Cardiomyopathy and right-sided congestive heart failure in a red-tailed hawk (Buteo jamaicensis).
Key words: cardiomyopathy, congestive heart failure, cardiac troponin I, avian, raptor, red-tailed hawk, Buteo jamaicensis
An approximately 15-year-old female red-tailed hawk (Buteo jamaicensis) was presented to the University of Georgia Veterinary Teaching Hospital with a 10-day history of dyspnea and a 3-day history of anorexia and vomiting. The bird was part of a university wildlife center raptor collection, had been in captivity for 11 years, and served as an educational animal. Its diet consisted of rats, mice, quail, and day-old chicks and was supplemented daily with a multivitamin. Previously, it had been a fit, flighted bird with an unremarkable medical history and maintained a flight weight of 1.4 kg.
Dyspnea was first observed by the caretakers 10 days before presentation. Severe distension of the caudal coelom was evident on physical examination. Although the bird's weight at that time was 1.6 kg, the caretakers noted that the weight gain was not reflected in the body condition (body condition score 3/9), because the keel was moderately prominent. The referring veterinarian examined the hawk one day after the onset of clinical signs and made a presumptive diagnosis of aspergillosis. Based on the clinical presentation, treatment with trimethoprim-sulfamethoxazole (60 mg/kg PO q12h) and itraconazole (10 mg/kg PO q12h; Sporonox, Ortho-McNeil-Janssen Pharmaceuticals Inc, Raritan, N J, USA) was initiated. These medications were taken well in food for 5 days until the bird became acutely anorexic and began to vomit. The hawk was referred for further evaluation and treatment.
The hawk was tachypneic and dyspneic upon presentation to the University of Georgia Veterinary Teaching Hospital. It was immediately placed in an oxygen cage and, after 20 minutes, was still tachypneic but less dyspneic. The hawk was anesthetized with isoflurane for physical examination and collection of blood samples for hematologic and serologic testing. Results of physical examination revealed a phthisical right eye and a white 1-2-mm plaque just inside the rima glottidis on midline. On cardiac auscultation, an underlying regular rhythm with occasional premature beats was noted. No heart murmur was ausculted, but heart sounds were muffled and difficult to assess. Pulmonary crackles were heard dorsally and bilaterally, and the coelom was markedly distended, with a palpable fluid wave and no masses. The bird's weight at admission was 1.3 kg.
The hawk was treated with crystalloid fluids (Normosol-R, 30 mL SC; Hospira Inc, Lake Forest, IL, USA), a canned dog food slurry (40 mL per feeding, Hills a/d, Hill's Pet Nutrition, Topeka, KS, USA) fed via crop tube, and furosemide (2 mg/kg IM), as well as the previously prescribed trimethoprim sulfa and itraconazole, all given q12h. Medical therapy and supportive care were continued for 2 days, at which time the bird was breathing more comfortably at rest in an oxygen cage. Dyspnea recurred when the hawk was restrained for treatment and examination. The weight during treatment with furosemide was 1.2 kg.
A blood sample was submitted for a complete blood cell count (CBC), serum biochemical analysis, measurement of vitamin E, selenium, lead, zinc, and taurine levels, and serologic testing for West Nile virus. Results of the CBC and biochemical analysis were unremarkable except for hypoproteinemia (plasma protein, 3.0 g/dL [reference range, 3.9-6.7 g/dL]). (1) The vitamin E level (9.39 [micro]g/mL [reference range, 16.7-46.1 [micro]g/ mL]) (2) was decreased. The blood selenium level was 0.199 ppm; however, because reference ranges for selenium levels in raptorial species have not been established, the significance of this value was unknown. The whole blood taurine level (9850 nmol/mL) was not consistent with a deficiency when using the reference range for domestic cats (normal, >60 nmol/mL). (3) The blood lead level was 0.1 ppm (10 [micro]g/dL) (reference range, <0.4 ppm [40 [micro]g/dg]) (4) and was considered normal. The blood zinc level was slightly high (2.3 ppm [reference range, <2 ppm). (4) Results of serologic testing for West Nile virus revealed a low titer not consistent with clinical infection; however, a second (convalescent) sample was not submitted.
A sample of the coelomic effusion was submitted for cytologic evaluation. The fluid was classified as a mixed inflammatory exudate, with a differential cell count of 41% heterophils, 55% macrophages, and 4% eosinophils, with minimal blood. The macrophages were large and foamy, and contained many discrete, round, nonstaining vacuoles, most consistent with lipid. The plasma cardiac troponin I (cTnI) level measured by a hand-held blood chemistry analyzer (i-STAT, Heska Corporation, Loveland, CO, USA) was 0.03 ng/mL, whereas the value measured by a sandwich enzyme-linked immunosorbent assay (ELISA) immunoassay (Beckman Coulter Delta X, Beckman Coulter Inc, Allendale, N J, USA) on serum sample was 0.4 ng/mL. Reference ranges for avian cTnI have not been established. Therefore, 4 additional red-tailed hawks with no evidence of cardiac disease, similarly anesthetized with isoflurane and oxygen by mask, were opportunistically tested (Table 1). One bird was from a zoological collection, and the other 3 were wild birds with evidence of trauma (soft-tissue wound, ulnar fracture, and head trauma, respectively) brought to the veterinary hospital for care. These birds were determined to be systemically healthy other than their respective soft-tissue and orthopedic injuries. The cTnI value measured by i-STAT in the affected hawk was similar to values in the 4 red-tailed hawks, whereas the value obtained by immunoassay was 3-20 times higher.
Results of whole-body radiographs taken with the bird under general anesthesia approximately 24 hours after presentation revealed that the cardiac silhouette was enlarged and lobulated (Fig 1). Enlargement of the hepatic shadow was indicative of hepatomegaly, given the lack of significant distension of the gastrointestinal tract. The lobulated soft-tissue structure superimposed over the proventriculus on the lateral view likely represented lobulated extension of the enlarged liver. The cranial pole of the renal-gonadal shadow was enlarged and bulbous on the lateral projection, which suggests either renomegaly or gonadomegaly. Four metallic shot pellets were evident in the left extra-coelomic tissues, and a malunion fracture of the distal third of the right radius was present. Findings of an enlarged cardiac silhouette and hepatomegaly were compatible with cardiac disease and right-sided congestive heart failure.
[FIGURE 1 OMITTED]
Ultrasound examination of the coelomic cavity revealed a large amount of free anechoic fluid. There was generalized hepatomegaly with prominent hepatic veins; multiple well-defined hyperechoic loci were also noted within the liver. The right atrium and right ventricle appeared severely dilated. The presence of free anechoic fluid, hepatomegaly, hepatic venous enlargement, and right-sided cardiomegaly were suggestive of right-sided congestive heart failure. The hyperechoic foci in the liver were suggestive of nodular hyperplasia, although neoplasia could not be ruled out. Echocardiography was recommended.
Results of echocardiography revealed right atrial and right ventricular dilatation (Fig 2). The right ventricular chamber appeared markedly dilated, with a transverse measurement of 23.3 mm during diastole and 20 mm during systole, and a longitudinal measurement of 28 mm during diastole and 24.4 mm during systole (Table 2). All values were increased compared with those of normal female diurnal raptors. (5) The right ventricular free wall and interventricular septum appeared thin and hypokinetic. The left heart chambers subjectively appeared diminished in size, however, this was difficult to assess critically given the severe degree of dilatation of the adjacent right heart chambers. The left ventricular chamber transverse measurement was 8.7 mm during diastole and 9.8 mm during systole, and the longitudinal measurement was 21.9 mm during diastole and 19.1 mm during systole (Table 2). All values for the left ventricle were within reference ranges for normal female diurnal raptors. (5) No valvular abnormalities or congenital heart defects were observed. A large volume of coelomic effusion was seen. A 6-lead electrocardiogram (Fig 3) was also performed and revealed a relatively slow ventricular tachycardia, at approximately 160 beats per minute. Based on these and previous clinical findings, the coelomic effusion was presumed to be caused by primary cardiac disease, and a diagnosis of right-sided congestive heart failure was made. Euthanasia was elected because of the severity of the bird's clinical signs, the advanced stage of the disease, and the requirement for intensive lifelong care.
Postmortem examination confirmed this hawk to be a female in good body condition. A large amount (42 mL) of transparent yellow fluid was present within the coelomic cavity. The heart was markedly enlarged (Fig 4), with marked dilatation of the right ventricular lumen (1.5 cm in diameter), thinning of the right ventricular wall (0.1-cm thick), and mild dilatation of the left ventricle (0.6-cm diameter, 0.5-cm thick; Fig 5). The liver was moderately enlarged, likely caused by chronic passive congestion from right-sided heart failure. The right kidney had a focally extensive area in the cranial third that was pale tan and swollen. On histologic examination, this area was associated with renal coccidiosis, with no tissue reaction. The liver had mild hepatic lipidosis and an area of focal fibrosis caused by a shot-pellet foreign body. The myocardium appeared histologically normal. There was no growth on aerobic culture of samples from the heart or liver, possibly as a result of ongoing antimicrobial therapy in this animal, and no gross or microscopic evidence of fungal infection in this hawk.
[FIGURE 2 OMITTED]
In this report, we describe the clinical presentation and diagnostic workup of a captive red-tailed hawk with cardiomyopathy. This hawk was not presented until the disease process was severe; however, if a diagnosis had been made earlier in the course of the disease, it may have been possible to successfully treat or mitigate clinical signs. Comparison of cTnI levels of this hawk with those from normal red-tailed hawks were of little diagnostic value in this case. However, as the use of these assays are investigated further in birds, these data may become part of a larger data set that allows for validation of troponin assays in birds and possible early detection of myocardial injury or dysfunction.
Cardiac disease in nondomestic birds is seldom reported. In a retrospective study of nearly 3400 raptors, no cases of cardiovascular disease as a cause of morbidity or mortality were reported. (6) Birds have a cardiovascular system designed for flight and to meet the high metabolic needs of these animals. Therefore, a captive bird living in a potentially abnormal environment, experiencing restricted activity, and being fed a substandard or unnatural diet may be predisposed to developing cardiovascular disease. (7) Clinical presentations of myocardial disease in birds are varied; however, the disease is generally characterized by poor contractility, chamber enlargement, and arrhythmias. (7)
[FIGURE 3 OMITTED]
Right-sided congestive heart failure in this bird appears to have resulted from a form of cardiomyopathy that predominantly if not completely affected the right side of the heart. Other structural cardiac causes of right-sided cardiac chamber dilatation without right ventricular hypertrophy, such as an atrial septal defect or tricuspid valvular regurgitation (congenital or acquired), were not apparent during the echocardiogram. Pulmonic stenosis and pulmonary hypertension could not be ruled out during this study; however, both would be expected to include some degree of right ventricular hypertrophy if severe enough to lead to heart failure. Anomalous pulmonary venous return is a rare congenital heart defect in other species, which could produce these echocardiographic findings. Although contrast angiocardiography would be required for definitive diagnosis, this defect was considered highly unlikely.
Both primary (intrinsic heart muscle disease) and secondary cardiomyopathy (with an identifiable underlying extracardiac cause) were considerations as the cause of heart failure in this hawk. Of the described primary cardiomyopathies, arrhythmogenic right ventricular cardiomyopathy would seem most likely based on the echocardiographic and gross necropsy findings. However, the characteristic histopathologic lesions were not seen (particularly fatty or fibro-fatty replacement of right ventricular myocardial tissue). In mammals, dilated cardiomyopathy typically includes 4-chamber or predominantly left-sided cardiac chamber dilatation, with primarily left ventricular systolic dysfunction; therefore, this was considered unlikely as well. Still, a form of this condition that manifests differently in avian species cannot be ruled out. Myocardial failure in birds has been described as mainly right sided? It has even been asserted that isolated left-sided myocardial failure is rare, (5) which suggests that this hawk's right-sided disease might be an expected presentation for cardiomyopathy in birds. Limited data exist that describe the clinical presentation and diagnosis of cardiomyopathy in raptorial species. Therefore, an unclassified idiopathic cardiomyopathy remains a distinct possibility.
[FIGURE 4 OMITTED]
Secondary cardiomyopathies of infectious, inflammatory, neoplastic, toxic, nutritional (vita min E selenium), or other metabolic etiology (round heart disease) are all potential causes of disease in this hawk. Infectious causes include Escherichia coli, Pasteurella species, polyomavirus, West Nile virus, proventricular dilatation disease (bornavirus), Toxoplasma gondii, and Sarcocystis species. (7) This bird did not have any microscopic lesions indicative of a specific cause of the right-sided cardiac dilatation. Right-sided myocardial failure in birds has been observed secondary to chronic extracardiac diseases, such as pulmonary mycosis. However, no evidence of infection or other systemic disease was observed, and hypertrophy of the right ventricle was not appreciated as would be expected with pulmonary hypertension. Furthermore, an infectious cause is unlikely, because no inflammation was present in the myocardium, and results of culture and serologic testing were negative. In addition, a nutritional cause, such as vitamin E-selenium deficiency is unlikely, despite low values in this hawk, because there was no evidence of myocyte degeneration or necrosis in the heart.
[FIGURE 5 OMITTED]
Round heart disease, a spontaneous and rapidly fatal cardiomyopathy in otherwise healthy poultry, was first described in chickens in Denmark in 1936 and in the United States in 1958. (8) In 1962, the disease was described in turkeys, (9) and it has been defined as a thinning of the right ventricle and subsequent ventricular enlargement in 1-4-week-old turkey poults. In older turkeys, the syndrome is characterized by left ventricular enlargement." Young poults frequently have varying amounts of ascites, however, this is an inconsistent finding in older turkeys with left-sided disease. In chickens, the disease is characterized by more degenerative changes of the myocardium. (8) The cause of the disease in turkeys and chickens remains unclear; however, implicated risk factors are environmental stress, dietary deficiencies, enzyme deficiencies, genetic variables, viral infection, hypoxia, and metabolic or immunologic disease.
Husbandry for the hawk we described was adequate for birds of prey in captivity. Despite satisfactory conditions and supplementation with a daily multivitamin, the bird may have had vitamin E and selenium deficiencies, because the blood vitamin E levels were low, based on research results in birds of prey. (2) Published reference ranges for psittacine birds and monogastric mammals are from 2 to 10 [micro]g/mL (10); however, studies that assessed the impact of diet on alpha-tocopherol levels in falcons suggest that this bird might have had a deficient level of vitamin E. (2) Vitamin E deficiency is defined histologically by pale muscle, edema of the cerebellum, and hemorrhage, (11) which were not present in this bird. In adult monogastric mammals, the reference range for blood selenium is 0.1-0.25 ppm. (12) In a survey of blood selenium levels in predatory birds in California, 14 red-tailed hawks had blood selenium levels that ranged from 1.9 to 4.1 ppm. (13) In poultry, hepatic selenium concentrations are considered adequate between 0.35 ppm and 1 ppm, and inadequate below 0.35 ppm. (14) Blood selenium levels were potentially inadequate in the hawk we described compared with normal hepatic selenium concentrations in poultry and with blood selenium levels reported in wild red-tailed hawks. Vitamin E-selenium deficiency can cause myocardial lesions in poultry (15) but more commonly causes encephalomalacia in affected birds. (16) None of these lesions were observed in this hawk. The clinical significance of the levels in this hawk is unclear because a comparison between blood and liver selenium levels may be inappropriate, and the small sample size in the report of red-tailed hawks is inadequate to establish a reference range. Furthermore, no myocardial or hepatic lesions to support selenium deficiency were present.
An additional dietary influence on the development of congestive heart failure is sodium. Even a moderate increase in dietary sodium can cause a secondary increase in blood volume, which, in only 1 week, can cause right-sided congestive heart failure in birds. (15) In addition, any increase in oxygen demand or decrease in oxygen delivery can cause compensatory polycythemia and increased blood viscosity. Pulmonary hypertension-induced right ventricular hypertrophy or failure can result, with coelomic effusion after 2 to 3 weeks. (17) This bird's hematocrit and sodium levels were not increased, and no histologic abnormalities were observed in the lungs or myocardium.
Cardiac troponin I is a sensitive and specific marker of cardiac injury in humans and other mammals. Results of numerous studies have demonstrated that cTnI is the most reliable indicator of myocardial cell damage, because it is a cardiac-specific protein released into the circulation from damaged myocytes. (18) Cardiac troponin ! has been well conserved between humans and other animals, with greater than 95% homology in the amino acid sequence between humans and mammals (19) and 71.5% homology between human and chickens. (20) Therefore, current mammalian assays might be useful in detecting cardiac injury in avian patients, although reference values have yet to be established.
Two different assays were used to assess cTnI levels in this bird: a hand-held device that uses a heparinized whole blood sample in a 2-site ELISA with electrochemical detection (i-STAT, Heska Corporation) and a sandwich ELISA kit that evaluates serum concentrations by using immunofluorescence (Beckman Coulter Delta X, Beckman Coulter). Although both of these test kits have been validated for dogs, (19) neither has been evaluated in birds. The hand-held device produced results with no clinical utility, however, the sandwich ELISA showed a cTnI value in the affected bird from 3 to 20 times higher than the values measured in the normal birds. Possible reasons for error in the hand-held readings are excessive heparinization (90 U/mL of heparin can decrease cTnI levels up to 20%) and the effect of adjustment for hematocrit, which may need to be treated differently because of the different morphology of avian red blood cells. The findings from the sandwich ELISA were more consistent with expected values, although the association with real values, as well as the clinical significance of cTnI in birds, is speculative.
We believe that this is the first described case of cardiomyopathy and right-sided congestive heart failure in a captive red-tailed hawk. Although the specific cause remains unknown, this bird did respond to initial therapy with a loop diuretic. Although the disease process was advanced at the time of diagnosis in this hawk, it indicates a potential to provide supportive treatment or to mitigate symptoms in captive raptors with cardiomyopathy before the onset of overt congestive heart failure.
Acknowledgments." We thank Steve Hein, director of the Center for Wildlife Education and the Lamar Q. Ball Jr, Raptor Center at Georgia Southern University for transport and fiscal support with this case.
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S. Emmanuelle Knafo, DVM, Gregg Rapoport, DVM, Dipl ACVIM, Jamie Williams, MS, DVM, Dipl ACVR, Benjamin Brainard, VMD, Dipl ACVECC, Dipl ACVA, Elizabeth Driskell, DVM, Elizabeth Uhl, DVM, PhD, Dipl ACVP, Sonia Crochik, MS, DVM, Dipl ACVR, and Stephen J. Divers, BVetMed, DZooMed, MRCVS, Dipl ACZM, Dipl ECZM
From the Departments of Small Animal Medicine and Surgery (Knafo, Rapoport, Brainard, Divers), Anatomy and Radiology (Crochik, Williams), and Pathology (Driskell, Uhl), College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA.
Table 1. Cardiac troponin I levels (ng/mL) measured by a hand-held blood chemistry analyzer and by ELISA immunoassay in a red-tailed hawk with right-sided congestive heart failure and in 4 red-tailed hawks with no evidence of cardiac disease. iSTAT ELISA Red-tail hawk (plasma) (serum) Clinical case (heart disease) 0.03 0.40 Wild; soft-tissue wound 0.00 0.02 Wild; ulnar fracture 0.00 0.02 Wild; head trauma 0.00 0.09 Zoo bird 0.00 0.14 Abbreviation: ELISA indicates enzyme-linked immunosorbent assay. Table 2. Measured heart parameters in a red-tailed hawk with congestive heart failure compared with ranges for normal female diurnal raptors. Normal female Measurement Red-tailed diurnal raptors parameter hawk, mm (mean [+ or -] 2 SD) (5) turn RVTD 23.3 0.3-4.7 RUTS 20 0.6-3.8 RVLD 28 5.8-22.6 RVLS 24.4 3.8-22.2 LVTD 8.7 4.7-13.1 LVTS 9.8 4.1-11.3 LVLD 21.9 9.7-30.5 LVLS 19.1 8.8-27.6 Abbreviations: RV indicates right ventricle; T, transverse; D, diastole; S, systole; L, longitudinal; LV, left ventricle.
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|Title Annotation:||Clinical Reports|
|Author:||Knafo, S. Emmanuelle; Rapoport, Gregg; Williams, Jamie; Brainard, Benjamin; Driskell, Elizabeth; Uhl|
|Publication:||Journal of Avian Medicine and Surgery|
|Date:||Mar 1, 2011|
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