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• W4295678306 abstract "Vol. 130, No. 9 Invited PerspectiveOpen AccessInvited Perspective: The Relevance of Animal Models of Domoic Acid Neurotoxicity to Human Healthis accompanied byProlonged, Low-Level Exposure to the Marine Toxin, Domoic Acid, and Measures of Neurotoxicity in Nonhuman Primates Lynn M. Grattan Lynn M. Grattan Address correspondence to Lynn M. Grattan, University of Maryland School of Medicine, 16 S. Eutaw St., 3rd Floor–Neurology, Baltimore, MD 21201 USA. Email: E-mail Address: [email protected] https://orcid.org/0000-0001-6509-2186 University of Maryland School of Medicine, Baltimore, Maryland, USA Search for more papers by this author Published:14 September 2022CID: 091302https://doi.org/10.1289/EHP11774AboutSectionsPDF ToolsDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InReddit On 18 August 1961, the Santa Cruz Sentinel reported1 that thousands of “crazed seabirds” were diving into lamp posts, buildings, cars, and streets to their death on the shores of North Monterey Bay, California. The birds appeared to be confused and disoriented, exhibited seizure activity, and flew at terrified residents. Eight people were bitten, but none suffered a related illness. Alfred Hitchcock contacted the newspaper for details. As the story is told, the Hollywood movie producer used the incident as research material for the classic 1963 thriller The Birds. About 30 years later it was established that the culprit of this extreme event was an algal bloom of Pseudo-nitzchia, select species of which produce domoic acid (DA).2 DA is a potent neurotoxin that bioaccumulates in filter-feeding shellfish and subsequently enters the food web. DA has been responsible for multiple mass illness and mortality events of shore birds3 and marine4–6 and coastal-dwelling mammals,7 particularly on the U.S. Pacific Coast. These events provided opportunities to capture the naturally occurring physical, physiological, neurologic, cardiac, and behavioral impacts of DA exposure, as well as advance understanding of delayed effects, reexposures, and rehabilitation possibilities.8,9 Laboratory studies of zebrafish, shellfish, marine mammals, and mice further expanded the capacity for hypothesis testing relevant to protecting public health.10–12 Nonhuman primate studies, such as that presented by Petroff et al.8 in this issue of Environmental Health Perspectives, represent a unique opportunity to improve understanding of an important contemporary issue: the neural mechanisms underlying chronic exposure to presumably safe levels of DA.The potential risk of domoic acid to human health was first discovered in Montreal, Canada, in 1987. People who consumed mussels harvested from the Prince Edward Island region with high levels of DA suffered the acute onset of severe gastrointestinal and neurologic symptoms, which in some cases included seizures, coma, and even death.13,14 Many survivors were left with a permanent anterograde memory disorder, amnesic shellfish poisoning (ASP). Autopsy findings of patients with ASP and early nonhuman primate studies identified damage to the hippocampus as central to seizures and memory problems associated with DA neurotoxicity.14,15 In the aftermath of this outbreak, extensive research using shellfish, rodent, and nonhuman primate models helped establish current regulatory limits of 20 ppm, ostensibly preventing new cases of ASP.16–19However, the evidence collected over the past decade—which came from epidemiological cohort studies of at-risk Native American communities,20–22 surveys of recreational and subsistence razor clam harvesters,23 and risk assessments,24 combined with zebrafish25 and rodent,26,27 models—indicates that repeated, chronic exposure to DA at presumably safe levels (<20 ppm) may have neurotoxic effects impacting many people. Studies of coastal Native American communities with repetitive, low-level exposure for up to 8 y identified the hallmark memory problems associated with ASP in attenuated form.20,21 Similarly, problems with spatial memory were found in mice exposed to low levels of DA in the absence of other neurologic symptoms.10 A key finding of this mouse study was the reversibility of the spatial memory problems with exposure cessation, signaling optimism for chronically exposed people.Petroff et al.8 conducted many studies in their effort to identify the neural mechanisms of repeated dietary exposure to lower levels of DA upon brain systems, behavior, and adaptation in adult female Macaca fascicularis monkeys. The investigators did not find the expected hippocampal excitability in the low-dose monkeys compared with controls. They also did not find differences in hippocampal and thalamic volume connectivity based upon in-life magnetic resonance imaging. What they did find was a “subtle shift” in the molecular profile of the hippocampus, as well as in the microglia phenotype of the thalamus. With appropriate caution, the investigators interpreted this as an adaptive or compensatory response to lower-level DA exposures over time. This could potentially explain the relatively small effect size of memory decline in similarly exposed people. Moreover, it highlights the critical role of the thalamus in the physiological adaptation and recovery of cognitive functions after disruption that have been similarly reported after mild traumatic brain injury.27 The authors also considered the extent to which these adaptations increase vulnerability to subsequent brain insults, including aging, thus also contributing to the evolving science of brain reserve capacity.28The DA story started with birds and a movie. Along the way, investigative efforts using rodents, fish, marine mammals, wildlife, nonhuman primates, and cohorts of at-risk people complemented, challenged, and advanced science toward the goal of protecting public health. These integrated efforts need to continue toward identifying a simple, reliable biomarker for human exposure assessment; establishing human thresholds for neurotoxicity across the life span; reevaluating current DA regulatory levels for vulnerable populations; further examining the reversibility of chronic exposures; elucidating the interactions of repetitive low-level DA exposure with aging, other exposures, or illnesses; and identifying robust models of community engagement and education.References1. Trabing W. 1961. Seabird invasion hits coastal homes: thousands of birds floundering in streets. Santa Cruz Sentinel 105(195):1. https://history.santacruzpl.org/omeka/items/show/82839#?c=0&m=0&s=0&cv=0 [accessed 21 July 2022]. Google Scholar2. 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Crossref, Medline, Google Scholar6. Greig DJ, Gulland FMD, Kreuder C. 2005. A decade of live California sea lion (Zalophus californianus) strandings along the Central California Coast: causes and trends, 1991–2000. Aquat Mamm 31(1):11–22, 10.1578/AM.31.1.2005.11. Crossref, Google Scholar7. Moriarty ME, Tinker MT, Miller MA, Tomoleoni JA, Staedler MM, Fujii JA, et al.2021. Exposure to domoic acid is an ecological driver of cardiac disease in southern sea otters. Harmful Algae 101:101973, PMID: 33526183, 10.1016/j.hal.2020.101973. Crossref, Medline, Google Scholar8. Goldstein T, Mazet JAK, Zabka TS, Langlois G, Colegrove KM, Silver M, et al.2008. Novel symptomatology and changing epidemiology of domoic acid toxicosis in California sea lions (Zalophus californianus): an increasing risk to marine mammal health. Proc Biol Sci 275(1632):267–276, PMID: 18006409, 10.1098/rspb.2007.1221. Crossref, Medline, Google Scholar9. Thomas K, Harvey JT, Goldstein T, Barakos J, Gulland F. 2009. 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Environ Health Perspect 130(9):097003, 10.1289/EHP10923. Link, Google Scholar13. Perl TM, Bédard L, Kosatsky T, Hockin JC, Todd EC, Remis RS. 1990. An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N Engl J Med 322(25):1775–1780, PMID: 1971709, 10.1056/NEJM199006213222504. Crossref, Medline, Google Scholar14. Teitelbaum JS, Zatorre RJ, Carpenter S, Gendron D, Evans AC, Gjedde A, et al.1990. Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. N Engl J Med 322(25):1781–1787, PMID: 1971710, 10.1056/NEJM199006213222505. Crossref, Medline, Google Scholar15. Cendes F, Andermann F, Carpenter S, Zatorre RJ, Cashman NR. 1995. Temporal lobe epilepsy caused by domoic acid intoxication: evidence for glutamate receptor-mediated excitotoxicity in humans. Ann Neurol 37(1):123–126, PMID: 7818246, 10.1002/ana.410370125. Crossref, Medline, Google Scholar16. Scallet AC, Binienda Z, Caputo FA, Hall S, Paule MG, Rountree RL, et al.1993. Domoic acid-treated cynomolgus monkeys (M. fascicularis): effects of dose on hippocampal neuronal and terminal degeneration. Brain Res 627(2):307–313, PMID: 8298975, 10.1016/0006-8993(93)90335-K. Crossref, Medline, Google Scholar17. Quilliam MA, Wright JLC. 1989. The amnesic shellfish poisoning mystery. Anal Chem 61(18):1053A–1060A, PMID: 2802153, 10.1021/ac00193a002. Crossref, Medline, Google Scholar18. Wekell JC, Jurst J, Lefebvre KA. 2004. The origin of the regulatory limits for PSP and ASP toxins in shellfish. J Shellfish Res 23(3):927–930. https://www.researchgate.net/profile/Kathi-Lefebvre/publication/285809374_The_origin_of_the_regulatory_limits_for_PSP_and_ASP_toxins_in_shellfish/links/56c7544908ae5488f0d2cc3a/The-origin-of-the-regulatory-limits-for-PSP-and-ASP-toxins-in-shellfish.pdf. Google Scholar19. Wright JLC, Boyd RK, de Freitas ASW, Falk M, Foxall RA, Jamieson WD, et al.1989. 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Crossref, Medline, Google ScholarThe author declares she has nothing to disclose.FiguresReferencesRelatedDetailsRelated articlesProlonged, Low-Level Exposure to the Marine Toxin, Domoic Acid, and Measures of Neurotoxicity in Nonhuman Primates14 September 2022Environmental Health Perspectives Vol. 130, No. 9 September 2022Metrics About Article Metrics Publication History Manuscript received26 June 2022Manuscript revised11 August 2022Manuscript accepted11 August 2022Originally published14 September 2022 Financial disclosuresPDF download License information EHP is an open-access journal published with support from the National Institute of Environmental Health Sciences, National Institutes of Health. All content is public domain unless otherwise noted. Note to readers with disabilities EHP strives to ensure that all journal content is accessible to all readers. However, some figures and Supplemental Material published in EHP articles may not conform to 508 standards due to the complexity of the information being presented. If you need assistance accessing journal content, please contact [email protected]. Our staff will work with you to assess and meet your accessibility needs within 3 working days." @default.
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