Abstract

Recently several cases of adult giant anteaters (Myrmecophaga tridactyla) that have died of cardiac insufficiency associated with severe dilated biventricular cardiomyopathy have been reported. The syndrome is similar to that seen with taurine deficiency in domestic felines and canines. Prolonged, progressive exercise intolerance and dyspnea are characteristic clinical signs. Current diagnostic methods include thoracic radiographs and echocardiography. Most affected animals are not diagnosed with dilated cardiomyopathy until clinical signs are present. Treatment at that stage has been unresponsive to oral cardioactive drugs and/or taurine supplementation. The purpose of this study was to evaluate plasma and blood taurine concentrations in giant anteaters with suspected cardiac disease. Initial results suggest that low blood and plasma taurine concentrations are associated with dilated cardiomyopathy and may be used as early diagnostic indicators. We recommend oral taurine supplementation in anteaters with whole blood taurine levels under 300 mg/ml.

Introduction

Dilated cardiomyopathy in giant anteaters resembles taurine deficiency associated cardiomyopathy in other species.^1,3,4,11,17 Dilated cardiomyopathy is an occasional finding in domestic dogs,^2,3,6 and cats,^4,5,15,17 humans, ferrets, and skunks^5,7. Myocardial disease of this type is observed in domestic cats due to insufficient dietary taurine.¹² Taurine, a beta-sulfonic amino acid, is ubiquitous in mammalian tissues, and is the most abundant free amino acid in the heart, retina, skeletal muscle, and brain.^7,13,15 Dietary taurine is essential for cats due to their limited ability to synthesize taurine from cysteine and methionine.^3,7-9,13,15 This is associated with a low concentration of cysteine sulfinic acid decarboxylase, an enzyme required for taurine biosynthesis. Cats are unable to conjugate significant amounts of bile acids with glycine and, therefore, must utilize taurine for conjugation of bile acids.⁸ This requirement may result in a taurine demand in excess of supply. Taurine has also been suggested to function in myocyte calcium binding, modulation of contractility (possibly associated with myocardial calcium homeostasis), osmotic regulation, blood pressure control, and platelet resistance to aggregation.^7,13 Dilation of the heart occurs when the left ventricle fails to generate normal contractile force and ejection fraction is severely reduced. End-systolic and end-diastolic ventricular volumes increase and myocardial wall tension becomes elevated. Left ventricular relaxation and diastolic compliance alterations occur, along with impaired contractile function. This contributes to elevated filling pressures. The activation of the sympathetic and renin-angiotensin­aldosterone systems further increases cardiac preload and afterload. End-systolic volume increases from impaired left ventricular contractility. The end result of these processes is pulmonary congestion, effusion, and signs of low cardiac output. Biventricular dilation and associated cardiac insufficiency are the hallmarks of a taurine-deficient cardiomyopathy in domestic cats.^{1,8-10,12,13,15} Cats also develop sequelae of retinal degeneration, reproductive and developmental anomalies, and increased platelet aggregation, as well as decreased leukocyte function.⁶ In felines and some breeds of canines, specifically American cocker spaniels, boxers, and Doberman pinschers, taurine and L­carnitine supplementation can ameliorate the clinical signs and, in many cases, improve cardiac condition and size to near normal parameters.^{4,6,8,9,11-13,15} Dogs usually don’t require taurine in their diet, provided there are sufficient sulfur amino acids present for adequate taurine synthesis.

A globoid heart with thin left and right ventricular walls is apparent at necropsy in giant anteaters with dilated cardiomyopathy. Mineralization of the aorta and stomach has also been found occasionally. Histopathology of cardiomyopathy in anteaters revealed varying degrees of right and left ventricular myofiber hypertrophy, atrophy, and disarray. Passive congestion of the lungs and liver supports the gross finding of bilateral dilated cardiomyopathy. Myocardial fibrosis varied from mild to severe. Occasional mineralization of myofibers and mild chronic inflammation were also seen. Anecdotal evidence in one case suggested a possible role of taurine in the development of dilated cardiomyopathy.¹ The purpose of this study was to evaluate plasma and blood taurine concentrations in giant anteaters with suspected cardiac disease and better characterize this relationship.

Materials and Methods

Whole blood samples were collected opportunistically from eight different giant anteaters from six different institutions that all appeared normal. Table 1 provides signalment information. Further examination, however, revealed that cardiomyopathy was present in all anteaters except anteater A2 in institute 2. Some animals were sampled serially over time. Taurine levels were measured in whole blood preserved in EDTA and in heparin and plasma samples. These samples were frozen and run in as a batch.¹⁴ Complete white blood cell counts were also done when possible. Radiographs of the thorax were performed during routine physical exams on all animals and echocardiography was performed on anteaters Al and A2 in institute 2.

Results

The results obtained in this study are presented in Table 1. In addition, all animals had subjectively enlarged hearts in radiographs, except for anteater A2 in institute 2.

Table 1. Signalment, WBC count, and taurine levels of anteaters with dilated cardiomyopathy

^aF = female; M = male; NA = not available.
^bFollowing taurine supplementation of 2 g SID PO total dose.

Discussion

These preliminary results suggest that in the anteaters examined, blood levels of taurine below 300–600 nmol/ml and plasma levels below 60–120 nmol/ml seem to be associated with the presence of cardiomyopathy, and the degree of deficiency may be associated with the degree of disease. Normal canine taurine levels are 60–120 nmol/ml for plasma, 200–350 nmol/ml for EDTA whole blood, and 200–350 nmol/ml for lithium heparinized whole blood.^5,9 Normal feline taurine levels are 60–120 nmol/ml for plasma, 300–600 nmol/ml for EDTA, and 300–600 nmol/ml for lithium heparinized whole blood.¹⁴

In our study, whole blood was used as an indicator of total body depletion, although it is a slower indicator of changes in systemic taurine levels. Whole blood did not require centrifugation, however, simplifying sample collection. Minimal sample processing after collection decreased the possibilities of technical error in the taurine assay. False elevations in blood taurine levels may occur when an animal presents with leukocytosis, however, since taurine binds to leukocytes. Plasma taurine levels were used as an early indicator for systemic taurine depletion, but thorough centrifugation and careful extraction were required to avoid false elevations due to leukocyte contamination. Both plasma and whole blood samples could be stored, provided there was no bacterial contamination. Whole blood is the recommended sample to submit for systemic taurine determination.¹⁴

Changes in the diets of captive anteaters had been made following reports of hyperostosis associated with hypervitaminosis A and D in tamanduas fed commercial feline diets.² Many institutions had changed commercial cat food-based diets to a paste made of moistened dog food and leafeater (Marion Leafeater, Marion Zoological, 13803 Industrial Park Boulevard, Plymouth, MN 55410 USA). Yogurt, omega fatty acids supplements, and vitamin K (Vetamix Inc. Shenandoah, IA, 51601 USA) were usually added. In at least one instance, the use of commercial dog food may have resulted in taurine deficient dilated cardiomyopathy in giant anteaters.¹ Anecdotal evidence points to disparate taurine levels in commercial dog foods. Nutritional consultants recommend the use of a high-quality commercial dog food to ensure adequate taurine levels. Supplementation with pinky mice and meats, as well as access to rotten logs and insects as enrichment, may ameliorate a taurine deficient diet. Oral taurine and carnitine supplementation (taurine, carnitine, 500-mg capsules, Solgar Vitamin and Herb, Leonia, NJ 07605 USA) has been shown to arrest and, occasionally, partially reverse myocardial failure and cardiac chamber dilatation in taurine depleted cats and dogs.⁶ Domestic cats require 1 g/kg of dry matter taurine for expanded diets, 2 g/kg of dry matter taurine for canned diets, and 500 mg/kg of dry matter taurine for purified diets. Relatively new commercial products on the market (Mazuri Insectivore 5MK8, PMI Nutrition International LLC, PO Box 19798 Brentwood, MO 63144 USA) specifically formulated for insectivores can contain taurine concentrations of up to 2.68 g/kg as fed. A few institutions possessing giant anteaters have begun to base their diets on these products. At this time we recommend oral taurine supplementation in anteaters with whole blood taurine levels under 300 nmol/ml. We suggest that, with early detection of taurine deficiency, high-level oral taurine supplementation may provide similar beneficial effects in giant anteaters and may even reverse myocardial failure and cardiac chamber dilatation. Further studies, however, are required to more precisely define the nutritional requirement of taurine in anteaters, adequate blood and plasma levels, the most appropriate treatment dosages, and the prognosis for recovery.

Acknowledgments

The authors are grateful to the San Francisco Zoo, Audubon Zoo, Santa Barbara Zoo, Disney Wild Animal Kingdom, Nashville Zoo, and Chaffe Zoo staff for their generous and timely contribution of samples and information.

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