859 Journal ofFood Protection, Vol. 43. No. I I, Pages 859-876 !November 1980) Copyright © 1980, lntemational Association of Milk, Food, and Environmental Sanitarians Epidemiology of Foodborne Diseases Transmitted by Fish, Shellfish and Marine Crustaceans in the United States, 1970-1978 FRANKL. BRYAN U.S. Department ofHealth and Human Services, Public Health Service, Center for Disease Control, Atlanta. Geo'1:ia 30333 (Received for publication Apri114, 1980) Downloaded from http://meridian.allenpress.com/jfp/article-pdf/43/11/859/1649529/0362-028x-43_11_859.pdf by guest on 23 September 2021 ABS1'RACT TABLE 1. Percentages of foodbome disease outbreaks of Fish, mollusks, marine crustaceans and marine mammals which fish, mollusks, and crustaceans were vehicles in the were implicated as vehicles in approximately 11 o/o of food borne United States from 1970 to 1978. disease outbreaks reported in the United States during the Percentage years 1970-1978. Tuna, clams, oysters, shrimp, and crab Vehicle frequently were vehicles. These animals can acquire the Fish 7.4 dinoflagellates responsible for ciguatera, paralytic shellfish Mollusks 1.9 poisoning and neurotoxic shellfish poisoning from their marine Marine crustaceans 1.4 habitats. Many common marine organisms found in and on Sea mammals 0.2 fish can decarboxylate histidine to histamine, and do so during Total 10.9 improper storage of fish. Vibrio parahaemolyticus and Clostridium botulinum type E are of marine origin, and C. outbreaks (fable 4), Vibrio parahaemolyticus gastro­ botulinum types A and B can wash from soil into aquatic enteritis was the most frequently reported disease environments. Pollution of estuaries by domestic sewage and attributed to marine crustaceans. subsequent ingestion of raw or improperly cooked shellfish Marine mammals also have been vehicles of a few harvested from the polluted waters have led to outbreaks of outbreaks. Three outbreaks of botulism were attributed typhoid fever, hepatitis A and cholera. Staphylococcal intoxication, shigellosis, salmonellosis, and Clostridium per­ to fermented seal meat, and whale meat was the vehicle fringens gastroenteritis (as well as typhoid fever, hepatitis A in two outbreaks of botulism. Walrus meat was the and cholera) have been acquired because seafoods were vehicle in an outbreak of trichinosis. mishandled during preparation. Preventive and control Previous epidemiologic reviews of fish -associated measures include safe disposal of sewage, monitoring of outbreaks in the United States have appeared in the sanitation practices and food-handling practices, monitoring literature (12,40.41). shellfish and their growing waters for pathogens and indicator Fish-borne and shellfish-borne diseases are described organisms, and education and training. under three categories on the basis of the primary source of their toxigenic or invasive etiologic agents: (a) agents naturally present in aquatic habitats, (b) sewage pollution of aquatic habitats and (c) contamination from Fish, mollusks, marine crustaceans and marine workers, equipment or the environment of food mammals were implicated as vehicles in approximately processing or foodservice establishments. Some diseases, 11 o/o of the outbreaks of foodborne disease reported in however, have multiple sources of contamination. the United States during the period 1970 to 1978 (20) (Table 1). Fish accounted for 7.4%. Outbreaks in which AGENTS NATURALLY PRESENT fish were involved as vehicles were usually ciguatera, IN AQUATIC HABITATS scombroid fish poisoning or botulism. Other etiologic Fish, mollusks, and crustaceans can acquire toxins or agents, however, accounted for up to five outbreaks of pathogens from their aquatic habitat. For example, V. fish-borne disease, and fish were suspected as vehicles of parahaemolyticus is of marine origin. Clostridium many outbreaks of diseases of unknown etiology botulinum type E is commonly isolated from fish, sea (fable 2). Tuna was the vehicle in the greatest number of water and mud. C. botulinum types A and B can wash fish-borne outbreaks. Mollusks were involved in 58, from soil into aquatic environments. Certain marine possibly 59, outbreaks during this period (Table 3). dinot1agellates produce toxins that are transvectored by Approximately 20 o/o of these were outbreaks of paralytic bivalve mollusks and fish. shellfish poisoning. Clams, oysters or dishes made from them were frequent vehicles of mollusk-borne outbreaks. Ciguatera Marine crustaceans, usually shrimp, crab or dishes Halstead (34) listed 6 orders, 28 families, 63 genera made from them, accounted for 42, possibly 43, and 113 species of marine animals reported as vehicles of JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 TABLE 2. Foodborne disease outbreaks in which fish were implicated as vehicles in the United States, 1970 to 1978. Common lllime or type of product Albacore 1 1 Anchovy 1 1 Barracuda 1 Bluefish 3 3 Bonito 1 1 Catfish 1 Codfish 1 1 Codfish stew 1 1 Dolphin/Mahi-mahi 21 2 24 Eel 2 Flounder 1 1 Goatfish 4 1 5 Grouper 24 24 Herring 1 ack, skipjack, amberjack 22 2 25 Kingfish 2 2 Mackeral 2 Mullet 1 3 Northern pike 1 Po'ou (cheilinus) 6 6 Porgy 1 1 Porkfish 1 Puffer fish 1 1 Salmon 3 s 9 Salmon eggs 6 1 7 Sardines Sea bass 1 1 Snapper, red snapper 2 8 12 Sturgeon 1 1 Tuna 19 7 26 Tuna salad 1 1 13 15 Tuna casserole 1 2 4 WhitefiSh s 1 6 Yellowtail 1 1 Fish, unspecified 2 1 3 12 (1)1 21 (1) Fish, marinated 1 1 Fish eggs, unspecified 2 2 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/43/11/859/1649529/0362-028x-43_11_859.pdf by guest on 23 September 2021 September 23 on guest by http://meridian.allenpress.com/jfp/article-pdf/43/11/859/1649529/0362-028x-43_11_859.pdf from Downloaded FOOD BORNE DISEASES TRANSMITTED BY SEAFOOD 861 ciguatera. Only grouper, skipjack and related species, NlflM,.....'<t"N~Mli) and red snapper, however, have been consistently ~M~ N reported as vehicles in the United States from 1970 to 1978. Most of the reported cases ingested fish caught NNM~~N~~G) from waters near Florida or Hawaii. ~ '4) ~ The fish responsible for ciguatera are usually found in spotty insular areas of the subtropics and tropics. At any 00 given time, fish in one locale around an island may be lf) toxic; in another locale, however, they may be safe. This situation may be reversed later. Poisonous fish are ..... usually found near reefs, and are often larger than the usual specimen of the species. Either they are bottom dwellers-and-feeders, or they are carnivores. The most N toxic organ is the liver; next are the intestines and then Downloaded from http://meridian.allenpress.com/jfp/article-pdf/43/11/859/1649529/0362-028x-43_11_859.pdf by guest on 23 September 2021 1-- the testes or ovaries. Muscles are the least toxic. A toxic dinoflagellate, Gambierdiscus toxicus, has been dis­ ..... covered and is a possible source of ciguatoxin for fish (78, 79). On some islands, the sale of certain fish that have a M history of causing ciguatera is prohibited. Neither the usual cooking procedures (baking, boiling, frying) nor salting or drying will attenuate ciguatoxin. ..... ..... Shellfish poisonings Paralytic shellfish poisoning is caused by a neurotoxin produced by certain marine dinoflagellates, principally ..... Gonyaulax catanella and Gonyaulax tamarensis. Other species of dinoflagellates that have been incriminated as sources of paralytic, neurotoxic or venerupin shellfish N poisons are Gonyaulax excavata, Gonyaulax acatanella, Gonylaulax polyeda, Pyrodinum phoneus, Prorocentrum micans, Exuvlaella baltica, Exuvlaella moriaelebouriae, ..... ..... lf) Glenodinum foliaceum, and Gymnodinium breve. Paralytic shellfish toxin, sometimes referred to as saxitoxin, is one of the most potent toxins known. ..... M Various mussels, clams, scallops and whelks have been vehicles of paralytic shellfish poisoning. These mollusks become toxic if they feed on toxinogenic dinoflagellates. N The toxin accumulates in the mollusks' digestive glands; high concentrations have been found in the syphons of butter clams and in the gills of other kinds of clams. The N M shellfish are not detrimentally affected by the toxin. Paralytic shellfish poisoning occurs primarily in temperate regions. It has been reported on the west coast ..... of the United States between May and October. On the east coast of the United States, shellfish have become toxic between July and September. Water temperature, 0\..... therefore, has a considerable influence on toxin production. Paralytic shellfish poisoning is often ,.c:: associated with "red tides." Red tides, which are not o+::"' necessarily red, are massive blooms of certain dinoflagel­ I!) OIJ .><:"' 1:: lates. Shellfish can, however, become toxic in waters that ~ :a () :::j do not contain enough toxigenic dinoflagellates to ....tli u I!) .S discolor water. Although mussels can become toxic in a "'I!) OIJ'"' ,.c:: .... I!) tli .;!3 :::j 1:: "C) few days when exposed to waters containing high "C) .D 1:: 0 ,..c:: .-d tn., ;; ~ .a concentrations of toxigenic dinoflagellates, detoxication, ~~~>o+:: 0..~ however, can take a month or more in waters either free "C) ~ ·- f-< I!) ·- 0.. C1) r.n ~ --.:t:: "'d ·.;:- ><..C::..C::..C::o+:l..C::-~ of or containing low concentrations of these agents. ·- r.n v:l v:l C1) v:l ::j ...... ::ED:D:D:oD:::E~ In the United States, most victims of paralytic shellfish JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 862 BRYAN TABLE 3. Foodbome disease outbreaks in which mollusks were implicated as vehicles in the United