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Abstract: Vascular diseases in birds are not uncommon, according to findings from
postmortem surveys. Although atherosclerosis affecting psittacine birds appears overrepresent-
ed, some degenerative, infectious, neoplastic, and congenital vascular diseases may also occur. A
variety of imaging diagnostic tools may be used to evaluate the avian vascular system, such as
conventional radiography, fluoroscopy, rigid endoscopy, computed tomography, angiography,
transcoelomic, and transesophageal ultrasound examination. The wide array of current
diagnostic imaging tools offers the clinician capabilities to investigate avian cardiovascular
abnormalities. Further research in this domain and constant efforts to apply several, and newer,
vascular imaging modalities in clinical cases are needed to expand our avian cardiovascular
knowledge base. The ability to diagnose vascular pathologic processes in small avian patients
may be improved by recent developments in diagnostic imaging technology.
Key words: vascular imaging, angiography, diagnostic imaging, radiology, ultrasound,
echocardiography, endoscopy, avian
174
BEAUFRÈRE ET AL—AVIAN VASCULAR IMAGING 175
postmortem surveys2,6,9,10 varies between 4.6% to case25 was reported in a yellow-naped Amazon
91%. In pathologic studies of psittacine birds in parrot (Amazona auropalliata) and was associated
Europe, a high incidence of atherosclerosis has with cerebral hemorrhage diagnosed by computed
been reported, with an approximately 91% tomography (CT) scan. Another case26 was
incidence in African grey and Amazon parrots diagnosed and followed by serial magnetic
in one study and 13% in psittacine birds in resonance imaging (MRI) in an African grey
another study.2,6 This contrasts with the reported parrot.
incidence in North America of 4.6% and lower.7,10 Vasculitis is relatively uncommon in birds and
These differences may be the result of different is usually associated with a systemic, infectious
environmental and nutritional factors as well as process. Vasculitis has occasionally been report-
different histopathologic criteria. In one study,7 ed, with Mycobacterium species and Aspergillus
atherosclerosis was considered significant enough species being identified as the underlying etiologic
to be the cause of death in 26% of the affected organisms.21 Mycobacterial granulomatous arter-
birds. In birds submitted for necropsy from a itis is infrequent and has been diagnosed as
zoologic collection, 13.3% of birds with cardio- primarily affecting the major and coronary
vascular lesions had evidence of atherosclerosis.4 arteries in 6 psittacine birds (budgerigar [Melop-
Additionally, cardiac complications, such as sittacus undulatus], cockatiel [Nymphicus hollandi-
congestive heart failure, are frequently reported cus], Moluccan cockatoo [Cacatua moluccensis],
in clinical cases of atherosclerosis involving avian grey-cheek parakeet [Brotogeris pyrrhopterus],
species.11–15 Several avian models have also been white-capped pionus [Pionus senilis], and rosella
used to investigate cardiovascular disease, includ- [Platycercus species]).27 Aspergillus species often
ing Japanese quail (Coturnix japonica), pigeons colonize the vasculature adjacent to air sac
(Columba livia), chickens, and turkeys.16 Birds lesions, which may lead to thrombosis and
develop a central form of atherosclerosis, with the emboli.21 Filarioid worms have also been de-
great vessels at the base of the heart being the scribed in the great vessels, particularly in the
primary site of pathologic lesions.1,5,9 Atheroscle- pulmonary arteries and aorta, of various avian
rosis of the coronary, carotid, and other periph- species. These include filaria of the genus
eral arteries has rarely been documented in avian Splendidofilaria (Anatidae, American crow [Cor-
species.17–19 vus brachyrhynchos]; black-billed magpie [Pica
Among other vascular diseases reported in pica]; and house sparrow [Passer domesticus]),
birds, arterial aneurysm, which may be described Sarconema (Anatidae), Paronchocerca (Ciconii-
as a focal, blood-filled dilation of the arterial wall dae, Odontophoridae), Cardiofilaria (Cacatuidae,
communicating with the arterial lumen, has been birds of prey), and Chandlerella (Cacatuidae,
documented in various locations. The underlying Corvidae).28
cause of arterial aneurysms may be a weakened Vascular tumors are relatively rare in birds.
arterial wall or a local disruption of the artery of Although hemangiomas and hemangiosarcoma
origin, which in either case may rupture.20,21 are more common in their cutaneous form, they
Examples of aneurysms diagnosed in avian can also develop on the main arteries. A
species include a coronary aneurysm identified hemangiosarcoma arising from the right internal
in an umbrella cockatoo (Cacatua alba),18 which carotid was diagnosed in a double yellow-headed
apparently developed secondary to atherosclero- Amazon parrot (Amazona ochrocephala oratrix).29
sis, and a mycotic aortic aneurysm in a wild, A retrovirus, the avian hemangioma virus, has
female eider duck (Somateria mollissima).22 Aortic been reported to induce multifocal vascular
aneurysms are also found occasionally in poultry, tumors in chickens.30
specifically chickens and turkeys, and anecdotally Reports of congenital vascular diseases are
in ostriches (Struthio camelus).21,23 In turkeys, scarce in birds. A ventricular septal defect,
aortic aneurysms may develop as a consequence diagnosed in an umbrella cockatoo and in a
of aortic atherosclerosis leading to aortic dissec- Moluccan cockatoo, was associated with persis-
tion.24 Copper deficiency has also been suggested tent truncus arteriosus in the first case and with
as a cause of dissecting aneurysm and is aortic hypoplasia in the second.31 In these 2 cases,
considered rare in birds other than turkeys.21,23 the diagnosis was obtained by transcoelomic
Acute ischemic stroke is occasionally seen in echocardiography and confirmed at necropsy.
parrots.19 Causes are uncertain but atherosclero- Ventricular septal defects have also been docu-
sis, arterial thromboembolism, or systemic hyper- mented in chickens, turkeys, and in a tundra swan
tension, as seen in humans, are suspected. One (Cygnus columbianus).32–34
176 JOURNAL OF AVIAN MEDICINE AND SURGERY
Figure 2. Lateral radiographic view on a palm cockatoo (Probosciger aterrimus) positioned in right lateral
recumbency. 1, brachiocephalic trunks; 2, aorta; 3, pulmonary arteries; 4, pulmonary veins.
BEAUFRÈRE ET AL—AVIAN VASCULAR IMAGING 177
Figure 3. Ventrodorsal radiographic view on a The procedure is easy and inexpensive and can be
yellow-naped Amazon parrot. 1, brachiocephalic recorded for further analysis and measurements.
trunks; 2, aorta; 3, pulmonary arteries. For measurement, to account for different
degrees of magnification, a calibrated marker
vessels is occasionally present with atheroscle- should be kept in the field during fluoroscopic
rosis and is fairly specific for this disease.11 acquisition.
Despite the lack of objectivity, the major arteries Digital subtraction angiography is a fluoro-
may appear prominent on radiographs with scopic technique used in interventional radiology
central atherosclerosis.36 A case of mycotic to clearly visualize blood vessels in a dense soft
aneurysm in an eider22 and another of vascular tissue or bone environment. Images are produced
neoplasia in a double yellow-headed Amazon by subtracting a precontrast image from later
parrot29 appeared as large, soft tissue opacities images once the contrast medium has been
on the right side of the heart. Although introduced into the vascular system, which results
nonspecific, secondary cardiomegaly may be in visualizing only the contrast-filled vessels,
seen in birds with atherosclerosis.13,14 without the background. It considerably increases
Fluoroscopic angiography: Fluoroscopic angi- the outlines of the arteries and the detection of
ography can visualize the heart and vascular tree smaller arteries not seen with conventional
in real time. Under general anesthesia, the bird is angiography, specifically for extremities, such as
initially positioned in left lateral recumbency on a legs, wings, and the head, but the images tend to
fluoroscopy table. A bolus of nonionic iodinated be easily degraded by small motions and noise
contrast agent (2 mL/kg IV; iohexol 240 mg/mL; (Fig 5) (H. B. and R. P., unpublished data,
Omnipaque, GE Healthcare Inc, Princeton, NJ, November 2009). A preliminary, nonenhanced
USA) is injected, at a rate of 1–2 mL/kg per fluoroscopic image is recorded before administer-
second, through a catheter inserted into the ing a bolus of contrast medium and is digitally
basilic or medial metatarsal vein during video subtracted during the angiography procedure.
acquisition at a rate of 30 frames/s for the best The same bolus technique and a similar dose of
resolution. The same bolus is repeated to obtain contrast medium as used for regular fluoroscopic
the ventrodorsal view with the bird placed in angiography are used for digital subtraction
dorsal recumbency. The brachiocephalic trunks, angiography, except that this option is selected
aorta, pulmonary arteries, pulmonary veins, and in the machine. Reports of angiography applica-
caudal vena cava can be seen (Fig 4). The tions are still limited in birds. A coronary
brachiocephalic trunks and aorta can be seen aneurysm was diagnosed with angiography in an
pulsating with the heartbeats. Marked lumen umbrella cockatoo.18 Angiocardiography has also
changes can be observed during the cardiac cycle. been used clinically in a racing pigeon, 2 blue and
178 JOURNAL OF AVIAN MEDICINE AND SURGERY
Figure 5. Digital subtraction angiography of the skull in a barred owl (Strix varia) in ventrodorsal with a
craniocaudal and left to right orientation. 1, internal carotid arteries; 2, jugular veins; 3, external carotid artery; 4,
rete ophthalmicum; arrow, cerebral carotid artery.
gold macaws (Ara ararauna), and a whooper for the aortic root diameter have been reported.39–41
swan (Cygnus cygnus).13,36,37 The aortic outflow velocity has also been investi-
Ultrasonography: Echocardiography is, to gated, and reference ranges have been provided for
date, the most useful diagnostic test in avian several psittacine birds and raptorial species.39,40,42
cardiology. Well-established protocols have been Transesophageal echocardiography presents an
published for transcoelomic and transesophageal alternative to the transcoelomic approach and
echocardiography.38–41 Images are typically ac- offers greater details and the possibility of perform-
quired with an 8–11 MHz phased-array trans- ing an M-mode examination of the left ventricle and
ducer. The base of the aorta and the aortic valves the aortic root (Fig 7). The transverse and longitu-
can be imaged via the vertical view in transcoe- dinal views, with the transesophageal echocardiog-
lomic echocardiography but the resolution is raphy probe placed in a cranial position, provide
often poor (Fig 6). Nevertheless, reference ranges adequate details of the aortic root in most species.38
Contrast echocardiography has been evaluated in
several avian species (H. B. and R. P., unpublished
data, November 2009). Ultrasound contrast, con-
sisting of perflutren lipid microspheres (Definity,
Lantheus Medical Imaging Inc, North Billerica,
MA, USA), can be injected slowly, at a dose of
0.1 mL/bird IV, after the contrast is shaken with a
mechanical activating device (Vialmix, Lantheus
Medical Imaging) following manufacturer recom-
mendations. During imaging, a low acoustic power
(mechanical index, 0.2–0.3) should be used to
prevent disruption of the intravascular micro-
spheres. The small size of the microspheres allows
them to go through the pulmonary capillary bed
Figure 6. Transcoelomic echocardiography, vertical
and they can consequently be visualized in the left
view, in an eclectus parrot (Eclectus roratus). The
ultrasound of the heart is from caudal to cranial. The cardiac chambers. This is an advantage over the
ventral aspect of the bird is located on the right of the injection of a small volume of agitated saline, which
image. 1, left ventricle; 2, right ventricle; 3, liver; 4, only opacifies the right cardiac chambers but can
sternum; arrow, aortic root. also reveal intracardiac and extracardiac right to
BEAUFRÈRE ET AL—AVIAN VASCULAR IMAGING 179
Figure 7. Transesophageal echocardiography, cranial position, longitudinal view, M-mode on the aorta in a
military macaw (Ara militaris). 1, aorta; 2, left ventricle; 3, aortic wall; 4 aortic valve.
left shunts. The addition of contrast may help better from the right carotid artery that was diagnosed
delineate the endocardial border of the left ventricle with the help of endoscopy in a double yellow-
and provide more accurate measurements of the headed Amazon parrot.
diastolic and systolic ventricular internal diameter CT angiography: A CT examination provides
and aortic root. The contrast is slowly injected via a an excellent assessment of all major arteries and
peripheral catheter while the heart is imaged with their anatomy in psittacine and raptorial birds.
transcoelomic or transesophageal echocardiogra- The addition of contrast media greatly enhances
phy. The contrast lasts several minutes, and the the visualization of the arteries and veins and
microspheres can be destroyed by increasing the their lumen. The patient should be anesthetized
acoustic power if deemed necessary. No adverse for intravenous catheter placement and contrast
effects have been noticed with the use of perflutren administration. We suggest first performing a
in the birds imaged. whole body scout in orthogonal planes, followed
Endoscopy: Several endoscopic approaches
can provide impressive visualization of several
arteries. The standard left and right lateral
approaches43,44 lead to the visualization of the
vessels supplying the abdominal organs in the
abdominal air sacs, such as the abdominal aorta,
iliac arteries, mesenteric artery, renal arteries, the
caudal vena cava, and the ischiatic veins (Fig 8).
Additionally, the pulmonary arteries and veins
can be seen close to the base of the heart in the left
and right cranial thoracic air sacs (Fig 9). The
least commonly used interclavicular approach43,44
provides access to the base of the heart in the
interclavicular air sac and should be considered
the approach of choice to evaluate the great
arteries, carotid arteries, and base of the heart. At
this site, all the major and cranial arteries, such as
the brachiocephalic trunks, the ascending aorta,
the brachial arteries, the carotid arteries, the
pulmonary arteries, and the jugular veins, can
easily be identified (Figs 10 through 12). Accu- Figure 8. Coelioscopy through the left lateral ap-
mulation of fat at the base of the heart can proach in a red-tailed hawk (Buteo jamaicensis) placed
significantly impair the visualization of the in right lateral recumbency. The tip of the endoscope is
arteries through the interclavicular approach. located in the left abdominal air sac, and the view is
There is a report29 of a hemangiosarcoma arising looking down at the mesenteric artery.
180 JOURNAL OF AVIAN MEDICINE AND SURGERY
Figure 9. Coelioscopy through the left lateral approach in a great horned owl (Bubo virginianus) placed in right
lateral recumbency. The tip of the endoscope is located in the left cranial thoracic air sac craniodorsal to the heart,
showing the pulmonary artery (Pa) and pulmonary vein (Pv).
by a survey precontrast examination with a built- allow the time of arrival of the contrast medium
in abdominal scan protocol and the following (time to enhancement peak) at the aorta or other
parameters: standard algorithm in helical scan selected artery to be determined. The CT angiog-
mode, 1.25-mm slice thickness, 1.375 pitch, raphy (CTA) is then performed by the same scan
100 kilovolt (peak), and 150 mA. A dynamic, parameters as the survey precontrast series with
axial CT scan is recommended on a predeter- 3 mL/kg of contrast media administered over
mined slice with a single initial bolus of iohexol, 3 seconds. When performing the angiographic
1 mL/kg given over 1 second. The starting time of portion of the series, the start of the contrast
the dynamic scan must coincide with the initiation
of the contrast administration. Dynamic scans
Figure 13. Computed tomography angiography in a Hispaniolan Amazon parrot. (A) Section at the level of the
brachiocephalic trunks (arrows); (B) section at the level of the ascending aorta (arrow); (C) section at the level of the
abdominal aorta before the celiac bifurcation (arrow); (D) section at the level of the right pulmonary artery (arrow);
and (E) section at the level of the left pulmonary artery (arrow).
Figure 14. Computed tomography angiography in a tal view obtained through multiplanar reformatting
blue-fronted Amazon parrot (Amazona aestiva). Sagit- showing the caudal vena cava (arrow).
BEAUFRÈRE ET AL—AVIAN VASCULAR IMAGING 183
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