Exploration of Serum Cardiac Troponin I as a Biomarker of Cardiomyopathy in Southern Sea Otters (Enhydra lutris nereis)
IAAAM 2022
Megan E. Moriarty1*+; Melissa A. Miller2; Michael J. Murray3; Pádraig J. Duignan4; Catherine T. Gunther-Harrington5; Cara L. Field4; Lance M. Adams6; Todd L. Schmitt7; and Christine K. Johnson1
1Karen C. Drayer Wildlife Health Center and EpiCenter for Disease Dynamics, One Health Institute, University of California, Davis School of Veterinary Medicine, Davis, CA, USA; 2Marine Wildlife Veterinary Care and Research Center, California Department of Fish and Wildlife, Santa Cruz, CA, USA; 3The Monterey Bay Aquarium, Monterey, CA, USA; 4The Marine Mammal Center, Sausalito, CA, USA; 5University of California, Davis School of Veterinary Medicine, Department of Medicine & Epidemiology, Davis, CA, USA; 6Aquarium of the Pacific, Long Beach, CA, USA; 7SeaWorld Animal Health and Rescue Center, San Diego, CA, USA

Abstract

Southern sea otters (Enhydra lutris nereis) are a federally listed threatened species that is intensively managed to help ensure population recovery. A recent study found that cardiomyopathy was a primary or contributing cause of death in 41% (229/552) of free-ranging otters that underwent necropsy from 1998 to 2012.1 This prevalent condition is often identified during postmortem examination, and antemortem diagnosis remains challenging, owing in part to a lack of overt clinical signs in the early to mid-stages of cardiomyopathy and a scarcity of analytic tools. The southern sea otter research, rescue, and rehabilitation community was in a unique position to bridge this knowledge gap by combining information from comprehensive necropsies and clinical case management of otters at aquariums and rehabilitation centers.

Cardiomyopathy in sea otters is a multifactorial condition, with protozoal infection and domoic acid exposure identified as risk factors. The protozoan parasites Toxoplasma gondii and Sarcocystis neurona cause neurological disease and cardiac abnormalities in sea otters.1,2,3 Domoic acid is a neurotoxin produced by harmful algae and is also associated with cardiovascular disease in sea otters1,2,4,5 and California sea lions (Zalophus californianus).6 The lack of clinical tools to detect cardiomyopathy has impeded the ability to provide optimal medical care to sea otters in various settings. Reliable biomarkers are needed to confirm a diagnosis, provide prognostic information, and identify cardiac damage. Cardiac troponins are highly conserved blood-based biomarkers of myocardial damage in mammals that are detectable by a highly sensitive immunoassay.7

The objective of this study was to compare cardiac troponin I (cTnI) concentrations in antemortem serum from sea otters with and without cardiomyopathy and describe two cases of cardiomyopathy with different etiologies. Serum cTnI concentration was measured in live sea otters: 25 free-ranging otters with (n=14; cases) and without (11; controls) cardiomyopathy and 17 healthy managed otters from aquariums or rehabilitation centers (controls). Histopathologic and gross necropsy findings were used to classify cardiomyopathy status in free-ranging otters; physical examination and echocardiography were used to assess health status of managed otters. Two otters received extensive medical evaluations under managed care, including diagnostic imaging, serial cTnI concentration measurement, and necropsy. A significant difference in cTnI concentrations was observed between cases and both control groups, with median values of 0.279 ng/mL for cases and <0.006 ng/mL for free-ranging and managed controls. A cutoff value of ≥0.037 ng/mL yielded respective sensitivity and specificity estimates for detection of cardiomyopathy of 64.3% and 90.9% for free-ranging cases versus free-ranging controls and 64.3% and 94.1% for free-ranging cases versus managed controls.

Serum cTnI concentration has promise as a biomarker for detection of cardiomyopathy in sea otters. It has the potential to greatly improve our ability to diagnose cardiac disease, particularly when combined with other clinical tools. Serial cTnI testing will be particularly useful for long-term management of chronic cardiac conditions in managed sea otters. Measurement of serum cTnI concentration may also provide prognostic information for injured and diseased free-ranging sea otters related to the likelihood of successful rehabilitation and release.

Acknowledgments

Funded by the California Department of Fish and Wildlife’s Oil Spill Prevention and Administration Fund through the Oiled Wildlife Care Network at the Karen C. Drayer Wildlife Health Center, School of Veterinary Medicine, University of California-Davis.

The authors thank Francesca Batac, Erin Dodd, Barbie Halaska, Jaclyn Isbell, and Carlos Rios for providing the laboratory samples and data; Shawn Johnson, Emily Whitmer, Abby McClain, Brittany Stevens, and Christine Parker-Graham for providing veterinary care and expertise, with assistance from Marissa Young, Erin Lenihan, Jessica Folck, Lauren Campbell, Sophie Guarasci, Sarah Pattison, and Juli Barron; Chris DeAngelo and Karl Mayer for providing animal care; and Robynne Gomez and Phillip Guadiano for performing the cTnI assays.

Literature Cited

1.  Miller MA, Moriarty ME, Henkel LA, et al. 2020. Predators, disease, and environmental change in the nearshore ecosystem: mortality in southern sea otters (Enhydra lutris nereis) from 1998–2012. Front Mar Sci 7:582.

2.  Kreuder C, Miller MA, Lowenstine LJ, et al. 2005. Evaluation of cardiac lesions and risk factors associated with myocarditis and dilated cardiomyopathy in southern sea otters (Enhydra lutris nereis). Am J Vet 66:289–299.

3.  Miller MA, Conrad PA, Harris M, et al. 2010. A protozoal-associated epizootic impacting marine wildlife: mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Vet Parasitol172:183–194.

4.  Moriarty ME, Tinker MT, Miller MA, et al. 2021. Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters. Harmful Algae 101:101973.

5.  Miller MA, Moriarty ME, Duignan PJ, et al. 2021. Clinical signs and pathology associated with domoic acid toxicosis in southern sea otters (Enhydra lutris nereis). Front Mar Sci 8:208.

6.  Zabka TS, Goldstein T, Cross C, et al. 2009. Characterization of a degenerative cardiomyopathy associated with domoic acid toxicity in California sea lions (Zalophus californianus). Vet Pathol 46:105–119.

7.  Langhorn R, Willesen JL. 2016. Cardiac troponins in dogs and cats. J Vet Intern Med 30:36–50.

Speaker Information
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Megan E. Moriarty
Karen C. Drayer Wildlife Health Center and EpiCenter for Disease Dynamics, One Health Institute
University of California, Davis School of Veterinary Medicine
Davis, CA, USA


MAIN : Session 3: <i>In Situ</i> Health : Southern Sea Otter Cardiomyopathy: cTnI
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