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A n U p d a t e o n Tra c h e a l a n d

A i r w a y C o l l a p s e in D o g s
Ann Della Maggiore, DVM

KEYWORDS
 Tracheal collapse  Airway collapse  Bronchomalacia  Chronic cough
 Tracheal stent

KEY POINTS
 Tracheal collapse is characterized by dorsoventral flattening of tracheal rings.
 Tracheal collapse affects the cervical and/or intrathoracic trachea and is seen most
commonly in middle-aged to older toy and miniature-breed dogs.
 Airway collapse or bronchomalacia affects large bronchi that contain cartilage and could
be associated with similar cartilage defects to those seen with tracheal collapse. This con-
dition is seen in any size of breed of dog.
 Medical management can include reduction of stress, weight loss, antitussives, broncho-
dilators, and possibly glucocorticoids (when concurrent bronchitis is present) and antibi-
otics (when infection is discovered).
 Surgical and minimally invasive treatment options are available when medical manage-
ment fails.

INTRODUCTION

Tracheal or airway collapse is a common cause of cough in dogs and can affect the
cervical trachea, intrathoracic trachea, or bronchial walls in isolation, or multiple re-
gions can be affected concurrently. Tracheal collapse most likely results from soft-
ening of the tracheal cartilage that results in dorsoventral flattening of the tracheal
rings and prolapse of the tracheal membrane into the lumen. This process leads to
narrowing of the trachea whenever extraluminal pressure exceeds intraluminal pres-
sure, causing airway collapse and impeding the passage of air. In some dogs with
the most severe form of tracheal collapse (grade 4 out of 4), the cartilage rings are
sometimes rigid but deviate dorsally into the trachea in a W shape. Clinically, tracheal
narrowing results in a persistent dry, paroxysmal goose-honk cough; tracheal sensi-
tivity; and varying degrees of respiratory difficulty. When the principal bronchi are
also involved, the condition is termed tracheobronchomalacia. Bronchomalacia,

MarQueen Pet Emergency and Specialty Group, 9205 Sierra College Boulevard #120, Roseville,
CA 95661, USA
E-mail address: adellamaggiore@yahoo.com

Vet Clin Small Anim - (2019) -–-


https://doi.org/10.1016/j.cvsm.2019.11.003 vetsmall.theclinics.com
0195-5616/19/ª 2019 Elsevier Inc. All rights reserved.
2 Della Maggiore

which is recognized in people and in dogs, is a defect of the principal bronchi and
other smaller airways supported by cartilage that causes narrowing and loss of luminal
dimensions in intrathoracic airways and a reduction in ability to clear secretions. These
changes result in bronchial collapse, causing chronic cough, wheezing, and intermit-
tent or chronic respiratory difficulty.1,2

CAUSE/PATHOPHYSIOLOGY

The cause of malacic airway disease is complex, incompletely understood, and likely
multifactorial. In people, proposed causes include congenital conditions, endotra-
cheal intubation, long-term ventilation, closed-chest trauma, chronic airway irritation
and inflammation, malignancy, asthma, mechanical anatomic factors, and thyroid dis-
ease, but a definitive cause is unknown.3–12 The cause of tracheobronchomalacia in
dogs is also unknown and could be primary (congenital) or secondary to chronic
inflammation (acquired). Given the common occurrence of tracheal collapse in
small-breed dogs, there could be a primary or congenital abnormality of cartilage
with secondary factors playing a role in progression and development of clinical signs.
Tracheal collapse is often associated with softening of cartilage rings caused by a
reduction of glycosaminoglycan and chondroitin sulfate, which leads to a weakness
and flattening of the tracheal rings. Changes to the tracheal matrix and inability to
retain water lead to a decreased ability to maintain functional rigidity.13,14 Extrinsic
compression, chronic inflammation, and alteration in elastic fibers in the dorsal
tracheal membrane and annular ligaments have also been considered as possible
causes or factors that contribute to collapse.15,16 Secondary factors that can initiate
clinical signs include airway irritants, chronic bronchitis, laryngeal paralysis, respira-
tory infection, obesity, and tracheal intubation. It is critical to identify these factors
for appropriate medical management.
Dynamic collapse of the airway perpetuates additional inflammation, tracheal
edema, alterations or failure in the mucociliary apparatus, increased mucus secretion,
and mucus trapping within the airways. The cervical trachea collapses during inspira-
tion and the thoracic trachea collapses during expiration because of the pressures
developed during the respiratory cycle. Tracheal collapse occurs almost exclusively
in small-breed dogs, whereas bronchial collapse occurs in both large-breed and
small-breed dogs and most commonly involves the right middle and the left cranial
bronchi.1 In some dogs only bronchial collapse (bronchomalacia) is noted.

PATIENT HISTORY

Tracheal or airway collapse is commonly seen in middle-aged to older miniature, toy,


and small-breed dogs. Age at presentation typically ranges from 1 to 15 years and
signs have been present for years, although about 25% of affected dogs show clinical
signs by the age of 6 months.17 Breeds over-represented include Yorkshire terriers,
Pomeranian, pugs, miniature poodle, Maltese, and Chihuahuas.18 No sex predilection
has been appreciated. Cats and large-breed dogs are rarely diagnosed with tracheal
collapse.
Bronchomalacia is reported in 45% to 83% of dogs with tracheal collapse1,19 and
has also been reported in dogs with eosinophilic bronchopneumopathy20 or bron-
chitis. Bronchomalacia, unlike tracheal collapse, can affect any canine breed and
can be seen in medium-breed and large-breed dogs,1,2 suggesting that the underlying
cause could be different from that of tracheal collapse, although histologic investiga-
tions are lacking. Within a population of coughing dogs, dogs with airway collapse are
often older, lower in body weight, and have a significantly higher body condition than
An Update on Tracheal and Airway Collapse in Dogs 3

dogs without airway collapse.1 Bronchomalacia, and specifically collapse of the left
cranial lobar bronchus, has been recognized in a large percentage (87%) of dogs
with brachycephalic airway syndrome. In 1 report, pugs were the most common
brachycephalic breed affected with this type of collapse, followed by English bulldogs
and French bulldogs.21
Dogs with tracheal or airway collapse usually present to the veterinarian for evalu-
ation of cough that is initiated by excitement, drinking or eating, or pulling on a leash
with a neck lead. Prolonged clinical history is common and ranges from weeks to
years, although some dogs present at a very young age with respiratory distress
caused by fixed airway narrowing and obstruction. These dogs often have grade 4,
or the W shape, to the trachea. Other dogs have paroxysmal or waxing and waning
respiratory signs, most often described as a dry, harsh, or honking cough. Worsening
tachypnea, exercise intolerance, and respiratory distress tend to occur during phys-
ical exertion, heat stress, or in humid conditions. Respiratory compromise can prog-
ress and become refractory to treatment. Cyanosis and syncope can also occur
because of complete airway obstruction, vagally mediated syncope, or pulmonary hy-
pertension.22 Occasionally animals present with acute respiratory distress from airway
obstruction, often exacerbated by stress, excitement, heat, and/or concurrent respi-
ratory disease.

PHYSICAL EXAMINATION

Dogs presenting for airway collapse are usually systemically healthy and are often
overweight. Respiratory pattern is often normal or the dog can show increased respi-
ratory effort caused by airway collapse. Cervical tracheal collapse typically causes
respiratory difficulty on inspiration, whereas intrathoracic collapse and bronchomala-
cia result in increased expiratory effort. Close observation or palpation at the thoracic
inlet can sometimes reveal cranial lung herniation through the inlet during expiration in
some dogs with intrathoracic airway collapse. Palpation of the trachea frequently ini-
tiates cough in affected dogs, indicating nonspecific tracheal sensitivity. This palpa-
tion should be performed cautiously because some animals become cyanotic,
develop syncope, or go into a life-threatening respiratory crisis because of paroxysmal
cough. Collapse of the cervical tracheal can sometimes be appreciated as a flattening
of the tracheal rings on cervical palpation.
Auscultation over the trachea can reveal stridorous sounds on both inspiration and
expiration caused by the fixed narrowing of the extrathoracic tracheal diameter. This
narrowing must be differentiated from laryngeal paralysis, which has been reported in
up to 60% of dogs with tracheal collapse,22 emphasizing the importance of a thorough
upper airway examination if the animal is anesthetized. Stertor or stridor could also
indicate laryngeal collapse in brachycephalic breeds, with 1 study reporting some de-
gree of laryngeal collapse in almost all brachycephalic dogs as well as an association
between laryngeal collapse and collapse of the left cranial lobar bronchus.21 During
thoracic auscultation, referred upper airway sounds are often noted and can compro-
mise assessment of lung sounds. Crackles on both inspiration and expiration are
sometimes appreciated in dogs with bronchomalacia and small airway collapse, or
this can suggest mucus accumulation in the airways associated with concurrent
bronchitis.
A thorough cardiac auscultation is recommended, and a heart murmur associated
with mitral regurgitation was found significantly more often in dogs with airway
collapse (17%) compared with animals presenting with cough without airway collapse
(2%).1 This finding most likely is related to the commonality of myxomatous mitral
4 Della Maggiore

valve disease and airway disease in small-breed dogs. The role of cardiomegaly and
specifically left atrial enlargement in airway collapse remains unclear. A recent study
showed similar severity and location of airway collapse in dogs with and without left
atrial enlargement and reported airway inflammation as the likely cause of cough in
dogs that had both left atrial enlargement and airway collapse.23
Hepatomegaly is common in dogs with tracheal collapse and could be a reflection of
obesity, although hepatic dysfunction (as indicated by increases in levels of bile acids)
has been reported in dogs with tracheal collapse.24

DIAGNOSTIC EVALUATION
Hematologic, Biochemical Evaluation, and Heartworm Screening
The diagnosis of tracheal collapse is strongly suspected based on signalment, history
of cough, and physical examination findings. Additional diagnostic evaluation should
be performed to rule out concurrent disorders and determine appropriate therapy.
A complete blood count, chemistry panel, and heartworm screening is recommen-
ded in any coughing dog before additional diagnostic evaluation. These tests are typi-
cally unremarkable in dogs with airway collapse, although evaluation of dogs with
severe tracheal collapse showed that 12 out of 26 dogs had increases in the levels
of 2 or more liver enzymes, and stimulated bile acid levels were increased in 25 out
of 26 dogs.24 Following stent placement for management of severe, refractory airway
obstruction, bile acid concentrations decreased but plasma liver enzyme activity was
not significantly influenced.24 The cause of these changes remains unknown, although
hypoxia and development of a centrilobular liver cell necrosis was suggested as a
possible cause of liver dysfunction, similar to what has been reported in humans
with acute exacerbation of chronic respiratory disease.

Thoracic and Cervical Radiographs


Detection and grading of tracheal collapse is used to identify the location and severity
of collapse and to monitor progression of the disease. Because tracheal and airway
collapse are considered dynamic processes, it is ideal to perform diagnostic imaging
in multiple stages of the respiratory cycle. Collapse of the cervical trachea should be
evident on inspiration and the intrathoracic trachea will collapse on expiration. It is

Fig. 1. Lateral thoracic (A) and cervical (B) radiographs of a dog with cervical tracheal
collapse at the thoracic inlet. Note that the additional view (B) improves the ability to iden-
tify cervical tracheal collapse. Retraction of the larynx in (B) likely reflects upper airway
obstruction. (Courtesy of Lynelle Johnson, DVM, MS, PhD, DACVIM, Davis, CA.)
An Update on Tracheal and Airway Collapse in Dogs 5

recommended to evaluate a lateral radiograph of the thorax and cervical region (Fig. 1)
in both the inspiratory and expiratory phases, although this only slightly improves ac-
curacy in detection of collapse.18 False-positives and false-negatives are common
with plain radiography. Radiographs often underestimate the frequency and severity
of tracheal collapse and often fail to detect collapse at the carina, which is reportedly
more severe than cervical collapse.18 Radiographs also underestimate the tracheal
diameter compared with computed tomography, making them inadequate for select-
ing tracheal stent size.25 However, radiographs are useful in evaluation of concurrent
respiratory or cardiac disease.

Fluoroscopy
A fluoroscopic study can be used to evaluate a coughing dog for the presence and
location of airway collapse but this technique is only available at universities and large
referral hospitals. When radiography was compared with fluoroscopy, assuming the
fluoroscopy was correct, radiographic evidence of collapse was at the incorrect loca-
tion in 44% of dogs and it was not detected in 8% of dogs with radiographs alone.18
Fluoroscopic identification of lower airway collapse versus tracheal collapse can be
important in determining therapy (discussed later) (Fig. 2). Importantly, radiography,
fluoroscopy, and bronchoscopy might be required to allow complete evaluation of
the type of airway collapse present in a dog.26

Bronchoscopy
Bronchoscopy is considered the gold standard for diagnosis of bronchomalacia in
humans because it allows visualization of the trachea and the principal, lobar, and
sublobar bronchi to assess for bronchomalacia.27 In addition to bronchoscopy, laryn-
goscopy and bronchoalveolar lavage are recommended in coughing dogs to detect
concurrent disease that affects treatment. Bronchoscopy does require anesthesia,
which can be associated with complications in animals with severe airway obstruction,

Fig. 2. Images captured from a fluoroscopic study on inspiration (A) and expiration (B) from
a dog with intrathoracic tracheal collapse clearly show the change in luminal diameter of
the intrathoracic airway during expiration. (Courtesy of Lynelle Johnson, DVM, MS, PhD,
DACVIM, Davis, CA.)
6 Della Maggiore

marked tracheal sensitivity, dramatic expiratory effort, or those that are obese or
overly excitable.
Laryngeal collapse and paralysis can be seen concurrently with tracheal collapse and
bronchomalacia, so a thorough upper airway evaluation is recommended and should
be performed before intubation at anesthetic induction. Laryngeal collapse is graded
in 3 stages based on severity.28 Stage I is characterized by eversion of the laryngeal sac-
cules, stage 2 by medial displacement of the cuneiform process of the arytenoid carti-
lages, and stage 3 by collapse of the corniculate processes of the arytenoid cartilages
with the loss of the dorsal arch of the rima glottis. Further details are provided in Catriona
M. MacPhail’s article, “Laryngeal Disease in Dogs and Cats: An Update,” elsewhere in
this issue. As mentioned previously, in 1 report, laryngeal collapse was significantly
correlated with severe bronchial collapse in brachycephalic dogs.21
Bronchoscopic examination should be performed in a standardized fashion with the
use of tracheal bronchial anatomy and nomenclature as proposed by Amis and
McKiernan29 for proper identification. Grading of tracheal collapse is based on a
scheme determined by Tagner and Hobson30 related to the reduction in luminal
dimension (Fig. 3, Table 1).
Bronchoscopy also allows evaluation of the principal and lobar bronchi for evidence
of bronchomalacia and identifies specific segments of bronchial collapse. Bronchial
collapse in both brachycephalic and nonbrachycephalic dogs most commonly involves
the left cranial and right middle bronchi.2,3,21,23 In 1 study, 48% of dogs diagnosed with
bronchomalacia had concurrent tracheal collapse,3 whereas, in another,1 41% had
tracheal collapse in conjunction with bronchial collapse. In dogs with collapse of sublo-
bar airways, focal airway collapse was identified in 48% and diffuse airway collapse was
present in 52% of dogs.1 Bronchomalacia commonly goes underdiagnosed because it
is not visible radiographically and endoscopy is required for definitive diagnosis.
In humans bronchomalacia and dynamic airway collapse are defined as 2 separate
entities, and until recently this had not been investigated in dogs. Normal airways are
recognized as round or ovoid with minimal luminal variation (subjectively <20%) during
the respiratory cycle.1 One study examined clinical evaluation and endoscopic classi-
fication of bronchomalacia in dogs and provided evidence that static and dynamic
bronchomalacia seem to occur both independently and concurrently. Dynamic bron-
chial collapse was found alone in 59% of cases or with static bronchial collapse in
37% of dogs, and most animals (71%) had dynamic bronchial collapse and tracheal
collapse.3 Bronchial collapse in that study was defined as static if a stable airway
diameter was seen or dynamic if changes in luminal diameter were noted during respi-
ration (Fig. 4). A grading system was developed with grade I collapse defined as static
or dynamic collapse with reduction in diameter less than or equal to 50%, grade 2
collapse as diameter reduction greater than 50% and less than or equal to 75%,
and grade 3 collapse as greater than 75%, with contact between the dorsal and
ventral mucosa of the collapsed bronchus.3 If use of this grading system becomes
widespread, prospective studies could be designed to assess progression of disease
and better establish prognosis, as well as guidelines for therapeutic intervention.
Common bronchoscopic findings in some dogs with airway collapse include gross
evidence of airway inflammation, hyperemia, and mucus accumulation. Bronchoal-
veolar lavage cytology is used to document infectious or inflammatory conditions,
and culture is used to rule out concurrent infection. Varying types of inflammation
have been identified in dogs with airway collapse, although a previous study
comparing dogs with airway collapse and dogs without airway collapse showed no
clear differences in airway inflammation between groups.1 In animals with bronchoma-
lacia that have had bronchoalveolar lavage performed, neutrophilic inflammation was
An Update on Tracheal and Airway Collapse in Dogs 7

Fig. 3. Grades of tracheal collapse. (From Johnson LR, Pollard RE. Tracheal collapse and
bronchomalacia in dogs: 58 cases (7/2001-1/2008). J Vet Intern Med 2010;24:298-305; with
permission.)
8 Della Maggiore

Table 1
Grading of tracheal collapse

Grade Reduction in Luminal Diameter (%)


1 25
2 50
3 75
4 90–100 obstruction of lumen or a double
lumen (W shaped) trachea

Modified from Maggiore AD. Tracheal and Airway Collapse in Dogs. Vet Clin North Am Small An-
imal Pract. 2014; 44(1):111-27; with permission.

found in 51%.3 In dogs with airway collapse and left atrial enlargement, both neutro-
philic and lymphocytic inflammation were commonly identified.21 It remains unclear
whether inflammation precedes or follows airway collapse.

TREATMENT

The approach to treatment of airway collapse varies with the location of collapse and
the severity of the animal’s clinical signs. An animal presenting in respiratory distress is
a medical emergency and requires stabilization before diagnostic testing. Stress
should be minimized and oxygen provided as flow-by or in an oxygen cage. Acepro-
mazine (0.01–0.1 mg/kg subcutaneously every 4–6 hours) and butorphanol (0.05–
0.1 mg/kg subcutaneously every 4–6 hours) can be synergistic in providing sedation
and cough suppression, but caution should be used because oversedation could
make intubation necessary. Dogs should be maintained in a cool environment
because patients with upper airway obstructions are predisposed to hyperthermia.
Glucocorticoids are sometimes necessary to decrease laryngeal inflammation or
edema. Once the dog is stabilized, additional diagnostics and treatment options
can be considered.

MEDICAL MANAGEMENT
Environmental Factors
As an adjunct to medical therapy, environmental changes should be instituted to main-
tain the animal in a cool environment with minimal humidity. The owner’s ability to

Fig. 4. Inspiratory (A) and expiratory (B) endoscopic images of the left cranial lobar bron-
chus in a dog with bronchomalacia. (Courtesy of Lynelle Johnson, DVM, MS, PhD, DACVIM,
Davis, CA.)
An Update on Tracheal and Airway Collapse in Dogs 9

recognize and reduce specific environmental factors that increase barking, anxiety,
and excitement can help decrease the stimulus to cough. Using a harness instead
of a neck collar reduces direct stimulation and compression of the trachea.
Encouraging weight loss is one of the single most important strategies for reducing
clinical signs in dogs with airway collapse. By increasing thoracic wall compliance and
reducing extrathoracic and intra-abdominal adipose tissue, cough and respiratory dif-
ficulty can be substantially reduced. However, weight loss is typically challenging
because many of these dogs cannot effectively exercise. Careful diet planning is
essential. Current caloric intake from all sources should be determined and resting en-
ergy requirement (RER) calculated through the formula: RER 5 70  (body weight)0.75.
It is important that owners are given realistic expectations for weight loss, and ideally,
a dog should lose 1% to 2% of its weight per week. Caloric restriction alone is used
initially with weekly monitoring of weight. If this is unsuccessful, a prescription low-
calorie, high-fiber diet should be used. Identification and treatment of secondary med-
ical conditions is also important for appropriate management.

Antitussive Agents
When infection and inflammation have been adequately treated, cough suppressants
are recommended to reduce chronic irritation and control cough. These cough sup-
pressants are often the sole therapy used for cough associated with cervical tracheal
collapse. Cough suppressants regularly used include hydrocodone (0.22 mg/kg by
mouth 2–4 times a day) and butorphanol (0.55 mg/kg by mouth 2–4 times a day).
When treating an animal with cough suppressants, it is recommended to start at a
frequent dosing interval and gradually prolong the time between dose administration
until the lowest effective dose is used at the longest interval. Side effects of these
drugs include sedation, constipation, and development of tolerance.

Glucocorticoids
Glucocorticoids are often used short term to reduce laryngeal, tracheal, and bronchial
inflammation, unless a concurrent infectious condition is suspected. Initial treatment
typically involves an antiinflammatory dose of prednisone (0.5 mg/kg by mouth twice
a day) for 5 to 7 days or inhaled steroids (fluticasone propionate, 110 mg/puff, admin-
istered via face mask and spacing chamber). A short course of therapy is advised to
avoid secondary effects such as panting, which puts added stress on the respiratory
system, and weight gain. Use of inhaled in place of systemic corticosteroids can mini-
mize side effects.

Bronchodilators
Bronchodilators are sometimes used when small airway disease is suspected to
contribute to intrathoracic airway collapse. Use is based on the theory that any in-
crease in diameter of small (<300 mm) airways improves expiratory airflow, alters pres-
sure dynamics, and reduces the tendency for intrathoracic airways to collapse.
Bronchodilators have no effect on the larger airways that are visible during endoscopy
and are not indicated for treatment of cervical tracheal collapse. Bronchodilators can
play an important role when lower airway collapse/bronchomalacia is suspected or
documented on bronchoscopic evaluation, although response is variable. Methylxan-
thine bronchodilators are most commonly used and extended-release theophylline is
recommended at 10 mg/kg by mouth every 12 hours. This drug is no longer available
commercially because it is not used in human medicine, and compounding pharma-
cies must be used to obtain this medication. The efficacy of these extended-release
products is unknown and cautious dosing must be used to avoid toxicity, along
10 Della Maggiore

with clinical assessment of efficacy. b2-Agonists are more effective as true broncho-
dilators but do not seem to be as useful in management of airway collapse.
Antibiotics
Infection rarely contributes to clinical signs in airway collapse, but antibiotics can play
an important role in treating secondary infections that act as an inciting cause to
airway irritation. Doxycycline can be considered pending culture results for treatment
of mycoplasma infection as well as for antiinflammatory effects.
Surgical Interventions
When medical management fails to control clinical signs, surgical intervention or
placement of an intraluminal stent should be considered. Extraluminal tracheal rings
are indicated for cervical tracheal collapse and excellent outcomes have been re-
ported in dogs managed by skilled surgeons.31 Postoperative laryngeal paralysis
can be anticipated as a potential problem caused by impingement or praxis of the
recurrent laryngeal nerve, and, if stridor or inspiratory respiratory distress occurs after
placement of extraluminal rings, laryngeal lateralization is generally needed. Tracheal
necrosis can also be encountered long term if blood supply is damaged.32–34
If intrathoracic tracheal collapse is diagnosed and cannot be managed medically,
placement of an intraluminal stent can be considered. Complications include bacterial
tracheitis, stent fracture/migration, stent collapse/deformation, tracheal perforation
during placement, and development of obstructive granulation tissue. Patient selec-
tion is important in obtaining good outcomes. Grade 4 W-shaped tracheal malforma-
tion and the tapering diameter of the trachea from the cervical to the intrathoracic
region could be associated with an increase in the risk of stent fracture and obstructive
granulation tissue.35 Intraluminal stents or surgical management can be lifesaving and
excellent short-term and long-term outcomes have been reported.19,36 Extensive
medical management is often required to control cough, infection, and inflammation
after stent placement.
Prognosis
Little has been published about overall prognosis in dogs with airway collapse that are
medically managed. There is concern that disease will gradually progress over time
and dogs will become refractory to treatment. However, most dogs can be success-
fully managed with diligent attention to weight control, identification and control of
infection and inflammation, and appropriate use of interventional therapy.

DISCLOSURE

None.

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