Ciguatera fish poisoning -Increasing due toreef destruction? Sara Nordström Degree project inbiology, Master ofscience (1year), 2013 Examensarbete ibiologi 30 hp tillmagisterexamen, 2013 Biology Education Centre, Uppsala University, and Livsmedelsverket Supervisors: Jan Örberg and Lilianne Abramsson Zetterberg, Christer Andersson Abstract Ciguatera fish poisoning (CFP) can occur after ingestion of different reef fish that contain a toxin or several toxins known as ciguatoxins. The focus of this essay is to describe what CFP is and if there is a connection between environmental problems and the occurrence of CFP. Focus will be on the following questions: What is CFP? Is there any risk of being poisoned from CFP in Sweden? What environmental factors can increase the occurrence of ciguatera outbreaks? Are human activities responsible for ciguatera outbreaks? The ciguatoxin origins from a benthic dinoflagellate called Gambierdiscus toxicus. CFP is a problem in the tropical regions of the world, and particularly in the small island countries around the pacific basin and the West Indies. Fish that cause the poisoning usually live in shallow waters close to coral reefs. The toxicity of the fish largely depends on where it lived and fed. Several species of fish have been associated with CFP. The moray eel is often regarded as the most poisonous species. Other species that often seem to cause the poisoning are species of snappers, groupers, barracudas and the narrow-barred Spanish mackerel. The symptoms of CFP usually are combination of gastrointestinal symptoms, and neurological symptoms. There is no specific treatment so focus is on reducing the symptoms. CFP is rarely fatal but sometimes there are complications associated to cardiac problems. The symptoms can persist for a long time and can return after eating fish, chicken or drinking alcohol, several years after the poisoning. The severity of the symptoms seem to be dose dependent and the lowest toxic dose to humans is 0.05 μg of the toxin or 0.01 μg /kg bodyweight. The toxins remain stable after heating. Several different ciguatoxins (CTX) have been identified that are responsible for causing CFP. The most potent ciguatoxin is P-CTX-1, where P stands for Pacific. CFP is not often reported to authorities and in Australia it is estimated that only 20% of the actual cases are reported. In 2001 the Swedish Poisons Information Centre reported that so far, to their knowledge, there had only been one single incident of CFP in Sweden where three people were poisoned during a vacation abroad. It is not known what initiates blooms of Gambierdiscus toxicus that is responsible for the ciguatera outbreaks. Reef destruction seems to cause outbreaks of CFP. One of the reasons for this is that there are more substrates (consisting of dead corals) for the hosts (macroalgae) of the dinoflagellate to grow on. Many different types of reef destruction can increase the frequency of the ciguatera outbreaks. Some of these are land erosion and coral bleaching, a phenomenon strongly associated to El Niño and an increase in water temperature. In order to prevent CFP it is important to bear in mind the relationship between coral destruction and outbreaks of CFP. It is also important to refrain from eating large servings of the same fish. i Contents Abstract i Contents ii 1 Introduction 1 2 The project 1 3 Literature 2 4 Ciguatera fish poisoning 2 4.1 History 2 4.2 Occurrence of ciguatera fish poisoning 3 4.3 Species associated with ciguatera fish poisoning 4 4.4 Toxins found in ciguateric fish 6 4.5 Symptoms of ciguatera fish poisoning 9 4.5.1 Duration of symptoms and persistence of ciguatoxin in the body 10 4.6 Pathological findings in experimental animals and man 10 4.6.1 Single dose administration of ciguatoxin 10 4.6.2 Repeated administration of ciguatoxin 11 4.7 Treatment of ciguatera fish poisoning 11 4.8 Prevention 12 4.9 Methods to identify and quantify ciguatoxins 13 4.10 Concentrations in fish and toxic doses 14 4.11 Mechanism of action 15 4.12 Toxicokinetics 16 4.13 Ciguatera fish poisoning and cardiac toxicity in humans 16 4.14 Ciguatera fish poisoning and foetal development in humans 16 4.15 Cases 17 4.16 Ciguatera fish poisoning in the world 18 4.17 Ciguatera fish poisoning in Sweden 19 5 Environmental aspects on ciguatera fish poisoning 19 5.1 Biology of Gambierdiscus toxicus 19 5.2 Maitotoxin 20 5.3 Environmental conditions causing ciguatera outbreaks 20 5.3.1 Bacteria 21 5.3.2 Destruction of corals 21 5.3.3 Coral bleaching 21 5.3.4 Land erosion 22 5.3.5 Increase in nutrients due to coral destruction 22 5.3.6 An acidic environment 22 5.4 Correlation between ciguatera fish poisoning and El Niño 22 5.5 Toxicity of Gambierdiscus toxicus 23 5.6 Can outbreaks of ciguatera fish poisoning be predicted? 23 6 Conclusions 25 Acknowledgements 26 7 References 27 Appendix 30 ii 1 Introduction Ciguatera fish poisoning, or CFP, is a type of poisoning that can occur in humans after the ingestion of various types of reef fish that contains a toxin or several related toxins called ciguatoxins. It is a major health problem in the tropical regions of the world and can be mistaken with several other forms of marine poisoning. The major toxin is lipid-soluble but there may also be other, water-soluble toxins involved in this type of poisoning. The initial signs of poisoning are gastrointestinal symptoms such as diarrhoea and abdominal pain that usually are followed by neurological symptoms (Lewis and King, 1996). Worldwide CFP is probably the most reported illness when it comes to seafood-poisonings. Still it is very under-reported, probably because the symptoms are not necessary severe and are easily confused with other seafood poisonings or diseases (Lehane and Lewis, 2000). The new technology and transportation techniques make it possible to transport marine organisms all over the world. But the knowledge about these exotic products is scarce in our parts of the world and it is therefore important to spread information to prevent possible food poisonings. In the Nordic countries there are only a few reports of CFP but there are people from Sweden who have been poisoned during their vacation to tropical parts of the world. There are results indicating a relationship between the destruction of coral reefs and an increase in the frequency of CFP. This relation is not yet clearly understood, and the scientists are looking at several different factors that can affect the frequency of the outbreaks, such as water temperature, salinity and amounts of nutrients that are available. The purpose of this essay is to describe what CFP is and if there is a connection between environmental problems and the occurrence of CFP. Focus will be on the following questions: What is CFP? Is there any risk of being poisoned from ciguatoxins in Sweden? What environmental factors can increase the occurrence of ciguatera outbreaks? Are human activities responsible for ciguatera outbreaks? 2 The Project This examination essay will be a part of a larger project initiated by Christer Andersson at the National Food Administration in Sweden. The project is funded by the Nordic council of ministers (Nordiska ministerrådet) and concerns natural toxins in seafood. Representatives from all of the Nordic countries are participating and contributing with their field of expertise. The completed project will be in the form of a dictionary concerning toxicological aspects of the consumption of marine organisms with regards to naturally occurring toxins. In this case the naturally occurring toxins mean those that the organism produces itself or substances produced naturally by another organism and then are accumulated into the organism via the intake of food. When completed the dictionary will be available in all the Nordic countries (Denmark, Finland, Iceland, Norway and Sweden). 1 3 Literature The material used in this essay have been obtained via PubMed (http://www.ncbi.nlm.nih.gov/pubmed), Toxline (http://toxnet.nlm.nih.gov/cgi- bin/sis/htmlgen?TOXLINE), and FishBase (http://www.fishbase.org/home.htm). PubMed is a database service by the National Library of Medicine, USA. Toxline is the U.S. National Library of Medicine’s collection of bibliographic information that concerns the biochemical, pharmacological, physiological and toxicological effects of drugs and other chemicals. FishBase is a large global online database of fish species that provides extensive species data, mostly on finfish. 4 Ciguatera Fish Poisoning CFP is a form of food poisoning that can occur in humans after ingestion of fish that contains one or several poisons known as ciguatoxins. 4.1 History CFP has been known to man for a long time, references of CFP go back as far as the T’ang Dynasty in China (618-907 AD) (Watters, 1995). Later, in 1606, sailors with the Spanish explorer Fernando de Quiros were reported to be affected by a fish called Pargos. Subsequently, many other reports of poisonings followed from the Caribbean region (Lewis and King, 1996). Captain Cook and four other crew-members got ill after eating a similar fish as the Pargos, caught in the waters of the New Hebrides. This was in July 1774 and was recorded in journals kept by two of the ship botanists. These two carefully took notes of the symptoms and at what time they started and ended. The only death that occurred on this occasion was a parakeet bird that had been fed the fish (Watters, 1995). The term ciguatera is believed to come from a marine turban shell called Turbo Pica, or cigua in Spanish (Lewis and King, 1996). This can be traced back to a Portuguese biologist, Don Antonio Parra, who noticed similar symptoms as from CFP, after ingestion of meat of cigua in 1771-1787 (Watters, 1995).