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Journal o{Food Protection Vol. 40, No. 10, Pages 712-717 (October, 1977) Copyright r,, 1977, International Association of Milk, Food, and Environmental Sanitarians

Fish, Shellfish, and Human Health

LARRY D. BROWNl and C. RICHARD DORN2

Webb Air Force Base, Texas 79720; and Department of Veterinary Preventive Medicine, College of Veterinary Medicine, Ohio State University, Columbus, Ohio 43210 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/40/10/712/1649611/0362-028x-40_10_712.pdf by guest on 27 September 2021

(Received for publication March 14, 1977)

ABSTRACT associated with envenomization, aflatoxicosis, food Food borne illness may result in human beings from ingestion of allergy reactions, and deficiency disease. Each food products containing bacterial or parasitic pathogens. The of these four general categories of fish-associated bacterial pathogens include Salmonella, Shigella, Streptococcus, illnesses will be presented in greater detail. Leptospira, Clostridium, Staphylococcus, Mycobacterium, Erysipelo­ trix, Francisella. and Vibrio species. Parasitic illness may result from Fishborne infections and intoxicants (bacterial) Diphllobothrium latum, Clonorchis sinesis, Opisthorchis Jelineus, Most of the fish-related foodborne illnesses in the Heterophyes heterophyes, Paragoniums westermani and Anisakis sp. United States are due to Salmonella, Staphylococcus, Fishborne intoxication include Ciguatera, Scombroid, and Puffer icthyosarcotoxins, mercury, nitrite-nitrate, pesticides, radionclides, and Streptococcus, Clostridium botulinum, and fish the toxm of Haff disease. Infections with Vibrio parahaemoiyticus, (2). Raw whole fish taken from waters not polluted by Salmonella typhi, and infectious hepatitis virus are associated with sewage rarely contain bacteria pathogenic for man, other shellfish. Toxic substances found in shellfish include paralytic shellfish than C. botulinum and Vibrio parahaemolyticus (18). poisor>, mercury, pesticides, and toxic hydrocarbons. Prevention offish­ Spoilage bacteria, however, normally abound in surface and shellfish-associated illnesses of man is possible by: (a) using only fish and shellfish from unpolluted waters, (b) use of proper slime and in gut contents. Fish may also be passive refrigeration facilities, (c) practicing strict sanitation in processing carriers of human pathogens in water environments plants and storage facilities, (d) assuring foodhandlers are free of polluted by human sewage or diseased animals (20). A disease, (e) cooking thoroughly all fish and shellfish before eating, and fish can retain in its digestive tract or on its integument \!! not handling aquatic foods when one has wounds or abrasions. many human pathogens (e.g. Escherichia coli, Salmonella sp., Shigella sp., Staphylococcus sp., and C This review has been divided into two parts: (a) fish botulinum) without becoming ilL Fish may also be and human health and (b) shellfish and human health. carriers of water-borne pathogenic bacteria of several The reader is also referred to reviews of aquatic animal genera: Erysipelas, Leptospira, Pasteurella, Aeromonas, biology, production, and management (10,17,35), patho­ Pseudomonas, Vibrio, and Mycobacterium. Aeromonas, logy (32), (16), hygiene (3,24,26), and aquatic Pseudomonas, Vibrio, Mycobacterium, and Pasteurella food preservation (6.7.12,28,36). Fishborne and shellfish­ species have been reported to cause active disease in fish. borne illnesses are also described in several monographs Salmonella, Shigella, Streptococcus, and Staphy­ of zoonotic disease (5, 11.13,19,31). lococcus. In Salmonella and Shigella food , fish may be contaminated by polluted water or during FISH AND HUMAN HEALTH processing. The reported Staphylococcus and Strepto­ Fish and fish products have been associated with coccus food borne illnesses are usually due to contamina­ several human illnesses (20). It has long been known that tion of fish on a fishing vessel or in a processing plant. fish may be a vehicleforfoodborne bacterial and parasitic Fish decompose rapidly enzymatically in comparison infections in human beings. Foodborne intoxications to red meat and poultry. Fish also deteriorate much are another important group of fish-associated human faster than other food products. This has been attributed illnesses. The third way fish can affect man's health is by to the greater free amino acid content of fish tissue. injury through physical attacks or accidents. A fourth Bacteria found on or in freshly caught fish do not usually miscellaneous category includes the human illnesses present a human health hazard, if fish are promptly

1 Webb Air Force Base. chilled on the boat and processed properly in the plant. If 'Ohio State Uni•·ersity. allowed to remain on the deck of the boat or if not FISH, SHELLFISH, AND HUMAN HEALTH 713

refrigerated, fish may become highly contaminated with waters, (b) use proper refrigeration facilities, (c) practice organisms or bacterial toxins. Seagulls and other strict sanitation in processing plants and storage waterfowl flying over or perching on boat masts and piers facilities, (d) foodhandlers should be disease-free, (e) have been incriminated as a source of Salmonella always cook fish well and never consume raw fish, and (j) contamination offish product. don't handle fish if you have wounds or abrasions. Clostridium. Botulism is produced by the Fishborne infections (parasitic) bacterium, C. botulinum. As a bacterial foodborne intoxication, botulism occurs at a relatively low Fish, like other animals, are often parasitized. Internal frequency, but when it does occur, it is often fatal. parasites may be found in the gastrointestional tract or Between the years 1899-1967, there were 1,669 cases of their larva or cysts may be found in muscle tissue or botulism in the U.S. with 948 deaths, or a case fatality subcutaneously just under the skin. The broad fish rate of 56.8% (8). During the 68-year period covered, fish tapeworm, Diphllobothrium latum, is the only fish were involved in 23% of the 640 reported outbreaks. parasite of public health importance in the U.S. Type E, C. botulinum organisms are widespread in However, a few other parasitic infections of fish have Downloaded from http://meridian.allenpress.com/jfp/article-pdf/40/10/712/1649611/0362-028x-40_10_712.pdf by guest on 27 September 2021 marine and aquatic environments. Fish harvested from been reported in humans in this country who have eaten most aquatic environment may be contaminated. imported fish or who had recently visited a foreign Vacuum-packed fish may present a potential hazard country. because the presence of a vacuum tends to encourage The definitive host of D. latum is man. It may also growth of anaerobic bacteria like C. botulinum. Smoke infect dogs and cats. Proglottids containing operculated deposited on the surface of smoked fish lowers the eggs, leave the body with the feces. oxidation-reduction potential and this can account for The first stage larvae, or coracidium, develop within development of the C. botulinum toxins in smoked the eggs. These larvae have dense cilia, and they are vacuum-packed fish. active swimmers when released from the eggs in the Vibrio. In the last few years several Vibrio parahae­ water. Each coracidium contains an oncosphere. They molyticus borne illnesses have been reported. This are eaten by a copepod in which the procercoid stage organism has been associated with more shellfish-related develops. Then pike, perch, turbot, salmon, trout, foodborne outbreaks than fish-related outbreaks, and it grayling, or eel eat the infected crustaceans. The will be discussed more thoroughly in the shellfish section. procercoid migrates through the intestinal wall of the Mycobacterium. Mycobacterium ballnei and Myco­ fish and matures into a pleurocercoid in the muscle. bacterium fortuitum are pathogens of fish. They have Man's ingestion of raw or poorly cooked fresh-water fish also been isolated from human lesions (JO). M. ballnei completes the cycle. The tapeworm may cause severe causes chronic granulomatous lesions of man's extremi­ anemia in man. D. latum presently occurs throughout ties (21). The disease is usually traced to swimming pools, much of the great Lakes Region of North America. aquaria, or tropical fish tanks. Few cases have been Prevention of diphyllobothriasis is dependent upon recorded. This is probably because the optimal growth abstinence from raw or poorly cooked fish. Researchers temperature for this organism is 25 C and the lethal have shown that freezing or heating to an internal temperature is 37 C. temperature of 56 C will destroy the pleurocercoids. Erysipelothix. Erysipelothix rhusiopathiae causes In East Asia the cat liver fluke (Opisthorchis felineus) swine and avian erysipelas and human erysipeloid. It is and the Chinese liver fluke (Clonorchis sinensis) are commonly found in the slime or mucus covering fresh frequently diagnosed in humans. Heterophyes hetero­ and salt water fish. This organism has no apparent effect phyes, a fluke of fish, and Paragonimus westermani, a on fish, but it causes a severe cutaneous infection in fluke of crab, are also transmissible to man. wounds or abrasions of fish handlers. This condition is Herring-worm disease has been reported in human commonly called "fish rose" and is considered an beings in the Netherlands (37). The etiologic agent has occupational disease. been identified as the larva of Anisakis sp. which usually Leptospirosis. Another occupational disease of fish inhabits the viscera of small fish that serve as workers in certain parts of the world is "Weil's disease" intermediate hosts. Human infections were contracted by or leptospirosis (JO). This is a severe febrile illness due to eating raw or improperly cured herring. The syndrome in Leptospira icterohemo"hagiae and it is contracted in man was characterized by acute abdominal pain and the same way as "fish rose." peritoneal irritation. The parasite apparently penetrates Francisella. The causative agent of tularemia, Fran­ the intestinal wall and migrates in the abdominal cavity. cisella tularensis, can infect fish. Contact with catfish has In the midwest, black and white parasitic grubs, been reported as a cause of human infection. Punctures commonly referred to as "black spot" and "white spot," by the contaminated spines of the fish served to inoculate are often found encysted in the muscle of freshwater bass handlers with the organism. and perch (J4). They are the larval stage of flukes that have their adult stage in fisheating . Based on Prevention current knowledge, these larvae present no public health Prevention of bacterial fishborne illness in man is hazard, however, it should be recommended that fish be dependent upon the following: (a) fish in unpolluted thoroughly cooked. 714 BROWN AND DORN

Otherfishbome intoxications In the spring of 1970, fish in Lake St. Clair, a small As well as being carriers of bacterial pathogens, fish lake adjacent to Detroit, Michigan, had mercury levels may contain other which have caused or have as high as 7 ppm almost 14 times that of the FDA's the potential for causing food borne disease in man. These guideline of 0.5 ppm. Ontario and Michigan subse­ include Ciguatera, Scombroid, and Puffer ichthyosarco­ quently closed the lake to commercial fishing. In toxins; mercury; nitrites-nitrates; pesticides; radio­ December 1970, the FDA recalled from grocers' shelves nuclides; and the toxic substance causing Haff disease. one million cans of tuna that had mercury levels above Ciguatera-Scombroid-Puffer. Ciguatera and Scorn­ FDA guidelines of 0.5 ppm. Danger of mercury braid are two different types of fish borne intoxications in poisoning in fish generally increases with the size of the man. These fish muscle toxins, or ichthyosarcotoxins, fish; swordfish are usually larger than 100 lb. In May, have been recognized for over 200 years. 1971, FDA issued a notice recommending that the public Ciguatera toxin has been found in more than 300 not eat swordfish. By September 1970, 18 states had

species of marine . Sea bass, jack, barracuda, closed either a major river or lake to fishing because of Downloaded from http://meridian.allenpress.com/jfp/article-pdf/40/10/712/1649611/0362-028x-40_10_712.pdf by guest on 27 September 2021 snapper, wrasse, parrot fish, and surgeon fish are all the mercury hazard present in the fish. In 1972, the renown for carrying this toxin. Gastrointestinal and mercury level in the muscle of pike was found to be as neurological disturbances, numbness around the lips, high as 20 ppm when the fish came from rivers and muscle pains are common in poisoned humans. The downstream from sites of pulp or paper industries where case fatality rate is less than 10o/o. This fish species phenyl mercury acetate was used as a slimicide. In producing this form of poisoning may be toxic in some uncontaminated areas, a level of 0.1 ppm in pike is areas of the world, but safe in others. It is thought that regarded as natural. the toxin is produced by blue green algae and transferred It was later determined that use of mercury fungicides to fish through the food chain. The is generally on golf course greens in the U.S. caused high mercury not destroyed by cooking procedures. levels in fish located in golf course lakes and ponds (25). When Scombroid fishes are kept at room temprature, Some of these impoundments were closed to fishing. bacterial spoilage can result in enzymatic decarboxyla­ Nitrite and nitrate. When nitrites and nitrates are tion offree histidine to produce histamine. Scombrotoxin added to meat that has begun to decompose, the meat is thought to be a combination of histamine and other becomes more red in color thus appearing fresh. This toxic substances. Scombroid poisoning produces symp­ practice of "camouflage" is obviously dangerous because toms resembling those of severe allergy or histamine the consumer can not recognize spoiled meat and intoxication. Symptoms in man are headache, dizziness, because excessive amounts of nitrites or nitrates added to abdominal pain, and gastrointestinal upset. Death due to food can result in human illness assocaited with suffocation and shock has been reported. Antihistamine methemglobinemia, cynosis, vomiting, and possibly agents may relieve the symptoms. death. Puffer fish poisoning is another form of fish poisoning Another possible risk from using nitrites and nitrates frequently diagnosed in Japan. Gastrointestional upset as "camouflage" or as curing salts in fish processing is may be present, but neurological disturbances are more the production of the carcinogen N-nitrosamine; common. Motor paralysis, convulsions and death by Reducing bacteria on fish convert nitrates to nitrites; respiratory failure within 24 h are common. The case these nitrites can interact with secondary amines in fatality rate is approximately 60o/o. Puffer poisoning in gastric fluids to form N-nitrosamine. Whether this Japan has accounted for as much as 44o/o of all fatal food occurs when people eat nitrite-containing fish products intoxications. has not been difinitely proven. Mercury. Fish were first recognized in Japan as being Pesticides. DDT, a chlorinted hydrocarbon insecticide, contaminated with and hence a source of mercury in the has been reported as the etiologic agent in cases on non diet (27). Between 1953 and 1956, more than 100 people foodborne acute and chronic in man (33). suffered severe central illness, and 12 Seafood was not involved in any of these cases. Chronic people died after eating mercury-contaminated fish toxicity from seafood has not been reported in man, but caught in Minamata Bay. A plastics factory on the bay the potential hazard is present in food fish because of: (a) was the source of inorganic mercury contamination in the phenomenon of biological magnification or concen­ the bay. Chemical analysis of the fish showed 40 ppm of tration of DDT in the food chain, and (b) DDT storage in nearly pure organic methyl mercury which is much more human fat and its slow excretion. toxic than inorganic mercury. In 1956, Japan banned The DDT threat in fish is well illustrated by studies of fishing in Minamata Bay. It was later discovered that Coho salmon in the Great Lakes. These salmon were microorganisms in the bottom muck of the lake had the found to contain much more than the permissible 5 ppm. ability to convert inorganic mercury to methyl mercury. The Cohos rapid weight gain, before migration up tribu­ In view of the biological magnification of the mercury taries, may be the primary reason the fish accumulated through the food chain in the bay and the 200-day large amounts of pesticide. half-life of mercury of fish. it is easy to see how fish In just 2 h, endrin concentration in blood of catfish concentrated mercury 1000 times the amount in water. can reach 1,000 or more times the amount present in FISH. SHELLFISH, AND HUMAN HEALTH 715 surrounding water. This is a major problem in catfish certain humans. Fish proteins act as allergens and farming on converted cotton land where pesticides was subsequent meals may initiate anaphylactoid or used as a cotton spray. Consumption of fish containing cutaneous hypersensitivity reactions. Allergic individuals DDT in concentrations of 5 ppm or less is permitted by are believed to have inherited a predisposition or FDA provided the menu does not contain fish items for capacity to become sensitized. In man, symptoms of days or weeks at a time. Variety in the diet is allergic reactions are urticaria, angio-neurotic edema, recommended. gastro-intestinal distrubances, and migrane headache. Radioactivity. Another potential threat seafood pre­ Allergy is usually confined to one general class or species sents to man is radiation. Oceans covering large portions offish. Sensitized people usually react more frequently to of the earth are major recipients of man-induced sardine and salmon than to cod and halibut. (military and industry) radionuclides. Today most foods Thiamine deficiency. A number of distinct nutritional have more radioactivity than present before 1945. problems are related to consumption of fish by animals.

Studies have shown that aquatic organisms can The first important nutritional disease of fur-bearing Downloaded from http://meridian.allenpress.com/jfp/article-pdf/40/10/712/1649611/0362-028x-40_10_712.pdf by guest on 27 September 2021 accumulate considerable quantities of nuclides. Re­ animals was noted on the fox ranch of J. S. Chastek of searchers at White Oak Lake and the Columbia River Glencoe, Minn. in 1932 (14). Foxes given a ration of 18% near Hanford, Washington, where plutonium production uncooked carp developed paralysis within a few weeks reactors are located, found that minnows could and died. Researchers reported;.4hat an enzyme was accumulate 32P to levels 150,000 times greater than involved and it seemed to be confined to fresh water fish, that of surrounding water. They also found that the total with the exception of ocean herring species. Later mink radioactivity of plankton was about 2,000 times that of ranchers found they could use fish in their mink diet if surrounding water. Clams and oysters collected off the fish was cooked at 82-93 C for 15 min to destroy the Marshall Islands after the Bikini Atomic Tests had enzyme. radioactivity 2,000 times greater than that of sea water. Fish also contain a high level of unsaturated fatty The concentrating of radioactivity by clams probably acids. It has been shown that low dietary level of Vitamin involved their ability to ftlter large volumes of water. In E and a high dietary level of u