ABSTRACT
Severe cardiomegaly with an atrial septal defect was discovered during necropsy of a subadult White-tailed Eagle (Haliaeetus albicilla) found dead in the wild. A thin membrane composed of fibromuscular tissue separated the left atrium into two chambers, most consistent with that described for cor triatriatum sinister (CTS) in other species. Seventeen months later, necropsy of an adult White-tailed Eagle again revealed CTS. This lesion has not been reported previously in raptors.
Heart defects occur in most species and can be either congenital or acquired. Congenital heart defects (CHDs) are related to anomalies in the fetal development of the heart. In birds, the total incidence of CHDs in chickens has been estimated at 0.6%, similar to the incidence of 0.5% in dogs and 0.5–0.8% in people (Taussing 1988). The most common CHD in chickens is ventricular septal defect (VSD; Siller 1968) followed by atrial septal defect (ASD), the corresponding lesion between the atrial compartments, and overriding aorta (Siller and Hemsley 1966). Congenital heart defects in wild birds are very rarely reported. We describe the congenital cardiac anomalies involving ASD and a left atrial fibromuscular membrane associated with severe cardiomegaly in two White-tailed Eagles (Haliaeetus albicilla), their etiology, and a comparison to similar lesions in other species.
The two eagles were found dead in the wild in the central and central east of Sweden, respectively, by citizens. The findings were separated both in time (17 mo) and location (more than 100 km). The birds were submitted for necropsy to the Department of Pathology and Wildlife Diseases at the National Veterinary Institute (Uppsala, Sweden) in conjunction with national law. Age was determined by plumage stage. All major internal organs were examined grossly and heart weight was recorded. Samples of heart, liver, lung, kidney, and spleen were fixed in 10% neutral buffered formalin and processed routinely to paraffin wax and 4-µm sections were stained with H&E. Selected sections of liver, lung, and heart were stained according to the Masson's trichrome method.
For the first eagle (E1), external and internal examination revealed that the bird was a subadult male White-tailed Eagle (4.8 kg) in poor nutritional condition and showing signs of moderate to severe decomposition. Macroscopic examination of the carcass revealed severe enlargement of the heart (Fig. 1A). Gross heart weight was 53.5 g, constituting 1.1% of the body weight. All four chambers of the heart were dilated, consistent with eccentric ventricular hypertrophy and severe cardiomegaly. By comparison, a subadult, healthy male White-tailed Eagle killed by a train had a normal heart with a weight of 38.3 grams (0.7% of the body weight). A centrally placed ASD was detected (Fig. 1D). In addition, a fibromuscular membrane was found in the left atrium, separating it into two distinct chambers (Fig. 1B, E). The membrane was composed of well-differentiated fibromuscular tissue with bundles of cardiomyocytes interlaced by variable amounts of connective tissue. The luminal compartments were demarcated by endothelial cells. The only communication between the chambers was a 3-mm opening at the dorsocaudal end of the septum. The right atrium communicated with the proximal atrial compartment of the left atrium through the ASD. Furthermore, the liver was enlarged and the lungs congested. The spleen, kidneys, intestines, and brain were unremarkable.
Cor triatriatum sinister in two White-tailed Eagles (Haliaeetus albicilla), denoted E1 and E2. ASD=atrial septal defect; E1=eagle 1; E2=eagle 2; fm=fibromuscular membrane; LA=left atrium; LV=left ventricle; RA=right atrium; RV=right ventricle. (A) Ventral view of the enlarged heart (*) in situ in E1 after removal of the sternum. Ruler in centimeters. (B) View of the fm (*) separating the LA into two compartments in the heart of E1 after formalin fixation. Forceps are inserted in the distal atrial compartment. (C) Formalin-fixed heart from E2. Note the fm (*) dividing the LA into two compartments. Plastic marker inserted in the distal atrial compartment. Ruler in centimeters, subdivided into millimeters and half millimeters. (D) The opened heart of E1 with the centrally placed ASD (*) observed between the atria (ostium secundum defect) with a probe inserted into the ASD. Each square on the background equals 1×1 cm. (E) A probe inserted into the left proximal atrial compartment in E1, demonstrating the fm (*). Each square on the background equals 1×1 cm. (F) Microscopic view of the fm dividing the atrium in E1. Masson trichrome stain. 100×. Bar=500 µm. (G) The fm dividing the atrium in E2. H&E stain. 100×. Bar=500 µm.
Cor triatriatum sinister in two White-tailed Eagles (Haliaeetus albicilla), denoted E1 and E2. ASD=atrial septal defect; E1=eagle 1; E2=eagle 2; fm=fibromuscular membrane; LA=left atrium; LV=left ventricle; RA=right atrium; RV=right ventricle. (A) Ventral view of the enlarged heart (*) in situ in E1 after removal of the sternum. Ruler in centimeters. (B) View of the fm (*) separating the LA into two compartments in the heart of E1 after formalin fixation. Forceps are inserted in the distal atrial compartment. (C) Formalin-fixed heart from E2. Note the fm (*) dividing the LA into two compartments. Plastic marker inserted in the distal atrial compartment. Ruler in centimeters, subdivided into millimeters and half millimeters. (D) The opened heart of E1 with the centrally placed ASD (*) observed between the atria (ostium secundum defect) with a probe inserted into the ASD. Each square on the background equals 1×1 cm. (E) A probe inserted into the left proximal atrial compartment in E1, demonstrating the fm (*). Each square on the background equals 1×1 cm. (F) Microscopic view of the fm dividing the atrium in E1. Masson trichrome stain. 100×. Bar=500 µm. (G) The fm dividing the atrium in E2. H&E stain. 100×. Bar=500 µm.
On histologic examination, a fibromuscular membrane was found at the site where the left atrium was divided (Fig. 1F). The lungs and liver were congested with an accumulation of eosinophilic homogenous material (fluid; a nonspecific finding) within alveoli as well as centrolobular fibrosis in the liver (visualized with Masson's trichrome).
The second eagle (E2) was an adult male, severely decomposed, but determined to be in average body condition, with normally developed musculature and moderate fat deposits within the body cavity, weighing a total of 3.9 kg. The macroscopic examination revealed an empty gastrointestinal tract and a pale, somewhat fragile liver of normal size with mild enlargement of the gallbladder. The heart weight was 63.2 g (1.6% of body weight) after formalin fixation compared to 48.6 g (0.8% of body weight) for a normal, formalin-fixed heart from an adult, female White-tailed Eagle killed by train collision. A fibromuscular membrane similar to that found in E1 was also found in the left atrium in this bird, again separating the atrium into two compartments (Fig. 1C) and again composed of cardiomyocytes with interwoven connective tissue (Fig. 1G). The communication between the compartments was a centrally placed, 20-mm opening, with no other anomalies of the heart detected. The spleen, lungs, and kidneys were unremarkable. Analysis for metals was performed, with levels exceeding lethal levels for lead in both the liver (9.20 parts per million wet weight) and kidney (20.3 parts per million). Histologically, the alveoli of the lungs contained homogenous material (fluid; unspecific finding) without fibrosis or presence of hemosiderin-containing histiocytes, suggesting chronicity. Liver, kidney, and spleen were unremarkable.
We describe two cases of wild raptors afflicted with cardiac anomalies. The most striking feature of E1 at first glance was the relative size of the heart compared to the coelomic cavity. The cause of cardiomegaly was determined to be the presence of cor triatriatum sinister (CTS) in conjunction with an ASD. The ASDs are further subdivided according to their position in the interatrial wall and thus their embryonic origin. In this particular case it would be most consistent with an ostium secundum defect (Webb and Gatzoulis 2006). Right-sided atrial dilation may be directly attributed to the ASD because of a left-to-right shunting phenomenon and eccentric ventricular hypertrophy. The ASD alone, however, did not explain the morphology of the left side of the heart, which may have been due to the presence of either the atrial fibromuscular membrane or to the intrinsic pathology of the myocardium. Cardiomegaly in lieu of CHDs in birds may be a sign of dilated cardiomyopathy (DCM). Cases of DCM have been well described in domestic turkeys (Meleagris gallopavo; round-heart disease), domestic chickens (Gallus gallus domesticus), and a case report in a Red-tailed Hawk (Buteo jamaicensis; Wu et al. 2003; Knafo et al. 2011). There were no signs of myocardial weaving or myocytolysis, which would be expected in the case of DCM. The presence of fibrosis along the margins of the hepatic central vein suggested the occurrence of intravital hepatic congestion, as would be expected in right-sided heart failure. The absence of ascites fluid indicated that the animal died before progression of the condition, possibly from onset of arrhythmia. Pathophysiologically, the mild chronic hepatic congestion was possibly an effect of the ASD causing left-to-right shunting or decreased right-sided systolic output from the dilated ventricle.
The presence of the fibromuscular membrane dividing the left atrium into two parts represented one of two diagnoses: CTS or a supravalvular mitral valve stenosis (SMS). In contrast to CTS, SMS denotes clear involvement of the mitral valve with subsequent obstruction.
Due to the orientation of the two membranes proximal to the mitral valve in the presented cases, the membranes separating the left atria were both clearly separated from the mitral valve. For that reason, CTS was deemed the more appropriate diagnosis. As a sequel, both CTS and SMS usually cause left ventricular inflow obstruction and congestive heart failure with chronic pulmonary edema (Fine et al. 2002). However, human cases of CTS presenting as adult onset atrial fibrillation have been described in several case reports (Ker 2013). Ker (2013) proposed that this finding might suggest that the defect in CTS is in fact a result of an anomaly affecting the whole atrial wall including the muscular parts. Death due to acute onset arrhythmia may explain the lack of chronic pulmonary congestion in E1. However, in E2, cause of death was likely not related to a cardiac anomaly at all but rather to a lead intoxication, likely an acute or subacute poisoning due to high levels of lead and a bird in a good body condition.
Although CTS is well characterized in people, it has not been described in raptors. In reports of CHD in birds, the majority of rare cardiac malformations have been observed in commercially kept chickens and include two cases of a double-outlet right ventricle, one case of cor trilocularis biatriatum, two cases with combined ASD and VSD (Siller and Hemsley 1966), and a case of anomalous venous connection where the pulmonary veins completely lacked connection to the left atrium (Aihara et al. 2013). Rare CHDs in other birds include the presence of a congenital right ventricular aneurysm in a Pigeon (Columba livia; Gal et al. 2012) and a case of mitral stenosis concurrent with subvalvular aortic stenosis in a duck (Mitchell et al. 2008). A VSD, along with aortic hypoplasia and a persistent truncus arteriosus, have been demonstrated in a Mollucan cockatoo (Cacatua moluccensis) and an umbrella cockatoo (Cacatua alba), respectively (Evans et al. 2001).
The embryonic origin of CTS is debatable. One theory is an abnormal development of the septum primum or the defective incorporation of the embryonic pulmonary vein into the atrium (Strickland et al. 2014). The condition is associated with other cardiac malformations in 24–80% of human cases (Ilhan et al. 2011). There may or may not be a communication between the chambers in CTS. The lesion is subdivided into groups I–III in human patients. Group I is defined by complete absence of communication between the chambers; group II consists of cases with narrow communication; and group III is defined by large communication between the atria (Strickland et al. 2014). Based on these criteria, E1 could be classified into group II and E2 into group III. Symptoms vary depending on the severity of the defect. Classically, the presence of the fibromuscular membrane in CTS creates a pressure gradient leading to increased pulmonary venous pressure with subsequent left-sided heart failure. Patients in group III may remain symptomless into adulthood (Ilhan et al. 2011). In our cases, E1 and E2 were subadult and adult, respectively, which suggested relative functionality of the heart.
The White-tailed Eagle population in Sweden has increased fivefold since the 1970s and currently amounts to more than 500 breeding pairs in inland and coastal Sweden (Herrmann et al. 2011). The ban of dichlorodiphenyltrichloroethane and other pesticides in the beginning of the 1970s is attributed to this increase because reproductive success and chick survival improved. The etiology behind development of cardiac anomalies in wild birds has been debated, but environmental toxins have been suggested to contribute to the problem. Cardiac anomalies have been observed among wild birds, including the Carolina Chickadee (Poecile carolinensis) and Tree swallows (Tachycineta bicolor), in polychlorinated biphenyl-contaminated areas (Dewitt et al. 2006). These anomalies include cardiac apical deformities, notches or indentations on the ventricular surface, roughness, ventricular thinning, and changes in overall heart shape. Dewitt et al. (2006) suggested cardiac morphology to be a sensitive indicator of polychlorinated biphenyl-contamination among birds. For this reason, environmental toxicity cannot be excluded as a contributing factor to the development of heart disease in these particular birds. A molecular cause has been suggested for mice and men, with a mutation in the gene for hyaluronidase 2 (Muggenthaler et al. 2017) supporting the theory of a heritable disease. The two eagles in this report were not found in close proximity to each other, but a familiar trait cannot be ruled out.
Although rare, we suggest that CTS should be considered as a differential diagnosis of wild birds, especially in raptors. Even when cardiomegaly is not observed, the findings we report testify that rare CHDs may be present, although not always attributable as the cause of death. The scarcity of reports may be an underestimation of their prevalence among wild birds.
We acknowledge the contribution of cardiologists Ingrid Ljungvall and Jens Häggström at the Swedish University of Agricultural Sciences in Uppsala, Sweden.