(Extracted from FAO FOOD AND NUTRITION PAPER 80, Marine Biotoxins, ISSN 0254-4725)
Introduction
Microscopic planktonic algae of the world’s oceans are critical food for filter-feeding bivalve shellfish (oysters, mussels, scallops, clams) as well as for the larvae of commercially important crustaceans and finfish. Among the 5 000 existing marine algal species, approximately 300 can sometimes occur in such high numbers (blooming) that they obviously discolour the surface of the sea, the so-called “red tides” (Hallegraeff et al., 1995; Lindahl, 1998). The word “bloom” is used to indicate the explosive growth of any of these organisms, which may vary in colour from the commonly cited red (so called “red tides”) to different shades of yellow, green, brown or blue depending on the type of protista and their depth and concentration. The commonly used term “red tide” comes from the fact that a massive number of organisms often appear as red streaks across the surface of the water (Bower et al., 1981). The conditions for an algal bloom are not yet fully elucidated but the phenomenon is probably influenced by climatic and hydrographic circumstances (Van Egmond and Speijers, 1999). The explosive growths sometimes appear during changes in weather conditions but important contributing causes may be variations in upwellings, temperature, transparency, turbulence or salinity of the water, the concentration of dissolved nutrients, wind or surface illumination (Bower et al., 1981).
There are no reasons to assume that shellfish intoxication can be predicted by the properties of the regional area. In general, red tides often occur when heating or freshwater runoff creates a stratified surface layer above colder, nutrient-rich waters. Fast-growing algae quickly strip away nutrients in the upper layer, leaving nitrogen and phosphorus only below the interface of the layers, called the pycnocline. Non-motile algae cannot easily get to this layer whereas motile algae, such as the dinoflagellates, can thrive. Many swim at speeds in excess of 10 metres a day, and some undergo daily vertical migration; they reside in surface water like sunbathers and then swim down to the pycnocline to take up nutrients at night. As a result, blooms can suddenly appear in surface waters that are devoid of nutrients and seem incapable of supporting such prolific growth (Anderson, 1994).
Evidence is increasing from diverse areas (such as the Hong Kong Harbour, the Seto Inland Sea in Japan and North European coastal waters) that “cultural eutrophication” from domestic, industrial and agricultural wastes can stimulate harmful algal blooms. It is even possible that algal species which are normally not toxic may be rendered toxic when exposed to atypical nutrient regimes (e.g. phosphate deficiencies) resulting from cultural eutrophication. Changed patterns of land use, such as deforestation, can also cause shifts in phytoplankton species composition by increasing the concentrations of humic substances in land runoff. Acid precipitation can further increase the mobility of humic substances and trace metals in soils (Hallegraeff, 1993).
Some species produce basically harmless water discolorations. On the other hand, some species can bloom so densely, under exceptional conditions in sheltered bays, that they indiscriminately kill fish and invertebrates due to oxygen depletion. Other algal species can be harmful to fish and invertebrates (especially in intensive aquaculture systems) by damaging or clogging their gills. Furthermore, there are micro-algal species (about 75) which have the capacity to produce potent toxins (called phycotoxins) that can find their way through levels of the food chain (e.g. molluscs, crustaceans and finfish) and are ultimately consumed by humans causing a variety of gastrointestinal and neurological illnesses. Some algal species already produce toxins at low abundances of some hundreds of cells per litre, while other algal species must occur in some millions of cells per litre in order to cause any harm. Most of the harmful species have a restricted distribution pattern but some harmful species have a worldwide distribution (Hallegraeff et al., 1995; Lindahl, 1998).
It is not clear why some micro-algal species produce toxins. These toxins are secondary metabolites with no explicit role in the internal economy of the organisms that produce them and with very specific activities in mammals. They are probably used by their producers as a way to compete for space, fight predation or as a defence against the overgrowth of other organisms (Botana et al., 1996).
During the past two decades, the frequency, intensity and geographic distribution of harmful algal blooms has increased, along with the number of toxic compounds found in the marine food chain. Different explanations for this trend have been given such as increased scientific awareness of toxic algal species, increased utilization of coastal waters for aquaculture, transfer of shellfish stocks from one area to another, cultural eutrophication from domestic, industrial and agricultural wastes, increased mobility of humic substances and trace metals from soil due to deforestation and/or by acid precipitation (acid rain), and unusual climatic conditions (Hallegraeff et al., 1995). In addition, monitoring for toxic algae and/or (shell)fish is now carried out in several coastal areas of the world. Figures 1.1 and 1.2 illustrate monitoring in coastal waters of European and North American countries in the International Council for the Exploration of the Sea (ICES)[1]. The transportation of dinoflagellate resting cysts, especially from paralytic shellfish poisoning toxin producers (McMinn et al., 1997), either in a ship’s ballast water or through the movement of shellfish stocks from one area to another provides another possible explanation for the increasing trend of harmful algal blooms (Hallegraeff et al., 1995).
The resting cyst or hypnozygote is the immobile form of some dinoflagellates. These cysts sink to the bottom of the sea and accumulate at the borderline of water and sediment where they over-winter. When favourable growth conditions return, the cysts may germinate and reinoculate the water with swimming cells that can subsequently bloom. In this way the survival of certain dinoflagellates from one season to the other season is assured (Mons et al., 1998).
Exchanges in mid-ocean of a ship’s ballast water that is derived from the open harbour, with ballast water from the open ocean can be partly effective in controlling not only cysts but also the harmful dinoflagellates and diatoms themselves. Incomplete elimination of harmful organisms is caused by the incomplete discharge of water and sediments in the ballast tank during reballasting (Zhang and Dickman, 1999). However, mid-water exchange within regional seas (for example the North Sea, Irish Sea or English Channel) is less efficient than within oceanic waters. Mid-water exchange in regional seas may reduce the risk from polluted European harbour waters but may result in the transportation of potentially harmful phytoplankton species from the regional seas (Macdonald and Davidson, 1998).
The most important marine phycotoxins are shellfish toxins and ciguatoxins. Until now, five groups of shellfish toxins have been distinguished, namely:
1. paralytic shellfish toxins causing paralytic shellfish poisoning (PSP);
2. diarrhoeic shellfish toxins causing diarrhoeic shellfish poisoning (DSP);
3. amnesic shellfish toxins causing amnesic shellfish poisoning (ASP);
4. neurotoxic shellfish toxins causing neurotoxic shellfish poisoning (NSP); and
5. azaspiracid shellfish toxins causing azaspiracid shellfish poisoning (AZP) (Hallegraeff et al., 1995; Lindahl, 1998).
6. Ciguatoxins cause ciguatera fish poisoning (CFP). PSP, DSP, ASP, NSP and AZP are caused by human consumption of contaminated shellfish products whereas CFP is caused by the consumption of subtropical and tropical marine carnivorous fish that have accumulated ciguatera toxins through the marine food chain. Various aspects of these toxins will be reviewed in this publication
Paralytic Shellfish Poisoning (PSP)
Paralytic shellfish poisoning (PSP) in humans is caused by ingestion of shellfish containing PSP toxins. These PSP toxins are accumulated by shellfish grazing on algae producing these toxins. Symptoms of human PSP intoxication vary from a slight tingling or numbness to complete respiratory paralysis. In fatal cases, respiratory paralysis occurs within 2 to 12 hours of consumption of the PSP contaminated food.
The PSP toxins are a group of 21 closely related tetrahydropurines (see Figure 2.1). The first PSP toxin chemically characterized was saxitoxin (STX). The various PSP toxins significantly differ in toxicity with STX being the most toxic. The PSP toxins are produced mainly by dinoflagellates belonging to the genus Alexandrium, which may occur both in the tropical and moderate climate zones. Shellfish grazing on these algae can accumulate the toxins but the shellfish itself is rather resistant to the harmful effects of these toxins. During the last 20 years, there seems to have been an increase in intoxications caused by PSP. However, as yet it is unclear whether the increase is real, whether it could be a consequence of improved identification, detection and medical registration, or whether it is due to expanded shellfish culture and consumption. A few dozen countries have regulations for PSP toxins. Most regulations are set for PSP toxins as a group.
Diarrhoeic Shellfish Poisoning (DSP)
Diarrhoeic Shellfish Poisoning (DSP) in humans is caused by the ingestion of contaminated bivalves such as mussels, scallops, oysters or clams. The fat soluble DSP toxins accumulate in the fatty tissue of the bivalves. DSP symptoms are diarrhoea, nausea, vomiting and abdominal pain starting 30 minutes to a few hours after ingestion and complete recovery occurs within three days. DSP toxins can be divided into different groups depending on chemical structure. The first group, acidic toxins, includes okadaic acid (OA) and its derivatives named dynophysistoxins (DTXs). The second group, neutral toxins, consists of polyether-lactones of the pectenotoxin group (PTXs). The third group includes a sulphated polyether and its derivatives the yessotoxins (YTXs) (see Figures 3.1 and 3.2).
DSP toxins are produced usually by dinoflagellates that belong to the genera Dinophysis spp., however, the dinoflagellate genus Prorocentrum has also been found to be a producer of DSP toxins. DSP toxin production may vary considerably among dinoflagellate species and among regional and seasonal morphotypes in one species. The number of dinoflagellate cells per litre of water needed to contaminate shellfish is also variable. The most affected areas seem to be Europe and Japan. DSP incidences, or at least the presence of DSP toxins, appear to be increasing and DSP toxins producing algae and toxic bivalves are frequently reported from new areas.
Amnesic Shellfish Poisoning (ASP)
Amnesic shellfish poisoning (ASP), also known as domoic acid poisoning (DAP) because amnesia is not always present, was first recognised in 1987 in Prince Edward Island, Canada. At this time, ASP caused three deaths and 105 cases of acute human poisoning following the consumption of blue mussels. The symptoms included abdominal cramps, vomiting, disorientation and memory loss (amnesia). The causative toxin (the excitatory amino acid domoic acid or DA) was produced by the diatom species Pseudo-nitzschiapungens f. multiseries (=Nitzschia pungens f. multiseries) (Hallegraeff, 1995).
In September 1991, the unexplained deaths of pelicans and cormorants in Monterey Bay, California were attributed to an outbreak of DA poisoning produced by a related diatom Pseudo-nitzschia australis. This diatom was consumed by anchovies that in turn were eaten by the birds. In October 1991, extracts of razor clams from the coast of Oregon were found to induce DA acid-like symptoms in mice. These incidents prompted the regulatory authorities in the United States to conduct a massive survey of many marine species for the presence of DA. The toxin was found widely from California to Washington, and was also found unexpectedly in crabs, the first time this toxin was demonstrated in a crustacean. Since these incidents, global awareness of DA and its producing sources has been raised (Wright and Quilliam, 1995).
Neurologic Shellfish Poisoning (NSP)
Neurologic or neurotoxic shellfish poisoning (NSP) is caused by polyether brevetoxins produced by the unarmoured dinoflagellate Gymnodinium breve (also called Ptychodiscus breve, since 2000 called Karenia brevis). The brevetoxins are toxic to fish, marine mammals, birds and humans, but not to shellfish. Until 1992/1993, neurologic shellfish poisoning was considered to be endemic to the Gulf of Mexico and the east coast of Florida, where “red tides” had been reported as early as 1844. An unusual feature of Gymnodinium breve is the formation by wave action of toxic aerosols which can lead to asthma-like symptoms in humans. In 1987, a major Florida bloom event was dispersed by the Gulf Stream northward into North Carolina waters where it has since continued to be present. In early 1993, more than 180 human shellfish poisonings were reported from New Zealand caused by an organism similar to G.breve. Most likely, this was a member of the hidden plankton flora (previously present in low concentrations), which developed into bloom proportions triggered by unusual climatic conditions (higher than usual rainfall, lower than usual temperature) coincident with an El Niño event (Hallegraeff, 1995).
Azaspiracid Shellfish Poisoning (AZP)
In November 1995, at least eight people in the Netherlands became ill after eating mussels (Mytilus edulis) cultivated at Killary Harbour, Ireland. Although the symptoms resembled those of diarrhoeic shellfish poisoning (DSP), concentrations of the major DSP toxins were very low (McMahon and Silke, 1996; Satake et al., 1998a). The known organisms producing DSP toxins were not observed in water samples collected at that time. In addition, a slowly progressing paralysis was observed in the mouse assay using the mussel extracts. These neurotoxic symptoms were quite different from typical DSP toxicity (Satake et al., 1998a). It was then that azaspiracid (formerly called Killary Toxin-3 or KT3) was identified and the new toxic syndrome was called azaspiracid poisoning (AZP).
Ciguatera Fish Poisoning (CFP)
Ciguatera fish poisoning (CFP) has been known for centuries. It was reported in the West Indies by Peter Martyr de Anghera in 1511, in the islands of Indian Ocean by Harmansen in 1601 and in the various archipelagos of the Pacific Ocean by De Quiros in 1606. Endemic areas are mainly the tropical and subtropical Pacific and Indian Ocean insular regions and the tropical Caribbean, but continental reef areas are also affected (Legrand, 1998). The name ciguatera was given by Don Antonio Parra in Cuba in 1787 to intoxication following ingestion of the “cigua”, the Spanish trivial name of an univalve mollusc, Turbo pica, reputed to cause indigestion. The term “cigua” was somehow transferred to an intoxication caused by the ingestion of coral reef fishes (De Fouw et al., 2001). The causative toxins, the ciguatoxins, accumulate through the food chain, from small herbivorous fish grazing on the coral reefs into organs of bigger carnivorous fish that feed on them (Angibaud and Rambaud, 1998; Lehane, 2000).
In the past, the ciguatera food poisoning in humans was highly localized to coastal, often island communities of indigenous peoples. However, with the increases in seafood trade, increased worldwide seafood consumption and international tourism, the target populations have become international. At present, ciguatera is the most common type of marine food poisoning worldwide and, with an estimated 10 000 to 50 000 people worldwide suffering from the disease annually, it constitutes a global health problem (De Fouw et al., 2001; Lehane, 2000).
No indicator such as the highly visible surface phenomenon, the so-called “red tide” as seen by shellfish poisonings, has ever been associated with ciguatera. It is this lack of warning signal that has contributed to the dread of ciguatera poisoning (De Fouw et al., 2001).
© Food and Agriculture Organization of The United Nations (FAO). Rome, 2004