Congestive Heart Failure Due to Endocardiosis of the Mitral Valves in an African Pygmy Hedgehog

Congestive Heart Failure Due to Endocardiosis of the Mitral Valves in an African Pygmy Hedgehog

AEMV FORUM CONGESTIVE HEART FAILURE DUE TO ENDOCARDIOSIS OF THE MITRAL VALVES IN AN AFRICAN PYGMY HEDGEHOG Joanna Hedley, BVM&S DZooMed (Reptilian), M...

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AEMV FORUM CONGESTIVE HEART FAILURE DUE TO ENDOCARDIOSIS OF THE MITRAL VALVES IN AN AFRICAN PYGMY HEDGEHOG Joanna Hedley, BVM&S DZooMed (Reptilian), MRCVS, Livia Benato, DVM, CertZooMed, GPCert (ExAP), MRCVS, Gemma Fraga, DVM, MRCVS, Dip. ECVIM-CA, Christopher Palgrave, BSc (Hons), BVM&S, PhD, MRCVS, and Kevin Eatwell, BVSc (Hons), DZooMed (Reptilian), Dip. ECZM (Herpetology)

Abstract A 2.5-year-old male African pygmy hedgehog (Atelerix albiventris) was presented with a 2-week history of lethargy, reduced appetite, and general weakness. Based on the clinical signs and heart valve abnormalities observed during an echocardiography examination, a provisional diagnosis of endocardiosis or endocarditis was made. Immediate therapeutic intervention consisted of furosemide, pimobendan, and amoxicillin/clavulanate. Despite medical treatment, 2 weeks following presentation, the hedgehog’s physical condition deteriorated to the point that euthanasia was recommended for the patient and agreed to by its owner. A postmortem examination was performed and tissue samples submitted for histopathology revealed a final diagnosis of valvular endocardiosis and wobbly hedgehog syndrome. Copyright 2013 Elsevier Inc. All rights reserved. Key words: Atelerix albiventris; cardiology; endocardiosis; hedgehog; wobbly hedgehog syndrome (WHS)

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frican pygmy hedgehogs (Atelerix albiventris) have recently become a popular companion animal in which a number of different disease conditions have been diagnosed. Cardiomyopathy is considered the most common cardiac disease in this species,1,2 whereas valvular endocardiosis, identified in this case, has not been previously reported in African pygmy hedgehogs.

A 2.5-year-old male African pygmy hedgehog was presented with a 2-week history of lethargy, reduced appetite, and general weakness. The hedgehog was housed indoors in a plastic open-top enclosure, maintained on a substrate of woodchips, and provided with supplemental heat. The patient’s diet consisted primarily of wet and dry complete cat food (Purina Adult Cat, Nestle Purina Pet Care, Crawley, UK) with mealworms provided as a treat. Results of a physical examination indicated the hedgehog was underweight at 262 g, was exhibiting hind limb weakness, and had difficulties curling up in a defensive position. The patient’s respiratory rate

was elevated at 120 breaths per minute (bpm). No other clinical abnormalities were noted on the external physical examination. The hedgehog was admitted into the hospital for further examination under general anesthesia. A blood sample was collected from the anterior vena cava for a complete blood count (CBC) and plasma biochemistry analysis. Lateral and dorsoventral whole-body radiographs were obtained, which revealed generalized cardiomegaly with a vertebral heart score of 10 (7.25 to 8.75 vertebra),3 dorsal displacement of the trachea, and an alveolar lung pattern (Fig. 1).

From the Exotic Animal and Wildlife Service, The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Midlothian, UK; the Chester Zoo, Chester, UK; the Department of Veterinary Science Small Animal Teaching Hospital, University of Liverpool, Neston, UK; and the Veterinary Pathology, School of Veterinary Sciences, University of Bristol, Langford, UK. Address correspondence to: Joanna Hedley, BVM&S, CertZooMed, MRCVS, Exotic Animal and Wildlife Service, The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Veterinary Centre, Midlothian EH25 9RG, UK. E-mail: [email protected]. Ó 2013 Elsevier Inc. All rights reserved. 1557-5063/13/2101-$30.00 http://dx.doi.org/10.1053/j.jepm.2013.05.012

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Journal of Exotic Pet Medicine 22 2013, pp 212–217

FIGURE 1. Lateral right thoracic radiograph of an African pygmy hedgehog with congestive heart failure. Note generalized cardiomegaly, dorsal displacement of the trachea, and an alveolar lung pattern.

The owner opted not to start treatment at this stage, preferring to take the hedgehog home for the weekend while awaiting the hematology results. Three days following the initial presentation, the hedgehog had deteriorated and was dyspneic. The respiratory rate was elevated to 176 bpm and a grade 4/6 systolic sternal heart murmur was identified upon auscultation. Hematologic results revealed minor changes in biochemical parameters, in addition to a severe leukocytosis (Table 1). The CBC confirmed a marked neutrophilia and a moderate lymphocytosis with the occasional atypical cell, but no left shift was noted. An echocardiography examination was performed on the unanesthetized patient. The echocardiography examination revealed severe mitral regurgitation with thickening and prolapse

of the mitral valve leaflets, and left atrium enlargement (LA:Ao 2.2) (Fig. 2). Moderate aortic insufficiency with mild thickening of the left coronary aortic valve cusp and the left ventricular walls were also present. There were no obvious discrete vegetations present in any of the cardiac valves and left ventricular systolic function was adequate. Full measurements were not recorded at this time to avoid unnecessary stress in a dyspneic patient. Based on clinical and echocardiographic findings, the top differential disease diagnoses included endocardiosis and valvular endocarditis. The hedgehog was stabilized by placing it in an oxygen cage with 40% oxygen and initially being treated with furosemide (Dimazon 5%, MSD Animal Health, Milton Keynes, UK) (3 mg/kg, subcutaneously, 3 times a day; Lasix,

TABLE 1. Hematology and biochemistry results for the African pygmy hedgehog Parameter Red blood cell count  1012/L PCV (%) Hemoglobin (g/dL) MCV (f/L) Total leukocyte count  109/L Neutrophils  109/L Lymphocytes  109/L Eosinophils  109/L Monocytes  109/L Total protein (g/L) Albumin (g/L) ALT (IU/L) AST (IU/L) Creatine kinase (IU/L) Urea (mg/dL) Creatinine (mg/dL) Sodium (mEq/L) Potassium (mEq/L) Calcium (mg/dL) Phosphorus (mg/dL)

Value 5.11 35 11.8 68 116.8 81.76 30.37 2.3 2.3 64 38 117 601 1162 103.3 0.75 150 5.9 10.18 9.97

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Reference Range (19) 3 to 16 22 to 64 7.0 to 21.1 41 to 94 3 to 43 0.6 to 37.4 0.9 to 13.1 0 to 5.1 0 to 1.6 40 to 77 18 to 42 16 to 134 8 to 137 333 to 1964 13 to 54 0 to 0.8 120 to 165 3.2 to 7.2 5.2 to 11.3 2.4 to 12.0

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FIGURE 2. Initial echocardiogram of the hedgehog. Note severe mitral regurgitation with thickening and prolapse of the mitral valve leaflets, and left atrial enlargement.

manufacturer, address of company) (subsequently, the dose was reduced to 2 mg/kg 3 times daily) and amoxicillin/clavulanate (Synulox RTU, Zoetis, London, UK) (12.5 mg/kg, subcutaneously, once a day). Within 24 hours after the initiation of the treatment, the patient’s respiratory rate and effort were significantly reduced, and its appetite and ability to curl in a defensive position had improved. Supplemental oxygen was discontinued and pimobendan (Vetmedin 1.25 mg, Boehringer Ingelheim Ltd, Bracknell, UK) (0.3 mg/kg, orally, 2 times daily) was administered with food. The following 2 days, clinical signs continued to improve to the point that the hedgehog was discharged on furosemide, pimobendan, and amoxicillin/clavulanate with instructions to the

owner to continue treatment as previously prescribed. When reevaluating the patient 5 days following discharge, there was no evidence of dyspnea unless stressed, and its appetite and attitude had returned to normal. A repeat echocardiogram showed a reduction in the left atrium-to-aortic ratio (LA:Ao 1.93). Also acquired during the echocardiography examination were more detailed cardiac measurements (Table 2). Repeat radiographic images were not obtained at this time in order to avoid further anesthetic risks to the patient. Medication was continued, but over the next 5 days respiratory effort and rate began to increase. Despite readmission to the veterinary hospital for oxygen therapy, and increasing

TABLE 2. Echocardiographic measurements for the hedgehog 5 days posttreatment Parameter 2D Ao diameter LA diameter LA/Ao M-Mode IVSd LVIDd LVFWd IVSs LVIDs LVFWs %FS Doppler MR maxPG LVOT Vmax RVOT Vmax

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Value

0.4 cm 0.7 cm 1.93 1.68 mm 8.27 mm 2.36 mm 2.45 mm 3.66 mm 3.31 mm 56% 111.50 mm Hg 0.87 m/s 0.51 m/s

Reference Range (3)

0.31 to 0.40 cm 0.51 to 0.62 cm 1.37 to 1.92 1.3 6.7 1.4 1.9 5.4 1.9 17.40%

to to to to to to to

1.7 mm 8.4 mm 1.8 mm 2.4 mm 6.5 mm 2.7 mm 26.80%

0.29 to 0.66 m/s 0.23 to 0.51 m/s

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FIGURE 3. Histological section of the mitral valve leaflets. Collagen bundles of the lamina fibrosa are diffusely hyalinized, fragmented and degenerated in appearance.

furosemide to 4 mg/kg 3 times daily, no treatment response was observed. In view of the poor prognosis, euthanasia was recommended and subsequently agreed to by the hedgehog’s owner. Gross postmortem examination revealed severe cardiomegaly with left atrial and ventricular dilation and moderate smooth nodular thickening of the mitral valve leaflets. The aortic valve appeared grossly normal, although subtle thickening may not have been evident due to the small size of the heart. No other cardiac abnormalities were grossly apparent. The trachea contained a profuse amount of pale-pink foamy fluid. The lungs were diffusely dark red and rubbery and contained abundant fluid when sectioned, consistent with edema. The liver had rounded borders and was markedly enlarged, but no ascites was present. Moderate lymphadenomegaly was also present affecting the cervical lymph nodes. On histological examination of the mitral valve leaflets, the collagen bundles of the lamina fibrosa were diffusely hyalinized, fragmented, and degenerated in appearance (Fig. 3). The valve was expanded by increased numbers of fibroblasts and abundant amphophilic to faintly basophilic myxoid matrix. This change extended into the subendocardial zone of the left ventricle at the attachment of the valve. Diffuse, severe pulmonary edema and alveolar histiocytosis, centrilobular hepatic congestion, and hepatocellular degeneration were noted. These changes were thought to be almost certainly related to the systemic repercussions of congestive heart failure (following chronic passive congestion and hypoxia). Mild renal tubular dilation, degeneration, and regeneration were also observed and thought to be related to a decreased renal

perfusion and subsequent tubular hypoxia. Diffuse, chronic white matter vacuolation was observed throughout the brain and spinal cord, as has been previously reported to being associated with wobbly hedgehog syndrome. DISCUSSION _________________________________ Valvular endocardiosis is the most common cardiac condition diagnosed in dogs,4 but it is rarely seen and reported in exotic animals. Valvular endocardiosis has been reported as an incidental finding on postmortem examinations in Rhesus monkeys,5 rabbits,6,7 ferrets,8-10 and a Gambian giant pouched rat.11 Valvular endocardiosis is a degenerative disease of the cardiac valves owing to unknown etiology. However, in dogs, a genetic predisposition for the development of this disease is suspected.12-14 The main clinical signs associated with valvular endocardiosis and congestive left-sided heart failure in dogs are coughing and dyspnea.15 In this case, the first clinical sign noted was hind limb weakness, followed by dyspnea and anorexia. The hind limb weakness could also be linked to wobbly hedgehog syndrome.16 A definitive diagnosis of valvular endocardiosis based on history and physical examination can be difficult to determine owing to the nonspecific clinical signs and findings related to the disease process. Cardiac auscultation is often unrewarding owing to the size of the animal, the elevated respiratory and cardiac rates, and the ability of a hedgehog to curl up. Cardiac murmurs and occasionally arrhythmias are generally more obvious in advanced cases. CBC and plasma biochemical analyses are valuable tests in cases of suspected cardiac disease in order to evaluate not

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only liver and kidney function, but also the general health of the affected patient. This hedgehog presented with mild elevation of hepatic and renal parameters. A leukocytosis was also present and potential infection was treated with the administration of amoxicillin/clavulanate, although the cause of leukocytosis was not determined in this case. Radiographic and echocardiographic examinations are generally the diagnostic tests of choice in cases of suspected cardiac disease. Two recent studies determined the reference cardiac values obtained from an echocardiogram,17 electrocardiogram, and radiographic imaging3 in healthy African pygmy hedgehogs. The cardiac measurements taken during the radiographic and echocardiographic examinations in this case were compared with the recently published values of these diagnostic tests. Despite the dimensions of the left ventricle being within the reported echocardiographic reference ranges, subjectively it was dilated. Consequently, the discrepancy in heart dimensions, in relation to disease, may be due to a difference in patient size. The study that established the reference ranges17 used larger hedgehogs with a mean body weight of 392 g ⫾ 108 g, compared with this patient weighing only 262 g, so it is possible that normal dimensions may differ slightly in a smaller animal. The fact that radiographic images showed a marked cardiomegaly with an elevated vertebral heart size (VHS) (10, ref. ranges: 7.25 to 9.75) also supports this.3 Initial treatment of the endocardiosis consisted of administration of a diuretic (furosemide) and an inodilator (pimobendan) based on previously reported treatments for dilated cardiomyopathy in African pygmy hedgehogs.18 An initial improvement in clinical signs and echocardiographic parameters was noted during treatment. However, full cardiac measurements were only recorded on repeat echocardiography once the patient was stabilized, and the effects of 5 days of furosemide treatment may have influenced the cardiac size by inducing diuresis and therefore reducing the degree of volume overload. Additional therapy included an angiotensin-converting enzyme (ACE) inhibitor once a normal appetite was regained, but unfortunately the hedgehog’s health deteriorated too rapidly before treatment could be initiated. In this case, wobbly hedgehog syndrome (WHS) was also considered as a differential diagnosis as it is not uncommon in 1- to 3-year2 1 6

old African pygmy hedgehogs that are presented with mild hind limb ataxia and weight loss.18 These neurologic signs progress over a period of approximately 15 months. The prognosis for a good quality of life and/or recovery is generally considered poor for the affected animal. Valvular endocardiosis was confirmed and WHS was diagnosed based on the pathology findings from tissues submitted following the necropsy examination. It is believed that both conditions may have played a role in the hedgehog’s initial presentation, but the rapid deterioration of the patient and concurrent respiratory signs are thought to be due to the underlying cardiac disease. To the authors’ knowledge, this is the first reported case of valvular endocardiosis in an African pygmy hedgehog. ACKNOWLEDGMENTS The authors would like to thank the Imaging Department and Veterinary Pathology Unit, Royal (Dick) School of Veterinary Studies, Edinburgh for their help with this case.

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