Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-25T08:16:10.890Z Has data issue: false hasContentIssue false

Neurobehavioral effects of harmful algal bloom (HAB) toxins: A critical review

Published online by Cambridge University Press:  04 May 2005

MELISSA A. FRIEDMAN
Affiliation:
The NIEHS Marine and Freshwater Biomedical Sciences Center, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Florida Department of Neurology, University of Miami School of Medicine, Florida Dr. Friedman is now affiliated with Carlos Albizu University, Miami, Florida 33172
BONNIE E. LEVIN
Affiliation:
The NIEHS Marine and Freshwater Biomedical Sciences Center, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Florida Department of Neurology, University of Miami School of Medicine, Florida

Abstract

Human exposure to naturally occurring marine toxins has been associated with a range of neurobehavioral abnormalities. The toxins are produced by harmful algal blooms (HABs) and are typically contracted through seafood consumption. The primary target of many of the HAB toxins is the neurologic system, and the neurobehavioral symptoms associated with the HAB illnesses have influenced public health policy. The HAB-related illnesses most frequently linked to neuropsychological disturbance are Amnesic Shellfish Poisoning, Ciguatera Fish Poisoning, and Possible Estuarine Associated Syndrome, which is associated with exposure to the Pfiesteria piscicida organism. Although the neurophysiologic mechanisms underlying many of the HAB illnesses have been well delineated, the literature examining the neuropsychological impairments is unclear and needs to be defined. This review is intended to introduce an emerging area of study linking HAB illnesses with neuropsychological changes. (JINS, 2005, 11, 331–338.)

Type
CRITICAL REVIEW
Copyright
© 2005 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arena, P., Levin, B., Fleming, L.E., Friedman, M.A., & Blythe, D.G. (2004). A pilot study of the cognitive and psychological correlates of chronic ciguatera poisoning. Harmful Algae, 3, 5160.Google Scholar
Backer, L.C., Dickey, R., Poli, M., Davis, C., Luber, G., Friedman, M., Fleming, L.E., Patel, M., & Blythe, D. (2004). Development of a biological marker for exposure to ciguatera toxins. A poster presented at the 11th International Conference on Harmful Algae Blooms, Cape Town, South Africa.
Baden, D.G., Fleming, L.E., & Bean, J.A. (1995). Marine toxins. In F.A. de Wolff (Ed.), Handbook of clinical neurology, 21: Intoxications of the nervous system, Part II, pp. 141175. Amsterdam, The Netherlands: Elsevier Science BV.
Bagnis, R. (1992). Public health, epidemiological and socioeconomic patterns of Ciguatera in Tahiti (pp. 157168). In Proceedings of the Third International Conference on Ciguatera Fish Poisoning, April 30–May 5, 1990, La Parguera, Puerto Rico. Quebec: Polyscience Publications.
Bagnis, R., Kuberski, T., & Laugier, S. (1979). Clinical observation on 3009 cases of ciguatera (fish poisoning) in the South Pacific. American Tropical Medical Hygiene, 28, 10671073.Google Scholar
Barker, R. (1997). And the waters turned to blood. New York: Simon & Shuster.
Barton, E.D., Tanner, P., Turchen, S.G., Tunget, C.L., Manoguerra, A., & Clark, R.F. (1995). Ciguatera fish poisoning: A Southern California epidemic. The Western Journal of Medicine, 163, 3136.Google Scholar
Blythe, D., Fleming, L.E., Ayyar, D.R., Baden, D., De Sylva, D., & Schrank, K. (1994). Mannitol treatment for acute and chronic ciguatera fish poisoning. Memoirs of the Queensland Museum, 34, 465470.Google Scholar
Blythe, D.G., De Sylva, D.P., Fleming, L.E., Ayyar, R.A., Baden, D.G., & Schrank, K. (1992). Clinical experience with i.v. Mannitol in the treatment of ciguatera. Bulletin Societal Pathologique Exp, 85, 425426.Google Scholar
Burkholder, J.M. & Glasgow, H.B. (2001). History of toxic Pfiesteria in North Carolina estuaries from 1991 to the present. BioScience, 51, 827841.CrossRefGoogle Scholar
Centers for Disease Control and Prevention (March 2004). About Harmful Algal Blooms. CDC Harmful Algal Blooms. Department of Health and Human Services. www.cdc.gov/hab/factsheet.pdf.
Dunn, J.T., Lees-Haley, P.R., Brown, R.S., Williams, C.W., & English, L.T. (1995). Neurotoxic complaint base rates of personal injury claimants: Implications for neuropsychological assessment. Journal of Clinical Psychology, 51, 577584.Google Scholar
Fleming, L.E., Backer, L., & Rowan, A. (2002). The epidemiology of human illnesses associated with harmful algal blooms. In D. Baden & D. Adams (Eds.), Neurotoxicology Handbook, Volume 1 (pp. 363381). Totowa, New Jersey: Humana Press, Inc.
Fleming, L.E., Bean, J.A., & Baden, D.G. (1995). Epidemiology of toxic marine phytoplankta. In G.M. Hallegraeff, D. Anderson, & A.D. Cembella (Eds.), UNESCO IOC manual on harmful marine phytoplankta (33) (pp. 475488). Paris, France: UNESCO.
Fleming, L.E., Easom, J., Baden, D., & Levin, B. (1999). Emerging harmful algal blooms and human health: Pfiesteria and related organisms. Toxicologic Pathology, 27, 573581.CrossRefGoogle Scholar
Fleming, L.E., Katz, D., Bean, J.A., & Hammond, R. (2001a). Epidemiology of seafood poisoning. In Y.H. Hui, D. Kitts, & P.S. Stanfield (Eds.), Foodborne disease handbook, 2nd Edition. New York: Marcel Dekker, Inc.
Fleming, L.E., Katz, D., Bean, J.A., & Hammond, R. (2001b). Epidemiology of Seafood Poisoning. In Y.H. Hui and D.D. Kits (Eds.) Seafood and Environmental Toxins, (pp. 287310). New York: Marcel Dekker.
Foo, S.J., Jeyatnam, J., & Koh, D. (1990). Chronic neurobehavioural effects of toluene. British Journal of Industrial Medicine, 47, 480484.Google Scholar
Gillespie, N.C., Lewis, R.J., Pearn, J.H., Bourke, A.T., Holmes, M.J., Bourke, J.B., & Shields, W.J. (1986). Ciguatera in Australia: Occurrence, clinical features, pathophysiology and management. The Medical Journal of Australia, 145, 584589.Google Scholar
Glasgow, H.B., Burkholder, J.M., Schmechel, D.E., Tester, P.A., & Rublee, P.A. (1995). Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health. Journal of Toxicology and Environmental Health, 46, 501522.CrossRefGoogle Scholar
Grant, M. (1997). The cell from hell. People, May 19, 1997.
Grattan, L.M. & Oldach, D. (1998). Learning and memory difficulties after environmental exposure to waterways containing toxin-producing pfiesteria or pfiesteria-like dinoflagellates. Lancet, 352, 532540.CrossRefGoogle Scholar
Grattan, L.M., Oldach, D., Tracy, J.K., & Greenberg, D.R. (1998). Neurobehavioral complaints of symptomatic persons exposed to Pfiesteria piscicida or morphologically related organisms. Maryland Medical Journal, 47, 127129.Google Scholar
Greenberg, D.R., Tracy, J.K., & Grattan, L.M. (1998). A critical review of the Pfiesteria hysteria hypothesis. Maryland Medical Journal, 47, 133136.Google Scholar
Griffin, J.R. (1997). Secretary John R. Griffin testimony before House Subcommittee on Fisheries Conservation, Wildlife and Oceans Committee on Resources. Maryland Department of Natural Resources. Chesapeake Bay Front Page (http://www.dnr.state.md.us).
Hudnell, K., House, D., Schmid, J., Koltai, D., Stopford, W., Wilkins, J., Savitz, D.A., Swinker, M., & Music, S. (2001). Human visual function in the North Carolina clinical study on possible estuary-associated syndrome. Journal of Toxicology and Environmental Health Part A, 62, 575594.Google Scholar
Hudnell, H.K. & Shoemaker, R.C. (2003). Neuropsychological testing versus visual contrast sensitivity: Response. Environmental Health Perspectives, 111, A14A15.CrossRefGoogle Scholar
Lees-Haley, P.R. (2000). Methodology in epidemiological studies of human neurobehavioral toxicity: A case study with critical review. Psychological Reports, 86, 85101.Google Scholar
Lees-Haley, P.R. & Williams, C.W. (1997). Neurotoxicity of chronic low-dose exposure to organic solvents: A skeptical review. Journal of Clinical Psychology, 53, 699712.3.0.CO;2-D>CrossRefGoogle Scholar
Lehane, L. & Lewis, R.J. (2000). Ciguatera: Recent advances but the risk remains. Journal of Food Microbiology, 61, 91125.CrossRefGoogle Scholar
Lewis, R.J. & King, G.K. (1996). Ciguatera (Fish Poisoning). In J.A. Williamson, P.J. Fenner, J.W. Burnett, & J.F. Rifkin (Eds.), Venomous and poisonous marine animals: A medical and biological handbook (pp. 346353). Sydney, Australia: University of New South Wales Press.
Lipton, D.W. (1998). Pfiesteria's economic impact on seafood industry sales and recreational fishing. Conference presentation, Pfiesteria: Where do we go from here? Economics of Policy Options for Nutrient Management and Dinoflagellates, Center for Agricultural and Natural Resource Policy, University of Maryland (www.arec.umd.edu/policycenter/Pfiesteria/brochure-front.htm).
Morrow, L.A., Kamis, H., & Hodgson, M.J. (1993). Psychiatric symptomatology in persons with organic solvent exposure. Journal of Consulting and Clinical Psychology, 61, 171174.Google Scholar
Olney, J.W., Teitelbaum, J., Pinsky, C., & Debonnel, G. (1990). Domoic acid toxicity. Panel Discussion: Treatment. Canada Diseases Weekly Report, Suppl. 1E, 117120.Google Scholar
Palafox, N.A., Jain, L.G., Pinano, A.Z., Gulick, T.M., Williams, R.K., & Schatz, I.J. (1988). Successful treatment of ciguatera fish poisoning with intravenous mannitol. Journal of the American Medical Association, 259, 27402742.Google Scholar
Perl, T.M., Bedard, L., Kosatsky, T., Hockin, J.C., Todd, E.C., & Remis, R.S. (1990). An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. New England Journal of Medicine, 322, 17751780.CrossRefGoogle Scholar
Quod, J.P. & Turquet, J. (1996). Ciguatera in Reunion Island (SW Indian Ocean): Epidemiology and clinical patterns. Toxicon, 34, 779785.CrossRefGoogle Scholar
Samet, J., Bignami, G.S., Feldman, R., Hawkins, W., Neff, J., & Smayda, T. (2001). Pfiesteria: Review of the science and identification of research gaps. Report for the National Center for Environmental Health, Centers for Disease Control and Prevention. Environmental Health Perspectives, 109, 639659.Google Scholar
Schmechel, D.E. & Koltai, D.C. (2001). Potential human health effects associated with laboratory exposures to Pfiesteria piscicida. Environmental Health Perspectives, 109, 775779.Google Scholar
Schreiber, J.S., Hudnell, H.K., Geller, A.M., House, D.E., Aldous, K.M., Force, M.S., Langguth, K., Prohonic, E.J., & Parker, J.C. (2002). Apartment residents' and day care workers' exposures to tetrachlorethylene and deficits in visual contrast sensitivity. Environmental Health Perspectives, 110, 655664.Google Scholar
Shoemaker, R.C. & Hudnell, H.K. (2001). Possible estuary-associated syndrome: Symptoms, vision and treatment. Environmental Health Perspectives, 109, 539545.Google Scholar
Simpson, T.W. (1998). A citizens guide to the Water Quality Improvement Act of 1998. Maryland Cooperative Extension, University of Maryland, College Park, Eastern Shore.
Snodgrass, S.R. (1990). Correspondence, neurologic sequelae after ingestion of mussels contaminated with domoic acid. New England Journal of Medicine, 323, 16311633.Google Scholar
Swinker, M., (2003). Neuropsychological testing versus visual contrast sensitivity in diagnosing PEAS. Environmental Health Perspectives, 111, A13A14.CrossRefGoogle Scholar
Swinker, M., Koltai, D., Wilkins, J., Hudnell, K., Hall, C., Darcey, D., Robertson, K., Schmechel, D., Stopford, W., & Music, S. (2001a). Estuary-associated syndrome in North Carolina: An occupational prevalence study. Environmental Health Perspectives, 109, 2126.Google Scholar
Swinker, M., Koltai, D., Wilkins, J., & Woodhall, S. (2001b). Is there an estuary-associated syndrome in North Carolina? Findings in a series of hotline callers. North Carolina Medical Journal, 62, 126132.Google Scholar
Teitelbaum, J.S., Zatorre, R.J., & Carpenter, S. (1990). Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. New England Journal of Medicine, 322, 17811787.CrossRefGoogle Scholar
Tryphonas, L. & Iverson, F. (1990). Neuropathology of excitatory neurotoxins: the domoic acid model. Toxicologic Pathology, 18 (1, Pt 2), 165169Google Scholar
Tryphonas, L., Truelove, J., & Iverson, F. (1990a). Acute parental neurotoxicity of domoic acid in cynomolgus monkeys. Toxicologic Pathology, 18, 297303.Google Scholar
Tryphonas, L., Truelove, J., Nera, E., & Iverson, F. (1990b). Acute neurotoxicity of domoic acid in the rat. Toxicologic Pathology, 18 (1, Pt 1), 19.Google Scholar
United States Environmental Protection Agency, Integrated Risk Information System (IRIS): Toluene (CASRN 108-88-2) (1992). http://www.epa.gov/iris/subst/0118.htm, http://cfpub.epa.gov/iris/quickview.cvm?substance_nmbr=0118
United States Food and Drug Administration, Foodborne Pathogenic Microorganisms and Natural Toxins Handbook (1992). http://www.cfsan.fda.gov/∼mow/chap37.html
University of Maryland (August 19, 1998). 6.3 million Federal grant funds Pfiesteria research; University of Maryland School of Medicine heads neurocognitive, neurotoxicologic studies. University of Maryland Press Release on Pfiesteria Grant. Press Contact: Jennifer Donovan. (http://www.niehs.nih.gov/oc/news/umdpfiesteria.html).
White, R.F., Feldman, R.G., & Proctor, S.P. (1992). Neurobehavioral effects of toxin exposures. In R.F. White (Ed.), Clinical Syndromes and Adult Neuropsychology. The Practitioner's Handbook, (pp. 151). Amsterdam, The Netherlands: Elsevier Science Publishers B.V.
White, R.F., Feldman, R.G., & Proctor, S.P. (2000). Neurotoxicology. In B.S. Fogel, R.B. Schiffer, & S.M. Rao (Eds.), Synopsis of neuropsychiatry, (pp. 503510). Philadelphia, Pennsylvania: Lippincott Williams & Wilkins.