Session #3002

Abstract

Limitations of diagnostic techniques in avian medicine make the ante-mortem diagnosis of cardiovascular diseases in birds challenging. Indications for examination of the cardiovascular system are often unspecific. A scoring system for criteria in anamnestic risk factors and clinical signs can facilitate the decision. Score assignment is discussed during the masterclass. Further, different pathologies are demonstrated in the individual diagnostic methods that are discussed.

Introduction

Ante-mortem diagnosis of cardiovascular diseases in birds is challenging due to the limitations of several diagnostic techniques in avian medicine. Frequently described cardiovascular lesions in pet birds include atherosclerosis, pericardial effusions, pericarditis, myocarditis, dilatation or hypertrophy of the ventricles, and valvular endocarditis. Right ventricular or biventricular heart failure seems to be more common than left ventricular heart failure. Some case reports are available on myxomatous degeneration or atrioventricular valve endocardiosis, bacterial endocarditis, and arteriopathy of the right brachiocephalic artery. Indications for examination of the cardiovascular system are often unspecific. A scoring system for given criteria in anamnestic risk factors and clinical signs can facilitate the decision.

Diagnostic Approach

Anamnestic Data

Relative predisposition to cardiovascular diseases is given by the species, breed, age, gender, lifestyle, and diet. Examination parameters that might indicate an increased risk of cardiac disease and atherosclerosis especially may include the following (score 1 point for each):

• Predisposed species
• Female gender
• Age >15–20 years
• Unbalanced, inappropriate feeding
• Decreased activity
• Inappropriate husbandry
• Pre-existing disease that may adversely affect the cardiovascular system

Cardiac disease is common in larger, elderly parrots living in captivity due to inadequate housing conditions, malnutrition, and long-life expectancy. A high prevalence of atherosclerosis, for example, is reported in African grey parrots (Psittacus erithacus), Amazon parrots (Amazona spp.), and cockatiels (Nymphicus hollandicus), in contrast to cockatoos and macaws. A higher incidence of atherosclerosis was also noted in birds of 15–20 years and older and in the female sex, especially in association with reproductive diseases. The predisposition to the development of atherosclerosis in female psittacine birds likely relates to the profound effects of estrogen in reproductively active birds.

In addition to age, female sex, and species, risk factors for the development of atherosclerosis also include high-calorie and fat diets, dyslipidemia (e.g., hypercholesterolemia), and limited physical activity.

Clinical Examination

Clinical Signs

Although often nonspecific, common examination findings that may indicate cardiac disease include the following (assign 1 point for each finding):

• Periorbital bluish discoloration/cyanosis
• Central nervous disorders/epileptiform seizures/ataxia
• Prolonged respiratory recovery with increased activity
• Exercise intolerance
• Disorientation or confusion
• Chronic untreatable skin changes
• Delayed absorption of administered subcutaneous medications

Clinical signs associated with atherosclerosis can have a subtle, insidious onset. Common findings are exercise intolerance, lethargy, dyspnea, cyanosis, seizures, as well as prolonged healing of dermal lesions.

Many birds do not show any clinical signs until they are stressed or the patient decompensates. As a result, atherosclerosis often is diagnosed postmortem. Severe lesions in the great vessels of the heart are often incidental findings at necropsy.

In general, owners of birds with cardiovascular disease mostly report nonspecific clinical signs such as progressively declining activity level and reduced appetite. Central nervous disorders, such as paresis or rigidity of one or more limbs or seizure activity, as well as behavioral changes, including disorientation or confusion, may be observed. Persistent exercise intolerance occurs regularly in birds with existing heart disease. Congestive heart failure can lead to a clinical presentation of coelomic effusion and hepatomegaly. Due to avian anatomy, the lack of a diaphragm, coelomic effusion reduces the patient’s ability to ventilate. This may result in tachypnea, increased respiratory effort, open-beak breathing, tail bobbing, and a wide stance may be observed. The typical heart cough in mammals cannot be observed in birds, in general, due to anatomic and physiologic particularities. Furthermore, cyanosis of the skin (or integument) may be observed periocularly (or around the eyes) in avian species lacking feathers in this area. Other dermal indicators of cardiac disease can include recurring or chronic skin lesions such as axillary or wing web dermatitis and focal feather loss, which have been reported in patients with atherosclerotic lesions. Congestive heart failure and peripheral venous congestion may be recognized by distension of the jugular and cutaneous ulnar veins. Edema is rarely found, most often appearing as swelling of the periorbital region or of the hocks and feet. In hospitalized patients receiving subcutaneous fluids, the first indication of circulatory compromise may be delayed absorption (>48 hours).

Additional Examination Methods

Standard examination methods for heart disease, as found in mammals, are partly lacking or hard to evaluate due to numerous physiologic peculiarities in birds. These include the following:

• Arterial pulse
• Auscultation
• Hematology
• Biochemistry
• Blood pressure measurement

For instance, arterial pulses cannot always be palpated or thoroughly assessed. The relative warmth of each extremity can be subjectively assessed. Auscultation of the avian heart only plays a subordinate role due to many limitations; however, it can provide subjective information about the rate, sound quality, and rhythm. Due to rapid heart rates, individual heartbeats are difficult to note by the examiner, making muffled heart sounds or heart murmurs very difficult to characterize. In the case of cardiogenic pulmonary edema, increased respiratory noise can be heard during auscultation in a calm bird, but characteristic crackles and wheezes are generally absent, except in severe cases.

Changes in the complete blood count have no correlation to cardiac disease; however, some alterations have been described in association with atherosclerosis. Plasma lipid levels may offer some observational data pertinent to population-level risk factors for cardiovascular diseases. Changes in plasma lipids, such as total cholesterol and total triglycerides, as well as HDL-C and LDL-C, may be noticed in an individual bird, but single measurement results should be interpreted with caution. Until now, dyslipidemias, as well as lipoprotein ratio and non-HDL concentrations, have not been statistically linked to cardiovascular disorders. Similarly, atherosclerosis has also been shown in birds with normal plasma cholesterol levels, whereas hypercholesterolemia in the blood cannot always be associated with atherosclerosis. Furthermore, cholesterol may increase independently from the occurrence of atherosclerosis (e.g., females displaying vitellogenesis).

In human medicine, an increased level of triglycerides in the blood is a prominent risk factor for cardiovascular diseases due to the presence of atherogenic particles. To what extent this factor can be transferred to the class Aves is questionable. Since the triglyceride value in the blood changes rapidly after a change in the feed ration of a bird and is subject to more postprandial fluctuations, this value must also be assessed critically.

Unfortunately, there is poor agreement between invasive and non-invasive blood pressure measurements in birds. Using non-invasive techniques in psittacine birds, high variabilities in the readings from different cuff placement sites on the same individual have been reported. The accuracy of the method used must be therefore assessed critically. Because of these technical issues, the significantly higher arterial blood pressure of birds compared to mammals, and the lack of scientific data on hypertension in birds, blood pressure measurement plays a subordinate role in assessing heart diseases in birds; however, it may help to define hypertension.

Imaging Techniques

Radiographs may show subjective changes in heart size and great vessel density (or radio-opacity); however, this is not an appropriate assessment of cardiac function. An echocardiogram is far more sensitive to assess cardiac function, while vascular health may require more advanced imaging. Because M-mode examination cannot be performed in birds, the spectral Doppler function is the only functional mode of evaluation of the heart in birds. It enables the investigator to visualize and measure the aortic root and take measurements of the aortic outflow. Reference intervals are available for the evaluation of the heart itself in 2D mode as well as for aortic measurements in different species (Table 1). Other techniques such as fluoroscopic angiography and computed tomography may help to detect signs of conditions like atherosclerosis in birds. Electrocardiography (ECG) has been considered but is not commonly used in avian practice due to a lack of standardization, artifacts, and problems with interpretation. In some instances, endoscopy, and rarely MRI, may be indicated as well.

Diagnostics of value for the detection of cardiac disease include the following:

• Echocardiogram
• Doppler ultrasonography
• Radiologic native examinations (radiology, computed tomography)
• Angiocardiography
• ECG
• Endoscopy
• MRI

Table 1. Reference values for selected bird species (mean±standard deviation)

a. Not known

Echocardiogram

Echocardiography is currently the diagnostic method of choice for suspected cardiac disease, especially in larger Psittaciformes, Columbiformes, and birds of prey. Echocardiograms in the awake avian patient are advisable in severely ill animals for which general anesthesia is associated with a higher risk. Sedatives, such as midazolam, may be warranted in severely stressed patients. Echocardiography is less invasive in comparison to other imaging methods and allows for the cardiovascular-compromised patient to be evaluated in an upright position during the examination.

To assess the avian heart, two coupling sites are described: a) the ventromedian approach with two horizontal longitudinal views; and b) the parasternal approach with several short and long axis views, which may be helpful for examination of the valves and the vessels.

As in mammal medicine, echocardiography in birds allows for the visualization of cardiac structures in motion and detailed imaging of internal structures. Due to anatomic peculiarities, the established method of choice in birds is the B-mode method (2D echocardiography), and reference values are already available for various species (Table 1). Furthermore, echocardiography is well suited for determining the degree of success in treating hydropericardium or controlling the contractility of the ventricle once the patient has been administered medication. The use of echocardiography to image blood vessel walls in birds is limited. At least the assessment of the aorta close to the heart is possible and clinical examination has shown that hyperechoic areas indicate the presence of calcification within the vessel wall; however, the examination of vascular disease using echocardiography is very subjective and requires an experienced examiner.

A routine echocardiogram exam assesses:

• Size of the ventricles
• Thickness of the interventricular septum
• Morphology and function of the valves
• Assessment of the aorta
• Contractility of the ventricles

The following parameters are important for evaluating the heart’s morphology and function. This includes the size of the ventricles and the thickness of the interventricular septum. Furthermore, the left atrioventricular valves, the aortic valves, and the muscular right AV valve can be examined independent of the image quality. The diameter of the aortic root can be assessed, as well as the blood outflow velocity (see below).

The aortic diameter is not an accurate measurement to evaluate for the presence of atherosclerosis in birds. In addition to cardiac size, ventricular contractility (fractional shortening) of the transverse diameter of the left ventricle is a valuable parameter for the assessment of cardiac function. To obtain ventricular contractility, fractional shortening should be calculated using the following formula:

Fractional shortening (%)=(diastolic diameter−systolic diameter)×100/diastolic value

Doppler Ultrasonography

The color Doppler function has been successfully utilized in various avian species and is considered a valuable tool in the diagnosis of aneurysms and valvular insufficiency; however, the color Doppler function significantly reduces the frame rate. The ultrasound image is known as a frame. On the ultrasound monitor, we see multiple frames produced in rapid succession. The frame rate, then, is the speed at which those images are shown. A reduced frame rate is associated with a reduced temporal resolution, making the examination results strongly dependent on the examiner’s experience. Therefore, its applicability in avian echocardiography is demanding.

Spectral Doppler ultrasonography is used for assessing the velocity of the blood flow. For this measurement, the ventromedian coupling side should be utilized. Spectral Doppler measures the rate of blood flow (inflow, outflow) and can be seen in a 2D curve against time. In most species, it is possible to visualize the diastolic blood flow at the left and the right atrioventricular valves and therefore obtain inflow rates to the right and the left ventricles, as well as aortic systolic outflow. For these measurements, reference values are available for some psittacine and raptor species. Due to stress-induced bias (increased heart rate and cardiac outflow), the examination is recommended to be done under general anesthesia or, at least, mild sedation.

In birds, spectral Doppler, specifically pulsed wave Doppler (PW Doppler), is preferred because the examiner can select a gate (the sample site from which the signal is obtained with pulsed Doppler) for the examination. This gate is positioned directly distal to the aortic valve in the aortic root. With the help of the angle correction on the ultrasonic device, the direction of measurement of the blood flow velocity in the aorta can be aligned manually. Afterwards the aortic flow is shown in a graphic representation on the ultrasonic device. By tracing the aortic flow with the trackball, the velocity time integral (VTI) and the heart rate can be calculated.

In the author’s experience, measurement of the blood velocity in the aortic root can provide useful information on possible atherosclerotic changes. This is because wall alterations result in smaller vessel diameter and therefore increase the aortic outflow. Values above 1–1.5 m/s are often documented in birds with suspected atherosclerotic vessels.

Another spectral Doppler, the continuous wave Doppler (CW Doppler), is rarely used in birds, as measurements of the blood flow velocities are required from an inaccessible point. Recently tissue Doppler imaging was used to quantify myocardial velocities by measuring the longitudinal peak velocities in systole and diastole in awake racing pigeons.

Radiographic Diagnostics (Conventional CR and CT)

In native lateral and ventrodorsal radiographs, the position, size, and shape of the heart silhouette, as well as the radiopacity of the major vessels, can be assessed. A discernible radiographic image of the apex of the heart is visible in a few avian species (e.g., cockatoos). In other species, a clear view of the apex of the heart indicates the presence of an air sac rupture as a result of trauma, as the air surrounding the heart works as a contrast medium. In such cases, echocardiographic imaging is limited because ultrasound waves striking the tissue-air interface are mostly reflected, limiting further tissue penetration.

To determine the size of the avian heart, measurements are described for various species using conventional radiographs. The maximal width of the cardiac silhouette and the thoracic width should be measured in ventrodorsal (VD) projection. The length of the sternum and the cardiac length is measured in lateral projection. Ratios are then calculated and compared to the published data.

A common radiographic finding is cardiomegaly, noted by an enlarged cardiac silhouette. Cardiomegaly indicates multiple etiologies such as cardiac hypertrophy, cardiac dilatation, pericardial effusions, aneurysms, inflammation, or neoplasms; however, the differentiation of these etiologies can only be determined by further diagnostics means. Additional radiographic findings, such as hepatomegaly, coelomic effusion, and respiratory disease, may be diagnosed secondary to cardiac diseases. A rare radiographic finding in birds is microcardia. Microcardia is most likely associated with severe dehydration.

By means of radiography, pathologies of the great vessels, such as atherosclerotic lesions, are only visible if they are very pronounced. Subjectively, soft tissue density or increased radio-opacity of the aorta can be assigned to atherosclerotic lesions. A massively increased radiographic density, which is comparable to that of the grit stones, can be rated for calcification. Such detectable mineralization of the aortic wall, which is described as stage VII atherosclerosis, is considered highly suspicious for the presence of atherosclerosis. Often these animals also have very high blood flow velocities in the aortic root.

Compared to radiography, computed tomography enables better identification of the cardiovascular system without interference from the overlaying structures. Also, CT examination provides an excellent assessment of major arteries, particularly with the use of intravascular (IV) contrast media. Likewise, the four distinct chambers of the heart can be visualized using IV contrast media. The limits to imaging structures are dependent on the spatial resolution of the CT scanner, differences in density between the object of interest, surrounding structures, and size of the object. Motion artifact may be noted due to the rapid heart rate in birds, which may decrease the accuracy of the diameter measurements. Severe limitations also exist for small bird species when attempting to visualize the smaller arteries within the patient.

Angiography

Currently, there are only a few case reports on the use of angiocardiography in avian medicine. The examination can be performed either by real-time fluoroscopy in conventional radiography or by computed tomography. Due to the high heart rate in birds, an examination of cardiac contractility is challenging. Angiocardiography allows the brachiocephalic trunk, the aorta, pulmonary arteries and veins, and the caudal vena cava to be visualized. Thus, angiocardiography can provide useful information, especially for diagnosing changes in the heart vessels, such as stenoses, dilatations, and aneurysms.

The angiocardiographic examination should include the following:

• Sedation/anesthesia
• Warmed iodinated contrast agent
• Iodine content 380 ml iodine/ml
• Dosage of 2–4 ml/kg BW IV

Angiographic techniques can be utilized to diagnose arterial luminal stenosis and atheromatous plaques. Angiography is likely to become the diagnostic test of choice for atherosclerosis with continued improvement of resolution artifacts through technological advances; however, disagreements of the luminal arterial diameters were found when comparing three different CT angiocardiography protocols, limiting the diagnostic power with the existing protocols and current available technical possibilities. Further studies of CT angiocardiography and protocols are warranted to become diagnostically useful in cases of cardiovascular disease. Again, the availability and the high cost of the examination must be considered in birds.

Electrocardiography (ECG)

Clinicians must be aware of the different characteristics of the avian ECG compared to small animals. Due to the patient's high susceptibility to stress, the result of the electrocardiography in the awake bird may be falsified and should therefore be classified as an exercise ECG. The application of ECG in awake birds is difficult due to restraint and patient stress. Problems may occur with the connection of the leads to the skin and, as previously mentioned, stress may contribute to alterations of the recorded ECG. Therefore, electrocardiography, for the detection of heart disease in birds, is still infrequently used in comparison to mammals.

For recording an electrocardiogram in birds, both the use of needle electrodes and the use of spring electrodes have been described in the literature. As in human medicine, the position of the leads is based on the scheme of Einthoven. A recording speed of 100 to 200 mm/s is necessary. Reference values for various bird species have been established in studies focused on electrocardiograms in selected species.

In principle, an ECG may be useful to evaluate heart rate and rhythm, but one should remember that electrical activity does not ensure mechanical (pumping) activity. The ECG can actually remain relatively normal in birds, with severe cardiopulmonary compromise or even cardiac arrest from an anesthetic overdose. It is also important to keep in mind that arrhythmias can be explained by extra-cardiac and cardiac causes, as well as changes in the autonomic nervous system. It is therefore important to rule out metabolic abnormalities. Changes in the P waves and/or QRS complex can suggest enlargement of the cardiac chambers and a low voltage ECG may indicate the presence of pericardial effusion, ascites, or obesity.

Endoscopy

Endoscopic examination and guided sampling can be especially valuable in the diagnosis of masses associated with the heart or the major vessels. Endoscopy allows direct visualization and detection of gross abnormalities, such as cardiomegaly, pericardial effusion, pericardial thickening or exudate, arterial discoloration, gross structural changes, and neighboring masses or granulomas. Standard lateral approaches can be used to visualize the abdominal organs and arteries. The more uncommon interclavicular approach allows direct visualization of the great arteries and the base of the heart but is more invasive and may be impaired by fat deposits in overweight birds.

Magnetic Resonance Imaging (MRI)

MRI is relatively rarely used in clinical avian medicine due to the high noise level and the long scanning time, which is a significant concern for the anesthesiologist who has limited access to the patient. The other reason is the small size of the structures to be imaged and motion artifacts due to rapid respiratory and heart rates, which makes it difficult to achieve images of diagnostic quality. Motion artifacts prevent adequate imaging of the avian heart using MRI and it is also not recommended for the vascular system because of the rate of contrast circulation. In addition, there is little empirical data available for avian MRI cardiac image assessment.

References

1.  Krautwald-Junghanns M-E, Schulz U, Pees M. Evaluation of diagnostic criteria in grey parrots (Psittacus erithacus erithacus) with suspected atherosclerosis. Tierärztliche Praxis K. 2022;epub.

2.  Krautwald-Junghanns M-E, Pees M, Reese S, Tully T. Avian chapters: radiology, ultrasonography, computed tomography, heart and large vessels. In: Diagnostic Imaging of Exotic Pets. Hannover: Schlütersche Verlagsgesell; 2011. ISBN 978-3-89993-049-8.

3.  Konicek C, Krautwald-Junghanns M-E. Heart disease in pet birds—diagnostic options. Vet Clin North Am Exot Anim Pract. 2022;25(2):409–433. doi: 10.1016/j.cvex.2022.01.004. PMID: 35422260.