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Respiratory Diseases by Clinical Signs
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The purpose of this chapter is to provide the reader with a "horizontal" approach to the diagnosis of equine respiratory diseases based on clinical signs. The following major clinical manifestations of respiratory diseases will be reviewed in detail: abnormal respiratory sounds, acute respiratory distress, cough, nasal discharge, and poor performance.
dorsal displacement of the soft palate
exercise-induced pulmonary hemorrhage
inflammatory airway disease
partial pressure of oxygen in arterial blood
partial pressure of carbon dioxide in arterial blood
packed cell volume
summer pasture-associated obstructive pulmonary disease
Abnormal Respiratory Sounds
Most of the investigations of respiratory sounds have been performed in humans and animal models other than the horse. Therefore, application of these findings to the horse should be made cautiously. Clinical experience suggests however, that acoustic properties of the equine respiratory tract are fundamentally similar to other mammals.
Respiratory sounds are generated by the vibration of airways during breathing. Vibrating airways produce pressure waves that travel along airways and through the body and are perceived by the ear as sounds if they are in the audible range (20 - 20,000 Hz) . Abnormal respiratory sounds are superimposed on normal sounds and reflect a change in the relationship between flow rate through the airways and their geometry and elastance .
From a clinical perspective, it is convenient to separate sounds based on their primary site of origin: 1) extra-thoracic airways (upper airway sounds), 2) intra-thoracic airways (lung sounds). However, one must realize that sounds heard during chest auscultation for example are a combination of sounds coming from airways close to the stethoscope and "referred" sounds originating from other pulmonary regions and upper airways .
Respiratory sounds are complex mix of different pressure waves that can be separated into a range of frequencies (sound spectrum). Sound may be further characterized by its intensity or energy, which is related to pressure wave amplitude.
The human ear is only responsive to a certain range of sound frequencies (audible range). Respiratory sounds heard with or without a stethoscope may be characterized by their pitch and loudness. Pitch is mainly related to the sound frequency spectrum and loudness depends on pressure wave amplitude . Transmission of respiratory sounds follows the same physical laws that determine the image quality generated by a practitioner using an ultrasound machine. Sound transmission through different structures depends on the acoustic properties (impedance) of these structures, which is primarily a function of their density. The intensity of a sound decreases as distance from the source increases. Sound transmitted through homogeneous tissue (i.e., similar acoustic properties) loses little energy. An analogy to this is a comparison to transmission of ultrasound signal. During ultrasonography of a horse's abdomen, spleen and liver may be imaged next to each other and appear to have relatively similar echogenicity because they have comparable acoustic properties. However, when sound travels through two regions of different acoustic properties, sound waves are partially reflected at the interface between the regions. Placing an ultrasound probe over the chest of a horse allows good visualization of the chest wall, however, the lung tissue cannot be imaged because sound waves are reflected at the interface between lung and chest wall that have markedly different acoustic impedance. This is why respiratory sounds auscultated over the trachea are significantly louder than sounds heard over the chest. In addition, transmission of breath sounds through the chest wall affects both amplitude and frequencies of sound waves resulting in filtration of sounds .
Stethoscopes are only conduits for sounds audible over the body surface. A lack of standardization and objective testing resulted in proliferation of a wide variety of stethoscopes that often differ in the way they amplify or attenuate particular sound spectrum, therefore affecting the original quality of sound . The recent availability of electronic stethoscopes (e.g., 3M Littmann, ADC, Cardionics, The E-Scope, JABES, Philips Agilent, Stethtron, Welch Allyn Meditron) and digital recording of sound will allow standardization of respiratory sound interpretation and may help clinicians derive more information from auscultation of the respiratory tract. In addition, progress in computer technology has allowed sophisticated analysis of respiratory sounds (spectral analysis) that may prove to be useful as a non-invasive diagnosis test of airway obstruction in the horse .
Classification of Respiratory Sounds
Respiratory sounds may be divided into lung sounds and upper airway sounds. The former are best heard by auscultation of the chest using a stethoscope. The latter may be heard directly at the nostril opening or by auscultation over the trachea. Increase in ventilation (e.g., post-exercise) and auscultation of animals with a thin chest wall (e.g., foals) will result in increase in sound intensity.
They are divided into breath sounds (normal) and adventitious (abnormal) lung sounds. Breath sounds are produced by turbulent flow associated with air movement through the large airways (diameter above 1-2 mm) . They range in frequency from 75 to 2000 Hz when recorded at the mouth or over the trachea . Breath sounds recorded over the chest peak in frequency below 100 Hz, then sound energy drop off abruptly between 100 and 200 Hz. Originally, Laënnec introduced the term "vesicular" sounds to refer to sounds heard over the chest . This terminology assumed that breath sounds originated from the alveoli and therefore should not be used.
Terminology for adventitious sounds has been clarified by the International Lung Sounds Association and is broadly accepted in veterinary medicine [10,11]. Adventitious sounds should be classified as wheezes or crackles. Wheezes are continuous, musical sounds (Video 1) that are generated principally by the flutter of airway walls and potentially by movement of airway secretions . Experiments conducted in vitro and in vivo showed that flow limitation was necessary for wheezing to occur and that critical transpulmonary pressures were required. Factors influencing the sound spectrum of wheezing are airway wall thickness, bending stiffness, and longitudinal tension . Crackles are short, non-musical sounds (Video 2) called "miniature explosions" by Forgacs . The early theory hypothesizing that crackles are produced by the explosive opening of small airways previously kept closed by surface forces has been supported by subsequent studies .
Video 1 - 2.93 Mo - Auscultation of inspiratory and expiratory wheezes in a horse with heaves. (Courtesy Dr. Michel Levy).
Video 2 - 3.53 Mo - Auscultation of increased breath sounds, inspiratory crackles, and expiratory wheezes in a horse with heaves. (Courtesy Dr. Michel Levy).
Upper Airway Sounds
At rest, normal respiratory sounds generated by the upper airways are predominant during tracheal auscultation but are difficult to hear at the level of the nostril opening. Because there is a close relation between airflow and sound intensity, increased ventilation (e.g., during exercise) results in more audible upper airway sounds. As for lung sounds, upper airway sounds are generated by vibration of airway walls during normal breathing. The relation between flow rate, airway elastance, and airway dimensions determines characteristics of the sound. Tracheal sounds recorded in humans reveal a broad spectrum of frequencies ranging from less than 100 Hz to more than 1500 Hz with a marked drop in energy above 800 Hz . Studies in exercising horses demonstrate that the spectrum of respiratory sounds recorded over the trachea or in front of the nose is in the audible range with most of the sound energy contained in frequencies up to 800 Hz [6,14]. Expiratory sounds predominate in horses exercising strenuously. Nomenclature of upper airway sounds is variable. Stridor refers to high intensity and frequency sounds in general and stertor describes high intensity sounds occurring in coma or deep sleep. Descriptions of abnormal sounds occurring during exercise use colorful terms such as roaring, rattling, or gurgling.
Pathogenesis of Abnormal Respiratory Sounds
Perturbation of airflow through the respiratory tract may be secondary to fixed or variable obstructions. Abnormal respiratory sounds have different characteristics depending on the site of obstruction (i.e., extrathoracic or intrathoracic) and on the type of obstruction (i.e., fixed or variable). Fixed obstructions (e.g., deviated nasal septum) result in a similar degree of airflow obstruction during inhalation and exhalation. Variable obstructions (e.g., laryngeal hemiplegia, DDSP) generate different degrees of airway obstruction based on flow rate, site of obstruction, and phase of the respiratory cycle. Clinically, different types of respiratory sounds may be associated with different types of obstructions.
Upper Airway Sounds
Respiratory muscles generate subatmospheric pressures inside airways during inspiration resulting in a tendency for extrathoracic airways not supported by rigid structures (e.g., nares, false nostril, pharynx, and larynx) to collapse . Collapse is prevented by dynamic contraction of upper respiratory muscles resulting in stabilization of these structures. The role of these muscles is particularly important during exercise because pressure changes across airway walls increase dramatically as ventilation increases. As soon as horses start exercising, muscle contraction dilate nostrils, tense the soft palate, and abduct arytenoid cartilages in order to increase airway diameter and accommodate for the increase ventilation. Extension of the horse's head and neck also stretches the trachea, which becomes stiffer and less susceptible to dynamic collapse .
Neuromuscular dysfunction may result in upper airway collapse during inspiration and generate variable degree of airway obstruction. The most common example is laryngeal hemiplegia that results in inward collapse and vibration of the arytenoid cartilage responsible for the characteristic "roaring" sound in the exercising horse . Studies in exercising horses with laryngeal hemiplegia reveal that expiratory sounds, flows, and pressures are not different from those recorded in horses with normal airway function [6,18]. However, inspiratory sounds are markedly different and are associated with airway obstruction resulting in significant reduction in inspiratory flows. These sounds appear to have unique frequency spectrum that may prove to be useful to diagnose laryngeal hemiplegia using an easy and non-invasive test both in laboratory condition and in the field [6,14]. Upper airway obstruction may occur during expiration as seen in cases of dorsal displacement of the soft palate (DDSP) in exercising horses . In this case, abnormal respiratory sounds develop throughout exhalation and are often described as rattling or gurgling noises. It is noteworthy that some horses may experience upper airway collapse (e.g., DDSP) without generating abnormal respiratory sounds . A combination of factors, including flow rates and airway properties, has to reach a critical value beyond which the upper airway becomes unstable and starts vibrating . Therefore, upper airway obstruction is not necessarily accompanied by abnormal respiratory sounds. Alternatively, abnormal respiratory sounds do not necessarily cause airflow obstruction. For example, young horses (1-2 year-old) in early stages of training often produce loud, rattling expiratory sounds that appear to originate from nostril fluttering. These abnormal sounds eventually disappear as the horse matures. Nasal diameter is minimal at the level of the rostral third of the nose (nasal valve) and at comparable body size, young horses have smaller nasal passages (Couëtil, unpublished data). We speculate that the relatively narrower nasal passages make these young horses more prone to develop abnormal respiratory sounds generated by nostril vibrations.
Fixed obstructions in the extrathoracic airways tend to generate abnormal respiratory sounds during both inhalation and exhalation (nasal mass).
Lung sounds are generally bilaterally symmetrical and asymmetry suggests disease. This is due to changes in lung structure that ultimately affect timing and amplitude of sound transmitted to the chest surface . Intensity of breath sounds will increase with increased ventilation regardless of the cause (exercise, fever, excitement, pulmonary disease) (Video 2). Horses with variable obstruction of intrathoracic airways (e.g., heaves) commonly have increased breath sounds because airflow velocity is higher through narrow airways [20,21]. Also, expiratory sounds are often louder than inspiratory sounds. Interestingly, lung sounds heard over consolidated lung may be louder despite the lack of airflow through the consolidated lung. Because sound is transmitted more efficiently between tissues of similar acoustic properties (e.g., consolidated lung and chest wall), sound with relatively low intensity originally may be transmitted with little attenuation and be heard as a louder sound at the chest surface. Pleural effusion and pneumothorax cause a marked reflection of lung sounds resulting in sharp decrease in breath sounds intensity that is useful clinically to localize the disease process. For example, a "fluid line" is often identified in horses with pleural effusion below which lung sounds are obliterated.
In the horse, wheezes are commonly associated with obstructive lung diseases such as heaves and bronchopneumonia. It is useful to characterize the sounds based on auscultation of single or multiple wheezes, their location and distribution, and their timing in the respiratory cycle. Wheezes originating from intrathoracic airways are more likely to be heard during expiration because airways are dynamically compression during that phase of respiration (e.g., heaves). Alternatively, wheezing is absent in many horses with significant airway obstruction underlining the lack of sensitivity of auscultation for the diagnosis of obstructive lung disease . Late-inspiratory wheezes are commonly heard in horses with atelectasis or consolidation as air starts flowing through previously collapsed airways . Extrathoracic airway obstruction frequently results in inspiratory wheezes. Determining the point of maximum intensity by comparing thoracic and tracheal sounds will help localize the site of obstruction.
Late-inspiratory crackles are often present in restrictive lung disease such as pulmonary edema, interstitial pneumonia, and pulmonary fibrosis . Restrictive diseases require higher respiratory efforts to combat the decreased lung compliance and volume. As a result, collapsed airways tend to reopen late during inhalation when significant lung expansion has occurred. Crackles are commonly heard during early inhalation or early exhalation in horses with obstructive lung diseases.
Loud abnormal respiratory sounds, audible without a stethoscope, invariably indicate extrathoracic or upper airway obstructive disease. Some horses with severe intrathoracic obstructive disease (e.g., heaves) produce wheezes audible at the nostril opening, however, sound intensity is maximal during thoracic auscultation. Abnormal respiratory sounds heard only during exercise indicate extrathoracic airway obstruction that we will refer to as upper airway obstruction in this discussion.
The first step in evaluating abnormal respiratory sounds that can be heard in the resting animal is to compare the sound intensity (loudness) at the nostril opening to auscultation over the trachea and thorax. Upper airway obstructions are associated with respiratory sounds that are louder at the nostril opening and over the trachea. Depending on the intensity of the respiratory sounds, it may be advantageous to make the horse breathe into a large plastic bag (10 - 15 liters) placed over the muzzle in order to increase ventilation (Video 3). Auscultation during the rebreathing maneuver will make breath sounds more audible and increase the likelihood of detecting abnormal sounds. Alternatively, administration of lobeline (0.2 mg/kg, IV) induces a hyperpnea that is of greater magnitude than that produced by rebreathing or moderate exercise . Lobeline-induced hyperpnea may be a useful diagnostic aid for upper and lower airway obstructive diseases [24,25]. Rebreathing maneuvers and lobeline administration are contraindicated in horses that exhibit increased respiratory effort at rest.
Video 3 - 3.27 Mo - Rebreathing maneuver performed by placing a plastic bag around the horse’s muzzle.
Abnormal Upper Respiratory Sounds
Variable (dynamic) obstructions are characterized by a marked difference between inspiratory and expiratory sounds (Fig. 1). Abnormal inspiratory sounds (inspiratory stridor) indicate airway obstruction by collapsible structures such as nostril, alar folds, pharynx, larynx, and extrathoracic trachea. A long list of diseases may result in upper airway collapse at rest or during exercise including facial paralysis, alar fold obstruction, DDSP, pharyngeal collapse, laryngeal hemiplegia (Video 5), epiglottic cyst, axial deviation of the aryepiglottic folds, epiglottic retroversion, rostral displacement of palatopharyngeal arch, and tracheal collapse to name a few (Video 4). Abnormal expiratory sounds may be due to nostril fluttering or DDSP (Video 6). Fixed obstructions result in similar inspiratory and expiratory sounds. Examples of fixed obstructions are nasal septum deviation, rhinitis, sinus disease (infection, cyst, tumor), choanal atresia, congenitally narrow nasal passages, ethmoid hematoma, abscess, tumor, granuloma, cyst, and chondritis. Comparison of respiratory efforts and sounds after obstruction of an individual nostril may help localize unilateral nasal obstruction. Diagnosis is often achieved by endoscopy or radiography of the upper airways. In some cases of exercise-induced stridor, dynamic endoscopy while the horse exercises on a treadmill is required in order to recreate airway pressures needed to generate the obstruction.
Figure 1. Diagnostic approach for horses with abnormal upper respiratory sounds. DDSP: dorsal displacement of the soft palate; ≠: different; ≈: similar.
Video 4 - 1 Mo - Miniature horse with inspiratory stridor secondary to tracheal collapse.
Video 5 - 4.19 Mo - Upper airway endoscopy of a horse with left sided-laryngeal hemiplegia during treadmill exercise. The typical inspiratory "roaring" noise is heard best during the second part of the recording.
Video 6 - 5.35 Mo - Upper airway endoscopy of a horse with dorsal displacement of the soft palate during treadmill exercise. Normal upper airway function during the first half of the recording (slow speed). Displaced soft palate accompanied by multiple swallowing in an attempt to replace the soft palate in the proper position.
Abnormal Lung Sounds
Increased lung sounds that may be heard diffusely over both sides of the chest are consistent with increased ventilation (Fig. 2). Physiologic causes of increased ventilation are exercise, hyperthermia, and excitement. Pathologic causes are fever, obstructive lung disease (heaves, SPAOPD, severe IAD), cardiac disease, acidemia, and severe anemia. Anemia itself has no major effect on pulmonary function because peripheral chemoreceptors are stimulated by a decrease in PaO2 and not arterial oxygen content. Stimulation of respiration in cases of severe anemia develops when tissue hypoxemia results in increased anaerobic metabolism and lactic acidosis .
Figure 2. Diagnostic approach for horses with abnormal lung sounds.
Increased lung sounds over a limited area suggest presence of lung consolidation or a mass (neoplasia, abscess, granuloma). Lung consolidation refers to the firmer texture of the pneumonic lung due to atelectasis and flooding of airspaces with exudate .
Decreased breath sounds may result from pleural effusion due to pleuropneumonia, pleuritis, pericarditis, peritonitis, viral respiratory diseases, mycoplasma infection, congestive heart failure, liver disease, diaphragmatic herniation, hypoproteinemia, neoplasia (e.g., lymphosarcoma, gastric squamous cell carcinoma), equine infectious anemia, pulmonary granulomas, chylothorax, and fungal pneumonia . Lung sounds are absent ventrally with pleural effusion and dorsally with pneumothorax. Percussion of the thorax also allows differentiation between pleural effusion resulting in ventral dullness and pneumothorax associated with increased dorsal resonance and normal percussion ventrally. Emphysema can also result in decreased or absent lung sounds because of decreased airflow velocity and increased sound reflection at the pleural surface .
Multiple expiratory wheezes heard over both sides of the chest indicate diffuse airflow obstruction and are often present in horses with heaves, SPAOPD, and severe IAD. Expiratory wheezes over focal areas are commonly heard in bronchopneumonia. Inspiratory wheezes are common in horses with atelectasis or consolidation. Atelectasis may be congenital like in foals with acute respiratory distress syndrome or acquired . Acquired atelectasis may develop from compression of the lung caused by pleural effusion, masses, pneumothorax, and excessive abdominal distension or from airway blockage by mucosal edema, exudates, foreign material, parasites, and neoplasms. Atelectasis is also common after prolonged recumbency.
Acute Respiratory Distress
Respiratory distress is defined as labored breathing characterized by an exaggerated effort to breathe relative to the degree of physical activity. Dyspnea is defined as "undue awareness of breathing or awareness of difficulty in breathing" . This term is therefore inappropriate to describe veterinary patients. Clinical signs associated with respiratory distress in the horse usually include inactivity, exercise intolerance, anxious expression, flaring of the nostrils, increased respiratory efforts, asynchrony between thoracic and abdominal movements, stridor, extended head and neck, cyanosis, and pumping of the anus synchronized with the respiratory cycle . Acute respiratory distress may be a manifestation of impaired gas exchanges that may result from obstruction of conducting airways, failure of the muscles and structures responsible for ventilation, pulmonary disease, or cardiac disease. Labored breathing in response to pain, hyperthermia, and metabolic acidosis is not associated with gas exchange abnormalities.
Breathing is controlled by several mechanisms that regulate delivery of air to the alveoli (ventilation) in response to metabolic demand. The respiratory center responds to information originating from central and peripheral receptors and in turn modulates the activity of the respiratory muscles. As a result, PaO2 and PaCO2 are maintained within close limits . An understanding of the basic control mechanisms and the mechanics of breathing is valuable to diagnose and treat the causes of respiratory distress.
Control of Breathing
Ventilation is coordinated by the respiratory center located in the medulla, which is responsible for respiratory pattern generation . The respiratory center is under the influence of neuronal and chemical control mechanisms.
Two types of chemoreceptors, central and peripheral, have excitatory effect on the respiratory center. Central chemoreceptors, located on the surface of the medulla, are sensitive to pH alteration in the cerebrospinal fluid. An increase in PaCO2 causes a rise in the partial pressure of CO2 in the cerebrospinal fluid and a proportional fall in pH. The reduction in pH stimulates respiratory neurons and results in increased respiratory rate and depth. Peripheral chemoreceptors located in the carotid and aortic bodies are stimulated by a decline in PaO2 and a rise in PaCO2 or H+ concentration. Horses' central and peripheral chemoreceptors respond similarly to other species . Stimulation of peripheral receptors is by decreased PaO2 and not reduced blood oxygen content. Therefore, diseases causing a decline in blood oxygen content (e.g., anemia, methemoglobinemia, carboxyhemoglobinemia) do not usually stimulate breathing. Stimulation of respiration in cases of severe anemia develops when tissue hypoxemia result in increased anaerobic metabolism and lactic acidosis .
The respiratory center receives input from the central nervous system and peripheral receptors. Increased ventilation may result from central nervous system stimulation via the cerebral cortex and the pons. For example the cortex can override the respiration center in response to excitement. Peripheral inputs from non-chemical reflexes may originate from the lungs, the upper respiratory tract, the musculoskeletal system, phrenic nerves, and baroreceptor reflexes. Pulmonary stretch receptors located mainly in the airways are responsible for the inflation and deflation reflexes (Hering-Breuer reflexes). Inspiration is inhibited in response to a sustained inflation of the lung and alternatively, deflation of the lung stimulates inspiratory activity. Another type of pulmonary receptors is juxta-capillary or "J" receptors associated with C-fiber endings. They are closely associated with alveolar capillaries. J receptors may be activated by tissue damage, accumulation of interstitial fluid, and release of inflammatory mediators. C-fibers appear to play a role in the respiratory response to pulmonary congestion, embolization, and exercise. The mechanoreceptors located in the pharynx and larynx respond to changes in transmural pressure. Negative pressure generated in the upper airway, particularly during exercise, leads to increased pharyngeal dilator muscle activity and can be blocked by topical anesthesia . Stimulation of chemical and irritant receptors located in the main conducting airways may result in cough, mucous production, hyperpnea, and bronchoconstriction. Afferent innervation from mechanical and chemical receptors travels to the respiratory center via vagal nerves. The role of these receptors in horses with pulmonary disease is underscored by the fact that vagal blockade abolishes tachypnea resulting from experimentally induced pulmonary disease [34,35].
Mechanics of Breathing
Ventilation of the lungs is produced by the effects of respiratory muscles on the chest wall. The diaphragm is the most important inspiratory muscle. Contraction of the diaphragm and external intercostal muscles results in enlargement of the thoracic cavity and inspiration. Expiration at rest requires no muscular activity in most species. The horse is an exception to this rule with active and passive phases to both inspiration and expiration . The first part of expiration is passive, however, the end of expiration results from contraction of abdominal muscles. Consequently, the first part of inspiration is passive and is followed by active inspiration. Respiratory distress may result from neuromuscular diseases affecting function of the respiratory muscles (e.g., botulism) or from mechanical dysfunction (e.g., increased abdominal pressure, pneumothorax) .
Ventilation occurs when the force developed by respiratory muscles rises above the elastic recoil of the lung, the resistance to airflow presented by the airways and lung tissue, and the inertial forces . For practical purposes, inertial forces are considered negligible except during exercise . Diseases resulting in decreased lung elasticity (compliance) will require increased work of breathing (e.g., pulmonary fibrosis, interstitial pneumonia). Lung expansion may also be impaired by diseases outside the lung (e.g., pleural effusion, chest wall trauma). Diseases of the lung or outside that limit lung expansion are called restrictive diseases. Obstructive diseases cause increase resistance to airflow as a result of intraluminal obstruction (e.g., mucus, foreign body), airway wall disease (e.g., mucosal edema, bronchoconstriction), or diseases outside airways (e.g., abscess compressing an airway). Upper airway resistance represents approximately 50-80% of total resistance to airflow with nasal passages being responsible for at least 50% of upper airway resistance [39,40]. In addition, the horse is an obligatory nose breather and cannot switch to oral breathing in the event of nasal obstruction. Lower airway obstruction is commonly associated with diseases causing bronchoconstriction (e.g., heaves). Administration of vagolytic drugs like atropine results in bronchodilation, and decreased airway resistance and breathing efforts . Bronchodilation may also be achieved by stimulation of adrenergic smooth muscle receptors, in particular beta2 receptors. Stimulation of beta2 receptors is mainly from circulating catecholamines and minimally from sympathetic innervation . Finally, nonadrenergic-noncholinergic innervation exerts an inhibitory function on airway smooth muscle that may be impaired in horses with diseases such as heaves [43,44].
Causes of Abnormal Gas Exchange
Respiratory distress most commonly results from the inability of the respiratory tract to meet metabolic demand while maintaining PaO2 and PaCO2 within physiologic ranges. There are five causes of decreased PaO2 or hypoxemia: hypoventilation, ventilation-perfusion inequality, shunt, diffusion impairment, and reduction of inspired PO2 . The latter situation is encountered in situations such as high altitude environment. Hypoventilation is a reduction in the delivery of fresh gas to the alveoli and is always accompanied by hypercapnia. The magnitude of the decrease in PaO2 is directly related to the increase in PaCO2 according to the alveolar gas equation. In the first approximation, every increase in PaCO2 of 1 mmHg results in a decrease in PaO2 of 1 mmHg. Causes of hypoventilation include depression of the respiratory center by pharmacologic agents (e.g., barbiturates) or diseases of the central nervous system, restrictive diseases, and upper airway obstruction . V/Q inequality is characterized by a mismatch of alveolar blood flow and ventilation. This mechanism is the most common cause of hypoxemia in obstructive and restrictive diseases . Respiratory diseases with high V/Q ratios are usually caused by decreased lung perfusion (e.g., shock, pulmonary thromboembolism). Diseases with low V/Q ratios are commonly associated with decreased ventilation such as obstructive lung diseases (e.g., heaves) and pulmonary atelectasis and consolidation . Shunt is one extreme of the V/Q inequality spectrum (V/Q = 0) where some blood reaches the arterial without passing through ventilated areas of the lung. Intrapulmonary causes of shunt are pulmonary consolidation, atelectasis, and arterial-venous fistulas. Extrapulmonary shunts are commonly associated with congenital cardiac diseases (e.g., patent-ductus arteriosus, atrial and ventricular septal defects). Diffusion limitation means that PO2 in alveoli and capillaries does not does not reach equilibrium. Diseases associated with thickening of the blood-gas barrier will slow down diffusion of oxygen (e.g., pulmonary interstitial fibrosis) and usually exercise will result in worsening of the hypoxemia . Hypoxemia may be readily reversed by administration of 100% oxygen in cases of hypoventilation, V/Q inequality, and diffusion impairment. In patients with shunt the increase in PaO2 in response to 100% oxygen is marginal.
Rapid questioning should identify important risk factors such as traumatic events, strenuous exercise, environmental factors, and prior respiratory or cardiac diseases. For example, strenuous exercise in hot and humidity conditions can result in hyperthermia and respiratory distress. Horses with a history of heaves may develop labored breathing within hours of exposure to moldy hay.
The first step is to determine if abnormal respiratory sounds are present and to identify their origin (i.e., upper vs. lower airways, Fig. 3). Acute respiratory distress associated with upper airway obstruction is usually associated with loud abnormal respiratory sounds (stridor). Fixed obstructions result in sounds, respiratory efforts, and respiratory times that are comparable during inspiration and expiration. Variable (dynamic) obstructions are characterized by a marked difference between inspiratory and expiratory sounds. Inspiratory stridor indicates airway obstruction by collapsible structures such as nostril, alar folds, pharynx, larynx, and extrathoracic trachea. Labored breathing may be evident at rest and amplified by light exercise or it may only occur during exercise (e.g., laryngeal hemiplegia). Endoscopic examination should be performed rapidly in order to localize the disease process. However, care should be taken to not increase the stress level of the horse because hypoxemia may worsen and result in neurological signs such as uncontrollable excitement, collapse, and death. Foals that are not accustomed to be restrained should be started on nasal oxygen supplementation and tranquilized with low doses of sedative. Emergency tracheostomy usually dramatically improves clinical signs in horses with acute upper respiratory tract obstruction, except if the obstruction occurs in the distal trachea (e.g., tracheal collapse). In these cases, tracheal intubation or breathing a mixture of helium and oxygen may help temporarily. In rare cases, acute upper airway obstruction may be complicated by pulmonary edema . Radiography of the upper airways may be useful to identify fracture, mass, fluid lines, and foreign body.
Figure 3. Diagnostic approach for horses with acute respiratory distress. CBC: complete blood count; U/S: ultrasonography; XRay: radiography.
Palpation of the horse may provide some important clues. Widespread subcutaneous emphysema in a horse with inspiratory dyspnea is strongly suggestive of tracheal laceration resulting in dynamic upper airway collapse. Foal with rib fractures resulting in pneumothorax and acute respiratory distress often have palpable evidence of pain, edema, and crepitation over the affected area of the rib cage.
Decreased lung sounds in the ventral thorax is usually indicative of pleural effusion or diaphragmatic hernia. Decreased lung sounds dorsally associated with increased resonance on percussion of the thorax is consistent with pneumothorax. Diagnosis may be confirmed by ultrasonography of the thoracic cavity. Presence of abnormal lung sounds (crackles, wheezes) in horses with fever and respiratory distress suggests infectious pulmonary disease (e.g., bronchopneumonia, pulmonary abscess, interstitial pneumonia, necrotizing pneumonia) [47,48].
Measurement of arterial blood gases and response to oxygen supplementation is helpful for treatment monitoring. For example, the neonatal foal's respiratory center may be suppressed by overzealous oxygen supplementation and result in severe hypercapnia.
Afebrile horses with acute respiratory distress and abnormal lung sounds should be treated with a fast acting bronchodilator (e.g., aerosolized albuterol, intravenous atropine) to assess the role of bronchoconstriction. Marked improvement in clinical signs strongly suggests reversible obstructive pulmonary disease such as heaves and summer pasture-associated obstructive pulmonary disease. Marginal or no improvement may be associated with restrictive pulmonary diseases (e.g., acute respiratory distress syndrome of neonatal foals, pulmonary edema, interstitial pneumonia, pulmonary fibrosis, silicosis, mediastinal mass), or non-respiratory diseases (e.g., cardiac failure). Thoracic radiography and cardiac ultrasonography are indicated to characterize the disease process and evaluate the severity of the lesion (Fig. 4).
Figure 4. Thoracic radiograph of a foal with acute respiratory distress. Notice the typical diffuse, ground-glass opacity of the lungs with presence of air bronchograms.
Horses in respiratory distress with no abnormal respiratory sounds should be further evaluated. Horses with synchronous diaphragmatic flutter present with pronounced abdominal contractions or flank twitching that might be mistaken for increased respiratory effort. However, in this case spasmodic contractions of the flank are synchronous with the first heart sound and are independent of the normal respiratory cycle . A markedly elevated rectal temperature may be associated with conditions causing hyperthermia (e.g., exercise, hot environment) or fever and contribute to respiratory distress. Collection of blood for packed cell volume measurement and hematology is valuable to detect anemia and diseases resulting in decreased oxygen carrying capacity of the blood (methemoglobinemia, carboxyhemoglobinemia). Only severe anemia resulting in packed cell volume < 8-10% may cause respiratory distress. Anemia does not cause hypoxemia but a decrease in the delivery of oxygen to tissues (i.e., tissue hypoxia). Therefore, anemic horses have a normal PaO2 and the increase in ventilation results from acidification of cerebrospinal fluid caused by enhanced anaerobic metabolism. An arterial blood gas sample is indicated in horses with normal hematologic findings. Hypercapnia may be associated with conditions impairing respiratory muscle function (e.g., botulism, nutritional muscular dystrophy, diaphragmatic paralysis) or chest wall movement (e.g., abdominal distension, chest trauma). Hypocapnia indicates hyperventilation and may be in response to painful conditions (e.g., colic) or to anxiety.
Cough is a defense mechanism of the respiratory tract with two major functions. One is to prevent or limit inhalation of foreign materials into the tracheobronchial tree and the other function is clearance of the airways. Cough is a reflex elicited by stimulation of receptors located in central airways from larynx to bronchi.
Description of Cough
Most of the discussion that follows is based on studies of cough in humans and animals other than the horse, however, clinical observations suggest that similar mechanisms occur in the horse. Four consecutive phases characterize a typical cough: inspiration, compression, expiration, and cessation . Coughing is usually preceded by inspiration of a variable volume followed by glottis closure, and forceful expiratory efforts which raises thoracoabdominal pressures more than 100 cmH2O above ambient pressure. The glottis is then suddenly opened allowing expiratory flow to peak rapidly as central intrathoracic airways collapse. After exhalation of a variable volume expiratory muscle efforts decrease quickly until expiratory flow drops to zero.
The inspired volume prior to a cough is quite variable. Inhalation of foreign material through the larynx may trigger an immediate cough without prior inspiration in order to prevent further entry into the tracheobronchial tree. In humans, clearance of respiratory secretions may be achieved by successive coughs initiated at progressively higher lung volumes. Alternatively, several consecutive coughs may occur without any inhalation in between. Clearance of secretions may be achieved by forced expirations without glottis closure. However, thoracic gas compression against a closed glottis allows generation of higher expiratory flow and airway pressure than during forced expiration and is thought to augment cough effectiveness 
When a forceful expiration is initiated, increasing expiratory effort increases flow up to a maximal value that is dependent on lung volume and not on effort. Expiratory flow limitation may be reached with relatively modest effort and is easily attained during coughing. The higher the lung volume, the higher the maximal expiratory flow. Consequently, coughing initiated from a high lung volume is more likely to be effective. Transient supramaximal flows are achieved during cough immediately after glottis opening . During a few milliseconds, expiratory flows as much as twice the maximal flow expected at a particular lung volume may be reached. Such high flows result from sudden collapse of intrathoracic airways. This rapid inward acceleration of the wall contributes to mucus clearance in the same way shaking a rug in the wind helps eliminate dust. Following these transient supramaximal flows, expiratory flow is limited in the same way it is limited during a forced expiration. High gas linear velocities generated by high flow cause shearing forces at the level of the airway walls and result in the suspension and clearing of secretions adherent to the airways. Higher flow velocities are achieved in large airways such as trachea and major bronchi. Therefore, coughing is likely to help clear materials from central airways but not from peripheral or small airways. Because the extrathoracic trachea does not collapse during coughing it is probably not cleared effectively during coughing. In animals with long extrathoracic trachea like the horse, maintaining the head in a low position, for example during grazing, appears to be an important clearance mechanism for secretions. Horses confined with head elevated for 6 to 12 hours experience bacterial colonization of the tracheobronchial tree despite development of a cough, and resolution occurs within 12 hours if horses are allowed to lower their heads .
Although the cough mechanism has been well described, the contribution of coughing to mucus transport towards the pharynx is poorly understood. Elimination of normal respiratory secretions appears to depend mainly upon mucociliary clearance mechanisms and not cough 
Maximal expiratory flows are decreased in horses with obstructive airway diseases such as recurrent airway obstruction or heaves . Consequently, coughing is expected to be less effective in horses with heaves and administration of bronchodilators may potentially enhance clearance of secretions.
Pathophysiology of Cough
Stimulation of irritant receptors located in the nasal passages produces sneezing. Cough is produced by stimulation of receptors located in the larynx and airways distal to it. Cough reflex is initiated by activation of nerve endings called irritant receptors that send impulses through myelinated vagal fibers to the cough center in the medulla of the brain and in return cause coughing, bronchoconstriction, and mucus secretion . Although bronchoconstriction accompanies cough, they can be produced individually and separated pharmacologically, indicating that they are different reflexes . Irritant receptors are rapidly adapting receptors and are located between airway epithelial cells from the larynx to the respiratory bronchioles. They are particularly abundant in the trachea, carina, and large bronchi as can be deducted by the cough response that may be induced by touching these regions during bronchoscopic examination.
Irritant receptors are stimulated by both mechanical and chemical stimuli. Mechanical stimulation of the respiratory epithelium may result from accumulation of secretions, inhalation of particulate matter, or bronchoconstriction. In the horse, irritant receptors seem to be less sensitive to mechanical stimuli than in other species because the presence of large amounts of mucopurulent exudate in central airways as seen in horses with heaves or recurrent airway obstruction is not necessarily accompanied by a cough. Chemical stimulation with various endogenous (histamine, prostaglandins) and exogenous substances (dusts, noxious gases) can also stimulate irritant receptors and trigger a cough.
Another type of receptor called C fibers receptors ("J receptors") are located in the alveolar walls in close association with the pulmonary capillaries and may cause coughing indirectly by releasing neurotransmitters such as tachykinins that, in turn, stimulate irritant receptors in the airways . C fiber receptors may play a role in the mechanism causing increased cough sensitivity in inflamed airways.
Coughing may result from a combination of pathways, which are important to understand in order to design an appropriate treatment plan. In respiratory diseases characterized by significant bronchoconstriction such as recurrent airway obstruction, the administration of bronchodilators is expected to help reduce coughing. Equine viral respiratory infections, in particular with influenza virus, are characterized by acute cough, nasal discharge, fever, inappetence, and lethargy. Clinical disease lasts on average 11 days, but can range from 1 to 46 days . In addition, mucociliary clearance may remain disrupted for up to 32 days after infection despite resolution of the cough and other clinical signs . Both airway inflammation and decreased mucus clearance contribute to coughing. The loss of epithelial integrity, seen after respiratory infections, may also lead to increased sensitivity of irritant receptors and result in increased bronchial responsiveness and coughing . This is highlighted by epidemiological studies that have shown an association between cough and inflammatory airway disease in racehorses [60,61]
Bronchial hyperresponsiveness is an increase in the ease with which airways narrow when exposed to provocative stimuli. This phenomenon is a common feature of infectious and non-infectious inflammatory diseases of the lower respiratory tract in horses [62-64]. Increased bronchoconstriction may contribute to cough pathogenesis via stimulation of irritant receptors.
Cardiac diseases leading to left-sided heart failure are rare in the horse, however, when they occur clinical signs of respiratory disease are common, in particular cough . In these cases, cough results from mechanical stimulation of receptors by pulmonary edema. Other clinical signs associated with left-sided congestive heart failure are increase respiratory rate, abnormal pulmonary auscultation (crackles or coarse breath sounds), and loud systolic murmur.
Coughing is an important defense mechanism of the tracheobronchial tree, however, in some instances it does not have a useful purpose (i.e., non productive) and sometimes it may be deleterious to the horse. Chronic cough can contribute to fatigue and decrease food intake. In humans, cough can result in syncope, cardiac arrhythmia, torn muscles, fractured rib and vertebrae, and lung disruption.
Clinical Examination of the Coughing Horse
The collection of historical and clinical findings will help the clinician determine the origin of a cough and generate a list of possible differential diagnoses.
Many respiratory diseases affect horses at a particular age. A neonatal foal coughing and displaying nasal regurgitation of milk while nursing bring to mind a possible congenital physical abnormality such as cleft palate, dorsal displacement of the soft palate, and subepiglottic cyst or, a functional abnormality such as hypoxic ischemic encephalopathy, hydrocephalus and pharyngeal-cricopharyngeal incoordination . Arabian foals that develop repeated pneumonia between birth and 2 month of age should raise the possibility of combined immunodeficiency. Foals between 1-3 month of age presenting signs of pneumonia unresponsive to beta-lactam and aminoglycosides antimicrobials strongly suggest Rhodococcus equi infection. An acute onset of cough, fever, and serous nasal discharge in young horses suggest a potential viral etiology (e.g., influenza, herpesvirus, viral arteritis).
Vaccination history of the horse and other horses on the premisses, or of the mare in case of a foal, are important information in cases of contagious diseases. The type of anthelmintic used and frequency of administration may suggest the possibility of lungworm infection. Horses sharing pasture with donkeys are at risk of acquiring lungworm infection.
The geographic location and history of travel may help determine the likelihood of certain diseases. For example, Rhodococcus equi can multiply in the intestine of foals and in soil under certain environmental conditions such as high temperature. In addition, the main route of infection is via dust inhalation . As a result, R. equi infection is endemic on some farms with high concentration on horses and hot climate. Previous medical history will help establish possible chronicity or recurrence of the condition. Weight loss would indicate chronicity of the disease. Seasonality of the clinical signs suggests an allergic condition. Horses suffering from summer pasture-associated obstructive pulmonary disease tend to develop clinical signs while at pasture between June and September . Similarly, horses with recurrent airway obstruction exhibit clinical signs during the cold season when they are housed indoors and fed hay.
Horses subjected to stressful situations such as long travel, strenuous exercise, or general anesthesia are more likely to be immunosuppressed and are at risk of developing diseases such as pneumonia and pleuropneumonia. A history of recent contact with other horses at a sale barn, show, racetrack, breeding farm, or the introduction of a new horse should raise the suspicion of contagious diseases such as strangles and viral respiratory diseases.
Assessing the housing conditions of the horse and type of feed is important. Horses housed in poorly ventilated stalls, fed badly cured hay, and bedded on straw are exposed to high levels of organic molds and endotoxin, which may result in lower airway inflammation and bronchial hyperresponsiveness. This type of environment is likely to induce or exacerbate signs of respiratory disease in horses with recurrent airway obstruction or infectious respiratory disease. Horses with recurrent airway obstruction kept outdoors but fed hay from round bales left in the field tend to exhibit worsening of the clinical signs.
Assessment of the timing of the cough may guide diagnostic tests. Cough associated with feeding may indicate allergy to inhaled molds (e.g., heaves), inflammatory diseases of the pharynx and larynx, esophageal obstruction, or dysphagia with passage of ingesta in the airways. Exercise often exacerbates coughing because of the higher mechanical stress placed on pulmonary cough receptors and the larger amount of particles inhaled with the increase in ventilation. Coughing following strenuous exercise is more suggestive of exercise-induced pulmonary hemorrhage.
It is important to try to make the horse cough because the cough's characteristics may help determine the anatomical location of the disease. One way is by squeezing the dorsal aspect of the tracheal rings just behind the larynx in between your thumb and index (Video 7a and Video 7b). A normal horse will cough once at most. Coughing will be triggered easily and result in multiple coughs in horses with upper airway inflammation. Making the horse breathe into a large plastic bag (10-15 liters) placed over the muzzle will increase depth of breathing (tidal volume) and respiratory rate (Video 3). Normal horses tolerate this procedure very well and do not cough. Horses with respiratory tract disease (e.g., heaves, pneumonia) will cough repeatedly as respiratory rate and depth of breathing increase.
Figure 5. Cough may be triggered by squeezing the trachea.
Video 7a - 1.47 Mo - How to perform tracheal compression and the normal response.
Video 7b - 0.7 Mo - Horse with tracheal inflammation where tracheal compression elicited a bout of coughing.
Dry, short, loud and harsh coughs with frequent bouts of coughing are common with upper respiratory tract inflammation, in particular secondary to viral infections. Deep, soft coughs usually result from lower respiratory tract diseases such as pneumonia and heaves. Painful conditions involving the upper (e.g., retropharyngeal abscess) or lower (e.g., pleuropneumonia) respiratory tract can both decrease the intensity of respiratory efforts and sounds produced during coughing.
It is important to note the aspect of the nasal discharge in coughing horses. Serous nasal discharge is commonly seen in cases of early viral respiratory infections and rhinitis. Bacterial infections often complicate viral infections and lead to mucopurulent discharges. However, horses with non-infectious respiratory diseases such as heaves and inflammatory airway disease often exhibit mucopurulent nasal discharge. Purulent discharges are common with strangles, guttural pouch empyema, and lower respiratory infections (e.g., pneumonia, lung abscess). Presence of feed material in the nasal discharge suggests dysphagia, which may be seen in conditions such as esophageal obstruction, pharyngeal neuromuscular disease (e.g., botulism, guttural pouch mycosis), and pharyngeal masses impairing deglutition (e.g., retropharyngeal abscess secondary to strangles).
Submandibular and retropharyngeal lymph nodes enlargement is common with viral or bacterial respiratory infections (Fig. 6). Abscess formation and drainage of lymph nodes may result from strangles or other bacterial infections. In rare cases, lymph node enlargement is secondary to neoplastic infiltration (e.g., lymphosarcoma).
Figure 6. Retropharyngeal lymph node enlargement secondary to Streptococcus equi infection (strangles).
Chest auscultation during rebreathing maneuver will make breath sounds more audible and increase the likelihood of detecting abnormal sounds (i.e., wheezes, crackles, friction rubs). This technique is contraindicated in horses that are already breathing with increased respiratory efforts. Auscultation of wheezes indicates airway narrowing. Crackles are thought to be associated with reopening of collapse airways or alveoli . Decreased intensity of breath sounds is associated with thick chest wall, pleural effusion, pulmonary consolidation, atelectasis, decreased ventilation, emphysema, diaphragmatic hernia, and pneumothorax. Sound transmission is more effective through consolidated or atelectatic lung than aerated lung. As a result, breath sounds over a consolidated or atelectatic lung region may be increased or decreased depending on intensity of sound and degree of attenuation  Increased intensity of breath sounds may be due to thin chest wall (e.g., foal), increased ventilation, lung mass, and pulmonary consolidation. Normally, breath sounds are fairly evenly audible over areas of auscultation. Breath sounds that are grossly different when comparing left to right side of the thorax or various areas on the same hemithorax suggest pulmonary, pleural, or chest wall abnormalities. Symmetric enlargement of the area of pulmonary auscultation indicates hyperinflation of the lungs (Fig. 2) and when it is accompanied by abnormal breath sounds widespread over the chest it is strongly suggestive of diffuse peripheral airway obstruction (e.g., heaves).
Percussion of the chest in adult horses should be interpreted with caution because thickness of the chest wall has a major influence on the findings. However, pain elicited upon percussion is often associated with pleuritis and ventral dullness suggests pleural effusion. Increased resonance upon percussion of the chest associated with decreased breath sounds is consistent with pneumothorax.
Diagnostic Approach to the Coughing Horse
An approach based on the rate of onset of the signs combined with physical examination findings should guide the clinician towards a diagnosis. This dichotomous approach is a simplification that applies to "classic" disease manifestation. Therefore the clinician must recognize that unusual presentations do occur and one should not discard differential diagnosis too soon.
Acute Onset of Cough
Horses with fever and cough should be carefully auscultated (Fig. 7). Abnormal breath sounds suggest lower airway disease and is an indication for TW. Infectious and neoplastic pulmonary diseases usually result in localized (e.g., lung abscess, tumor) or multifocal lung disease (e.g., pneumonia). Respiratory secretions originating from all regions of the lungs collect in the trachea before being expectorated. In these cases, cytologic examination and culture of TW fluid is likely yield an etiologic diagnosis. Because fluid collected by BAL is only representative of a discrete lung region, if the disease is not diffuse (i.e., uniformly distributed), it may be missed .
Figure 7. Diagnostic approach for horses with acute cough. BAL: bronchoalveolar lavage; EIPH: exercise induced pulmonary hemorrhage; SPAOPD: summer pasture-associated obstructive pulmonary disease; TW: tracheal wash; UAW: upper airway; U/S: ultrasonography; XRay: radiography.
Cytology specimen demonstrating predominance of neutrophils with various degrees of degenerative changes (karyolysis and cytoplasmic vacuolation) and presence of intracellular or extracellular bacteria is consistent with an infection and should prompt microbiologic culture of the fluid. However, the absence of bacteria or degenerative neutrophils does not rule out the possibility of an infectious disease. Improper handling of TW fluid may lead to degenerative changes of neutrophils in cases of non-infectious purulent inflammation  Aerobic and anaerobic cultures are recommended in febrile horses. A Gram stain may help guide antibiotic therapy while waiting for culture results. Culture of TW fluid from infectious cases resulting in no growth may be due to an insufficient number of bacteria, prior antimicrobial therapy, inappropriate culture medium (e.g., mycoplasma and fungal infections), or viral infection without secondary bacterial infection. Absence of significant bacterial growth is common in cases of interstitial pneumonia except in foals [71,72]. Clinical signs in horses with interstitial pneumonia are characterized by fever, cough, nasal discharge, and respiratory distress, which are often unresponsive to antimicrobials and supportive care. Main causes identified are infectious agents (bacteria, fungi, parasites, protozoa, and viruses) and toxins (inhaled and ingested) . Thoracic radiographs and lung biopsy usually provide the definitive diagnosis. Horses with acute onset of tachypnea, abnormal breath sounds, fever, and serosanguinous nasal discharge may suffer from acute pulmonary infarction .
Decreased or increased intensity of breath sounds in the ventral chest should prompt ultrasonographic examination to determine the presence of pleural fluid, pulmonary consolidation or atelectasis. Thoracocentesis is indicated when there is evidence of pleural effusion or a thoracic mass. Pleural effusion may result from a variety of causes including pleuritis, pneumonia, pulmonary abscess, hypoalbuminemia, chronic liver disease, thoracic neoplasia, trauma, esophageal rupture, diaphragmatic rupture, parasitism, chronic heart failure, hemothorax, chylothorax, lymphatic obstruction, and idiopathic causes [73,74]. Cytology and culture of the fluid collected are essential in reaching a diagnosis. For example, evidence of septic fluid containing a mixed population of bacteria and feed particles is consistent with a ruptured esophagus (Fig. 5). Thoracic radiographs are often useful to detect interstitial disease, pulmonary abscesses, thoracic neoplasms, and to determine the extent of pulmonary disease. Pleural effusion may prevent radiographic visualization of pulmonary or other thoracic abnormalities. Therefore, it is important to repeat thoracic radiographs after drainage of pleural fluid (Fig. 8 - Fig. 9).
Figure 8. Thoracic radiograph of a horse with pleural effusion secondary to pleuropneumonia.
Figure 9. Same horse as in Figure 8 after drainage of pleural fluid.
Normal breath sounds do not rule out pulmonary disease and, in the case of a horse with fever and cough, further diagnostic tests should be pursued such as endoscopy of the upper respiratory tract. Presence of serous discharge may be normal or indicative of viral respiratory infection. Horses with viral infection such as influenza have inflamed airways that often result in red appearance of the mucosa and paroxysm of coughing during endoscopic examination. Most horses with viral respiratory disease have normal or diffusely increased breath sounds . Auscultation of wheezes or crackles usually suggests severe viral infection or secondary bacterial pneumonia. Although presumptive diagnosis of viral infection can be made based on historical and physical examination findings, definitive diagnosis requires detection of the virus in respiratory secretions (nasal swab, TW fluid) or demonstration of a significant rise in serum antibody titer in samples collected 2 to 3 weeks apart . Cytology and culture from TW fluid will help detect bacterial infections such as low-grade pneumonia and bronchitis that often do not have detectable abnormalities on chest auscultation. A presumptive diagnosis of strangles based on acute onset of fever, lymph node enlargement, and purulent nasal discharge may be confirmed by culture of nasal swab and isolation of Streptococcus equi (Fig. 5).
Decreased breath sounds in the dorsal thorax accompanied by respiratory distress, fever, and cough are suggestive of pneumothorax. Thoracic percussion, radiography, and ultrasonography are particularly helpful to confirm the diagnosis. Reported cases are frequently secondary to pleuropneumonia and thoracic trauma (Fig. 10) [77,78]. Horses with pneumothorax secondary to closed trauma to the chest are often non-febrile and coughing is uncommon in horses with pneumothorax resulting from open chest wounds.
Figure 10. Pus draining from perforating chest trauma that caused septic pleuritis.
Non-febrile horses with acute cough should be carefully examined for respiratory and cardiovascular abnormalities. Abnormal breath sounds and cough associated with clinical signs of heart disease strongly suggest left-sided heart failure with secondary pulmonary edema . Severe mitral insufficiency (bacterial endocarditis, ruptured chordae tendineae) and large ventricular septal defects are often associated with left heart failure . Left-sided heart failure may go unnoticed for sometimes until the more easily recognizable signs of right-sided heart failure develop such as jugular distension and pulsation, peripheral vein distension, and ventral edema . Fever may be present when cardiac disease result from infectious disease (e.g., bacterial endocarditis). Horses with pulmonary edema secondary to smoke inhalation, anuric renal failure, or acute upper airway obstruction often display sudden onset of cough, dyspnea, crackles and wheezes with a normal cytologic examination of TW and BAL fluids [46,81,82]. In such cases, historical and clinical examination findings will easily guide to the final diagnosis. An increase in the percentage of neutrophils in TW and BAL fluids with no signs of sepsis in a horse with abnormal lung sounds and acutely increased respiratory efforts is consistent with heaves (recurrent airway obstruction) or SPAOPD. Susceptible horses are often asymptomatic as long as they are not exposed to the offending allergen. Heaves and SPAOPD are chronic diseases. However, clinical signs including cough and breathing difficulties may develop within 1.5 - 5 hours of exposure to the allergen . Mild airway obstruction is difficult to detect clinically because breathing sounds and respiratory efforts are often normal . Generally, affected horses have mucopurulent secretions in their airways characterized by the predominance of neutrophils.
Endoscopic examination is indicated in horses with acute onset of cough or nasal discharge and no other signs of respiratory disease. Presence of blood in the trachea shortly after a bout of strenuous exercise is consistent with exercise-induced pulmonary hemorrhage (Fig. 11) . Diagnosis may also be confirmed by visualization of phagocytized red blood cells and hemosiderin containing alveolar macrophages in TW or BAL fluid samples. Cough associated with feeding may be triggered by direct irritation of the pharynx and larynx, or secondary to aspiration of feed or saliva into the trachea. Causes of pain include trauma from nasogastric intubation, inflammatory diseases of the pharynx and larynx, and ingestion of foreign bodies (e.g., twigs). A common complication of upper airway surgery (e.g., prosthetic laryngoplasty, staphylectomy) is coughing that may occur immediately postoperatively . Coughing associated with dysphagia may result from obstruction, pain, or neurologic causes . Causes of acute obstruction are esophageal obstruction (choke, Fig. 12), strangles, pharyngitis, and laryngeal disease (arytenoid chondritis, Fig. 13; epiglottiditis) most of which are also painful conditions. Various causes of neurogenic dysphagia may result in acute coughing (e.g., botulism, lead toxicity, guttural pouch empyema or mycosis, encephalitides) . A careful evaluation of the lower respiratory tract for signs of aspiration pneumonia is mandatory in dysphagic horses. Tracheal collapse has been reported as a cause of sudden onset of cough and stridor in aged ponies 
Figure 11. Blood visualized by endoscopy of the trachea in a horse with exercise-induced pulmonary hemorrhage.
Figure 12. Endoscopic view of an esophageal obstruction.
Figure 13. Endoscopic view of arytenoid chondritis.
Hematology findings may be helpful, however, they are often non-specific. Leukocytosis with neutrophilia is commonly found with bacterial respiratory infections. However, it may be difficult to differentiate from physiologic leukocytosis in response to stress. During the acute phase of a bacterial infection, increased numbers of immature neutrophils ("left shift") may be observed. Persistent neutropenia associated with increased immature neutrophils is consistent with an overwhelming inflammation. Horses with chronic bacterial respiratory infections will tend to show a mature neutrophilia and foals tend to have marked neutrophilia especially with Rhodococcus equi pneumonia. Neutrophilia may also accompany non-infectious inflammatory diseases (e.g., toxins), neoplasia, mycotic, and parasitic infections. Toxemia, in particular from gram negative bacterial infections may affect neutrophil maturation in the bone marrow and result in morphologic changes called "toxic" neutrophil. Hematologic changes during the early phase of a viral respiratory infection (e.g., influenza) are often characterized by normocytic, normochromic anemia, lymphopenia or lymphocytosis, and sometimes neutropenia [75,89] Neutrophilia may follow within a week of initial clinical signs, particularly in cases of secondary bacterial infection. Monocytosis may develop during the recovery phase of a viral infection.
Coughing is usually considered chronic if it is persistent for more than 3 weeks . Diseases resulting in acute cough may lead to chronic coughing if the initiating cause is persistent. Alternatively, several slowly progressive diseases and congenital abnormalities are associated with chronic coughing (Fig. 14a & Fig. 14b). Presence of abnormal breath sounds in a chronically coughing horse is consistent with pulmonary disease (Fig. 14a). Crackles or wheezes that can be heard symmetrically over both sides of the chest suggest diffuse pulmonary disease. In these cases, cytologic examination of TW or BAL fluid is often useful to reach a final diagnosis. However, BAL fluid is preferred in case of diffuse pulmonary disease because contrary to TW, BAL fluid cytology is more representative of lung histopathology [91,92]. A marked neutrophilia is commonly observed in BAL fluid from horses with heaves, SPAOPD, and IAD [93-95]. Horses with heaves and SPAOPD typically display exercise intolerance and increased respiratory efforts characterized by nostrils flaring and exaggerated abdominal lift during expiration (Video 8). Horses affected with IAD usually only display poor performance. Horses with mild form of heaves and SPAOPD may show similar clinical signs to horses with severe IAD . Eosinophilic inflammation is often associated with parasitic pneumonitis (Parascaris equorum, Dictyocaulus arnfieldi) [96,97]. However IAD, hypersensitivity pneumonitis, fungal pneumonia, and cutaneous habronemiasis may also reveal eosinophils [98,99]. Clinical signs of parasitic pneumonitis are non-specific. Fecal flotation (Baermann technique) is often not diagnostic of P. equorum infection because migration through the lungs occurs during the prepatent period . D. arnfieldi follows a complete cycle in donkeys, mules, and asses, however, the infection is usually not patent in horses. Therefore, the Baermann fecal flotation is not useful either. P. equorum pneumonitis are more commonly detected in foals less than 6 month of age. D. arnfieldi usually occurs in horses in contact with infected donkeys and rarely by ingesting larvae excreted by infected horses . A presumptive diagnosis may be reached when respiratory secretions reveal eosinophilic inflammation with sometimes evidence of parasite eggs or larvae, exposure to donkeys exists, and anthelmintic therapy results in clinical improvement . Increased metachromatic cells (mast cells, basophils) have been described in horses with IAD with chronic cough and exercise intolerance [98,102].
Video 8 - 3.62 Mo - Increased respiratory efforts characterized by nostrils flaring and exaggerated abdominal lift during expiration in a horse with heaves.
Figure 14a. Diagnostic approach for horses with chronic cough and abnormal lung sounds. BAL: bronchoalveolar lavage; IAD: inflammatory airway disease; SPAOPD: summer pasture-associated obstructive pulmonary disease; TW: tracheal wash; U/S: ultrasonography; XRay: radiography.
Figure 14b. Diagnostic approach for horses with chronic cough and no abnormal lung sounds. BAL: bronchoalveolar lavage; TW: tracheal wash; XRay: radiography.
When abnormal breath sounds suggest focal or multifocal disease, radiography and ultrasonography may help characterize the disease process. Detection of pleural effusion should be followed by thoracocentesis for cytologic examination and microbiologic culture. Chronic pleural disease may be caused by infectious or neoplastic diseases. Chronic pleural infection is often sequelae of pleuropneumonia or abscess rupturing in pleural space. Neoplastic disease may result in pleural effusion by impairing lymphatic drainage of the chest (e.g., mediastinal lymphosarcoma) or by causing inflammation. A TW is indicated when pulmonary disease is suspected. Cytologic and culture findings may help diagnosing pneumonia (bacterial, fungal), pulmonary abscess, and neoplasia. Chronic infections are often accompanied by intermittent fever, decreased appetite, and weight loss. Primary lung tumors (granular cell carcinoma, bronchial myxoma, pulmonary carcinoma) and pulmonary metastasis may cause chronic cough [103-105]. Diagnostic biopsy specimens may be obtained using biopsy forceps introduced through an endoscope or using a percutaneous biopsy needle (Fig. 15). The former technique is safe, however, sample size is small and only diseases infiltrating airway walls or protruding inside airways may be diagnosed. The later technique provides significantly more tissue including airways and lung parenchyma, however, life-threatening complications may occur (hemorrhage, pneumothorax). Alternatively, large lung biopsy specimens may be obtained relatively safely during thoracoscopy using specialized equipment .
Figure 15. Trans-endoscopic biopsy of a pulmonary tumor (granular cell carcinoma).
Horses with chronic cough and normal breath sounds suggest upper airway abnormalities or low-grade pulmonary disease (Fig. 15b). Endoscopy of the respiratory tract is often helpful to localize a disease process. Endoscopy of a normal respiratory tract may reveal mild amounts of serous secretions to a few islets of mucopus in the trachea. Presence of moderate to large amounts of seromucoid or mucopurulent secretions in the tracheobronchial tree (Fig. 16) or bronchial edema (Fig. 17) is consistent with pulmonary inflammation. Further diagnostic tests such as BAL and TW fluid cytology may help identify horses with low-grade inflammatory lung diseases such as IAD, heaves, SPAOPD, and parasitic pneumonitis. In unusual cases, abnormal cytologic findings require additional tests including radiography, lung function testing, or lung biopsy in order to confirm the diagnosis (e.g., silicate pneumoconiosis, pulmonary fibrosis, interstitial pneumonia) [107-109].
Figure 16. Large amounts of mucopurulent secretions in the trachea of a horse with heaves.
Figure 17. Bronchial edema in a horse with heaves.
Endoscopic examination is important for the diagnosis of functional or structural abnormalities of the upper respiratory tract. Coughing may be triggered by diseases causing pharyngeal and laryngeal irritation or by conditions resulting in dysphagia with aspiration of ingesta inside the tracheobronchial tree. Irritation of the pharynx and larynx tend to manifest as intermittent cough that is not necessarily associated with feeding. Alternatively, cough resulting from dysphagia is associated with feeding. Horses may tolerate large amounts of tracheal contamination by feed materials because of effective protective mechanisms such as coughing, mucociliary clearance, and immune response. Consequently, horses that are persistently dysphagic may remain clinically normal except for a chronic cough. Aspiration pneumonia develops when defense mechanisms are overwhelmed by large contamination or impaired by factors such as transportation, exercise, general anesthesia, and concurrent diseases . Causes of chronic coughing associated with feeding are dorsal displacement of the soft palate, rostral displacement of the palatopharyngeal arch (Fig. 18), cleft palate (Fig. 19), laryngeal hemiplegia, pharyngeal and laryngeal masses (tumor, abscess, granuloma, cyst; Fig. 20) and causes of neurogenic dysphagia (e.g., guttural pouch empyema and mycosis, stylohyoid bone fracture, otitis media-interna; Fig. 21) [87,111]. Common causes of dysphagia and chronic cough in foals are congenital abnormalities such as cleft palate and dorsal displacement of the soft palate. Causes of upper airway trauma, infection, and inflammation are commonly associated with chronic intermittent coughing including pharyngeal abscess, severe pharyngitis, arytenoid chondritis, suture from laryngeal prosthesis, and epiglottic entrapment (Fig. 22).
Figure 18. Rostral displacement of the palatopharyngeal arch.
Figure 19. Cleft palate.
Figure 20. Pharyngeal abscess resulting in dorsoventral nasopharyngeal collapse.
Figure 21. Enlarged stylohyoid bone (fracture) visualized by endoscopy of the guttural pouch.
Figure 22. Epiglottic entrapment.
Nasal discharge can originate from lesions involving any part of the respiratory tract from nasal passages to alveoli. In addition, diseases involving structures adjacent or communicating with the respiratory tract can result in nasal discharge. Nasal discharge is commonly associated with cough, abnormal respiratory sounds, or respiratory distress and these clinical signs have been discussed in detail in this chapter.
The respiratory tract is constantly exposed to a variety of microbes, particles, and potentially toxic gases present in the air. Protection of the tract is based on mechanical and immunologic defense mechanisms. The design of conducting airways, in particular the nose, allows trapping of larger particles (> 10 µm) onto the mucosa. Deposited particles are trapped on the surface of the mucus layer that is being constantly produced by goblet (mucous) cells, serous cells, submucosal glands, and transepithelial fluid exchange along conducting airways . Toxic gases may also be trapped in the mucus layer. The mucociliary apparatus creates a constant flow of mucus toward the pharynx where it is eventually swallowed. As a result, horses do not normally show evidence of a nasal discharge. The nasal passages also play the important role of conditioning the inspired air by adding moisture and adjusting temperature toward that of the body . Mucus secretion is influenced by environmental factors and a very rich submucosal vascular network under the control of the autonomic nervous system. For example, when breathing dry cold air the nose adds significantly more water to the air, which results in more condensation and dripping of clear secretions from the nose. Inhalation of allergens or irritants may result in inflammation of the respiratory tract and increased mucus secretion. In the horse, intranasal administration of sympathomimetic drugs (e.g., phenylephrine) reduces mucosal congestion and may improve clinical signs associated with rhinitis [113,114].
Detailed information concerning the history of the nasal discharge and patient's medical history in general are essential. Questioning should be of determined duration and onset of clinical signs, nature of the discharge, draining side (unilateral or bilateral), associated clinical signs, and history concerning other animals on the premises. Acute nasal discharge is common with primary viral or bacterial infections, trauma, or acute dysphagia. Chronic discharge usually indicates chronic infection, neoplasia, or progressive neurologic disease . A discharge that is consistently unilateral indicates a lesion within the nasal passage or sinuses on the same side. Bilateral discharges result from lesions located caudal to the nasal cavities or involving nasal passages or sinuses on both sides . Exceptions to this general rule are not uncommon. For example, unilateral guttural pouch disease may produce a predominantly unilateral discharge on the same side.
Fever suggests a primary infectious disease or secondary complication such as aspiration pneumonia. Coughing indicates respiratory disease involving larynx, trachea, and lungs or conditions causing passages of ingesta in the tracheobronchial tree. A history of several horses on the same premises with fever, purulent nasal discharge and upper respiratory lymph nodes swelling and abscesses strongly suggest strangles (Streptococcus equi infection). Dysphagia with the presence of ingesta at the nose is a common complication of upper airway surgery.
Nature of the Discharge
Inflammation of the nasal passages results in increased glandular secretion. Secretions are initially serous, then mucoid, and may become purulent as a result of neutrophilic accumulation. It is not possible to predict the cause of a purulent discharge based on its color and aspect. Thick, white to yellow purulent discharges may be associated with infectious (e.g., strangles) and non-infectious diseases (e.g., heaves; Fig. 23). Some discharges have a yellow-green color caused by enzymes released during neutrophil breakdown . Various ocular conditions can result in increased lacrimal secretions and nasal discharge on the affected side via drainage from the nasolacrimal duct. Secretions from the tracheobronchial tree are usually swallowed when they reach the pharynx without draining into the nose. However, nasal discharge may develop from lower airway disease in cases of increased volume of secretions, coughing, or maintenance of the head and neck in a low position (e.g., grazing). Pulmonary edema may lead to clear serous nasal discharge and in some severe cases to bilateral foamy exudate (Fig. 24).
Figure 23. Purulent nasal discharge.
Figure 24. Foamy nasal discharge in a horse with severe pulmonary edema.
Bleeding from the nose (epistaxis) may range a few drops of blood-tinged secretions to profuse fatal hemorrhage (Fig. 25). Depending on the cause of bleeding, blood may be mixed with serous, mucoid, or purulent discharge. Nasal discharge containing a mixture of blood and purulent secretions are usually seen with infections, neoplasia, and necrotic lesions.
Figure 25. Unilateral epistaxis.
Malodorous nasal discharge usually indicates anaerobic infection and is often associated with tooth root abscess, tissue necrosis, or trauma [117-119].
Presence of ingesta in the nasal discharge points to impaired deglutition and may be secondary to a variety of physical or functional abnormalities . The discharge is usually mixed with saliva.
Collection of basic information should include mucous membrane color, capillary refill time, rectal temperature, heart rate, and respiratory rate. The primary focus should then be on the respiratory tract. Assessment of respiratory efforts and abnormal respiratory sounds may help localize the origin of the disease process. Examination of the nasal opening allows determination of the nature and volume of the discharge, whether it is unilateral or bilateral, or is malodorous. Unilateral nasal airflow obstruction may be detected in severe cases by comparison of respiratory efforts and sounds during manual occlusion of an individual nostril. Sinuses should be evaluated for symmetry and any deformation, and then percussed. Maintaining the horse's mouth opened during percussion of the sinuses will significantly enhance sound intensity and make subtle differences in resonance easier to detect. Dullness of the sound upon percussion of the sinus suggests presence of fluid or tissue density within the sinus. Pain upon percussion of the sinuses is often associated with sinus disease. However, sinus disease is commonly present without detectable abnormalities upon percussion. Lymph nodes of the head drain specific regions, so palpation of enlarged nodes may provide clues concerning location of the disease process. The rostral part of the nasal cavities is drained by submandibular lymph nodes . Retropharyngeal lymph nodes drain the caudal nasal cavities, pharynx (including guttural pouches), and larynx. Auscultation of trachea and lung for abnormal sounds should be conducted (see discussion on "Abnormal respiratory sounds). Intensity of respiratory sounds can be increased by making the horse breathe in a plastic bag or by obstructing both nostrils until ventilation increases. Horses with a history of dysphagia should be examined while eating and drinking to assess the nature of the dysfunction. Careful examination of the oral cavity should focus on evidence of dental disease, in particular maxillary cheek teeth with roots contained in the maxillary sinuses.
Serous or Mucoid Nasal Discharge
Increased glandular secretions may be triggered by inflammation of the nasal epithelium and result in serous to mucoid nasal discharge (Fig. 26). Unilateral discharge is uncommon and may be observed following nasal trauma (e.g., intubation, endoscopy). In rare cases, unilateral chronic mucoid nasal discharge may be associated with progressive ethmoid hematoma . Acute onset of serous to mucoid discharge is a common feature of viral respiratory diseases and usually associated with a history of cough and fever. An etiologic diagnosis may be determined using paired serum titers and virus isolation from nasopharyngeal swabs.
Figure 26. Serous nasal discharge.
High levels of environmental dusts or chemical irritants (e.g., ammonia, disinfectants, paint fumes) can cause serous nasal discharge . Careful evaluation of the feed, housing conditions, and management of the horse is recommended to evaluate the potential role of those factors. Some horses with chronic inflammatory airway disease such as heaves, IAD, and SPAOPD may exhibit intermittent serous to mucoid nasal discharge. Horses with low-grade obstructive pulmonary disease usually display limited clinical signs, however, endoscopic examination typically reveals significant amounts of mucopurulent discharge in the tracheobronchial tree. Diagnosis may be confirmed by cytologic examination of respiratory secretions. Athletic horses with IAD commonly have an increased amount of bilateral seromucoid discharge post-exercise.
Purulent Nasal Discharge
Purulent nasal discharge from structures located rostral to the choanae (e.g., nasal cavity, sinuses) result in unilateral nasal discharge. In some cases, drainage occurs primarily from one nostril, however, the source of the discharge is caudal to the choana (e.g., unilateral guttural pouch empyema, bacterial bronchopneumonia) [115,118]. Therefore, the initial goal is to determine if the discharge originates from the upper respiratory tract and communicating structures, or if it comes from the pulmonary tract (Fig. 27).
Figure 27. Diagnostic approach for a horse with purulent nasal discharge. BAL: bronchoalveolar lavage; SPAOPD: summer pasture-associated obstructive pulmonary disease; TW: tracheal wash; U/S: ultrasonography; XRay: radiography.
Auscultation of abnormal lung sounds suggests an infectious or inflammatory pulmonary disease. Infectious diseases are usually accompanied by fever and should be further investigated with collection of TW fluid to help establish an appropriate diagnosis and treatment. The type and extent of pulmonary disease may be further characterized by radiography and ultrasonography. Horses with pneumonia, pleuropneumonia, and pulmonary abscess usually exhibit additional signs of systemic disease such as lethargy, decreased feed intake, and cough. Some horses with chronic low-grade or localized infections, like an abscess, may be afebrile and display few systemic signs. In these cases, hematology findings may reveal mature neutrophilia and hypergammaglobulinemia. Auscultation of crackles and wheezes and purulent nasal discharge in a non-febrile horse suggests parasitic or inflammatory lung disease. Increased expiratory efforts and nostril flaring suggests obstructive lung disease such as heaves and SPAOPD. An elevation in the percentage of neutrophils in BAL or TW fluid would support the diagnosis. Respiratory secretions from horses with parasitic pneumonitis (lungworm) are usually characterized by eosinophilic inflammation .
Percussion of frontal and maxillary sinuses revealing areas of dullness or pain suggests sinus disease. Dental disease, in particular tooth root infection is a common cause of sinus infection and is usually associated with fetid-smelling breath. Horses usually have a history of chronic nasal discharge, however, mastication is often unimpaired .A complete oral examination should be performed focusing on the third to sixth upper cheek teeth that have roots located in the maxillary sinuses . Bacteria and feed particles may gain access to the sinuses because of missing or cracked tooth, patent infundibulum, unstable tooth, or periodontal disease (Fig. 28). Other causes of secondary sinus disease that commonly result in purulent nasal discharge are cysts, neoplasia, and fungal granulomas [123,125]. Facial swelling and draining tract may develop in chronic cases. Deformation of the maxillary sinus may result in obstruction of the nasolacrimal duct and epiphora. Radiographic examination of the skull is particularly useful for the diagnosis of sinus and dental diseases . Good-quality radiographs are needed because, unless the disease is chronic and severe (facial swelling, draining tract), it is often difficult to correctly identify the tooth or teeth involved . Fluid opacities are commonly identified with both primary and secondary sinusitis (Fig. 29). Sinus centesis or endoscopy may help reach a diagnosis. Endoscopy of the nasal cavity may reveal exudate draining from the nasomaxillary opening in the middle meatus or deformation of the nasal passages resulting from sinus enlargement.
Figure 28. Missing maxillary cheek tooth replaced by feed impacted in gum line.
Figure 29. Three fluid lines are visible in the maxillary sinuses.
Enlargement of submandibular and retropharyngeal lymph nodes in a horse with purulent nasal discharge indicate upper respiratory tract disease (Fig. 6). The most common causes of lymphadenopathy and purulent nasal discharge are bacterial infections (Streptococcus equi and S. zooepidemicus). Definitive localization of the disease process is often achieved by endoscopic examination. It is important to examine both nasal cavities, compare them for symmetry, and look in the middle nasal meatus for drainage from the paranasal sinuses. Nasal disease is an uncommon cause of nasal discharge. Infection (bacterial, fungal), neoplasia, polyp, granuloma, and foreign body have been described and usually result in purulent nasal discharge from the affected side (Fig. 30) [118,128]. Radiography, biopsy and cytologic examination may be necessary to achieve a final diagnosis, establish the extent of the lesion, and plan treatment. For example, mycotic infection of the nasal cavity may present as nodules or ulcerated areas that may require a combination of surgical debridement and local antifungal therapy . Repeated trauma from nasal intubation commonly leads to mucopurulent discharge. Endoscopic examination of the nasal cavities should be followed by evaluation of the pharynx and larynx. Inflammation, infection, trauma, neoplasia, and granuloma of the pharynx and larynx can result in purulent nasal discharge. Depending on the severity and extent of the lesion, horses may present signs of dysphagia or cough while eating. It is particularly important to evaluate pharyngeal and laryngeal function in cases of neurogenic or obstructive dysphagia because they commonly result in secondary aspiration pneumonia and purulent nasal discharge. Radiography is also indicated to further explore soft tissue involvement, bony changes, or presence of foreign body. Detection of mucopurulent discharge on the ventral aspect of the nasopharynx without evidence of pharyngeal or laryngeal disease suggests either guttural pouch disease (empyema, mycosis) or inflammatory pulmonary disease. Introduction of the endoscope in the guttural pouch is facilitated by passage of a flexible instrument through the biopsy channel of the endoscope and into the pharyngeal opening to serve as a guide wire. Both guttural pouches should be explored for the presence of pus, chondroid, mass, and mycotic plaque (Fig. 31). A sterile sample may be collected for microbiological culture by introducing a sterile catheter through the biopsy channel of the endoscope. Evidence of mucopurulent secretion in the trachea indicates lower airway inflammation (Fig. 32). Evaluation of BAL or TW fluid should establish the nature of the inflammation (i.e., infectious vs. non-infectious).
Figure 30. Fungal infection involving nasal cavity and nasopharynx.
Figure 31. Guttural pouch empyema. Note the presence of a round chondroid on the floor of the medial compartment.
Figure 32. Mucopurulent discharge in the trachea of a horse with pneumonia.
Bleeding from the nose is usually intermittent which makes finding the source challenging. In some cases, epistaxis can result in fatal hemorrhage (e.g., guttural pouch mycosis). Therefore, prompt examination during active epistaxis should be performed without delay. Evidence of bleeding diathesis such as petechiae and prolonged bleeding time suggests coagulopathy or vasculitis. Laboratory tests including coagulation times and platelet count should be performed. Severe systemic diseases (e.g., enterocolitis) can result in disseminated intravascular coagulopathy. Spontaneous epistaxis is rare unless platelet count decreases below 10,000/ul (Fig. 33) . Causes of immune-mediated vasculitis such as purpura hemorrhagica may result in epistaxis.
Figure 33. Epistaxis in a horse with severe thrombocytopenia.
If there is no evidence of bleeding diathesis, endoscopic examination is often the most definitive means of diagnosing the cause of epistaxis. Epistaxis associated with exercise is usually secondary to EIPH. Although the majority of horses exercising strenuously has evidence of pulmonary hemorrhage, less than 10% exhibit epistaxis [130-132]. Severity of epistaxis can range from scant amount of blood tinged nasal secretions to massive fatal hemorrhage. Previous bleeding episodes may be detected by presence of hemosiderin-containing macrophages in TW or BAL fluid. Pneumonia and lung abscess may also result in EIPH .
Epistaxis may result secondary to vascular damage from trauma, infection, or mass. Skull fracture can result in epistaxis. Horses often have a history of trauma. Radiographic evaluation of the skull is indicated for evidence of facial and basisphenoid bones (Fig. 34). Bleeding originating from the nasal passages may be secondary to nasal or paranasal sinus disease. Horses bleeding from the nose secondary to an infection or mass (neoplasia, cyst) often have a history of chronic, intermittent mucopurulent nasal discharge. Ethmoid hematoma should be considered when a mass is detected protruding inside the nasal cavity from the caudal aspect (Fig. 35) . Ethmoid hematoma is usually irregularly lobulated, variable in color (red to green-yellow), and associated with epistaxis. Some horses may have bilateral lesions but present only with unilateral hemorrhage. Hemorrhage from guttural pouch mycosis is generally unilateral and may present as mild to severe epistaxis occurring intermittently over days to weeks. Dysphagia secondary to cranial nerve damage is also common and usually results in cough during eating and presence of food particles in nasal discharge .
Figure 34. Basisphenoid bone fracture.
Figure 35. Ethmoid hematoma.
Nasal Discharge Containing Ingesta
Causes may be separated into obstructive diseases (e.g., esophageal obstruction), pharyngeal defects (e.g., cleft palate), painful conditions, and neurologic diseases (e.g., botulism) [87,116]. Reflux of milk through the nose soon after nursing is most commonly associated with cleft palate and dorsal displacement of the soft palate (DDSP). A variety of congenital (e.g., subepiglottic cyst, esophageal atresia) and acquired (e.g., esophagitis, gastric ulcers) causes have also been reported . Coughing is often observed during nursing as a result of milk dripping into the tracheobronchial tree. If enough milk accumulates inside the trachea, the foal will present a delayed apparition of milk at the nostrils when it lowers the head and neck. This delay may also be observed with defects involving esophagus and stomach . Endoscopic examination of the upper respiratory tract is a valuable diagnostic tool, in particular for detection of palatal defects (Fig. 20). Large palatal defects may be seen during an oral examination. Pharyngeal dysfunction may also be caused by hyperkalemic periodic paralysis, selenium/vitamin E deficiency, dysmaturity/prematurity, and idiopathic causes .
In the adult horse, the most common causes of ingesta in nasal discharge are esophageal obstruction (choke), retropharyngeal abscess (e.g., strangles), and neurogenic pharyngeal dysfunction associated with guttural pouch disease . Palpation of the pharyngeal area should be performed to detect evidence of pain, swelling, and scaring. Passage of a nasogastric tube may result in frequent deglutition and sometimes violent response if the horse suffers from a painful condition (e.g., pharyngeal abscess). Alternatively, difficulty in triggering a deglutition in response to pharyngeal stimulation with the tube may result from neurologic diseases. The next step is to advance the tube into the esophagus in order to detect any obstruction. Endoscopy of the upper airways is important to evaluate pharyngeal function and possible lesions (infection, mass, defect. foreign body) that could impair deglutition. Endoscopy of the esophagus and stomach should follow. Various esophageal (e.g., fistula, diverticulum, stricture, laceration, cyst, neoplasia, abscess, esophagitis, megaesophagus, persistent right aortic arch) and gastric (e.g., ulcers, pyloric obstruction, gastric dilation) diseases can also result in nasal regurgitation of ingesta (Fig. 36) .
Figure 36. Megaesophagus.
A complete neurologic examination should be performed in dysphagic horses with no evident cause of pharyngeal dysfunction. Involuntary swallowing is usually preserved with diseases of the forebrain (e.g., lead toxicity, equine viral encephalitides, hepatic encephalopathy, neonatal maladjustment syndrome) . Diseases affecting pharyngeal and laryngeal centers in the caudal brainstem result in loss of both voluntary and involuntary swallowing (e.g., equine protozoal myelitis, equine rhinopneumonitis, abscess, and neoplasia).
A common complication of impaired deglutition is aspiration pneumonia, therefore particular attention should be placed on the examination of the lower respiratory tract.
Poor performance refers to horses that experienced a decrease in performance level or that are unable to exercise at a level expected based on their physical characteristics, genetic potential and training status. The term exercise intolerance is more restrictive and usually reserved for horses that are not capable of training at the expected level.
A variety of conditions are associated with poor performance in the athletic horse. Several retrospective studies found that the majority of problems associated with poor performance involve the musculoskeletal, respiratory, cardiovascular, and neurologic systems [134-136]. Metabolic disorders are also a well known cause of poor performance . An important observation is that a large number of horses are affected by a combination of problems often involving different body systems. This finding underscores the value of a systematic diagnostic approach to cases of poor performance. Often horse owners and trainers have a preconceived idea of what the horse's problem might be that may skew the clinician's investigation. It is essential to resist this focused approach and to keep an open mind.
Investigation of horses with decreased performance is usually straightforward when a rigorous approach is followed. However, horses that never performed to their expected level are more of a diagnostic challenge because it may be difficult to differentiate between unreasonable expectation from the owner or trainer, lack of athletic potential and potential behavior abnormalities affecting the horse's performance.
The systematic approach to the diagnosis of poor performance includes a careful review of the history, a comprehensive physical examination at rest and exercise, and appropriate use of ancillary diagnostic tools. The following discussion will focus on respiratory causes of poor performance.
Collection of historical information is time consuming and often owners or trainers omit information that they perceive as irrelevant. However, this part of the investigation is essential to make sure that we will focus on the right problems. Adopting a standardized history form is advantageous because it will prevent omission of important facts. The form should include questions concerning signalment, presenting complaint, nutrition, training status, performance in competition, and medical history . Ideally, the form should be tailored to the type of activity performed by the horse. Objective data concerning racing times, track surface, and distances raced are useful in racehorses whereas cardiac recovery data after competitive trail rides and environmental conditions are an important part of poor performance evaluation in endurance horses [135,138].
A clear understanding of the presenting complaint is crucial because the clinical examination may reveal a significant respiratory problem when the original complaint from the trainer was lameness. A common reaction from the trainer is to dismiss the unexpected finding saying for example "the horse always had that problem but was performing fine with it". It is not unusual for horses to be able to cope with one or more clinical problems, but the occurrence of another one might precipitate the onset of poor performance. Addressing only the latest problem often does not restore the performance level. Questioning the owner should reveal the timing of onset (acute or chronic), the duration, and the severity of poor performance. General information needed include housing conditions, nutrition, prophylactic measures, medications given for competition (e.g., furosemide, phenylbutazone, etc.), and detailed medical history.
A careful inspection should reveal the horse temperament, body condition, hair coat quality, conformation, symmetry of muscle masses, hoof condition, nasal discharge, and breathing pattern. Physical examination starts by recording mucous membranes color, capillary refill time, heart rate, respiratory rate, and rectal temperature.
Respiratory System Evaluation at Rest
The main focus of the examination is to detect any abnormality that may obstruct conducting airways or impair alveolar gas exchanges. Comparison of airflow through each nostril is a crude and insensitive way of detecting nasal obstruction. Assessment of respiratory sounds is important and is detailed in this publication (Couëtil, abnormal respiratory sounds). Examination of the nostrils includes inspection for nasal discharge and palpation of the alar folds, nasal septum, and rostral turbinates. Thickened and edematous nasal folds and turbinates are associated with rhinitis and cervical vagosympathetic trunk abnormalities (e.g., Horner's syndrome), which causes increased resistance to airflow. Neuromotor function responsible for nostril dilation should be assessed. Impaired function may cause exercise-induced collapse of the nostrils resulting in severe airway obstruction. Percussion of maxillary and frontal sinuses is useful to detect areas of pain or dullness. The cricoarytenoideus dorsalis muscle is palpated to detect potential atrophy and scars or nodules from previous surgery. Further palpation of the throat latch area is indicated to reveal retropharyngeal lymph nodes swelling and cough response to compression of the trachea (Fig. 6 & Fig. 6).
Next, is the evaluation of the lower respiratory tract (intrathoracic airways and lungs). Characterization of the breathing pattern is performed by comparing the contribution of thoracic and abdominal movement to inspiration and expiration. Increased abdominal muscle contraction during expiration and a prolonged expiratory phase indicate intrathoracic airway obstruction. Hypertrophy of external abdominal oblique musculature is common in horses with heaves and SPAOPD . Percussion and auscultation of the thorax should follow and has been described in detail above.
Respiratory System Evaluation during Exercise
An important reason for examining the horse during exercise is to detect and characterize abnormal respiratory sounds originating from upper airway obstruction. Sounds are best heard while exercising the horse on a lounge line. Inspiratory stridor usually indicates variable upper respiratory obstruction (e.g., nostril collapse, laryngeal hemiplegia, pharyngeal collapse, epiglottic entrapment, etc.). An exception to this rule is dorsal displacement of the soft palate, which results in expiratory stridor and airway obstruction . Determination of the type of airway obstruction is based mainly on endoscopy.
Hematology findings and fibrinogen concentration may support a diagnosis of inflammatory or infectious disease. Leukocytosis with neutrophilia is commonly found with bacterial respiratory infections and in response to stress. During the acute phase of a bacterial infection, increased numbers of immature neutrophils ("left shift") may be observed. Hematologic changes during the early phase of a viral respiratory infection (e.g., influenza) are often characterized by normocytic, normochromic anemia, lymphopenia or lymphocytosis, and sometimes neutropenia [75,89] Neutrophilia may follow within a week of initial clinical signs, particularly in cases of secondary bacterial infection. Monocytosis may develop during the recovery phase of a viral infection. Paired serum titers should help confirm suspicion of viral respiratory infection. Serum biochemistry is useful to evaluate non-respiratory disorders that may affect performance such as muscle, liver, and renal diseases. Arterial blood gases may reveal acid-base imbalances or gas exchange impairment, however, this test is not sensitive in the resting horse. Measurement of arterial blood gases is useful in the exercising horse when a standardized protocol is used, however, it requires use of a high-speed treadmill. Horses with inflammatory airway disease, heaves, and exercise-induced pulmonary hemorrhage exhibit a significantly more severe hypoxemia than control horses [139-142].
TW is recommended if an infectious etiology is suspected. BAL is recommended in non-infectious inflammatory pulmonary disease because cytology correlates well with pulmonary histopathology and it is more sensitive than TW cytology [22,91,92]. Both tests are in fact complementary and should be performed when feasible. Because strenuous exercise results in an influx of neutrophils in the epithelial lining fluid and inhalation of airborne particles it is recommended to perform these tests before strenuous exercise or at least 48 hours after .
Endoscopic examination is a crucial diagnostic test for respiratory diseases. Careful examination of nasal passages, pharynx, larynx, and trachea allows localizing a lesion, however, it often requires sedation of the horse. Assessment of upper respiratory tract function is best performed on the non-sedated horse and should therefore be conducted first. The examination should be accomplished first during normal breathing and then during nasal occlusion until strong respiratory efforts are generated (usually at least 30 seconds). Nasal occlusion maneuver produces airway pressure changes comparable to exercise-induced pressure swings and may allow detection of dynamic airway obstruction . Endoscopic examination may be performed during repeated flexion and extension of the neck to assess the effect of head and neck position on upper airway patency. This test can also be performed while the horse exercises on the treadmill.
Radiography is helpful to detect masses and decreased airway diameter that may result in upper airway obstruction. Thoracic radiography allows detection of pulmonary, mediastinal, and pleural disease, however, the method is not sensitive and cannot be performed with portable units. Ultrasonography is a sensitive method for the detection of pleural disease.
A dichotomous approach to the diagnosis respiratory disease in the poorly performing horse is described in Fig. 37. This approach is meant to help reach a diagnosis efficiently, however, the clinician should recognize that it is sometimes difficult to determine the contribution of a respiratory abnormality to poor performance. For example, detection of blood in the tracheobronchial tree of a thoroughbred horse post-racing is consistent with EIPH. However, up to 80% of racing thoroughbreds have evidence of blood in the trachea . Endoscopic grading of bleeding severity is useful as more severe bleeding is associated with decreased odds of success [144,145].
Figure 37. Diagnostic approach for a horse with poor performance. BAL: bronchoalveolar lavage; BG: arterial blood gases; EIPH: exercise induced pulmonary hemorrhage; IAD: inflammatory airway disease; PFTs: pulmonary function tests; SPAOPD: summer pasture-associated obstructive pulmonary disease; TW: tracheal wash; U/S: ultrasonography; XRay: radiography.
Detection of abnormal upper respiratory sounds should prompt an endoscopic examination of the airways in the resting horse. Dynamic endoscopy during treadmill exercise is indicated if an abnormality is not detected during resting examination or if the abnormality is of uncertain significance. Assessment of nasal patency is difficult and endoscopy is often not able to detect partial nasal obstruction. Skull radiographs may help identify lesions such as thickened nasal septum and sinus disease.
Abnormal lung sounds, cough, and abnormal nasal discharge suggest pulmonary disease and should be investigated by collection of respiratory secretions by TW or BAL. Cytologic findings from TW revealing predominance of neutrophils with various degrees of degenerative changes and presence of intracellular or extracellular bacteria are consistent with an infection. A microbiologic culture of the fluid is indicated to identify the etiologic agent. Further evaluation using radiography and ultrasonography is indicated in order to identify lesions consistent with bronchopneumonia, pulmonary abscess, or pleuropneumonia. Culture of TW fluid from infectious cases may result in no growth in cases of insufficient number of bacteria, prior antimicrobial therapy, inappropriate culture medium (e.g., mycoplasma and fungal infections), or viral infection without secondary bacterial infection. Alternatively, isolation of bacteria from TW fluid is not sufficient to establish causality and recommend antibiotic therapy. For example, the role of bacteria in IAD of young racehorses is controversial. Epidemiologic studies have shown an association between the number of bacteria isolated from TW and inflammation severity . However, no bacteria were isolated in 35% of horses with IAD. In addition, inhaled dust and endotoxins may induce neutrophilic inflammation in respiratory secretions and could play a role in IAD.
Horses with negative TW culture and evidence of neutrophilic inflammation in TW or BAL fluid suggest IAD, heaves, SPAOPD, or viral respiratory disease [93,95,147]. Historical findings such as acute onset of respiratory disease, cough, and fever are consistent with viral disease. Horses with IAD, heaves, and SPAOPD often have a history of chronic cough and are not febrile. Horses with heaves or SPAOPD usually exhibit increased respiratory efforts, whereas horses with IAD do not [22,68,148]. Horses with IAD, heaves, or SPAOPD may have significant intrathoracic airway obstruction without evidence of clinical signs. Specialized pulmonary function testing is often useful to identify subclinical airway obstruction [22,149].
Eosinophilic inflammation of TW or BAL fluid may be associated with parasitic pneumonitis, IAD, hypersensitivity pneumonitis, fungal pneumonia, and cutaneous habronemiasis [96-99]. Fecal flotation (Baermann technique) is often not diagnostic in cases of parasitic pneumonitis [100-101]. A presumptive diagnosis may be reached when respiratory secretions reveal evidence of parasite eggs or larvae, exposure to donkeys is documented, and anthelmintic therapy results in clinical improvement . Increased metachromatic cells (mast cells, basophils) in BAL fluid have been described in horses with IAD with chronic cough and exercise intolerance [98,102].
Endoscopy is indicated in horses that have no evidence of respiratory disease on physical examination. The optimal time to detect the presence of blood in the tracheobronchial tree of strenuously exercising horses is 30-90 minutes post-exercise . Presence of mucopurulent secretions should be investigated by performing a TW or BAL. Cytology findings revealing a high percentage of hemosiderin-laden alveolar macrophages and red blood cells are consistent with EIPH.
Treadmill stress testing is indicated in horses with no detectable signs of respiratory disease based on clinical examination. Arterial blood gas measurement during standardized exercise may be helpful to detect subclinical respiratory disease or to assess the potential effect of respiratory disease on performance [140-142]. Measurement of blood or plasma lactate concentration during exercise is also a valuable test to assess fitness. Training results in an increase in aerobic capacity and a delay in the onset of blood lactate accumulation . Inappropriate fitness level may be detected by measuring indices of lactate kinetics during standardized laboratory or field testing [151,152]. Exercise capacity is dependent on aerobic capacity and can be determined by measuring maximum oxygen consumption (VO2max) during exercise . Specialized pulmonary function tests are sensitive tests of airflow obstruction that may detect subclinical pulmonary disease [22,63,154]. Unfortunately, most pulmonary function tests and exercise testing are only available at a few referral institutions.
Finally, horses with no detectable cause of poor performance fall into three categories: cause other than respiratory, behavior problem, or unknown.
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Affiliation of the authors at the time of publication
Department of Veterinary Clinical Sciences, School of Veterinary Medicine, West Lafayette, IN, USA.