The initiating cause of coughing is the activation of sensory receptors, which may be rapidly adapting (stretch) receptors (RARs) and augmented by bronchial C-fibres. These receptors are primarily found in the large and transitional airways and are predominantly sensitive to mechanical stimulation, but also to chemical stimuli. Pulmonary C-fibres are considered sparse in small animal species.
The main cause of coughing therefore tends to be pathologies that either perform a mechanical or chemical irritant effect within the airways, though cough may also occur with parenchymal and pleural space disorders.
Cardiogenic pulmonary oedema is often cited as a cause of cough, and indeed in those dogs presenting with fulminating pulmonary oedema with accumulation of large amounts of pink-tinged oedema fluid within larger airways, this may be a prominent clinical feature. However, in the majority of dogs with pulmonary oedema causing alveolar flooding, cough receptor excitation would not be an expected feature, with tachypnoea/hyperpnoea (‘breathlessness’) being a more consistent feature.
Myxomatous mitral valve disease
The most common acquired cardiac disease associated with development of pulmonary oedema is myxomatous mitral valve disease (MMVD). Heart murmurs consistent with MMVD may be identified in 3.54% of all dogs examined in UK first opinion clinics (Mattin et al., 2015), and the prevalence of heart murmurs in dogs, especially in small breed dogs, increases with age.
In one study, 24% of dogs aged nine to 12, and 37% of dogs aged 13 and over, were found to have murmurs consistent with MMVD (Detweiler and Patterson, 1965) and in some breeds, notably the Cavalier King Charles spaniel, prevalence in dogs older than eight years of age may become very high indeed.
However, mitral valve disease is typically characterised by a very long pre-clinical period, and only a minority of patients with asymptomatic MMVD in most longitudinal studies progress to a point where symptoms of congestive heart failure develop. Thus, the typical busy small animal clinician will encounter many dogs with heart murmurs consistent with MMVD who will not be (and might never be within their lifetimes) in congestive heart failure. When patients with such murmurs present with cough, clinicians are presented with a diagnostic dilemma as to how relevant the finding of a heart murmur typical of MMVD may be.
Studies have shown that the presence of congestive heart failure is not significantly associated with coughing in dogs with MMVD, but that radiographic evidence of airway disease and left atrial enlargement is (Ferasin et al., 2013).
Might some dogs cough, not due to presence of pulmonary oedema, but due to the effects of left atrial enlargement as a result of mitral regurgitation compressing the bronchi (and thus exciting mechanoreceptor-mediated coughing)? One study specifically examining this failed to show an association between left atrial enlargement and bronchial collapse, and many dogs with bronchial collapse and left atrial enlargement have collapse (Singh et al., 2012) that is not just confined to the left-sided bronchi, suggesting more wide-spread bronchomalacia (Figure 1).
Distinguishing between potential
causes of a cough
Cough may have many potential inciting causes. The history and the physical examination are the most important features in helping distinguish between them.
The timing of coughing may be important and it should always be ascertained whether cough occurs in association with eating and drinking (which may implicate aspiration due to failure of effective laryngeal guarding), or whether cough is associated with excitement/exercise.
The latter is a hallmark of dynamic airway collapse, not heart disease. Loud, harsh coughs are most typical of large airway disease, and if accompanied by honking sounds, typify dynamic large airway collapse (Figure 2). Softer, wetter coughs are more consistently reported with lower airway disorders.
Exercise tolerance should always be specifically questioned, because while there are many potential non-cardiac causes of exercise intolerance, it would not be expected for an animal with heart failure to be able to exercise normally. Most dogs with primarily inflammatory or dynamic airway disorders will be able to exercise quite normally, the principal exception being those patients with laryngeal paralysis.
Dysphonia, exercise intolerance, audible stridor with exercise and heat intolerance are all useful historical clues to the possibility of laryngeal paralysis.
Sudden onset of cough associated with field exercise (and often showing partial response to antibiotic therapy with relapse on cessation) typifies airway foreign bodies. However, infectious tracheobronchitis also occurs with sudden onset, and health status of in-contact dogs should always be ascertained.
Physical examination should be preceded by observation of the patient’s respiratory rate and effort, paying particular attention to whether (assuming alteration in respiratory pattern is seen) breathing is rapid and shallow (so-called ‘choppy’ or ‘restrictive’ respiratory pattern) or is slow and forceful (‘obstructive’ respiratory pattern). For the latter, determination should be made whether most effort occurs during inspiration or expiration.
Respiratory sounds audible without the aid of a stethoscope include stridor (high-pitched due to fixed upper airway obstructive lesions) and stertor (low-pitched/snoring due to oscillating softer tissues in the upper airways), which are compatible with obstructive upper airway disease.
Auscultation should proceed in a systematic fashion, with the cardiac precordial pulse being palpated prior to application of the stethoscope in order to appreciate distribution and shifting of position, as well as precordial thrills associated with grade V and VI/VI heart murmurs.
Assessment of cardiac-origin sounds should always be accompanied by interpretive palpation of the peripheral pulse rate, rhythm, quality and pressure needed to occlude and the clinical questions of ‘what is the heart rate and rhythm?’, ‘does it alter with respiration and if so, does it do this cyclically?’ and ‘are there additional cardiac sounds (such as murmurs) and what is their intensity, position, timing and duration?’
Of particular importance is the finding of a respiratory sinus arrhythmia. This normal acceleration of rate during inspiration and deceleration during expiration, being mediated by parasympathetic (vagal) tone, is absent in patients with congestive heart failure (since sympathetic nervous system activation is provoked), and its presence excludes congestive heart failure (though not all clinically-relevant heart disease) at the time of examination. Furthermore, a potent cause of enhanced vagal tone (and thus of a respiratory sinus arrhythmia) are primary respiratory diseases, especially those that are obstructive in nature. A sinus arrhythmia, if present, is a very important clinical ‘clue’ in distinguishing between cardiogenic and respiratory causes of respiratory signs in patients who may also have a heart murmur detected (provided that the clinician auscultates for long enough and with observation of the patient’s respiration to appreciate it).
Cardiac apex and base should be auscultated bilaterally. The respiratory structures should be auscultated in their entirety, bearing in mind that normal laminar air flow in the small respiratory airways should be silent and normal ‘bronchovesicular’ sounds auscultated over the thoracic wall are really ‘pseudosounds’ originating from larger airways whose transmission through lung parenchyma, pleural space and thoracic wall dictates their audibility or lack of. Attenuation of such sounds should prompt percussion to distinguish between fluid/tissue and air as an interrupting interface, for example in pleural effusion or pneumothorax. Crackles and wheezes are truly lower-airway origin adventitial lung sounds, the former having a low sensitivity for detection of congestive heart failure. Provocation of harsh/honking cough with palpation of the trachea or with excitement suggests inflammatory tracheal disease or dynamic large airway collapse.
Investigation of coughing will usually necessitate some form of diagnostic imaging (of which radiography is the most accessible, useful and cost-effective) and where airway disorders are present, some form of direct visualisation of airway structures. If congestive heart failure is a possibility, good-quality and well-positioned orthogonal thoracic radiographs are the most useful diagnostic test to evaluate this.
Radiography of the large airways should always include the extrathoracic as well as intrathoracic structures, and sensitivity of detection of dynamic collapse is enhanced by taking exposures during both inspiration and expiration.
The upper airways are best radiographed under general anaesthesia once congestive heart failure is excluded, and consideration should be given to evaluation of laryngeal under a very light plane of anaesthesia at induction.
Tracheobronchoscopy remains the best means of examining the airways and to collect material by bronchoalveolar lavage for cytology and culture (Figure 3). Examination should be rapid but thorough, based on a sound knowledge of the airway anatomy, to ensure no errors of omission arise.
The pharynx and trachea are not sterile and many commensal bacterial organisms from these regions may be cultures as contaminants if samples are not collected via bronchoscopic direction. Diagnosis by response to empirical treatment, other than parasiticides, is generally fraught with interpretive difficulty. Therapeutic trials for treatment of congestive heart failure are problematic since dogs with respiratory disorders may show apparent response and thoracic radiography is preferred.