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. 2019 Jan 5;17(1):28. doi: 10.3390/md17010028

The Incidence of Tetrodotoxin and Its Analogs in the Indian Ocean and the Red Sea

Isidro José Tamele 1,2,3, Marisa Silva 1,4, Vitor Vasconcelos 1,4,*
PMCID: PMC6357042  PMID: 30621279

Abstract

Tetrodotoxin (TTX) is a potent marine neurotoxin with bacterial origin. To date, around 28 analogs of TTX are known, but only 12 were detected in marine organisms, namely TTX, 11-oxoTTX, 11-deoxyTTX, 11-norTTX-6(R)-ol, 11-norTTX-6(S)-ol, 4-epiTTX, 4,9-anhydroTTX, 5,6,11-trideoxyTTX, 4-CysTTX, 5-deoxyTTX, 5,11-dideoxyTTX, and 6,11-dideoxyTTX. TTX and its derivatives are involved in many cases of seafood poisoning in many parts of the world due to their occurrence in different marine species of human consumption such as fish, gastropods, and bivalves. Currently, this neurotoxin group is not monitored in many parts of the world including in the Indian Ocean area, even with reported outbreaks of seafood poisoning involving puffer fish, which is one of the principal TTX vectors know since Egyptian times. Thus, the main objective of this review was to assess the incidence of TTXs in seafood and associated seafood poisonings in the Indian Ocean and the Red Sea. Most reported data in this geographical area are associated with seafood poisoning caused by different species of puffer fish through the recognition of TTX poisoning symptoms and not by TTX detection techniques. This scenario shows the need of data regarding TTX prevalence, geographical distribution, and its vectors in this area to better assess human health risk and build effective monitoring programs to protect the health of consumers in Indian Ocean area.

Keywords: Indian Ocean, Red Sea, tetrodotoxin, pufferfish poisoning

1. Introduction

The tropical and subtropical climates predominant in the Indian Ocean zone, accompanied by industrialization and population increase, are pointed to as the main factors that, together with eutrophication, contribute to the development of toxic phytoplankton blooms—harmful algal blooms (HABs) and bacteria [1]. HABs and some bacteria are marine toxin (MT) producers, turning the Indian Ocean zone vulnerable to this phenomenon [2,3,4,5]. One of the main Indian Ocean MTs is tetrodotoxin (a neurotoxin) and its analogs (TTXs), of which the main producers were reported to belong to different bacteria genera [6,7,8,9,10,11,12,13,14,15]. Cases of human poisoning are recurrent, especially after consumption of TTX-contaminated fish, with the puffer fish as the most common vector reported since Egyptian times [16,17,18,19,20,21,22,23,24,25,26,27,28,29]. Due to the lack of TTX monitoring programs, the episodes of human seafood poisoning are still common in the Indian Ocean area, since seafood is the most common food for many people living along coastal zones [16,17,18,19,20,21,22,24,26,28,29,30,31,32,33,34,35,36,37,38]. Thus, the objective of this paper was to review the incidence of TTX in the Indian Ocean and the Red Sea zones and associated human seafood poisoning incidents. The monitoring of TTXs in this geographic zone is also recommended.

2. Tetrodotoxin

TTX (Figure 1) is a potent neurotoxin group [39] that can provoke severe poisoning after consumption of contaminated seafood. Several species of distinct marine organisms of human consumption were identified as TTX vectors: puffer fish [16,17,18,19,20,21,22,23,24,25,26,27,28,29], gastropods [40], crustaceans [41,42,43,44], and bivalves [45]. Also, the occurrence of TTXs in terrestrial vertebrates such as Polypedates sp., Atelopus sp., Taricha granulosa, [46] and Cynops ensicauda popei [47] was reported [48,49]. TTX is an alkaloid isolated for the first time in 1909 by Tahara and Hirata from the ovaries of globefish [50]. In the marine environment, bacteria are pointed to as the main producers of this group of toxins, namely Serratia marcescens [51], Vibrio alginolyticus, V. parahaemolyticus, Aeromonas sp. [52], Microbacterium arabinogalactanolyticum [13], Pseudomonas sp. [14], Shewanella putrefaciens [6], Alteromonas sp. [8], Pseudoalteromonas sp. [10], and Nocardiopsis dassonvillei [12]. Physicochemically, TTXs are colorless, crystalline weak heterocyclic basic compounds (Figure 1 and Table 1), highly hydro-soluble and also heat-stable [45]; thus, the toxin is not destroyed by cooking procedures.

Figure 1.

Figure 1

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Tetrodotoxin (TTX) and analogs modified from European Food Safety Authority (EFSA) 2017 [45] and Yotsu-Yamasshita et al. (2007) [15,53,54]. (*) indicates TTX analogs that occur in marine organisms with known relative toxicity. (A) 4-cysTTX(*), (B) tetrodonic acid, (C) 4,9-anhydroTTX(*), (D) 1-hydroxy-5,11-dideoxyTTX, (E) TTX and 12 analogs, (F) 5-deoxyTTX(*) and three analogs, (G) trideoxyTTX and two analogs, (H) 4-epi-5,6,11-trideoxyTTX and another analog, and (I) 4,4a-anhydro-5,6,11-trideoxyTTX and 1-hydroy-4,4a-anhydro-8-epi-5,5,11-trideooxyTTX (see radicals of the analogs in the Table 1).

Table 1.

Tetrodotoxin (TTX) and analogs shown in Figure 1 and modified from European Food Safety Authority (EFSA) 2017 [45] and Yotsu-Yamasshita et al. (2007) [15,53].

E R1 R2 R3 R4 R5
TTX (*) H OH OH CH2OH OH
4-epiTTX (*) OH H OH CH2OH OH
6-epiTTX (*) H OH CH2OH OH OH
11-deoxyTTX (*) H OH OH CH3 OH
6,11-dideoxyTTX H OH H CH3 OH
8,11-dideoxyTTX H OH OH CH3 H
11-oxoTTX (*) H OH OH CH(OH)2 OH
11-norTTX-6,6-diol H OH OH OH OH
11-norTTX-6(R)-ol (*) H OH H OH OH
11-norTTX-6(S)-ol (*) H OH OH H OH
Chiriquitoxin H OH OH CH(OH)CH(NH3+)COO− OH
TTX-8-O-hemisuccinate H OH OH CH2OH OOC(CH2)2COO−
TTX-11-carboxylic acid H OH OH COO− OH
TTX (*) H OH OH CH2OH OH
F R1 R2 R3 R4 R5 R6
5-deoxyTTX(*) OH CH2OH H H OH H
5,11-dideoxyTTX (*) OH CH3 H H OH H
5,6,11-trideoxyTTX (*) H CH3 H H OH H
8-epi-5,6,11-trideoxyTTX H CH3 H H H OH
G R1 R2
4,9-anhydro-5,6,11-trideoxyTTX H OH
4.9-anhydro-8-epi-5,6,11-trideoxyTTX OH H
H R1 R2 R3 R4 R5
1-hydroxy-8-epi-5,6,11-trideoxyTTX OH H OH OH H
4-epi-5,6,11-trideoxyTTX H OH H H OH
I R1 R2 R3
4,4a-anhydro-5,6,11-trideoxyTTX H OH H
1-hydroxy-4,4a-anhydro-8-epi-5,5,11-trideooxyTTX OH H OH
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To date, around 28 analogs of TTX were described (Figure 1 and Table 1) and some of them were detected in marine organisms [53], with their relative toxicity well known [45] (chemical structures pointed with asterisks in Figure 1): TTX, 11-oxoTTX, 11-deoxyTTX, 11-norTTX-6(R)-ol, 11-norTTX-6(S)-ol, 4-epiTTX, 4,9-anhydroTTX, 5,6,11-trideoxyTTX [45], 4-CysTTX, 5-deoxyTTX, 5,11-dideoxyTTX, and 6,11-dideoxyTTX [54,55,56,57] (Table 1). Their relative toxicity ranges from 0.01 to 1.0, with 5,6,11-trideoxyTTX and TTX as the least and most toxic, respectively [45], and there are still no available data regarding the toxicity for 4-CysTTX and 5,11-dideoxyTTX. Chemical abstract numbers (CAS) are also listed in Table 2.

Table 2.

Chemical abstract numbers (CAS) and relative toxicity of TTX analogs [58,59].

TTX Analogs TEF CAS Number
TTX 1.0 4368-28-9
11-oxoTTX 0.75 123665-88-3
11-deoxyTTX 0.14 -
11-norTTX-6(R)-ol 0.17 -
11-norTTX-6(S)-ol 0.19 -
4-epiTTX 0.16 98242-82-1
4,9-anhydroTTX 0.02 13072-89-4
6,11-dideoxyTTX 0.02 -
5-deoxyTTX 0.01 -
5,6,11-trideoxyTTX 0.01 -
4-CysTTX - -
5,11-dideoxyTTX - -
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* TEF—toxic equivalency factor.

The action mechanism of TTXs occurs through the occlusion of the external pore of site 1 of voltage-gated sodium channels on the surface of nerve membranes, blocking cellular communication and causing death by cardio-respiratory paralysis [60]. Paralysis occurs by affecting the respiratory system, the diaphragm, skeletal muscles, and tissues in the digestive tract in humans [39]. TTXs normally accumulate in skin, intestines, liver, muscle, gonads, viscera, and ovaries in different species of puffer fish [16,21,22,29,33,34,35,36,37,61,62,63,64,65]. The symptoms that can be used partially as an indication of TTX human poisoning (wt = 50 kg and TTX amount = 2 mg) were grouped into four levels depending on the amount ingested [66] and are described in Table 3. These symptoms normally appear 40 min after consumption of contaminated food and, in some cases, even six hours after [67].

Table 3.

Characteristic symptoms of TTX human poisoning modified from Noguchi and Ebesu (2001) [66].

Level Affected System Specific Symptoms
1 Neuromuscular Paresthesia of lips, tongue, and pharynx, taste disturbance, dizziness, headache, diaphoresis, pupillary constriction
Gastrointestinal Salivation, hypersalivation, nausea, vomiting, hyperemesis, hematemesis, hypermotility, diarrhea, abdominal pain
2 Neuromuscular Advanced general paresthesia, paralysis of phalanges and extremities, pupillary dilatation, reflex changes
3 Neuromuscular Dysarthria, dysphagia, aphagia, lethargy, incoordination, ataxia, floating sensation, cranial nerve palsies, muscular fasciculation
Cardiovascular/pulmonary Hypotension or hypertension, vasomotor blockade, cardiac arrhythmias, atrioventricular node conduction abnormalities, cyanosis, pallor, dyspnea
Dermatologic Exfoliative dermatitis, petechiae, and blistering
4 Respiratory failure, impaired mental faculties, extreme hypotension, seizures, loss of deep tendon and spinal reflexes
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Currently, there is no antidote for TTX; however, some studies indicate that the application of activated charcoal could help in reversing the clinical stage of poisoning victims since it reduces the toxin free amount [68]. Also, alkaline gastric lavage with sodium bicarbonate (2%) is indicated as a treatment within the first hour of the incident, due to TTX instability in alkaline media [69]. Another clinical intervention recommendation is the use of cholinesterase inhibitors such as neostigmine [28], and mechanical respiratory help may reduce mortality probability by muscle paralysis [38].

3. TTX Detection Methods

Several methodologies were developed to analyze TTXs and, in recent years, chemical methods became more popular due to their sensitivity with limits of detection (LODs) ranging from 0.9 ng to 0.063 μg. Liquid chromatography with tandem mass spectrometry (LC–MS/MS) techniques, the first choice compared to mouse bioassays (MBAs) and enzymatic methods due to their greater sensitivity and specificity, have the capacity to detect and determine TTXs in complex matrices [70]. Also, due to ethical reasons and lack of specificity, MBA fell into disuse, with the latter reason also attributed to the enzymatic methods. When a poisoning case occurs, it is recommended, when available, to screen the liver, muscle, skin, gonads, and ovaries of the suspected poisoning marine vector samples [28,36,40,41,42,53,54,55,56,62,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88]. Human urine and plasma should also be analyzed for TTX in these cases [80].

Methods for TTX analysis and their respective limits of quantification (LOQs) and detection (LODs) are described in Table 4 and include the mouse bioassay [12,36,52,89], receptor-based assay [90], immunoassay [31,36,52,73,77,82,89,91,92,93], thin-layer chromatography [13,72], high-performance liquid chromatography [84,94,95], gas chromatography–mass spectrometry [76,84,95], liquid chromatography coupled to mass spectrometry [33,40,96,97,98], surface plasmon resonance [30], and liquid chromatography with fluorescence detection (FLD) [15,32,89].

Table 4.

TTX detection methods, their limits of quantification (LOQs), limits of detection (LODs), and toxicity equivalency factors (TEFs) according to the European Food Safety Authority (EFSA). MBA—mouse bioassay; FLD—fluorescence detection; RB—receptor-based; LC—liquid chromatography; MS—mass spectrometry; HPLC—high-performance liquid chromatography; UVD—ultraviolet detection; SPR—surface plasmon resonance; TLC—thin-layer chromatography; GC—gas chromatography.

Analysis Method LOD LOQ
MBA [12,36,52,89] 1.1 μg·g−1 [89] -
Enzymatic assays [31,36,52,73,77,82,89,91,92,93] 2 ng·mL−1 [92] -
TLC–MS [13,72] 0.1 μg [72] -
HPLC–FLD [84,94,95] 1.27 μg·g−1 [94]
GC–MS [76,84,95] 0.5 μg·g−1 [76] 1.0 μg·g−1 [76]
LC–MS/MS/UPLC–MS/MS [33,40,96,97,98] 0.09–16 ng·mL−1 [33,40,96,97,98] 5–63 ng·mL−1 [40]
SPR [30] 0.3–20 ng·mL−1 [30] -
HPLC–FLD [15,32,99] 40-100 ng·g−1 [15] -
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4. Geographic Occurrence and Incidence of TTXs in the Indian Ocean and the Red Sea

As described in the introduction section, TTXs were reported in several marine organisms [71], regarding poisoning incidents [71]; the main TTX vectors involved in the Indian Ocean and the Red Sea (Table 4) belong to the Tetraodontidae family: Arothron hispidus in India [65], Takifugu oblongus in Bangladesh [16,33] and India [35,62], Lageocephalus scitalleratus in Singapure [20], Pleuranacanthus sceleratus in Egypt [21,34,37], Reunion Island [29], and Australia [23,24], Chelonodon pataca, Sphaeroides oblongus, Lagocephalus inermis, and Lagocephalus lunaris in India [35,62], Xenopterus naritus in Malaysia [63], Arothron stellatus in India [64], Tetractenos hamiltoni in Australia [80,100], and Tetroadon sp. [17], Tetraodon nigroviridis, and Arothron reticularis in Thailand [99]. The records of TTX occurrence in other marine species such as mollusks are scarce in the Indian Ocean. Gastropods were reported as TTX vectors in other locations: Charonia lampas [85], Gibbula umbilicalis, and Monodonta lineata on the Portuguese coast [40], Nassarius spp. in China [94], Polinices didyma, Natica lineata [84,101], Oliva miniacea, O. mustelina, and O. nirasei [95] in Taiwan, Charonia sauliae [102], Babylonia japonica [86], Niotha spp. [75,81], and Tutufa lissostoma [103] in Japanese crabs, Demania cultripes, Demania toxica, Demania reynaudi, Lophozozymus incises, Lophozozymus pictor, Atergatis floridus [104], and Atergatopsis germaini [83], highlightinh these organisms as potential indicator species [11]. Data on these groups are scarce in the Indian Ocean area, suggesting that further studies and monitoring programs for TTXs are needed. Available data regarding this geographic region are displayed in Table 5.

Table 5.

The incidence of TTXs in the Indian Ocean. NPI—no poisoning incidents, MBA—mouse bioassay; FLD—fluorescence detection; LC—liquid chromatography; MS—mass spectrometry; HPLC—high-performance liquid chromatography; UVD—ultraviolet detection; TLC—thin-layer chromatography; GC—gas chromatography.

Producing Species Vector Sample Tissue Location Country Poisoning Date TTX Detection Maximum Concentration Poisoning Victims Reference
Australia
Unknown Puffer fish Lagocephalus scleratus Close to Fremantle Hospital Australia 13 May 1996 TTX Symptomatology - 3 people [23]
Unknown Puffer fish Lagocephalus scleratus Port Hedland Australia 1998 TTX Symptomatology - 1 person [24]
Unknown Toad fish Tetractenos hamiltoni New South Wales Australia 1 January 2001 to 13 April 2002 TTX Symptomatology - 11 people [100]
Unknown Toad fish Tetractenos hamiltoni Urine Australia 2004 TTX HPLC–UVD 5 ng/mL 7 people [80]
Serum 20 ng/mL
Asian countries
Unknown Puffer fish Khulna Bangladesh April 18 2002 TTX Symptomatology - 45 people [27]
Unknown Puffer fish Takifugu oblongus Skin Khulna Bangladesh 18 May 2002 TTX MBA 18.9 MU/g 36 people, 7 deaths [16]
Muscle 4.4 MU
Liver 4.9 MU/g
Gonads 132.0 MU/g
Viscera categories 37.0 MU/g
Natore -
Dhaka
Unknown Puffer fish Liver Khulna Bangladesh 24 July 2005 TTX Symptomatology - 6 people [22]
Unknown Skin Khulna Bangladesh 25 March 2006 TTX LC–MS/MS 25.35 μg·g−1 NPI [33]
Anhydro 7.71 μg·g−1
11-Deoxy 1.12 μg·g−1
Trideoxy 15.31 μg·g−1
Muscle TTX 1.64 μg·g−1
Anhydro -
11-Deoxy -
Trideoxy -
Liver TTX 45.71 μg·g−1
Anhydro 29.17 μg·g−1
11-Deoxy -
Trideoxy 9.09 μg·g−1
Ovary TTX 356.00 μg·g−1
Anhydro 85.87 μg·g−1
11-Deoxy 26.00 μg·g−1
Trideoxy 2,929.70 μg·g−1
Unknown Puffer fish Dhaka Bangladesh 2008 TTX Symptomatology - 11 people [25]
Unknown Puffer Fish Narshingdi Bangladesh April and June 2008 TTX Symptomatology - 95 people, 14 deaths [26]
Natore
Dhaka
Unknown Puffer Fish Dhaka City Bangladesh October 2014 TTX Symptomatology - 11 people, 4 deaths [18]
Unknown Puffer fish - Khulna Bangladesh - TTX Symptomatology - 37 people, 8 deaths [28]
Unknown Puffer fish Chelonodon patoca Liver Bay of Bengal India June 1998 to March 2001 TTX MBA 25.9 MU/g NPI [61]
Ovary 183 MU/g
Sphaeroides oblongus Liver 16 MU/g
Ovary 7.9 MU/g
Lagocephalus inermis Liver 5.5 MU/g
Ovary 28.9 MU/g
Lagocephalus lunaris Liver 5.9 MU/g
Ovary 16.6 MU/g
Unknown Puffer fish Chelenodon potoca Liver Bengal coast India June 2000–March 2001 TTX MBA 27.8 MU/g NPI [35]
Ovary 156.7 MU/g
Takifugu oblongus Liver 11.75 MU/g
Ovary 29.1 MU/g
Lagocephalus lunaris Liver 9 MU/g
Ovary 30.1 MU/g
Lagocephalus inermis Liver 5.7 MU/g
Ovary 9.64 MU/g
Kytococcus sedentarius Puffer fish Arothron hispidus Skin Annankil fish landings at Parangipettai India 2010 TTX MBA - NPI [65]
Intestine -
Liver -
Cellulomonas fimi Muscle 4.4 MU
Liver 4.9 MU/g
Gonads 132.0 MU/g
Bacillus lentimorbus Viscera categories 37.0 MU/g
Natore -
Dhaka -
Unknown Puffer fish Arothron stellatus Muscles Parangipettai India 2016 TTX HPLC–FLD, TLC–UVD Qualitative NPI [64]
Gonads 4-epi
Liver anhydro
Unknown Puffer fish Takifugu oblongus Skin Kasimedu fishing harbor, Chennai, Tamil Nadu India 2016 TTX MBA 75.88 MU/g NPI [62]
GC–MS 16.5 MU/g
HPLC 18 MU/g
Liver MBA 143.33 MU/g
GC–MS 32.5 MU/g
HPLC 48 MU/g
Ovary MBA 163 MU/g
GC–MS 34.5 μg
HPLC 51 μg
Unknown Puffer fish - Johor Malaysia May 2008 TTX Symptomatology - 34 people [68]
Unknown Carcinoscorpius rotundicauda Urine Kota Marudu Malaysia June–August 2011 TTX GC–MS 1.3–602 ng/mL 30 people [88]
Unknown Puffer fish Xenopterus naritus Muscle Manggut Malaysia February and July 2013 TTX LC–MS/MS 27.19 μg/g NPI [63]
Kaong 16.09 μg/g
Unknown Puffer fish Lageocephalus scitalleratus Alexandra Hospital Singapore 2013 TTX Symptomatology 1 person [20]
Unknown Tetraodon nigroviridis Reproduc tive tissue Satun Thailand April to July 2010 TTX LC–MS/MS, MBA 63.57 MU/g NPI [36]
Liver 97.08 MU/g
Digestive tissue 43.33 MU/g
Muscle 22.12 MU/g
Arothron reticularis Reproductive tissue -
Liver 2.08 MU/g
Digestive tissue 3.16 MU/g
Muscle 4.02 MU/g
African countries
Unknown Puffer fish Lagocephalus lunaris Gonads National Research Center, Dokki, Cairo, Egypt September 1990 through May 1991 TTX TLC–UVD, MBA 752 MU/g NPI [34]
Liver 246 MU/g
Muscles 127 MU/g
Digestive tract 221 MU/g
Skin 119 MU/g
Unknown Puffer fish Lagocephalus sceleratus Gonads Attaka fishing harbor Egypt October 2002 and June 2003 TTX MBA 3950 MU/g NPI [37]
Unknown Puffer fish Lagocephulus scleratus Muscle Suez Gulf Egypt 23 December 2004 TTX 7 people [21]
Unknown Puffer fish Nosy Be Island Madagascar July 1998 TTX MBA 16 UM/g 3 people, 1 death [19]
Unknown Puffer fish Lagocephalus sceleratus Liver Reunion Island Reunion Island 10 September 2013 TTX MBA, LC–MS/MS 95 MU/g 10 people [29]
Flesh 5 MU/g
Unknown Puffer fish, Tetraodontidae family Zanzibar Tanzania TTX Symptomatology - 1 death [17]
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5. Final Considerations

TTX data in the Indian Ocean and Red Sea are usually related to fatal outbreaks due to seafood poisoning and not to scientific research, indicating the lack of MT monitoring programs. The symptomatology reports and MBA are used to identify seafood poisoning caused by TTX and analogs, indicating the need for analytical methods such as liquid chromatography to obtain better quantitative data. Both symptomatology and MBA in isolation are not enough to conclude that TTXs are the causative agent of seafood poisoning, since there are other toxins (PSTs) with similar action mechanism that overlap in symptomatology with TTX poisoning. Additionally, MBA cannot discriminate between the different TTX analogs. MBA and symptomatology are used in countries of the Indian Ocean and the Red Sea to identify TTX poisoning due to the lack of availability and accessibility to chemical methods and the absence of TTX monitoring programs.

Thus, the implementation of monitoring programs using chemical analytical methods such as LC–MS/MS instead of MBA in the Indian Ocean and the Red Sea is urgently needed in different species of shellfish and puffer fish, including Arothron hispidus, Takifugu oblongus, Lageocephalus scitalleratus, Pleuranacanthus sceleratus, Chelonodon patoca, Sphaeroides oblongus, Lagocephalus inermis, Lagocephalus lunaris, Xenopterus naritus, Arothron stellatus, Tetractenos hamiltoni, Tetraodon nigroviridis, Arothron reticularisand, Charonia sauliae, Babylonia japonica, Niotha spp., and Tutufa lissostoma, since they are most consumed and are already confirmed to be vectors of TTX in the Indian Ocean and the Red Sea. These species can be used as indicators for monitoring programs using the maximum limit permitted of 2 mg·kg−1 (from Japan).

Acknowledgments

We acknowledge the project H2020 RISE project EMERTOX—Emergent Marine Toxins in the North Atlantic and Mediterranean: New Approaches to Assess their Occurrence and Future Scenarios in the Framework of Global Environmental Changes—Grant Agreement No. 778069.

Author Contributions

V.V. and M.S. conceived the idea. I.J.T. drafted the manuscript. The final version of the manuscript was approved by all authors.

Funding

This research was partially supported by the framework of the Atlantic Interreg project ALERTOXNET—Network for introduction of Innovative Toxicity Alert Systems for safer seafood products—EAPA_317/2016.

Conflicts of Interest

The authors declare no conflicts of interest.

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