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Tetrodotoxin and Paralytic Shellfish Toxins in Philippine Crabs Daisuke Yasumura, Yasukatsu Oshima, Takeshi Yasumoto,1 Angel C

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Tetrodotoxin and Paralytic Shellfish Toxins in Philippine Crabs Daisuke Yasumura, Yasukatsu Oshima, Takeshi Yasumoto,1 Angel C Agric. Biol. Chem., 50 (3), 593-598, 1986 593 Tetrodotoxin and Paralytic Shellfish Toxins in Philippine Crabs Daisuke Yasumura, Yasukatsu Oshima, Takeshi Yasumoto,1 Angel C. Alcala* and Lawton C. Alcala* Faculty of Agriculture, TohokuUniversity, Tsutsum ido ri- A mamiyamach i, Sendai 980, Japan * Marine Laboratory, Silliman University, Dumaguete City, Philippines Received July 23, 1985 The frequent occurrence of lethal specimens of Zosimus aeneus and Atergatis floridus on southern Negros Island, Philippines, was confirmed by mouse lethality tests. Among eight specimens of Z. aeneus analyzed by fluorometric liquid chromatography, tetrodotoxin and its derivatives were dominant in five indicating the possible involvement of tetrodotoxin in human intoxication. The three other specimens of Z. aeneus and one specimen of A. floridus contained paralytic shellfish toxins as the major toxins. Occasional outbreaks of crab poisoning re- MATERIALS AND METHODS sulting in 12 fatalities on Negros Island, Philippines, and the lethal potencies of the Specimens. Crabs were collected by scuba and skin diving at various localities on Negros Island, central following five species have been reported by Philippines, during the period from August 1982 to Alcala and colleagues: Zosimus aeneus, September 1984. The locations and the species of crab are Atergatis floridus, Lophozozymus pictor, shown in Fig. 1 and Table I. One specimen each of Z. Demania toxica and Demania alcalai.ia) As the aeneus collected at Suva barrier reef, Viti Levu Island, Fiji, and at Kabira reef, Ishigaki Island, Okinawa, Japan, was presence of paralytic shellfish toxins (PST) in used to test regionality. All specimens were frozen im- Z. aeneus and A. floridus has been established mediately after collection and kept at -20°C until use. in other areas of the Pacific,3~5) Negros speci- menswerealso assumedto contain the same Lethality test. Individual whole crabs were pulverized in toxins.2) However,recent reports on the occur- a mortar and a portion of each homogenatethus obtained rence of tetrodotoxin (TTX) in A. floridus6^ was tested according to the standard mouseassay method indicated the necessity of further analysis to for PST.8) The lethal potency of the crabs was expressed as mouse units per g of crab (MU/g), where 1 MUwas identify the causative toxins. defined as the amount of toxic material required to kill a In the present study marine crab specimens mouse of20g body weight in 15 min. TTXwas assayed by belonging to 15 species were screened for the method standardized by Kawabata.9) lethality by mouseassays to assess their poten- Chromatography. TTXand its derivatives were analyzed tial danger. Particular attention was paid to with a fluorometric liquid chromatographic analyzer.10) the determination of the toxic principle in Z. Extraction and chromatographic purification of TTXfor aeneus because of its frequent implication in spectral measurementswere carried out as described pre- humanintoxication. Specimens of Z. aeneus viously for TTXin pufFerfish.11* Analysis of PST with a from Fiji and Okinawa were also tested for fluorometric analyzer was conducted according to the regional variation. method described in the previous report.12) Spectrometry. A XHNMRspectrum ofTTX acetate was obtained in D2O solution with a Nicolet NT-300 To whomcorrespondence should be addressed. 594 D. Yasumura et al. Fig. 1. Maps Showing Crab Collecting Localities on Negros Island, Philippines. The left mapis an enlargement of southern Negros to pinpoint the sampling sites. The location of Negros Island in the Philippines is shownin the map to the right. (300 MHz)spectrometer. A secondary ion mass spectrum Etisus rhynchophorus, Etisus splendidus, was obtained with a Hitachi M-80 spectrometer with glycerol as the matrix. Calappa calappa and Dromidiopsis sp. Toxicity was undetectable in the other seven species. RESULTS Toxin analysis Toxicity levels Liquid chromatographic analysis revealed The results of the lethality tests are sum- that amongeight specimens of Z. aeneus from marized in Table I. As the mouse assay the Philippines, TTXwas the principal toxin in method cannot distinguish between PST and five and PST in three (Table I). Figure 2 shows TTX, lethal potencies are expressed in PST some chromatograms of the crab extracts. As MU.Specimens for which the principal toxin in the case of pufferfish extracts,11} TTXco- was confirmed by chromatographic analysis existed with 4-epiTTX and anhydroTTX. The are shown in the last column. Of the 69 Fijian and Okinawan specimens also con- Philippine specimens of Z. aeneus, lethality tained TTX and its derivatives (Fig. 2). About was detected in 50 (72.5%), with a mean value 90%of the lethality of the Fijian specimen and 20MU/g. In seven specimens (10.1%), the 1.5% of that of the Okinawan specimen were toxin content in the whole body exceeded 3000 attributable to TTX.A. integerrimus contained MU,a PST level considered lethal for humans almost exclusively TTXand its derivatives. On when taken orally.3) Z. aeneus was toxic in all the other hand, chromatographic analysis of a the surveyed areas, except Selinog Is., but the Bindoy specimen of A. floridus showed the lethal potency of individual specimens varied presence of neosaxitoxin and saxitoxin in a remarkably. No correlation of lethal potency 1 :2 ratio (Fig. 3) but no TTX. with body weight was found (r=0.0418). Firm evidence for the presence ofTTXin Z. Specimens of A. floridus, especially those aeneus was obtained by spectral measurements from Bindoy, were highly toxic. All 25 speci- of a toxic sample prepared from Philippine mens tested were lethal, with a meanvalue of specimens. As shown in Fig. 4, characteristic 157MU/g. In ten specimens (40%), the toxin proton signals assigned to 4a-H and 4-H of contents in the whole body exceeded 3000 MU, TTXwere clearly recognizable at £2.21 ppm with a maximum value of21,200MU. As in Z. (d, /=10.0Hz) and 5.36ppm (d,.7=10.0Hz) aeneus, no correlation between lethality and in the *H NMRspectrum. Other proton sig- body weight was observed (r= -0.0931). nals between (5 3.6 and 4.7ppm also matched Marginal levels of toxicity were detected in those of TTX.n) The secondary ion mass Atergatis integerrimus, Carpilius maculatus, spectrum (inset in Fig. 4) exhibited ions assign- Tetrodotoxin and PS toxins in Philippine Crabs 595 Table I. Lethal Potencies of Marine Crabs from Negros and Other Philippine Islands Species and . , Lethal x^. Species and __... Lethal . placeofcapture (g)W«f Sexpotency(MU/g) T°XlnfJor placeofcapture W^ht(g) Sexpotency(MU/g) T°Xm!^°r (Umore-ougi-gani)Zosimus aeneus ZosimusDumagueteaeneus 37 M 16 Bindoy 154 M ND 68 F 2.0 152 M 2.0 Dauin 1 14 M 52* 144 M 2.3 55 M 34 134 M 2.0 64 F 84* TTX99%< 106 M ND Zamboanguita 72 F ND 106 M 28 TTX99%< 64 F ND 90 M 2.0 62 F 5.0 49 M 2.0 45 F 16 47 M 2.0 Selinogls. 107 M ND 39 M 2.0 78 M ND 120 F ND 60 M ND 103 F 7.9 48 M ND 98 F 2.1 53 F ND 88 F 2.7 SanJose 81 M 215* PST98% 83 F 36 PST94% 63 M ND 81 F 36 Danjugan ls. 79 M 3.8 77 F 8.4 Tubig 43 M ll 77 F 2.6 62 F 4.7 73 F 5.4 A tergatis floridus 7 1 F ND (Subesube-manju-gani) 50 F 2.0 Bindoy 72 M 2.3 32 F 2.0 62 M 2.3 27 F ND 38 M 14 Siaton 128 M 30* 35 M 440* 126 M 85* 32 M 6.2 113 M 26 31 M 150* 78 M 22 29 M 730* PST99%< 74 M ND 29 M 130* 67 M 17 26 M 290* 54 M 12 26 M 200* 51 M 3.8 23 M 92 44 M ND 22 M 470* 37 M 2.0 21 M 3.5 23 M 32 20 M 190* 16 M ND 13 M 350* 111 F 14 ll M 6.1 104 F 15 TTX99%< 17 F 140 87 F ND 14 F 480* 78 F 19 12 F 7.7 78 F 2.0 Dumaguete 3 1 M 1 1 77 F 26 7 M 3.6 68 F 45* ll F 170 68 F 34 Siaton 23 M 1 3 62 F 39 13 F 7.2 60 F 259* PST98% 10 F 9.2 51 F 48 TTX99%< 47 F 47 TTX99%< Atergatis integerrimus 32 F ND (Hoshi-manju-gani) 32 F ND Dauin 132 M ND 29 F ll 126 M 2.0 TTX99%< 596 D. Yasumura et al. Table I. (Continued) Species and .... Lethal Species and __.. , Lethal ^f. placeof W"fl Sexpotency ^jor placeof Wffl Sexpotency ^0I capture (g) (MU/g) ToM capture (g) (MU/g) Toxm Dumaguete 151 M ND Calappa calappa 86 M ND (Marusode-karappa) Bindoy 192 F 2.2 Atergatis reticulatus (Heritori-manju-gani)Zamboanguita 64 F ND Calappa(Megane-karappa)philargius Selinogls. 241 F ND Siaton 53 F ND Carpilius convexus Calappa sp. (Yumon-gani) Bindoy 20 M ND Bindoy 58 M ND 45 M ND Etisussplendidus 30 M ND (Oaka-hizume-gani) 79 F ND Dumaguete 185 M 2.0 59 F ND Zamboanguita 243 M ND 47 F ND 236 M ND Dumaguete 53 M ND 168 M ND 44 M ND 31 M ND Etisusrhynchophorus 17 M ND (Tama-hizume-gani) Dauin 19 M ND Dumaguete 193 M 2.0 Siaton 1 8 F ND 64 F ND Danjuganls. 113 M ND 75 M ND Pilumnusvespertilio 17 M ND (Kebuka-gani) Selinogls. 230 M ND Siaton ll M ND Selinogls.
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