Bull Vet Inst Pulawy 53, 765-770, 2009

SOME ELEMENTS OF THE HEART STRUCTURE AND THE ASCENDING AORTA IN SELECTED SPECIES

OF BIRDS IN MORPHOLOGICAL AND MSCT AND MRI IMAGING ASPECTS

BARTŁOMIEJ J. BARTYZEL

Department of Morphological Sciences, Faculty of Veterinary Medicine, Warsaw University of Life Sciences - SGGW, 02-776 Warsaw, Poland

bartlomiej_bartyzel@sggw.pl

Received for publication June 15, 2009

Abstract

Eight hearts of birds of prey were used in the research: Northern Eagle Owl Bubo bubo (Linnaeus, 1758) (two hearts), White-tailed Sea Eagle Haliaeetus albicilla (Linnaeus, 1758) (four hearts), Steller's Sea-Eagle Haliaeetus pelagicus (Pallas, 1811) (one heart) and Northern Goshawk Accipiter gentilis (Linnaeus, 1758) (one heart). The collected material was analysed morphologically as far as the aortic valve and its adjacent structures were concerned. The hearts also underwent imaging with the use of a Multi-Slice Computed Tomography Scanner and 3 Tesla Magnetic Resonance Imaging scanner. A range of new terms was suggested to describe the aortic valve and its adjacent structures. The above-mentioned morphological and image examinations will enable better understanding of the biomechanics of the aortic valve of birds of prey and will allow us to relate basic research to clinical sciences.

Key words: birds of prey, heart, morphology, tomography, magnetic resonance.

Thirty-nine species of birds of prey belong to European fauna (26). They have become more and more susceptible to various types of diseases, including those of the cardio-vascular system. Fast technological progress of electroradiology in medicine provides new diagnostic opportunities also for other species of mammals and birds (6, 7, 15, 16, 23). Optimal use of morphological research and non-invasive imaging makes it possible to solve problems regularly occurring in clinical practice, including congenital heart defects, ischaemic heart disease (IHD) and other diseases of the cardiac muscle and the pericardium (4, 17). Such research with the use of modern imaging techniques while diagnosing various diseases are not usually used in veterinary medicine (24). In the future it would be valuable to relate morphological research with imaging in multislice computed tomography and functional (fMRI) with the use of functional magnetic resonance imaging, which will be able to determine the functioning of the cardiac muscle of birds belonging to different systematic groups while resting and in working conditions. Different conditions of the environment, various ways of moving and gaining feed, as well as accessibility to it, are connected with significant differences in expending energy, which also has an influence on the structure of the cardiovascular system (21).

The results of observations of particular structures of the heart of such rare birds of prey hardly occur in literature. Most information can be found in papers concerning results of microbiological and genetic research (11, 25). In this study an attempt has been made to relate the structure of the entrance of the aorta to various lifestyles. Some new anatomical terms have been suggested to define the morphology of the aortic valve and its adjacent structures in the heart of birds of prey. There have also been attempts to show the validity of using modern imaging techniques combined with morphological research. Such types of study will allow us to extend the scope of the diagnostics of the cardiovascular system of wild birds, which nowadays is unsatisfactory.

Material and Methods

The research concerned the ascending aorta and its adjacent structures of two hearts of the Northern Eagle Owl Bubo bubo (Linnaeus, 1758) – order Strigiformes, four hearts of the White-tailed Sea Eagle Haliaeetus albicilla (Linnaeus, 1758), one heart of the Steller's Sea-Eagle Haliaeetus pelagicus (Pallas, 1811),

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and one heart of the Northern Goshawk Accipiter gentilis (Linnaeus, 1758) – order Falconiformes (18).

The birds lived in the wild. Only the Steller's Sea-Eagle grew up in captivity. All the birds were adults (the causes of their death were unknown). The domestic population of the Northern Eagle Owl is estimated at 250-380 breeding couples, whereas the White-tailed Sea Eagle’s population is around 560 breeding couples (3, 8, 26). Considering the type of the research material (unusually rare) and the number of the examined individuals, the comparative study concerning age and sex was not conducted (macroscopically, the examined organs did not show any pathological or developmental changes). The research material was the part of a collection of exhibits from the Department of Morphological Sciences and the Warsaw Zoological Garden. The investigations were conducted in two stages:

I - Morphological research. The material was kept in 10% formalin. Each heart was irrigated in running water. Then, they were dried using filtering paper. The pulmonary trunk and the right and left pulmonary arteries were separated from the aorta. On such prepared material, a morphological analysis of the ascending aorta was conducted (the opening, valves of the aorta, initial openings of the coronary arteries). The attempts to analyse the left conus arteriosus and the left and right brachiocephalic trunks were also made. The ascending aorta and its adjacent structures were studied with the use of surgical microscopes (PZO: OpM-1 and Ecleris HaloLux 150) and a stereoscopic microscope (PZO: MsT-130). The photographic documentation was taken with a computer-linked camera (MikroOkular 3.0MP and i Sony HDR-SR11E). II - Imaging research. The study was conducted using Computed Tomography Scanner and magnetic resonance. Heart cavities were injected through the ascending aorta and the right atrium with Omnipaque TM 350 diluted in 0.9% saline solution (1:6). - A computed tomography study was conducted with an X-ray apparatus GE LightSpeed® PRO16 (KVP: 120.0 kv; Exposure: 5 mAs; Farm size: 411x411; Slice thick: 0.63 mm; Bit depih: 16). Only the Northern Eagle Owl’s heart had a volume rendering done in various planes with the use of the General Electric graphics station. - A magnetic resonance study was conducted using Simens Magnetom Trio A TIM System (Magnet: 3.0 TL; Farm size 160x160; TR: 12.7 ms; TE: 4.8 ms; ET: 1; Flip Angle 10.0; Slice Location: 52.93 mm; Slice Thick: 0.40 mm). Tomography and magnetic resonance were performed in AP projection in a long and transverse axis of the heart and were conducted at the Medical University of Warsaw and Bioimaging Research Centre of the Institute of Physiology and Pathology of Hearing in Kajetany. All imaging research was performed according to Digital Imaging and Communications in Medicine –

DICOM standard. Viewing and analysis of radiological documentation was conducted using DicomViewerFree by UniPacs Inc. Then it was converted into BMP format.

Results

Having passed the smooth-walled subaortic (left) conus arteriosus, conus arteriosus sinister, (a suggested name) the ascending aorta starts. It ascends together with the right brachiocephalic trunk. Directly below the opening of the aorta, just over the fibrous ring of the aorta, the left brachiocephalic trunk ascends in all the studied birds (Figs 1 - 4). In the aortic orifice there was the aortic valve, which in all the examined birds consisted of three cusps. The aortic bulb was composed of the following structures: the left aortic sinus (sinus aortae sinister), the right aortic sinus (sinus aortae dexter), and the posterior aortic sinus, (sinus aortae posterior) (suggested names). Each aortic sinus had four descriptive elements: free margin of the cusp, bottom of the sinus, inferior surface of the sinus, and the superior surface of the sinus, for which Latin terms have been suggested as: margo liber valvulae aortae, fundus sinus valvulae aortae, facies inferior valvulae aortae, facies superior valvulae aortae. All the mentioned structures were Ampulla - shaped. In the centre of every free margin of the cusp in Northern Eagle Owls, White-tailed Sea Eagles, and Northern Goshawk there were nodules of semilunar cusps, noduli valvulae semilunaris. The suggested names for them are as follows: the left nubule of the semilunar cusp - nodulus valvulae semilunaris sinistri, the right ventral nubule of the semilunar cusp - nodulus valvulae semilunaris dextri ventralis, the right dorsal nubule of the semilunar cusp - nodulus valvulae semilunaris dextri dorsalis (Fig. 5). Within one free margin of the cusp there were two lunules: left lunule of the semilunar cusp, lanula valvulae semilunaris sinistra, and right lunule of the semilunar cusp, lanula valvulae semilunaris dextra. Only the Steller's Sea Eagle did not seem to have nubules of the semilunar cusp. There was also only one lunule of the semilunar cusp with no secondary division. The valves of the all studied birds had three commissures and the suggested names for them are as follows: the left commissure, commissura sinistra, between the left semilunar cusp and the right dorsal semilunar cusp, the right commissure - commissura dextra between the dorsal semilunar cusp and the right abdominal semilunar cusp and the posterior, commissura posterior, between the left semilunar cusp and the right dorsal semilunar cusp (Fig. 6).

The initial openings of the left and right coronary artery in all the investigated birds were located on the surface of the superior sinus below the free margin of the cusp. Only in the case of a White-tailed Sea Eagle living in the wild did the left and right aortic sinus have three initial openings of the right and left coronary artery on the surface of the superior sinus above the free margin of the cusp.

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Fig. 1. White-tailed Sea Eagle’s heart I, II (top view). III (side view - open from the anterio-inferior surface) 1 - ascending aorta; 2 - right brachiocephalic trunk; 3 - left brachiocephalic trunk; 4 - left pulmonary artery; 5 - right pulmonary artery; 6 - left atrium; 7 - right atrium; 8 - left conus arteriosus; 9 - aortic valve; 10 - right atrioventricular valve; 11 - left atrioventricular valve.

Fig. 2. Volume rendering - Northern Eagle Owl’s heart in a computed tomography image (digital image). I (arterio-interior view); II (posterio-top view); III (arterio-inferior view); IV (side view). 12 - coronary groove; 13 - apex of the heart; 14 - left ventricle; 15 - right ventricle; 16 - interventricular septum; 17 - opening of pulmonary trunk; 18 - aortic orifice; 19 - left atrioventricular orifice (for other denotations see Fig. 1).

Fig. 3. White-tailed Sea Eagle - computed tomography image (digital image). I (longitudinal cross-section); II, III (transverse cross-section) - for other denotations see Figs 1, 2.

Fig. 4. White-tailed Sea Eagle’s heart - magnetic resonance image (digital image). I (longitudinal cross-section); II (transverse cross-section) - for other denotations see Figs 1, 2.

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Fig. 5. White-tailed Sea Eagle‘s aortic valve. I, II, III (side view); 20 - left nubule of the semilunar cusp; 21 - right ventral nubule of the semilunar cusp; 22 - free margin of the cusp; 23 - inferior surface of the sinus; 24 - bottom surface of the sinus; 25 - superior surface of the sinus; 26 - initial opening of the right coronary artery.

Fig. 6. The White-tailed Sea Eagle‘s aortic valve I, II (cut and half-open - anterior view); 27 - left commissure; 28 - right commissure; 29 - posterior commissure; 30 - left aortic sinus; 31 - right aortic sinus; 32 - posterior aortic sinus; 33 - left nubule of the semilunar cusp; 34 - right abdominal nubule of the semilunar cusp; 35 - right dorsal nubule of the semilunar cusp (for other denotations see Fig. 5). The computed tomography images of the studied hearts and the volume rendering of the heart of the Northern Eagle Owl clearly show structures adjacent to the aortic valve for example the aortic orifice and the left ventricle (Figs 2, 3). However, photos with the use of magnetic resonance imaging mostly show the aortic valve (Fig. 4).

Discussion

The presented medical and veterinary terminology comes from Latin and Greek. Getting to know the etymology of terms has not only a medical/historical value (5, 9, 13, 20); it allows us to create new terms defining data concerning the structure of birds’ heart, which has not been named until today. The aortic valve is the most frequently-described structure of the heart. It takes part in the flow of blood from the left ventricle to the aorta and it prevents blood from moving backwards during the ventricular diastole through a sudden closure of the semilunar cusps (1, 2, 19). Damage to the valves occurs mostly during rheumatic fever or infective endocarditis

(IE) and may result in, for example, ventricular ectasia occurring in ecstatic (14, 22). Changing human heart valves for artificial or natural ones achieved from pigs may be recommended in the case of their extensive narrowing (stenosis) or regurgitation, which cause serious haemodynamic disorders (12). Such diseases also occur in different species of birds; however, they are diagnosed sporadically. They require further morphological and clinical research.

The route of outflow of the blood from the left ventricle towards the aortic orifice is tube-shaped and can be defined as the subaortic (left) conus arteriosus in the anatomical and medical terminology. It is responsible for the outflow of the blood from the left ventricle towards the alveus of the aorta (2, 9). In the veterinary terminology of mammals and birds the term of the conus arteriosus is mentioned; however, it is not specified to which part of the heart it belongs (5, 20). Thus it has been suggested that the blanks should be filled with the following terms: the left conus arteriosus, (belonging to the left ventricle), conus arteriosus sinister, and the right conus arteriosus (belonging to the right ventricle), conus arteriosus dexter.

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The basic common feature of all the examined hearts of birds (apart from the Steller's Sea Eagle living in captivity), humans, and other mammals are the nubules of the semilunar cusps and lunules of the semilunar cusp located on the free margin of the cusp of the aortic valve. The presence of these structures may be evidence of better adaptation of the organ to the extensive effort individuals living in the wild. Mammals do not show the division into various surfaces of the aortic sinus. Prominences of the aortic wall visible in mammals are shallow in comparison with those of the same structures in the studied birds of prey. The biggest prominences could be observed in White-tailed Sea Eagles and the Northern Goshawk. It can be the evidence of the better efficiency of these structures forming the valvular system of the birds and is certainly a way of adaptation to various living conditions. In all the studied cases the initial openings of the left and right coronary artery were located on the surface of the superior sinus above the free margin of the cusp. Only in the case of the a White-tailed Sea Eagle living in the wild, the left and right aortic sinus had three initial openings of the right and left coronary artery. Such an example concerning an increased number of initial openings of the coronary arteries occurs frequently in humans and other mammals. It is also treated in clinical research as anatomically regular (1, 9). Similar research has been conducted in humans with the use of morphological and imaging methods. The latter applied to humans are an alternative to coronography. It is also a standard to analyse such reconstructions as MIP (maximum intensity projection), MPR (multiplanar reformated reconstruction), SSD (shaded surface display), and VR (volume rendering) using retrospective ECG-gated reconstruction (10, 27). In all the research it is possible to analyse the place of origin, progress, and the end of anomalies in the coronary arteries. In the research, volume rendering VR was used, which enabled to achieve three-dimensional images allowing reconstruction of their topographic relations, both ventricles and their adjacent structures. Such types of research are very rare. Such studies should be conducted, especially concerning endangered birds. Morphological research connected with imaging techniques of the heart of wild birds is a modern method of non-invasive diagnosis of the organ and its adjacent structures (24). They allow us to present the image of anatomical structures such as coronary vessels, heart ventricles, and the valvular system. In the nearest future it will evaluate their functionality (measurement of contractility or the ejection fraction of the heart). Research of this type falls within the domain of a new developing branch of veterinary sciences - clinical anatomy. The study should be definitely continued on a more numerous population of both wild and domestic birds. However, these initial observations already show the connection between the structure of the cardiovascular system and various lifestyles, which is very significant as far as cardiological diagnostics is concerned. These aspects are particularly important in the study on rare and endangered species.

Acknowledgments: Hereby I would like to thank Professor H. Kobryń for all his help, Dr A. Kruszewicz from the Warsaw Zoological Garden for making the research material accessible, Dr L. Bakoń from the II Department of Radiology, Medical University of Warsaw, for their help in MSCT image preparation, Professor B. Ciszek and Dr A. Koleśnik from Department. of Anatomy, Medical University of Warsaw for valuable advice, T. Wolak, MSc and K.P. Krasucki, MSc from the Institute of Physiology and Pathology of Hearing in Kajetany for their help in MRI image preparation and D. Krasuska for all her help.

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