Avian Respiratory Anatomy

Upper Airway

The avian respiratory system is complex, and the anatomy is much different than mammalian species. The information presented here is a brief overview of this topic, and complete anatomic details can be found elsewhere.^6,8 The upper respiratory tract of birds begins with the nares, which, in some species, are surrounded by a soft tissue protuberance termed the cere. Chronic upper respiratory disease can lead to abnormally shaped nares or grooves in the rhinotheca immediately ventral to the nares. Most species have three nasal conchae - rostral, middle, and caudal. The caudal nasal conchae are connected dorsally with the infraorbital sinus, which is the largest sinus in the avian skull.

Large Airway

The avian larynx is composed of four partially ossified cartilages, which form the laryngeal mound. There is no epiglottis, and unlike in mammals, the larynx is not responsible for voice production. The trachea is composed of complete tracheal rings, which are ossified in some of the larger species and in passerines. The tracheal cartilages are actually signet-ring shaped and partially overlap with one another. The trachea ends with the syrinx and is the origin of the left and right primary bronchi. The structure of the syrinx is highly variable between species, and this is the source of voice production in birds through vibrations of the tympaniform membranes.

Lungs and Air Sacs

The avian lungs are firmly affixed to the ribs and are non-lobed. Each primary bronchi continues through the lung parenchyma as the intrapulmonary primary bronchus to the caudal-most portion of the lung. Four groups of secondary bronchi (medioventral, mediodorsal, lateroventral, and laterodorsal) originate from the intrapulmonary bronchus. Numerous parabronchi branch off each of the secondary bronchi and freely anastomose with one another. Air capillaries arise from the parabronchi, and these are the site of gas exchange. They are an average of 3–10 μm in diameter - by comparison, the smallest mammalian alveolus is about 35 μm in diameter. These air capillaries branch and anastomose with each other, and intertwine with a network of blood capillaries.

The number of air sacs varies between species; in psittacines, there are 9 air sacs (2 cervical, 1 clavicular, 2 cranial thoracic, 2 caudal thoracic, and 2 abdominal). The walls of the air sacs consist of a thin layer of simple squamous epithelium, and these structures play no part in gas exchange. As birds lack a diaphragm, the air sacs function as a bellows to push air through the avian respiratory tract. Air sacs have connections to the lungs (via an ostium) and to the pneumatic bones such as the humerus, femur, and certain vertebrae. The air sacs expand during inhalation and shrink during exhalation.

History and Physical Exam

The standard anamnesis should be obtained from the owner; however, there are several specific questions the clinician should ask, especially in an emergency situation. In addition to duration and frequency of illness, it is important to know if the bird has experienced any voice change or loss of voice. As voice production in birds originates from the syrinx, this historical detail could help determine if this anatomic position is affected.

Exposure to respiratory irritants, such as smoke (of any kind, from any source), aerosols, or Teflon (polytetrafluoroethylene), should also be determined. Usually, these exposures are acute in nature; however, owners may present a bird with an acute-on-chronic disease for suspected "toxin" exposure. If a thorough history is obtained, the clinician will be able to distinguish between the two. Owners may not be aware of certain toxins, such as Teflon toxicity, so it is always important to ask about exposure, and also to determine where the bird is housed in the house - is the patient's cage next to or in the kitchen? There is a variety of infectious diseases that may cause respiratory disease, which could culminate in acute respiratory distress. It is important for the clinician to know if the patient has been exposed to other birds (either wild or domestic), or if there are other birds in the household. Of course, if other birds in the house are unaffected, an airborne toxin or an infectious disease is less likely.

The initial physical exam of any dyspneic patient is often brief. Therefore, it is important to maximize the data which can be collected in the first interaction with the patient. Brief observation of the bird in the carrier is always important to help characterize the dyspnea (see below) and obtain a respiratory rate. The bird's mentation and stance (normal or wide-based) should also be recorded. Are the wings held out from the body or in a normal position? Is there open-beak breathing or a tail bob? With experience, the clinician may then determine the stability of the patient for restraint.

If possible, flow-by oxygen supplementation should be delivered during manual restraint for the physical. The bird should always be maintained in an upright position throughout the physical exam. The key points to focus on include auscultation (heart, lungs, ventral air sacs), palpation of body condition, and coelomic palpation. Remember, as birds do not have pulmonary alveoli, they cannot have "crackles" as you could auscultate a mammal with pulmonary disease. Crackles and other similar sounds may be auscultated in the air sacs if fluid is present within or around these structures. As with other species, audible wheezes or other abnormal loud respiratory sounds are often attributed to upper respiratory disease. A bird with a thin body condition score is more likely to have a chronic condition even if the owner presented the patient for an acute illness. The presence of coelomic effusion may require more immediate treatment than just oxygen supplementation including coelomocentesis. If the bird remains stable, the clinician can proceed with a more thorough physical exam. If not, the bird should be placed in a warm incubator with oxygen supplementation. It is also important to monitor the bird briefly after manual restraint to help determine its stability for future restraint - how quickly did the bird recover?

Divisions of Avian Dyspnea

There are several published criteria for divisions of avian dyspnea.^1,9 The author prefers to use a combination of these criteria in clinical practice. One of the first clinical decisions to make for a dyspneic bird is whether or not to place an air sac tube. To help determine if this is an appropriate treatment, the bird's respiratory pattern can be classified as obstructive or restrictive.

Obstructive Respiratory Pattern:

 Acute to peracute onset, often in good body condition

 Audible wheezing, +/– loud inspiratory stridor, respiratory rate may be normal

Restrictive Respiratory Pattern:

 Acute to chronic condition, normal to thin body condition score

 No respiratory noise

 +/– coelomic mass, +/– coelomic effusion

An obstructive breathing pattern is associated with such conditions as a tracheal obstruction or syringeal mass (i.e., fungal granuloma). In these cases, placement of an air sac tube will help alleviate the dyspnea and allow the clinician to treat the inciting cause. If any coelomic effusion is present, regardless of the breathing pattern, an air sac tube is contraindicated.

Air sac tubes are placed in the caudal thoracic air sac or abdominal air sac using a similar approach as coelomic endoscopy. General anesthesia is necessary for placement. The clinician should select a tube that is of similar diameter to the patient's trachea. The author has used red rubber feeding tubes, endotracheal tubes, and air sac cannulas for this purpose. The patient is placed in right lateral recumbency, with the leg pulled cranially. The skin overlying the placement site is routinely prepped, and a small skin incision is made just ventral to the flexor cruris medialis muscle and caudal to the last rib. A pointed hemostat is used to create a defect in the coelomic wall with gentle downward pressure using a short finger stop on the instrument. The tube is secured routinely with a purse string suture followed by a Chinese finger trap suture. The author also then secures the tube on the bird's dorsum to prevent self-trauma to the tube. E-collars may be necessary to protect the integrity of the tube depending on the bird's temperament. Whole body radiographs and confirmation of airflow through the tube will help determine if the air sac tube is in the correct location.

Restrictive breathing patterns are seen for diseases of the small airways, lung parenchyma, and in cases of coelomic cavity effusion or masses. Additional classification of dyspnea will help localize the disease process. This will allow the clinician to formulate an appropriate diagnostic and therapeutic plan for each patient.

Upper Airway (Nares, Infraorbital Sinus)

 Nasal discharge, +/– infraorbital swelling

 Increased rate without increased effort unless bilateral nasal obstruction is present

Differential Diagnosis

URI secondary to hypovitaminosis A and squamous metaplasia, bacterial infections (Gram-negative bacteria, Mycoplasma sp., Mycobacterium, Chlamydia psittaci), fungal infections (Aspergillus species, yeast), viral infections (poxvirus, avian influenza), and parasitic infections (Knemidokoptes).

Large Airway (Trachea, Syrinx)

 Loud inspiratory stridor

 Increased rate and effort, usually with open-beak breathing

Differential Diagnosis

Tracheal foreign body,³ tracheal stenosis,⁴ postintubation tracheal obstruction,¹⁰ traumatic tracheal collapse,⁵ tracheal masses,⁷ syringeal masses (infectious and noninfectious).

Lungs and Air Sacs

 Soft expiratory wheeze or no audible sounds

 Extreme respiratory distress with open-beak breathing

Differential Diagnosis

Airborne respiratory toxins/irritants (smoke, aerosols, polytetrafluoroethylene [Teflon]), bacterial infections (Gram-negative bacteria, Mycobacterium, Chlamydia psittaci), fungal infections (Aspergillus species, yeast), viral infections (poxvirus, avian influenza, polyomavirus, paramyxoviruses), and parasitic infections (air sac mites, Syngamus sp.).

Coelomic Cavity Disease

 Increased respiratory rate and effort, exacerbated by handling/stress

 No audible respiratory sounds, +/– distended coelom

Differential Diagnosis

Transudate (liver failure, heart failure), exudate (septic peritonitis, egg-yolk peritonitis), neoplasia, organomegaly (numerous), egg-binding/dystocia.

Treatments

Oxygen therapy is essential and ideally will be administered to the patient in a quiet incubator with heat support. Some authors advocate administration of a bronchial dilator, terbutaline (0.01 mg/kg IM), initially prior to obtaining additional diagnostics.⁹ Sedation with butorphanol (1–2 mg/kg IM) is also indicated as an initial treatment if the patient is anxious or appears painful. If heart failure is suspected, some authors recommend administration of furosemide (2–4 mg/kg IM or IV).⁴ Use of this drug in avian species is controversial as only 10–30% of avian nephrons have a loop of Henle - the remainder are reptilian-type nephrons that lack this anatomical structure.²

Nebulization of either sterile saline or antibiotics are also beneficial for certain cases of avian dyspnea. A recent study examined the distribution of fluorescent microspheres after nebulization in domestic pigeons as a model for nebulization of birds with respiratory disease in clinical practice.¹² Nebulization of 30 minutes to one hour in the pigeons resulted in limited numbers of the microspheres in the secondary bronchi and pulmonary parenchyma; 2–4 hours of nebulization therapy resulted in a more significant number in the ostia of the lungs and air sac membranes. A similar study also determined that traditional medical nebulizers designed for use in humans do not create aerosol droplets small enough to reach the avian lungs and air sacs - these nebulizers create aerosols with an average diameter of 5–10 μm, and only aerosols 3 μm and smaller were noted throughout the pigeon respiratory tract.¹¹

References

1.  Antinoff N. Understanding and treating the infraorbital sinus and respiratory system. In: Proceedings from the Annual Association of Avian Veterinarians Conference; 2001.

2.  Braun EJ. Comparative renal function in reptiles, birds, and mammals. Semin Avian Exotic Pet Med. 1998;7:62–71.

3.  Clayton LA, Ritzman TK. Endoscopic-assisted removal of a tracheal seed foreign body in a cockatiel (Nymphicus hollandicus). J Avian Med Surg. 2005;19:14–18.

4.  de Matos REC, Morrisey JK, Steffey M. Postintubation tracheal stenosis in a blue and gold macaw (Ara ararauna) resolved with tracheal resection and anastomosis. J Avian Med Surg. 2006;20:167–174.

5.  Guzman DS, Mitchell M, Hedlund CS, Walden M, Tully TN Jr. Tracheal resection and anastomosis in a mallard duck (Anas platyrhynchos) with traumatic segmental tracheal collapse. J Avian Med Surg. 2007;21:150–157.

6.  King A, McLelland J. Female reproductive system. In: King A, McLelland J, eds. Birds, Their Structure and Function. East Sussex, UK: Bailliere Tindall; 1984:145–165.

7.  Monks DJ, Zsivanovits HP, Cooper JE, Forbes NA. Successful treatment of tracheal xanthogranulomatosis in a red-tailed hawk (Buteo jamaicensis) by tracheal resection and anastomosis. J Avian Med Surg. 2006;20:247–252.

8.  O'Malley B. Clinical Anatomy and Physiology of Exotic Species. Edinburgh, UK: Elsevier Saunders; 2005.

9.  Orosz SE, Lichtenberger M. Avian respiratory distress: etiology, diagnosis, and treatment. Vet Clin North Am Exot Anim Pract. 2011;14(2):241–255.

10. Sykes JM, Neiffer D, Terrell S, Powell DM, Newton A. Review of 23 cases of postintubation tracheal obstructions in birds. J Zoo Wild Med. 2013;44:700–713.

11. Tell LA, Smiley-Jewell S, Hinds D, et al. An aerosolized fluorescent microsphere technique for evaluating particle deposition in the avian respiratory tract. Avian Dis. 2006;50:238–244.

12. Tell LA, Stephens K, Teague SV, Pinkerton KE, Raabe OG. Study of nebulization delivery of aerosolized fluorescent microspheres to the avian respiratory tract. Avian Dis. 2012;56:381–386.