Ciguatera is a widespread food-borne
disease. It is a form of ichtyosarcotoxism whereby humans
are poisoned by eating fish intoxicated with toxins
generated by micro-algae at the base of the food chain.
The main algae involved in the production of toxins is the dinoflagellate Gambierdiscus toxicus (Adachi and Fukyo, 1979) although other species are also presumed to be associated with the disease but their role is more circumstantial. (Gramade and Dickey, 1990; Bomber, 1991)
- As stated in Bagnis (1981), the history of the disease dates back as far as 1555, when the first case was reported in the West Indies. The term itself originates from the marine snail "cigua", due to the fact that the symptoms of the disease are similar to those resulting from snail-consumption. It was first reported in the Indian Ocean in 1601. In the South Pacific Ocean, the first noted case of ciguatera was in 1770 when the crew of the Fernandez de Quiros became intoxicated. In 1776, Cook and Forster had noted in their ships journals further cases of poisoning by fish coming from the Pacific. In French Polynesia, the historic references of intoxicated fish date back to 1792.
- Ciguatera is widespread around the
circumtropics and globally around 20,000-50,000 people
annually are estimated to suffer from the poisoning (Lewis,
1992; Yasumoto and Satake, 1996). The geographical
distribution of ciguatera is mainly confined to a
circumglobal belt of latitude 35°N-35°S. The main areas
are in the Carribean, the Indian and the Pacific Oceans. However,
even within this range there is a large variability in
its occurance. For example, it is almost unknown in the
Maldives, the Seychelles, Guam, the Solomans, Wallis,
Futuna and several other places. On the other hand
there are areas that are toxic, including the area north
of Reunion Island and Mauritius.
There are now also cases of ciguatera in the USA and Canada as a result of tourism to contaminated areas and from the export of intoxicated fish.
- Symptoms are rarely fatal, although
mortality can result. This is normally brought about by
the consumption of the most toxic part of the fish, like
the liver or the roe. The severity of the symptoms varies
widely, as do the symptoms themselves. Normally, the
victim will suffer from parasthesia, head-ache and
vertigo in the first two to twelve hours after ingestion.
Following this, symptoms include nausea, vomitting, a
fall in blood pressure, irregular heart beat and an
increase in parasympathetic activity. In severe cases
paralysis, comatosis and death can result.
Natural antidotes against ciguatera have been proposed; plant remedies have been traditionally used. Laurent et al. (1993) reported a list of about 100 plants known in New Caledonia and Vanuatu, but tests have yet to be done to determine their effective detoxification action. Currently, mannitol is the advised treatment in the acute phase of the intoxivation (Lewis, 1992). An intravenous injection at a dose of 0.5 to 1.0g/kg body weight has recently been used with success ( Palafox et al., 1992).
- It was not until 1958 that Randall
first specutaled that the primary vector of ciguatera was
a benthic micro-organism and it wasn't until two decades
later in 1977 that Bagnis et al. and then Yasumoto et al.
(1979) suggested that this organism was a
dinoflagellate. It is now known that the cause of
ciguatera lies with the production of toxins by benthic
dinoflagellates, in particular, the species Gambierdiscus
toxicus. These dinoflagellates become
problematic when populations increase after the
destruction of coral reefs, as this provides an ideal
habitat for population expansion. When a reef is
destroyed, either by natural factors, such as storms,
earthquakes (Bagnis and Denizot, 1978; Bagnis, 1994) or a
rise in temperature (bleaching), or by anthropogenic
influence such as dredging work, construction of
ports and peers (Bagnis, 1968, 1987; Koike et al., 1991)
and eutrophication, the freshly denuded surfaces are
colonised by opportunistic macro-algae such as Halymenia
sp., Portieria sp., Turbinaria sp. and Sargassum sp.
etc. . These macro-algae are the hosts for the
dinoflagellates responsible for ciguatera as they provide
support and some of them excrete beneficial substances
such as polyphenols, nitrogenous compounds and vitamins (Bomber
et al., 1989) or inhibitive substances towards the
different epiphytic species. It seems that the
different macro-algal species are associated with
different dinoflagellate species. For example,
G.toxicus growth has been found to be stimulated
by Turbunaria ornata.(Grzebyk et al., 1994)
while P.lima, P.concavum and O.lenticularlis
are associated with filamentous green algae (Kohler and
Kohler, 1992). Generally, there is a preference for
red algae. Turf algae, like Jania and Amphiroa
are also preferential substrates for ciguateric
dinoflagellates. Gambierdiscus toxicus has been
observed on drift algae (Bomber et al., 1988)Suitable
light conditions and salinity as well as the availability
of a growth stimulant are also important for the
spatial distribution of these protists.
These dinofllagellates are not just epiphytic, some are benthic-detrital, like P.mexicamum, P.rueztlerianum, P.foraminosum, P.maculosum, P.hoffmannianum, P.emarginatum, Coolia monotis and Amphidinium sp., others are sand-dwellling like P.lima, P.sculptile, P.areanarium, and P.hoffmannianum while others are bloom-forming such as P.elegans and also P.mexicamum (Faust, 1995).
Herbivorous fish, such as the surgeon fish (Ctenochaetus striatus) and the parrot fish (Scaridae) consume the dinoflagellates and their toxins and so become toxic themselves. As larger, carnivorous fish ingest these fish, the toxins become concentrated and biotransformed. These carnivorous fish include species such as Moray eels (Murenidae), Jacks (Carangidae), Sea-bass (Serranidae) and Barracuda (Sphyraenidae). More than 425 species, from 60 different families have been found to carry ciguatera toxins (Bruslé 1997). Invertebrates and shellfish can also become toxic and transfer toxins up the food chain. For example; cladocera species and shrimps have been implicated in the poisoning of fish as have gastropod species and molluscs. (Russel and Egen, 1991) This transfer of toxins up through the trophic levels is known as the "food chain theory". (Glaziou and Legrand, 1994)
Dinoflagellates and toxins
- The main dinoflagellate thought to be the
causitive agent of ciguatera is Gambierdiscus toxicus
(Adachi and Fukyo, 1979; Fukuyo and Ishimaru, 1986).
There are also other species involved, including Prorocentrum
lima, P. concavum, P. hoffmannianum, P. cassubicum, P.
mexicanum, P.miniumum, Ostreopsis lenticularis, O.
siamensis, O. ovata, O. mascarensis, O.heptagona,
Amphidinium carteri, A. klebsii and Coolia montis.
These different species produce a number of toxins and
this is thought to be the cause of the multiplicity of
symptoms in the pathology of ciguatera (Bomber, 1991).
Ciguateric fish poisoning involves multiple toxins (Gramade and Dickey, 1990). The principal toxins involved are natual lipidic toxins known as ciguatoxins (CTX). However, maitotoxin (MTX), scaritoxin (STX) and okadaic acid are also involved. Maitotoxin, a water soluble compound is associated with the digestive tract of the herbivorous fish whilst ciguatoxins are associated with the viscera but also with the liver and muscle of the herbivorous and carnivorous fish.
G. toxicus can produce two types of toxin but other types appear as they are transferred up the food-chain and undergo acidic digestion and biotransformation. G. toxicus also produces maitotoxin which is the most potent marine toxin and gambiertoxin (GTX) which is a precursor for ciguatoxin. This is a less polar type of ciguatoxin, which can be oxidatively metabolised in fish to produce ciguatoxin.
P. lima , P. concavum and P. hoffmannianum are known to produce okadaic acid and are thought to be the cause of the gastro-intestinal symptoms. (Bomber, 1991)
|Species||Compound||Action of toxin|
|P.mexicanum||fast acting toxin||hemolytic|
- The presence of these dinoflagellates does not necessarily mean ciguatera will be present. For example, in the Lagoon of Mayotte numbers of G toxicus have been increasing since 1988, but as yet, no ciguatera poisoning has been found (Grzebyk, 1993). However, it has been said that the initial requirement for an iniation of ciguatera in a region is an increase in the population of G. toxicus (Gillespie et al., 1985). Despite this, even when numbers increase the population can still be non-toxic. It has been hypothesised that CTX is not always a growth product of G toxicus but that a specific stimulus may be required to begin the sequence of events leading to the formation of CTX (Gillespie et al., 1985; Faust, 1995). There is also the hypothesis that genetic differences in populations of dinoflagellates result in lack of production of ciguatoxin precursors. (Lewis et al. 1988) It has also been suggested that these polyether toxins may be produced to serve as allelochemical agents directed against close competitors or pathogens or to inhibit grazers. (Morton et al., 1994)
- As well as the poor heath as a result of poisoning, ciguatera has profound social and economic impacts. The loss of working days due to illness negatively effects the economy. To add to this, the prohibition of fish sales causes massive losses for the fish industry. There is also a large negative impact on aquaculture and tourism as a result of ciguatera.
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