Pathology of Domoic Acid Toxicity in California Sea Lions (Zalophus californianus)

Abstract

Abstract. Over 100 free-ranging adult California sea lions (Zalophus californianus) and one Northern fur seal (Callorhinus ursinus), predominantly adult females, were intoxicated by domoic acid (DA) during three harmful algal blooms between 1998 and 2000 in central and northern California coastal waters. The vector prey item was Northern anchovy (Engraulis mordax) and the primary DA-producing algal diatom was Psuedonitzschia australis. Postmortem examination revealed gross and histologic findings that were distinctive and aided in diagnosis. A total of 109 sea lions were examined, dying between 1 day and 10 months after admission to a marine mammal rehabilitation center. Persistent seizures with obtundation were the main clinical findings. Frequent gross findings in animals dying acutely consisted of piriform lobe malacia, myocardial pallor, bronchopneumonia, and complications related to pregnancy. Gross findings in animals dying months after intoxication included bilateral hippocampal atrophy. Histologic observations implicated limbic system seizure injury consistent with excitotoxin exposure. Peracutely, there was microvesicular hydropic degeneration within the neuropil of the hippocampus, amygdala, pyriform lobe, and other limbic structures. Acutely, there was ischemic neuronal necrosis, particularly apparent in the granular cells of the dentate gyrus and the pyramidal cells within the hippocampus cornu ammonis (CA) sectors CA4, CA3, and CA1. Dentate granular cell necrosis has not been reported in human or experimental animal DA toxicity and may be unique to sea lions. Chronically, there was gliosis, mild nonsuppurative inflammation, and loss of laminar organization in affected areas.Key words: Amnesic shellfish poisoning; California sea lions; domoic acid; excitotoxin; marine toxin; neurotoxin; red tide; seizure; Zalophus californianus. Domoic acid (DA) is a neurotoxic analog of the excitatory neurotransmitter L-glutamate. DA is produced by marine algae of several genera and has been identified from the North Atlantic, Pacific, Gulf of Mexico, Sea of Japan, and European and New Zealand coastal waters. Toxic exposures to DA usually occur in the context of harmful algal blooms (HAB) created when local water conditions foster explosive growth of a toxigenic algal species. DA produced during a HAB may undergo trophic transfer by accumulating in algivorous or filter-feeding species such as anchovy, 13 Dungeness crab, razor clam, 36 or mussels. 19 Other algal toxins of concern in US waters include saxitoxin, brevetoxin, okadaic acid, ciguatoxin, and Pfeisteria-associated toxin. DA gained notoriety as the causative agent of amnesic shellfish poisoning in 1987, when human consumption of contaminated mussels led to illness and deaths. 19 DA may also pose a risk to marine wildlife and has caused mass mortalities of seabirds 25,37 and marine mammals. Initially described as the antihelmintic component of ''domoi,'' a Japanese folk medicine derived from the red algae Chondria armata, 28 DA is a potent agonist of the alph...

Neuroanatomy and Volumes of Brain Structures of a Live California Sea Lion (Zalophus californianus) From Magnetic Resonance Images

“…Of particular concern are the acute, chronic, and possible developmental effects of DA on the brain of California sea lions (Silvagni et al, 2005;Goldstein et al, 2008; as reviewed by Ramsdell and Zabka, 2008). The MRI atlas presented here of a neurologically normal California sea lion will allow us to better evaluate the hippocampus in the oblique plane and determine the volumes of brain structures.…”

“…Sea lions that died acutely and contained detectable levels of DA in blood and urine exhibited lesions in the limbic system (Scholin et al, 2000). These lesions were characterized by neuronal necrosis in the hippocampal formation, specifically granule cells in the dentate gyrus and pyramidal cells in sectors CA4, CA3, and CA1 of the cornu ammonis (Silvagni et al, 2005).…”

Ischemic Cardiomyopathy Following Seizure Induction by Domoic Acid

“…26,27 Cardiac lesions within a Californian sea otter population have been described to include myocardial pallor and multifocal myocardial necrosis associated with myocardial hemorrhage. Inflammatory cells were also observed in both the atrial and ventricular myocardium.…”

Volumetric Neuroimaging of the Atlantic White‐Sided Dolphin (Lagenorhynchus acutus) Brain from in situ Magnetic Resonance Images

“…These include anthropogenic chemicals such as hydroxylated polychlorinated biphenyls (OH-PCBs; Sandala et al, 2004;Houde et al, 2006;McKinney et al, 2006) and polybrominated diphenyl ethers (PBDEs; De Boer et al, 1998), as well as biotoxins from harmful algal blooms (Scholin et al, 2000). These chemicals can target the brain (Viberg et al, 2003;Kimura-Kuroda et al, 2005;Silvagni et al, 2005). For example, domoic acid (a type of biotoxin produced by some diatom Pseudo-nitzschia species and associated with harmful algal blooms) is neurotoxic and has been shown to cause bilateral hippocampal atrophy in California sea lions (Silvagni et al, 2005).…”

“…These chemicals can target the brain (Viberg et al, 2003;Kimura-Kuroda et al, 2005;Silvagni et al, 2005). For example, domoic acid (a type of biotoxin produced by some diatom Pseudo-nitzschia species and associated with harmful algal blooms) is neurotoxic and has been shown to cause bilateral hippocampal atrophy in California sea lions (Silvagni et al, 2005). It is possible that biotoxins and environmental pollutants cause subtle differences in the size of brain structures that are not detectable to the unaided eye; therefore, volumetric neuroimaging would be a valuable approach to identify subtle abnormalities.…”