Ciguatera fish poisoning

OBJECTIVE: To review history, biology, and medical aspects associated with fish and shellfish poisoning.

DATA SOURCES: Current literature, various Web sites, and Halstead's Volume II of Poisonous and Venomous Marine Animals.

STUDY SELECTION: Determined by author.

DATA SELECTION: Determined by author.

DATA SYNTHESIS: Fish and shellfish poisoning occur through the natural event of the food chain. Fish and shellfish consume algae that contain toxin-producing dinoflagellates. As a result they become contaminated and the toxin is concentrated as it moves up the food chain. Fish and shellfish can tolerate high levels of toxins, thereby appearing healthy while posing a significant danger to man. The toxin cannot be detected by sight, smell, or taste and is not destroyed by cooking or freezing. Thus man becomes an unsuspecting victim. There are several types of poisoning that occur through fish and shellfish consumption. They are ciguatera and scombroid fish poisoning; and paralytic, diarrheic, neurotoxic, and amnesic shellfish poisoning. A different toxin produces each of these poisonings; however, sources and symptoms may be similar among these poisonings making them difficult to diagnose. These intoxications can vary in severity from mild to fatal depending on the type and amount of toxin ingested. Age and underlying illnesses may also contribute to the outcome of these poisonings.

CONCLUSION: Though people are aware of health warnings and may think they are important, it is human nature to think that "this could not possibly happen to me". Therefore, they fail to make the necessary changes required to reduce the incidence of fish and shellfish poisoning.

ABBREVIATIONS: ASP = amnesic shellfish poisoning; DSP = diarrheic shellfish poisoning; NSP = neurotoxic shellfish poisoning; PSP = paralytic shellfish poisoning.

INDEX TERMS: Fish poisoning; seafood borne illnesses; shellfish toxins.

Clin Lab Sci 1998;11(5):309

The world's seafood supply has remained stable over the last few years. In 1994 it reached a record level of 110 million metric tons. In 1995 consumers in the United States spent an estimated $38.2 billion on seafood consumption, $26.2 billion in food service establishments, and $12 billion in retail sales for home consumption. In 1996 the Commerce Department's National Oceanic and Atmospheric Administration announced that seafood consumption had remained steady with Americans consuming 3.90 billion pounds of domestic and imported fish or 14.8 pounds per person.1

In view of this seafood consumption and the fact that approximately 50% of it is imported from around the world, the safety of our seafood supply should be a major concern to us all. Just how safe is our seafood supply and what precautions should we take to decrease our risk of fish and shellfish poisoning?

The poisonous effects of fish and shellfish were well known in ancient times and can be found recorded throughout history.2 In the United States, due to strong control programs, seafood can be considered relatively safe. Prevention of poisonous effects, however, is not so easily managed. Contaminated fish or shellfish appear healthy and the toxins they contain are not detected by taste. Therefore, individual cases and sporadic outbreaks still occur.3

Biological events such as red tides or an increased mortality of sandeels and birds, especially shags, are thought to precede human outbreaks of seafood poisoning.4 Fish and shellfish poisoning occur through the natural event of the food chain. Plankton is a term used to describe a variety of marine and freshwater organisms that drift on the surface of water. These organisms provide food for marine life. A component of plankton is the dinoflagellates.

Dinoflagellates are unicellular aquatic organisms in the order Dinoflagellida. There are several thousand species and they exhibit traits of both plant and animal. These marine creatures are capable of reproducing in enormous numbers, called a bloom, in warm shallow water. This population explosion can result in mass mortality for fishes and other marine life. Certain species of dinoflagellates in the genera Gymnodinium and Gonyaulax produce a strong nerve toxin. When they are responsible for the bloom called red tide the consequences can be wide spread and severe.4 Fish and shellfish (bivalue molluscs) feed on these toxin-producing dinoflagellates and in turn become contaminated. As larger fish feed on smaller contaminated fish the toxin becomes concentrated in the viscera of the larger fish with each feeding event. Shellfish feed continuously by filtering minute particles from large volumes of water. As this process continues the toxins become concentrated in the viscera of the molluscs. Bivalve molluscs can tolerate high levels of toxin thus posing the greatest danger to man while still appearing healthy.

Some of the most common fish poisonings are ciguatera and scombroid fish poisoning, and paralytic (PSP), diarrheic (DSP), neurotoxic (NSP) and amnesic shellfish poisoning (ASP). Characteristics associated with these poisoning are summarized in Table 1. PSP, DSP, and ASP occur through contaminated shellfish that are acquired primarily from the northeast and northwest coastal regions of the United States and from imported shellfish that come from similar climates. NSP is acquired through contaminated shellfish from the southeastern United States. ASP has been identified as a problem in the viscera of Dungeness crab and anchovies along the west coast of the United States.5 Though these poisonings most often occur abroad, we are still susceptible due to our substantial importation of seafood and the dinoflagellates which inhabit the coastal waters of the United States (Figure 1). In 1992, 19 outbreaks involving 205 individual cases of fish and shellfish poisoning were reported in the United States.5 The true incidence of fish and shellfish poisoning may remain forever obscure for two important reasons. The first is that it is not well recognized clinically, and second, it may go unreported when it is of short duration. In this article we will review the history, biology, and medical aspects of fish and shellfish poisoning. CIGUATERA

Ciguatera is a form of human poisoning caused by the consumption of subtropical and tropical marine finfish that have naturally accumulated toxins through their diet. Approximately 50,000 cases occur annually world-wide.3 Ciguatera poisoning has been documented far back in ancient Greece (ca. 800 B.C.) when the Greeks avoided eating certain marine fish because they believed them to be harmful to the body. Alexander the Great (356-323 B.C.) is said to have forbidden his soldiers to eat fish during conquests because he believed some species were dangerous to eat causing skin disorders and other maladies. One of the earliest reported outbreaks occurred during the exploration of the Spanish explorer Pedro Fernandez Quiros while in New Hebrides in 1606. He describes his crew of being in great danger of their lives and all the soldiers expected to die.2 Between 1971 and 1981, there were 94 outbreaks which affected 418 people reported in the United States. An outbreak of ciguatera occurred in Puerto Rico between April and June 1981 affecting 49 people including two fatalities. In Palm Beach Florida in May 1988 there were over 100 human ciguatera poisonings with no fatalities. In Florida in 1991, the Department of Health and Rehabilitative Services investigated an outbreak involving eleven people who suffered ciguatera poisoning including three individuals who required hospitalization. Isolated cases have occurred with some regularity along the eastern coast of the United States as well as in Hawaii, the Virgin Islands, and Puerto Rico.3,6,7

Ciguatera is relatively limited in the United States however, it still ranks among the four top annually reported seafoodborne illnesses.8 The primary areas of ciguatera poisoning are Hawaii, Guam, and other South Pacific states that consume many fish from tropical sources. The fish involved in ciguatera poisoning are diverse in nature covering a wide phylogenetic range. They vary in body shape and biological characteristics.2 Thus far no species of fish has been reported to be universally poisonous all the time thereby validating the food chain theory. Some of the fish associated with this poisoning include groupers, barracudas, snappers, amberjacks and other jacks, mackerel, moray eels, and triggerfish.3

Ciguatera toxin is a heat-resistant, acid stable collection of toxic substances produced by certain species of dinoflagellate such as Gambierdiscus toxicus, Prorocentrum mexicanum, and Ostreopsis lenticulris.6 These organisms are usually found in warm tropical waters such as the Caribbean or Indo-Pacific regions. As marine life feeds on these toxin producing dinoflagelletes, they in turn harbor the toxin. The toxin is concentrated as it moves up the food chain without exhibiting any ill effects in marine life. Freezing or cooking does not destroy the toxin and when man ingests the contaminated food he develops ciguatera poisoning.

Clinical manifestations of the disease in humans involve gastrointestinal, neurological, and cardiovascular disorders. All humans are believed to be susceptible to ciguatera toxins. Initial signs of ciguatera poisoning typically occur within 24 hours of consumption of contaminated fish, though some have been reported to occur anywhere between one to six hours.6,9 Initial symptoms include perioral numbness and tingling which may spread to the extremities.3 Gastrointestinal symptoms include nausea, vomiting, and diarrhea. Neurological symptoms include myalgia, headache, and vertigo. Cardiovascular signs include arrhythmia, bradycardia, tachycardia, or reduced blood pressure. Ciguatera poisoning is usually self-limiting with symptoms subsiding several days after onset. The incidence of death from ciguatera poisoning due to cardiac or respiratory failure is low, however, complications vary with the amount of toxin consumed and the age and underlying medical condition of the patient.

Clinical testing for ciguatera poisoning is not presently available. Diagnosis is based on clinical presentation and recent history. Treatment consists of trying to eliminate the poison from the body and providing supportive therapy. Mannitol IV, tocainide, and amitriptyline have also been used with some success in the treatment of ciguatera poisoning.9

Suspected cases of ciguatera should be reported to your local public health authorities and suspected food should be quarantined (tightly packed and frozen) for testing.8 A method for detecting ciguatera toxins from fish is available. It consists of a tedious extraction process and the use of a mouse bioassay. A simplified EIA method is under evaluation.3

Though there are many native rituals for detecting poisonous fish none can be relied upon as a means of prevention. Some things to keep in mind however include: 1) never eat the viscera of the tropical marine fish, i.e. liver, gonads, intestines, etc.; 2) usually large reef fishes such as snappers, barracuda, or jack should not be eaten; 3) ordinary cooking procedures to do not render a toxic fish safe to eat; and 4) tropical moray eels should never be eaten. Some are so toxic they cause convulsions and a quick death.

SCOMBROTOXIN

Scombrotoxin poisoning, also called histamine poisoning, is the result of consuming improperly stored fish. One of the earliest accounts of scombrotoxic poisoning occurred in 1799 when the ability of "herring" to produce an "irritation that resulted in the efflorescence of the skin" was noted. Since 1815 numerous accounts of scombrotoxic poisoning have been recorded in the literature.2 Many observers noted that the majority of outbreaks could be traced to improperly stored or preserved fish. Recent outbreaks include those in 1970 when 40 children in a school lunch program became ill from imported canned tuna and in 1973 when 200 individuals became ill after consuming domestic tuna.3 From 1973 to 1981 there were 178 outbreaks of scombrotoxin poisoning that affected 1096 individuals. From 1977 to 1981 scombrotoxin poisoning represented 37% of all seafoodborne illnesses.6

Scombroid fish are characterized by their adaptation for swift locomotion, having a sharp anterior profile and a slender tail with a wide forked caudal. They have a series of detached fins behind the dorsal fin and on the under surface, a characteristic that differentiates them from other fish.2 Fish associated with scombrotoxic poisoning include: tuna, mahi mahi, bluefish, sardines, mackerel, amberjack, and abalone.3

Scombrotoxin formation is the product of the combined effects of histamine, other vasoactive amines, and possibly other toxins produced by decaying fish. Histidine, found in the tissues of scombroid fish, is decarboxylated by bacteria to form histamine. High levels of histamine are produced when the fish is improperly stored or preserved at elevated temperatures. The products of decay and the combination of elevated histamine levels result in the formation of scombrotoxin.2,3

Clinical manifestations of the disease occur immediately or within 30 minutes of consuming contaminated fish. All humans are susceptible to scombrotoxic poisoning. Symptoms of the poisoning include: tingling or burning of the mouth, rash on upper body, drop in blood pressure, nausea, vomiting, and diarrhea. Though the duration of the illness is short, usually three hours, it can last for several days and have a severe effect on the elderly.3

Clinical testing for scombrotoxin is not presently available. Diagnosis is based on clinical symptoms, time of onset, and effect of treatment with antihistamine. A method has been developed by the FDA to detect histamine in seafood using alcohol extractions and fluorescence spectroscopy.3

Treatment of the poisoning includes the immediate evacuation of the stomach and the use of epinephrine to counteract all symptoms. If the toxin has been absorbed, epinephrine, cortisone, or intravenous benadryl may be used to counteract the effects of the poisoning. Scombroid poisoning is one of the most common forms of fish poisonings in the United States. In spite of this fact its true incidence is unknown due to under reporting. Many cases of scombroid poisoning may go unreported due to lack of required reporting, uninformed medical personnel, or the confusion of symptoms with other illnesses.

Preventative measures include rapid chilling of fish immediately after death. The internal temperature of the fish should be brought to 50 deg F (10 deg C) or below within six hours after death.10 Toxic scombroid fish cannot always be detected by appearance, however. If a sharp or peppery taste is noted, the fish should be discarded.

SHELLFISH POISONING

All shellfish (filter feeding molluscs) can become poisonous by consuming toxin-producing algae (dinoflagellates, in most cases). The harmful alga is consumed by shellfish in which it concentrates and is sometimes metabolized.11 Shellfish are able to tolerate high concentrations of these toxins and therefore exhibit no ill effects; man on the other hand is not so lucky. There have been several outbreaks and deaths associated with shellfish poisoning. There are four types of shellfish poisoning that may be acquired through the consumption of contaminated shellfish; these are paralytic, diarrheic, neurotoxic, and amnesic shellfish poisoning. Each of these intoxications has characteristic symptoms and clinical course, yet they share many similarities making them difficult to diagnose. Simultaneous occurrence of diarrheic and paralytic shellfish poisoning has been reported to occur.12 Paralytic shellfish poisoning appears to be the most serious of these four poisonings and the cause of several outbreaks and deaths.13,14,15

PARALYTIC SHELLFISH POISONING

Historical descriptions of paralytic shellfish poisoning (PSP) associated with red tides can be traced to the 18th century.16 From 1971 to 1977 there were 12 outbreaks that affected 68 people reported in the United States.6 In 1987 a major outbreak occurred in Guatemala following the ingestion of clam soup. The outbreak resulted in 187 cases with 26 deaths due to PSP.15 In 1991 five cases of PSP were reported following the ingestion of contaminated oysters in Nagato, Japan.17 Due to strong control programs relatively few outbreaks occur in the United States.

Alexandrium spp., Gymnodinium catenatum, and Pyrodinium bahamense are some of the dinoflagellate species that are responsible for producing the toxins associated with PSP Paralytic shellfish poisoning is caused by a combination of any of 20 known toxins produced by dinoflagellates or by toxins that are created by chemical or enzymatic conversion within the shellfish.11 Although saxitoxin accounts for only 5% to 10% of total toxin components, it is a major contributor to PSP and one of the most potent toxins known.18 It is a heat resistant, acid stable toxin that can have a widespread effect on the cardiovascular and respiratory systems.19 It is also known to block the sodium channels in skeletal and nerve muscles resulting in neurological symptoms and respiratory paralysis.6 Necropsy findings of ten subjects who died of PSP between March 1991 and January 1992 demonstrate the widespread effects of this toxin. All subjects were found to have extensive swelling and edema of the brain, lungs, liver, and spleen. Airway obstruction and digestive and respiratory mucosal congestion and friability were also noted.13 PSP is usually associated with mussels, clams, cockles, and scallops; however, it has also been found in starfish and Bangladeshi freshwater puffers.3,20,21

Clinical manifestations of PSP are dependent upon the toxins present, their concentrations, and the amount of contaminated seafood ingested. All humans are susceptible. Cases often occur in tourists or others who are not native to the area where toxic fish are harvested. Symptoms occur rapidly, within 30 minutes to two hours after ingestion of the contaminated seafood. In severe cases respiratory paralysis is common. Death may occur without respiratory support.3 PSP effects are predominantly neurological. Symptoms include tingling and burning of the lips and mouth, drowsiness, incoherent speech, and respiratory paralysis.

Diagnosis may prove difficult due to other paralytic illnesses such as botulism, fisher syndrome, myasthenia gravis, and periodic paralysis.17 There is no clinical method for detecting PSP; therefore diagnosis must be based solely on clinical presentation and recent history. The frequency of PSP is unavailable due to frequent misdiagnosis and infrequent reporting.

The toxin is undetectable by sight or smell and is not destroyed by normal cooking, freezing, or smoking. The best form of prevention is to detect the toxin before the shellfish reach market. The mouse bioassay has been historically used for this purpose. There are a number of disadvantages to this method and alternate methods are being tested.6

DIARRHEIC SHELLFISH POISONING

Diarrheic shellfish (DSP) poisoning has been recognized in Japan, Europe, and Eastern Canada. DSP is caused by the dinoflagellate species of Dinophysis. Eight lipid soluble toxins are known to be involved in the production of DSP These toxins consists of acidic and neutral toxins which are okadaic acid, dinophysistoxin 1 and 2, and pectenotoxin 1-5 respectively. DSP has been associated with mussels, oysters, and scallops.

Clinical manifestations are gastrointestinal in nature with nausea, vomiting, diarrhea, and abdominal pain accompanied by fever, chills, and headache. All humans are susceptible with symptoms beginning anywhere from 30 minutes to 15 hours, depending on the degree of intoxication. No known fatalities have occurred and recovery is usually expected after three days.6

There is no clinical method of detecting DSP. Diagnosis is based on symptoms and recent history. DSP has not been definitely documented in the United States though there have reports of cases suggestive of DSP The causative toxin cannot be detected by usual means therefore the best means of prevention is by detection of the toxins before the seafood reaches market. Several assays are available for this purpose.6

NEUROTOXIC SHELLFISH POISONING

Outbreaks of neurotoxic shellfish poisoning (NSP) are sporadic and continuous along the Gulf coast of Florida. NSP has also been reported in Texas and North Carolina.

NSP is caused by the dinoflagellate Pytchodiscus brevis (formally Gymnodinium breve).3 P brevis produces three known toxins: brevetoxin B, C, and GB-3. NSP has been associated only with oysters and clams. However it should be assumed that all filter feeder molluscs are capable of producing NSP.6

Clinical manifestations are similar to that of ciguatera with gastrointestinal and neurological involvement. All humans are susceptible; symptoms usually occur within 15 minutes to three hours. Symptoms usually include: tingling of face and other parts of the body, cold to hot sensory reversal, diarrhea, dizziness, bradycardia, dilation of the pupils, and a feeling of inebriation. Full recovery is expected within 48 hours.6

Diagnosis is based on clinical presentation and prevention is dependent on early detection of contaminated fish supply.

AMNESIC SHELLFISH POISONING

Amnesic shellfish poisoning (ASP)first came to the attention of the public health authorities in 1987 when 156 cases of intoxication due to the ingestion of contaminated blue mussels occurred. The outbreak resulted in 22 individuals requiring hospitalization and the death of three elderly people.3

The diatom Nitzschia pungens causes ASP. It is commonly found in coastal water alga of the Atlantic, Pacific, and Indian Oceans. The toxin produced by this organism is domoic acid. Thus far only mussels have been implicated, however, it should be assumed that all shellfish are capable of producing this intoxication in man.3,6

Clinical manifestations include gastrointestinal and neurological disorders. All humans are susceptible. Gastrointestinal symptoms usually develop within 24 hours and include: nausea, vomiting, diarrhea, and abdominal cramping. In severe cases neurological symptoms appear within 48 hours. These symptoms include: dizziness, headache, seizures, disorientation, short-term memory loss, respiratory difficulty, and coma.zz Toxicosis can be particularly severe in elderly patients. To date all fatalities have involved this population group.3

There are no clinical tests to detect ASP; therefore diagnosis is based on clinical presentation. Blooms that occurred in 1987 and 1988 in Canada resulted in approximately 130 cases, which included two fatalities.6

Detection and prevention of ASP is based upon detection of domoic acid in seafood before it reaches market. Domoic acid can be detected using high performance liquid chromatography.

CONCLUSION

There are many toxins involved in fish and shellfish poisoning. These toxins arise as a natural occurring phenomenon in the food chain of marine life. Man is essentially an accidental victim. The degree of his intoxication with these poisonings is largely dependent on the concentration and amount of the toxin ingested. The toxins produced are heat stable and not detected by the usual senses of sight, smell, or taste; therefore, it is essential to follow any and all recommendations associated with the safe and proper storage of seafood. Though it is hopeful that public awareness would decrease the incidence of fish and shellfish poisoning it is highly unlikely. This has been demonstrated by a study of the Santa Monica Bay area that involved 930 individuals who were aware of contaminated seafood warnings. Though all thought the warnings were important, only 50% altered their seafood consumption in an attempt to prevent illness.23 Due to the habits of man, the difficulty of diagnosis, and the lack of proper reporting, the incidence of fish and shellfish poisoning may forever remain obscure.

REFERENCES

1. National Oceanic and Atmospheric Administration, "Get a Line" on the Numbers about Seafood. http://www.nfi.org/sfdnumbers.html 2. Halstead BW. Poisonous and Venomous Marine Animals of the World, United States Government Printing Office, 1967. 3. U.S. Food and Drug Administration, Foodborne Pathogenic Microorganisms and Natural Toxins Handbook, http://vm.cfsan.fda.gov/mow/ 4. Clark RB. Biological causes and effects of paralytic shellfish poisoning. Lancet 1968;2(7571):770-2.

5. FDA Fish and Fishery Products Hazards and Controls Guide, SpeciesRelated Hazards and Control #3 Hazard: Natural Toxins. http:// www. foodsafety.org/sf/sf100.htm OO.htm

6. National Oceanic and Atmospheric Administration, Seafood Safety. http://www-seafood.ucdavis.edu/Pubs/safety1 .htm 7. Centers for Disease Control and Prevention, Ciguatera Fish Poisoning-Florida, 1991, MMWR 1993;Jun 4:42(21). 8. Florida Sea Grant Program, Ciguatera. http://www.foodsafety.org/sf/ sf049.htm

9. Novak SM. Foodborne illness-chemical fish and shellfish poisoning, Clin Microbiol Newsletter; Feb 1998:Vol 20;No.3. 10. National Oceanic and Atmospheric Administration, Scombrotoxin (Histamine) Formation. http//www.seafood.ucdavis.edu/haccp/compendium/chemical/scombroi.htm

11. Shimizu, Y, Yoshioka M. Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. Sci 1981;212(4494):547-9. 12. Gago-Martinez A, Rodriguez-Vazquez JA, and others, Simultaneous occurrence of diarrheic and paralytic shellfish poisoning toxins in Spanish mussels in 1993. Nat Toxins 1996;4(2):72-9. 13. Montebruno D. Poisoning by the consumption of shellfish contaminated with paralytic venom in the XII Region, Chile. Anatomopathological study. Rev Med Chil 1993;121(1):94-7.

14. Tan CT, Lee EJ. Paralytic shellfish poisoning in Singapore. Ann Acad Med Singapore 1986;15(1):77-9.

15. Rodrigue DC, Etzel RA, Hall S, and others. Lethal paralytic shellfish poisoning in Guatemala. Am J Trop Med Hyg 1990;42(3):267-71. 16. Fortuine R Paralytic shellfish poisoning in the North Pacific: Two historical accounts and implications for today, Alaska Med 17: 71-5. 17. Negoro K, Morimatsu M. Clinical analysis of paralytic shellfish poisoning following ingestion of oysters. Rinsho Shinkeigaku 1993;33(2):207-9. 18. Anderson DM, Sullivan JJ, Reguera B. Paralytic shellfish poisoning in northwest Spain: the toxicity of the dinoflagellate Gymnodinium catenatum. Toxicol 1989;27(6):665-674.

19. Evans MH. Cause of death in experimental paralytic shellfish poisoning (PSP). Br J Exp Pathol 1965;46(3):245-53. 20. Asakawa M, Nishimura F, Miyazawa K, and others. Occurrence of paralytic shellfish poison in the starfish, Asterias amurenis in Kure Bay, Hiroshima Prefecture, Japan, Toxicol 1997;35(7):1081-7. 21. Zaman L, Arakawa O, Shimosu A, and others. Occurrence of paralytic shellfish poison in Bangladeshi freshwater puffers, Toxicol 1997;35(3):423-31.

22. National Office for Marine Biotoxins and Harmful Algal Blooms. The Harmful Algae, http://www.redtide.whoi.edu/hab/illness/illness.html 23. Allen MJ. Seafood Consumption Habits of Recreational Anglers in Santa Monica Bay, http://www.sccwrp.org/pubs/annrpt/artO6.htm

Sherry Trevino MPH, CLS(NCA) is the Core I Microbiology Supervisor at Wilford Hall Medical Center, Lackland AFB, TX

Address for correspondence: Sherry Trevino, Microbiology Department (MTLLM), Wi ford Hall Medical Center 2200 Bergquist Drive, Ste 1. Lackland AFB TX 78236

Connie R Mahon is the Focus: Foodborne Illness guest editor. Focus Continuing Education Credit: see pages 315 to 317for learning objectives, test questions, and application form.

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