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      Saxitoxin Puffer Fish Poisoning in the United States, with the First Report of Pyrodinium bahamense as the Putative Toxin Source

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          Abstract

          Background

          From January 2002 to May 2004, 28 puffer fish poisoning (PFP) cases in Florida, New Jersey, Virginia, and New York were linked to the Indian River Lagoon (IRL) in Florida. Saxitoxins (STXs) of unknown source were first identified in fillet remnants from a New Jersey PFP case in 2002.

          Methods

          We used the standard mouse bioassay (MBA), receptor binding assay (RBA), mouse neuroblastoma cytotoxicity assay (MNCA), Ridascreen ELISA, MIST Alert assay, HPLC, and liquid chromatography-mass spectrometry (LC-MS) to determine the presence of STX, decarbamoyl STX (dc-STX), and N-sulfocarbamoyl (B1) toxin in puffer fish tissues, clonal cultures, and natural bloom samples of Pyrodinium bahamense from the IRL.

          Results

          We found STXs in 516 IRL southern ( Sphoeroides nephelus), checkered ( Sphoeroides testudineus), and bandtail ( Sphoeroides spengleri) puffer fish. During 36 months of monitoring, we detected STXs in skin, muscle, and viscera, with concentrations up to 22,104 μg STX equivalents (eq)/100 g tissue (action level, 80 μg STX eq/100 g tissue) in ovaries. Puffer fish tissues, clonal cultures, and natural bloom samples of P. bahamense from the IRL tested toxic in the MBA, RBA, MNCA, Ridascreen ELISA, and MIST Alert assay and positive for STX, dc-STX, and B1 toxin by HPLC and LC-MS. Skin mucus of IRL southern puffer fish captive for 1-year was highly toxic compared to Florida Gulf coast puffer fish. Therefore, we confirm puffer fish to be a hazardous reservoir of STXs in Florida’s marine waters and implicate the dinoflagellate P. bahamense as the putative toxin source.

          Conclusions

          Associated with fatal paralytic shellfish poisoning (PSP) in the Pacific but not known to be toxic in the western Atlantic, P. bahamense is an emerging public health threat. We propose characterizing this food poisoning syndrome as saxitoxin puffer fish poisoning (SPFP) to distinguish it from PFP, which is traditionally associated with tetrodotoxin, and from PSP caused by STXs in shellfish.

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          Most cited references34

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          A Review of the Effects of Algal Blooms on Shellfish and Aquaculture

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            Three novel hydroxybenzoate saxitoxin analogues isolated from the dinoflagellate Gymnodinium catenatum.

            In a recent survey of paralytic shellfish poisoning (PSP) toxins in Gymnodinium catenatum Graham extracts, using LC with postcolumn oxidation and fluorescence detection, three novel saxitoxin analogues were revealed in isolates from several locations, including Australian waters. We have named them as G. catenatum toxins, GC1 (1), GC2 (2), and GC3 (3). The compounds were isolated from a culture of the Australian strain by LC-MS-guided fractionation employing a C18-silica column and hydrophilic interaction chromatography. The unusual structures of these novel compounds were characterized by low- and high-resolution MS, MS/MS, and NMR spectroscopy. GC3 (3) was found to be the 4-hydroxybenzoate ester derivative of decarbamoylsaxitoxin, while GC1 (1) and GC2 (2) are the epimeric 11-hydroxysulfate derivatives of GC3 (3).
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              Occurrence of saxitoxins as a major toxin in the ovary of a marine puffer Arothron firmamentum.

              Eleven male and 14 female specimens of a marine puffer Arothron firmamentum were collected from Oita and Iwate Prefectures, Japan. The toxicity assay using mouse showed that only ovary and skin of the female specimens were toxic, the toxicity scores being 5-740 as paralytic shellfish poison and <5-30 MU/g as tetrodotoxin (TTX), respectively. The toxin extracts from the both tissues were then treated with cartridge columns, and subjected to high performance liquid chromatography and liquid chromatography-mass spectral analyses. In the analyses, saxitoxin (STX) and decarbamoylSTX (dcSTX) were identified as the major toxins in the ovary, while the skin contained only TTX.
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                Author and article information

                Journal
                Environ Health Perspect
                Environmental Health Perspectives
                National Institute of Environmental Health Sciences
                0091-6765
                October 2006
                6 July 2006
                : 114
                : 10
                : 1502-1507
                Affiliations
                [1 ] Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, St. Petersburg, Florida, USA
                [2 ] Food and Drug Administration, Center for Food Safety and Applied Nutrition, Laurel, Maryland, USA
                [3 ] Food and Drug Administration, Office of the Commissioner, Rockville, Maryland, USA
                [4 ] Food and Drug Administration, Center for Food Safety and Applied Nutrition, College Park, Maryland, USA
                [5 ] Food and Drug Administration, Center for Food Safety and Applied Nutrition, Gulf Coast Seafood Laboratory, Dauphin Island, Alabama, USA
                [6 ] National Oceanic and Atmospheric Administration, National Ocean Service, Center for Coastal Environmental Health and Biomolecular Research, Charleston, South Carolina, USA
                [7 ] Key Laboratory of Science and Engineering for Marine Ecology and Environment, First Institute of Oceanography, State Oceanic Administration, Qingdao, China
                [8 ] Florida Institute of Oceanography, University of South Florida, St. Petersburg, Florida, USA
                Author notes
                Address correspondence to J.H. Landsberg, Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 100 Eighth Ave. SE, St. Petersburg, FL 33701 USA. Telephone: (727) 896-8626. Fax: (727) 893-9840. E-mail: jan.landsberg@ 123456myfwc.com

                The authors declare they have no competing financial interests.

                Article
                ehp0114-001502
                10.1289/ehp.8998
                1626430
                17035133
                243cef24-b4b8-4225-b9c2-9e7c63d73039
                This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original DOI
                History
                : 11 January 2006
                : 5 July 2006
                Categories
                Research

                Public health
                dinoflagellate,sphoeroides spp,puffer fish,pyrodinium bahamense,saxitoxins,saxitoxin puffer fish poisoning,harmful algae,florida

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