Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis)

American Journal of Veterinary Research

Volumn 66, Issue 2, 2005, Pages 289-299

  Kreuder, Christine ^a   Miller, Melissa A ^a,c   Lowenstine, Linda J ^b   Conrad, Patricia A ^a,b   Carpenter, Tim E ^b   Jessup, David A ^c   Mazet, Jonna A K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CALIFORNIA DEPARTMENT OF FISH AND GAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; CARNITINE; DOMOIC ACID; SELENIUM; TAURINE;

AGE; ANIMAL EXPERIMENT; ARTICLE; AUTOPSY; BODY CONSTITUTION; CARNIVORA; CLUSTER ANALYSIS; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; GEOGRAPHIC DISTRIBUTION; HEART INJURY; INFECTION; MULTIVARIATE ANALYSIS; MYOCARDITIS; NONHUMAN; NUTRITIONAL STATUS; PATHOGENESIS; RISK FACTOR; SARCOCYSTIS NEURONA; SEASONAL VARIATION; TOXICITY;

ANIMALS; ANIMALS, WILD; CARDIOMYOPATHY, DILATED; CAUSE OF DEATH; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; KAINIC ACID; MARINE TOXINS; MYOCARDITIS; OTTERS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; SARCOCYSTIS; SARCOCYSTOSIS;

ANIMALIA; CARNIVORA; ENHYDRA; ENHYDRA LUTRIS; ENHYDRA LUTRIS NEREIS; LUTRINAE; NEREIS; SARCOCYSTIS NEURONA;

EID: 14844284575     PISSN: 00029645     EISSN: None     Source Type: Journal    
DOI: 10.2460/ajvr.2005.66.289     Document Type: Article

References (78)

1. Thomas NJ, Cole RA. The risk of disease and threats to the wild population. Endangered Species Update 1996;13:23-27.
2. Kreuder C, Miller MA, Jessup DA, et al. Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001. J Wildl Dis 2003;39:495-509.
3. Richardson PMC, McKenna WM, Bristow MM, et al. Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of Cardiomyopathies. Circulation 1996;93:841-842.
4. D'Ambrosio A, Patti G, Manzoli A, et al. The fate of acute myocarditis between spontaneous improvement and evolution to dilated cardiomyopathy: a review. Heart 2001;85:499-504.
5. Dec GWJ, Palacios IF, Fallon JT, et al. Active myocarditis in the spectrum of acute dilated cardiomyopathies. Clinical features, histologic correlates, and clinical outcome. N Engl J Med 1985;312:885-890.
6. Friman G, Wesslen L, Fohlman J, et al. The epidemiology of infectious myocarditis, lymphocytic myocarditis and dilated carchomyopathy. Eur Heart J 1995;16:36-41.
7. Liu PP, Mason JW. Advances in the understanding of myocarditis. Circulation 2001;104:1076-1082.
8. Maisch B, Ristic AD, Portig I, et al. Human viral cardiomyopathy. Front Biosci 2003;8:s39-s67.
9. Barker IK, Parrish CR. Parvovirus infections In: Williams ES, Barker IK, eds. Infectious diseases of wild mammals. 3rd ed. Ames, Iowa: Iowa State University Press, 2001;131-146.
10. Woods LW. Adenoviral diseases In: Williams ES, Barker IK, eds. Infectious diseases of wild mammals. 3rd ed. Ames, Iowa: Iowa State University Press, 2001;202-212.
11. Blanchard J, Soike K, Baskin G. Encephalomyocarditis virus infection in African green and squirrel monkeys: comparison of pathological effects. Lab Anim Sci 1987;37:635-639.
12. Hubbard G, Soike K, Butler T, et al. An encephalomyocarditis virus epizootic in a baboon colony. Lab Anim Sci 1992; 42:233-239.
13. Gainer J, Sandefur J, Bigler W. High mortality in a Florida swine herd infected with the encephalomyocarditis virus. Cornell Vet 1968; 58:31-47.
14. Wells S, Gutter A. Encephalomyocarditis virus: epizootic in a zoological collection. J Zoo Wildl Med 1989;20:291-296.
15. Reddacliff L, Kirkland P, Hartley W et al. Encephalomyocarditis virus infections in an Australian zoo. J Zoo Wildl Med 1997;28:153-157.
16. Grobler DG, Raath JP, Braack LEO, et al. An outbreak of encephalomyocarditis-virus infection in free-ranging African elephants in the Kruger National Park. Onderstepoort J Vet Res 1995;62:97-108.
17. Maxson TR, Meurs KM, Lehmkuhl LB, et al. Polymerase chain reaction analysis for viruses in paraffin-embedded myocardium from dogs with dilated cardiomyopathy or myocarditis. Am J Vet Res 2001;62:130-135.
18. Tidholm A, Haggstrom J, Borgarelli M, et al. Canine idiopathic dilated cardiomyopathy Part I: aetiology, clinical characteristics, epidemiology and pathology. Vet J 2001; 162:92-107.
19. Levitan M, Murphy J, Sherwood W, et al. Adult onset systemic carnitine deficiency: favorable response to L-carnitine supplementation. Can J Neurol Sci 1987;14:50-54.
20. Waber L, Valle D, Neill C, et al. Carnitine deficiency presenting a familial cardiomyopathy: a treatable defect in carnitine transport. J Pediatr 1982;101:700-705.
21. Keene BW. Myocardial L-carnitine deficiency in a family of dogs with dilated cardiomyopathy. J Am Vet Med Assoc 1991;198:647-650.
22. Hoppel C, Tandler B, Parland S, et al. Hamster cardiomyopathy. A defect in oxidative phosphorylation in the cardiac interfibrillar mitochondria. J Biol Chem 1982;257:1540-1548.
23. Zaugg CE, Spaniol M, Kaufmann P, et al. Myocardial function and energy metabolism in carnitine-deficient rats. Cell Mol Life Sci 2003;60:767-775.
24. Pion PD, Kittleson D, Rogers QR, et al. Myocardial failure in cats associated with low plasma taurine: a reversible cardiomyopathy. Science 1987;237:764-768.
25. Nafstad I, Tollersrud S. The vitamin-E deficiency syndrome in pigs. I. Pathological changes. Acta Vet Scand 1970;11:452-480.
26. Miller M, Gardner IA, Packham A, et al. Evaluation and application of an indirect fluorescent antibody test (IFAT) for detection of Toxoplasma gondii in sea otters (Enhydra lutris). J Parasitol 2002;88:594-599.
27. Cole RA, Lindsay DS, Howe DK, et al. Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). J Parasitol 2000;86:526-530.
28. Miller MA, Crosbie PR, Sverlow K, et al. Isolation and characterization of Sarcocystis from brain tissue of a free-living southern sea otter (Enhydra lutris nereis) with fatal meningoencephalitis. Parasitol Res 2001;87:252-257.
29. Hofman P, Drici M, Gibelin P, et al. Prevalence of toxoplasma myocarditis in patients with the acquired immunodeficiency syndrome. Br Heart J 1993;70:376-381.
30. Matturri L, Quattrone P, Varesi C, et al. Cardiac toxoplasmosis in pathology of acquired immunodeficiency syndrome. Panminerva Med 1990;32:194-196.
31. Arnold SJ, Kinney MC, McCormick MS, et al. Disseminated toxoplasmosis: unusual presentations in the immunocompromised host. Arch Pathol Lab Med 1997;121:869-873.
32. Migaki G, Allen JF, Casey HW. Toxoplasmosis in a California sea lion. Am J Va Res 1977;38:135-136.
33. Holshuh HJ, Sherrod AE, Taylor CR, et al. Toxoplasmosis in a feral northern fur seal. J Am Vet Med Assoc 1985;187:1229-1230.
34. Inskeep W, Gardiner CH, Harris RK, et al. Toxoplasmosis in Atlantic bottle-nosed dolphins (Tursiops truncatas). J Wildl Dis 1990;26:377-382.
35. Hamir A, Dubey J. Myocarditis and encephalitis associated with Sarcocystis neurona infection in raccoons (Procyon lotor). Vet Parasitol 2001;95:335-340.
36. Lindsay D, Thomas NJ, Dubey JP. Biological characterization of Sarcocystis neurona isolated from a southern sea otter (Enhydra lutris nereis). Int J Parasitol 2000;30:617-624.
37. Silvagni P, Lowenstine LJ, Spraker T, et al. Domoic acid toxicity in California sea lions. Vet Pathol 2004;in press.
38. Scholin CA, Gulland F, Doucette GJ, et al. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 2000;403:80-84.
39. Gulland FMD, Haulena M, Fauquier D, et al. Domoic acid toxicity in California sea lions (Zalophus californianus): clinical signs, treatment, and survival. Vet Rec 2002;150:475-480.
40. Schwartz JA, Aldridge B, Blanchard M, et al. The development of methods for immunophenotypic and lymphocyte function analyzes for assessment of southern sea otter (Enhydra lutris nereis) health. Vet Immunol Immunopathol 2004;in press.
41. Miller MA, Sverlow K, Crosbie P, et al. Isolation and charcterization of protozoal parasites from a pacific harbor seal (Phoca vitulina richardsi) with meningoencephalitis. J Parasitol 2001;87:816-822.
42. Arkush KD, Miller MA, Leutenegger CM, et al. Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int J Parasitol 2003;33:1087-1097.
43. Brewer LA, Lwamba HC, Murtaugh MP, et al. Porcine encephalomyocarditis virus persists in pig myocardium and infects human myocardial cells. J Virol 2001;75:11621-11629.
44. Kassimi LB, Gonzague M, Boutrouille A, et al. Detection of encephalomyocarditis virus in clinical samples by immunomagnetic separation and one-step RT-PCR. J Virol Methods 2002;101:197-206.
45. Tracy ML, Moller G. Continuous flow vapor generation for inductively coupled argon plasma spectrometric analysis. Part 1: Selenium. J Assoc Off Anal Chem 1990;73:404-410.
46. Welz B, Melcher M. Decomposition of marine biologocal tissues for determination of aresnic, selenium, and mercury using hydride generation and cold-vapor atomic absorption spectrometers. Anal Chem 1985;57:427-431.
47. McMurray C, Blanchflower W. Application of a high-performance liquid chromatography fluorescence method for the rapid determination of alpha-tocopherol in the plasma of cattle and pigs and its comparison with direct fluorescence and high-performance liguid chromatography-ultraviolet detection methods. J Chromatogr 1979; 178:525-531.
48. Miller K, Lorr N, Yang C. Simultaneous determination of plasma retinol, alpha-tocopherol, lycopene, alpha-carotene, and beta-carotene by high-performance liquid chromatography. Anal Biochem 1984;138:340-345.
49. Pacioretty L, Hickman M, Morris J, et al. Kinetics of taurine depletion and repletion in plasma, serum, whole blood, and skeletal muscle in cats. Amino Acids 2001;21:417-427.
50. Parvin R, Pande S. Microdetermination of (-)carnitine and carnitine acetyl transferase. Anal Biochem 1977;79:190-201.
51. Suzuki CAM, Hierlihy SL. Renal clearance of domoic acid in the rat. Food Chem Toxicol 1993;31:701-706.
52. Horner RA, Kusske MB, Moynihan BP, et al. Retention of domoic acid by Pacific razor clams, Siliqua patula (Dixon, 1789): preliminary study. J Shellfish Res 1993;12:451-456.
53. Kulldorf M, Athas W, Feuer E, et al. Evaluating cluster alarms: a space-times can statistic and brain cancer in Los Alamos. Am J Public Health 1998;88:1377-1380.
54. Kulldorf M, Nagarwalla N. Spatial disease clusters: detection and inference. Stat Med 1995;14:799-810.
55. Stanek JF, Dubey JP, Oglesbee MJ, et al. Life cycle of Sarcocystis neurona in its natural intermediate host, the raccoon, Procyon lotor. J Parasitol 2002;88:1151-1158.
56. Miller MA, Gardner I, Kreuder C, et al. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nercis). Int J Parasitol 2002;32:997-1006.
57. Altwein DM, Foster K, Doose G, et al. The detection and distribution of the marine neurotoxin domoic acid on the Pacific coast of the United States 1991-1993. J Shellfish Res 1995;14:217-222.
58. Ferdin ME, Kvitek RG, Bretz CK, et al. Emerita analoga (Stimpson): possible new indicator species for the phycotoxin domoic acid in California coastal waters. Toxicon 2002;40:1259-1265.
59. Berman FW, LePage KT, Murray TF. Domoic acid neurotoxicity in cultured cerebellar granule neurons is controlled preferentially by the NMDA receptor Ca(2+) influx pathway. Brain Res 2002;924:20-29.
60. Mos L. Domoic acid: a fascinating marine toxin. Environ Toxicol Pharmacol 2001;9:79-85.
61. Corbett EK, Saba S, Deuchars J, et al. Ionotropic glutamate receptor subunit immunoreactivity of vagal preganglionic neurones projecting to the rat heart. Auton Neurosci 2003;105:105-117.
62. Gill SS, Mueller RW, McGuire PF, et al. Potential target sites in peripheral tissues for excitatory neurotransmission and excitotoxicity. Toxicol Pathol 2000;28:277-284.
63. Mueller RW, Gill SS, Pulido OM. The monkey (Macaca fascicularis) heart neural structures and conducting system: An immunochemical study of selected neural biomarkers and glutamate receptors. Toxicol Pathol 2003;31:227-234.
64. Gill S, Pulido O, Mueller R, et al. Molecular and immunological characterization of the ionotropic glutamate receptors in the rat heart. Brain Res Bull 1998;46:429-434.
65. DiMicco J, Monroe AJ. Stimulation of metabotropic glutamate receptors in the dorsomedial hypothalamus elevates heart rate in rats. Am J Physiol 1996;270:R1115-R1121.
66. Rockhold RW, Acuff CG, Clower BR. Excitotoxin-induced myocardial necrosis. Eur J Pharmacol 1989;166:571-576.
67. Kang YJ. Molecular and cellular mechanisms of cardiotoxicity. Environ Health Perspect 2001;109:27-34.
68. Cao Y, Kennedy R, Klimberg VS. Glutamine protects against doxorubicin-induced cardiotoxicity. J Surg Res 1999;85:178-182.
69. Rebouche CJ, Engel AG. Carnitine metabolism and deficiency syndromes. Mayo Clin Proc 1983;58:533-540.
70. Llansola M, Erceg S, Hernandez-Viadel M, et al. Prevention of ammonia and glutamate neurotoxicity by carnitine: molecular mechanisms. Metab Brain Dis 2002;17:389-397
71. Bigini P, Larini S, Pasquali C, et al. Acetyl-L-carnitine shows neuroprotective and neurotrophic activity in primary culture of rat embryo motoneurons. Neurosci Lett 2002;329:334-338.
72. Forloni G, Angeretti N, Smiroldo S. Neuroprotective activity of acetyl-L-carnitine: studies in vitro. J Neurosci Res 1994; 37:92-96.
73. Felipo V, Minana MD, Cabedo H, et al. L-carnitine increases the affinity of glutamate for quisqualate receptors and prevents glutamate neurotoxicity. Neurochem Res 1994;19:373-377.
74. Malone JI, Schocken DD, Morrison AD, et al. Diabetic cardiomyopathy and carnitine deficiency. J Diabetes Complications 1999;13:86-90.
75. Broderick TL, Panagakis G, DiDomenico D, et al. L-carnitine improvement of cardiac function is associated with a stimulation in glucose but not fatty acid metabolism in carnitine-deficient hearts. Cardiovasc Res 1995;30:815-820.
76. Zaugg CE, Spaniol M, Kaufmann P, et al. Myocardial function and energy metabolism in carnitine-deficient rats. Cell Mol Life Sci 2003;60:767-775.
77. Pierpont ME, Foker JE, Pierpont GL. Myocardial carnitine metabolism in congestive heart failure induced by incessant tachycardia. Basic Res Cardiol 1993;88:362-370.
78. Mc Entee K, Flandre T, Dessy C, et al. Metabolic and structural abnormalities dogs with early left ventricular dysfunction induced by incessant tachycardia. Am J Vet Res 2001;62:889-894.