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,.....' 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 States, 1970 to 1978. OIJ .5 <=I 6il ;.::: i3"' 0 0 0 "' "; 0 ~ :~ :g.E a·8 "'g § 0 .... 1( ) = Questionable vehicle. TABLE 4. Foodbome disease outbreaks in which marine crustaceans were implicated as vehicles in the United States from 1970 to 1978. ;:! 6il "' 0 "' .;a "; -~ r.tJ 0 E ~ :E ~:; 4-o·.g ..s"' .;a "'0 <=I0 0 !il .:: 5 ..!l Ql E..- 0 <=I ~ .... <=I "'0"'"' <=I "'0 »u·- "" <=I i(J f:t ·s ..: g 0 - "' ·@ ,g 1S "' 0 'il ..c::c..>< ·- "' <=I s .S!P ~~!::1 :';l.-"1 ] "'{'"'0 ·~ "; "' 0 0 ..c:: ·- <=I Product t)~~ til til en .5 >"J:l.,OiJ ~ Cl ::; E-< Oayfish 1 1 Crab 5 5 (1)1 10 (1) Crab cocktail, salad 1 1 2 Crab raviatte 1 1 Lobster 2 2 Lobster salad 2 2 Lobster bisque 1 1 Shrimp 4 7 11 Shrimp kalaquin 1 1 Shrimp salad 2 3 3 8 Shrimp newburg 1 1 Shrimp fried rice 1 1 Seafood newburg 1 1 Total 1 2 1 5 11 22 (1) 42 (1) 1 ( ) = Questionable vehicle. poisoning are tourists and picnickers who gather the hazard. Discolored sea water and identification of shellfish for their own consumption. Commercially toxic dinoflagellates from samples of sea water can serve harvested shellfish have seldom been involved. as indicators of potential danger. The primary effort to control paralytic shellfish Usual methods of cooking (steaming, boiling, baking poisoning consists of collecting samples of mollusks and or frying) do not destroy paralytic shellfish toxin; testing them for toxin by mouse bioassay during the however, its concentration can be reduced by the high danger periods that occur from May through October. temperatures that can occur during pan-frying and The tolerance level is 400 mouse units/100 g of shellfish during retorting in commercial canning operations. or 80 ~/1000 g, and no package can exceed 2000 mouse units (65). When shellfish are found to be at or above this Scombroidfish poisoning level, their growing area is quarantined and their sale is Scombroid fish poisoning can be caused by fish (such as prohibited. Under these circumstances, warning signs those of the families Scombresocidae. Scombridae, and should be posted in shellfish-growing areas and on Coryphaenidae) that contain a sufficient concentration of beaches. The news media also should warn the public of free histidine in their flesh. Under certain environmental JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 FOODBORNE DISEASES TRANSMITTED BY SEAFOOD 863 conditions, bacteria that are able to make amino acid hot (above 60 C; 140 F) or rapidly chilled and held at or decarboxylases, decarboxylate histidine producing hista below 7 C (45 F). mine (2). These bacteria include members of the Botulism Enterobacteriaceae (Escherichia, Klebsiella, Salmonella, Fish can become contaminated by C. botulinum spores Shigella, Proteus, Citrohacter, Enterohacter, Serratia, from water or mud. Small numbers of this organism are Hafnia), C. perfringens, Bacillus cereus, Pseudomonas sometimes found in the intestines of fish, and they can be aeruginosa, Pseudomonas repilivora, Streptococcus fae· spread to flesh during cleaning. The level of contamina calis. Streptococcus faecium, and Brevihacter spp. tion in or on fresh fish, however, is small, and such ftsh Members of the genera Betahacter and Ristella also are not considered to be hazardous. Hazardous make this enzyme. Proteus morganii has frequently been situations usually occur after seafood has been recovered from fish that have been incriminated as inadequately heat-processed so that C. botulinum spores vehicles in outbreaks ofscombroid fish poisoning. survive. Such products support germination of spores Histamine is quite heat-resistant. According to and multiplication of resulting vegetative cells and toxin Ienistea (44), histamine is partially destroyed by boiling 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 production, as they are stored at room temperature. for 3 h and is destroyed at 116 C (223 F) for 90 min. If Anaerobic conditions favorable to growth of C. this is so, retorting would destroy histamine during some, botulinum exist or develop while fish or toe are stored in but not all, commercial canning operations. Scombroid cans, in plastic bags or in bulk. The processed fish must fish poisoning, however, has occurred in persons who also be eaten without thorough cooking which would have ingested commercially canned and processed tuna destroy neurotoxin, to cause illness. The microbiology of (57). Prompt and proper refrigeration from the time fish fish-associated botulism has been reviewed by Hobbs are caught until they are heat-processed (or otherwise (37). preserved to inhibit microbial growth) is essential to Fermented salmon eggs and unspecified types of fish prevent scombroid fish poisoning. eggs have been reported frequently as vehicles in Vibrio parahaemolyticus gastroenteritis outbreaks of botulism in the United States (Table 6). V. parahaemolyticus frequently contaminates fish, Whitefish, particularly smoked whitefiSh, and tuna fish crustaceans and mollusks in their marine habitat, have also been reported frequently as vehicles. Whale particularly in warm waters. Fish, mollusks and meat or blubber and seal meat or oil have been crustaceans that ate contaminated by V. parahaemolyti important vehicles in outbreaks of this disease in cus and have been stored at temperatures that are Eskimos. Many other foods of marine origin have been conducive to its multiplication can become vehicles of V. sporadically reported as vehicles. Approximately two parahaemolyticus gastroenteritis. Illness can result if thirds of the vehicles were fermented, smoked, canned or they are eaten raw. Usual heat processing kills V. otherwise processed in homes; the others, however, parahaemolyticus, but cooked seafood can be reconta were processed in commercial operations. Type E toxin minated by being touched by (a) contaminated raw was responsible for most of the outbreaks. seafood, (h) workers who previously touched raw seafood, Botulism can be prevented by (a) killing C. botulinum (c) equipment that was previously used to process raw spores in seafood during processing, (h) preventing seafood or (d) being rinsed with sea water. If subsequent contamination of processed seafood, (c) recontaminated seafood is not thoroughly reheated, and formulating seafood products in a way that spores cannot it is left at room temperature or refrigerated in large germinate and vegetative cells cannot multiply, (d) masses, it can cause illness. storing seafood in a way that prevents growth of Table 5 lists outbreaks of V. parahaemolyticus vegetative cells, (e) destroying toxin by thorough heating gastroenteritis that have been reported in the United of home-processed foods just before serving and (fJ States. The epidemiology of V. parahaemolyticus discarding products that show signs of spoilage (e.g., gastroenteritis has been reviewed (5,59). Strains of V. bulging cans, off-odors, bubbles of gas). parahaemolyticus isolated from patients are almost always Kanagawa-positive, while those from foods are SEWAGE POLLUTION OF AQUA TIC HABITATS Kanagawa-negative (59). Also, more than one serotype is Pollution of estuaries by domestic sewage and often isolated from patients and implicated foods as well subsequent ingestion of raw or improperly cooked as from the environment. These features make definite shellfiSh harvested from the polluted waters have led to epidemiologic associations difficult. outbreaks of typhoid fever, hepatitis A and cholera. The best way to prevent V. parahaemo/yticus Diseases caused by Enterobacteriaceae and enteric gastroenteritis is to keep fish at low temperatures while viruses can conceivably be caused by the same stored on boats, in markets and in foodservice circumstances, but there is little epidemiologic evidence establishments. (As previously mentioned, thorough that this happens. cooking kills V. parahaemolyticus.) Preventing cross contamination of cooked foods by raw seafood will also Typhoid fever help to prevent V. parahaemo/yticus gastroenteritis. In the past, as referenced in Table 7, raw bivalve Cooked seafood should either be eaten immediately, kept mollusks were commonly involved in outbreaks of JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 864 BRYAN TABLE 5. Outbreaks ofVibrio parahaemolyticus gastroenteritis reported in the United States. Year Location Number ill Vehicle Contributory factors Reference 1971 Maryland 320 Steamed crabs Cross-contamination (live crabs 26 put on top of cooked crabs) 1971 Maryland 16 Steamed crabs Cross-contamination (live crabs 26 put on top of cooked crabs) 1971 Maryland 8 Steamed crabs Cross-contamination (live crabs 26 put on top of cooked crabs) 1971 Maryland 24 Crab salad 26 1972 Maryland 20 Steamed crabs Cross-contamination from 10 basket previously used for raw crabs; improper refrigeration 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 1972 Louisiana 600+ Boiled shrimp Improper refrigeration 33 1972 New Jersey 12 Shrimp and crabs Cross-contamination from 74 basket previously used for raw crabs 1975 Cruise ship 252 Seafood cocktail Cross-contamination by sea 23 water; improper refrigeration 50 1975 Cruise ship 445 Shrimp cocktail and lobster Cross-contamination by sea 23 water; improper refrigeration 50 1978 Cruise ship 98+ Seafood salad (Cross-contamination) 24 1978 Louisiana 1133 Boiled shrimp Cross-contamination from boxes 32 previously used for raw crabs; improper hot holding; improper refrigeration Unconfirmed but suspected outbreaks 1969 Airline 24 Unknown 11,69 1969 Airline 52 Unknown 11.69 1969 Washington 21 Roasted oysters 22 1971 Texas 52 Raw oysters 22 1971 Maryland 43 Steamed crabs 22 1972 Florida 6 Steamed crabs 22 1972 Hawaii 38 Crab and raw fish Improper refrigeration 71 1973 California 1 Conch meat 16 typhoid fever. Today in the United States, shellfish-borne Hepatitis A typhoid fever is unlikely, because there are few cases of Mollusks become contaminated with hepatitis A this disease or carriers to discharge Salmonella typhi into viruses when their growing areas are grossly polluted by sewerage. Also, many communities have effective sewage sewage. Hepatitis A virus is probably taken up by the treatment facilities so that only small numbers of S. typhi mollusks while they feed. Shellfish could also become ever reach waters from which shellfish are harvested. contaminated during handling by carriers in the Humans develop typhoid fever when they ingest rather pre-icteric or early icteric stages of hepatitis A, but large quantities (10 5 or more) of S. typhi; consequently. specific proof of this mode of contamination of mollusks shellfish from only grossly polluted waters have that have been vehicles in outbreaks is lacking. Other transmitted typhoid fever. Mollusks usually acquire S. foods, however, have become contaminated by this typhi from sewage-polluted water. but they are means. so it could also happen during fish handling. sometimes introduced by workers during shucking, Table 8 lists shellfish-associated outbreaks that have processing or preparation. Phagetyping organisms been reported in the United States. isolated from stool specimens, from sewers, from shellfish harvesting areas and from mollusks is useful for The hepatitis A virus is relatively heat resistant; it can identifYing source, transmission, and vehicle. withstand the effects of steaming clams for short periods. JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 FOOD BORNE DISEASES TRANSMITTED BY SEAFOOD 865 TABLE 6. Outbreaks ofbotulism attributed to seafood in the United States from 1899 to 1978. Process Type Product Outbreaks Cases Deaths Home Commercial A B E Unk Salmon Unspecified 7(1)1 16(1) 5(1) 7 (1) 2 5(1) Smoked 3 5 1 2 1 2 Salted 2 0 1 Eggs 10 17 7 10 7 2 Whitefish Unspecified 3 5 3 2 1 2 1 Smoked 8(1) 22(9) 9 (1) 8 (1) 8 Frozen 2 0 1 1 Tuna 8(1) 29(2) 14(2) 7 2(1) 2 1 1 5(1) 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 Whale Beluga, flippers 5 13 5 5 3 2 Whale/whale fluke 2 8 2 2 Fermented 1 1 1 1 Seal (and oil) 4 7 1 4 4 Clam juice 3 7 5 3 3 Clams 2 5 5 1 1 1 Sardines 4 7 6 1 3 1 3 Sprats 1 3 1 1 Ougruk 2 1 1 1 Crab 1 1 1 Lobster, frozen 1 0 Mullet 1 0 (1) Lampryeel 1 2 1 1 Fish 1 1 0 Fish, marinated 3 0 1 Fish, pickled 2 2 2 1 1 Fish, head soup 8 0 1 1 Fish eggs 2 4 1 2 1 1 Total 75(3) 174(12) 70(3)2 53(2) 22(2) 14 3(1) 34 25(2) 1( ) = Questionable vehicle. 2Case fatality rate is 39%. Cooked shellfish, however, have rarely been reported as V. cholerae organisms in sewage enter estuaries or vehicles. coastal waters. These organisms persist in water only for Cholera a short while, but during that time they can either contaminate fish, crustaceans, or mollusks or be ingested In areas where cholera occurs, several cases usually by them. Foods can become contaminated also if occur within a short time. This is characteristic of handled by persons who are infected with V. cholerae common-source outbreaks spread by contaminated food and who do not practice proper personal hygiene. If or water. Fish and shellfish have been identified as contaminated seafood or other foods are either not vehicles more frequently than other kinds of foods. Some refrigerated or are improperly refrigerated, populations fish- and shellfish-associated outbreaks that have been of V. cholerae can multiply to numbers of sufficient reported throughout the world are listed in Table 9. magnitude to cause cholera. Large numbers (usually more than 106) of Vibrio cholerae must usually be ingested to cause cholera, Control because many of these organisms succumb to the effect Essential for the control of shellfish-borne diseases of the low pH of the stomach. Reduced gastric acid associated with sewage-polluted waters is to intercept production, as can result from gastric surgery or sewage and to treat it in such a manner that pathogens medications to neutralize gastric acid, can impair this are killed, removed or substantially reduced in number host-defense mechanism. before the effluent flows into estuaries or coastal waters. JOURNAL OF FOOD PROTECTION, VOL.43, NOVEMBER 1980 866 BRYAN TABLE 7. Foodbome outbreaks of typhoid fever reported in nuclides and/or harmful industrial wastes are not the United States in which the implicated vehicles were discharged or otherwise reach shellfish-growing areas. shellfish. Areas are unapproved (prohibited) whenever raw sewage enters the water or the median coliform MPN of the Year Number Vehicle Reference water exceeds 700 per 100 ml (39). Harvesting shellfish 1894 Oysters from unapproved areas should be prohibited unless the 1902 80 Oysters/clams 54 shellfish are to be subsequently subjected to approved 1911 66 Oysters/clams 51 treatment processes. 1911 18 Oysters 70 Relaying bivalve mollusks in clean waters is an 1917 Oysters 4 acceptable sanitation practice. Mollusks from polluted 1925 Oysters 15,52 waters release sewage-borne bacteria and take up the 1925 263129} Estimated Oysters 52 characteristic microbial flora of their new habitat. 1925 23 1500 cases Oysters 52 1925 66 Oysters 52 Although purification often takes a few days only, they 1928 Oysters 64 are normally kept in the clean area for at least 2 weeks. 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 1930 11 Lobster 1 Bivalve mollusks can also be placed in specially 1938 6 Oysters 75 designed tanks of clean sea water as well as in the open 1940 94 Oysters 61 sea. Sometimes the sea water in these tanks is treated 1945 Clams 35 with ultraviolet light; sometimes fresh water that has 1962 6 Oysters 8 been treated with chlorine or ozone is used, and salt is added to adjust the content to that approximating sea water. The mollusks are placed in a thin layer, usually TABLE 8. Outbreaks of hepatitis A attributed to contami- less than 6 em deep, in trays or baskets, on the bottom of nated raw shellfoh reported in the United States. the tank. The shellfish are flushed with water to remove grit, and the tanks are then flooded with clean sea water Year Number ill Vehicle Reference or treated fresh water. During the 2 or more days the 1953 30 Oysters 18 mollusks are immersed, sewage-borne bacteria that have 1961 84 Oysters 55 accumulated in the mollusks are shed in feces. The feces 1961 459 Clams 29 are not easily dissolved and do not repollute the shellfish 1961 15 Clams 66 unless there is excessive agitation of the water. After 1964 183 Clams 18 purification, the mollusks are again flushed with water 1964 123 Clams 67 (77). Viruses are not necessarily removed by purification 1964 3 Oysters 18 procedures; however, mollusks that have undergone such 1963-1966 185 Oysters/clams 48 1966 4 Clams 27 treatment have not been epidemiologically linked, up to 1969 6 Clams 19 the present time, with products so treated. 1971 5 Clams 21 Samples of shellfish on the wholesale market should be 1971 12 Clams 6 collected and examined for compliance with a microbio 1973 265 Oysters 53 logical standard. The standard for satisfactory shellfish 1977 17 Shellfish 25 is not more than 230 (MPN) fecal coliforms per 100 g and 1979 10 Oysters 68,76 not more than 500,000 mesophilic (35 C) aerobic colony count per g (39). Waters from which shellfish are harvested need to be CONTAMINATION FROM WORKERS, evaluated for sewage discharges, and monitored by EQUIPMENT, OR THE ENVIRONMENT bacteriological surveys to determine the degree of contamination, using suitable indicators of fecal The pathogens that cause typhoid fever, hepatitis A pollution. Shellfish taken from lightly polluted sea water and cholera (discussed under the heading "sewage are usually of an acceptable quality. The water in pollution of aquatic habitats") can also be acquired as a approved shellfish-growing areas should have a median result of contamination of seafoods after they are caught, coliform most probable number (MPN) of not more than frequently during processing or preparation. Other 70 per 100 ml, and fewer than 10o/oof the samples should pathogens that are sometimes acquired as a result of contain no more than 230 per 100 ml for a 5-tube, mishandling and mistreatment of seafood can cause 3-dilution test or 330 for a 3-tube, 3-dilution test (39). An staphylococcal intoxication, shigellosis, salmonellosis, interim standard for growing areas is that the median and C. perfringens gastroenteritis. MPN fecal coliform value for a sampling station should Staphylococcal intoxication not exceed 14 per 100 ml of sample and not more than Important ecological niches of Staphylococcus aureus 10o/o of the samples shall exceed 43 for the 5-tube, are the anterior nares and skin of humans. Heat 3-dilution test or 49 for a 3-tube, 3-dilution test (43). processed seafood can become contaminated with these Also, a sanitary survey should indicate that dangerous organisms as workers prepare salads and other dishes. If concentrations of pathogenic microorganisms, radio- foods that are contaminated in this manner are either JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 FOODBORNE DISEASES TRANSMITIED BY SEAFOOD 867 TABLE 9. Outbreaks ofcholera with epidemiologic association offish or shellfish as vehicles. Year Country Number ill Vehicle Contributing factor Reference 1886 Japan Fish Eaten raw 28 1907 England Oysters Sewage contamination 60 of oyster beds 1908 Philippines Dried fish 36 1925 Philippines Small fish 63 Crayfish 1926 Japan Fish 73 1930 Burma Prawns 49 1965 Philippines 72+ Small raw shrimp Sewage contamination of 47 water habitat Eaten raw 1971 Mal asia Shrimp Eaten raw 32 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 1974 Portugal Shellfish Sewage contamination 7 of mud flats, eaten raw 1974 Italy 278 Mussels Sewage contamination 3 of water habitat, eaten raw eaten raw, gastric surgery 1977 Guam 6 Pad as (home-preserved fish) Sewage contamination 58 of bays, inadequate refrigeration 1978 USA 8 Crab Sewage contamination 9,17 ( + 3 asympto- of water habitat, matic persons) inadequate cooking, inadequate refrigeration 1979 Gilbert Islands 572 Salted and partially Eaten raw, sewage 56 19 deaths dried lagoon flsh, raw contaminated lagoon raw clams, sardines, and other fish kept at room temperature or stored in large pots while in Shigellosis refrigerators, enterotoxigenic staphylococci can multiply Fish and shellfish salads are sometimes implicated as and produce enterotoxin. The lower water activity of vehicles of outbreaks of shigellosis. This happens only smoked and salted fish, as compared to fresh fish, when a human carrier of Shigella. who does not practice selectively favors growth of staphylococci over the growth adequate personal hygiene and whose hands consequent of spoilage microflora. The principal factors that ly become contaminated with feces, prepares fish or contribute to outbreaks of staphylococcal intoxication, shellfish products that are not subsequently heated to whatever the vehicle, are: infected persons contaminat temperatures that kill shigellae. Such contaminated ing foods, preparing foods a day or more before serving foods frequently are either kept at room temperature for and improper cooling of foods (13). long periods or are stored in large batches in large pots or Because staphylococci are so intimately associated pans during refrigeration. Preventive procedures should with humans, foods are likely to become contaminated emphasize personal hygiene of workers, thorough during preparation. Prevention of fish-borne staphy cooking or reheating (where applicable) and rapid lococcal intoxication depends on treating fish products cooling and proper refrigeration. so that any contaminating staphylococci are kept in their lag phase. This can be done by rapidly chilling prepared Salmonellosis seafood products and dishes, by storing them in shallow Salmonellae are common in animal feces and wastes pans during refrigeration, or by holding them at 5.6 C from slaughtering houses and poultry processing plants. (42 F) or below or at 60 C (140 F) or above. The practice These organisms sometimes reach fresh water from of strict personal hygiene by workers and the thorough which fish are caught and eventually reach estuaries. cleaning and disinfection of equipment will limit Salmonellae also can reach these waters in community contamination but not always ensut'e freedom from sewage. Fish and shellfish either acquire salmonellae staphylococci. Heat processing that produces tempera while in polluted waters, or subsequently while they are tures of 71.1 C to 73.9 C (160 F to 165 F) will kill stored in the holds of vessels and as they are being staphylococci but will not destroy their enterotoxins. processed. Improper storage of contaminated fish fosters After heat or salt treatment of foods, great care must be multiplication of salmonellae to the quantity that can taken to prevent contamination by staphylococci and cause illness. This is of particular concern if cooked their subsequent multiplication. seafood becomes contaminated, either by contact with JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 868 BRYAN surfaces previously used to process raw foods of animal control procedures. Hazards that have led to the spread origin or by persons who previously handled these raw of specific diseases have either been specified or alluded foods. Factors that frequently contribute to outbreaks of to, and they are summarized in Table 10. Factors that salmonellosis are: improper cooling, contaminated raw contribute to the spread offish-borne and shellfish-borne ingredients, inadequate heat processing and cross diseases differ somewhat with each disease, but they are contamination (13). similar to the factors that relate to foodborne disease To prevent salmonellosis, fresh-water fish from warm involving any vehicle. The descriptions of these factors waters should be cooked to time-temperature combina and their relative importance have been published (13). tions that have been shown to kill salmonellae. Also, They include: (a) Improper cooling (as allowing cooked efforts must be made to prevent raw poultry and meat foods to cool at room temperature and stored foods in from contaminating cooked foods, by using different large pots in refrigerators). (b) Improper hot-holding of equipment and utensils for raw foods than used for food at temperatures within a range at which pathogenic cooked foods. Because large numbers (10 5 or more) of bacteria can multiply. (c) Lapse of a day or more between salmonellae must usually be ingested to cause illness preparing food and serving it (coupled with improper 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 and because such quantities are found only when storage practices). (d) Use of leftover foods (coupled with salmonellae multiply in foods, prevention of multiplica· improper storage practices). (e) Reheating of previously tion is essential. After seafood has been processed and TABLE 10. Hazard analysis of seafood operations. prepared, it should be cooled rapidly to below 7 C (45 F), and stored either frozen or refrigerated or held at a Potential temperature (such as 60 C, 140 F) that exceeds the Con· Survi- Operation Organism/Toxin tarnin- viva! Growth upper limit at which salmonellae multiply. ation Clostridium perfringens gastroenteritis Development Anisakis + C. perfringens spores can reach fish and shellfish in in sea Gonyaulax + their water habitats (particularly near sewage outfalls), Hepatitis A virus ( + )2 from surfaces of holds in vessels, from surfaces of Escherichia coli ( + )2 3 ( + )2 equipment and utensils used for processing and Proteus Salmonella typhi ( + )2 preparation or from workers. The usual cooking (other Salmonella ( + )4 than retorting) of seafood does not kill spores, but it does Vibrio cholerae ( + )2 reduce the oxidation-reduction potential of the flesh and Vibrio parahaemolyticus + surfaces of seafood and it heat-activates the spores. Development in Clostridium botulinum + Vegetative cells which result either from germination of fresh water Diphyllobothrium latum ( + )2 spores or subsequently are acquired, can multiply in the Hepatitis A virus ( + )2 cooked products when temperatures fall to SO C (122 F) Escherichia coli ( + )2 or below, and multiplication is very rapid at tempera Salmonella typhi ( + )2 tures around 46 C (115 F). Numbers greater than 106 are Salmonellae ( + )4 necessary to cause illness. Such quantities do not reach Shigellae ( + )2 foods by mere contamination, but accumulate as a result Vibrio cholerae ( + )2 of multiplication of vegetative cells. Storage on ships Salmonellae + + Factors that contribute to outbreaks of C. peifringens or boats and in Proteus3, Scombroid toxin + gastroenteritis are improper cooling, lapse of a day or markets Vibrio parahaemolyticus -t5 + more between preparation and serving, improper Processing/ Clostridium botulinum + hot-holding and improper reheating U 3). Prevention of C. preparation Clostridium peifringens + + + perfringens gastroenteritis, therefore, can be accom Escherichia coli + + + plished by inhibiting the germination of spores and the Hepatitis A virus + + multiplication of vegetative cells. This can be done by (a) Monosodium glutamate + eating seafood immediately after it is cooked, (b) holding Salmonella typhi + + + cooked seafood at 55 C (131 F) or higher, (c) cooling Salmonellae + + + cooked seafood rapidly to temperatures below which C. Staphylococcus aureus + + + Proteus3, Scombroid toxin perfringens can multiply and (d) holding cooked food at + + temperatures of 7 C (45 F) or below. Vegetative cells can Streptococcus pyogenes + + + Vibrio cholerae + + be killed by thorough reheating. + Vibrio +5 + + MONITORING SANITATION AND FOOD-HANDLING 1Seasonal, higher contamination in warmer waters. PRACTICES IN PROCESSING PLANTS, MARKETS 2Conditional, depending on sewage pollution of water. AND FOODSERVICE ESTABLISHMENTS 3Proteus and other organisms present that decarboxylate During surveys or inspections of processing plants, histidine to histamine. markets or foodservice establishments. sanitarians and 4 Conditional, depending on sewage, animal waste, or food of quality assurance personnel should make hazard animal origin processing waste pollution. analyses, designate critical control points and specify 5Cross-contamination originating from raw fish. JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 FOODBORNE DISEASES TRANSMITTED BY SEAFOOD 873 cooked foods to insufficiently high temperatures. (j) analyses, immediate corrective action must be taken. Cooking raw foods to time-temperature exposures that Persons involved with these operations should be trained are not lethal to nonsporeforming pathogens. (g) Infected in proper procedures, and periodic evaluations should be persons (usually nasal carriers of S. aureus) touching made to see that they are being followed. cooked foods, (h) Inadequate cleaning of kitchen MONITORING SEAFOOD FOR MICROORGANISMS equipment (such as slicers, grinders, cutting boards, knives, storage pots). (i) Cross contamination of In addition to the microbiological standards for pathogenic microorganisms on raw foods of animal shellfish-growing waters and for wholesale market origin, by workers' hands or equipment, to foods that samples of mollusks, other microbiological specifications either have already been cooked or that require no for seafood have been proposed. The International further heating. (J) Storing high-acid foods in containers Commission on Microbiological Specifications for Foods made of or coated with toxic metals. (k) Contaminated (45) recommended specifications for aerobic colony raw ingredient added to foods that are either eaten raw counts (at 25 C) in fresh and frozen fish; freshwater fish; frozen raw shrimp. prawns, and lobster tails; and frozen or insufficiently cooked.([) Poisonous chemicals reaching 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 foods because of carelessness, accident, improper storage raw, breaded shrimp and prawns at n1 = 5, c1 = 3, or because they are mistaken for food ingredients. (m) m 1 = 10 6, M1 10 7; for breaded, precooked fish, n = 5, Foods obtained from unsafe sources. (n) Contaminated c = 2, m = 106, M = 10 7; for cold-smoked fish (to be water. The control of these factors must be given cooked), n = 5, c 3, m = 10 5, M = 106 ; for cold-smoked 5 6 precedence over all other activities that relate to fish (to be eaten raw), n = 5, c = 1, m = 10 , M = 10 • sanitation and consumer expectation (1 4). The recommended aerobic colony count (at 35 C) Operations (from the delivery of foods until the specifications for frozen cooked shrimp. prawns, and 7 product is sold, shipped or eaten) should be observed lobster tails are n = 5, c = 1, m = 106, M = 10 , and for 5 to detect probable sources of contamination, and those cooked, picked crabmeat, n = 5, c = 1, m = 10 , 7 processing steps at which a foodborne pathogen is likely M 10 • to contaminate a product. Activities should be evaluated All of the Commission's specifications for fecal for situations in which workers do or could contaminate coliforms in seafood have an n value of 5, m value of 4, foods. Each process step should also be evaluated for its M value of 400; c values, however, vary. The C value for effect on increasing or decreasing numbers of bacteria. fresh and frozen fish; freshwater fish; cold-smoked fish Processes that increase contamination should either be (to be cooked); frozen, raw shrimp, prawns, and lobster eliminated or modified. Alternatively, a subsequent tails; frozen raw, breaded shrimp and prawns is 3; for process can be added either to modify, reduce, or breaded, precooked fish is 2; and for raw, cold-smoked eliminate the problem. fish (to be eaten raw); frozen, cooked shrimp, prawns, Specifications for thermal processes intended to kill and lobster tails; and cooked, picked crabmeat is 1. microorganisms should be based on appropriate testing All specifications for S. aureus in seafood have an n 3 and calculations to ensure an appropriate reduction of value of 5, m value of 10 3, and M value of 2 x 10 • The c microbial populations that could be in a food. A hazard values are as stated for fecal coliforms. analysis should include time-temperature evaluations to Specifications for V. parahaemolyticus of n = 5, c = 0, confirm the effectiveness of heating, hot-holding, and m = 102 (2-class plan) have been recommended for fish to cooling processes. The possibility for contamination of be eaten raw; frozen raw shrimp, prawns, and lobster cooked foods after processing (particularly by contact tails; frozen cooked shrimp, prawns, and lobster tails; with raw foods of animal origin, contact with equipment frozen raw, breaded shrimp; and cooked, picked previously used for such raw foods, or by hands of crabmeat. workers who previously handled these raw products) The specifications for Salmonella in fresh-water fish should be evaluated. from warm waters are n 5, c = 0, and m = 0 (2-class Evaluation ofthe time-temperature exposure of foods plan). after heat processing is crucial in hazard analyses. EDUCATION AND TRAINING Equipment for hot- and cold·holding must be of a design and capacity that will keep seafood at temperatures that Education and training are the keystones of effective will not permit pathogenic foodborne bacteria to disease prevention and quality control. Persons who need multiply. Foods that are to be stored cold should be to be trained or informed about seafood-borne diseases cooled rapidly to temperatures at which pathogenic and their prevention and control include: regulatory bacteria associated with these products cannot multiply. personnel, supervisory and quality control personnel, Whenever deficiencies are found during hazard plant and foodservice personnel, fishermen, and shellfish harvesters. 'n refers to the number ofsamples that must be examined.from each lot Regulatory and quality control personnel should be or production batch; c refers to the number of defective samples that trained in principles and techniques of fish preservation are acceptable and fall within m and M ranges; m refers to the number and processing, in epidemiology of diseases that are of or~anisms that separates good quality .from marginally acceptable quahty; M refers to the number of organisms that separates marginally transmitted by fish and shellfish, in the biology and acceptable quality from unacceptable quality. · chemistry of the etiologic agents of these diseases, in JOURNAL OF FOOD PROTECTION, VOL. 43, NOVEMBER 1980 874 BRYAN shellfish-related laws and ordinances, in the impact of DiGioia, E. lzzo, E. J. Gangarosa, and F. Pocchiori. 1974. sewage disposal on contamination of shellfish and in Epidemiology of cholera in Italy in 1973. Lancet 2:1370-1382. 4. Banks, A. E. 1917. Typhoid fever traced to polluted oyster.;. Bull. plant sanitation. Ideally, they should qualify for their California State Board of Health (Cited by I ens en, 1956). jobs on the basis of educational requirements and 5. Barker, W. H., Jr. 1974. Vibrio parahaemolyticus outbreaks in the certification that conforms to the standards established United States. Lancet 1: 1·9. by professional groups. Maintenance of certification 6. Berman, H. A., G. Waterman, and N.J. Fiumara. 1972. Shellfish should be based on continued training and up-dating of associated hepatitis · Massachusetts. Morbidity Mortality Weekly Rep. 21 (2):20. education. 7.Blake, P. A., M. L. Rosenberg, J. B. Costa, P. S. Ferreira, C. L. Managers and supervisors in the seafood industry and Guimaraes, and E. J. Gangarosa. 1977. Cholera in Portugal, 1974. in foodservice establishments should become aware of I. Mode of transmission. Am. J. Epidemiol. 105:337-343. foodborne disease problems that confront the industry. 8.Bond,J. 0., W.J. Murphy, W. H. Y. Smith, and J. Koomen.1962. They must learn the principal sources of foodborne Morbidity Mortality Weekly Rep. 11(13):98. 9. Bradford, H. B., C. T. Caraway, Food and Drug Administration, disease agents, and they must learn the other factors that and Center for Disease Control. 1978. Follow-up on Vibrio cholerae contribute to foodborne disease outbreaks. They must infection. Morbidity Mortality Weekly Rep. 27(38):365-368; 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 become motivated to ensure that their operations are free 388-389;402;412-413;442;447;550. of such situations; or, failing that, they must be able to 10. Bread, I. H., R. Nelson, A. Salinger, J. Molenda, and J. D. recognize undesirable situations and either take appro Stafford. 1972. Vibrio parahaemolyticu.s gastroenteritis. Maryland. Morbidity Mortality Weekly Rep. 21 (29):245-246. priate measures to prevent their recurrence or seek 11.Brolnitshy, 0., W. J. Rose, W. J. Fiumara, M. Saslaw, E. C. professional consultation. Official agencies or industrial Prather, H. L. Smith, N. Egoz, and Center for Disease Control. organizations should train managers in these matters, 1969. Acute gastroenteritis among tour groups to the Orient and certify that they can manage a safe operation. These United States. Morbidity Mortality Weekly Rep. 18(35):301-302. managers and supervisors should, in turn, train the 12. Bryan, F. L. 1973. Activities of the Center for Disease Control in public health problems related to the consumption of fish and workers under their direction in safe preparation of fishery products. In C. 0. Chichester and H. Graham (eds.) seafood and proper sanitation of equipment. Certifica Microbial safety of fishery products. Academic Press, New York. tion of managers should be based on their actions to 13. Bryan, F. L. 1978. Factors that contribute to foodborne disease train their staff. on establishment of a sanitary outbreaks. I. Food Prot.41:816-827. maintenance schedule and on their supervision of an 14. Bryan, F. L. 1979. Prevention of food borne diseases in foodservice establishments. J. Environ. Health 41:198-206. operation that is free of factors that can contribute to 15. Bundesen, H. N. 1925. Typhoid epidemic in Chicago apparently outbreaks of food borne disease. due to oysters. J. Am. Med. Assoc. 84:641·6.50. Workers must be introduced to the basic principles of 16. California State Health Department. 1973. Vibrio parahaemolyti· foodborne disease prevention and sanitation. This cus gastroenteritis - California. Morbidity Mortality Weekly Rep. includes an understanding that (a) raw seafood can be a 22(.50):418. 17.Caraway, C. T .. and Center for Disease Control. 1978. Vibrio source of pathogens; (b) hands should be washed after cholerae - Louisiana. Morbidity Mortality Weekly Rep. 27(36): touching raw fish as well as after coughing, sneezing, 341 ;351. smoking and using the toilet; (c) cooked seafood should 18. Center for Disease Control. 1967. Common-source epidemics of not be touched, rinsed with sea water or put in contact infectious hepatitis. Center for Disease Control, Atlanta. with raw fish or equipment previously used for raw foods, 19. Center for Disease Control. 1969. Food borne outbreaks. Annual summary. Center for Disease Control, Atlanta. without intervening cleaning and disinfection; (d) cooked 20. Center for Disease Control. 1971-1980. Food borne and waterborne seafood must be held at 7 C (45 F) or below or 60 C disease outbreaks. Annual summaries. 1970, 1971, 1972, 1973, (140 F) or higher; (e) leftover seafood be stored in small 1974, 1975,1976, 1977. 1978. Center for Disease Control, Atlanta. quantities in shallow containers and cooled rapidly and 21. Center for Disease Control. 1972. Food borne outbreaks. Annual (/'} leftover seafood be thoroughly reheated [probably to summary J 971. Center for Disease Control, Atlanta. 22. Center for Disease Control. 1973. Vibrio parahaemolyticus 74 C (165 F)] before serving. gastroenteritis - United States. 1969-1972. Morbidity Mortality Fishermen should be able to identify poisonous ftsh in Weekly Rep. 22(27):231-232. their areas; they should know the hazards associated 23. Center for Disease Control. 1975. Vibrw parahaemolyticus with harvesting shellfish from restricted or prohibited gastroenteritis on cruise ships. Morbidity Mortality Weekly Rep. areas, or from "red tide" waters; and they should 24(]2):109-115. 24. Center for Disease Control. 1978. Gastroenteritis caused by understand the necessity for cooling or otherwise Vibrio parahaemolyticus abroad a cruise ship. 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Multi-element analysis of animal feed, animal wastes. and The authors thank Ed Mincher, Frank Moses and Jon Kindschy for sewage sludge. Environ. Sci. Techno1.12:785-790. their help in performing the analyses and sample collection. We also 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 6. Calvert, C. C., and L W. Smith. 1976. Heavy metal differences in acknowledge the assistance provided by Pat Maietta, Frank Lootens, tissues of dairy steers fed either cottonseed meal or dehydrated Stan Ziegler, Pat Evertsen and Myrna Griggs. This work was supported poultry excreta supplements. Paper presented at the 71st Meeting by grants from the U.S. Environmental Protection Agency, the Chino of American Dairy Science Association, Raleigh, North Carolina. Basin Municipal Water District and the State of California Water 7. Fontenot, J. P., and K. E. Webb. 1975. 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