Ciguatera

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Ciguatera is a foodborne illness caused by eating certain reef fish whose flesh is contaminated with a toxin made by dinoflagellates such as Gambierdiscus toxicus which live in tropical and subtropical waters. These dinoflagellates adhere to coral, algae and seaweed, where they are eaten by herbivorous fish which in turn are eaten by larger carnivorous fish like barracudas, shark, [1] and even omnivorous fish like basses and other fish like mullet. This is called biomagnification. Affected fish may show no sign of infection or, in more advanced cases, will be weakened and visibly thin, with yellowish eyes. As well, fish may be pale or a different color than usual.

Foodborne illness illness resulting from food that is spoiled or contaminated by pathogenic bacteria, viruses, parasites, or toxins

Foodborne illness is any illness resulting from the food spoilage of contaminated food, pathogenic bacteria, viruses, or parasites that contaminate food, as well as toxins such as poisonous mushrooms and various species of beans that have not been boiled for at least 10 minutes.

A toxin is a poisonous substance produced within living cells or organisms; synthetic toxicants created by artificial processes are thus excluded. The term was first used by organic chemist Ludwig Brieger (1849–1919), derived from the word toxic.

<i>Gambierdiscus toxicus</i> species of protist

Gambierdiscus toxicus is a species of dinoflagellates that can cause ciguatera. and is known to produce several polyether marine toxins, including ciguatoxin, maitotoxin, gambieric acid, and gambierol. The species was discovered attached to the surface of brown macroalgae in the Gambier Islands, French Polynesia.

Contents

Gambierdiscus toxicus is the primary dinoflagellate responsible for the production of a number of similar polyether toxins, including ciguatoxin, maitotoxin, gambieric acid and scaritoxin, as well as the long-chain alcohol palytoxin. [2] [3] Other dinoflagellates that may cause ciguatera include Prorocentrum spp., Ostreopsis spp., Coolia monotis , Thecadinium spp. and Amphidinium carterae . [4] Predator species near the top of the food chain in tropical and subtropical waters are most likely to cause ciguatera poisoning, although many other species cause occasional outbreaks of toxicity. [5]

Ciguatoxins are a class of toxic polycyclic polyethers found in fish that cause ciguatera.

Maitotoxin chemical compound

Maitotoxin is an extremely potent toxin produced by Gambierdiscus toxicus, a dinoflagellate species. Maitotoxin is so potent that it has been demonstrated that an intraperitoneal injection of 130 ng/kg was lethal in mice. Maitotoxin was named from the ciguateric fish Ctenochaetus striatus—called "maito" in Tahiti—from which maitotoxin was isolated for the first time. It was later shown that maitotoxin is actually produced by the dinoflagellate Gambierdiscus toxicus.

Fatty alcohols (or long-chain alcohols) are usually high-molecular-weight, straight-chain primary alcohols, but can also range from as few as 4–6 carbons to as many as 22–26, derived from natural fats and oils. The precise chain length varies with the source. Some commercially important fatty alcohols are lauryl, stearyl, and oleyl alcohols. They are colourless oily liquids (for smaller carbon numbers) or waxy solids, although impure samples may appear yellow. Fatty alcohols usually have an even number of carbon atoms and a single alcohol group (–OH) attached to the terminal carbon. Some are unsaturated and some are branched. They are widely used in industry. As with fatty acids, they are often referred to generically by the number of carbon atoms in the molecule, such as "a C12 alcohol", that is an alcohol having 12 carbons, for example dodecanol.

Ciguatoxin is odourless, tasteless and cannot be removed by conventional cooking. [6] [7]

Cooking art of preparing food for consumption with the use of heat

Cooking or cookery is the art, technology, science and craft of preparing food for consumption. Cooking techniques and ingredients vary widely across the world, from grilling food over an open fire to using electric stoves, to baking in various types of ovens, reflecting unique environmental, economic, and cultural traditions and trends. The ways or types of cooking also depend on the skill and type of training an individual cook has. Cooking is done both by people in their own dwellings and by professional cooks and chefs in restaurants and other food establishments. Cooking can also occur through chemical reactions without the presence of heat, such as in ceviche, a traditional South American dish where fish is cooked with the acids in lemon or lime juice.

Researchers, such as Ross M. Brown with his "New Religion" theory suggest that ciguatera outbreaks caused by warm climatic conditions in part propelled the migratory voyages of Polynesians between 1000 and 1400AD. [8] [9]

In 2017 an updated review of "Clinical, Epidemiological, Environmental, and Public Health Management" was published and is available at the National Institute of Health website.

Signs and symptoms

Hallmark symptoms of ciguatera in humans include gastrointestinal, cardiovascular, and neurological effects. [10] [11] Gastrointestinal symptoms include nausea, vomiting, and diarrhea, usually followed by neurological symptoms such as headaches, muscle aches, paresthesia, numbness of extremities, mouth and lips, reversal of hot and cold sensation, [12] [13] ataxia, vertigo, and hallucinations. [6] [11] Severe cases of ciguatera can also result in cold allodynia, which is a burning sensation on contact with cold. [10] Neurological symptoms can persist and ciguatera poisoning is occasionally misdiagnosed as multiple sclerosis. [14] Cardiovascular symptoms include bradycardia, tachycardia, hypotension, hypertension, orthostatic tachycardia, exercise intolerance, and rhythm disorders. [15] Death from the condition can occur, but is extremely rare. [16]

Nausea medical symptom or condition

Nausea is an unpleasant, diffuse sensation of unease and discomfort, often perceived as an urge to vomit. While not painful, it can be a debilitating symptom if prolonged, and has been described as placing discomfort on the chest, upper abdomen, or back of the throat.

Vomiting involuntary, forceful expulsion of stomach contents, typically via the mouth

Vomiting is the involuntary, forceful expulsion of the contents of one's stomach through the mouth and sometimes the nose.

Diarrhea Loose or liquid bowel movements

Diarrhea is the condition of having at least three loose, liquid, or watery bowel movements each day. It often lasts for a few days and can result in dehydration due to fluid loss. Signs of dehydration often begin with loss of the normal stretchiness of the skin and irritable behaviour. This can progress to decreased urination, loss of skin color, a fast heart rate, and a decrease in responsiveness as it becomes more severe. Loose but non-watery stools in babies who are exclusively breastfed, however, are normal.

Dyspareunia and other ciguatera symptoms have developed in otherwise healthy males and females following sexual intercourse with partners suffering ciguatera poisoning, signifying that the toxin may be sexually transmitted. [17] Diarrhea and facial rashes have been reported in breastfed infants of poisoned mothers, suggesting that ciguatera toxins migrate into breast milk. [18]

The symptoms can last from weeks to years, and in extreme cases as long as 20 years, often leading to long-term disability. [19] Most people do recover slowly over time. [20]

Detection methods

Folk methods

In Northern Australia, where ciguatera is a common problem, two different folk science methods are widely believed to detect whether fish harbor significant ciguatoxin. The first method is that flies are supposed not to land on contaminated fish. The second is that cats will either refuse to eat or vomit/display symptoms after eating contaminated fish. A third, less common testing method involves putting a silver coin under the scales of the suspect fish. If the coin turns black, according to the theory, it is contaminated.

On Grand Cayman and other islands the locals will test barracuda by placing a piece of the fish on the ground and allowing ants to crawl on it. If the ants do not avoid the flesh and will eat it, then the fish is deemed safe. [ citation needed ]

In Dominican Republic, another common belief is that during months whose names do not include the letter "R" (May through August), it is not recommended to eat certain kinds of fish, because they are more likely to be infected by the ciguatera toxin.

The validity of many of these tests has been scientifically rejected. [21]

Treatment

There is no effective treatment or antidote for ciguatera poisoning. The mainstay of treatment is supportive care. There is some evidence that calcium channel blockers like nifedipine and verapamil are effective in treating some of the symptoms that remain after the initial sickness passes, such as poor circulation and shooting pains through the chest. These symptoms are due to the cramping of arterial walls caused by maitotoxin [11] [22] [23] [24] Ciguatoxin lowers the threshold for opening voltage-gated sodium channels in synapses of the nervous system. Opening a sodium channel causes depolarization, which could sequentially cause paralysis, heart contraction, and changing the senses of hot and cold. Some medications such as amitriptyline may reduce some symptoms, such as fatigue and paresthesia, [25] although benefit does not occur in every case. [26]

Mannitol was once used for poisoning after one study reported symptom reversal. [11] [27] Follow-up studies in animals [28] and case reports in humans [29] also found benefit from mannitol. However, a randomized, double-blind clinical trial found no difference between mannitol and normal saline, [30] and based on this result, mannitol is no longer recommended. [10]

Folk remedies

Leaves of Heliotropium foertherianum (Boraginaceae) – also known as octopus bush – are used in many Pacific islands as a traditional medicine to treat ciguatera fish poisoning. Senescent octopus bush leaves contain rosmarinic acid and derivatives, which are known for their antiviral, antibacterial, antioxidant, and anti-inflammatory properties. [31] Rosmarinic acid may remove the ciguatoxins from their sites of action, as well as being an anti-inflammatory.

An account of ciguatera poisoning from a linguistics researcher living on Malakula island, Vanuatu, indicates the local treatment: "We had to go with what local people told us: avoid salt and any seafood. Eat sugary foods. And they gave us a tea made from the roots of ferns growing on tree trunks. I don't know if any of that helped, but after a few weeks, the symptoms faded away." [32]

Various Caribbean folk and ritualistic treatments originated in Cuba and nearby islands. The most common old-time remedy involves bed rest subsequent to a guanabana juice enema.[ citation needed ] In Puerto Rico, natives drink a tea made from mangrove buttons, purportedly high in B vitamins, to flush the toxic symptoms from the system.[ citation needed ] There has never been a funded study of these treatments. Other folk treatments range from directly porting and bleeding the gastrointestinal tract to "cleansing" the diseased with a dove during a Santería ritual.[ citation needed ]

Epidemiology

The current estimated global incidence annually is 20,000 to 50,000 people, though a large number of cases are believed to go unreported. [33]

Due to the limited habitats of ciguatoxin-producing microorganisms, ciguatera is common only in subtropical and tropical waters, particularly the Pacific and Caribbean, and usually is associated with fish caught in tropical reef waters. [10] Exportation of reef fish, as well as tourism, often account for cases that develop in other regions. [33]

Ciguatoxin is found in over 400 species of reef fish. Avoiding consumption of all reef fish is the only sure way to avoid exposure. [7] Imported fish served in restaurants may contain the toxin and produce illness which often goes unexplained by physicians unfamiliar with the symptoms of a tropical toxin. [7] [34] Ciguatoxin can also occur in farm-raised salmon. [35] Furthermore, species substitution, labeling a reef fish as a non-reef fish at restaurants and retail, can complicate efforts by consumers to avoid ciguatera.

Incidents in the 21st century

History

Ciguatera was first described by one of the surgeon's mates, William Anderson, on the crew of HMS Resolution in 1774. [44]

See also

Footnotes

  1. Diogène, Jorge; Reverté, Laia; Rambla-Alegre, Maria; del Río, Vanessa; de la Iglesia, Pablo; Campàs, Mònica; Palacios, Oscar; Flores, Cintia; Caixach, Josep (2017-08-15). "Identification of ciguatoxins in a shark involved in a fatal food poisoning in the Indian Ocean". Scientific Reports. 7. doi:10.1038/s41598-017-08682-8. ISSN   2045-2322. PMC   5557899 Lock-green.svg. PMID   28811602.
  2. Faust, MA and Gulledge RA. Identifying Harmful Marine Dynoflagellates. Smithsonian Institution, Contributions from the United States National Herbarium. Volume 42:1-144. 2002.
  3. National Office for Harmful Algal Blooms, Ciguatera Fish Poisoning. Woods Hole Oceanographic Institution.
  4. National Office for Harmful Algal Blooms, Ciguatera Fish Poisoning: Causative organisms:. Woods Hole Oceanographic Institution.
  5. FAO Agriculture and Consumer Protection. Ciguatera Fish Poisoning (CFP) In: Marine Biotoxins, Food and Agriculture Organization of the United Nations, Rome, 2004.
  6. 1 2 Swift A, Swift T (1993). "Ciguatera". J. Toxicol. Clin. Toxicol. 31 (1): 1–29. doi:10.3109/15563659309000371. PMID   8433404.
  7. 1 2 3 Schep LJ, Slaughter RJ, Temple WA, Beasley DM (2010). "Ciguatera poisoning: an increasing occurrence in New Zealand". N. Z. Med. J. 123 (1308): 100–102. PMID   20173810.
  8. Rongo, Teina; Bush, Mark; Van Woesik, Robert (2009). "Did ciguatera prompt the late Holocene Polynesian voyages of discovery?". Journal of Biogeography. 36 (8): 1423–32. doi:10.1111/j.1365-2699.2009.02139.x.
  9. Did fish poisoning drive Polynesian colonization of the Pacific? [ full citation needed ]
  10. 1 2 3 4 Isbister G, Kiernan M (2005). "Neurotoxic marine poisoning". The Lancet Neurology. 4 (4): 219–28. doi:10.1016/S1474-4422(05)70041-7. PMID   15778101.
  11. 1 2 3 4 Clark RF, Williams SR, Nordt SP, Manoguerra AS (1999). "A review of selected seafood poisonings". Undersea Hyperb Med. 26 (3): 175–84. PMID   10485519 . Retrieved 2008-08-12.
  12. Patel, Ryan; Brice, Nicola L.; Lewis, Richard J.; Dickenson, Anthony H. (December 2015). "Ionic mechanisms of spinal neuronal cold hypersensitivity in ciguatera". The European Journal of Neuroscience. 42 (11): 3004–3011. doi:10.1111/ejn.13098. ISSN   0953-816X. PMC   4744673 Lock-green.svg. PMID   26454262.
  13. Vetter, Irina; Touska, Filip; Hess, Andreas; Hinsbey, Rachel; Sattler, Simon; Lampert, Angelika; Sergejeva, Marina; Sharov, Anastasia; Collins, Lindon S (2012-10-03). "Ciguatoxins activate specific cold pain pathways to elicit burning pain from cooling". The EMBO Journal. 31 (19): 3795–3808. doi:10.1038/emboj.2012.207. ISSN   0261-4189. PMC   3463840 Lock-green.svg. PMID   22850668.
  14. Ting J, Brown A (2001). "Ciguatera poisoning: a global issue with common management problems". Eur. J. Emerg. Med. 8 (4): 295–300. doi:10.1097/00063110-200112000-00009. PMID   11785597.
  15. Hokama, Y. (1988-01-01). "Ciguatera fish poisoning". Journal of Clinical Laboratory Analysis. 2 (1): 44–50. doi:10.1002/jcla.1860020110. ISSN   1098-2825.
  16. 1 2 "Newlywed bride dies 10 days after wedding from heart attack believed to have been caused by 'contaminated fish'". The Daily Telegraph. Telegraph Media Group. 13 October 2016. Retrieved 14 October 2016.
  17. Lange W, Lipkin K, Yang G (1989). "Can ciguatera be a sexually transmitted disease?". J. Toxicol. Clin. Toxicol. 27 (3): 193–7. doi:10.3109/15563658909038583. PMID   2810444.
  18. Blythe D, de Sylva D (1990). "Mother's milk turns toxic following fish feast". JAMA. 264 (16): 2074. doi:10.1001/jama.264.16.2074b. PMID   2214071.
  19. Gillespie N, Lewis R, Pearn J, Bourke A, Holmes M, Bourke J, Shields W (1986). "Ciguatera in Australia. Occurrence, clinical features, pathophysiology and management". Med. J. Aust. 145 (11–12): 584–90. PMID   2432386.
  20. Pearn J (2001). "Neurology of ciguatera". J. Neurol. Neurosurg. Psychiatry. 70 (1): 4–8. doi:10.1136/jnnp.70.1.4. PMC   1763481 Lock-green.svg. PMID   11118239.
  21. Park, D. L. (1994). "Evaluation of methods for assessing ciguatera toxins in fish". Reviews of Environmental Contamination and Toxicology. 136: 1–20.
  22. Attaway D, Zaborsky O (1993). Marine Biotechnology. p. 8.
  23. Fleming L. "Ciguatera Fish Poisoning | ".External link in |title= (help);
  24. Schlossberg D (1999). Infections of leisure. p. 13. ISBN   3-540-94069-3.
  25. Davis R, Villar L (1986). "Symptomatic improvement with amitriptyline in ciguatera fish poisoning". N. Engl. J. Med. 315 (1): 65. doi:10.1056/NEJM198607033150115. PMID   3713788.
  26. Hampton M, Hampton A (1989). "Ciguatera fish poisoning". J. Am. Acad. Dermatol. 20 (3): 510–1. doi:10.1016/S0190-9622(89)80094-5. PMID   2918120.
  27. Palafox N, Jain L, Pinano A, Gulick T, Williams R, Schatz I (1988). "Successful treatment of ciguatera fish poisoning with intravenous mannitol". JAMA. 259 (18): 2740–2. doi:10.1001/jama.259.18.2740. PMID   3128666.
  28. Mattei C, Molgó J, Marquais M, Vernoux J, Benoit E (1999). "Hyperosmolar D-mannitol reverses the increased membrane excitability and the nodal swelling caused by Caribbean ciguatoxin-1 in single frog myelinated axons". Brain Res. 847 (1): 50–8. doi:10.1016/S0006-8993(99)02032-6. PMID   10564735.
  29. Williamson J (1990). "Ciguatera and mannitol: a successful treatment". Med. J. Aust. 153 (5): 306–7. PMID   2118229.
  30. Schnorf H, Taurarii M, Cundy T (2002). "Ciguatera fish poisoning: a double-blind randomized trial of mannitol therapy". Neurology. 58 (6): 873–80. doi:10.1212/WNL.58.6.873. PMID   11914401.
  31. Rossi, Fanny; Jullian, Valérie; Pawlowiez, Ralph; Kumar-Roiné, Shilpa; Haddad, Mohamed; Darius, H. Taiana; Gaertner-Mazouni, Nabila; Chinain, Mireille; Laurent, Dominique (2012). "Protective effect of Heliotropium foertherianum (Boraginaceae) folk remedy and its active compound, rosmarinic acid, against a Pacific ciguatoxin". Journal of Ethnopharmacology. 143 (1): 33–40. doi:10.1016/j.jep.2012.05.045. PMID   22706150.
  32. Dimock, Laura (June 2010). "Rescue mission for fading tongue". New Zealand Education Review.
  33. 1 2 Marcus, Erin N., Ciguatera fish poisoning , retrieved 6 April 2015
  34. Geller R, Olson K, Senécal P (1991). "Ciguatera fish poisoning in San Francisco, California, caused by imported barracuda". West. J. Med. 155 (6): 639–642. PMC   1003121 Lock-green.svg. PMID   1812639.
  35. DiNubile M, Hokama Y (1995). "The ciguatera poisoning syndrome from farm-raised salmon". Annals of Internal Medicine. 122 (2): 113–114. doi:10.7326/0003-4819-122-2-199501150-00006. PMID   7992985.
  36. Bizarre fish poisoning sparks alarm
  37. "FDA Advises Seafood Processors About Ciguatera Fish Poisoning in the Northern Gulf of Mexico Near the Flower Garden Banks National Marine Sanctuary" (Press release). U.S. Food and Drug Administration. 2008-02-05. Retrieved 2008-02-07.
  38. Centers for Disease Control and Prevention (CDC) (2013). "Ciguatera fish poisoning - New York City, 2010-2011". MMWR. Morbidity and Mortality Weekly Report. 62 (4): 61–5. PMID   23364271.
  39. Cliffe-Jones, Mike "Jules" (April 17, 2012). "Isolated Cases of Ciguatera Poisoning in Lanzarote". Information Lanzarote. Information Lanzarote. Retrieved 31 October 2015.
  40. "Ciguatera poisoning from Spanish Mackerel caught off Scotts Head". ABC News. 2014-03-04. Retrieved 2017-10-16.
  41. "Balsa 85 ID'd as ship in Saint John whose crew was hit by food poisoning". CBC New Brunswick. CBC. CBC. 13 April 2015. Retrieved 31 October 2015.
  42. "Seafarers told no fishing!". The Sea (236). Mission to Seafarers Limited. Jul–Aug 2015.
  43. "Love your fish? Then know about seafood poisoning too". Times of India. 4 October 2016. Retrieved 14 October 2016.
  44. Sanders, Lisa (April 5, 2010). "Fish Tale". New York Times . Retrieved 2010-04-10. The illness was first described in 1774 by a surgeon's mate on the crew of Captain Cook's South Pacific exploration aboard the HMS Resolution. The crewman, John Anderson, documented the symptoms described by several shipmates who had eaten a large fish caught in the tropical waters. (The New York Times incorrectly gives William Anderson's first name as John.)

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References