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Saxitoxin puffer fish poisoning in the United States, with the first report of Pyrodinium bahamense as the putative toxin source.

Publication: Environmental Health Perspectives
Publication Date: 01-OCT-06
Format: Online
Delivery: Immediate Online Access
Full Article Title: Saxitoxin puffer fish poisoning in the United States, with the first report of Pyrodinium bahamense as the putative toxin source.(Research)

Article Excerpt
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 [micro]g STX equivalents (eq)/100 g tissue (action level, 80 [micro]g 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.

KEY WORDS: dinoflagellate, Florida, harmful algae, puffer fish, Pyrodinium bahamense, saxitoxin puffer fish poisoning, saxitoxins, Sphoeroides spp. Environ Health Perspect 114:1502-1507 (2006). doi:10.1289/ehp.8998 available via http://dx.doi.org/ [Online 6 July 2006]

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Puffer fish poisoning (PFP) is usually caused by ingestion of tetrodotoxins (TTXs) found naturally in certain species of puffer fish (Halstead 1967; Mosher and Fuhrmann 1984). In Japan, 20-100 people die annually from PFP, in spite of stringent controls by authorities (Ogura 1971). TTXs can cause fatal human poisoning, which is similar to paralytic shellfish poisoning (PSP) caused by saxitoxins (STXs). PSP is caused by the consumption of toxic shellfish (Shumway 1990) and rarely by fish that have have become toxic after feeding on STX-producing microalgae (Maclean 1979). As well as TTXs, STXs have also been found in at least 12 marine and freshwater puffer fish species in Asia (Ahmed et al. 2001; Kodama et al. 1983; Kungsuwan et al. 1997; Nakamura et al. 1984; Nakashima et al. 2004; Sato et al. 1997, 2000; Zaman et al. 1997), but their bioorigin has not been identified.

TTXs are chemically distinct from STXs, but both neurotoxins produce similar symptoms in mammals because they act on site 1 of the voltage-dependent sodium channel, blocking the influx of sodium into excitable cells and restricting signal transmission along nerve and muscle membranes (Ahmed 1991). The symptoms of traditional PFP from TTXs and of PSP from STXs include tingling and numbness of the mouth, lips, tongue, face, and fingers; paralysis of the extremities; nausea; vomiting; ataxia; drowsiness; difficulty in speaking; progressively decreasing ventilatory efficiency; and finally in extreme cases, death by asphyxiation caused by respiratory paralysis (Ahmed 1991; Catterall 1985; Kao 1993).

PFP cases in Europe (Kao 1993) and Mexico (Nunez-Vazquez et al. 2000) have occasionally been reported. In the United States, PFP has been associated with imports of puffer fish [Centers for Disease Control and Prevention (CDC) 1996]; rarely have fatalities occurred after the consumption of indigenous puffer fish. In Hawaii, white-spotted puffer fish, Arothron hispidus, were implicated in seven deaths (Ahmed 1991). Until 1974, seven PFP cases in Florida, outside of the Indian River Lagoon (IRL), were caused by the consumption of locally caught "blowfish" or puffer fish (Ahmed 1991; Benson 1956; Bigler 1999; Hemmert 1974; Mosher and Fuhrmann 1984). These cases included three fatalities, likely from TTX; for example, one woman died 45 min after consuming toxic liver from a checkered puffer fish (Sphoeroides testudineus) (Benson 1956). The toxins involved in the previous Florida PFP cases were not characterized, but because PFP is usually associated with TTX, investigators likely assumed that TTX was the cause (Benson 1956; Bigler 1999; Hemmert 1974). Tissues from Florida bandtail (Sphoeroides spengleri), checkered, and southern puffer fish (Sphoeroides nephelus) were found to be lethal in the mouse bioassay (MBA) (Burklew and Morton 1971; Lalone et al. 1963), but, again, the toxins were not determined.

Until January 2002 the harvest and consumption of puffer fish from the IRL was not a risk to public health. Since then (until May 2004), however, 28 PFP cases occurring in Florida (n = 21), New Jersey (n = 3), Virginia (n = 2), and New York (n = 2) caused by puffer fish originating from the IRL were reported (Bodager 2002; CDC 2002a, 2002b). Analyses of toxins from unidentified puffer fish fillet remnants from one of the early 2002 PFP cases in New Jersey revealed STXs (Quilliam et al. 2004), not TTXs, a distinction that alone could not be made on the basis of consumer symptoms or traditional screening methods (i.e., MBA).

During 2002-2004, all PFP cases were linked to puffer fish originating from the northern IRL and the Banana River on Florida's east coast (Figure 1). Except for one case, where puffer fish were commercially harvested and reached a New Jersey fish market, puffer fish were caught recreationally [Bodager 2002; Florida Fish and Wildlife Conservation Commission (FWC)...

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