aspiration-Related Respiratory Disorders in Dogs

Aspiration-related upper airway disorders (GER)

Upper airway inflammation secondary to GER is well recognized in human medicine.10–12 Repeated microaspiration of gastric contents (both acidic and nonacidic) in the upper airways can result in oropharyngeal, nasopharyngeal, laryngeal, and proximal tracheal inflammation.1,13 Clinical signs vary and include but are not limited to voice change, stertor, cough, and, in severe cases, respiratory distress secondary to upper airway obstruction.14–16

In humans, GER is diagnosed on the basis of a combination of clinical signs and diagnostic test results.17 Some patients have a clinical history and symptoms consistent with GER disease that may include heartburn, belching, nausea, nocturnal cough, or dysphagia; others will have no gastroesophageal manifestations of reflux.12 Clinical signs of reflux in combination with visible evidence of laryngeal or oropharyngeal inflammation are often enough to make a diagnosis and institute treatment. Occasionally, esophageal pH monitoring is performed to further assess a patient for GER, with decreases in esophageal pH interpreted as corresponding to GER.18 However, nonacidic reflux, which is not captured by esophageal pH monitoring, can also result in tissue irritation, thereby complicating the interpretation of this test.

In a case report,16 laryngeal dysfunction in a dog was attributed to GER on the basis of abnormalities detected on laryngeal examination and resolution of clinical signs with treatment for GER disease. This would be considered an extraesophageal manifestation of GER and may occur in the absence of concurrent gastrointestinal signs.19 In a prospective study20 of dogs with subacute or chronic cough without clinical signs of upper airway disease, 73 of 134 (54%) dogs had hyperemia of the larynx. The prevalence of laryngeal hyperemia did not change across disease states, suggesting that this was a nonspecific product of cough.

Gastric esophageal reflux is a known contributor to perpetuation of airway disease in humans, with cough acting as a trigger for reflux and vice versa. In experimental studies21,22 involving dogs, low pH and pepsin application to the larynx resulted in reflex laryngospasm as well as induction and perpetuation of laryngeal inflammation. Proper identification of patients with aspiration-related upper airway disorders may provide new avenues for therapeutic intervention. That is, for dogs with primarily upper respiratory clinical signs, identification and direct management of the disorders underlying the GER as well as signs-based treatment with proton pump inhibitors may represent a novel treatment approach.

In dogs, tonsillitis, pharyngitis, laryngitis, and proximal tracheitis secondary to GER can result in signs of stertor, stridor, cough, and exercise tolerance.15,16,23 Obesity can predispose dogs to more severe clinical signs,24 with thoracic radiography classically revealing marked hypoinflation secondary to so-called Pickwickian syndrome (Figure 1).

Figure 1—
Figure 1—

Right lateral (A) and dorsoventral (B) thoracic radiographic images of a 9-year-old Dachshund with a diagnosis of stertor and intermittent stridor secondary to upper airway inflammation induced by GER. Interpretation is complicated by severe obesity, causing hypoinflation and a mild diffuse unstructured interstitial pattern, but no tracheal airway obstruction or primary lung lesions are visible. The trachea (arrows) and tracheal bifurcation (asterisks) are indicated.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Videofluoroscopy of the airways can be useful to highlight static or dynamic changes in airway caliber from the oropharynx to the principal bronchi. Oral and functional laryngeal examination of anesthetized dogs given doxapram to stimulate respiration may reveal decreases in laryngeal abduction during inspiration, severe oropharyngeal and laryngeal hyperemia, enlarged tonsils bilaterally, or a thickened or elongated soft palate (Figure 2). Laryngeal dysfunction or paresis may be related to laryngitis rather than a primary neurologic abnormality. In humans, vocal cord dysfunction is a common manifestation of GER.1

Figure 2—
Figure 2—

Oral photograph (A) and side-by-side tracheoscopic images (B) of a 10-year-old spayed female Dachshund with aspiration-related upper airway inflammation attributable to GER. A—Oropharyngeal examination reveals severe hyperemia of the tonsils and tonsillar crypts, soft palate, and larynx. The tonsils are enlarged, and the soft palate appears thickened. B—A striking difference in mucosal hyperemia is visible between the proximal (left image; hyperemic) and distal (right image; less hyperemic) regions of the trachea, reflective of how deeply the reflux penetrated the trachea.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

To further elucidate anatomic abnormalities in dogs with upper airway inflammation secondary to GER, CT examination of the head and thoracic cavity can be performed. Nonspecific findings such as a thickened soft palate with no evidence of a nasal or nasopharyngeal mass may be apparent (Figure 3). Thoracic CT can facilitate detection of a wide variety of lesions from the trachea to the bronchioles (airways) and the pulmonary parenchyma secondary to micro-or macroaspiration. In dogs with repetitive microaspiration from GER, tracheoscopy may reveal mucosal hyperemia of the proximal tracheal region, with a clear demarcation in the mid region and normally appearing mucosa in the distal region (Figure 2). These regional changes reflect what can be seen in humans with GER25 and, in the authors' experience, are classic findings in dogs with GER-associated upper airway disease.

Figure 3—
Figure 3—

Transverse (A) and sagittal (B) CT head images of the dog in Figure 1. The soft palate (double-headed arrow) appears thickened. The nasal cavities and nasopharynx (NP) appear well aerated, with no visible masses.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

After a thorough oropharyngeal and laryngeal examination has been performed and GER has been confirmed, a treatment trial of a proton-pump inhibitor26 such as omeprazole (1 mg/kg [0.45 mg/lb], PO, q 12 h) may help increase gastric pH and reduce signs related to acid reflux, although additional research would be needed to assess risks and benefits of indefinite use. In obese dogs, nutritional management to induce weight loss would be important given that obesity leading to high intragastric pressure can exacerbate GER disease in humans.27

Aspiration-related large airway obstruction

Large airway obstruction due to foreign body inhalation is uncommon, but potentially life-threatening, and needs to be recognized and addressed immediately. In a study28 of tracheobronchial foreign bodies in adult humans, 43% of patients had documented risk factors for aspiration. Foreign bodies in dogs may include food, plant material (eg, acorns), or other foreign objects (eg, plastic materials) that some dogs may chew and accidentally inhale. Patients with (vs without) dysphagia or laryngeal dysfunction are presumed at increased risk for all aspiration disorders, including foreign body inhalation.

Diagnosis of foreign body aspiration can be challenging in some patients, particularly when the aspirated object is not visible radiographically. Diagnosis of large airway obstruction by a foreign object may be made via thoracic radiography in some dogs, depending on the components of the foreign object and its location within the airway (Figure 4).29 However, in humans, most (90%) foreign bodies are radiolucent, and diagnosis of a foreign body by conventional radiography is further complicated by summation artifact.a Despite these limitations, use of radiography for humans with respiratory foreign bodies is reportedly diagnostically helpful in 72% of cases.30 Described radiographic abnormalities in these instances include metallic or mineral foreign bodies, atelectasis, and air trapping. Air trapping is observed when the foreign object acts as a so-called ball valve, leading to regional hyperinflation.30

Figure 4—
Figure 4—

Right lateral (A) and ventrodorsal (B) thoracic radiographic views of an 8-week old male Dachshund that inhaled a metallic pellet (arrows). The pellet is lodged in the right principal bronchus. The tracheal bifurcation (asterisks) is indicated.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

When results of thoracic radiography are equivocal for humans with a history and clinical findings supportive of foreign body aspiration, CT provides an alternative diagnostic approach. Spiral CT has a sensitivity of 100% and specificity of 66.7% for detecting aspirated foreign bodies.31 Thoracic CT allows for quantitative identification of air trapping and atelectasis through evaluation of Hounsfield units and luminal airway diameter.31,a The more readily the obstruction site can be identified, the more likely the appropriate treatment approach, such as endoscopic removal, can be determined.

In addition to fixed airway obstruction from foreign objects, dynamic tracheal obstruction can occur from inhalation of a plastic or flexible foreign body and mimic other dynamic airway disorders, such as tracheal collapse. Cervical and thoracic radiography may reveal an area of increased opacity in the cervical (Figure 5) or intrathoracic portion of the trachea. A high index of suspicion for a foreign object rather than a soft tissue mass should be based on the sharp edges and clear demarcation in the trachea. Tracheoscopy, involving a flexible endoscope when manipulation or investigation of lower airways is required, is the definitive diagnostic test and may reveal marked tissue hyperemia and evidence of irritation (eg, hemorrhage, erosions or ulceration, or thickened or cobblestoned mucosa) along with the presence of a foreign object.32 The foreign object may be removed by use of alligator forceps alongside the endoscope. Episodic airway obstruction can be due to dynamic repositioning of the foreign body, causing partial occlusion of the airway.

Figure 5—
Figure 5—

Right lateral cervical radiograph (A) and tracheoscopic image (B) of a 2-year-old castrated male Cavalier King Charles Spaniel with intermittent dynamic large airway obstruction following aspiration of a 20 × 4-mm plastic foreign body. A—The foreign body (arrows) can be seen in the lumen of the cervical portion of the trachea. B—Partial large airway obstruction with a plastic foreign body (arrows) and mucoid secretions are visible.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Aspiration-related bronchiectasis

Bronchiectasis is defined as irreversible widening of the bronchi due to destruction of the elastic and muscular components of the airway walls. This structural change often results from congenital or acquired defects, leading to chronic cycles of inflammation, infection, and damage to the airways.33 Epithelial injury and altered mucociliary clearance predispose patients to infection and further airway injury and inflammation.

Thoracic radiography, high-resolution CT, and bronchoscopy aid in the diagnosis of bronchiectasis in dogs, with high-resolution CT being superior in most instances.34–36 Thoracic radiography can reveal a multifocal unstructured interstitial pattern (Figure 6) or the more typical alveolar pattern of the dependent lung lobes associated with aspiration. Features of bronchiectasis include thickened bronchial walls, and bronchi that have a wide diameter and do not taper as they track to the periphery or have saccular or cystic dilations.33 Computed tomography is sensitive for the diagnosis of bronchiectasis and can help clinicians determine whether the bronchiectasis is focal, multifocal, or diffuse (Figure 7). In rare instances, CT findings may suggest the presence of well-circumscribed foreign material within a bronchus.

Figure 6—
Figure 6—

Right lateral (A) and ventrodorsal (B) thoracic radiographic images of a 4-year-old spayed female Australian Shepherd with a chronic cough. A—The bronchial walls in the caudoventral lung field appear thickened, and their lumen appears dilated (double-headed arrows). The bronchi do not taper as they extend toward the periphery of the lungs, indicating bronchiectasis. Multifocal ill-defined soft tissue opacities (asterisks) are visible in the caudoventral lung field in the region of the dilated bronchi, obscuring delineation of the caudal vena cava (CVC) and diaphragm. Tu = Endotracheal tube. B—Opacity of the accessory lung lobe region is increased (arrows). The thickened and dilated bronchial walls are not clearly demarcated. Multifocal ill-defined areas of increased soft tissue opacity (asterisks) are visible in the peripheral lateral aspect of the left caudal lung lobe. A small mediastinal shift to the left is seen.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Figure 7—
Figure 7—

Thoracic CT images of 4-year-old spayed female Australian Shepherd that had silent aspiration of kibble several months previously, leading to bronchiectasis. Transverse images at the level of the heart (A) and caudal mediastinal regions (B and C) reveal soft tissue-attenuating foreign material (black arrows) in the bronchial lumen of the accessory lung lobe, the borders of which are outlined by white arrowheads. The lumens of several segmental bronchi (double-headed arrows) in the accessory lung lobe are dilated throughout their length. A large amount of fluid attenuation (asterisks) occupies the dilated and saccular ventral terminal portion of the segmental accessory bronchi. Images in the dorsal (D) and sagittal (E) planes reveal the topographical location of the soft tissue-attenuating material (arrow on sagittal image) in the lumen of the right accessory lobar bronchus (RB3) in relation to the end of the trachea (Tr) and right principal bronchus (RPB). The accessory lobar and segmental bronchi are severely dilated (double-headed arrows), compared with the right principal bronchus, and the bronchial walls are irregular. A 3-D multiplanar reconstruction image (F) shows the left caudal lung lobe supplied by lobar (LB2) and segmental bronchi of apparently normal diameter. The bronchial walls are thin and regular, and their diameter tapers toward the periphery. A second 3-D multiplanar reconstruction image (G) shows an elongation of the first ventral branch of the accessory lobar bronchus with soft tissue-attenuating material at its proximal aspect (arrows). In contrast to the left caudal bronchial tree, the accessory bronchus is severely dilated throughout its length, has a saccular appearance, and is fluid filled at its ventral terminal portion (asterisk). Images were acquired after administration of a standard dose of iodinated contrast medium (iohexol). Ao = Aorta. CVC = Caudal vena cava. LA = Left atrium. PV = Pulmonary veins draining portions of the caudal and accessory lung lobes. RB4 = Right caudal lobar bronchus. RPV = Right pulmonary vein.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Bronchoscopic results depend on the experience of the user and may provide an adequate alternative to CT for dogs with bronchiectasis. In 1 study,35 bronchoscopy allowed accurate identification of bronchiectasis in 92% of examined dogs. Bronchoscopic examination can also allow identification of any associated mucus and foreign material (eg, aspirated kibble) within the lobar bronchi and downstream branches (Figure 8). Friable material is not amenable to endoscopic removal; such a procedure would run the risk of the material entering other lung lobes.

Figure 8—
Figure 8—

Bronchoscopic images of a 4-year-old Australian Shepherd with prior aspiration of kibble. A—Complete occlusion of the accessory lobar bronchus by mucoid secretions is visible (arrows). B—After gentle suction was applied, foreign material was noted to occlude the proximal lobar bronchus. C—With additional attempts to dislodge the foreign material, a severely bronchiectatic airway was noted distal to the obstruction.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Bronchoalveolar lavage and subsequent cytologic evaluation typically allow detection of suppurative inflammation with or without bacterial growth on culture.35 Bacterial organisms isolated from the airway of a dog with bronchiectasis may be secondary to the bronchiectasis and do not necessarily suggest bacterial infection as the primary disease process. Rather, the presence of bacterial organisms must be evaluated in conjunction with the presence or absence of septic suppurative inflammation, given that bronchiectasis is a known risk factor for secondary bacterial dysbiosis due to reduced mucociliary clearance. In the previously mentioned study35 of dogs with bronchiectasis, the most common underlying disease was pneumonia, which was likely aspiration pneumonia in most cases. This finding supports the correlation between airway injury and aspiration.

In dogs, other identifiable causes of bronchiectasis include bacterial infections, eosinophilic bronchopneumopathy, and ciliary dyskinesia.33,35,37,38 Silent aspiration plays a role in humans with bronchiectasis and may be underrecognized in dogs. Dogs with acute-onset vomiting that subsequently develop a persistent cough may have aspirated without the owners' knowledge. Indeed, 66% of pediatric human patients with chronic pulmonary aspiration subsequently developed bronchiectasis in 1 study.36 If bronchiectasis affects a single lung lobe, surgical removal may be curative; diffuse bronchiectasis will require lifelong medical management.

Aspiration-related small airway disease (DAB)

In humans, DAB is a chronic inflammatory disorder of the small airways caused by recurrent aspiration.39 Diagnosis is made by a combination of clinical history and features, documentation of aspiration on videofluoroscopic swallow assessment, CT imaging, and histologic evaluation.40 Classic findings in humans include an identifiable predisposing factor for aspiration and bilateral characteristic CT features, such as centrilobular nodules, so-called tree-in-bud opacities, and sometimes bronchiectasis.40 In a large case series40 of humans with DAB, aspiration went clinically unrecognized as the cause of the lung disease in 75% of patients; GER was ultimately identified as the most common predisposing factor. Because silent aspiration is likely to occur at night, it was speculated that the diffuse nature of the lesions (vs classic gravity-dependent lesions of typical aspiration pneumonia) in that study29 resulted from frequent changes in position during sleep.

Treatment strategies for DAB in dogs in large part involve addressing the underlying cause of aspiration, with no clear guidelines available on the optimal strategy for addressing small airway inflammation. We have identified features compatible with DAB in a dog secondary to recurrent aspiration, including a videofluoroscopic swallow assessment that revealed megaesophagus with retention and retrograde movement of fluid within the esophagus (a known predisposing factor) and CT evidence of bilateral diffuse bronchiolocentric lesions (Figure 9).

Figure 9—
Figure 9—

Transverse thoracic CT images of a 12-year-old Chihuahua with chronic regurgitation and cough suggestive of DAB. A—Immediately caudal to the first branch of the principal bronchus, the lumen of the principal bronchus (double-headed arrow) appears severely dilated, with a bronchial lumen-to-pulmonary artery diameter ratio > 2, indicating bronchiectasis. B—Ill-defined areas of ground glass opacification are seen surrounding small bronchi (arrows). The esophagus (e) is mildly distended with air and gravity-dependent fluid. C—Nodular opacities, small branching lines, and tree-in-bud lesions (arrowheads) are seen diffusely involving the right and left lungs. Images were acquired after administration of a standard dose of iodinated contrast medium (iohexol). LCPa = Left caudal pulmonary artery.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Aspiration pneumonitis and pneumonia

Aspiration pneumonia is the most commonly recognized pathological connection between the respiratory and digestive tracts in veterinary medicine.3 Esophageal dysfunction in elderly dogs with laryngeal paralysis (ie, geriatric-onset laryngeal paralysis polyneuropathy) is just 1 example.41 As previously mentioned, in human medicine, microaspiration (ie, small-volume aspiration) occurs in healthy individuals without clinical consequence, which is also likely, yet unproven, in dogs. Bacterial infection is typically associated with aspiration of a large volume of higher pH (> 2.5) contents containing bacteria from the oropharyngeal or upper gastrointestinal tracts into the lungs.6 In human medicine, a distinction exists between the initial inflammatory reaction associated with aspiration and subsequent chemical pneumonitis (aspiration pneumonitis) and those events associated with bacterial infection (aspiration pneumonia).6

Aspiration pneumonitis is caused by macroaspiration (ie, large-volume aspiration), resulting in acute onset of hypoxemia, pyrexia, and radiographic changes independent of bacterial infection. Although the pathological effects of aspiration may not initially be infectious in nature, the aspirated material may promote bacterial growth. Additionally, damage of clearance mechanisms allows for the generation of permissive niches for bacterial growth and secondary infection.6

In veterinary medicine, there is no clear, well-accepted distinction between aspiration pneumonitis and pneumonia, which is likely attributable to challenges distinguishing between the 2 etiologies. Both conditions can result in pyrexia and evidence of respiratory dysfunction. With aspiration pneumonitis in humans, characteristic radiographic changes include bilateral infiltrates involving nondependent pulmonary regions. However, these changes are not consistent, and coughing can result in dispersion of the aspirate.1,11 Computed tomography may provide further distinguishing features but is not routinely used in veterinary medicine.

The clinical course of aspiration pneumonitis is more rapid, with damage occurring within hours after the aspiration event, leading to clinical signs and associated radiographic changes within 48 hours after aspiration. In humans with aspiration pneumonitis, a large volume of material is typically required to cause clinically important damage; this is in contrast to aspiration pneumonia, for which the aspiration event is rarely identified.6 Given differences between humans and dogs in client vigilance and patient observation at home, witnessing an aspiration event is not a reliable discriminating feature for dogs.

Treatment of the 2 conditions varies, with aspiration pneumonitis treated largely on a supportive basis and aspiration pneumonia requiring antimicrobials. The use of antimicrobials for humans with aspiration pneumonitis is believed to likely result in bacterial antimicrobial resistance without sufficient clinical benefit to the patient.11 If the conditions are similar for dogs, then value would exist in research to help discriminate between aspiration pneumonitis and aspiration pneumonia in dogs and determine optimal therapeutic interventions.

Prospective research in human medicine has shown that 16.5% of patients with aspiration pneumonia develop a severe subtype of ARDS.6 Rapid clinical recognition of this condition is important, given the high mortality rate in humans (30% to 60%), with pulmonary protective ventilation identified as the only intervention to improve mortality rates.6,42 It remains unknown whether identification and appropriate treatment of at-risk dogs early after aspiration would improve outcomes.

A diagnosis of ARDs requires that several clinical and diagnostic criteria be met, including an acute onset (< 72 hours after an inciting event), evidence of impaired gas exchange, presence of known risk factors, and evidence of an increase in capillary leakage in the absence of high pulmonary capillary pressures. Although the final listed criterion may be demonstrated by documentation of protein-rich fluid within the airways or an increase in the amount of extravascular water in the lungs, thoracic imaging is used most commonly in clinical veterinary practice.43 The presence of bilateral infiltrates on radiographs (ie, infiltrates that involve > 1 lobe/quadrant) likely represents the most widely accessible means of supporting a diagnosis of ARDs through thoracic imaging (Figure 10). However, the use of thoracic CT, which is considered the reference standard in human medicine, may improve the characterization of pulmonary lesions and improve accuracy for detecting affected patients.44

Figure 10—
Figure 10—

Right lateral (A) and ventrodorsal (B) thoracic radiographic images of a 4-year-old sexually intact male Mastiff obtained 24 hours after surgical treatment for cervical spondylomyelopathy; the Mastiff subsequently developed aspiration pneumonitis and ARDS. A—Multiple patchy and coalescing areas of soft tissue opacity with several air bronchograms (arrows) are seen creating border effacement with the cardiac silhouette. The ventral lung field is more severely affected, although a severe unstructured interstitial pattern can be seen in the perihilar region, obscuring part of the caudal vena cava (CVC). B—Both lungs have signs of an alveolar pattern (asterisks) and air bronchogram (arrow), although the left lung is more severely affected than the right.

Citation: Journal of the American Veterinary Medical Association 253, 3; 10.2460/javma.253.3.292

Aspiration-related lipid pneumonia (exogenous lipid pneumonia)

Lipid (or lipoid) pneumonia is an example of an inflammatory and fibrotic parenchymal disorder secondary to an immune response to endogenous or exogenous lipids. Endogenous lipid pneumonia is not linked to aspiration and will not be discussed further; exogenous lipid pneumonia results from aspiration or inhalation of animal, vegetable, or mineral oils. Most cases of exogenous lipid pneumonia occur from accidental aspiration of lipids.1 This disorder has been identified in dogs, albeit rarely.45,46 Diagnosis is generally made through a combination of relevant historical factors (inadvertent inhalation of a lipid-containing compound), patchy pneumonic consolidation, and cytologic or histologic evidence of extracellular fat globules and lipid-laden macrophages.

Aspiration-related interstitial lung diseases (eg, pulmonary fibrosis)

In dogs, interstitial lung diseases are defined as a heterogenous group of inflammatory or fibrotic disorders affecting the space between the pulmonary epithelium and vascular endothelium, with overlapping clinicopathologic features.47 Repetitive microaspiration may contribute to the development of interstitial lung diseases; this role is particularly well established in exacerbations of idiopathic pulmonary fibrosis in humans.48 Although the veterinary medical understanding of interstitial lung diseases and fibrotic lung disease remains in its infancy, the possible contribution of microaspiration deserves further investigation to clarify its role in disease development and progression and whether treatment ultimately slows declines in lung function.

Conclusion

Aspiration can result in a broad range of clinical disorders, with pathological effects extending to the upper airways, lower airways, and pulmonary parenchyma. Many aspiration events are likely occult; therefore, identification of dogs at risk for aspiration is important, with respect to appropriate diagnosis and management. A better understanding of the types of aspiration-associated respiratory disorders in dogs will be important going forward to improve early recognition, investigate optimum therapeutic protocols, and provide better prognostic information.

Acknowledgments

The authors report that there were no conflicts of interest. No financial support was received for this report.

ABBREVIATIONS

ARDS

Acute respiratory distress syndrome

DAB

Diffuse aspiration bronchiolitis

GER

Gastroesophageal reflux

Footnotes

a.

Hsu A. Tracheobronchial foreign bodies in adults (abstr). Am J Respir Crit Care Med 2014;189:A4387.

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    • Export Citation
  • 20. Johnson LR. Laryngeal structure and function in dogs with cough. J Am Vet Med Assoc 2016;249:195201.

  • 21. Little FB, Koufman JA, Kohut RI, et al. Effect of gastric acid on the pathogenesis of subglottic stenosis. Ann Otol Rhinol Laryngol 1985;94:516519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Loughlin CJ, Koufman JA, Averill DB, et al. Acid-induced laryngospasm in a canine model. Laryngoscope 1996;106:15061509.

  • 23. Adhami T, Goldblum JR, Richter JE, et al. The role of gastric and duodenal agents in laryngeal injury: an experimental canine model. Am J Gastroenterol 2004;99:20982106.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Xing JH, Lei Y & Chen JDZ. Gastric electrical stimulation (GES) with parameters for morbid obesity elevates lower esophageal sphincter (LES) pressure in conscious dogs. Obes Surg 2005;15:13211327.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Gaynor EB. Otolaryngologic manifestations of gastroesophageal reflux. Am J Gastroenterol 1991;86:801808.

  • 26. Portnoy JE, Gregory ND, Cerulli CE, et al. Efficacy of super high dose proton pump inhibitor administration in refractory laryngopharyngeal reflux: a pilot study. J Voice 2014;28:369377.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Bredenoord AJ, Pandolfino JE, Smout AJ. Gastro-oesophageal reflux disease. Lancet 2013;381:19331942.

  • 28. Limper AH, Prakash UB. Tracheobronchial foreign bodies in adults. Ann Intern Med 1990;112:604609.

  • 29. Schultz RM & Zwingenberger A. Radiographic, computed tomographic, and ultrasonographic findings with migrating intrathoracic grass awns in dogs and cats. Vet Radiol Ultrasound 2008;49:249255.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Swanson KL. Endoscopic foreign body removal. In: Interventions in pulmonary medicine. New York: Springer, 2013;441450.

  • 31. Hong S-J, Goo HW & Roh J-L. Utility of spiral and cine CT scans in pediatric patients suspected of aspirating radiolucent foreign bodies. Otolaryngol Head Neck Surg 2008;138:576580.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Tenwolde AC, Johnson LR, Hunt GB, et al. The role of bronchoscopy in foreign body removal in dogs and cats: 37 cases (2000–2008). J Vet Intern Med 2010;24:10631068.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Hawkins EC, Basseches J, Berry CR, et al. Demographic, clinical, and radiographic features of bronchiectasis in dogs: 316 cases (1988–2000). J Am Vet Med Assoc 2003;223:16281635.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Cannon MS, Johnson LR, Pesavento PA, et al. Quantitative and qualitative computed tomographic characteristics of bronchiectasis in 12 dogs. Vet Radiol Ultrasound 2013;54: 351357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Johnson LR, Johnson EG, Vernau W, et al. Bronchoscopy, imaging, and concurrent diseases in dogs with bronchiectasis: (2003–2014). J Vet Intern Med 2016;30:247254.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Piccione JC, McPhail GL, Fenchel MC, et al. Bronchiectasis in chronic pulmonary aspiration: risk factors and clinical implications. Pediatr Pulmonol 2012;47:447452.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Reichler IM, Hoerauf A, Guscetti F, et al. Primary ciliary dyskinesia with situs inversus totalis, hydrocephalus internus and cardiac malformations in a dog. J Small Anim Pract 2001;42:345348.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38. Mesquita L, Lam R, Lamb CR, et al. Computed tomographic findings in 15 dogs with eosinophilic bronchopneumopathy. Vet Radiol Ultrasound 2015;56:3339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39. Matsuse T, Fukuchi Y, Oka T, et al. Importance of diffuse aspiration bronchiolitis caused by chronic occult aspiration in the elderly. Chest 1996;110:12891293.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Hu X, Yi ES, Ryu JH. Diffuse aspiration bronchiolitis: analysis of 20 consecutive patients. J Bras Pneumol 2015;41:161166.

  • 41. Stanley BJ, Hauptman JG, Fritz MC, et al. Esophageal dysfunction in dogs with idiopathic laryngeal paralysis: a controlled cohort study. Vet Surg 2010;39:139149.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42. Seeley E, McAuley DF, Eisner M, et al. Predictors of mortality in acute lung injury during the era of lung protective ventilation. Thorax 2008;63:994998.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43. Wilkins PA, Otto CM, Baumgardner JE, et al. Acute lung injury and acute respiratory distress syndromes in veterinary medicine: consensus definitions: The Dorothy Russell Havemeyer Working Group on ALI and ARDS in Veterinary Medicine. J Vet Emerg Crit Care 2007;17:333339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44. Figueroa-Casas JB, Brunner N, Dwivedi AK, et al. Accuracy of the chest radiograph to identify bilateral pulmonary infiltrates consistent with the diagnosis of acute respiratory distress syndrome using computed tomography as reference standard. J Crit Care 2013;28:352357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45. Corcoran B, Martin M, Darke P, et al. Lipoid pneumonia in a rough Collie dog. J Small Anim Pract 1992;33:544548.

  • 46. Hudson JA, Montgomery RD, Powers RD, et al. Presumed mineral oil aspiration and cavitary lung lesions in a dog. Vet Radiol Ultrasound 1994;35:277281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47. Reinero CR, Cohn LA. Interstitial lung diseases. Vet Clin North Am Small Anim Pract 2007;37:937947.

  • 48. Johannson KA, Collard HR. Acute exacerbation of idiopathic pulmonary fibrosis: a proposal. Curr Respir Care Rep 2013;2:233240.

Contributor Notes

Address correspondence to Dr. Reinero (reineroc@missouri.edu).
  • Figure 1—

    Right lateral (A) and dorsoventral (B) thoracic radiographic images of a 9-year-old Dachshund with a diagnosis of stertor and intermittent stridor secondary to upper airway inflammation induced by GER. Interpretation is complicated by severe obesity, causing hypoinflation and a mild diffuse unstructured interstitial pattern, but no tracheal airway obstruction or primary lung lesions are visible. The trachea (arrows) and tracheal bifurcation (asterisks) are indicated.

  • Figure 2—

    Oral photograph (A) and side-by-side tracheoscopic images (B) of a 10-year-old spayed female Dachshund with aspiration-related upper airway inflammation attributable to GER. A—Oropharyngeal examination reveals severe hyperemia of the tonsils and tonsillar crypts, soft palate, and larynx. The tonsils are enlarged, and the soft palate appears thickened. B—A striking difference in mucosal hyperemia is visible between the proximal (left image; hyperemic) and distal (right image; less hyperemic) regions of the trachea, reflective of how deeply the reflux penetrated the trachea.

  • Figure 3—

    Transverse (A) and sagittal (B) CT head images of the dog in Figure 1. The soft palate (double-headed arrow) appears thickened. The nasal cavities and nasopharynx (NP) appear well aerated, with no visible masses.

  • Figure 4—

    Right lateral (A) and ventrodorsal (B) thoracic radiographic views of an 8-week old male Dachshund that inhaled a metallic pellet (arrows). The pellet is lodged in the right principal bronchus. The tracheal bifurcation (asterisks) is indicated.

  • Figure 5—

    Right lateral cervical radiograph (A) and tracheoscopic image (B) of a 2-year-old castrated male Cavalier King Charles Spaniel with intermittent dynamic large airway obstruction following aspiration of a 20 × 4-mm plastic foreign body. A—The foreign body (arrows) can be seen in the lumen of the cervical portion of the trachea. B—Partial large airway obstruction with a plastic foreign body (arrows) and mucoid secretions are visible.

  • Figure 6—

    Right lateral (A) and ventrodorsal (B) thoracic radiographic images of a 4-year-old spayed female Australian Shepherd with a chronic cough. A—The bronchial walls in the caudoventral lung field appear thickened, and their lumen appears dilated (double-headed arrows). The bronchi do not taper as they extend toward the periphery of the lungs, indicating bronchiectasis. Multifocal ill-defined soft tissue opacities (asterisks) are visible in the caudoventral lung field in the region of the dilated bronchi, obscuring delineation of the caudal vena cava (CVC) and diaphragm. Tu = Endotracheal tube. B—Opacity of the accessory lung lobe region is increased (arrows). The thickened and dilated bronchial walls are not clearly demarcated. Multifocal ill-defined areas of increased soft tissue opacity (asterisks) are visible in the peripheral lateral aspect of the left caudal lung lobe. A small mediastinal shift to the left is seen.

  • Figure 7—

    Thoracic CT images of 4-year-old spayed female Australian Shepherd that had silent aspiration of kibble several months previously, leading to bronchiectasis. Transverse images at the level of the heart (A) and caudal mediastinal regions (B and C) reveal soft tissue-attenuating foreign material (black arrows) in the bronchial lumen of the accessory lung lobe, the borders of which are outlined by white arrowheads. The lumens of several segmental bronchi (double-headed arrows) in the accessory lung lobe are dilated throughout their length. A large amount of fluid attenuation (asterisks) occupies the dilated and saccular ventral terminal portion of the segmental accessory bronchi. Images in the dorsal (D) and sagittal (E) planes reveal the topographical location of the soft tissue-attenuating material (arrow on sagittal image) in the lumen of the right accessory lobar bronchus (RB3) in relation to the end of the trachea (Tr) and right principal bronchus (RPB). The accessory lobar and segmental bronchi are severely dilated (double-headed arrows), compared with the right principal bronchus, and the bronchial walls are irregular. A 3-D multiplanar reconstruction image (F) shows the left caudal lung lobe supplied by lobar (LB2) and segmental bronchi of apparently normal diameter. The bronchial walls are thin and regular, and their diameter tapers toward the periphery. A second 3-D multiplanar reconstruction image (G) shows an elongation of the first ventral branch of the accessory lobar bronchus with soft tissue-attenuating material at its proximal aspect (arrows). In contrast to the left caudal bronchial tree, the accessory bronchus is severely dilated throughout its length, has a saccular appearance, and is fluid filled at its ventral terminal portion (asterisk). Images were acquired after administration of a standard dose of iodinated contrast medium (iohexol). Ao = Aorta. CVC = Caudal vena cava. LA = Left atrium. PV = Pulmonary veins draining portions of the caudal and accessory lung lobes. RB4 = Right caudal lobar bronchus. RPV = Right pulmonary vein.

  • Figure 8—

    Bronchoscopic images of a 4-year-old Australian Shepherd with prior aspiration of kibble. A—Complete occlusion of the accessory lobar bronchus by mucoid secretions is visible (arrows). B—After gentle suction was applied, foreign material was noted to occlude the proximal lobar bronchus. C—With additional attempts to dislodge the foreign material, a severely bronchiectatic airway was noted distal to the obstruction.

  • Figure 9—

    Transverse thoracic CT images of a 12-year-old Chihuahua with chronic regurgitation and cough suggestive of DAB. A—Immediately caudal to the first branch of the principal bronchus, the lumen of the principal bronchus (double-headed arrow) appears severely dilated, with a bronchial lumen-to-pulmonary artery diameter ratio > 2, indicating bronchiectasis. B—Ill-defined areas of ground glass opacification are seen surrounding small bronchi (arrows). The esophagus (e) is mildly distended with air and gravity-dependent fluid. C—Nodular opacities, small branching lines, and tree-in-bud lesions (arrowheads) are seen diffusely involving the right and left lungs. Images were acquired after administration of a standard dose of iodinated contrast medium (iohexol). LCPa = Left caudal pulmonary artery.

  • Figure 10—

    Right lateral (A) and ventrodorsal (B) thoracic radiographic images of a 4-year-old sexually intact male Mastiff obtained 24 hours after surgical treatment for cervical spondylomyelopathy; the Mastiff subsequently developed aspiration pneumonitis and ARDS. A—Multiple patchy and coalescing areas of soft tissue opacity with several air bronchograms (arrows) are seen creating border effacement with the cardiac silhouette. The ventral lung field is more severely affected, although a severe unstructured interstitial pattern can be seen in the perihilar region, obscuring part of the caudal vena cava (CVC). B—Both lungs have signs of an alveolar pattern (asterisks) and air bronchogram (arrow), although the left lung is more severely affected than the right.

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    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Lux CN, Archer TM, Lunsford KV. Gastroesophageal reflux and laryngeal dysfunction in a dog. J Am Vet Med Assoc 2012;240:11001103.

  • 17. Molyneux ID, Morice AH. Airway reflux, cough and respiratory disease. Ther Adv Chronic Dis 2011;2:237248.

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  • 19. de Bortoli N, Nacci A, Savarino E, et al. How many cases of laryngopharyngeal reflux suspected by laryngoscopy are gastroesophageal reflux disease-related? World J Gastroenterol 2012;18:43634370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Johnson LR. Laryngeal structure and function in dogs with cough. J Am Vet Med Assoc 2016;249:195201.

  • 21. Little FB, Koufman JA, Kohut RI, et al. Effect of gastric acid on the pathogenesis of subglottic stenosis. Ann Otol Rhinol Laryngol 1985;94:516519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Loughlin CJ, Koufman JA, Averill DB, et al. Acid-induced laryngospasm in a canine model. Laryngoscope 1996;106:15061509.

  • 23. Adhami T, Goldblum JR, Richter JE, et al. The role of gastric and duodenal agents in laryngeal injury: an experimental canine model. Am J Gastroenterol 2004;99:20982106.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Xing JH, Lei Y & Chen JDZ. Gastric electrical stimulation (GES) with parameters for morbid obesity elevates lower esophageal sphincter (LES) pressure in conscious dogs. Obes Surg 2005;15:13211327.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Gaynor EB. Otolaryngologic manifestations of gastroesophageal reflux. Am J Gastroenterol 1991;86:801808.

  • 26. Portnoy JE, Gregory ND, Cerulli CE, et al. Efficacy of super high dose proton pump inhibitor administration in refractory laryngopharyngeal reflux: a pilot study. J Voice 2014;28:369377.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Bredenoord AJ, Pandolfino JE, Smout AJ. Gastro-oesophageal reflux disease. Lancet 2013;381:19331942.

  • 28. Limper AH, Prakash UB. Tracheobronchial foreign bodies in adults. Ann Intern Med 1990;112:604609.

  • 29. Schultz RM & Zwingenberger A. Radiographic, computed tomographic, and ultrasonographic findings with migrating intrathoracic grass awns in dogs and cats. Vet Radiol Ultrasound 2008;49:249255.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Swanson KL. Endoscopic foreign body removal. In: Interventions in pulmonary medicine. New York: Springer, 2013;441450.

  • 31. Hong S-J, Goo HW & Roh J-L. Utility of spiral and cine CT scans in pediatric patients suspected of aspirating radiolucent foreign bodies. Otolaryngol Head Neck Surg 2008;138:576580.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Tenwolde AC, Johnson LR, Hunt GB, et al. The role of bronchoscopy in foreign body removal in dogs and cats: 37 cases (2000–2008). J Vet Intern Med 2010;24:10631068.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Hawkins EC, Basseches J, Berry CR, et al. Demographic, clinical, and radiographic features of bronchiectasis in dogs: 316 cases (1988–2000). J Am Vet Med Assoc 2003;223:16281635.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Cannon MS, Johnson LR, Pesavento PA, et al. Quantitative and qualitative computed tomographic characteristics of bronchiectasis in 12 dogs. Vet Radiol Ultrasound 2013;54: 351357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Johnson LR, Johnson EG, Vernau W, et al. Bronchoscopy, imaging, and concurrent diseases in dogs with bronchiectasis: (2003–2014). J Vet Intern Med 2016;30:247254.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Piccione JC, McPhail GL, Fenchel MC, et al. Bronchiectasis in chronic pulmonary aspiration: risk factors and clinical implications. Pediatr Pulmonol 2012;47:447452.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Reichler IM, Hoerauf A, Guscetti F, et al. Primary ciliary dyskinesia with situs inversus totalis, hydrocephalus internus and cardiac malformations in a dog. J Small Anim Pract 2001;42:345348.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38. Mesquita L, Lam R, Lamb CR, et al. Computed tomographic findings in 15 dogs with eosinophilic bronchopneumopathy. Vet Radiol Ultrasound 2015;56:3339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39. Matsuse T, Fukuchi Y, Oka T, et al. Importance of diffuse aspiration bronchiolitis caused by chronic occult aspiration in the elderly. Chest 1996;110:12891293.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Hu X, Yi ES, Ryu JH. Diffuse aspiration bronchiolitis: analysis of 20 consecutive patients. J Bras Pneumol 2015;41:161166.

  • 41. Stanley BJ, Hauptman JG, Fritz MC, et al. Esophageal dysfunction in dogs with idiopathic laryngeal paralysis: a controlled cohort study. Vet Surg 2010;39:139149.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42. Seeley E, McAuley DF, Eisner M, et al. Predictors of mortality in acute lung injury during the era of lung protective ventilation. Thorax 2008;63:994998.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43. Wilkins PA, Otto CM, Baumgardner JE, et al. Acute lung injury and acute respiratory distress syndromes in veterinary medicine: consensus definitions: The Dorothy Russell Havemeyer Working Group on ALI and ARDS in Veterinary Medicine. J Vet Emerg Crit Care 2007;17:333339.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44. Figueroa-Casas JB, Brunner N, Dwivedi AK, et al. Accuracy of the chest radiograph to identify bilateral pulmonary infiltrates consistent with the diagnosis of acute respiratory distress syndrome using computed tomography as reference standard. J Crit Care 2013;28:352357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45. Corcoran B, Martin M, Darke P, et al. Lipoid pneumonia in a rough Collie dog. J Small Anim Pract 1992;33:544548.

  • 46. Hudson JA, Montgomery RD, Powers RD, et al. Presumed mineral oil aspiration and cavitary lung lesions in a dog. Vet Radiol Ultrasound 1994;35:277281.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47. Reinero CR, Cohn LA. Interstitial lung diseases. Vet Clin North Am Small Anim Pract 2007;37:937947.

  • 48. Johannson KA, Collard HR. Acute exacerbation of idiopathic pulmonary fibrosis: a proposal. Curr Respir Care Rep 2013;2:233240.

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