Avian vascular imaging: a review.
Abstract: Vascular diseases in birds are not uncommon, according to findings from postmortem surveys. Although atherosclerosis affecting psittacine birds appears overrepresented, 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
Cardiovascular diseases are common in avian species. (1-5) Diagnostic imaging of the cardiovascular system is complicated by the small size of the patients, the fast heart rates of birds, the presence of air sacs, and the presence of the keel bone. The recognition of a high incidence of atherosclerosis in birds (1,2,6,7) has generated an interest in developing imaging modalities that will help identify lesions antemortem. Techniques have been developed to image the avian heart, but avian vascular imaging, itself, is still in its infancy. This article reviews the vascular diseases that have been documented in birds and the diagnostic imaging techniques that have been investigated in these species. We hope to stimulate the much-needed research in this field to develop current and future applications of avian vascular imaging modalities.
Avian vascular diseases
Although birds may present with a variety of vascular conditions, atherosclerosis is the most common vascular disease encountered in birds from various orders (ie, Psittaciformes, Accipitriformes, Falconiformes, Coraciiformes, Bucerotiformes, Struthioniformes, Galliformes, and Columbiformes). (5) Atherosclerosis is characterized by calcification, lipid retention, proteolytic injury, and a chronic inflammatory response of the arterial wall, resulting in a loss of arterial elasticity, a risk of atherosclerotic plaque rupture, or a narrowing of the vessel lumen. (1,8) The disease is well described in captive birds and has similarities to human atherosclerosis in that it is more prevalent in aging individuals fed an unbalanced diet. (1) Atherosclerosis has been reported in many birds in the Psittaciformes order, including Amazon parrots (Amazona species), African grey parrots (Psittacus erithacus), macaws (Ara species), and cockatoos (Cacatua species). (1) Anecdotally, the disease was diagnosed in several avian species that were maintained in zoological collections. (4,5,7) In psittaciform species, the reported incidence of atherosclerosis from recent postmortem surveys (2,6,9,10) varies between 4.6% to 91%. In pathologic studies of psittacine birds in Europe, a high incidence of atherosclerosis has been reported, with an approximately 91% incidence in African grey and Amazon parrots in one study and 13% in psittacine birds in another study. (2,6) This contrasts with the reported incidence in North America of 4.6% and lower. (7,10) These differences may be the result of different environmental and nutritional factors as well as different histopathologic criteria. In one study, (7) atherosclerosis was considered significant enough to be the cause of death in 26% of the affected birds. In birds submitted for necropsy from a zoologic collection, 13.3% of birds with cardiovascular lesions had evidence of atherosclerosis. (4) Additionally, cardiac complications, such as congestive heart failure, are frequently reported in clinical cases of atherosclerosis involving avian species. (11-15) Several avian models have also been used to investigate cardiovascular disease, including Japanese quail (Coturnix japonica), pigeons (Columba livia), chickens, and turkeys. (16) Birds develop a central form of atherosclerosis, with the great vessels at the base of the heart being the primary site of pathologic lesions. (1,5,9) Atherosclerosis of the coronary, carotid, and other peripheral arteries has rarely been documented in avian species. (17-19)
Among other vascular diseases reported in birds, arterial aneurysm, which may be described as a focal, blood-filled dilation of the arterial wall communicating with the arterial lumen, has been documented in various locations. The underlying cause of arterial aneurysms may be a weakened arterial wall or a local disruption of the artery of origin, which in either case may rupture. (20,21) Examples of aneurysms diagnosed in avian species include a coronary aneurysm identified in an umbrella cockatoo (Cacatua alba), (18) which apparently developed secondary to atherosclerosis, and a mycotic aortic aneurysm in a wild, female eider duck (Somateria mollissima). (22) Aortic aneurysms are also found occasionally in poultry, specifically chickens and turkeys, and anecdotally in ostriches (Struthio camelus). (21,23) In turkeys, aortic aneurysms may develop as a consequence of aortic atherosclerosis leading to aortic dissection. (24) Copper deficiency has also been suggested as a cause of dissecting aneurysm and is considered rare in birds other than turkeys. (21,23)
Acute ischemic stroke is occasionally seen in parrots. (19) Causes are uncertain but atherosclerosis, arterial thromboembolism, or systemic hypertension, as seen in humans, are suspected. One case (25) was reported in a yellow-naped Amazon parrot (Amazona auropalliata) and was associated with cerebral hemorrhage diagnosed by computed tomography (CT) scan. Another case (26) was diagnosed and followed by serial magnetic resonance imaging (MRI) in an African grey parrot.
Vasculitis is relatively uncommon in birds and is usually associated with a systemic, infectious process. Vasculitis has occasionally been reported, with Mycobacterium species and Aspergillus species being identified as the underlying etiologic organisms. (21) Mycobacterial granulomatous arteritis is infrequent and has been diagnosed as primarily affecting the major and coronary arteries in 6 psittacine birds (budgerigar [Melopsittacus undulatus], cockatiel [Nymphicus hollandicus], Moluccan cockatoo [Cacatua moluccensis], grey-cheek parakeet [Brotogeris pyrrhopterus], white-capped pionus [Pionus senilis], and rosella [Platycercus species]). (27) Aspergillus species often colonize the vasculature adjacent to air sac lesions, which may lead to thrombosis and emboli. (21) Filarioid worms have also been described in the great vessels, particularly in the pulmonary arteries and aorta, of various avian species. These include filaria of the genus Splendidofilaria (Anatidae, American crow [Corvus brachyrhynchos]; black-billed magpie [Pica pica]; and house sparrow [Passer domesticus]), Sarconema (Anatidae), Paronchocerca (Ciconiidae, Odontophoridae), Cardiofilaria (Cacatuidae, birds of prey), and Chandlerella (Cacatuidae, Corvidae). (28)
Vascular tumors are relatively rare in birds. Although hemangiomas and hemangiosarcoma are more common in their cutaneous form, they can also develop on the main arteries. A hemangiosarcoma arising from the right internal carotid was diagnosed in a double yellow-headed Amazon parrot (Amazona ochrocephala oratrix). (29) A retrovirus, the avian hemangioma virus, has been reported to induce multifocal vascular tumors in chickens. (30)
Reports of congenital vascular diseases are scarce in birds. A ventricular septal defect, diagnosed in an umbrella cockatoo and in a Moluccan cockatoo, was associated with persistent truncus arteriosus in the first case and with aortic hypoplasia in the second. (31) In these 2 cases, the diagnosis was obtained by transcoelomic echocardiography and confirmed at necropsy.
Ventricular septal defects have also been documented in chickens, turkeys, and in a tundra swan (Cygnus columbianus). (32-34)
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Other vascular diseases that may have significant health implications, but are poorly characterized in birds, are systemic hypertension and arterial thromboembolism.
Diagnosis of vascular diseases
Currently, little information is available regarding the diagnosis, treatment, and management of avian vascular diseases. Specifically, the diagnosis of atherosclerosis remains challenging. Antemortem diagnosis of atherosclerosis is primarily obtained in advanced cases, with severe calcification of the arteries, or in association with congestive heart failure. (11,14,35) A better knowledge and use of current and advanced imaging techniques to assess avian blood vessels may help in early diagnosis of avian vasculopathy in general and atherosclerosis in particular.
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Vascular diseases target the major arteries in birds and, fortunately, these arteries are the most accessible to diagnostic imaging. The blood vessels that are readily visible on imaging include the 2 brachiocephalic trunks, which are the largest arteries in most birds; the ascending aorta, which arises from the right brachiocephalic trunk; the abdominal aorta; the 2 pulmonary arteries and veins; and the 2 carotid arteries that start from the brachiocephalic trunks (Fig 1). Occasionally, the jugular veins, cranial and caudal vena cava, mesenteric artery, and some visceral arteries may also be visualized.
Radiography: Radiographs are often one of the first diagnostic tests performed in the avian patient. The central arteries can usually be well visualized and delineated (Figs 2 and 3). The brachiocephalic trunks, aorta, pulmonary arteries, and the pulmonary veins can usually be localized. On the ventrodorsal view, the ascending aorta can be visualized on the right of the midline (Fig 3). Central vessels are more conspicuous in large birds and in birds with hyperinflated air sacs. Radiographs are a relatively insensitive method of detecting vascular diseases, but significant calcification of the great vessels is occasionally present with atherosclerosis and is fairly specific for this disease. (11) Despite the lack of objectivity, the major arteries may appear prominent on radiographs with central atherosclerosis. (36) A case of mycotic aneurysm in an eider (22) and another of vascular neoplasia in a double yellow-headed Amazon parrot (29) appeared as large, soft tissue opacities on the right side of the heart. Although nonspecific, secondary cardiomegaly may be seen in birds with atherosclerosis. (13,14)
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Fluoroscopic angiography: Fluoroscopic angiography can visualize the heart and vascular tree in real time. Under general anesthesia, the bird is initially positioned in left lateral recumbency on a fluoroscopy table. A bolus of nonionic iodinated contrast agent (2 mL/kg IV; iohexol 240 mg/mL; Omnipaque, GE Healthcare Inc, Princeton, NJ, USA) is injected, at a rate of 1-2 mL/kg per second, through a catheter inserted into the basilic or medial metatarsal vein during video acquisition at a rate of 30 frames/s for the best resolution. The same bolus is repeated to obtain the ventrodorsal view with the bird placed in dorsal recumbency. The brachiocephalic trunks, aorta, pulmonary arteries, pulmonary veins, and caudal vena cava can be seen (Fig 4). The brachiocephalic trunks and aorta can be seen pulsating with the heartbeats. Marked lumen changes can be observed during the cardiac cycle. The procedure is easy and inexpensive and can be recorded for further analysis and measurements. For measurement, to account for different degrees of magnification, a calibrated marker should be kept in the field during fluoroscopic acquisition.
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Digital subtraction angiography is a fluoroscopic technique used in interventional radiology to clearly visualize blood vessels in a dense soft tissue or bone environment. Images are produced by subtracting a precontrast image from later images once the contrast medium has been introduced into the vascular system, which results in visualizing only the contrast-filled vessels, without the background. It considerably increases the outlines of the arteries and the detection of smaller arteries not seen with conventional angiography, specifically for extremities, such as legs, wings, and the head, but the images tend to be easily degraded by small motions and noise (Fig 5) (H. B. and R. P., unpublished data, November 2009). A preliminary, nonenhanced fluoroscopic image is recorded before administering a bolus of contrast medium and is digitally subtracted during the angiography procedure. The same bolus technique and a similar dose of contrast medium as used for regular fluoroscopic angiography are used for digital subtraction angiography, except that this option is selected in the machine. Reports of angiography applications are still limited in birds. A coronary aneurysm was diagnosed with angiography in an umbrella cockatoo. (18) Angiocardiography has also been used clinically in a racing pigeon, 2 blue and gold macaws (Ara ararauna), and a whooper swan (Cygnus cygnus). (13,36,37)
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Ultrasonography: Echocardiography is, to date, the most useful diagnostic test in avian cardiology. Well-established protocols have been published for transcoelomic and transesophageal echocardiography. (38-41) Images are typically acquired with an 8-11 MHz phased-array transducer. The base of the aorta and the aortic valves can be imaged via the vertical view in transcoelomic echocardiography but the resolution is often poor (Fig 6). Nevertheless, reference ranges for the aortic root diameter have been reported. (39-41) The aortic outflow velocity has also been investigated, and reference ranges have been provided for several psittacine birds and raptorial species. (39,40,42) Transesophageal echocardiography presents an alternative to the transcoelomic approach and offers greater details and the possibility of performing an M-mode examination of the left ventricle and the aortic root (Fig 7). The transverse and longitudinal views, with the transesophageal echocardiography probe placed in a cranial position, provide 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, consisting 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 recommendations. During imaging, a low acoustic power (mechanical index, 0.2-0.3) should be used to prevent disruption of the intravascular microspheres. The small size of the microspheres allows them to go through the pulmonary capillary bed and they can consequently be visualized in the left cardiac chambers. This is an advantage over the injection of a small volume of agitated saline, which only opacities the right cardiac chambers but can also reveal intracardiac and extracardiac right to left shunts. The addition of contrast may help better delineate the endocardial border of the left ventricle and provide more accurate measurements of the diastolic and systolic ventricular internal diameter and aortic root. The contrast is slowly injected via a peripheral catheter while the heart is imaged with transcoelomic or transesophageal echocardiography. The contrast lasts several minutes, and the microspheres can be destroyed by increasing the acoustic power if deemed necessary. No adverse effects have been noticed with the use of perflutren in the birds imaged.
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Endoscopy: Several endoscopic approaches can provide impressive visualization of several arteries. The standard left and right lateral approaches (43,44) 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 approach (43,44) 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). Accumulation of fat at the base of the heart can significantly impair the visualization of the arteries through the interclavicular approach. There is a report (29) of a hemangiosarcoma arising from the right carotid artery that was diagnosed with the help of endoscopy in a double yellow-headed Amazon parrot.
CT angiography: A CT examination provides an excellent assessment of all major arteries and their anatomy in psittacine and raptorial birds. The addition of contrast media greatly enhances the visualization of the arteries and veins and their lumen. The patient should be anesthetized for intravenous catheter placement and contrast administration. We suggest first performing a whole body scout in orthogonal planes, followed
by a survey precontrast examination with a built-in abdominal scan protocol and the following parameters: standard algorithm in helical scan mode, 1.25-mm slice thickness, 1.375 pitch, 100 kilovolt (peak), and 150 mA. A dynamic, axial CT scan is recommended on a predetermined slice with a single initial bolus of iohexol, 1 mL/kg given over 1 second. The starting time of the dynamic scan must coincide with the initiation of the contrast administration. Dynamic scans allow the time of arrival of the contrast medium (time to enhancement peak) at the aorta or other selected artery to be determined. The CT angiography (CTA) is then performed by the same scan parameters as the survey precontrast series with 3 mL/kg of contrast media administered over 3 seconds. When performing the angiographic portion of the series, the start of the contrast administration should preceed the start of scanning by the time to the enhancement peak previously determined by the dynamic axial CT. (45) Additional reconstruction series with thinner slices (eg, 0.625 mm) and a soft tissue algorithm are recommended.
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An injection pump may be used, but it can be problematic with the small injection volume required in birds, and we prefer manual injection. In small to medium sized birds, because of their fast circulation of contrast in the vascular tree, the time to enhancement peak in the aorta is very fast, and it is recommended that the CTA scan be performed immediately after administration of the contrast. (45) Reference ranges have been published (45) for arterial diameters of the brachiocephalic trunks, ascending aorta, abdominal aorta, and pulmonary arteries (Fig 13). The use of a mediastinal window or a manual angiography window is recommended for more accurate and repeatable measurements. A previously described (45) technique was performed with a 16-slice, multidetector CT; and the exact timing for injection and acquisition of images recommended for CT machines that are not 16-slice will likely vary, as will the resolution of the image.
Computed tomography angiography also allows the caudal and cranial vena cava (Fig 14), the carotid arteries, the mesenteric artery and some of its ramifications, and several of the smaller arteries of the avian body to be visualized. In addition, 3-dimensional reformatting and segmentation on the heart and central arteries are possible and may help in the diagnosis of aneurysm and congenital vascular anomalies (Fig 15). Although no case report, to our knowledge, documents the use of CTA in a clinical context in birds, its use may prove to be invaluable in assessing arterial luminal stenosis, aneurysm, dilatation of the arteries, and calcification of the walls. In humans, CTA remains one of the preferred methods for measuring arterial diameters, and multiple studies have investigated its accuracy. (46-49) High-resolution CTA has also been used in birds to describe normal vascular anatomy. (50)
Magnetic resonance imaging: Magnetic resonance angiography has not been investigated in birds so far. In a study on MRI in healthy pigeons, the hepatic and renal vasculature were discernable. (51) However, motion artifacts prevented adequate imaging of the heart. Additionally, MRI was not of good diagnostic value for the vascular system because of the fast circulation of contrast media (gadolinium) through the vasculature and the small size of the vessels to be investigated. To achieve a diagnostic quality image in such small vessels, higher magnetic fields would be required (3 T or higher), which further limits its clinical use.
A variety of imaging modalities are available for the avian vascular system. These techniques are presently underused, despite a significant incidence of atherosclerosis in the captive bird population. Angiography by fluoroscopy and CT scan may become the diagnostic tests of choice to better characterize gross vascular lesions. Endoscopy by the interclavicular approach allows direct visualization of the great arteries but is more invasive and may be impaired by fat stores in overweight animals. More studies and clinical reports are needed to document the usefulness of vascular diagnostic imaging in birds. As avian vascular imaging finds inspiration and application from human cardiovascular imaging and pediatric cardiology, the span of diagnostic tests and clinical applications will undoubtedly expand. In the near future, the use of high technology imaging systems, such as high-speed CTA, magnetic resonance angiography, smaller and higher frequency transesophageal ultrasound probes, and intravascular ultrasound probes will hopefully advance the resolution and details of the small arteries of avian patients and improve the sensitivity available for diagnosing vascular pathologic processes.
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Hugues Beaufrere, Dr Med Vet, Romain Pariaut, Dr Med Vet, Dipl ACVIM, Dipl ECVIM-CA, Daniel Rodriguez, MVZ Esp, Dipl ACVR, and Thomas N. Tully, DVM, MS, Dipl ABVP (Avian), Dipl ECZM
From the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70803, USA.