Sains Malaysiana 43(7)(2014):
1003–1011
Distribution of Tetrodotoxin among Tissues of Pufferfish
fromSabah and Sarawak Waters
(Taburan Tetrodotoksin antara Tisu di dalam Ikan Buntal dari
Perairan Sabah dan Sarawak)
A.
MOHD NOR AZMAN2*, M. SAMSUR1 &
M.
OTHMAN2
1Faculty of Resource
Science and Technology, Universiti Malaysia Sarawak
94300 Kota Samarahan, Sarawak, Malaysia
2Fisheries Research
Institute, 11960 Batu Maung, Penang, Malaysia
Received: 10 October 2012/Accepted: 16 September 2013
ABSTRACT
Puffer fish, mainly from Tetraodontidae family known to possess a
neurotoxin or tetrodotoxin (TTX) which can cause a puffer fish poisoning
and adverse effect to human health. In current study, the tetrodotoxin (TTX)
concentration in different tissues (liver, skin, muscle) of 14 species of
puffer fish from Sabah and Sarawak waters were analysed and determined by
application of liquid chromatography-mass spectrometry/mass spectrometry (LC-MS/MS).
Overall, extracted toxin for all specimens were shown to be toxic with result
more than 0.2 μg/g as calculated based on TTX standard curve. Among
the tissues, liver were found to be highest in TTX concentration (91.0
μg/g), followed by muscle (51.1 μg/g) and skin (6.87 μg/g).
Moreover, TTX concentrations among puffer fish species were significantly
differences (p<0.05) with Arothron
immaculatus (275 μg/g) showed highest mean value, while the lowest
value was detected in Lagocephalus lunaris (4.92 μg/g). From this
finding, LC-MS/MS application could be a potential tools to determine the TTX and
advisedly used as a procedure in screening of seafood for monitoring program.
Furthermore, baseline data of TTX levels in selected puffer fish from the
study could be important information and used as guideline in order to mitigate
puffer fish poisoning cases especially in East Malaysia waters.
Keywords: East Malaysia; LC-MS/MS; puffer fish; Tetrodotoxin; tissues
ABSTRAK
Ikan buntal, terutamanya daripada famili
Tetraodontidae diketahui mengandungi neurotoksin atau tetrodotoxin (TTX)
yang boleh menyebabkan keracunan ikan buntal dan memberi kesan buruk kepada
kesihatan manusia. Dalam kajian ini, kepekatan tetrodotoxin (TTX) dalam tisu yang
berbeza (hati, kulit, otot) dalam 14 spesies ikan buntal dari perairan Sabah
dan Sarawak telah dianalisis dan ditentukan menggunakan spektrometri jisim
kromatografi cecair/spektrometri jisim (LC-MS/MS). Secara
keseluruhannya, toksin yang diekstrak daripada semua spesimen adalah toksik
dengan keputusan melebihi daripada 0.2 μg/g berdasarkan pengiraan daripada
keluk piawai TTX. Antara tisu yang dikaji, kepekatan TTX yang tertinggi
didapati dalam hati (91.0 μg/g), diikuti oleh otot (51.1 μg/g) dan
kulit (6.87 μg/g). Tambahan lagi, terdapat perbezaan ketara (p<0.05) dalam kepekatan TTX antara spesies ikan
buntal dengan Arothron immaculatus (275 μg/g) menunjukkan nilai min
tertinggi, manakala nilai terendah dikesan pada Lagocephalus lunaris (4.92
μg/g). Daripada penemuan ini, penggunaan LC-MS/MS boleh menjadi
alat yang berpotensi untuk menentukan TTX dan boleh digunakan sebagai prosedur dalam
pemeriksaan makanan laut bagi program pemantauan. Tambahan
pula, data asas tahap TTX dalam ikan buntal yang dipilih daripada
kajian boleh menjadi maklumat penting dan digunakan sebagai garis panduan dalam
usaha untuk mengurangkan kes keracunan ikan buntal terutamanya di perairan
Malaysia Timur.
Kata kunci: Ikan buntal; LCMS/MS;
Malaysia Timur; Tetrodotoksin; tisu
REFERENCES
Ahasan, H.A.M.N., Mamun, A.A., Karim,
S.R., Bakar, M.A., Gazi, E.A. & Bala, C.S. 2004. Paralytic complications of puffer fish (Tetrodotoxin)
poisoning. Singapore Medical Journal 45(2): 73-74.
Arakawa, O., Hwang, D.F., Taniyama, S.
& Takatani, T. 2010. Toxins
of pufferfish that cause human intoxications. In Coastal
Environmental and Ecosystem Issues of the East China Sea, edited by
Ishimatsu, A. & Lie, H.J. pp. 227-244.
Brillantes, S., Samosorn, W., Faknoi, S. & Oshima, Y.
2003. Toxicity of puffers landed and marketed in Thailand. Fisheries Science 69: 1224-1230.
Berry, P.Y. & Hassan, A.A. 1973. Comparative lethality
of tissue extracts from the Malaysian puffer fishes Lagocephalus lunaris
lunaris, L. l. spadiceus and Arothron stellatus. Toxicon 11:
249-254.
Che Nin, M., Norjuliana, M.N., Gan,
L.H., Razak, L. & Samsur, M. 2010. Screening of tetrodotoxin in puffers using gas chromatography-mass
spectrometry. Journal of Chromatography A 1217(47): 7455-7459.
Chew, S.K., Goh, C.H., Wang, K.W., Mah, P.K. & Tan, B.Y. 1983. Puffer fish (Tetrodotoxin) poisoning: Clinical
report and role of anti-cholinesterase drugs in therapy. Singapore Medical
Journal 24: 168-171.
Chou, S.S., Tsai, Y.H., Chang, P.C.
& Hwang, D.F. 1994. Tetrodotoxin-associated
food poisoning due to ingesting fish. Journal Food and Drug Analysis 2(1):
77.
Chua, H.H. & Chew, L.P. 2009. Puffer
fish poisoning: A family affair. Medical Journal of Malaysia
64(2): 181-182.
Chulanetra, M., Soonkrung, N.,
Srimanote, P., Indrawattana, N., Thanongsaksrikul, J., Sakolvaree, Y.,
Chongsa-Nguan, M., Kurazono, H. & Chaicumpa, W. 2011. Toxic marine puffer fish in Thailand seas and tetrodotoxin
they contained. Toxins 3: 1249-1262.
Diener, M., Christian, B., Ahmed, M.S.
& Luckas, B. 2007. Determination of
tetrodotoxin and its analogs in the puffer fish Takifugu oblongus from
Bangladesh by hydrophilic interaction chromatography and mass-spectrometric
detection. Analytical Bioanalytical Chemistry 389: 1997- 2002.
EC (European Commission). 2004. Corrigendum to Regulation (EC) No 853/2004 of the
European Parliament and of the Council of 29 April 2004 laying down specific
hygiene rules for food of animal origin. Official Journal
of the European Union L 139. pp L226/68 (25/6/2004).
El-Sayed, M., Yacout, G.A., El-Samra,
M., Ali, A. & Kotb, S.M. 2003. Toxicity of the Red Sea pufferfish Pleuranacanthus sceleratus “El-Karad”. Ecotoxicology and Environmental Safety 56(3): 367-372.
Fisheries Research Institute (FRI). 2004. Field Guide to
Selected Commercial Marine Fishes of Malaysian Waters. Pulau Pinang,
Department of Fisheries Malaysia.
Froese, R. & Pauly, D. 2011. FishBase. www.fishbase.org. Accessed on August 2011.
Helbig, T. & Luckas, B. 2010. Determination of tetrodotoxins (TTXs) and
paralytic shellfish poisoning (PSP) toxins in puffer fish from Malaysia and
Japan by application of a ZIC-HILIC column and mass spectrometric detection. Current Development in Oceanography 1(2): 69-83.
Isbister, G.K., Son, J., Wang, F.,
Maclean, C.J., Lin, C.S., Ujma, J., Balit, C.R., Smith, B., Milder, D.G. &
Kiernan, M.C. 2002. Puffer fish
poisoning: A potentially life-threatening condition. Medical Journal of
Australia 177(11-12): 650-653.
Jang, J.H., Lee, J.S. &
Yotsu-Yamashita, M. 2010. LC/MS
analysis of Tetrodotoxin and its deoxy analogs in the marine puffer fish Fugu
niphobles from the southern coast of Korea, and in the brackishwater puffer
fishes Tetraodon nigroviridis and Tetraodon biocellatus from
South East Asia. Marine Drugs 8: 1049-1058.
Japan Food Hygiene Association. 2005. Puffer toxin. In Environmental
Health Bureau, Ministry of Health and Welfare, edited by Shokuhin Eisei
Kensa Shishin. Manual for Methods for Food Sanitation
Testing, Tokyo. pp. 661-673.
Jen, H.C., Lin, S.J., Tsai, Y.H., Chen,
C.H., Lin, Z.C. & Hwang, D.F. 2008. Tetrodotoxin poisoning evidenced by solid-phase extraction combining with
liquid chromatography-tandem mass spectrometry. Journal of Chromatography B 871:
95-100.
Kan, S.K., Chan, M.K. & David, P. 1987. Nine fatal cases
of puffer fish poisoning in Sabah, Malaysia. Medicine Medical Journal of
Malaysia 42(3): 199-200.
Katikou, P., Georgantelis, D.,
Sinouris, N., Petsi, A. & Fotaras, T. 2009. First report on toxicity assessment of the Lessepsian
migrant pufferfish Lagocephalus sceleratus (Gmelin, 1789) from European
waters (Aegean Sea, Greece). Toxicon 54: 50-55.
Kungsuwan, A. 1994. Survey on poisonous pufferfish in Andaman Seas. Proceeding
of the Seminar on Fisheries 1993, Department of Fisheries, Bangkok,
Thailand, 15-17 September 1993.
Kungsuwan, S., Arakawa, O., Promdet, M.
& Onoue, Y. 1997. Occurrence of
paralytic shellfish poisons in Thai freshwater puffers. Toxicon 35:
1341-1346.
Laobhripatr, S., Limpakarnjanarat, K., Sangwonloy, O.,
Sudhasaneya, S., Anuchatvorakul, B., Leelasitorn, S. & Saitanu, K. 1990. Food poisoning due to consumption of the freshwater puffer Tetraodon
fangi in Thailand. Toxicon 28(11): 1372-1375.
Lin, S.J. & Hwang, D.F. 2001. Possible
source of tetrodotoxin in the starfish Astropecten scoparius. Toxicon 39: 573-579.
Lyn, P.C.W. 1985. Puffer fish poisoning: Four case reports. Medical
Journal of Malaysia 40(1): 31-34.
Mahmud, Y., Tanu, M.B., Takatani, T.,
Asayama, E., Arakawa, O. & Noguchi, T. 2001. Chelonodon patoca, a highly toxic marine puffer in
Japan. Journal of Natural Toxins 10: 69-74.
Matsui, T., Taketsugu, S., Sato, H.,
Yamamori, K., Kodama, K., Ishi, A., Hirose, H. & Shimizu, C. 1990. Toxification of cultured puffer fish by
the administration of tetrodotoxin producing bacteria. Nippon Suisan
Gakkaishi 56(4): 705.
Miyazawa, K. & Noguchi, T. 2001. Distribution and origin of tetrodotoxin. Journal of Toxicology Toxin Reviews 20: 11-33.
Mohamad, S., Lim, P.T., Bojo, O., Nyanti, L., Ismail, N.,
Rahim, K.A. & M. Long, S. 2008. Toxicity of freshwater puffer fish Xenopterus
naritus (Tetraodontidae) collected from East Malaysia. IOC-WESTPAC
Scientific Symposium. 21st- 25th May 2008.
Monaliza, M.D. & Mohamad, S. 2011. Toxicity and toxin
properties study of pufferfish collected from Sabah waters. Health and the
Environment Journal 2(1): 14-17.
Mosher, H.S. & Fuhrman, F.A. 1984. Occurrence
and origin of tetrodotoxin. In Seafood Toxins, edited by Edward,
P.R. Washington, D.C.: American Chemical Society. pp. 333-344.
Nagashima,
Y., Matsumoto, T., Kadoyama, K., Ishizaki, S. & Terayama, M. 2011. Toxicity
and molecular identification of Green Toadfish Lagocephalus lunaris collected
from Kyushu Coast, Japan. Journal of Toxicology 2011: 801285.
Nakagawa, T., Junho, J. & Yotsu-Yamashita, M. 2006. Hydrophilic interaction
liquid chromatography-electrospray ionization mass spectrometry of tetrodotoxin
and its analogs. Analytical Biochemistry 352: 142-144.
Nakamura, M. & Yasumoto, T. 1985. Tetrodotoxin derivatives in puffer fish. Toxicon 23: 271-276.
Ngy, L., Yu, C.F., Taniyama, S., Takatani, T. & Arakawa,
O. 2009. Co-occurence of tetrodotoxin and saxitoxin in
Cambodian marine pufferfish Takifugu oblongus. African Journal
of Marine Science 31(3): 349-354.
Noguchi, T. & Arakawa, O. 2008. Tetrodotoxin – distribution and accumulation in
aquatic organisms and cases of human intoxication. Marine Drugs 6:
220-242.
Noguchi, T., Arakawa, O. &
Takatani, T. 2006. TTX accumulation in
pufferfish. Comparative Biochemistry and Physiology, Part D 1:
145-152.
Nunez-Vazquez, E.J., Yotsu-Yamashita,
M., Sierra-Beltran, A.P., Yasumoto, T. & Ochoa, J.L. 2000. Toxicities and distribution of
tetrodotoxin in the tissues of puffer fish found in the coast of the Baja
California Peninsula, Mexico. Toxicon 38: 729-734.
Oliveira, J.S., Fernandes, S.C.R., Schwartz, C.A., Bloch
Jr., C., Melo, J.A.T., Pires Jr., O.R. & Freitas, J.C. 2006. Toxicity and toxin identification in Colomesus asellus, an
Amazonian (Brazil) freshwater puffer fish. Toxicon 48: 55-63.
Othman, B., Khairul Adha, A.R., Samsur,
M., Shabdin, M.L., Lee, N., Norhadi, I. & Lim, P.T. 2006. Toxicity of the yellow puffer fish Xenopterus naritus from
Sungai Saribas Sarawak. Research Bulletin, FRST 1
(June). pp 5-6.
Pires, O.R., Sebben, A., Schwartz,
E.F., Largura, S.W.R., Bloch, C., Morales, R.A.V. & Schwartz, C.A. 2002. Occurrence of tetrodotoxin and its analogues in the Brazilian
frog Brachycephalus ephippium (Anura: Brachycephalidae). Toxicon 40(6):
61-766.
Rodriquez, P., Alfonso, A., Otero, P.,
Katikou, P., Georgantelis, D. & Botana, L.M. 2012. Liquid chromatography-mass spectrometry method to detect
Tetrodotoxin and its analogues in the puffer fish Lagocephalus sceleratus (Gmelin,
1789) from European waters. Food Chemistry 132: 1103-1111.
Sato, S., Kodama, M., Ogata, T.,
Saitanu, K., Furuya, M., Hirayama, K. & Kakinuma, K. 1997. Saxitoxin as a toxic principle of a
freshwater puffer, Tetraodon Fangi, in Thailand. Toxicon 35:
137-140.
Shoji, Y., Yotsu-Yamashita, M.,
Miyazawa, T. & Yasumoto, T. 2001. Electrospray ionization mass spectrometry of tetrodotoxin and its analogs:
Liquid chromatography/ mass spectrometry, tandem mass spectrometry and liquid
chromatography/tandem mass spectrometry. Analytical Biochemistry 290:
10-17.
Simon, K.D., Mazlan, A.G. & Usup, G. 2009. Toxicity of
puffer fishes (Lagocephalus wheeleri Abe, Tabeta and Kitahama, 1984 and Lagocephalus
sceleratus Gmelin, 1789) from the east coast waters of Peninsular Malaysia. Journal of Biological Sciences 9(5): 482-487.
Tani, I. 1945. Studies on Japanese
Pufferfish in Association with Poisoning due to Ingestion of Them. Tokyo: Teikoku, Tosho. p. 103.
Tsai, Y.H., Chao, S.M., Lin, G.T., Noguchi, T. & Hwang,
D.F. 2004. Tetrodotoxins of the starfish Astropecten vappa collected
from western Taiwan. Fisheries Science 70: 930- 932.
Yasumoto, T. & Michishita, T. 1985. Fluorometric determination of
tetrodotoxin by high performance liquid chromatography. Agricultural
and Biological Chemistry 49: 3077-3080.
Yasumoto, T., Yasumura, D., Yotsu, M.,
Michishita, T., Endo, A. & Kotaki, Y. 1986. Bacterial production of tetrodotoxin and
anhydrotetrodotoxin. Agricultural and Biological Chemistry 50(3):
793-795.
Yotsu-Yamashita, M., Jang, J.H., Cho,
Y. & Konoki, K. 2011. Optimization for simultaneous analysis of tetrodotoxin,
4-epitetrodotoxin, 4,9-anhydrotetrodotoxin and 5,6,11-trideoxytetrodotoxin by
hydrophilic interaction liquid chromatography-tandem mass spectrometry. Forensic
Toxicology 29: 61-64.
Yu, C.F. & Yu, P.H.F. 2002. Are puffer fish more toxic
in their spawning seasons? Marine Biology 140: 1053-1057.
*Corresponding
author; email: mohayo01@yahoo.com
|