Rupture of the right auricle in broiler chickens

Abstract

This report describes a case of cardiac right auricle rupture (RAR) in a flock of 11 500 broilers that were 14 days old. The birds were housed at an altitude of 300 m, with an external temperature of −10°C and an internal temperature of 15°C. There was 3.6% mortality, due to sudden deaths, from 10 to 14 days of age. All necropsied birds had haemopericardium due to RAR at the point of the junction with the vena cava, and 85% of them had blood in the oral cavity and external acoustic meatus. The vena cava and its caudal branches, the intestinal vessels, and the sinus durae matris and sinus saggitalis were distended. Histological examination showed haemorrhages into the myocardium, degeneration of the cardiac muscle fibres, as well as oedema of the lungs and hypertrophy of the smooth muscle bundles of the parabronchial walls. Blood in the mouth of the broilers may have been due to haemoptysis, which in humans is caused mainly by mitral stenosis. In broilers, mitral stenosis and/or insufficiency, and left ventricular failure with consequent pulmonary hypertension (PH) were considered as possible triggers for right ventricular failure. The alarm reaction in hypoxaemia, due to secondary factors such as cold, caused tachycardia and tachypnoea, may have induced further elevation of PH, and acute myocardial infarction causing cardiac rupture and haemopericardium in this case. Hypertension and PH, due to possible mitral stenosis/insufficiency in association with acute myocardial ischaemia, were probably the determinant factors causing this acute episode. This opens the possibility that the RAR may be cardiogenic.

Rupture de l'oreillette droite chez le poulet de chair

Cet article décrit un cas de rupture de l'oreillette cardiaque droite (RAR) dans un troupeau de 11 500 poulets de chair âgés de 14 jours. Les animaux étaient élevés à 300 m d'altitude; la température extérieure du bâtiment était de −10°C et celle intérieure de 15°C. La mortalité était de 3,6%, correspondant à une mortalité subite de sujets âgés de 10 à 14 jours. Tous les animaux autopsiés présentaient un hémopéricarde du à une RAR au point de jonction de la veine cave; et 85% d'entre eux avaient du sang dans la cavité orale et dans le conduit auditif (acoustique) externe. La veine cave et ses branches caudales, les vaisseaux intestinaux le sinus de la dure-mère et le sinus longitudinal étaient distendus. L'examen histologique a montré des hémorragies au niveau du myocarde, une dégénérescence des fibres musculaires cardiaques, ainsi que de l'oedème des poumons, et une hypertrophie des paquets de muscles lisses des parois parabronchiques. Le sang dans la cavité buccale des poulets peut être due à une hémoptysie, qui chez l'homme est due principalement à une sténose mitrale. Chez les poulets de chair, la sténose et/ou insuffisance mitrale, et la rupture du ventricule gauche (LVF) avec pour conséquence une hypertension pulmonaire (PH) sont considérées comme pouvant être des facteurs déclanchant une rupture du ventricule droit (RVF). La réaction d'alerte de l'hypoxémie due à des facteurs secondaires tel le froid, a entraîné de la tachycardie et de la tachypnée qui, dans ce cas, peuvent avoir induit ultérieurement une élévation de la PH et une ischémie myocardique aiguë (AMI) causant une rupture cardiaque et un hémopéricarde. L'hypertension et la PH dues à une éventuelle sténose/insuffisance mitrale associé à l'AMI, ont été probablement les facteurs déterminants causant un épisode aigu. Ceci laisse à penser que le RAR soit cardiogène.

Ruptur des rechen Herzohrs bei Broilerküken

In diesem Bericht wird ein Fall von Rupturen des rechten Herzohrs in einer Herde von 11500 vierzehntägigen Broilern beschrieben. Die Broiler waren in einem Stall, der sich 300 Meter über dem Meeresspiegel befand, bei einer Innentemperatur von 15°C und einer Außentemperatur von −10°C untergebracht. Aufgrund von plötzlichen Todesfällen zwischen dem 10. und 14. Lebenstag wurde eine Mortalitätsrate von 3,6 % erreicht. Alle pathomorphologisch untersuchten Tiere wiesen bedingt durch eine Ruptur des rechten Herzohrs an der Verbindungsstelle zur Vena cava ein Hämoperikard auf und 85 % von ihnen hatten Blut in der Schnabelhöhle und im äußeren Gehörgang. Die Vena cava und ihre kaudalen Aufzweigungen, die intestinalen Gefäße, der Sinus durae matrix und der Sagittalsinus waren dilatiert. Bei der histologischen Untersuchung wurden Blutungen ins Myokard, Degeneration von Herzmuskelfasern sowie Lungenödem und Hypertrophie der glatten Muskelfasern der parabronchialen Wände festgestellt. Das Blut in den Schnäbeln der Broiler kann von einer Lungenblutung verursacht sein, wie sie beim Mensch hauptsächlich bei einer Mitralstenose auftritt. Bei Broilern wird eine Mitralstenose und/oder –insuffizienz und ein Herzlinksversagen mit nachfolgender pulmonaler Hypertonie als möglicher Auslöser für ein Herzrechtsversagen angesehen. Die Alarmreaktion einer Hypoxämie aufgrund von Sekundärfaktoren wie Kälte verursachte Tachykardie und Tachypnoe und kann eine weitere Erhöhung des Lungenhochdrucks und eine akute myokardiale ischaemia induziert haben, was in diesem Fall Herzruptur und Hämoperikard zur Folge hatte. Blut- und Lungenhochdruck, möglicherweise verursacht durch eine Mitralstenose/Insuffizienz in Verbindung mit myokardialer Ischaemie, waren wahrscheinlich die bestimmenden Auslösefaktoren für diese Todesfälle. Dies weist darauf hin, dass die Ursachen für die Ruptur des rechten Herzohrs kardiogen bedingt sind.

Rotura de la aurícula derecha en pollos de engorde

Este artículo describe un caso de rotura de la aurícula derecha del corazón (RAR) en un lote de 11,500 pollos de engorde de 14 días de edad. Se encontraban alojados a una altitud de 300 m, con una temperatura externa de −10^o C y 15^o C en el interior. Hubo un 3.6% de mortalidad, debido a muertes súbitas, de los 10 a los 14 días de edad. Todas las aves necropsiadas presentaron hemopericardio debido a RAR en el punto de unión con la vena cava, y el 85% de ellos presentaron sangre en la cavidad oral y en el meato acústico externo. La vena cava y sus ramas caudales, los vasos intestinales y los senos durae matris y saggitalis estaban distendidos. El examen histológico mostró hemorragias en el miocardio, degeneración de las fibras musculares cardíacas, así como edema de los pulmones e hipertrofia de los haces de músculo liso de las paredes de los parabronquios. La sangre en la boca de los pollos de engorde podría haber sido debida a la hemoptisis, que en humanos es básicamente debida a una estenosis mitral. En pollos de engorde, la estenosis y/o insuficiencia mitral, así como el fallo ventricular izquierdo (LVF) con la consiguiente hipertensión pulmonar (PH) se consideraron posibles factores desencadenantes del fallo ventricular derecho (RVF). La reacción de alarma en hipoxemia, debido a factores secundarios como el frío, causó taquicardia y taquipnea, podría haber inducido un incremento del PH, e ischaemia miocárdica aguda (AMI) causando rotura cardiaca y hemopericardio en este caso. La hipertensión y la PH, debido a la posible estenosis/insuficiencia mitral en asociación con AMI, fueron probablemente los factores determinantes que causaron este episodio agudo. Esto abre la posibilidad que el RAR sea cardiogénico.

Introduction

Hypoxaemia in birds triggers tachycardia and tachypnoea due to chemical mediators and may lead to hypertension (Broom & Kirden, 2004). It is commonly believed that in broilers the main factor causing a marked rise in venous pressure is right ventricular failure (RVF) caused by pulmonary hypertension (PH) (Hernantez, 1987; Julian, 1993). Some researchers have reported that the cause of increased pulmonary arterial pressure in hypoxaemic chickens may be the rise in left atrial pressure caused by mitral stenosis/insufficiency, and left ventricular failure (LVF), which elevates the pressure in pulmonary veins and arteries (Olkowski et al., 1998). Similar haemodynamic effects have been found to occur in humans/mammals with mitral regurgitation (Goutebenos & Petsas, 1984; Hamlin & Stokhof, 2004).

Spontaneous arterial ruptures in animals are rare (Hamlin & Stokhof, 2004). In birds, and particularly in male turkeys, there are reports of aortic rupture (Crespo & Shivaprasad, 2003) and, recently, of coronary artery rupture (Shivaprasad et al., 2004).

In humans, arterial aneurysms and their subsequent rupture, which causes haemopericardium, are a common disease, and the haemodynamic changes are well known (Goutebenos & Petsas, 1984). Myocardial ischaemia is triggered by a lack of oxygen to the heart, thereby causing myocardial necrosis, which is known as myocardial infarction. Cardiac rupture is a typical mechanical complication of acute myocardial infarction or ischaemia in humans, which causes haemopericardium, and is more frequent in patients with a history of hypertension (Reif & Silver, 1995; Exadactylos et al., 2002; Hutchins et al., 2002).

In this paper, a case of sudden death in 2-week-old broilers caused by right auricle rupture (RAR) is described. This paper is the first report of rupture of any cardiac chamber in chickens.

Materials and Methods

Twenty dead broilers, 14 days old, hatched from 54-week-old breeders, were submitted for necropsy. The mortality rate from 10 days of age was 3.6%. The chicks came from an open-sided broiler building housing 11 500 chicks, at an altitude of 300 m. The broiler density was calculated to be 15/m², and feed and water were available ad libitum. Food contained 48% corn, 10% wheat, 10% bran, 25% soya, 2.5% fish-meal, 1.8% marble-meal and 2.5% vitamins, amino acids, and so on. The external temperature was about −10°C, and the internal temperature about 15°C. The owner found the chicks dead on their backs, scattered inside the broiler house, and some of them had blood in their mouths and acoustic meatus.

Birds were necropsied and cultures from the lung, liver, and spleen were made on McConkey agar, 7% ovine blood agar and Sabouraud agar. Intestines were incubated for 24 h in selenite broth and then cultured to the aforementioned substrates. All culture plates were incubated at 37°C in 6% carbon dioxide and examined for bacterial growth at 24 and 48 h. Parasitological examinations were made of smears of the gastrointestinal tract by direct microscopic examination. Samples of feed and water were collected and analysed for Na⁺. Analysis for mycotoxins (aflatoxin B1, fusarenon X, nivalenol, acetyldeoxynivalenol and deoxynivalenol) was performed by liquid chromatography (Tsechpenakis & Gerakis, 2004). Samples of the liver, spleen, heart, lung and cerebrum from each chick was fixed in 10% neutral-buffered formalin and embedded in paraffin for histopathological examination.

Results

Necropsy showed good body condition in all chicks and their gizzards were full of feed. All 20 birds had haemopericardium (Figure 1), pale and slightly swollen livers, and some had prominent subcutaneous veins on their legs. Seventeen chicks (85%) had small amounts of clotted blood in the oral cavity (Figure 2a) and a plug of clotted blood in their external acoustic meatus. In their dura mater, all necropsied chicks had enlarged sinus durae matris and sinus saggitalis (Figure 2b). Bilateral pulmonary oedema and slight congestion was also observed. The legs of 14 birds (70%) were oedematous without fibrinous or caseous exudate in the joints. The heart showed pronounced pallor and the RAR occurred at the junction of the vena cava and the translucent thin-walled right auricle (Figure 2c). The kidneys were slightly pale and there was distension of the vena cava and its caudal branches, as well as the intestinal vessels.

Figure 1.  Haemopericardium, slightly swollen pale liver and prominent vessels in the legs of the bird on the right, in 14-day-old broilers.

Figure 2.  2a: Small amount of clotted blood in the oral cavity (arrow). 2b:Internal view of the cranium (ventral surface) with the dura mater showing enlargement of the sinus durae matris and the sinus saggitalis (black arrows). The cranium on the right has a normal dura mater. 2c: Rupture of the auricle of the junction with the vena cava and the translucent thin-walled right auricle (arrow).

No parasites were found in the gastrointestinal tract and no bacterium or fungus was isolated.

Histopathologically, there were multifocal haemorrhages ranging from mild to extensive in the myocardium and the adipose tissue. There was oedema of the interstitium and loss of cross-striation of cardiac muscle. Moreover, intrasarcoplasmic oedema located around the nuclei was observed. In the most severe cases, disorganization of scattered myocardial fibres was detected, characterized by fine granular and distorted eosinophilic sarcoplasm and pyknotic nuclei (Figure 3a). The latter was predominantly found in the subendocardial area while the former was deep in the myocardium. The lungs were congested and focally haemorrhagic. Pale-stained material thought to be oedema, red blood cells and debris were prominent in the lumen of the parabronchial lobules. Oedema was also seen around the blood vessels and in the interstitium. Additionally, there was hypertrophy of smooth muscle bundles of the parabronchial walls (Figure 3b). The vessels and the sinusoids of the liver were congested and a small number of haemorrhagic foci were found. Additionally, oedema, which caused expansion of the hepatic sinusoids and the spaces of Disse, was detected. Lipid-filled vacuoles in the cytoplasm of hepatocytes were evident in most of the cases examined, while a few foci of hepatocyte necrosis accompanied by mononuclear inflammatory cell infiltrates were also seen.

Figure 3.  3a: Heart with degeneration. Cardiac muscle cells with hyper-eosinophilic sarcoplasm and pyknotic nuclei (arrows). Haematoxylin and eosin, bar = 25 µm. 3b: Lungs with oedema and smooth muscle bundle hypertrophy. Intense congested lung with perivascular (arrows) and interlobular (arrowhead) oedema. Haematoxylin and eosin, bar = 100 µm. Inset: Red blood cells and debris in the lumen of a parabronchial lobule and hypertrophic smooth muscle bundles. Haematoxylin and eosin, bar = 25 µm.

The Na⁺ chemical analysis showed a concentration of 0.17% in feed and 3.8 mg/l in water. The concentration of aflatoxin B1 was less than 1.0 µg/kg in feed and the concentration of the other mycotoxins less than 50 µg/kg. Feed energy was 2820 kcal metabolizable energy/kg and protein was 20.2%.

Discussion

The modern broiler has been selected for rapid growth and has an improved growth rate of about 5% per year, thereby increasing oxygen requirements (Wideman et al., 2000). The high oxygen demand in fast-growing birds, combined with the inadequate vascular capacity for blood flow through the lungs is the most important primary factor in hypoxaemia, which induces PH at low altitude, with differences in susceptibility between the commercial broiler strains (Mirsalimi & Julian, 1991; Martinez et al., 1992; Jones, 1995; Wideman & Kirby, 1995; Wideman & French, 2000). Low temperature can cause, as a secondary factor, an increase of up to 185% in oxygen requirement (Gleeson, 1986; Julian et al., 1989; Huchzermeyer et al., 1989; Wideman & Tackett, 2000), which could have occurred in our case. Other secondary factors that can contribute to PH were not identified in the present study, such as breeder's age (Belly, 1995), toxic levels of Na⁺ and mycotoxins (Julian, 1987; Owen et al., 1995) and high proteins in feed (Dales & Villagres, 1986). Neither monensin nor other drugs were administered and no microscopic lesions of vitamin E deficiency were observed. Also, no evidence of liver fibrosis, cholangiohepatitis or amyloidosis, which can contribute to PH (Maxwell et al., 1986; Hernantez, 1987; Wilson et al., 1988; Julian, 2000), was found in the present case.

Some unusual macroscopic lesions for broilers were observed, such as the enlargement of the sinus durae matris and sinus saggitalis, the clotted blood in the oral cavity and external acoustic meatus, the haemopericardium and the RAR.

Hypoxaemia, which may have been caused by low temperature in this case, is a physiological stress factor and increases corticosteroid and epinephrine levels, leading to tachycardia, tachypnoea and hypertension (Broom & Kirden, 2004). The veins of the dura mater have no smooth muscle and have a stabile lumen (Mihail, 1985; Magras, 1986). The enlargement of those veins and the plug of clotted blood in the external acoustic meatus may caused by hypertension.

It is known that RVF induces a marked rise in venous blood pressure (Huchzermeyer & DeRuyck, 1986; Hernantez, 1987; Julian & Mirsalimi, 1992; Julian, 1993; Wideman et al., 1999). The enlargement of subcutaneous veins and the oedema in the legs, as well as the enlargement of the abdominal veins, was caused by RVF.

The blood in the mouth may have been due to haemoptysis, which was very difficult for the producer to observe in the house. In humans the main cause of haemoptysis is mitral stenosis (Goutebenos & Petsas, 1984). Pulmonary venous bleeding arises from the bronchial circulation and occurs primarily in association with pulmonary venous hypertension, particularly in association with LVF caused by mitral stenosis (Goutebenos & Petsas, 1984). Similar haemodynamic effects occur in almost all animals but particularly in dogs with mitral regurgitation (Hamlin & Stokhof, 2004). The blood in the mouth and/or the pallor of the heart may indicate that in this case there was mitral stenosis/insufficiency. This may support the hypothesis that mitral stenosis/insufficiency and LVF should be considered as possible triggers of RVF in broilers (Olkowski et al., 1998).

Haemopericardium was recently reported in a case of coronary artery rupture in turkeys (Shivaprasad et al., 2004). In the present case haemopericardium was caused by RAR. In humans the causes of cardiac rupture are the onset of acute myocardial infarction or ischaemia, blunt and penetrating cardiac trauma, primary cardiac infection, primary and secondary cardiac tumours, infiltrative diseases of the heart and aortic dissection (Goutebenos & Petsas, 1984; Reif & Silver, 1995; Exadactylos et al., 2002; Hutchins et al., 2002). Oxygen is the main factor determining blood flow in the myocardium. Myocardial ischemia can result from factors that reduce coronary blood flow, including spasm of the arteries, resistance of the blood vessels, aortic valve stenosis and regurgitation, increased right atrial pressure and increased oxygen demand of the myocardium. During periods of increased oxygen demand by the myocardium, the flow of blood in the endocardium is poorer than in the epicardium. In myocardial infarction, myocardial necrosis is more severe in the subendocardium than in the subepicardium. The lesions that we found in the myocardium were similarly disturbed.

Hypertension and elevated PH, due to possible mitral stenosis/insufficiency in association with acute myocardial ischaemia, were probably the determinant factors causing this acute episode. This opens the possibility that the RAR may be cardiogenic and a possible indication of mitral stenosis/insufficiency.

Translations of the abstract in French, Germany and Spanish are available on the Avian Pathology website.