Neurotoxic marine poisoning

doi:10.1016/S1474-4422(05)70041-7

The Lancet Neurology

Volume 4, Issue 4, April 2005, Pages 219-228

https://doi.org/10.1016/S1474-4422(05)70041-7 Get rights and content

Summary

Marine poisoning results from the ingestion of marine animals that contain toxic substances and causes substantial illness in coastal regions. Three main clinical syndromes of marine poisoning have important neurological symptoms—ciguatera, tetrodotoxin poisoning, and paralytic shellfish poisoning. Ciguatera is the commonest syndrome of marine poisoning and is characterised by moderate to severe gastrointestinal effects (vomiting, diarrhoea, and abdominal cramps) and neurological effects (myalgia, paraesthesia, cold allodynia, and ataxia), but is rarely lethal. Tetrodotoxin poisoning and paralytic shellfish poisoning are less common but have a higher fatality rate than ciguatera. Mild gastrointestinal effects and a descending paralysis are characteristic of these types of poisoning. In severe poisoning, paralysis rapidly progresses to respiratory failure. Diagnosis of all types of marine poisoning is made from the circumstances of ingestion (type of fish and location) and the clinical effects. Because there are no antidotes, supportive care, including mechanical ventilation in patients with severe paralysis, is the mainstay of treatment.

Section snippets

Marine poisoning

An important distinction between envenoming and poisoning is pertinent to marine poisoning. Venomous animals have a specialised gland that produces venom, and the venom is applied or injected parenterally. Other marine animals accumulate toxic compounds from their environment and do not have specialised toxin-producing glands; consequently, these animals must be ingested to produce toxic effects.⁶ Marine poisons generally consist of heat and gastric-acid stable low-molecular-weight toxins.⁶

Impulse conduction

In peripheral-nerve myelinated axons, voltage-sensitive Na⁺ channels in the nodal axon are clustered at high densities (up to 1000/μm²) compared with the internodal region (25/μm²).⁷ The high density of Na⁺ channels at the node reflects the need of saltatory conduction for a large inward current at the node (figure 1).⁸ When the nodal membrane is depolarised, an inward current forms, carried by Na⁺. The Na⁺ conductance is voltage sensitive and regenerative: it increases with depolarisation, and

Ciguatera poisoning

The commonest marine poisoning, ciguatera is endemic throughout subtropical and tropical regions of the Indo-Pacific and Caribbean.12, 13, 14, 15, 16, 17, 18, 19, 20 Ciguatera is rarely fatal and causes moderate neurological and gastrointestinal effects in most people. With the transportation of fish to distant locations, ciguatera is now also being reported in non-endemic regions.⁶

Ciguatera is caused by the ingestion of ciguatoxins that accumulate in certain tropical and subtropical finfish.¹³

Puffer fish (tetrodotoxin) poisoning

Puffer fish poisoning results from the ingestion of fish containing tetrodotoxin and is the commonest lethal marine poisoning. Tetrodotoxin poisoning mainly occurs in southeast Asia, most commonly in Japan where fugu (puffer fish fillet) is a delicacy.50, 51, 52, 53 In the early part of the 20th century, 100 deaths per year from ingestion of fugu were reported in Japan;⁵² the rate of deaths has decreased substantially with improved legislation of fugu preparation and marketing. However,

Shellfish poisoning

Shellfish contamination is a medical and economic problem affecting fisheries mainly in temperate regions. Although viral and bacterial infections resulting from shellfish ingestion are more common, toxin-mediated shellfish poisoning can cause severe and life-threatening neurological effects. Toxic shellfish poisoning makes up about 1·1% of food-borne illness, or 7·4% of marine intoxications in the USA.⁶

Four major toxic syndromes result from shellfish ingestion and three of these are mostly

Other neurotoxic marine poisoning

Clupeotoxism is an enigmatic marine poisoning reported from the Caribbean and Indo-Pacific region that results from the ingestion of plankton-eating fish, such as herring and sardines.6, 73, 95 The effects of clupeotoxism are more severe than for other marine poisoning and the fatality rate is high.⁹⁵ Gastrointestinal symptoms include nausea, vomiting, abdominal cramping, and diarrhoea associated with an unusual sharp metallic taste. Neurological effects include dilated pupils, paraesthesia,

Conclusion

Description of the common neurotoxic marine poisonings is important for increased awareness of these syndromes. However, prevention of potentially life-threatening poisoning is key and clearly, people should exercise caution—discretion rather than valour—whenever confronted with a plate of exotic shellfish or large tropical fish. Travellers should consult appropriate medical travel-information services for region and season specific information.

Search strategy and selection criteria

MEDLINE 1966 to October 2004 and EMBASE 1980 to October 2004 were searched for: “marine poisoning”, “nerve conduction studies”, “neurotoxicity”, “ciguatera”, “tetrodotoxin poisoning”, and “shellfish poisoning”. Further articles were included from reference lists, review articles, and major textbook chapters on marine toxinology. Abstracts and reports from meetings were also included. The final reference list was generated based on originality and relevance to the topics covered in the

References (98)

D Burke et al.
Excitability of human axons
Clin Neurophysiol
(2001)
N Ogata et al.
Molecular diversity of structure and function of the voltage-gated Na+ channels
Jpn J Pharmacol
(2002)
RJ Lewis
The changing face of ciguatera
Toxicon
(2001)
L Lehane et al.
Ciguatera: recent advances but the risk remains
Int J Food Microbiol
(2000)
RJ Lewis et al.
Origin and transfer of toxins involved in ciguatera
Comp Biochem Physiol C
(1993)
C Mattei et al.
Hyperosmolar D-mannitol reverses the increased membrane excitability and the nodal swelling caused by Caribbean ciguatoxin-1 in single frog myelinated axons
Brain Res
(1999)
RJ Lewis et al.
Comparative action of three major ciguatoxins on guinea-pig atria and ilea
Toxicon
(1993)
J Cameron et al.
Effects of ciguatoxin on nerve excitability in rats (part I)
J Neurol Sci
(1991)
J Cameron et al.
Electrophysiological studies on ciguatera poisoning in man (part II)
J Neurol Sci
(1991)
CE Purcell et al.
Action of mannitol in ciguatoxin-intoxicated rats
Toxicon
(1999)

RJ Lewis et al.

Ciguatera and mannitol: in vivo and in vitro assessment in mice

Toxicon

(1993)

WR Lange et al.

Potential benefit of tocainide in the treatment of ciguatera: report of three cases

Am J Med

(1988)

C-K How et al.

Tetrodotoxin poisoning

Am J Emerg Med

(2003)

YH Tsai et al.

Occurrence of tetrodotoxin and paralytic shellfish poison in the Taiwanese crab Lophozozymus pictor

Toxicon

(1995)

LE Llewellyn et al.

Post-mortem analysis of samples from a human victim of a fatal poisoning caused by the xanthid crab, Zosimus aeneus

Toxicon

(2002)

B Hille

The receptor for tetrodotoxin and saxitoxin: a structural hypothesis

Biophys J

(1975)

S Cestele et al.

Molecular mechanisms of neurotoxin action on voltage-gated sodium channels

Biochimie

(2000)

R Littlewood et al.

Clinical findings in three cases of zombification

Lancet

(1997)

MA O'Leary et al.

Use of high performance liquid chromatography to measure tetrodotoxin in serum and urine of poisoned patients

Toxicon

(2004)

S Fukiya et al.

Active and passive immunization for tetrodotoxin in mice

Toxicon

(1992)

QH Xu et al.

Toxin-neutralizing effect and activity-quality relationship for mice tetrodotoxin-specific polyclonal antibodies

Toxicology

(2005)

N Lagos et al.

The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil

Toxicon

(1999)

H Ishida et al.

Study on neurotoxic shellfish poisoning involving the oyster, Crassostrea gigas, in New Zealand

Toxicon

(1996)

P Vale et al.

Domoic acid in Portuguese shellfish and fish

Toxicon

(2001)

AP Sierra-Beltran et al.

An overview of the marine food poisoning in Mexico

Toxicon

(1998)

GB Glavin et al.

Mussel poisoning and excitatory amino acid receptors

Trends Pharmacol Sci

(1989)

Y Onuma et al.

Identification of putative palytoxin as the cause of clupeotoxism

Toxicon

(1999)

C Frelin et al.

Palytoxin: recent electrophysiological and pharmacological evidence for several mechanisms of action

Gen Pharmacol

(1995)

P Boisier et al.

Fatal mass poisoning in Madagascar following ingestion of a shark (Carcharhinus leucas): clinical and epidemiological aspects and isolation of toxins

Toxicon

(1995)

J Brusle

Ciguatera fish poisoning—a review: sanitary and economic aspects

(1992)

J White et al.

Clinical toxicology—where are we now?

J Toxicol Clin Toxicol

(2003)

DR Smart

Scombroid poisoning: a report of seven cases involving the Western Australian salmon, Arripis truttaceus

Med J Aust

(1992)

JD Morrow et al.

Evidence that histamine is the causative toxin of scombroid-fish poisoning

N Engl J Med

(1991)

M Hall

Something fishy: six patients with an unusual cause of food poisoning!

Emerg Med

(2003)

J Meier et al.

Handbook of clinical toxicology of animal venoms and poisons

(1995)

SG Waxman et al.

Molecular dissection of the myelinated axon

Ann Neurol

(1993)

B Hille

Ionic channels of excitable membranes

(1992)

F Porreca et al.

A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain

Proc Natl Acad Sci USA

(1999)

H Schnorf et al.

Ciguatera fish poisoning: a double-blind randomized trial of mannitol therapy

Neurology

(2002)

R Bagnis et al.

Clinical observations on 3009 cases of ciguatera (fish poisoning) in the South Pacific

Am J Trop Med Hyg

(1979)

R Bagnis et al.

Clinical features of 12 890 cases of ciguatera (fish poisoning) in French Polynesia

NC Gillespie et al.

Ciguatera in Australia: occurrence, clinical features, pathophysiology, and management

Med J Aust

(1986)

R Johnson et al.

Ciguatera: Caribbean and Indo-Pacific Fish Poisoning

West J Med

(1983)

Y Narayan

Fish poisoning in Fiji

Fiji Med

(1980)

DN Lawrence et al.

Ciguatera fish poisoning in Miami

JAMA

(1980)

JG Morris et al.

Ciguatera fish poisoning: epidemiology of the disease on St Thomas, US Virgin Islands

Am J Trop Med Hyg

(1982)

JE Connell et al.

Risk of ciguatera fish poisoning: impact on recommendations to eat more fish

Asia Pac J Clin Nutr

(2003)

J Pearn et al.

Ciguatera and pregnancy

Med J Aust

(1982)

RE Lucas et al.

Pacific ciguatoxin-1 associated with a large common-source outbreak of ciguatera in east Arnhem Land, Australia

Nat Toxins

(1997)

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Ciguatera is a common marine, toxin-borne illness caused by the consumption of fish that contain toxins that activate voltage-sensitive sodium channels. The clinical manifestations of ciguatera are typically self-limited, but chronic symptoms may occur in a minority of patients. This report describes a case of ciguatera poisoning with chronic symptoms, including pruritus and paresthesias. A 40-y-old man was diagnosed with ciguatera poisoning after consuming amberjack while vacationing in the US Virgin Islands. His initial symptoms, including diarrhea, cold allodynia, and extremity paresthesias, evolved into chronic, fluctuating paresthesias and pruritus that became worse after the consumption of alcohol, fish, nuts, and chocolate. After a comprehensive neurologic evaluation failed to reveal another cause for his symptoms, he was diagnosed with chronic ciguatera poisoning. His neuropathic symptoms were treated with duloxetine and pregabalin, and he was counseled to avoid foods that triggered his symptoms. Chronic ciguatera is a clinical diagnosis. Signs and symptoms of chronic ciguatera can include fatigue, myalgias, headache, and pruritus. The pathophysiology of chronic ciguatera is incompletely understood but may involve genetic factors or immune dysregulation. Treatment involves supportive care and avoidance of foods and environmental conditions that may exacerbate symptoms.
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Harmful algal blooms (HABs) in marine, brackish, and fresh-water environments are caused by a variety of microscopic algae and cyanobacteria. HABs are hazardous and sometimes fatal to human and animal populations, either through toxicity, or by creating ecological conditions, such as oxygen depletion, which can kill fish and other economically or ecologically important organisms. HAB hazards have increased globally since the 1970s because of eutrophication, climate change, species translocations, and the interactions of these influences. Human vulnerability to HABs is greatest in communities that are nutritionally and economically reliant on fishery resources, but locally HABs also cause damage to tourist industries and have health-associated costs. There have been major research advances in the monitoring, detection, modeling, forecasting, prevention, communication, and treatment of HAB events, which have helped mitigate health and economic risks. However, reducing HAB incidents in the future will be challenging, due to heavily entrenched socio-ecological systems of food production and land management where nutrient fluxes are likely to increase.
Simple and fast determination of tetrodotoxin in human plasma based on hydrophilic-interaction/ion-exchange mixed-mode solid phase extraction combined with liquid chromatography-tandem mass spectroscopy
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ReviewNeurotoxic marine poisoning

Summary

Section snippets

Marine poisoning

Impulse conduction

Ciguatera poisoning

Puffer fish (tetrodotoxin) poisoning

Shellfish poisoning

Other neurotoxic marine poisoning

Conclusion

Search strategy and selection criteria

Clin Neurophysiol

Jpn J Pharmacol

Toxicon

Int J Food Microbiol

Comp Biochem Physiol C

Brain Res

Toxicon

J Neurol Sci

J Neurol Sci

Toxicon

Toxicon

Am J Med

Am J Emerg Med

Toxicon

Toxicon

Biophys J

Biochimie

Lancet

Toxicon

Toxicon

Toxicology

Toxicon

Toxicon

Toxicon

Toxicon

Trends Pharmacol Sci

Toxicon

Gen Pharmacol

Toxicon

Ciguatera fish poisoning—a review: sanitary and economic aspects

Clinical toxicology—where are we now?

J Toxicol Clin Toxicol

Scombroid poisoning: a report of seven cases involving the Western Australian salmon, Arripis truttaceus

Med J Aust

Evidence that histamine is the causative toxin of scombroid-fish poisoning

N Engl J Med

Something fishy: six patients with an unusual cause of food poisoning!

Emerg Med

Handbook of clinical toxicology of animal venoms and poisons

Molecular dissection of the myelinated axon

Ann Neurol

Ionic channels of excitable membranes

A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain

Proc Natl Acad Sci USA

Ciguatera fish poisoning: a double-blind randomized trial of mannitol therapy

Neurology

Clinical observations on 3009 cases of ciguatera (fish poisoning) in the South Pacific

Am J Trop Med Hyg

Clinical features of 12 890 cases of ciguatera (fish poisoning) in French Polynesia

Ciguatera in Australia: occurrence, clinical features, pathophysiology, and management

Med J Aust

Ciguatera: Caribbean and Indo-Pacific Fish Poisoning

West J Med

Fish poisoning in Fiji

Fiji Med

Ciguatera fish poisoning in Miami

JAMA

Ciguatera fish poisoning: epidemiology of the disease on St Thomas, US Virgin Islands

Am J Trop Med Hyg

Risk of ciguatera fish poisoning: impact on recommendations to eat more fish

Asia Pac J Clin Nutr

Ciguatera and pregnancy

Med J Aust

Pacific ciguatoxin-1 associated with a large common-source outbreak of ciguatera in east Arnhem Land, Australia

Nat Toxins

Review
Neurotoxic marine poisoning