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Right heart failure in an African penguin (Spheniscus demersus).

Abstract: A 19-year-old male African penguin (Spheniscus demersus) was presented with coelomic distention after a 6-week history of lethargy and decreased appetite. Results of radiographs showed loss of coelomic detail, and ultrasound and computed tomography results revealed coelomic fluid and dilated hepatic veins. Echocardiography revealed moderate right atrial enlargement. Findings were consistent with right-sided cardiac disease. Treatment with furosemide initially reduced ascites, but the clinical condition worsened weeks later and enalapril, pimobendan, and sildenafil were added to the medical therapy. At 12 weeks after presentation, results of an echocardiogram revealed persistent right atrioventricular valve regurgitation, moderate ascites, and dilation of hepatic veins. Clinical signs of right heart failure were managed through adjustments in medical therapy and coelomic fluid aspiration, but the bird died 18 weeks after initial presentation. Gross and microscopic findings were consistent with valvular insufficiency and right-sided heart failure. To our knowledge, this case is the first documented report of cardiac disease in an African penguin.

Key words: congestive heart failure, right heart failure, avian, penguin, Spheniscus demersus

Clinical Report

A 19-year-old male African penguin (Spheniscus demersus) was examined because of coelomic distention and development of a wide-legged stance and abnormal gait. The penguin had a 6week history of lethargy and decreased appetite. Originally hatched in captivity, the bird was housed in an aquarium and fed a varied diet of whole fish and an avian multivitamin (Mazuri Vita-Zu Small Bird, Mazuri Exotic Animal Nutrition/PMI Nutrition Inti LLC, St Louis, MO, USA). Initial results of hematologic testing and plasma biochemical analysis revealed mild anemia (hematocrit 37%; individual reference intervals [IRIs] of 14 clinically healthy samples 51 % 60%, reference interval 29.6%-57.8%), and hypoproteinemia (4.0 g/dL; IRI 4.3-6.1 g/dL, reference interval 4.1-8.0 g/dL). (1) Results of survey radiographs revealed generalized loss of coelomic detail and enlargement of the cardiac silhouette (Fig 1), consistent with intra-abdominal or cardiac disease.

Further diagnostic imaging was done. Results of a computed tomography scan revealed fluid density throughout the coelom. Coelomic ultrasound and echocardiography (5.5-7 MHz phased array probe; Aloka ProSound Alpha 7, Hitachi, Troy, MI; placed on the ventral brood pouch) were performed. Results revealed a large amount of anechoic free fluid, dilation of hepatic vessels, and hyperechoic hepatic architecture. On ultrasound-guided aspirate, approximately 160 mL of straw-colored fluid was removed from the coelom. Echocardiography revealed mild to moderate right atrial enlargement and thickening of the right atrioventricular (AV) valve. Although normal echocardiographic findings have not been reported in this species, subjective evaluation suggested moderate right-sided cardiac disease resulting in congestive heart failure. Coelomic fluid analysis revealed sparse to moderate cellularity, consisting primarily of white blood cells, with 60% mononuclear cells (plasma cells and lymphocytes) and 40% heterophils. Total solids, measured via refractom eter, were 1.4 g/dL. No other significant findings were noted.

Treatment with furosemide was initiated (1mg/ kg IM, followed by 1 mg/kg PO q24h). After 7 days, the bird was asymptomatic, and coelomic fluid appeared resolved on radiographs. The furosemide dose was decreased to 0.5 mg/kg PO q24h. Between days 22 and 57, clinical and diagnostic findings included the commencement and completion of a molt, mild increases in coelomic fluid, and mild tachycardia (heart rate 120 beats/min). Alterations in hematologic and biochemical values included a relative heterophilia (91%; IR1 52%-77%, no reference interval available, hypoproteinemia (3.9 g/dL), hyponatremia (135 mEq/L; IRI 153-161 mEq/L, reference interval 139-168 mEq/L), and hypochloremia (112 mEq/L; IRI 114-121 mEq/L, reference interval 101-131 mEq/L). (1) Periodic adjustment of the furosemide dose and the salinity of drinking water resulted in normalization of these values.

Because of persistent coelomic fluid accumulation, treatment with enalapril (0.8 mg/kg PO q12h) was begun on day 63. The next day, the bird was lethargic, inappetant, and mildly hypernatremic (167 mEq/L). Drinking water was changed to a mix of 25% salt water and 75% fresh water, after which electrolytes normalized and appetite improved.

Over the next 2 weeks, clinical and diagnostic findings indicated worsening right-sided heart disease. Pimobendan (6 mg/kg PO ql2h) was added to the drug regimen. Because of development of a grade 3/6 right-sided heart murmur, an echocardiogram (3-6 MHz phased array probe [Aplio 300, Toshiba, Tustin, CA, USA] on the ventral brood pouch) was performed on day 67. The right atrium was moderately to severely enlarged, the right ventricle was moderately dilated, and right ventricle systolic function was normal. Moderate to severe regurgitation of the right AV valve, mild to moderate pulmonary hypertension, enlargement of hepatic veins, and systolic flow reversal in the hepatic veins were noted. There was moderate coelomic effusion and laminar blood flow across the aortic valve. Primary valvular disease was considered the most likely etiology of the AV regurgitation, resulting in moderate to severe right-sided congestive heart failure.

On day 106, exercise intolerance, periodic open-mouth breathing, severe coelomic distension, and muffled heart sounds were noted. Results of blood tests revealed hypokalemia (2.5 mEq/L; IR1 3.14.1 mEq/L, reference interval 2.5-8.1 mEq/L). (1) Severe coelomic fluid accumulation, generalized cardiac enlargement, and distension of the pulmonary vasculature were noted on radiographs (Fig 2). Treatment with potassium chloride (0.5 mEq/kg PO q24h) and sildenafil (1 mg/kg PO ql2h) was initiated. Coelomic aspiration and adjustments to the furosemide dose were continued to manage fluid accumulation. Despite continued treatment, the bird continued to decline and died 124 days after initial presentation.

Postmortem examination revealed a bird in fair to good nutritional condition. The subcutaneous cervical, jugular, and hepatic veins and the caudal vena cava were moderately dilated (Fig 3). Approximately 10 and 15 mL of clear fluid was present in the pericardial sac and coelomic cavity, respectively. The right atrium and ventricle bulged from the enlarged 72-g (2.64% body weight) heart (Fig 4A), and the right atrial free wall was thin and semitransparent. Multiple 1-2-mm opaque nodules were present along the 12-15-mm-wide free margin of the right AV valve (Fig 4B). Additional cardiac measurements are presented in Table 1.

Microscopically, cardiac myocytes were well organized and relatively uniform in diameter. There was mild anisokaryosis, and perinuclear vacuoles containing lipofuscin granules were widespread. The right AV valve leaflet was diffusely muscular, becoming blunted and thickened by an irregular, multinodular focus of subendothelial fibrosis at the free margin (Fig 5). In the liver, diffuse mild to moderate fibrosis surrounded central veins and radiated into lobules. The lungs were congested and interparabronchial septa contained widespread, variably sized foci of bone that often replaced areas of air capillaries and rarely protruded into parabronchial lumens. Vascular walls were not involved. Inflammatory infiltrates consisted of rare heterophils and lymphocytes (Fig 6). Results of aerobic, anaerobic, and fungal cultures of liver, spleen, kidneys, and heart were negative for growth.

Discussion

This report describes the clinical presentation, assessment, and management of primary right-sided heart failure in an African penguin. Multimodal diagnostic tests and treatments were used over a period of 18 weeks to evaluate disease progression and to manage clinical signs and electrolyte imbalances with some efficacy.

Although comparatively well described in poultry, examples of cardiovascular disease in companion birds and avian species typically displayed in zoos and aquaria are relatively limited and poorly documented. (2,3) However, a recent review of postmortem examination results of 107 psittacine birds revealed that 36% had gross lesions involving the heart, major vessels, or both and that 99% had microscopic changes. (4) The paucity of avian cardiac cases may be related to their often subtle and nonspecific clinical signs, as well as to difficulty in antemortem diagnosis. (2,3,5) Electrocardiography remains underutilized, although techniques have been established for some species. (3,6) Echocardiography has been described in poultry and, more recently, in nondomestic birds, although specialized avian skeletal and respiratory anatomy limits sonographic approaches. (7) The dense feather layer and lack of apteria in penguins create a greater diagnostic challenge. (7) The use of transesophageal echocardiography, which allows for increased resolution and detail, is in its infancy in avian patients and includes the risk of gastrointestinal perforation. (6) Although anatomic limitations prevented complete echocardiographic evaluation, coelomic and cardiac ultrasound, along with radiographic assessment, facilitated diagnostic monitoring and clinical management in this case.

Treatment goals for avian cardiovascular disease are as for patients of other species: stabilization, improvement of cardiac function, and treatment of secondary conditions, such as ascites. (2,3) However, medical management of cardiovascular disease in birds is also minimally described, the pharmacokinetics of cardiac drugs are largely unknown, and dosages are typically extrapolated from other species. (2,5,8-10) In this case, furosemide, enalapril, and pimobendan were used for treatment. Pharmacokinetic data for enalapril has been established in the racing pigeon. (11) It has been used successfully to treat hydropericardium in a Fischer's lovebird (Agapornis fischeri) and right heart failure in a blue-fronted Amazon parrot (Amazona aestiva) and an African grey parrot (Psittacus erithacus). (8-10) Results of a recent study in Hispaniolan Amazon parrots (Amazona ventralis) suggest that birds require significantly higher doses of pimobendan than doses extrapolated from canine data. (12)

Although no scientific studies describe the use of the angiotensin-converting enzyme inhibitor enalapril or the phosphodiesterase-3 inhibitor/calcium sensitizer pimobendan in penguins, these drugs were administered with some efficacy in this case. Although higher doses may have improved clinical response, the lack of species-specific pharmacokinetic data led to initiating treatment at the low end of recommended avian dose ranges to minimize possible adverse effects. (13) Sildenafil, a phosphodiesterase-5 inhibitor, was not used long enough to evaluate efficacy.

It is postulated that avian cardiac and pulmonary anatomy may favor the development of rightsided (versus left-sided) myocardial failure. (8,14) Increased pulmonary rigidity may contribute to more rapid development of pulmonary hypertension, and the unique muscular anatomy of the avian right AV valve may predispose to malfunction in response to pressure overload. (14) The gross structure of the right AV valve of this African penguin was similar that of other avian species. (3)

Echocardiographic evidence of right AV regurgitation and postmortem findings of valvular endocardiosis, engorgement of the vena cava, and hepatic chronic passive congestion are consistent with right-sided heart failure secondary to AV valve insufficiency. While enlargement of the right heart and valvular changes appeared grossly severe, normal comparative parameters have not been established for African penguins.

Pulmonary osseous metaplasia has not been documented in penguins, but it occurs in the lungs of aged birds of other species, in rapidly growing poultry, and in birds reared at high altitudes. (15) While often interpreted as an incidental finding, the degree of bone formation in this bird was severe and may have exacerbated disease progression by increasing vascular resistance and pulmonary hypertension.

Reports of cardiac disease in penguins include acute aortic rupture and atherosclerosis in Antarctic penguins and nutritional cardiomyopathy in rock-hopper penguins (Eudyptes chrysocome). (16,17) To our knowledge, this is the first documented case of right heart failure in an African penguin. This case highlights the value of multimodal diagnostic tests in the early identification and evaluation of avian cardiac disease and the need for further investigation into the pharmacokinetics and efficacy of cardiac medications in avian species.

References

(1.) Teare JA. Spheniscus demersus Standard International Units, Selection criteria: Age grouping 15-20 years old. In: ISIS Physiological Reference Intervals for Captive Wildlife [CD-ROM], Bloomington. MN: International Species Information System; 2013.

(2.) Strunk A, Wilson GH. Avian cardiology. Vet Clin North Am Exot Anim Pract. 2003:6(1): 1-28.

(3.) Lumeij JT, Ritchie BW. Cardiology. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:695-722.

(4.) Krautwald-Junghanns ME, Braun S, Pees M, et al. Research on the anatomy and pathology of the psittacine heart. J Avian Med Sarg. 2004; 18(1):2-11.

(5.) Pees M, Straub J, Krautwald-Junghanns ME. Echocardiographic examinations of 60 African grey parrots and 30 other psittacine birds. Vet Rec. 2004; 155(3):73-76.

(6.) Beaufrere H, Pariaut R, Nevarez J, Tully T. Feasibility of transesophageal echocardiography in birds without cardiac disease. J Am Vet Med Assoc. 2010;236(5):540-547.

(7.) Krautwald-Junghanns ME, Schultz M, Hagner D, et al. Transcoelomic two-dimensional echocardiography in the avian patient. J Avian Med Surg. 1995; 9(1): 19-31.

(8.) Sedacca C, Campbell T, Bright J, et al. Chronic corpulmonale secondary to pulmonary atherosclerosis in an African grey parrot. J Am Vet Med Assoc. 2009;234(8):1055-1059.

(9.) Pees M, Straub J, Krautwald-Junghanns ME. Insufficiency of the muscular atrioventricular valve in the heart of a blue-fronted Amazon (Amazona aestiva aestiva). Vet Rec. 2001; 148(17): 540-543.

(10.) Straub J, Pees M, Enders F, Krautwald-Junghanns ME. Pericardiocentesis and the use of enalapril in a Fischer's lovebird (Agapornis fischeri). Vet Rec. 2003; 152(1)24-26.

(11.) Pees M, Pees K, Abraham G, et al. Examinations on the pharmacokinetics and compatibility of enalapril in racing pigeons. Tieraerztl Prax Ausg K Heimtiere. 2013;41(5):319-325.

(12.) Guzman D, Beaufrere H, Tully T, et al. Pharmacokinetics of single oral dose of pimobendan in Hispaniolan Amazon parrots (Amazona ventralis). J Avian Med Surg. 2014;28(2):95 101.

(13.) Carpenter JW. Exotic Animal Formulary. 4th ed. St Louis, MO: Elsevier Saunders; 2012.

(14.) Oglesbee BL, Oglesbee MJ. Results of postmortem examination of psittacine birds with cardiac disease: 26 cases (1991-1995). J Am Vet Med Assoc. 1998; 212(11):1737-1742.

(15.) Borst GHA, Zwart P, Mullink FIWMA, Vroege C. Bone structures in avian and mammalian lungs. Vet Pathol. 1976; 13(2):98-103.

(16.) St Leger JJ. Acute aortic rupture in Antarctic penguins. Proc Annu Conf Am Assoc Zoo Vet. 2003:154.

(17.) Keymer IF, Malcolm HM, Flunt A, Horsley DT. Health evaluation of penguins (Sphenisciformes) following mortality in the Falklands (South Atlantic). Dis Aquat Org. 2001;45(3): 159-169.

Lara Cusack, DVM, Cara Field, DVM, PhD, Alexa McDermott, DVM, Brandon Pogue, DVM, Dipl ACVIM (Cardiology), Tonya Clauss, DVM, MS, Gregory Bossart, VMD, PhD, and Alvin Camus, DVM, PhD

From the Georgia Aquarium, 225 Baker Street NW, Atlanta, GA 30313, USA (Cusack. Field, McDermott. Clauss, Bossart); Georgia Veterinary Specialists, 455 Abernathy Road NE, Sandy Springs, GA 30328, USA (Pogue); the Division of Comparative Pathology, Miller School of Medicine, University of Miami, PO Box 016960 (R-46), Miami, FL 33101, USA (Bossart); and the Department of Pathology, University of Georgia, 501 D. W. Brooks Drive, Athens, GA 30602, USA (Camus).

Table 1. Postmortem measurements of the heart
of an African penguin with right heart failure.

             Parameter (a)                  Measurement

Weight of heart                            72 g (2.64% of
                                             body weight)
Right AV valve, thickness at free          1 mm
  margin
Right AV valve, thickness at base          1.5 mm
Right AV valve, length                     5.6 cm
Right ventricular free wall thickness      4 mm
  at AV valve
Right ventricular free wall thickness      1 mm
  at apex
Right atrial free wall thickness           <1 mm
Mitral valve length                        4.3 cm
Left ventricular free wall, thickness at   7 mm
  mitral valve
Left ventricular free wall, thickness at   4 mm
  apex
Interventricular septum thickness          1-2 mm

(a) Abbreviation: AV indicates atrioventricular.
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Article Details
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Author:Cusack, Lara; Field, Cara; McDermott, Alexa; Pogue, Brandon; Clauss, Tonya; Bossart, Gregory; Camus,
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Sep 1, 2016
Words:2518
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